Review: Development of SARS-CoV-2 immuno-enhanced COVID-19 vaccines with nano-platform
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Vaccination is the most effective way to prevent coronavirus disease 2019 (COVID-19). Vaccine development approaches consist of viral vector vaccines, DNA vaccine, RNA vaccine, live attenuated virus, and recombinant proteins, which elicit a specific immune response. The use of nanoparticles displaying antigen is one of the alternative approaches to conventional vaccines. This is due to the fact that nano-based vaccines are stable, able to target, form images, and offer an opportunity to enhance the immune responses. The diameters of ultrafine nanoparticles are in the range of 1–100 nm. The application of nanotechnology on vaccine design provides precise fabrication of nanomaterials with desirable properties and ability to eliminate undesirable features. To be successful, nanomaterials must be uptaken into the cell, especially into the target and able to modulate cellular functions at the subcellular levels. The advantages of nano-based vaccines are the ability to protect a cargo such as RNA, DNA, protein, or synthesis substance and have enhanced stability in a broad range of pH, ambient temperatures, and humidity for long-term storage. Moreover, nano-based vaccines can be engineered to overcome biological barriers such as nonspecific distribution in order to elicit functions in antigen presenting cells. In this review, we will summarize on the developing COVID-19 vaccine strategies and how the nanotechnology can enhance antigen presentation and strong immunogenicity using advanced technology in nanocarrier to deliver antigens. The discussion about their safe, effective, and affordable vaccines to immunize against COVID-19 will be highlighted.
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Review: Development of SARS-CoV-2 immuno-enhanced COVID-19 vaccines with nano-platform
)
Abstract
Vaccination is the most effective way to prevent coronavirus disease 2019 (COVID-19). Vaccine development approaches consist of viral vector vaccines, DNA vaccine, RNA vaccine, live attenuated virus, and recombinant proteins, which elicit a specific immune response. The use of nanoparticles displaying antigen is one of the alternative approaches to conventional vaccines. This is due to the fact that nano-based vaccines are stable, able to target, form images, and offer an opportunity to enhance the immune responses. The diameters of ultrafine nanoparticles are in the range of 1–100 nm. The application of nanotechnology on vaccine design provides precise fabrication of nanomaterials with desirable properties and ability to eliminate undesirable features. To be successful, nanomaterials must be uptaken into the cell, especially into the target and able to modulate cellular functions at the subcellular levels. The advantages of nano-based vaccines are the ability to protect a cargo such as RNA, DNA, protein, or synthesis substance and have enhanced stability in a broad range of pH, ambient temperatures, and humidity for long-term storage. Moreover, nano-based vaccines can be engineered to overcome biological barriers such as nonspecific distribution in order to elicit functions in antigen presenting cells. In this review, we will summarize on the developing COVID-19 vaccine strategies and how the nanotechnology can enhance antigen presentation and strong immunogenicity using advanced technology in nanocarrier to deliver antigens. The discussion about their safe, effective, and affordable vaccines to immunize against COVID-19 will be highlighted.
References(447)
Zhang, L.; Wang, W.; Wang, S. X. Effect of vaccine administration modality on immunogenicity and efficacy. Expert Rev. Vaccines 2015, 14, 1509–1523.
Lemiale, F.; Kong, W. P.; Akyürek, L. M.; Ling, X.; Huang, Y.; Chakrabarti, B. K.; Eckhaus, M.; Nabel, G. J. Enhanced mucosal immunoglobulin a response of intranasal adenoviral vector human immunodeficiency virus vaccine and localization in the central nervous system. J. Virol. 2003, 77, 10078–10087.
Bregu, M.; Draper, S. J.; Hill, A. V. S.; Greenwood, B. M. Accelerating vaccine development and deployment: Report of a royal society satellite meeting. Philos. Trans. Roy. Soc. Lond B Biol. Sci. 2011, 366, 2841–2849.
Deming, M. E.; Michael, N. L.; Robb, M.; Cohen, M. S.; Neuzil, K. M. Accelerating development of SARS-CoV-2 vaccines-the role for controlled human infection models. N. Engl. J. Med. 2020, 383, e63.
Nguyen, L. C.; Bakerlee, C. W.; McKelvey, T. G.; Rose, S. M.; Norman, A. J.; Joseph, N.; Manheim, D.; McLaren, M. R.; Jiang, S.; Barnes, C. F. et al. Evaluating use cases for human challenge trials in accelerating SARS-CoV-2 vaccine development. Clin. Infect. Dis. 2021, 72, 710–715.
Torchilin, V. P. Recent advances with liposomes as pharmaceutical carriers. Nat. Rev. Drug Discov. 2005, 4, 145–160.
Tang, X. L.; Wu, C. C.; Li, X.; Song, Y. H.; Yao, X. M.; Wu, X. K.; Duan, Y. G.; Zhang, H.; Wang, Y. R.; Qian, Z. H. et al. On the origin and continuing evolution of SARS-CoV-2. Natl. Sci. Rev. 2020, 7, 1012–1023.
Wu, F.; Zhao, S.; Yu, B.; Chen, Y. M.; Wang, W.; Song, Z. G.; Hu, Y.; Tao, Z. W.; Tian, J. H.; Pei, Y. Y. et al. A new coronavirus associated with human respiratory disease in China. Nature 2020, 579, 265–269.
Belouzard, S.; Millet, J. K.; Licitra, B. N.; Whittaker, G. R. Mechanisms of coronavirus cell entry mediated by the viral spike protein. Viruses 2012, 4, 1011–1033.
Andersen, K. G.; Rambaut, A.; Lipkin, W. I.; Holmes, E. C.; Garry, R. F. The proximal origin of SARS-CoV-2. Nat. Med. 2020, 26, 450–452.
Konno, Y.; Kimura, I.; Uriu, K.; Fukushi, M.; Irie, T.; Koyanagi, Y.; Sauter, D.; Gifford, R. J.; USFQ-COVID19 Consortium; Nakagawa, S. et al. SARS-CoV-2 ORF3b is a potent interferon antagonist whose activity is increased by a naturally occurring elongation variant. Cell Rep. 2020, 32, 108185.
Hadjadj, J.; Yatim, N.; Barnabei, L.; Corneau, A.; Boussier, J.; Smith, N.; Péré, H.; Charbit, B.; Bondet, V.; Chenevier-Gobeaux, C. et al. Impaired type I interferon activity and inflammatory responses in severe COVID-19 patients. Science 2020, 369, 718–724.
Ivashkiv, L. B.; Donlin, L. T. Regulation of type I interferon responses. Nat. Rev. Immunol. 2014, 14, 36–49.
Park, A.; Iwasaki, A. Type I and type III interferons-induction, signaling, evasion, and application to combat COVID-19. Cell Host Microbe 2020, 27, 870–878.
Chan, J. F.; Kok, K. H.; Zhu, Z.; Chu, H.; To, K. K. W.; Yuan, S. F.; Yuen, K. Y. Genomic characterization of the 2019 novel human-pathogenic coronavirus isolated from a patient with atypical pneumonia after visiting Wuhan. Emerg. Microbes Infect. 2020, 9, 221–236.
Muth, D.; Corman, V. M.; Roth, H.; Binger, T.; Dijkman, R.; Gottula, L. T.; Gloza-Rausch, F.; Balboni, A.; Battilani, M.; Rihtarič, D. et al. Attenuation of replication by a 29 nucleotide deletion in SARS-coronavirus acquired during the early stages of human-to-human transmission. Sci. Rep. 2018, 8, 15177.
Su, Y. C. F.; Anderson, D. E.; Young, B. E.; Linster, M.; Zhu, F.; Jayakumar, J.; Zhuang, Y.; Kalimuddin, S.; Low, J. G. H.; Tan, C. W. et al. Discovery and Genomic Characterization of a 382-Nucleotide Deletion in ORF7b and ORF8 during the Early Evolution of SARS-CoV-2. mBio 2020, 11, e01610–e01620.
Young, B. E.; Fong, S. W.; Chan, Y. H.; Mak, T. M.; Ang, L. W.; Anderson, D. E.; Lee, C. Y. P.; Amrun, S. N.; Lee, B.; Goh, Y. S. et al. Effects of a major deletion in the SARS-CoV-2 genome on the severity of infection and the inflammatory response: An observational cohort study. Lancet 2020, 396, 603–611.
Kim, D.; Lee, J. Y.; Yang, J. S.; Kim, J. W.; Kim, V. N.; Chang, H. The architecture of SARS-CoV-2 transcriptome. Cell 2020, 181, 914–921.e10.
Bojkova, D.; Klann, K.; Koch, B.; Widera, M.; Krause, D.; Ciesek, S.; Cinatl, J.; Münch, C. Proteomics of SARS-CoV-2-infected host cells reveals therapy targets. Nature 2020, 583, 469–472.
Davidson, A. D.; Williamson, M. K.; Lewis, S.; Shoemark, D.; Carroll, M. W.; Heesom, K. J.; Zambon, M.; Ellis, J.; Lewis, P. A.; Hiscox, J. A. et al. Characterisation of the transcriptome and proteome of SARS-CoV-2 reveals a cell passage induced in-frame deletion of the furin-like cleavage site from the spike glycoprotein. Genome Med. 2020, 12, 68.
Li, M. Y.; Li, L.; Zhang, Y.; Wang, X. S. Expression of the SARS-CoV-2 cell receptor gene ACE2 in a wide variety of human tissues. Infect. Dis. Poverty 2020, 9, 45.
Hoffmann, M.; Kleine-Weber, H.; Pöhlmann, S. A multibasic cleavage site in the spike protein of SARS-CoV-2 is essential for infection of human lung cells. Mol. Cell 2020, 78, 779–784.e5.
Sawicki, S. G.; Sawicki, D. L.; Siddell, S. G. A contemporary view of coronavirus transcription. J. Virol. 2007, 81, 20–29.
Snijder, E. J.; van der Meer, Y.; Zevenhoven-Dobbe, J.; Onderwater, J. J. M.; van der Meulen, J.; Koerten, H. K.; Mommaas, A. M. Ultrastructure and origin of membrane vesicles associated with the severe acute respiratory syndrome coronavirus replication complex. J. Virol. 2006, 80, 5927–5940.
de Haan, C. A. M.; Rottier, P. J. M. Molecular interactions in the assembly of coronaviruses. Adv. Virus Res. 2005, 64, 165–230.
Raamsman, M. J. B.; Locker, J. K.; de Hooge, A.; de Vries, A. A. F.; Griffiths, G.; Vennema, H.; Rottier, P. J. M. Characterization of the coronavirus mouse hepatitis virus strain A59 small membrane protein E. J. Virol. 2000, 74, 2333–2342.
Wu, C. R.; Zheng, M. Z.; Yang, Y. Y.; Gu, X. X.; Yang, K. Y.; Li, M. X.; Liu, Y.; Zhang, Q. Z.; Zhang, P.; Wang, Y. L. et al. Furin: A potential therapeutic target for COVID-19. iScience 2020, 23, 101642.
Daly, J. L.; Simonetti, B.; Klein, K.; Chen, K. E.; Williamson, M. K.; Antón-Plágaro, C.; Shoemark, D. K.; Simón-Gracia, L.; Bauer, M.; Hollandi, R. et al. Neuropilin-1 is a host factor for SARS-CoV-2 infection. Science 2020, 370, 861–865.
Teesalu, T.; Sugahara, K. N.; Kotamraju, V. R.; Ruoslahti, E. C-end rule peptides mediate neuropilin-1-dependent cell, vascular, and tissue penetration. Proc. Natl. Acad. Sci. USA 2009, 106, 16157–16162.
Guo, H. F.; Vander Kooi, C. W. Neuropilin functions as an essential cell surface receptor. J. Biol. Chem. 2015, 290, 29120–29126.
Parker, M. W.; Guo, H. F.; Li, X. B.; Linkugel, A. D.; Vander Kooi, C. W. Function of members of the neuropilin family as essential pleiotropic cell surface receptors. Biochemistry 2012, 51, 9437–9446.
De Winter, F.; Holtmaat, A. J. G. D.; Verhaagen, J. Neuropilin and class 3 semaphorins in nervous system regeneration. Adv. Exp. Med. Biol. 2002, 515, 115–139.
Roy, S.; Bag, A. K.; Singh, R. K.; Talmadge, J. E.; Batra, S. K.; Datta, K. Multifaceted role of neuropilins in the immune system: Potential targets for immunotherapy. Front. Immunol. 2017, 8, 1228.
Kielian, M. Enhancing host cell infection by SARS-CoV-2. Science 2020, 370, 765–766.
Cantuti-Castelvetri, L.; Ojha, R.; Pedro, L. D.; Djannatian, M.; Franz, J.; Kuivanen, S.; van der Meer, F.; Kallio, K.; Kaya, T.; Anastasina, M. et al. Neuropilin-1 facilitates SARS-CoV-2 cell entry and infectivity. Science 2020, 370, 856–860.
Cheng, Y. W.; Chao, T. L.; Li, C. L.; Chiu, M. F.; Kao, H. C.; Wang, S. H.; Pang, Y. H.; Lin, C. H.; Tsai, Y. M.; Lee, W. H. et al. Furin inhibitors block SARS-CoV-2 spike protein cleavage to suppress virus production and cytopathic effects. Cell Rep. 2020, 33, 108254.
Hoffmann, M.; Kleine-Weber, H.; Schroeder, S.; Krüger, N.; Herrler, T.; Erichsen, S.; Schiergens, T. S.; Herrler, G.; Wu, N. H.; Nitsche, A. et al. SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor. Cell 2020, 181, 271–280.e8.
Heinrich, M. A.; Martina, B.; Prakash, J. Nanomedicine strategies to target coronavirus. Nano Today 2020, 35, 100961.
Xia, S.; Liu, M. Q.; Wang, C.; Xu, W.; Lan, Q. S.; Feng, S. L.; Qi, F. F.; Bao, L. L.; Du, L. Y.; Liu, S. W. et al. Inhibition of SARS-CoV-2 (previously 2019-nCoV) infection by a highly potent pan-coronavirus fusion inhibitor targeting its spike protein that harbors a high capacity to mediate membrane fusion. Cell Res. 2020, 30, 343–355.
Chan, J. F. W.; Yuan, S. F.; Kok, K. H.; To, K. K. W.; Chu, H.; Yang, J.; Xing, F. F.; Liu, J. L.; Yip, C. C. Y.; Poon, R. W. S. et al. A familial cluster of pneumonia associated with the 2019 novel coronavirus indicating person-to-person transmission: A study of a family cluster. Lancet 2020, 395, 514–523.
Fennelly, K. P. Particle sizes of infectious aerosols: Implications for infection control. Lancet Respir. Med. 2020, 8, 914–924.
Lednicky, J. A.; Lauzardo, M.; Fan, Z. H.; Jutla, A.; Tilly, T. B.; Gangwar, M.; Usmani, M.; Shankar, S. N.; Mohamed, K.; Eiguren-Fernandez, A. et al. Viable SARS-CoV-2 in the air of a hospital room with COVID-19 patients. Int. J. Infect. Dis. 2020, 100, 476–482.
