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Immunotherapy, a burgeoning field differs from traditional cancer treatments, is revolutionizing oncologic therapeutics. It aims to stimulate the innate and adaptive immune system of a patient to fight against tumor cells. However, low response rate and immune-related adverse effects (irAEs) remain problems during its management. A novel technology using nanomaterials may bring a solution. Various nanoparticles have been investigated as delivery systems to augment cancer therapeutic efficacy in the lab and clinic. In this review, we briefly summarize the connotation of immunotherapy, the application of nanotechnology in cancer, especially focusing on the synergistic effect of nanoplatform-based technology combined with cancer immunotherapy, hoping to make readers a deep insight into this interdisciplinary field.


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Nanotechnologies for enhancing cancer immunotherapy

Show Author's information Jingxian YangChunhui WangShuo Shi( )Chunyan Dong( )
Breast cancer center, Shanghai East Hospital, School of Medicine, Shanghai Key Laboratory of Chemical Assessment and Sustainability, School of Chemical Science and Engineering, Tongji University, Shanghai 200120, China

Abstract

Immunotherapy, a burgeoning field differs from traditional cancer treatments, is revolutionizing oncologic therapeutics. It aims to stimulate the innate and adaptive immune system of a patient to fight against tumor cells. However, low response rate and immune-related adverse effects (irAEs) remain problems during its management. A novel technology using nanomaterials may bring a solution. Various nanoparticles have been investigated as delivery systems to augment cancer therapeutic efficacy in the lab and clinic. In this review, we briefly summarize the connotation of immunotherapy, the application of nanotechnology in cancer, especially focusing on the synergistic effect of nanoplatform-based technology combined with cancer immunotherapy, hoping to make readers a deep insight into this interdisciplinary field.

Keywords: cancer immunotherapy, combination therapy, synergistic effect, nanoplatform-based technology

References(207)

[1]
Torre, L. A.; Bray, F.; Siegel, R. L.; Ferlay, J.; Lortet-Tieulent, J.; Jemal, A. Global cancer statistics, 2012. CA Cancer J. Clin. 2015, 65, 87-108.
[2]
Ferlay, J.; Soerjomataram, I.; Dikshit, R.; Eser, S.; Mathers, C.; Rebelo, M.; Parkin, D. M.; Forman, D.; Bray, F. Cancer incidence and mortality worldwide: Sources, methods and major patterns in globocan 2012. Int. J. Cancer 2015, 136, E359-E386.
[3]
Fidler, M. M.; Bray, F.; Soerjomataram, I. The global cancer burden and human development: A review. Scand. J. Public Health 2018, 46, 27-36.
[4]
Nam, J.; Son, S.; Park, K. S.; Zou, W. P.; Shea, L. D.; Moon, J. J. Cancer nanomedicine for combination cancer immunotherapy. Nat. Rev. Mater. 2019, 4, 398-414.
[5]
Shi, J.; Kantoff, P. W.; Wooster, R.; Farokhzad, O. C. Cancer nanomedicine: Progress, challenges and opportunities. Nat. Rev. Cancer 2017, 17, 20-37.
[6]
Kim, K. Y. Nanotechnology platforms and physiological challenges for cancer therapeutics. Nanomedicine: Nanotechnol., Biol. Med. 2007, 3, 103-110.
[7]
Kalaydina, R. V.; Bajwa, K.; Qorri, B.; Decarlo, A.; Szewczuk, M. R. Recent advances in “smart” delivery systems for extended drug release in cancer therapy. Int. J. Nanomedicine 2018, 13, 4727-4745.
[8]
Van Der Meel, R.; Sulheim, E.; Shi, Y.; Kiessling, F.; Mulder, W. J. M.; Lammers, T. Smart cancer nanomedicine. Nat. Nanotechnol. 2019, 14, 1007-1017.