Setti, L.; Passarini, F.; De Gennaro, G.; Barbieri, P.; Perrone, M. G.; Borelli, M.; Palmisani, J.; Di Gilio, A.; Piscitelli, P.; Miani, A. Airborne transmission route of COVID-19: Why 2 meters/6 feet of inter-personal distance could not be enough. Int. J. Environ. Res. Public Health 2020, 17, 2932.
Fiegel, J.; Clarke, R.; Edwards, D. A. Airborne infectious disease and the suppression of pulmonary bioaerosols. Drug Discov. Today 2006, 11, 51–57.
Thomas, R. J. Particle size and pathogenicity in the respiratory tract. Virulence 2013, 4, 847–858.
van Doremalen, N.; Bushmaker, T.; Morris, D. H.; Holbrook, M. G.; Gamble, A.; Williamson, B. N.; Tamin, A.; Harcourt, J. L.; Thornburg, N. J.; Gerber, S. I. et al. Aerosol and surface stability of SARS-CoV-2 as compared with SARS-CoV-1. N. Engl. J. Med. 2020, 382, 1564–1567.
Aboubakr, H. A.; Sharafeldin, T. A.; Goyal, S. M. Stability of SARS-CoV-2 and other coronaviruses in the environment and on common touch surfaces and the influence of climatic conditions: A review. Transbound. Emerg. Dis. 2021, 68, 296–312.
Chia, P. Y.; Coleman, K. K.; Tan, Y. K.; Ong, S. W. X.; Gum, M.; Lau, S. K.; Lim, X. F.; Lim, A. S.; Sutjipto, S.; Lee, P. H. et al. Detection of air and surface contamination by SARS-CoV-2 in hospital rooms of infected patients. Nat. Commun. 2020, 11, 2800.
Santarpia, J. L.; Rivera, D. N.; Herrera, V. L.; Morwitzer, M. J.; Creager, H. M.; Santarpia, G. W.; Crown, K. K.; Brett-Major, D. M.; Schnaubelt, E. R.; Broadhurst, M. J. et al. Aerosol and surface contamination of SARS-CoV-2 observed in quarantine and isolation care. Sci. Rep. 2020, 10, 12732.
Buonanno, M.; Welch, D.; Shuryak, I.; Brenner, D. J. Far-UVC light (222 nm) efficiently and safely inactivates airborne human coronaviruses. Sci. Rep. 2020, 10, 10285.
Pastorino, B.; Touret, F.; Gilles, M.; de Lamballerie, X.; Charrel, R. N. Heat inactivation of different types of SARS-CoV-2 samples: What protocols for biosafety, molecular detection and serological diagnostics? Viruses 2020, 12, 735.
Anderson, D. E.; Sivalingam, V.; Kang, A. E. Z.; Ananthanarayanan, A.; Arumugam, H.; Jenkins, T. M.; Hadjiat, Y.; Eggers, M. Povidone-iodine demonstrates rapid in vitro virucidal activity against SARS-CoV-2, the virus causing COVID-19 disease. Infect. Dis. Ther. 2020, 9, 669–675.
Kampf, G. Potential role of inanimate surfaces for the spread of coronaviruses and their inactivation with disinfectant agents. Infect. Prev. Pract. 2020, 2, 100044.
Huang, C. L.; Wang, Y. M.; Li, X. W.; Ren, L. L.; Zhao, J. P.; Hu, Y.; Zhang, L.; Fan, G. H.; Xu, J. Y.; Gu, X. Y. et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet 2020, 395, 497–506.
Qiu, H. Y.; Wu, J. H.; Hong, L.; Luo, Y. L.; Song, Q. F.; Chen, D. Clinical and epidemiological features of 36 children with coronavirus disease 2019 (COVID-19) in Zhejiang, China: An observational cohort study. Lancet Infect. Dis. 2020, 20, 689–696.
Du, R. H.; Liang, L. R.; Yang, C. Q.; Wang, W.; Cao, T. Z.; Li, M.; Guo, G. Y.; Du, J.; Zheng, C. L.; Zhu, Q. et al. Predictors of mortality for patients with COVID-19 pneumonia caused by SARS-CoV-2: A prospective cohort study. Eur. Respir. J. 2020, 55, 2000524.
Agyeman, A. A.; Chin, K. L.; Landersdorfer, C. B.; Liew, D.; Ofori-Asenso, R. Smell and taste dysfunction in patients with COVID-19: A systematic review and meta-analysis. Mayo Clin. Proc. 2020, 95, 1621–1631.
Klopfenstein, T.; Kadiane-Oussou, N. J.; Toko, L.; Royer, P. Y.; Lepiller, Q.; Gendrin, V.; Zayet, S. Features of anosmia in COVID-19. Med. Mal. Infect. 2020, 50, 436–439.
Vaira, L. A.; Salzano, G.; Deiana, G.; De Riu, G. Anosmia and ageusia: Common findings in COVID-19 patients. Laryngoscope 2020, 130, 1787.
Al-Zaidi, H. M. H.; Badr, H. M. Incidence and recovery of smell and taste dysfunction in COVID-19 positive patients. Egypt. J. Otolaryngol. 2020, 36, 47.
Lechien, J. R.; Chiesa-Estomba, C. M.; De Siati, D. R.; Horoi, M.; Le Bon, S. D.; Rodriguez, A.; Dequanter, D.; Blecic, S.; El Afia, F.; Distinguin, L. et al. Olfactory and gustatory dysfunctions as a clinical presentation of mild-to-moderate forms of the coronavirus disease (COVID-19): A multicenter European study. Eur. Arch. Oto-Rhino-Laryngol. 2020, 277, 2251–2261.
Guan, W. J.; Ni, Z. Y.; Hu, Y.; Liang, W. H.; Ou, C. Q.; He, J. X.; Liu, L.; Shan, H.; Lei, C. L.; Hui, D. S. C. et al. Clinical characteristics of coronavirus disease 2019 in China. N. Engl. J. Med. 2020, 382, 1708–1720.
Pung, R.; Chiew, C. J.; Young, B. E.; Chin, S.; Chen, M. I. C.; Clapham, H. E.; Cook, A. R.; Maurer-Stroh, S.; Toh, M. P. H. S.; Poh, C. et al. Investigation of three clusters of COVID-19 in Singapore: Implications for surveillance and response measures. Lancet 2020, 395, 1039–1046.
Yan, Y.; Chang, L.; Wang, L. N. Laboratory testing of SARS-CoV, MERS-CoV, and SARS-CoV-2 (2019-nCoV): Current status, challenges, and countermeasures. Rev. Med. Virol. 2020, 30, e2106.
Zhou, H.; Chen, X.; Hu, T.; Li, J.; Song, H.; Liu, Y. R.; Wang, P. H.; Liu, D.; Yang, J.; Holmes, E. C. et al. A novel bat coronavirus closely related to SARS-CoV-2 contains natural insertions at the S1/S2 cleavage site of the spike protein. Curr. Biol. 2020, 30, 2196–2206.e3.
Zhao, J. J.; Yuan, Q.; Wang, H. Y.; Liu, W.; Liao, X. J.; Su, Y. Y.; Wang, X.; Yuan, J.; Li, T. D.; Li, J. X. et al. Antibody responses to SARS-CoV-2 in patients with novel coronavirus disease 2019. Clin. Infect. Dis. 2020, 71, 2027–2034.
Li, Z. T.; Yi, Y. X.; Luo, X. M.; Xiong, N.; Liu, Y.; Li, S. Q.; Sun, R. L.; Wang, Y. Q.; Hu, B. C.; Chen, W. et al. Development and clinical application of a rapid IgM-IgG combined antibody test for SARS-CoV-2 infection diagnosis. J. Med. Virol. 2020, 92, 1518–1524.
Xiao, A. T.; Gao, C.; Zhang, S. Profile of specific antibodies to SARS-CoV-2: The first report. J. Infect. 2020, 81, 147–178.
Yu, H. Q.; Sun, B. Q.; Fang, Z. F.; Zhao, J. C.; Liu, X. Y.; Li, Y. M.; Sun, X. Z.; Liang, H. F.; Zhong, B.; Huang, Z. F. et al. Distinct features of SARS-CoV-2-specific IgA response in COVID-19 patients. Eur. Respir. J. 2020, 56, 2001526.
Zhou, P.; Yang, X. L.; Wang, X. G.; Hu, B.; Zhang, L.; Zhang, W.; Si, H. R.; Zhu, Y.; Li, B.; Huang, C. L. et al. A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature 2020, 579, 270–273.
Katze, M. G.; He, Y. P.; Gale, M. Jr. Viruses and interferon: A fight for supremacy. Nat. Rev. Immunol. 2002, 2, 675–687.
Stanifer, M. L.; Kee, C.; Cortese, M.; Zumaran, C. M.; Triana, S.; Mukenhirn, M.; Kraeusslich, H. G.; Alexandrov, T.; Bartenschlager, R.; Boulant, S. Critical role of type III interferon in controlling SARS-CoV-2 infection in human intestinal epithelial cells. Cell Rep. 2020, 32, 107863.
Broggi, A.; Ghosh, S.; Sposito, B.; Spreafico, R.; Balzarini, F.; Lo Cascio, A.; Clementi, N.; De Santis, M.; Mancini, N.; Granucci, F. et al. Type III interferons disrupt the lung epithelial barrier upon viral recognition. Science 2020, 369, 706–712.
Blanco-Melo, D.; Nilsson-Payant, B. E.; Liu, W. C.; Uhl, S.; Hoagland, D.; Møller, R.; Jordan, T. X.; Oishi, K.; Panis, M.; Sachs, D. et al. Imbalanced host response to SARS-CoV-2 drives development of COVID-19. Cell 2020, 181, 1036–1045.e9.
Pedersen, S. F.; Ho, Y. C. SARS-CoV-2: A storm is raging. J. Clin. Invest. 2020, 130, 2202–2205.
Mantlo, E.; Bukreyeva, N.; Maruyama, J.; Paessler, S.; Huang, C. Antiviral activities of type I interferons to SARS-CoV-2 infection. Antiviral Res. 2020, 179, 104811.
Weiskopf, D.; Schmitz, K. S.; Raadsen, M. P.; Grifoni, A.; Okba, N. M. A.; Endeman, H.; van den Akker, J. P. C.; Molenkamp, R.; Koopmans, M. P. G.; van Gorp, E. C. M. et al. Phenotype and kinetics of SARS-CoV-2–specific T cells in COVID-19 patients with acute respiratory distress syndrome. Sci. Immunol. 2020, 5, eabd2071.
Grifoni, A.; Weiskopf, D.; Ramirez, S. I.; Mateus, J.; Dan, J. M.; Moderbacher, C. R.; Rawlings, S. A.; Sutherland, A.; Premkumar, L.; Jadi, R. S. et al. Targets of T cell responses to SARS-CoV-2 coronavirus in humans with COVID-19 disease and unexposed individuals. Cell 2020, 181, 1489–1501,e15.
Chu, D. K. W.; Pan, Y.; Cheng, S. M. S.; Hui, K. P. Y.; Krishnan, P.; Liu, Y. Z.; Ng, D. Y. M.; Wan, C. K. C.; Yang, P.; Wang, Q. Y. et al. Molecular diagnosis of a novel coronavirus (2019-nCoV) causing an outbreak of pneumonia. Clin. Chem. 2020, 66, 549–555.
Wang, D. W.; Hu, B.; Hu, C.; Zhu, F. F.; Liu, X.; Zhang, J.; Wang, B. B.; Xiang, H.; Cheng, Z. S.; Xiong, Y. et al. Clinical characteristics of 138 hospitalized patients with 2019 novel coronavirus-infected pneumonia in Wuhan, China. JAMA 2020, 323, 1061–1069.
Yan, C.; Cui, J.; Huang, L.; Du, B.; Chen, L.; Xue, G.; Li, S.; Zhang, W.; Zhao, L.; Sun, Y. et al. Rapid and visual detection of 2019 novel coronavirus (SARS-CoV-2) by a reverse transcription loop-mediated isothermal amplification assay. Clin. Microbiol. Infect. 2020, 26, 773–779.
Patchsung, M.; Jantarug, K.; Pattama, A.; Aphicho, K.; Suraritdechachai, S.; Meesawat, P.; Sappakhaw, K.; Leelahakorn, N.; Ruenkam, T.; Wongsatit, T. et al. Clinical validation of a Cas13-based assay for the detection of SARS-CoV-2 RNA. Nat. Biomed. Eng. 2020, 4, 1140–1149.
Kim, C.; Ahmed, J. A.; Eidex, R. B.; Nyoka, R.; Waiboci, L. W.; Erdman, D.; Tepo, A.; Mahamud, A. S.; Kabura, W.; Nguhi, M. et al. Comparison of nasopharyngeal and oropharyngeal swabs for the diagnosis of eight respiratory viruses by real-time reverse transcription-PCR assays. PLoS One 2011, 6, e21610.
Vashist, S. K. In vitro diagnostic assays for COVID-19: Recent advances and emerging trends. Diagnostics 2020, 10, 202.
Liu, W. B.; Liu, L.; Kou, G. M.; Zheng, Y. Q.; Ding, Y. J.; Ni, W. X.; Wang, Q. S.; Tan, L.; Wu, W. L.; Tang, S. et al. Evaluation of nucleocapsid and spike protein-based enzyme-linked immunosorbent assays for detecting antibodies against SARS-CoV-2. J. Clin. Microbiol. 2020, 58, e00461–20.
Wölfel, R.; Corman, V. M.; Guggemos, W.; Seilmaier, M.; Zange, S.; Müller, M. A.; Niemeyer, D.; Jones, T. C.; Vollmar, P.; Rothe, C. et al. Virological assessment of hospitalized patients with COVID-2019. Nature 2020, 581, 465–469.
Zhang, W.; Du, R. H.; Li, B.; Zheng, X. S.; Yang, X. L.; Hu, B.; Wang, Y. Y.; Xiao, G. F.; Yan, B.; Shi, Z. L. et al. Molecular and serological investigation of 2019-nCoV infected patients: Implication of multiple shedding routes. Emerg. Microbes Infect. 2020, 9, 386–389.
Li, Y.; Xia, L. M. Coronavirus disease 2019 (COVID-19): Role of chest CT in diagnosis and management. Am. J. Roentgenol. 2020, 214, 1280–1286.
Ng, M. Y.; Lee, E. Y. P.; Yang, J.; Yang, F. F.; Li, X.; Wang, H. X.; Lui, M. M. S.; Lo, C. S. Y.; Leung, B.; Khong, P. L. et al. Imaging profile of the COVID-19 infection: Radiologic findings and literature review. Radiol. Cardiothorac. Imaging 2020, 2, e200034.
Mueller, S.; Papamichail, D.; Coleman, J. R.; Skiena, S.; Wimmer, E. Reduction of the rate of poliovirus protein synthesis through large-scale codon deoptimization causes attenuation of viral virulence by lowering specific infectivity. J. Virol. 2006, 80, 9687–9696.