[9]
Shao, K.; Singha, S.; Clemente-Casares, X.; Tsai, S.; Yang, Y.; Santamaria, P. Nanoparticle-based immunotherapy for cancer. ACS Nano 2015, 9, 16-30.
[10]
Asadujjaman, M.; Cho, K. H.; Jang, D. J.; Kim, J. E.; Jee, J. P. Nanotechnology in the arena of cancer immunotherapy. Arch. Pharm. Res. 2020, 43, 58-79.
[11]
Helmy, K. Y.; Patel, S. A.; Nahas, G. R.; Rameshwar, P. Cancer immunotherapy: Accomplishments to date and future promise. Ther. Deliv. 2013, 4, 1307-1320.
[12]
Sun, Q. X.; Barz, M.; De Geest, B. G.; Diken, M.; Hennink, W. E.; Kiessling, F.; Lammers, T.; Shi, Y. Nanomedicine and macroscale materials in immuno-oncology. Chem. Soc. Rev. 2019, 48, 351-381.
[13]
Shi, Y.; Lammers, T. Combining nanomedicine and immunotherapy. Acc. Chem. Res. 2019, 52, 1543-1554.
[14]
Song, W. T.; Musetti, S. N.; Huang, L. Nanomaterials for cancer immunotherapy. Biomaterials 2017, 148, 16-30.
[15]
Chen, D. S.; Mellman, I. Oncology meets immunology: The cancer- immunity cycle. Immunity 2013, 39, 1-10.
[16]
Sanmamed, M. F.; Chen, L. P. A paradigm shift in cancer immunotherapy: From enhancement to normalization. Cell 2018, 175, 313-326.
[17]
Dunn, G. P.; Bruce, A. T.; Ikeda, H.; Old, L. J.; Schreiber, R. D. Cancer immunoediting: From immunosurveillance to tumor escape. Nat. Immunol. 2002, 3, 991-998.
[18]
Galluzzi, L.; Vacchelli, E.; Bravo-San Pedro, J. M.; Buqué, A.; Senovilla, L.; Baracco, E. E.; Bloy, N.; Castoldi, F.; Abastado, J. P.; Agostinis, P. et al. Classification of current anticancer immunotherapies. Oncotarget 2014, 5, 12472-12508.
[19]
Demaria, O.; Cornen, S.; Daëron, M.; Morel, Y.; Medzhitov, R.; Vivier, E. Harnessing innate immunity in cancer therapy. Nature 2019, 574, 45-56.
[20]
Abril-Rodriguez, G.; Ribas, A. SnapShot: Immune checkpoint inhibitors. Cancer Cell 2017, 31, 848-848.e1.
[21]
Kennedy, L. B.; Salama, A. K. S. A review of cancer immunotherapy toxicity. CA Cancer J. Clin. 2020, 70, 86-104.
[22]
Zhang, H. M.; Chen, J. B. Current status and future directions of cancer immunotherapy. J. Cancer 2018, 9, 1773-1781.
[23]
Sakaguchi, S.; Mikami, N.; Wing, J. B.; Tanaka, A.; Ichiyama, K.; Ohkura, N. Regulatory T cells and human disease. Annu. Rev. Immunol. 2020, 38: 541-566.
[24]
Vinay, D. S.; Ryan, E. P.; Pawelec, G.; Talib, W. H.; Stagg, J.; Elkord, E.; Lichtor, T.; Decker, W. K.; Whelan, R. L.; Kumara, H. M. C. S. et al. Immune evasion in cancer: Mechanistic basis and therapeutic strategies. Semin. Cancer Biol. 2015, 35, S185-S198.
[25]
Schreiber, R. D.; Old, L. J.; Smyth, M. J. Cancer immunoediting: Integrating immunity's roles in cancer suppression and promotion. Science 2011, 331, 1565-1570.
[26]
Motz, G. T.; Coukos, G. Deciphering and reversing tumor immune suppression. Immunity 2013, 39, 61-73.
[27]
Jensen-Jarolim, E.; Bax, H. J.; Bianchini, R.; Crescioli, S.; Daniels- Wells, T. R.; Dombrowicz, D.; Fiebiger, E.; Gould, H. J.; Irshad, S.; Janda, J. et al. AllergoOncology: Opposite outcomes of immune tolerance in allergy and cancer. Allergy 2018, 73, 328-340.
[28]
Makkouk, A.; Weiner, G. J. Cancer immunotherapy and breaking immune tolerance: New approaches to an old challenge. Cancer Res. 2015, 75, 5-10.
[29]
Nishino, M.; Hatabu, H.; Hodi, F. S. Imaging of cancer immunotherapy: Current approaches and future directions. Radiology 2019, 290, 9-22.
[30]
Mulder, W. J. M.; Ochando, J.; Joosten, L. A. B.; Fayad, Z. A.; Netea, M. G. Therapeutic targeting of trained immunity. Nat. Rev. Drug Discov. 2019, 18, 553-566.
[31]
Fan, W. P.; Yung, B.; Huang, P.; Chen, X. Y. Nanotechnology for multimodal synergistic cancer therapy. Chem. Rev. 2017, 117, 13566-13638.
[32]
Russell, L. M.; Liu, C. H.; Grodzinski, P. Nanomaterials innovation as an enabler for effective cancer interventions. Biomaterials 2020, 242, 119926.
[33]
Liu, Y. Y.; Qiao, L. N.; Zhang, S. P.; Wan, G. Y.; Chen, B. W.; Zhou, P.; Zhang, N.; Wang, Y. S. Dual pH-responsive multifunctional nanoparticles for targeted treatment of breast cancer by combining immunotherapy and chemotherapy. Acta Biomater. 2018, 66, 310-324.
[34]
Desale, S. S.; Raja, S. M.; Kim, J. O.; Mohapatra, B.; Soni, K. S.; Luan, H. T.; Williams, S. H.; Bielecki, T. A.; Feng, D.; Storck, M. et al. Polypeptide-based nanogels co-encapsulating a synergistic combination of doxorubicin with 17-aag show potent anti-tumor activity in erbb2-driven breast cancer models. J. Control. Release 2015, 208, 59-66.
[35]
Wang, C.; Chen, S. Q.; Wang, Y. X.; Liu, X. R.; Hu, F. Q.; Sun, J. H.; Yuan, H. Lipase-triggered water-responsive “pandora’s box” for cancer therapy: Toward induced neighboring effect and enhanced drug penetration. Adv. Mater. 2018, 30, 1706407.
[36]
Shi, L. L.; Hu, F.; Duan, Y. K.; Wu, W. B.; Dong, J. Q.; Meng, X. J.; Zhu, X. Y.; Liu, B. Hybrid nanospheres to overcome hypoxia and intrinsic oxidative resistance for enhanced photodynamic therapy. ACS Nano 2020, 14, 2183-2190.
[37]
Gulzar, A.; Xu, J. T.; Yang, D.; Xu, L. G.; He, F.; Gai, S. L.; Yang, P. P. Nano-graphene oxide-ucnp-ce6 covalently constructed nanocomposites for nir-mediated bioimaging and ptt/pdt combinatorial therapy. Dalton Trans. 2018, 47, 3931-3939.
[38]
Zhang, C.; Bu, W. B.; Ni, D. L.; Zhang, S. J.; Li, Q.; Yao, Z. W.; Zhang, J. W.; Yao, H. L.; Wang, Z.; Shi, J. L. Synthesis of iron nanometallic glasses and their application in cancer therapy by a localized fenton reaction. Angew. Chem., Int. Ed. 2016, 55, 2101-2106.
[39]
Deepagan, V. G.; You, D. G.; Um, W.; Ko, H.; Kwon, S.; Choi, K. Y.; Yi, G. R.; Lee, J. Y.; Lee, D. S.; Kim, K. et al. Long-circulating au-TiO2 nanocomposite as a sonosensitizer for ros-mediated eradication of cancer. Nano Lett. 2016, 16, 6257-6264.