Nogales, A.; Baker, S. F.; Ortiz-Riaño, E.; Dewhurst, S.; Topham, D. J.; Martínez-Sobrido, L. Influenza a virus attenuation by codon deoptimization of the NS gene for vaccine development. J. Virol. 2014, 88, 10525–10540.
Dilucca, M.; Forcelloni, S.; Georgakilas, A. G.; Giansanti, A.; Pavlopoulou, A. Codon usage and phenotypic divergences of SARS-CoV-2 genes. Viruses 2020, 12, 498.
Tort, F. L.; Castells, M.; Cristina, J. A comprehensive analysis of genome composition and codon usage patterns of emerging coronaviruses. Virus Res. 2020, 283, 197976.
Dudek, T.; Knipe, D. M. Replication-defective viruses as vaccines and vaccine vectors. Virology 2006, 344, 230–239.
Lau, S. Y.; Wang, P.; Mok, B. W. Y.; Zhang, A. J.; Chu, H.; Lee, A. C. Y.; Deng, S. F.; Chen, P.; Chan, K. H.; Song, W. J. et al. Attenuated SARS-CoV-2 variants with deletions at the S1/S2 junction. Emerg. Microbes Infect. 2020, 9, 837–842.
Bull, J. J.; Smithson, M. W.; Nuismer, S. L. Transmissible viral vaccines. Trends Microbiol. 2018, 26, 6–15.
Seo, H. S. Application of radiation technology in vaccines development. Clin. Exp. Vaccine Res. 2015, 4, 145–158.
He, Y. X.; Zhou, Y. S.; Siddiqui, P.; Jiang, S. B. Inactivated SARS-CoV vaccine elicits high titers of spike protein-specific antibodies that block receptor binding and virus entry. Biochem. Biophys. Res. Commun. 2004, 325, 445–452.
Gao, Q.; Bao, L. L.; Mao, H. Y.; Wang, L.; Xu, K. W.; Yang, M. N.; Li, Y. J.; Zhu, L.; Wang, N.; Lv, Z. et al. Development of an inactivated vaccine candidate for SARS-CoV-2. Science 2020, 369, 77–81.
Bouard, D.; Alazard-Dany, D.; Cosset, F. L. Viral vectors: From virology to transgene expression. Br. J. Pharmacol. 2009, 157, 153–165.
Pinschewer, D. D. Virally vectored vaccine delivery: Medical needs, mechanisms, advantages and challenges. Swiss Med. Wkly. 2017, 147, w14465.
Robert-Guroff, M. Replicating and non-replicating viral vectors for vaccine development. Curr. Opin. Biotechnol. 2007, 18, 546–556.
Billeter, M. A.; Naim, H. Y.; Udem, S. A. Reverse genetics of measles virus and resulting multivalent recombinant vaccines: Applications of recombinant measles viruses. Curr. Top. Microbiol. Immunol. 2009, 329, 129–162.
Malczyk, A. H.; Kupke, A.; Prüfer, S.; Scheuplein, V. A.; Hutzler, S.; Kreuz, D.; Beissert, T.; Bauer, S.; Hubich-Rau, S.; Tondera, C. et al. A highly immunogenic and protective middle east respiratory syndrome coronavirus vaccine based on a recombinant measles virus vaccine platform. J. Virol. 2015, 89, 11654–11667.
Escriou, N.; Callendret, B.; Lorin, V.; Combredet, C.; Marianneau, P.; Février, M.; Tangy, F. Protection from SARS coronavirus conferred by live measles vaccine expressing the spike glycoprotein. Virology 2014, 452–453, 32–41.
Liniger, M.; Zuniga, A.; Tamin, A.; Azzouz-Morin, T. N.; Knuchel, M.; Marty, R. R.; Wiegand, M.; Weibel, S.; Kelvin, D.; Rota, P. A. et al. Induction of neutralising antibodies and cellular immune responses against SARS coronavirus by recombinant measles viruses. Vaccine 2008, 26, 2164–2174.
Mura, M.; Ruffié, C.; Combredet, C.; Aliprandini, E.; Formaglio, P.; Chitnis, C. E.; Amino, R.; Tangy, F. Recombinant measles vaccine expressing malaria antigens induces long-term memory and protection in mice. npj Vaccines 2019, 4, 12.
Liniger, M.; Zuniga, A.; Morin, T. N.; Combardiere, B.; Marty, R.; Wiegand, M.; Ilter, O.; Knuchel, M.; Naim, H. Y. Recombinant measles viruses expressing single or multiple antigens of human immunodeficiency virus (HIV-1) induce cellular and humoral immune responses. Vaccine 2009, 27, 3299–3305.
Kapadia, S. U.; Rose, J. K.; Lamirande, E.; Vogel, L.; Subbarao, K.; Roberts, A. Long-term protection from SARS coronavirus infection conferred by a single immunization with an attenuated VSV-based vaccine. Virology 2005, 340, 174–182.
Nicklin, S. A.; Wu, E.; Nemerow, G. R.; Baker, A. H. The influence of adenovirus fiber structure and function on vector development for gene therapy. Mol. Ther. 2005, 12, 384–393.
Charman, M.; Herrmann, C.; Weitzman, M. D. Viral and cellular interactions during adenovirus DNA replication. FEBS Lett. 2019, 593, 3531–3550.
Fessler, S. P.; Young, C. S. H. Control of adenovirus early gene expression during the late phase of infection. J. Virol. 1998, 72, 4049–4056.
Persson, H.; Philipson, L. Regulation of adenovirus gene expression. Curr. Top. Microbiol. Immunol. 1982, 97, 157–203.
Bauer, U.; Flunker, G.; Bruss, K.; Kallwellis, K.; Liebermann, H.; Luettich, T.; Motz, M.; Seidel, W. Detection of antibodies against adenovirus protein IX, fiber, and hexon in human sera by immunoblot assay. J. Clin. Microbiol. 2005, 43, 4426–4433.
Hashimoto, S.; Gonzalez, G.; Harada, S.; Oosako, H.; Hanaoka, N.; Hinokuma, R.; Fujimoto, T. Recombinant type Human mastadenovirus D85 associated with epidemic keratoconjunctivitis since 2015 in Japan. J. Med. Virol. 2018, 90, 881–889.
Bridge, E.; Ketner, G. Redundant control of adenovirus late gene expression by early region 4. J. Virol. 1989, 63, 631–638.
Rubinchik, S.; Woraratanadharm, J.; Schepp, J.; Dong, J. Y. Improving the transcriptional regulation of genes delivered by adenovirus vectors. Methods Mol. Med. 2003, 76, 167–199.
Bett, A. J.; Prevec, L.; Graham, F. L. Packaging capacity and stability of human adenovirus type 5 vectors. J. Virol. 1993, 67, 5911–5921.
Wold, W. S. M.; Toth, K. Adenovirus vectors for gene therapy, vaccination and cancer gene therapy. Curr. Gene Ther. 2013, 13, 421–433.
Zhu, F. C.; Li, Y. H.; Guan, X. H.; Hou, L. H.; Wang, W. J.; Li, J. X.; Wu, S. P.; Wang, B. S.; Wang, Z.; Wang, L. et al. Safety, tolerability, and immunogenicity of a recombinant adenovirus type-5 vectored COVID-19 vaccine: A dose-escalation, open-label, non-randomised, first-in-human trial. Lancet 2020, 395, 1845–1854.
Ng, P.; Parks, R. J.; Cummings, D. T.; Evelegh, C. M.; Graham, F. L. An enhanced system for construction of adenoviral vectors by the two-plasmid rescue method. Hum. Gene Ther. 2000, 11, 693–699.
Bos, R.; Rutten, L.; van der Lubbe, J. E. M.; Bakkers, M. J. G.; Hardenberg, G.; Wegmann, F.; Zuijdgeest, D.; de Wilde, A. H.; Koornneef, A.; Verwilligen, A. et al. Ad26 vector-based COVID-19 vaccine encoding a prefusion-stabilized SARS-CoV-2 Spike immunogen induces potent humoral and cellular immune responses. npj Vaccines 2020, 5, 91.
Abbink, P.; Lemckert, A. A. C.; Ewald, B. A.; Lynch, D. M.; Denholtz, M.; Smits, S.; Holterman, L.; Damen, I.; Vogels, R.; Thorner, A. R. et al. Comparative seroprevalence and immunogenicity of six rare serotype recombinant adenovirus vaccine vectors from subgroups B and D. J. Virol. 2007, 81, 4654–4663.
Yu, J.; Tostanoski, L. H.; Mercado, N. B.; McMahan, K.; Liu, J. Y.; Jacob-Dolan, C.; Chandrashekar, A.; Atyeo, C.; Martinez, D. R.; Anioke, T. et al. Protective efficacy of Ad26.COV2.S against SARS-CoV-2 B.1.351 in macaques. Nature 2021, 596, 423–427.
Tostanoski, L. H.; Wegmann, F.; Martinot, A. J.; Loos, C.; McMahan, K.; Mercado, N. B.; Yu, J. Y.; Chan, C. N.; Bondoc, S.; Starke, C. E. et al. Ad26 vaccine protects against SARS-CoV-2 severe clinical disease in hamsters. Nat. Med. 2020, 26, 1694–1700.
Mercado, N. B.; Zahn, R.; Wegmann, F.; Loos, C.; Chandrashekar, A.; Yu, J. Y.; Liu, J. Y.; Peter, L.; McMahan, K.; Tostanoski, L. H. et al. Single-shot Ad26 vaccine protects against SARS-CoV-2 in rhesus macaques. Nature 2020, 586, 583–588.
Stephenson, K. E.; Le Gars, M.; Sadoff, J.; de Groot, A. M.; Heerwegh, D.; Truyers, C.; Atyeo, C.; Loos, C.; Chandrashekar, A.; McMahan, K. et al. Immunogenicity of the Ad26. COV2. S vaccine for COVID-19. JAMA 2021, 325, 1535–1544.
Sadoff, J.; Le Gars, M.; Shukarev, G.; Heerwegh, D.; Truyers, C.; de Groot, A. M.; Stoop, J.; Tete, S.; Van Damme, W.; Leroux-Roels, I. et al. Interim results of a phase 1–2a trial of Ad26. COV2. S Covid-19 vaccine. N. Engl. J. Med. 2021, 384, 1824–1835.
Alter, G.; Yu, J. Y.; Liu, J. Y.; Chandrashekar, A.; Borducchi, E. N.; Tostanoski, L. H.; McMahan, K.; Jacob-Dolan, C.; Martinez, D. R.; Chang, A. Q. et al. Immunogenicity of Ad26.COV2.S vaccine against SARS-CoV-2 variants in humans. Nature 2021, 596, 268–272.
Rux, J. J.; Kuser, P. R.; Burnett, R. M. Structural and phylogenetic analysis of adenovirus hexons by use of high-resolution X-ray crystallographic, molecular modeling, and sequence-based methods. J. Virol. 2003, 77, 9553–9566.
Rogers, N. G.; Basnight, M.; Gibbs Jun, C. J.; Gajdusek, D. C. Latent viruses in chimpanzees with experimental kuru. Nature 1967, 216, 446–449.
Basnight, M. Jr.; Rogers, N. G.; Gibbs, C. J. Jr.; Gajdusek, D. C. Characterization of four new adenovirus serotypes isolated from chimpanzee tissue explants. Am. J. Epidemiol. 1971, 94, 166–171.
Davison, A. J.; Benkő, M.; Harrach, B. Genetic content and evolution of adenoviruses. J. Gen. Virol. 2003, 84, 2895–2908.
Roy, S.; Gao, G. P.; Clawson, D. S.; Vandenberghe, L. H.; Farina, S. F.; Wilson, J. M. Complete nucleotide sequences and genome organization of four chimpanzee adenoviruses. Virology 2004, 324, 361–372.
Farina, S. F.; Gao, G. P.; Xiang, Z. Q.; Rux, J. J.; Burnett, R. M.; Alvira, M. R.; Marsh, J.; Ertl, H. C. J.; Wilson, J. M. Replication-defective vector based on a chimpanzee adenovirus. J. Virol. 2001, 75, 11603–11613.
Wang, X.; Xing, M.; Zhang, C.; Yang, Y.; Chi, Y. D.; Tang, X. Y.; Zhang, H. B.; Xiong, S. D.; Yu, L. G.; Zhou, D. M. Neutralizing antibody responses to enterovirus and adenovirus in healthy adults in China. Emerg. Microbes Infect. 2014, 3, 1–6.
Chirmule, N.; Propert, K. J.; Magosin, S. A.; Qian, Y.; Qian, R.; Wilson, J. M. Immune responses to adenovirus and adeno-associated virus in humans. Gene Ther. 1999, 6, 1574–1583.
Xiang, Z. Q.; Li, Y.; Cun, A.; Yang, W.; Ellenberg, S.; Switzer, W. M.; Kalish, M. L.; Ertl, H. C. J. Chimpanzee adenovirus antibodies in humans, sub-Saharan Africa. Emerg. Infect. Dis. 2006, 12, 1596–1599.
Fitzgerald, J. C.; Gao, G. P.; Reyes-Sandoval, A.; Pavlakis, G. N.; Xiang, Z. Q.; Wlazlo, A. P.; Giles-Davis, W.; Wilson, J. M.; Ertl, H. C. J. A simian replication-defective adenoviral recombinant vaccine to HIV-1 gag. J. Immunol. 2003, 170, 1416–1422.
Xiang, Z. Q.; Gao, G. P.; Reyes-Sandoval, A.; Cohen, C. J.; Li, Y.; Bergelson, J. M.; Wilson, J. M.; Ertl, H. C. J. Novel, chimpanzee serotype 68-based adenoviral vaccine carrier for induction of antibodies to a transgene product. J. Virol. 2002, 76, 2667–2675.
Kobinger, G. P.; Feldmann, H.; Zhi, Y.; Schumer, G.; Gao, G. P.; Feldmann, F.; Jones, S.; Wilson, J. M. Chimpanzee adenovirus vaccine protects against Zaire Ebola virus. Virology 2006, 346, 394–401.
Hillis, W. D.; Goodman, R. Serologic classification of chimpanzee adenoviruses by hemagglutination and hemagglutination inhibition. J. Immunol. 1969, 103, 1089–1095.
Dicks, M. D. J.; Spencer, A. J.; Edwards, N. J.; Wadell, G.; Bojang, K.; Gilbert, S. C.; Hill, A. V. S.; Cottingham, M. G. A novel chimpanzee adenovirus vector with low human seroprevalence: Improved systems for vector derivation and comparative immunogenicity. PLoS One 2012, 7, e40385.
van Doremalen, N.; Haddock, E.; Feldmann, F.; Meade-White, K.; Bushmaker, T.; Fischer, R. J.; Okumura, A.; Hanley, P. W.; Saturday, G.; Edwards, N. J. et al. A single dose of ChAdOx1 MERS provides protective immunity in rhesus macaques. Sci. Adv. 2020, 6, eaba8399.
van Doremalen, N.; Lambe, T.; Spencer, A.; Belij-Rammerstorfer, S.; Purushotham, J. N.; Port, J. R.; Avanzato, V. A.; Bushmaker, T.; Flaxman, A.; Ulaszewska, M. et al. ChAdOx1 nCoV-19 vaccine prevents SARS-CoV-2 pneumonia in rhesus macaques. Nature 2020, 586, 578–582.
Ramasamy, M. N.; Minassian, A. M.; Ewer, K. J.; Flaxman, A. L.; Folegatti, P. M.; Owens, D. R.; Voysey, M.; Aley, P. K.; Angus, B.; Babbage, G. et al. Safety and immunogenicity of ChAdOx1 nCoV-19 vaccine administered in a prime-boost regimen in young and old adults (COV002): A single-blind, randomised, controlled, phase 2/3 trial. Lancet 2021, 396, 1979–1993.
Chaplin, D. D. Overview of the immune response. J. Allergy Clin. Immunol. 2010, 125, S3–S23.
Pollard, A. J.; Bijker, E. M. A guide to vaccinology: From basic principles to new developments. Nat. Rev. Immunol. 2021, 21, 83–100.
Ng, O. W.; Chia, A.; Tan, A. T.; Jadi, R. S.; Leong, H. N.; Bertoletti, A.; Tan, Y. J. Memory T cell responses targeting the SARS coronavirus persist up to 11 years post-infection. Vaccine 2016, 34, 2008–2014.
Kang, S. S.; Yang, M.; Hong, Z. S.; Zhang, L. P.; Huang, Z. X.; Chen, X. X.; He, S. H.; Zhou, Z. L.; Zhou, Z. C.; Chen, Q. Y. et al. Crystal structure of SARS-CoV-2 nucleocapsid protein RNA binding domain reveals potential unique drug targeting sites. Acta Pharm. Sin. B 2020, 10, 1228–1238.
Dutta, N. K.; Mazumdar, K.; Gordy, J. T. The nucleocapsid protein of SARS-CoV-2: A target for vaccine development. J. Virol. 2020, 94, e00647–20.
Chen, H. Z.; Tang, L. L.; Yu, X. L.; Zhou, J.; Chang, Y. F.; Wu, X. Bioinformatics analysis of epitope-based vaccine design against the novel SARS-CoV-2. Infect. Dis. Poverty 2020, 9, 88.
Sun, Q. H.; Radosz, M.; Shen, Y. Q. Challenges in design of translational nanocarriers. J. Control. Release 2012, 164, 156–169.
Sun, Q. H.; Zhou, Z. X.; Qiu, N. S.; Shen, Y. Q. Rational design of cancer nanomedicine: Nanoproperty integration and synchronization. Adv. Mater. 2017, 29, 1606628.
Ganguly, P.; Breen, A.; Pillai, S. C. Toxicity of nanomaterials: Exposure, pathways, assessment, and recent advances. ACS Biomater. Sci. Eng. 2018, 4, 2237–2275.
Sharifi, S.; Behzadi, S.; Laurent, S.; Forrest, M. L.; Stroeve, P.; Mahmoudi, M. Toxicity of nanomaterials. Chem. Soc. Rev. 2012, 41, 2323–2343.
Moitra, P.; Alafeef, M.; Dighe, K.; Frieman, M. B.; Pan, D. Selective naked-eye detection of SARS-CoV-2 mediated by N gene targeted antisense oligonucleotide capped plasmonic nanoparticles. ACS Nano 2020, 14, 7617–7627.
Balagna, C.; Perero, S.; Percivalle, E.; Nepita, E. V.; Ferraris, M. Virucidal effect against coronavirus SARS-CoV-2 of a silver nanocluster/silica composite sputtered coating. Open Ceram. 2020, 1, 100006.
Islam, N.; Ferro, V. Recent advances in chitosan-based nanoparticulate pulmonary drug delivery. Nanoscale 2016, 8, 14341–14358.
Schwendener, R. A. Liposomes as vaccine delivery systems: A review of the recent advances. Ther. Adv. Vaccines 2014, 2, 159–182.
Gharbavi, M.; Amani, J.; Kheiri-Manjili, H.; Danafar, H.; Sharafi, A. Niosome: A promising nanocarrier for natural drug delivery through blood–brain barrier. Adv. Pharmacol. Sci. 2018, 2018, 6847971.
Bobo, D.; Robinson, K. J.; Islam, J.; Thurecht, K. J.; Corrie, S. R. Nanoparticle-based medicines: A review of FDA-approved materials and clinical trials to date. Pharm. Res. 2016, 33, 2373–2387.
Gabizon, A.; Papahadjopoulos, D. Liposome formulations with prolonged circulation time in blood and enhanced uptake by tumors. Proc. Natl. Acad. Sci. USA 1988, 85, 6949–6953.
Bal, S. M.; Hortensius, S.; Ding, Z.; Jiskoot, W.; Bouwstra, J. A. Co-encapsulation of antigen and Toll-like receptor ligand in cationic liposomes affects the quality of the immune response in mice after intradermal vaccination. Vaccine 2011, 29, 1045–1052.
Zhuang, Y.; Ma, Y. F.; Wang, C.; Hai, L.; Yan, C.; Zhang, Y. J.; Liu, F. Z.; Cai, L. T. PEGylated cationic liposomes robustly augment vaccine-induced immune responses: Role of lymphatic trafficking and biodistribution. J. Control. Release 2012, 159, 135–142.
Kumari, A.; Yadav, S. K.; Yadav, S. C. Biodegradable polymeric nanoparticles based drug delivery systems. Colloids Surf. B Biointerfaces 2010, 75, 1–18.
Makadia, H. K.; Siegel, S. J. Poly lactic-co-glycolic acid (PLGA) as biodegradable controlled drug delivery carrier. Polymers 2011, 3, 1377–1397.
Feczkó, T.; Tóth, J.; Dósa, G.; Gyenis, J. Optimization of protein encapsulation in PLGA nanoparticles. Chem. Eng. Proc. Process Intensificat. 2011, 50, 757–765.
Moon, J. J.; Suh, H.; Polhemus, M. E.; Ockenhouse, C. F.; Yadava, A.; Irvine, D. J. Antigen-displaying lipid-enveloped PLGA nanoparticles as delivery agents for a Plasmodium vivax malaria vaccine. PLoS One 2012, 7, e31472.
Tamada, J. A.; Langer, R. Erosion kinetics of hydrolytically degradable polymers. Proc. Natl. Acad. Sci. USA 1993, 90, 552–556.
Abbasi, E.; Aval, S. F.; Akbarzadeh, A.; Milani, M.; Nasrabadi, H. T.; Joo, S. W.; Hanifehpour, Y.; Nejati-Koshki, K.; Pashaei-Asl, R. Dendrimers: Synthesis, applications, and properties. Nanoscale Res. Lett. 2014, 9, 247.
Kannan, R. M.; Nance, E.; Kannan, S.; Tomalia, D. A. Emerging concepts in dendrimer-based nanomedicine: From design principles to clinical applications. J. Intern. Med. 2014, 276, 579–617.
Braun, C. S.; Vetro, J. A.; Tomalia, D. A.; Koe, G. S.; Koe, J. G.; Middaugh, C. R. Structure/function relationships of polyamidoamine/DNA dendrimers as gene delivery vehicles. J. Pharm. Sci. 2005, 94, 423–436.
Daftarian, P.; Kaifer, A. E.; Li, W.; Blomberg, B. B.; Frasca, D.; Roth, F.; Chowdhury, R.; Berg, E. A.; Fishman, J. B.; Al Sayegh, H. A. et al. Peptide-conjugated PAMAM dendrimer as a universal DNA vaccine platform to target antigen-presenting cells. Cancer Res. 2011, 71, 7452–7462.
Ma, C.; Zhu, D. D.; Chen, Y.; Dong, Y. W.; Lin, W. Y.; Li, N.; Zhang, W. J.; Liu, X. X. Amphiphilic peptide dendrimer-based nanovehicles for safe and effective siRNA delivery. Biophys. Rep. 2020, 6, 278–289.
Hong, F.; Zhang, F.; Liu, Y.; Yan, H. DNA origami: Scaffolds for creating higher order structures. Chem. Rev. 2017, 117, 12584–12640.
Eskandari, S.; Guerin, T.; Toth, I.; Stephenson, R. J. Recent advances in self-assembled peptides: Implications for targeted drug delivery and vaccine engineering. Adv. Drug Deliv. Rev. 2017, 110–111,169-187.
López-Sagaseta, J.; Malito, E.; Rappuoli, R.; Bottomley, M. J. Self-assembling protein nanoparticles in the design of vaccines. Comput. Struct. Biotechnol. J. 2016, 14, 58–68.
Kim, I.; Moon, J. S.; Oh, J. W. Recent advances in M13 bacteriophage-based optical sensing applications. Nano Converg. 2016, 3, 27.
Moon, J. S.; Kim, W. G.; Kim, C.; Park, G. T.; Heo, J.; Yoo, S. Y.; Oh, J. W. M13 bacteriophage-based self-assembly structures and their functional capabilities. Mini. Rev. Org. Chem. 2015, 12, 271–281.
Henry, K. A.; Arbabi-Ghahroudi, M.; Scott, J. K. Beyond phage display: Non-traditional applications of the filamentous bacteriophage as a vaccine carrier, therapeutic biologic, and bioconjugation scaffold. Front. Microbiol. 2015, 6, 755.
Anselmo, A. C.; Mitragotri, S. A review of clinical translation of inorganic nanoparticles. AAPS J. 2015, 17, 1041–1054.
He, H.; Pham-Huy, L. A.; Dramou, P.; Xiao, D. L.; Zuo, P. L.; Pham-Huy, C. Carbon nanotubes: Applications in pharmacy and medicine. BioMed Res. Int. 2013, 2013, 578290.
Steinman, R. M.; Cohn, Z. A. Identification of a novel cell type in peripheral lymphoid organs of mice. I. Morphology, quantitation, tissue distribution. J. Exp. Med. 1973, 137, 1142–1162.
Palucka, K.; Banchereau, J. Dendritic cells: A link between innate and adaptive immunity. J. Clin. Immunol. 1999, 19, 12–25.
Mehta-Damani, A.; Markowicz, S.; Engleman, E. G. Generation of antigen-specific CD4+ T cell lines from naive precursors. Eur. J. Immunol. 1995, 25, 1206–1211.
Mehta-Damani, A.; Markowicz, S.; Engleman, E. G. Generation of antigen-specific CD8+ CTLs from naive precursors. J. Immunol. 1994, 153, 996–1003.
Steinman, R. M.; Nussenzweig, M. C. Avoiding horror autotoxicus: The importance of dendritic cells in peripheral T cell tolerance. Proc. Natl. Acad. Sci. USA 2002, 99, 351–358.
Bonifaz, L.; Bonnyay, D.; Mahnke, K.; Rivera, M.; Nussenzweig, M. C.; Steinman, R. M. Efficient targeting of protein antigen to the dendritic cell receptor DEC-205 in the steady state leads to antigen presentation on major histocompatibility complex class I products and peripheral CD8+ T cell tolerance. J. Exp. Med. 2002, 196, 1627–1638.
Hawiger, D.; Inaba, K.; Dorsett, Y.; Guo, M.; Mahnke, K.; Rivera, M.; Ravetch, J. V.; Steinman, R. M.; Nussenzweig, M. C. Dendritic cells induce peripheral T cell unresponsiveness under steady state conditions in vivo. J. Exp. Med. 2001, 194, 769–779.
Soares, H.; Waechter, H.; Glaichenhaus, N.; Mougneau, E.; Yagita, H.; Mizenina, O.; Dudziak, D.; Nussenzweig, M. C.; Steinman, R. M. A subset of dendritic cells induces CD4+ T cells to produce IFN-γ by an IL-12-independent but CD70-dependent mechanism in vivo. J. Exp. Med. 2007, 204, 1095–1106.
Albert, M. L.; Pearce, S. F. A.; Francisco, L. M.; Sauter, B.; Roy, P.; Silverstein, R. L.; Bhardwaj, N. Immature dendritic cells phagocytose apoptotic cells via αvβ5 and CD36, and cross-present antigens to cytotoxic T lymphocytes. J. Exp. Med. 1998, 188, 1359–1368.
de Baey, A.; Lanzavecchia, A. The role of aquaporins in dendritic cell macropinocytosis. J. Exp. Med. 2000, 191, 743–748.
Geijtenbeek, T. B. H.; Gringhuis, S. I. Signalling through C-type lectin receptors: Shaping immune responses. Nat. Rev. Immunol. 2009, 9, 465–479.
Kawasaki, T.; Kawai, T. Toll-like receptor signaling pathways. Front. Immunol. 2014, 5, 461.
Trombetta, E. S.; Mellman, I. Cell biology of antigen processing in vitro and in vivo. Annu. Rev. Immunol. 2005, 23, 975–1028.
Fujimoto, Y.; Tu, L. L.; Miller, A. S.; Bock, C.; Fujimoto, M.; Doyle, C.; Steeber, D. A.; Tedder, T. F. CD83 expression influences CD4+ T cell development in the thymus. Cell 2002, 108, 755–767.
Kurd, N.; Robey, E. A. T-cell selection in the thymus: A spatial and temporal perspective. Immunol. Rev. 2016, 271, 114–126.
Vacchio, M. S.; Bosselut, R. What happens in the thymus does not stay in the thymus: How T cells recycle the CD4+-CD8+ lineage commitment transcriptional circuitry to control their function. J. Immunol. 2016, 196, 4848–4856.
Pennock, N. D.; White, J. T.; Cross, E. W.; Cheney, E. E.; Tamburini, B. A.; Kedl, R. M. T cell responses: Naive to memory and everything in between. Adv. Physiol. Educ. 2013, 37, 273–283.
Nurieva, R. I.; Chung, Y. Understanding the development and function of T follicular helper cells. Cell. Mol. Immunol. 2010, 7, 190–197.
Dalod, M.; Chelbi, R.; Malissen, B.; Lawrence, T. Dendritic cell maturation: Functional specialization through signaling specificity and transcriptional programming. EMBO J. 2014, 33, 1104–1116.
Blum, J. S.; Wearsch, P. A.; Cresswell, P. Pathways of antigen processing. Annu. Rev. Immunol. 2013, 31, 443–473.
Embgenbroich, M.; Burgdorf, S. Current concepts of antigen cross-presentation. Front. Immunol. 2018, 9, 1643.
Lanzavecchia, A. Mechanisms of antigen uptake for presentation. Curr. Opin. Immunol. 1996, 8, 348–354.
Reddy, S. T.; Rehor, A.; Schmoekel, H. G.; Hubbell, J. A.; Swartz, M. A. In vivo targeting of dendritic cells in lymph nodes with poly(propylene sulfide) nanoparticles. J. Control. Release 2006, 112, 26–34.
Cho, K.; Wang, X.; Nie, S. M.; Chen, Z.; Shin, D. M. Therapeutic nanoparticles for drug delivery in cancer. Clin. Cancer Res. 2008, 14, 1310–1316.