[40]
Zhu, J. Y.; Zheng, D. W.; Zhang, M. K.; Yu, W. Y.; Qiu, W. X.; Hu, J. J.; Feng, J.; Zhang, X. Z. Preferential cancer cell self-recognition and tumor self-targeting by coating nanoparticles with homotypic cancer cell membranes. Nano Lett. 2016, 16, 5895-5901.
[41]
Cun, X. L.; Ruan, S. B.; Chen, J. T.; Zhang, L.; Li, J. P.; He, Q.; Gao, H. L. A dual strategy to improve the penetration and treatment of breast cancer by combining shrinking nanoparticles with collagen depletion by losartan. Acta Biomater. 2016, 31, 186-196.
[42]
Ma, T. C.; Liu, Y. D.; Wu, Q.; Luo, L. F.; Cui, Y. L.; Wang, X. H.; Chen, X. W.; Tan, L. F.; Meng, X. W. Quercetin-modified metal- organic frameworks for dual sensitization of radiotherapy in tumor tissues by inhibiting the carbonic anhydrase IX. ACS Nano 2019, 13, 4209-4219.
[43]
Wang, J. T. W.; Klippstein, R.; Martincic, M.; Pach, E.; Feldman, R.; Šefl, M.; Michel, Y.; Asker, D.; Sosabowski, J. K.; Kalbac, M. et al. Neutron activated 153Sm sealed in carbon nanocapsules for in vivo imaging and tumor radiotherapy. ACS Nano 2020, 14, 129-141.
[44]
Tavallaie, R.; McCarroll, J.; Le Grand, M.; Ariotti, N.; Schuhmann, W.; Bakker, E.; Tilley, R. D.; Hibbert, D. B.; Kavallaris, M.; Gooding, J. J. Nucleic acid hybridization on an electrically reconfigurable network of gold-coated magnetic nanoparticles enables microrna detection in blood. Nat. Nanotechnol. 2018, 13, 1066-1071.
[45]
Xie, Y.; Hang, Y.; Wang, Y. Z.; Sleightholm, R.; Prajapati, D. R.; Bader, J.; Yu, A.; Tang, W. M.; Jaramillo, L.; Li, J. et al. Stromal modulation and treatment of metastatic pancreatic cancer with local intraperitoneal triple mirna/sirna nanotherapy. ACS Nano 2020, 14, 255-271.
[46]
Wang, S.; Liu, X.; Chen, S. Z.; Liu, Z. R.; Zhang, X. D.; Liang, X. J.; Li, L. L. Regulation of Ca2+ signaling for drug-resistant breast cancer therapy with mesoporous silica nanocapsule encapsulated doxorubicin/sirna cocktail. ACS Nano 2019, 13, 274-283.
[47]
Yang, W. J.; Zhu, G. Z.; Wang, S.; Yu, G. C.; Yang, Z.; Lin, L. S.; Zhou, Z. J.; Liu, Y. J..; Dai, Y. L.; Zhang, F. W. et al. In situ dendritic cell vaccine for effective cancer immunotherapy. ACS Nano 2019, 13, 3083-3094.
[48]
Qiu, F.; Becker, K. W.; Knight, F. C.; Baljon, J. J.; Sevimli, S.; Shae, D.; Gilchuk, P.; Joyce, S.; Wilson, J. T. Poly(propylacrylic acid)-peptide nanoplexes as a platform for enhancing the immunogenicity of neoantigen cancer vaccines. Biomaterials 2018, 182, 82-91.
[49]
Gulla, S. K.; Rao, B. R.; Moku, G.; Jinka, S.; Nimmu, N. V.; Khalid, S.; Patra, C. R.; Chaudhuri, A. In vivo targeting of DNA vaccines to dendritic cells using functionalized gold nanoparticles. Biomater. Sci. 2019, 7, 773-788.
[50]
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.
[51]
Colzani, B.; Pandolfi, L.; Hoti, A.; Iovene, P. A.; Natalello, A.; Avvakumova, S.; Colombo, M.; Prosperi, D. Investigation of antitumor activities of trastuzumab delivered by plga nanoparticles. Int. J. Nanomedicine 2018, 13, 957-973.
[52]
Shae, D.; Becker, K. W.; Christov, P.; Yun, D. S.; Lytton-Jean, A. K. R.; Sevimli, S.; Ascano, M.; Kelley, M.; Johnson, D. B.; Balko, J. M. et al. Endosomolytic polymersomes increase the activity of cyclic dinucleotide sting agonists to enhance cancer immunotherapy. Nat. Nanotechnol. 2019, 14, 269-278.
[53]
Steeland, S.; Vandenbroucke, R. E.; Libert, C. Nanobodies as therapeutics: Big opportunities for small antibodies. Drug Discov. Today 2016, 21, 1076-1113.
[54]
Song, S. L.; Jin, X. X.; Zhang, L.; Zhao, C.; Ding, Y.; Ang, Q. Q.; Khaidav, O.; Shen, C. L. Pegylated and CD47-conjugated nanoellipsoidal artificial antigen-presenting cells minimize phagocytosis and augment anti-tumor t-cell responses. Int. J. Nanomedicine 2019, 14, 2465-2483.
[55]
Smith, T. T.; Stephan, S. B.; Moffett, H. F.; McKnight, L. E.; Ji, W. H.; Reiman, D.; Bonagofski, E.; Wohlfahrt, M. E.; Pillai, S. P. S.; Stephan, M. T. In situ programming of leukaemia-specific t cells using synthetic DNA nanocarriers. Nat. Nanotechnol. 2017, 12, 813-820.
[56]
Lang, J. Y.; Zhao, X.; Qi, Y. Q.; Zhang, Y. L.; Han, X. X.; Ding, Y. P.; Guan, J. J.; Ji, T. J.; Zhao, Y.; Nie, G. J. Reshaping prostate tumor microenvironment to suppress metastasis via cancer-associated fibroblast inactivation with peptide-assembly-based nanosystem. ACS Nano 2019, 13, 12357-12371.
[57]
Shen, S.; Li, H. J.; Chen, K. G.; Wang, Y. C.; Yang, X. Z.; Lian, Z. X.; Du, J. Z.; Wang, J. Spatial targeting of tumor-associated macrophages and tumor cells with a pH-sensitive cluster nanocarrier for cancer chemoimmunotherapy. Nano Lett. 2017, 17, 3822-3829.
[58]
Liu, D. C.; Chen, B. L.; Mo, Y. L.; Wang, Z. H.; Qi, T.; Zhang, Q.; Wang, Y. G. Redox-activated porphyrin-based liposome remote-loaded with indoleamine 2,3-dioxygenase (IDO) inhibitor for synergistic photoimmunotherapy through induction of immunogenic cell death and blockage of ido pathway. Nano Lett. 2019, 19, 6964-6976.
[59]
Lang, T. Q.; Liu, Y. R.; Zheng, Z.; Ran, W.; Zhai, Y. H.; Yin, Q.; Zhang, P. C.; Li, Y. P. Cocktail strategy based on spatio-temporally controlled nano device improves therapy of breast cancer. Adv. Mater. 2019, 31, 1806202.
[60]
Gao, S. Q.; Li, T. Y.; Guo, Y.; Sun, C. X.; Xianyu, B. R.; Xu, H. P. Selenium-containing nanoparticles combine the NK cells mediated immunotherapy with radiotherapy and chemotherapy. Adv. Mater. 2020, 32, 1907568.
[61]
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.
[62]
Goldberg, M. S. Improving cancer immunotherapy through nanotechnology. Nat. Rev. Cancer 2019, 19, 587-602.