Moghimi, S. M.; Hunter, A. C.; Murray, J. C. Long-circulating and target-specific nanoparticles: Theory to practice. Pharmacol. Rev. 2001, 53, 283–318.
Wei, Y. C.; Quan, L.; Zhou, C.; Zhan, Q. Q. Factors relating to the biodistribution & clearance of nanoparticles & their effects on in vivo application. Nanomedicine 2018, 13, 1495–1512.
Narasimhan, B.; Goodman, J. T.; Vela Ramirez, J. E. Rational design of targeted next-generation carriers for drug and vaccine delivery. Annu. Rev. Biomed. Eng. 2016, 18, 25–49.
Peek, L. J.; Middaugh, C. R.; Berkland, C. Nanotechnology in vaccine delivery. Adv. Drug Deliv. Rev. 2008, 60, 915–928.
Ura, T.; Okuda, K.; Shimada, M. Developments in viral vector-based vaccines. Vaccines 2014, 2, 624–641.
Biswas, S. K.; Boutz, P. L.; Nayak, D. P. Influenza virus nucleoprotein interacts with influenza virus polymerase proteins. J. Virol. 1998, 72, 5493–5501.
Portela, A.; Digard, P. The influenza virus nucleoprotein: A multifunctional RNA-binding protein pivotal to virus replication. J. Gen. Virol. 2002, 83, 723–734.
Keech, C.; Albert, G.; Cho, I.; Robertson, A.; Reed, P.; Neal, S.; Plested, J. S.; Zhu, M. Z.; Cloney-Clark, S.; Zhou, H. X. et al. Phase 1-2 trial of a SARS-CoV-2 recombinant spike protein nanoparticle vaccine. N. Engl. J. Med. 2020, 383, 2320–2332.
Blanco, E.; Shen, H. F.; Ferrari, M. Principles of nanoparticle design for overcoming biological barriers to drug delivery. Nat. Biotechnol. 2015, 33, 941–951.
Monopoli, M. P.; Åberg, C.; Salvati, A.; Dawson, K. A. Biomolecular coronas provide the biological identity of nanosized materials. Nat. Nanotechnol. 2012, 7, 779–786.
Ritz, S.; Schöttler, S.; Kotman, N.; Baier, G.; Musyanovych, A.; Kuharev, J.; Landfester, K.; Schild, H.; Jahn, O.; Tenzer, S. et al. Protein corona of nanoparticles: Distinct proteins regulate the cellular uptake. Biomacromolecules 2015, 16, 1311–1321.
Billeskov, R.; Beikzadeh, B.; Berzofsky, J. A. The effect of antigen dose on T cell-targeting vaccine outcome. Hum. Vaccin. Immunother. 2019, 15, 407–411.
Arvin, A. M.; Fink, K.; Schmid, M. A.; Cathcart, A.; Spreafico, R.; Havenar-Daughton, C.; Lanzavecchia, A.; Corti, D.; Virgin, H. W. A perspective on potential antibody-dependent enhancement of SARS-CoV-2. Nature 2020, 584, 353–363.
Vert, M.; Doi, Y.; Hellwich, K. H.; Hess, M.; Hodge, P.; Kubisa, P.; Rinaudo, M.; Schué, F. Terminology for biorelated polymers and applications (IUPAC Recommendations 2012). Pure Appl. Chem. 2012, 84, 377–410.
Zhao, J. C.; Stenzel, M. H. Entry of nanoparticles into cells: The importance of nanoparticle properties. Polym. Chem. 2018, 9, 259–272.
Behzadi, S.; Serpooshan, V.; Tao, W.; Hamaly, M. A.; Alkawareek, M. Y.; Dreaden, E. C.; Brown, D.; Alkilany, A. M.; Farokhzad, O. C.; Mahmoudi, M. Cellular uptake of nanoparticles: Journey inside the cell. Chem. Soc. Rev. 2017, 46, 4218–4244.
Foroozandeh, P.; Aziz, A. A. Insight into cellular uptake and intracellular trafficking of nanoparticles. Nanoscale Res. Lett. 2018, 13, 339.
Bachmann, M. F.; Jennings, G. T. Vaccine delivery: A matter of size, geometry, kinetics and molecular patterns. Nat. Rev. Immunol. 2010, 10, 787–796.
Moghimi, S. M.; Patel, H. M. Serum-mediated recognition of liposomes by phagocytic cells of the reticuloendothelial system-the concept of tissue specificity. Adva. Drug Deliv. Rev. 1998, 32, 45–60.
Storm, G.; Belliot, S. O.; Daemen, T.; Lasic, D. D. Surface modification of nanoparticles to oppose uptake by the mononuclear phagocyte system. Adv. Drug Deliv. Rev. 1995, 17, 31–48.
Anselmo, A. C.; Mitragotri, S. Nanoparticles in the clinic: An update. Bioeng. Transl. Med. 2019, 4, e10143.
Bulbake, U.; Doppalapudi, S.; Kommineni, N.; Khan, W. Liposomal formulations in clinical use: An updated review. Pharmaceutics 2017, 9, 12.
Ventola, C. L. Progress in nanomedicine: Approved and investigational nanodrugs. P T 2017, 42, 742–755.
Talmage, D. W. The acceptance and rejection of immunological concepts. Annu. Rev. Immunol. 1986, 4, 1–12.
Strugnell, R.; Zepp, F.; Cunningham, A.; Tantawichien, T. Vaccine antigens. Perspect. Vaccinol. 2011, 1, 61–88.
Hamborg, M.; Jorgensen, L.; Bojsen, A. R.; Christensen, D.; Foged, C. Protein antigen adsorption to the DDA/TDB liposomal adjuvant: Effect on protein structure, stability, and liposome physicochemical characteristics. Pharm. Res. 2013, 30, 140–155.
Hansen, B.; Sokolovska, A.; HogenEsch, H.; Hem, S. L. Relationship between the strength of antigen adsorption to an aluminum-containing adjuvant and the immune response. Vaccine 2007, 25, 6618–6624.
Blakney, A. K.; McKay, P. F.; Yus, B. I.; Aldon, Y.; Shattock, R. J. Inside out: Optimization of lipid nanoparticle formulations for exterior complexation and in vivo delivery of saRNA. Gene Ther. 2019, 26, 363–372.
Takamura, S.; Niikura, M.; Li, T. C.; Takeda, N.; Kusagawa, S.; Takebe, Y.; Miyamura, T.; Yasutomi, Y. DNA vaccine-encapsulated virus-like particles derived from an orally transmissible virus stimulate mucosal and systemic immune responses by oral administration. Gene Ther. 2004, 11, 628–635.
Cao, P.; Han, F. Y.; Grøndahl, L.; Xu, Z. P.; Li, L. Enhanced oral vaccine efficacy of polysaccharide-coated calcium phosphate nanoparticles. ACS Omega 2020, 5, 18185–18197.
Pawar, D.; Mangal, S.; Goswami, R.; Jaganathan, K. S. Development and characterization of surface modified PLGA nanoparticles for nasal vaccine delivery: Effect of mucoadhesive coating on antigen uptake and immune adjuvant activity. Eur. J. Pharm. Biopharm. 2013, 85, 550–559.
van Broekhoven, C. L.; Parish, C. R.; Demangel, C.; Britton, W. J.; Altin, J. G. Targeting dendritic cells with antigen-containing liposomes. Cancer Res. 2004, 64, 4357–4365.
Zeng, B. J.; Middelberg, A. P. J.; Gemiarto, A.; MacDonald, K.; Baxter, A. G.; Talekar, M.; Moi, D.; Tullett, K. M.; Caminschi, I.; Lahoud, M. H. et al. Self-adjuvanting nanoemulsion targeting dendritic cell receptor Clec9A enables antigen-specific immunotherapy. J. Clin. Invest. 2018, 128, 1971–1984.
de Titta, A.; Ballester, M.; Julier, Z.; Nembrini, C.; Jeanbart, L.; van der Vlies, A. J.; Swartz, M. A.; Hubbell, J. A. Nanoparticle conjugation of CpG enhances adjuvancy for cellular immunity and memory recall at low dose. Proc. Natl. Acad. Sci. USA 2013, 110, 19902–19907.
Scaria, P. V.; Chen, B.; Rowe, C. G.; Jones, D. S.; Barnafo, E.; Fischer, E. R.; Anderson, C.; MacDonald, N. J.; Lambert, L.; Rausch, K. M. et al. Protein-protein conjugate nanoparticles for malaria antigen delivery and enhanced immunogenicity. PLoS One 2017, 12, e0190312.
Friedman, A. D.; Claypool, S. E.; Liu, R. H. The smart targeting of nanoparticles. Curr. Pharm. Des. 2013, 19, 6315–6329.
Jeanbart, L.; Ballester, M.; de Titta, A.; Corthésy, P.; Romero, P.; Hubbell, J. A.; Swartz, M. A. Enhancing efficacy of anticancer vaccines by targeted delivery to tumor-draining lymph nodes. Cancer Immunol. Res. 2014, 2, 436–447.
Harding, C. V.; Collins, D. S.; Slot, J. W.; Geuze, H. J.; Unanue, E. R. Liposome-encapsulated antigens are processed in lysosomes, recycled, and presented to T cells. Cell 1991, 64, 393–401.
Sancho, D.; Reis e Sousa, C. Signaling by myeloid C-type lectin receptors in immunity and homeostasis. Annu. Rev. Immunol. 2012, 30, 491–529.
Azad, A. K.; Rajaram, M. V. S.; Schlesinger, L. S. Exploitation of the macrophage mannose receptor (CD206) in infectious disease diagnostics and therapeutics. J. Cytol. Mol. Biol. 2014, 1, 1000003.
Ponka, P.; Lok, C. N. The transferrin receptor: Role in health and disease. Int. J. Biochem. Cell Biol. 1999, 31, 1111–1137.
Nimmerjahn, F.; Ravetch, J. V. Fcγ receptors as regulators of immune responses. Nat. Rev. Immunol. 2008, 8, 34–47.
Treanor, B. B-cell receptor: From resting state to activate. Immunology 2012, 136, 21–27.
Al-Barwani, F.; Young, S. L.; Baird, M. A.; Larsen, D. S.; Ward, V. K. Mannosylation of virus-like particles enhances internalization by antigen presenting cells. PLoS One 2014, 9, e104523.
Hong, S.; Zhang, Z. M.; Liu, H. T.; Tian, M. J.; Zhu, X. P.; Zhang, Z. Q.; Wang, W. H.; Zhou, X. Y.; Zhang, F. P.; Ge, Q. et al. B Cells are the dominant antigen-presenting cells that activate naive CD4+ T cells upon immunization with a virus-derived nanoparticle antigen. Immunity 2018, 49, 695–708.e4.
Storni, T.; Lechner, F.; Erdmann, I.; Bächi, T.; Jegerlehner, A.; Dumrese, T.; Kündig, T. M.; Ruedl, C.; Bachmann, M. F. Critical role for activation of antigen-presenting cells in priming of cytotoxic T cell responses after vaccination with virus-like particles. J. Immunol. 2002, 168, 2880–2886.
Tanaka, Y.; Taneichi, M.; Kasai, M.; Kakiuchi, T.; Uchida, T. Liposome-coupled antigens are internalized by antigen-presenting cells via pinocytosis and cross-presented to CD8+ T cells. PLoS One 2010, 5, e15225.
Taneichi, M.; Ishida, H.; Kajino, K.; Ogasawara, K.; Tanaka, Y.; Kasai, M.; Mori, M.; Nishida, M.; Yamamura, H.; Mizuguchi, J. et al. Antigen Chemically coupled to the surface of liposomes are cross-presented to CD8+ T cells and induce potent antitumor immunity. J. Immunol. 2006, 177, 2324–2330.
Dykman, L. A. Gold nanoparticles for preparation of antibodies and vaccines against infectious diseases. Expert Rev. Vaccines 2020, 19, 465–477.
Wang, C.; Zhu, W. D.; Luo, Y.; Wang, B. Z. Gold nanoparticles conjugating recombinant influenza hemagglutinin trimers and flagellin enhanced mucosal cellular immunity. Nanomedicine:Nanotechnol. Biol. Med. 2018, 14, 1349–1360.
Zhou, Q. Q.; Zhang, Y. L.; Du, J.; Li, Y.; Zhou, Y.; Fu, Q. X.; Zhang, J. G.; Wang, X. H.; Zhan, L. S. Different-sized gold nanoparticle activator/antigen increases dendritic cells accumulation in liver-draining lymph nodes and CD8+ T cell responses. ACS Nano 2016, 10, 2678–2692.
Raghuwanshi, D.; Mishra, V.; Das, D.; Kaur, K.; Suresh, M. R. Dendritic cell targeted chitosan nanoparticles for nasal DNA immunization against SARS CoV nucleocapsid protein. Mol. Pharm. 2012, 9, 946–956.
Brenner, S.; Jacob, F.; Meselson, M. An unstable intermediate carrying information from genes to ribosomes for protein synthesis. Nature 1961, 190, 576–581.
Wolff, J. A.; Malone, R. W.; Williams, P.; Chong, W.; Acsadi, G.; Jani, A.; Felgner, P. L. Direct gene transfer into mouse muscle in vivo. Science 1990, 247, 1465–1468.
Garneau, N. L.; Wilusz, J.; Wilusz, C. J. The highways and byways of mRNA decay. Nat. Rev. Mol. Cell Biol. 2007, 8, 113–126.
Ross, J. mRNA stability in mammalian cells. Microbiol. Rev. 1995, 59, 423–450.
Holtkamp, S.; Kreiter, S.; Selmi, A.; Simon, P.; Koslowski, M.; Huber, C.; Türeci, Ö.; Sahin, U. Modification of antigen-encoding RNA increases stability, translational efficacy, and T-cell stimulatory capacity of dendritic cells. Blood 2006, 108, 4009–4017.
Pardi, N.; Hogan, M. J.; Porter, F. W.; Weissman, D. mRNA vaccines-a new era in vaccinology. Nat. Rev. Drug Dis. 2018, 17, 261–279.
Brito, L. A.; Kommareddy, S.; Maione, D.; Uematsu, Y.; Giovani, C.; Berlanda Scorza, F.; Otten, G. R.; Yu, D.; Mandl, C. W.; Mason, P. W. et al. Self-amplifying mRNA vaccines. Adv. Genet. 2015, 89, 179–233.
Schlake, T.; Thess, A.; Fotin-Mleczek, M.; Kallen, K. J. Developing mRNA-vaccine technologies. RNA Biol. 2012, 9, 1319–1330.
Sato, K.; Akiyama, M.; Sakakibara, Y. RNA secondary structure prediction using deep learning with thermodynamic integration. Nat. Commun. 2021, 12, 941.
Mao, K. K.; Wang, J.; Xiao, Y. Prediction of RNA secondary structure with pseudoknots using coupled deep neural networks. Biophys. Rep. 2020, 6, 146–154.
Bellaousov, S.; Reuter, J. S.; Seetin, M. G.; Mathews, D. H. RNAstructure: Web servers for RNA secondary structure prediction and analysis. Nucleic Acids Res. 2013, 41, W471–W474.
Janssen, S.; Giegerich, R. The RNA shapes studio. Bioinformatics 2015, 31, 423–425.
Zeng, C. X.; Hou, X. C.; Yan, J. Y.; Zhang, C. X.; Li, W. Q.; Zhao, W. Y.; Du, S.; Dong, Y. Z. Leveraging mRNA sequences and nanoparticles to deliver SARS-CoV-2 antigens in vivo. Adv. Mater. 2020, 32, 2004452.
Wrapp, D.; Wang, N.; Corbett, K. S.; Goldsmith, J. A.; Hsieh, C. L.; Abiona, O.; Graham, B. S.; McLellan, J. S. Cryo-EM structure of the 2019-nCoV spike in the prefusion conformation. Science 2020, 367, 1260–1263.
Hassett, K. J.; Benenato, K. E.; Jacquinet, E.; Lee, A.; Woods, A.; Yuzhakov, O.; Himansu, S.; Deterling, J.; Geilich, B. M.; Ketova, T. et al. Optimization of lipid nanoparticles for intramuscular administration of mRNA vaccines. Mol. Ther. Nucleic Acids 2019, 15, 1–11.
Graham, B. S.; Gilman, M. S. A.; McLellan, J. S. Structure-based vaccine antigen design. Annu. Rev. Med. 2019, 70, 91–104.
Jackson, L. A.; Anderson, E. J.; Rouphael, N. G.; Roberts, P. C.; Makhene, M.; Coler, R. N.; McCullough, M. P.; Chappell, J. D.; Denison, M. R.; Stevens, L. J. et al. An mRNA vaccine against SARS-CoV-2-preliminary report. N. Engl. J. Med. 2020, 383, 1920–1931.
Baden, L. R.; El Sahly, H. M.; Essink, B.; Kotloff, K.; Frey, S.; Novak, R.; Diemert, D.; Spector, S. A.; Rouphael, N.; Creech, C. B. et al. Efficacy and Safety of the mRNA-1273 SARS-CoV-2 Vaccine. N. Engl. J. Med. 2021, 384, 403–416.
Wang, P. F.; Nair, M. S.; Liu, L. H.; Iketani, S.; Luo, Y.; Guo, Y. C.; Wang, M.; Yu, J.; Zhang, B. S.; Kwong, P. D. et al. Antibody resistance of SARS-CoV-2 variants B. 1.351 and B. 1.1. 7. Nature 2021, 593, 130–135.
Wu, K.; Werner, A. P.; Koch, M.; Choi, A.; Narayanan, E.; Stewart-Jones, G. B. E.; Colpitts, T.; Bennett, H.; Boyoglu-Barnum, S.; Shi, W. et al. Serum neutralizing activity elicited by mRNA-1273 vaccine. N. Engl. J. Med. 2021, 384, 1468–1470.
Karikó, K.; Muramatsu, H.; Welsh, F. A.; Ludwig, J.; Kato, H.; Akira, S.; Weissman, D. Incorporation of pseudouridine into mRNA yields superior nonimmunogenic vector with increased translational capacity and biological stability. Mol. Ther. 2008, 16, 1833–1840.
Tai, W. B.; Zhao, G. Y.; Sun, S. H.; Guo, Y.; Wang, Y. F.; Tao, X. R.; Tseng, C. T. K.; Li, F.; Jiang, S. B.; Du, L. Y. et al. A recombinant receptor-binding domain of MERS-CoV in trimeric form protects human dipeptidyl peptidase 4 (hDPP4) transgenic mice from MERS-CoV infection. Virology 2016, 499, 375–382.
Kranz, L. M.; Diken, M.; Haas, H.; Kreiter, S.; Loquai, C.; Reuter, K. C.; Meng, M.; Fritz, D.; Vascotto, F.; Hefesha, H. et al. Systemic RNA delivery to dendritic cells exploits antiviral defence for cancer immunotherapy. Nature 2016, 534, 396–401.
Mulligan, M. J.; Lyke, K. E.; Kitchin, N.; Absalon, J.; Gurtman, A.; Lockhart, S.; Neuzil, K.; Raabe, V.; Bailey, R.; Swanson, K. A. et al. Phase I/II study of COVID-19 RNA vaccine BNT162b1 in adults. Nature 2020, 586, 589–593.
Walsh, E. E.; Frenck, R. W. Jr.; Falsey, A. R.; Kitchin, N.; Absalon, J.; Gurtman, A.; Lockhart, S.; Neuzil, K.; Mulligan, M. J.; Bailey, R. et al. Safety and immunogenicity of two RNA-based Covid-19 vaccine candidates. N. Engl. J. Med. 2020, 383, 2439–2450.
Polack, F. P.; Thomas, S. J.; Kitchin, N.; Absalon, J.; Gurtman, A.; Lockhart, S.; Perez, J. L.; Pérez Marc, G.; Moreira, E. D.; Zerbini, C. et al. Safety and efficacy of the BNT162b2 mRNA Covid-19 vaccine. N. Engl. J. Med. 2020, 383, 2603–2615.
Planas, D.; Bruel, T.; Grzelak, L.; Guivel-Benhassine, F.; Staropoli, I.; Porrot, F.; Planchais, C.; Buchrieser, J.; Rajah, M. M.; Bishop, E. et al. Sensitivity of infectious SARS-CoV-2 B. 1.1. 7 and B. 1.351 variants to neutralizing antibodies. Nat. Med. 2021, 27, 917–924.
Jose, J.; Snyder, J. E.; Kuhn, R. J. A structural and functional perspective of alphavirus replication and assembly. Future Microbiol. 2009, 4, 837–856.
Atkins, G. J.; Fleeton, M. N.; Sheahan, B. J. Therapeutic and prophylactic applications of alphavirus vectors. Expert Rev. Mol. Med. 2008, 10, e33.
Tubulekas, I.; Berglund, P.; Fleeton, M.; Liljeström, P. Alphavirus expression vectors and their use as recombinant vaccines: A minireview. Gene 1997, 190, 191–195.
Zhou, X.; Berglund, P.; Rhodes, G.; Parker, S. E.; Jondal, M.; Liljeström, P. Self-replicating Semliki Forest virus RNA as recombinant vaccine. Vaccine 1994, 12, 1510–1514.
Vogel, A. B.; Lambert, L.; Kinnear, E.; Busse, D.; Erbar, S.; Reuter, K. C.; Wicke, L.; Perkovic, M.; Beissert, T.; Haas, H. et al. Self-amplifying RNA vaccines give equivalent protection against influenza to mRNA vaccines but at much lower doses. Mol. Ther. 2018, 26, 446–455.
Geall, A. J.; Verma, A.; Otten, G. R.; Shaw, C. A.; Hekele, A.; Banerjee, K.; Cu, Y.; Beard, C. W.; Brito, L. A.; Krucker, T. et al. Nonviral delivery of self-amplifying RNA vaccines. Proc. Natl. Acad. Sci. USA 2012, 109, 14604–14609.
Goswami, R.; Chatzikleanthous, D.; Lou, G.; Giusti, F.; Bonci, A.; Taccone, M.; Brazzoli, M.; Gallorini, S.; Ferlenghi, I.; Berti, F. et al. Mannosylation of LNP results in improved potency for self-amplifying RNA (SAM) vaccines. ACS Infect. Dis. 2019, 5, 1546–1558.
Kirchdoerfer, R. N.; Wang, N. S.; Pallesen, J.; Wrapp, D.; Turner, H. L.; Cottrell, C. A.; Corbett, K. S.; Graham, B. S.; McLellan, J. S.; Ward, A. B. Stabilized coronavirus spikes are resistant to conformational changes induced by receptor recognition or proteolysis. Sci. Rep. 2018, 8, 15701.
Blakney, A. K.; McKay, P. F.; Shattock, R. J. Structural Components for amplification of positive and negative strand VEEV splitzicons. Front. Mol. Biosci. 2018, 5, 71.
Pardi, N.; Tuyishime, S.; Muramatsu, H.; Kariko, K.; Mui, B. L.; Tam, Y. K.; Madden, T. D.; Hope, M. J.; Weissman, D. Expression kinetics of nucleoside-modified mRNA delivered in lipid nanoparticles to mice by various routes. J Control. Release 2015, 217, 345–351.
McKay, P. F.; Hu, K.; Blakney, A. K.; Samnuan, K.; Brown, J. C.; Penn, R.; Zhou, J.; Bouton, C. R.; Rogers, P.; Polra, K. et al. Self-amplifying RNA SARS-CoV-2 lipid nanoparticle vaccine candidate induces high neutralizing antibody titers in mice. Nat. Commun. 2020, 11, 3523.
Kinney, R. M.; Chang, G. J.; Tsuchiya, K. R.; Sneider, J. M.; Roehrig, J. T.; Woodward, T. M.; Trent, D. W. Attenuation of Venezuelan equine encephalitis virus strain TC-83 is encoded by the 5'-noncoding region and the E2 envelope glycoprotein. J. Virol. 1993, 67, 1269–1277.
Desbien, A. L.; Reed, S. J.; Bailor, H. R.; Cauwelaert, N. D.; Laurance, J. D.; Orr, M. T.; Fox, C. B.; Carter, D.; Reed, S. G.; Duthie, M. S. Squalene emulsion potentiates the adjuvant activity of the TLR4 agonist, GLA, via inflammatory caspases, IL-18, and IFN-γ. Eur. J. Immunol. 2015, 45, 407–417.
Yu, E. Y.; Chandrasekharan, P.; Berzon, R.; Tay, Z. W.; Zhou, X. Y.; Khandhar, A. P.; Ferguson, R. M.; Kemp, S. J.; Zheng, B.; Goodwill, P. W. et al. Magnetic particle imaging for highly sensitive, quantitative, and safe in vivo gut bleed detection in a Murine model. ACS Nano 2017, 11, 12067–12076.
Erasmus, J. H.; Khandhar, A. P.; O’Connor, M. A.; Walls, A. C.; Hemann, E. A.; Murapa, P.; Archer, J.; Leventhal, S.; Fuller, J. T.; Lewis, T. B. et al. An Alphavirus-derived replicon RNA vaccine induces SARS-CoV-2 neutralizing antibody and T cell responses in mice and nonhuman primates. Sci. Transl. Med. 2020, 12, eabc9396.
Kay, M. A.; He, C. Y.; Chen, Z. Y. A robust system for production of minicircle DNA vectors. Nat. Biotechnol. 2010, 28, 1287–1289.
Schleef, M.; Schirmbeck, R.; Reiser, M.; Michel, M. L.; Schmeer, M. Minicircle: Next generation DNA vectors for vaccination. Methods Mol. Biol. 2015, 1317, 327–339.
Farris, E.; Brown, D. M.; Ramer-Tait, A. E.; Pannier, A. K. Micro- and nanoparticulates for DNA vaccine delivery. Exp. Biol. Med. 2016, 241, 919–929.
McCluskie, M. J.; Brazolot Millan, C. L.; Gramzinski, R. A.; Robinson, H. L.; Santoro, J. C.; Fuller, J. T.; Widera, G.; Haynes, J. R.; Purcell, R. H.; Davis, H. L. Route and method of delivery of DNA vaccine influence immune responses in mice and non-human primates. Mol. Med. 1999, 5, 287–300.
Xu, Y. Y.; Yuen, P. W.; Lam, J. K. W. Intranasal DNA vaccine for protection against respiratory infectious diseases: The delivery perspectives. Pharmaceutics 2014, 6, 378–415.
Ulmer, J. B.; Donnelly, J. J.; Parker, S. E.; Rhodes, G. H.; Felgner, P. L.; Dwarki, V. J.; Gromkowski, S. H.; Deck, R. R.; DeWitt, C. M.; Friedman, A. et al. Heterologous protection against influenza by injection of DNA encoding a viral protein. Science 1993, 259, 1745–1749.
Quaak, S. G. L.; Haanen, J. B. A. G.; Beijnen, J. H.; Nuijen, B. Naked plasmid DNA formulation: Effect of different disaccharides on stability after lyophilisation. AAPS PharmSciTech 2010, 11, 344–350.
Carabineiro, S. A. C. Applications of gold nanoparticles in nanomedicine: Recent advances in vaccines. Molecules 2017, 22, 857.
Dean, H. J.; Fuller, D.; Osorio, J. E. Powder and particle-mediated approaches for delivery of DNA and protein vaccines into the epidermis. Comp. Immunol., Microbiology and Infectious Diseases 2003, 26, 373–388.
Perrie, Y.; Frederik, P. M.; Gregoriadis, G. Liposome-mediated DNA vaccination: The effect of vesicle composition. Vaccine 2001, 19, 3301–3310.
Wang, Z.; Troilo, P. J.; Wang, X.; Griffiths II, T. G.; Pacchione, S. J.; Barnum, A. B.; Harper, L. B.; Pauley, C. J.; Niu, Z.; Denisova, L. et al. Detection of integration of plasmid DNA into host genomic DNA following intramuscular injection and electroporation. Gene Ther. 2004, 11, 711–721.
Diehl, M. C.; Lee, J. C.; Daniels, S. E.; Tebas, P.; Khan, A. S.; Giffear, M.; Sardesai, N. Y.; Bagarazzi, M. L. Tolerability of intramuscular and intradermal delivery by CELLECTRA® adaptive constant current electroporation device in healthy volunteers. Hum. Vaccin. Immunother. 2013, 9, 2246–2252.
Sardesai, N. Y.; Weiner, D. B. Electroporation delivery of DNA vaccines: Prospects for success. Curr. Opin. Immunol. 2011, 23, 421–429.
Xu, Z. Y.; Wise, M. C.; Choi, H.; Perales-Puchalt, A.; Patel, A.; Tello-Ruiz, E.; Chu, J. D.; Muthumani, K.; Weiner, D. B. Synthetic DNA delivery by electroporation promotes robust in vivo sulfation of broadly neutralizing anti-HIV immunoadhesin eCD4-Ig. EBioMedicine 2018, 35, 97–105.
Smith, T. R. F.; Patel, A.; Ramos, S.; Elwood, D.; Zhu, X. Z.; Yan, J.; Gary, E. N.; Walker, S. N.; Schultheis, K.; Purwar, M. et al. Immunogenicity of a DNA vaccine candidate for COVID-19. Nat. Commun. 2020, 11, 2601.
Noad, R.; Roy, P. Virus-like particles as immunogens. Trends Microbiol. 2003, 11, 438–444.
Fersht, A.; Winter, G. Protein engineering. Trends Biochem. Sci. 1992, 17, 292–294.
Da Silva, D. M.; Velders, M. P.; Nieland, J. D.; Schiller, J. T.; Nickoloff, B. J.; Kast, W. M. Physical interaction of human papillomavirus virus-like particles with immune cells. Int. Immunol. 2001, 13, 633–641.
Nasir, W.; Bally, M.; Zhdanov, V. P.; Larson, G.; Höök, F. Interaction of virus-like particles with vesicles containing glycolipids: Kinetics of detachment. J. Phys. Chem. B 2015, 119, 11466–11472.