[63]
Zhou, Q.; Shao, S. Q.; Wang, J. Q.; Xu, C. H.; Xiang, J. J.; Piao, Y.; Zhou, Z. X.; Yu, Q. S.; Tang, J. B.; Liu, X. R. et al. Enzyme- activatable polymer-drug conjugate augments tumour penetration and treatment efficacy. Nat. Nanotechnol. 2019, 14, 799-809.
[64]
Zhang, S. Q.; Liu, X.; Sun, Q. X.; Johnson, O.; Yang, T.; Chen, M. L.; Wang, J. H.; Chen, W. Cus@PDA-FA nanocomposites: A dual stimuli-responsive DOX delivery vehicle with ultrahigh loading level for synergistic photothermal-chemotherapies on breast cancer. J. Mater. Chem. B 2020, 8, 1396-1404.
[65]
Zhu, X. H.; Tang, R.; Wang, S. G.; Chen, X. Y.; Hu, J. J.; Lei, C. Y.; Huang, Y.; Wang, H. H.; Nie, Z.; Yao, S. Z. Protein@inorganic nanodumpling system for high-loading protein delivery with activatable fluorescence and magnetic resonance bimodal imaging capabilities. ACS Nano 2020, 14, 2172-2182.
[66]
Kosmides, A. K.; Sidhom, J. W.; Fraser, A.; Bessell, C. A.; Schneck, J. P. Dual targeting nanoparticle stimulates the immune system to inhibit tumor growth. ACS Nano 2017, 11, 5417-5429.
[67]
Yong, T. Y.; Zhang, X. Q.; Bie, N. N.; Zhang, H. B.; Zhang, X. T.; Li, F. Y.; Hakeem, A.; Hu, J.; Gan, L.; Santos, H. A. et al. Tumor exosome-based nanoparticles are efficient drug carriers for chemotherapy. Nat. Commun. 2019, 10, 3838.
[68]
He, J. Y.; Li, C. C.; Ding, L.; Huang, Y. N.; Yin, X. L.; Zhang, J. F.; Zhang, J.; Yao, C. J.; Liang, M. M.; Pirraco, R. P. et al. Tumor targeting strategies of smart fluorescent nanoparticles and their applications in cancer diagnosis and treatment. Adv. Mater. 2019, 31, 1902409.
[69]
Wang, X. H.; Wang, X. Y.; Jin, S. X.; Muhammad, N.; Guo, Z. J. Stimuli-responsive therapeutic metallodrugs. Chem. Rev. 2019, 119, 1138-1192.
[70]
Xu, P. P.; Wang, X. Y.; Li, T. W.; Wu, H. H.; Li, L. L.; Chen, Z. L.; Zhang, L.; Guo, Z.; Chen, Q. W. Biomineralization-inspired nanozyme for single-wavelength laser activated photothermal-photodynamic synergistic treatment against hypoxic tumors. Nanoscale 2020, 12, 4051-4060.
[71]
Dasgupta, S.; Rajapakshe, K.; Zhu, B. K.; Nikolai, B. C.; Yi, P.; Putluri, N.; Choi, J. M.; Jung, S. Y.; Coarfa, C.; Westbrook, T. F. et al. Metabolic enzyme PFKFB4 activates transcriptional coactivator SRC-3 to drive breast cancer. Nature 2018, 556, 249-254.
[72]
Gao, R. F.; Li, D.; Xun, J.; Zhou, W.; Li, J.; Wang, J.; Liu, C.; Li, X. R.; Shen, W. Z.; Qiao, H. et al. CD44ICD promotes breast cancer stemness via PFKFB4-mediated glucose metabolism. Theranostics 2018, 8, 6248-6262.
[73]
Sarkar Bhattacharya, S.; Thirusangu, P.; Jin, L.; Roy, D.; Jung, D.; Xiao, Y. N.; Staub, J.; Roy, B.; Molina, J. R.; Shridhar, V. PFKFB3 inhibition reprograms malignant pleural mesothelioma to nutrient stress-induced macropinocytosis and er stress as independent binary adaptive responses. Cell Death Dis. 2019, 10, 725.