Zdanowicz, M.; Chroboczek, J. Virus-like particles as drug delivery vectors. Acta Biochim. Pol. 2016, 63, 469–473.
Schwarz, B.; Uchida, M.; Douglas, T. Chapter one-biomedical and catalytic opportunities of virus-like particles in nanotechnology. Adv. Virus Res. 2017, 97, 1–60.
McAleer, W. J.; Buynak, E. B.; Maigetter, R. Z.; Wampler, D. E.; Miller, W. J.; Hilleman, M. R. Human hepatitis B vaccine from recombinant yeast. Nature 1984, 307, 178–180.
Grgacic, E. V. L.; Anderson, D. A. Virus-like particles: Passport to immune recognition. Methods 2006, 40, 60–65.
Vicente, T.; Roldão, A.; Peixoto, C.; Carrondo, M. J.; Alves, P. M. Large-scale production and purification of VLP-based vaccines. J. Invertebr. Pathol. 2011, 107 Suppl, S42–S48.
Zhu, N.; Zhang, D. Y.; Wang, W. L.; Li, X. W.; Yang, B.; Song, J. D.; Zhao, X.; Huang, B. Y.; Shi, W. F.; Lu, R. J. et al. A novel coronavirus from patients with pneumonia in China, 2019. N. Engl. J. Med. 2020, 382, 727–733.
Mortola, E.; Roy, P. Efficient assembly and release of SARS coronavirus-like particles by a heterologous expression system. FEBS Lett. 2004, 576, 174–178.
Xu, R. D.; Shi, M. F.; Li, J.; Song, P.; Li, N. Construction of SARS-CoV-2 virus-like particles by mammalian expression system. Front. Bioeng. Biotechnol. 2020, 8, 862.
Fernandes, F.; Teixeira, A. P.; Carinhas, N.; Carrondo, M. J. T.; Alves, P. M. Insect cells as a production platform of complex virus-like particles. Expert Rev. Vaccines 2013, 12, 225–236.
Liu, F. X.; Wu, X. D.; Li, L.; Liu, Z. S.; Wang, Z. L. Use of baculovirus expression system for generation of virus-like particles: Successes and challenges. Protein Expr. Purif. 2013, 90, 104–116.
Shen, S.; Lin, P. S.; Chao, Y. C.; Zhang, A. H.; Yang, X. M.; Lim, S. G.; Hong, W. J.; Tan, Y. J. The severe acute respiratory syndrome coronavirus 3a is a novel structural protein. Biochem. Biophys. Res. Commun. 2005, 330, 286–292.
Siu, Y. L.; Teoh, K. T.; Lo, J.; Chan, C. M.; Kien, F.; Escriou, N.; Tsao, S. W.; Nicholls, J. M.; Altmeyer, R.; Peiris, J. S. M. et al. The M, E, and N structural proteins of the severe acute respiratory syndrome coronavirus are required for efficient assembly, trafficking, and release of virus-like particles. J. Virol. 2008, 82, 11318–11330.
Zhao, P.; Ke, J. S.; Qin, Z. L.; Ren, H.; Zhao, L. J.; Yu, J. G.; Gao, J.; Zhu, S. Y.; Qi, Z. T. DNA vaccine of SARS-Cov S gene induces antibody response in mice. Acta Biochim. Biophys. Sin. 2004, 36, 37–41.
Wang, C. Y.; Li, W. T.; Drabek, D.; Okba, N. M. A.; van Haperen, R.; Osterhaus, A. D. M. E.; van Kuppeveld, F. J. M.; Haagmans, B. L.; Grosveld, F.; Bosch, B. J. A human monoclonal antibody blocking SARS-CoV-2 infection. Nat. Commun. 2020, 11, 2251.
Cao, W. C.; Liu, W.; Zhang, P. H.; Zhang, F.; Richardus, J. H. Disappearance of antibodies to SARS-associated coronavirus after recovery. N. Engl. J. Med. 2007, 357, 1162–1163.
Le Bert, N.; Tan, A. T.; Kunasegaran, K.; Tham, C. Y. L.; Hafezi, M.; Chia, A.; Chng, M. H. Y.; Lin, M. Y.; Tan, N.; Linster, M. et al. SARS-CoV-2-specific T cell immunity in cases of COVID-19 and SARS, and uninfected controls. Nature 2020, 584, 457–462.
de Haan, C. A. M.; Kuo, L. L.; Masters, P. S.; Vennema, H.; Rottier, P. J. M. Coronavirus particle assembly: Primary structure requirements of the membrane protein. J. Virol. 1998, 72, 6838–6850.
DeDiego, M. L.; Álvarez, E.; Almazán, F.; Rejas, M. T.; Lamirande, E.; Roberts, A.; Shieh, W. J.; Zaki, S. R.; Subbarao, K.; Enjuanes, L. A severe acute respiratory syndrome coronavirus that lacks the e gene is attenuated in vitro and in vivo. J. Virol. 2007, 81, 1701–1713.
Ortego, J.; Ceriani, J. E.; Patiño, C.; Plana, J.; Enjuanes, L. Absence of E protein arrests transmissible gastroenteritis coronavirus maturation in the secretory pathway. Virology 2007, 368, 296–308.
Tissot, A. C.; Renhofa, R.; Schmitz, N.; Cielens, I.; Meijerink, E.; Ose, V.; Jennings, G. T.; Saudan, P.; Pumpens, P.; Bachmann, M. F. Versatile virus-like particle carrier for epitope based vaccines. PLoS One 2010, 5, e9809.
Li, K. Y.; Peers-Adams, A.; Win, S. J.; Scullion, S.; Wilson, M.; Young, V. L.; Jennings, P.; Ward, V. K.; Baird, M. A.; Young, S. L. Antigen incorporated in virus-like particles is delivered to specific dendritic cell subsets that induce an effective antitumor immune response in vivo. J. Immunother. 2013, 36, 11–19.
Ruedl, C.; Storni, T.; Lechner, F.; Bächi, T.; Bachmann, M. F. Cross-presentation of virus-like particles by skin-derived CD8– dendritic cells: A dispensable role for TAP. Eur. J. Immunol. 2002, 32, 818–825.
Liu, Y. V.; Massare, M. J.; Barnard, D. L.; Kort, T.; Nathan, M.; Wang, L.; Smith, G. Chimeric severe acute respiratory syndrome coronavirus (SARS-CoV) S glycoprotein and influenza matrix 1 efficiently form virus-like particles (VLPs) that protect mice against challenge with SARS-CoV. Vaccine 2011, 29, 6606–6613.
Gillitzer, E.; Willits, D.; Young, M.; Douglas, T. Chemical modification of a viral cage for multivalent presentation. Chem. Commun. 2002, 21, 2390–2391.
Smith, M. T.; Hawes, A. K.; Bundy, B. C. Reengineering viruses and virus-like particles through chemical functionalization strategies. Curr. Opin. Biotechnol. 2013, 24, 620–626.
Thrane, S.; Janitzek, C. M.; Agerbæk, M. Ø.; Ditlev, S. B.; Resende, M.; Nielsen, M. A.; Theander, T. G.; Salanti, A.; Sander, A. F. A novel virus-like particle based vaccine platform displaying the placental malaria antigen VAR2CSA. PLoS One 2015, 10, e0143071.
Zakeri, B.; Fierer, J. O.; Celik, E.; Chittock, E. C.; Schwarz-Linek, U.; Moy, V. T.; Howarth, M. Peptide tag forming a rapid covalent bond to a protein, through engineering a bacterial adhesin. Proc. Natl. Acad. Sci. USA 2012, 109, E690–E697.
Brune, K. D.; Leneghan, D. B.; Brian, I. J.; Ishizuka, A. S.; Bachmann, M. F.; Draper, S. J.; Biswas, S.; Howarth, M. Plug-and-display: Decoration of virus-like particles via isopeptide bonds for modular immunization. Sci. Rep. 2016, 6, 19234.
Liu, Z. D.; Zhou, H.; Wang, W. J.; Tan, W. J.; Fu, Y. X.; Zhu, M. Z. A novel method for synthetic vaccine construction based on protein assembly. Sci. Rep. 2014, 4, 7266.
Lee, C. D.; Yan, Y. P.; Liang, S. M.; Wang, T. F. Production of FMDV virus-like particles by a SUMO fusion protein approach in Escherichia coli. J. Biomed. Sci. 2009, 16, 69.
Liew, M. W. O.; Rajendran, A.; Middelberg, A. P. J. Microbial production of virus-like particle vaccine protein at gram-per-litre levels. J. Biotechnol. 2010, 150, 224–231.
Sasnauskas, K.; Buzaite, O.; Vogel, F.; Jandrig, B.; Razanskas, R.; Staniulis, J.; Scherneck, S.; Krüger, D. H.; Ulrich, R. Yeast cells allow high-level expression and formation of polyomavirus-like particles. Biol. Chem. 1999, 380, 381–386.
Santi, L.; Batchelor, L.; Huang, Z.; Hjelm, B.; Kilbourne, J.; Arntzen, C. J.; Chen, Q.; Mason, H. S. An efficient plant viral expression system generating orally immunogenic Norwalk virus-like particles. Vaccine 2008, 26, 1846–1854.
Santi, L.; Huang, Z.; Mason, H. Virus-like particles production in green plants. Methods 2006, 40, 66–76.
Maranga, L.; Cruz, P. E.; Aunins, J. G.; Carrondo, M. J. Production of core and virus-like particles with baculovirus infected insect cells. Adv. Biochem. Eng. Biotechnol. 2002, 74, 183–206.
Hsieh, P. K.; Chang, S. C.; Huang, C. C.; Lee, T. T.; Hsiao, C. W.; Kou, Y. H.; Chen, I. Y.; Chang, C. K.; Huang, T. H.; Chang, M. F. Assembly of severe acute respiratory syndrome coronavirus RNA packaging signal into virus-like particles is nucleocapsid dependent. J. Virol. 2005, 79, 13848–13855.
Kost, T. A.; Condreay, J. P. Recombinant baculoviruses as mammalian cell gene-delivery vectors. Trends Biotechnol. 2002, 20, 173–180.
Bundy, B. C.; Franciszkowicz, M. J.; Swartz, J. R. Escherichia coli-based cell-free synthesis of virus-like particles. Biotechnol. Bioeng. 2008, 100, 28–37.
Shi, X. Z.; Jarvis, D. L. Protein N-glycosylation in the baculovirus-insect cell system. Curr. Drug Targets 2007, 8, 1116–1125.
Watanabe, Y.; Allen, J. D.; Wrapp, D.; McLellan, J. S.; Crispin, M. Site-specific glycan analysis of the SARS-CoV-2 spike. Science 2020, 369, 330–333.
Margine, I.; Martinez-Gil, L.; Chou, Y. Y.; Krammer, F. Residual baculovirus in insect cell-derived influenza virus-like particle preparations enhances immunogenicity. PLoS One 2012, 7, e51559.
Khan, K. H. Gene expression in Mammalian cells and its applications. Adv. Pharm. Bull. 2013, 3, 257–263.
Chen, Q.; Lai, H. F. Plant-derived virus-like particles as vaccines. Hum. Vaccin. Immunother. 2013, 9, 26–49.
Kim, H. S.; Jeon, J. H.; Lee, K. J.; Ko, K. N-Glycosylation modification of plant-derived virus-like particles: An application in vaccines. BioMed Res. Int. 2014, 2014, 249519.
Roldão, A.; Mellado, M. C. M.; Castilho, L. R.; Carrondo, M. J.; Alves, P. M. Virus-like particles in vaccine development. Expert Rev. Vaccines 2010, 9, 1149–1176.
Hiatt, A.; Caffferkey, R.; Bowdish, K. Production of antibodies in transgenic plants. Nature 1989, 342, 76–78.
Goodin, M. M.; Zaitlin, D.; Naidu, R. A.; Lommel, S. A. Nicotiana benthamiana: Its history and future as a model for plant-pathogen interactions. Mol. Plant Microbe Interact. 2008, 21, 1015–1026.
Mason, H. S.; Lam, D. M.; Arntzen, C. J. Expression of hepatitis B surface antigen in transgenic plants. Proc. Natl. Acad. Sci. USA 1992, 89, 11745–11749.
Lacasse, P.; Denis, J.; Lapointe, R.; Leclerc, D.; Lamarre, A. Novel plant virus-based vaccine induces protective cytotoxic T-lymphocyte-mediated antiviral immunity through dendritic cell maturation. J. Virol. 2008, 82, 785–794.
Pillet, S.; Aubin, É.; Trépanier, S.; Bussière, D.; Dargis, M.; Poulin, J. F.; Yassine-Diab, B.; Ward, B. J.; Landry, N. A plant-derived quadrivalent virus like particle influenza vaccine induces cross-reactive antibody and T cell response in healthy adults. Clin. Immunol. 2016, 168, 72–87.
Shriver, L. P.; Plummer, E. M.; Thomas, D. M.; Ho, S.; Manchester, M. Localization of gadolinium-loaded CPMV to sites of inflammation during central nervous system autoimmunity. J. Mater. Chem. B 2013, 1, 5256–5263.
D'Aoust, M. A.; Lavoie, P. O.; Couture, M. M. J.; Trépanier, S.; Guay, J. M.; Dargis, M.; Mongrand, S.; Landry, N.; Ward, B. J.; Vézina, L. P. Influenza virus-like particles produced by transient expression in Nicotiana benthamiana induce a protective immune response against a lethal viral challenge in mice. Plant Biotechnol. J. 2008, 6, 930–940.
Lindsay, B. J.; Bonar, M. M.; Costas-Cancelas, I. N.; Hunt, K.; Makarkov, A. I.; Chierzi, S.; Krawczyk, C. M.; Landry, N.; Ward, B. J.; Rouiller, I. Morphological characterization of a plant-made virus-like particle vaccine bearing influenza virus hemagglutinins by electron microscopy. Vaccine 2018, 36, 2147–2154.
Gelvin, S. B. Agrobacterium-mediated plant transformation: The biology behind the "gene-jockeying" tool. Microbiol. Mol. Biol. Rev. 2003, 67, 16–37.
Zupan, J. R.; Zambryski, P. Transfer of T-DNA from Agrobacterium to the plant cell. Plant Physiol. 1995, 107, 1041–1047.
Morein, B.; Simons, K. Subunit vaccines against enveloped viruses: Virosomes, micelles and other protein complexes. Vaccine 1985, 3, 83–93.
Hansson, M.; Nygren, P. Å.; Ståhl, S. Design and production of recombinant subunit vaccines. Biotechnol. Appl. Biochem. 2000, 32, 95–107.
Schiller, J. T.; Lowy, D. R. Raising expectations for subunit vaccine. J. Infect. Dis. 2015, 211, 1373–1375.
Trimaille, T.; Lacroix, C.; Verrier, B. Self-assembled amphiphilic copolymers as dual delivery system for immunotherapy. Eur. J. Pharm. Biopharm. 2019, 142, 232–239.
Trimaille, T.; Verrier, B. Micelle-based adjuvants for subunit vaccine delivery. Vaccines 2015, 3, 803–813.
Zaman, M.; Skwarczynski, M.; Malcolm, J. M.; Urbani, C. N.; Jia, Z. F.; Batzloff, M. R.; Good, M. F.; Monteiro, M. J.; Toth, I. Self-adjuvanting polyacrylic nanoparticulate delivery system for group A streptococcus (GAS) vaccine. Nanomedicine Nanotechnol. Biol. Med. 2011, 7, 168–173.
Silva, A. L.; Soema, P. C.; Slütter, B.; Ossendorp, F.; Jiskoot, W. PLGA particulate delivery systems for subunit vaccines: Linking particle properties to immunogenicity. Hum. Vaccin. Immunother. 2016, 12, 1056–1069.
Radošević, K.; Rodriguez, A.; Mintardjo, R.; Tax, D.; Bengtsson, K. L.; Thompson, C.; Zambon, M.; Weverling, G. J.; UytdeHaag, F.; Goudsmit, J. Antibody and T-cell responses to a virosomal adjuvanted H9N2 avian influenza vaccine: Impact of distinct additional adjuvants. Vaccine 2008, 26, 3640–3646.
Reimer, J. M.; Karlsson, K. H.; Lövgren-Bengtsson, K.; Magnusson, S. E.; Fuentes, A.; Stertman, L. Matrix-M™ adjuvant induces local recruitment, activation and maturation of central immune cells in absence of antigen. PLoS One 2012, 7, e41451.
Shinde, V.; Fries, L.; Wu, Y. K.; Agrawal, S.; Cho, I.; Thomas, D. N.; Spindler, M.; Lindner, E.; Hahn, T.; Plested, J. et al. Improved titers against influenza drift variants with a nanoparticle vaccine. N. Engl. J. Med. 2018, 378, 2346–2348.
Madhun, A. S.; Haaheim, L. R.; Nilsen, M. V.; Cox, R. J. Intramuscular Matrix-M-adjuvanted virosomal H5N1 vaccine induces high frequencies of multifunctional Th1 CD4+ cells and strong antibody responses in mice. Vaccine 2009, 27, 7367–7376.
Shinde, V.; Bhikha, S.; Hoosain, Z.; Archary, M.; Bhorat, Q.; Fairlie, L.; Lalloo, U.; Masilela, M. S. L.; Moodley, D.; Hanley, S. et al. Efficacy of NVX-CoV2373 Covid-19 vaccine against the B. 1.351 variant. N. Engl. J. Med. 2021, 384, 1899–1909.
Honda-Okubo, Y.; Barnard, D.; Ong, C. H.; Peng, B. H.; Tseng, C. T. K.; Petrovsky, N. Severe acute respiratory syndrome-associated coronavirus vaccines formulated with delta inulin adjuvants provide enhanced protection while ameliorating lung eosinophilic immunopathology. J. Virol. 2015, 89, 2995–3007.
McPherson, C.; Chubet, R.; Holtz, K.; Honda-Okubo, Y.; Barnard, D.; Cox, M.; Petrovsky, N. Development of a SARS coronavirus vaccine from recombinant spike protein plus delta inulin adjuvant. Methods Mol. Biol. 2016, 1403, 269–284.
Zhou, Z. M.; Post, P.; Chubet, R.; Holtz, K.; McPherson, C.; Petric, M.; Cox, M. A recombinant baculovirus-expressed S glycoprotein vaccine elicits high titers of SARS-associated coronavirus (SARS-CoV) neutralizing antibodies in mice. Vaccine 2006, 24, 3624–3631.
Kerekes, K.; Cooper, P. D.; Prechl, J.; Józsi, M.; Bajtay, Z.; Erdei, A. Adjuvant effect of γ-inulin is mediated by C3 fragments deposited on antigen-presenting cells. J. Leukoc. Biol. 2001, 69, 69–74.
Müller-Eberhard, H. J. Molecular organization and function of the complement system. Annu. Rev. Biochem. 1988, 57, 321–347.
Mai-Prochnow, A.; Hui, J. G. K.; Kjelleberg, S.; Rakonjac, J.; McDougald, D.; Rice, S. A. ‘Big things in small packages: The genetics of filamentous phage and effects on fitness of their host’. FEMS Microbiol. Rev. 2015, 39, 465–487.
Hajitou, A.; Rangel, R.; Trepel, M.; Soghomonyan, S.; Gelovani, J. G.; Alauddin, M. M.; Pasqualini, R.; Arap, W. Design and construction of targeted AAVP vectors for mammalian cell transduction. Nat. Protoc. 2007, 2, 523–531.
Namdee, K.; Khongkow, M.; Boonrungsiman, S.; Nittayasut, N.; Asavarut, P.; Temisak, S.; Saengkrit, N.; Puttipipatkhachorn, S.; Hajitou, A.; Ruxrungtham, K. et al. Thermoresponsive bacteriophage nanocarrier as a gene delivery vector targeted to the gastrointestinal Tract. Mol. Ther. Nucleic Acids 2018, 12, 33–44.
Goracci, M.; Pignochino, Y.; Marchiò, S. Phage display-based nanotechnology applications in cancer immunotherapy. Molecules 2020, 25, 843.
Parmiani, G.; Russo, V.; Maccalli, C.; Parolini, D.; Rizzo, N.; Maio, M. Peptide-based vaccines for cancer therapy. Hum. Vaccin. Immunother. 2014, 10, 3175–3178.
Coley, A. M.; Campanale, N. V.; Casey, J. L.; Hodder, A. N.; Crewther, P. E.; Anders, R. F.; Tilley, L. M.; Foley, M. Rapid and precise epitope mapping of monoclonal antibodies against Plasmodium falciparum AMA1 by combined phage display of fragments and random peptides. Protein Eng. Des. Sel. 2001, 14, 691–698.
Frenkel, D.; Katz, O.; Solomon, B. Immunization against Alzheimer's β-amyloid plaques via EFRH phage administration. Proc. Natl. Acad. Sci. USA 2000, 97, 11455–11459.
Umscheid, C. A.; Margolis, D. J.; Grossman, C. E. Key concepts of clinical trials: A narrative review. Postgrad. Med. 2011, 123, 194–204.
Bao, L. L.; Deng, W.; Huang, B. Y.; Gao, H.; Liu, J. N.; Ren, L. L.; Wei, Q.; Yu, P.; Xu, Y. F.; Qi, F. F. et al. The pathogenicity of SARS-CoV-2 in hACE2 transgenic mice. Nature 2020, 583, 830–833.
Gu, H. J.; Chen, Q.; Yang, G.; He, L.; Fan, H.; Deng, Y. Q.; Wang, Y. X.; Teng, Y.; Zhao, Z. P.; Cui, Y. J. et al. Adaptation of SARS-CoV-2 in BALB/c mice for testing vaccine efficacy. Science 2020, 369, 1603–1607.
Chan, J. F. W.; Zhang, A. J.; Yuan, S. F.; Poon, V. K. M.; Chan, C. C. S.; Lee, A. C. Y.; Chan, W. M.; Fan, Z. M.; Tsoi, H. W.; Wen, L. et al. Simulation of the clinical and pathological manifestations of Coronavirus Disease 2019 (COVID-19) in a golden Syrian hamster model: Implications for disease pathogenesis and transmissibility. Clin. Infect. Dis. 2020, 71, 2428–2446.
Kim, Y. I.; Kim, S. G.; Kim, S. M.; Kim, E. H.; Park, S. J.; Yu, K. M.; Chang, J. H.; Kim, E. J.; Lee, S.; Casel, M. A. B. et al. Infection and rapid transmission of SARS-CoV-2 in ferrets. Cell Host Microbe 2020, 27, 704–709.e2.
Richard, M.; Kok, A.; de Meulder, D.; Bestebroer, T. M.; Lamers, M. M.; Okba, N. M. A.; van Vlissingen, M. F.; Rockx, B.; Haagmans, B. L.; Koopmans, M. P. G. et al. SARS-CoV-2 is transmitted via contact and via the air between ferrets. Nat. Commun. 2020, 11, 3496.
Chandrashekar, A.; Liu, J. Y.; Martinot, A. J.; McMahan, K.; Mercado, N. B.; Peter, L.; Tostanoski, L. H.; Yu, J. Y.; Maliga, Z.; Nekorchuk, M. et al. SARS-CoV-2 infection protects against rechallenge in rhesus macaques. Science 2020, 369, 812–817.
Ursino, M.; Zohar, S.; Lentz, F.; Alberti, C.; Friede, T.; Stallard, N.; Comets, E. Dose-finding methods for Phase I clinical trials using pharmacokinetics in small populations. Biom. J. 2017, 59, 804–825.
Rai, S. N.; Qian, C.; Pan, J. M.; Seth, A.; Srivastava, D. K.; Bhatnagar, A. Statistical design of Phase II/III clinical trials for testing therapeutic interventions in COVID-19 patients. BMC Med. Res. Methodol. 2020, 20, 220.
Hodgson, S. H.; Mansatta, K.; Mallett, G.; Harris, V.; Emary, K. R. W.; Pollard, A. J. What defines an efficacious COVID-19 vaccine? A review of the challenges assessing the clinical efficacy of vaccines against SARS-CoV-2. Lancet Infect. Dis. 2021, 21, E26–E35.
Werbel, W. A.; Boyarsky, B. J.; Ou, M. T.; Massie, A. B.; Tobian, A. A. R.; Garonzik-Wang, J. M.; Segev, D. L. Safety and immunogenicity of a third dose of SARS-CoV-2 vaccine in solid organ transplant recipients: A case series. Ann. Intern. Med. 2021, L21–0282.
’t Hart, B. A.; Bogers, W. M.; Haanstra, K. G.; Verreck, F. A.; Kocken, C. H. The translational value of non-human primates in preclinical research on infection and immunopathology. Eur. J. Pharmacol. 2015, 759, 69–83.
Johansen, M. D.; Irving, A.; Montagutelli, X.; Tate, M. D.; Rudloff, T. I.; Nold, M. F.; Hansbro, N. G.; Kim, R. Y.; Donovan, C.; Liu, G. et al. Animal and translational models of SARS-CoV-2 infection and COVID-19. Mucosal Immunol. 2020, 13, 877–891.
Muñoz-Fontela, C.; Dowling, W. E.; Funnell, S. G. P.; Gsell, P. S.; Riveros-Balta, A. X.; Albrecht, R. A.; Andersen, H.; Baric, R. S.; Carroll, M. W.; Cavaleri, M. et al. Animal models for COVID-19. Nature 2020, 586, 509–515.
Dearlove, B.; Lewitus, E.; Bai, H. J.; Li, Y. F.; Reeves, D. B.; Joyce, M. G.; Scott, P. T.; Amare, M. F.; Vasan, S.; Michael, N. L. et al. A SARS-CoV-2 vaccine candidate would likely match all currently circulating variants. Proc. Natl. Acad. Sci. USA 2020, 117, 23652–23662.
Koyama, T.; Platt, D.; Parida, L. Variant analysis of SARS-CoV-2 genomes. Bull. World Health Organ. 2020, 98, 495–504.
Kis, Z.; Kontoravdi, C.; Dey, A. K.; Shattock, R.; Shah, N. Rapid development and deployment of high-volume vaccines for pandemic response. J. Adv. Manuf. Process. 2020, 2, e10060.
Bahamondez-Canas, T. F.; Cui, Z. R. Intranasal immunization with dry powder vaccines. Eur. J. Pharm. Biopharm. 2018, 122, 167–175.
Pissuwan, D.; Nose, K.; Kurihara, R.; Kaneko, K.; Tahara, Y.; Kamiya, N.; Goto, M.; Katayama, Y.; Niidome, T. A solid-in-oil dispersion of gold nanorods can enhance transdermal protein delivery and skin vaccination. Small 2011, 7, 215–220.
Perlman, S.; Netland, J. Coronaviruses post-SARS: Update on replication and pathogenesis. Nat. Rev. Microbiol. 2009, 7, 439–450.
McGrath, B. A.; Brenner, M. J.; Warrillow, S. J.; Pandian, V.; Arora, A.; Cameron, T. S.; Añon, J. M.; Hernández Martínez, G.; Truog, R. D.; Block, S. D. et al. Tracheostomy in the COVID-19 era: Global and multidisciplinary guidance. Lancet Respir. Med. 2020, 8, 717–725.
Apostolopoulos, V.; Thalhammer, T.; Tzakos, A. G.; Stojanovska, L. Targeting antigens to dendritic cell receptors for vaccine development. J. Drug Deliv. 2013, 2013, 869718.
Xia, S. L.; Duan, K.; Zhang, Y. T.; Zhao, D. Y.; Zhang, H. J.; Xie, Z. Q.; Li, X. G.; Peng, C.; Zhang, Y. B.; Zhang, W. et al. Effect of an inactivated vaccine against SARS-CoV-2 on safety and immunogenicity outcomes: Interim analysis of 2 randomized clinical trials. JAMA 2020, 324, 951–960.
Isakova-Sivak, I.; Rudenko, L. A promising inactivated whole-virion SARS-CoV-2 vaccine. Lancet Infect. Dis. 2021, 21, 2–3.
Logunov, D. Y.; Dolzhikova, I. V.; Zubkova, O. V.; Tukhvatulin, A. I.; Shcheblyakov, D. V.; Dzharullaeva, A. S.; Grousova, D. M.; Erokhova, A. S.; Kovyrshina, A. V.; Botikov, A. G. et al. Safety and immunogenicity of an rAd26 and rAd5 vector-based heterologous prime-boost COVID-19 vaccine in two formulations: Two open, non-randomised phase 1/2 studies from Russia. Lancet 2020, 396, 887–897.
Folegatti, P. M.; Ewer, K. J.; Aley, P. K.; Angus, B.; Becker, S.; Belij-Rammerstorfer, S.; Bellamy, D.; Bibi, S.; Bittaye, M.; Clutterbuck, E. A. et al. Safety and immunogenicity of the ChAdOx1 nCoV-19 vaccine against SARS-CoV-2: A preliminary report of a phase 1/2, single-blind, randomised controlled trial. Lancet 2020, 396, 467–478.
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Acknowledgements
This work was supported by OCSC Royal Thai Government-UCAS Scholarship under research collaboration between National Nanotechnology Center (NANOTEC), Thailand, and National Center for Nanoscience and Technology, China (No. P1852764). This work was also supported by the National Natural Science Foundation of China (NSFC) key projects (Nos. 31630027 and 32030060), NSFC international collaboration key project (No. 51861135103), and NSFC-German Research Foundation (DFG) project (No. 31761133013). The authors also appreciate the support by “the Beijing-Tianjin-Hebei Basic Research Cooperation Project” (No. 19JCZDJC64100), and National Key Research & Development Program of China (No. 2018YFE0117800). The authors are grateful for Prof. Dr. S. Seraphin at the Professional Authorship Center, Thailand National Science, and Technology Development Agency (NSTDA) for fruitful discussions on the manuscript preparation.
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