[74]
Mondal, S.; Roy, D.; Sarkar Bhattacharya, S.; Jin, L.; Jung, D.; Zhang, S.; Kalogera, E.; Staub, J.; Wang, Y. X.; Xuyang, W. et al. Therapeutic targeting of pfkfb3 with a novel glycolytic inhibitor pfk158 promotes lipophagy and chemosensitivity in gynecologic cancers. Int. J. Cancer 2019, 144, 178-189.
[75]
Li, Y.; He, L. H.; Dong, H. Q.; Liu, Y. Q.; Wang, K.; Li, A.; Ren, T. B.; Shi, D. L.; Li, Y. Y. Fever-inspired immunotherapy based on photothermal cpg nanotherapeutics: The critical role of mild heat in regulating tumor microenvironment. Adv. Sci. 2018, 5, 1700805.
[76]
Hu, X. C.; Lu, Y. L.; Shi, X. K.; Yao, T. M.; Dong, C. Y.; Shi, S. Integrating in situ formation of nanozymes with mesoporous polydopamine for combined chemo, photothermal and hypoxia- overcoming photodynamic therapy. Chem. Commun. 2019, 55, 14785-14788.
[77]
Hu, X. C.; Lu, Y. L.; Dong, C. Y.; Zhao, W. R.; Wu, X. W.; Zhou, L. L.; Chen, L.; Yao, T. M.; Shi, S. A RuII polypyridyl alkyne complex based metal-organic frameworks for combined photodynamic/ photothermal/chemotherapy. Chemistry 2020, 26, 1668-1675.
[78]
Wang, W. Q.; Jin, Y. L.; Xu, Z. A.; Liu, X.; Bajwa, S. Z.; Khan, W. S.; Yu, H. J. Stimuli-activatable nanomedicines for chemodynamic therapy of cancer. Wiley Interdiscip. Rev. Nanomedicine. Nanobiotechnol. 2020, 12, e1614.
[79]
Lin, L. S.; Song, J. B.; Song, L.; Ke, K. M.; Liu, Y. J.; Zhou, Z. J.; Shen, Z. Y.; Li, J.; Yang, Z.; Tang, W. et al. Simultaneous fenton-like ion delivery and glutathione depletion by Mno2-based nanoagent to enhance chemodynamic therapy. Angew. Chem., Int. Ed. 2018, 57, 4902-4906.
[80]
Gao, F. L.; He, G. L.; Yin, H.; Chen, J.; Liu, Y. B.; Lan, C.; Zhang, S. R.; Yang, B. C. Titania-coated 2D gold nanoplates as nanoagents for synergistic photothermal/sonodynamic therapy in the second near- infrared window. Nanoscale 2019, 11, 2374-2384.
[81]
Shen, Z. Y.; Song, J. B.; Zhou, Z. J.; Yung, B. C.; Aronova, M. A.; Li, Y.; Dai, Y. L.; Fan, W. P.; Liu, Y. J.; Li, Z. H. et al. Dotted core-shell nanoparticles for T1 -weighted MRI of tumors. Adv. Mater. 2018, 30, 1803163.
[82]
Liu, Y. J.; Bhattarai, P.; Dai, Z. F.; Chen, X. Y. Photothermal therapy and photoacoustic imaging via nanotheranostics in fighting cancer. Chem. Soc. Rev. 2019, 48, 2053-2108.
[83]
Wong, X. Y.; Sena-Torralba, A.; Álvarez-Diduk, R.; Muthoosamy, K.; Merkoçi, A. Nanomaterials for nanotheranostics: Tuning their properties according to disease needs. ACS Nano 2020, 14, 2585-2627.
[84]
Ali, E. S.; Sharker, S. M.; Islam, M. T.; Khan, I. N.; Shaw, S.; Rahman, M. A.; Uddin, S. J.; Shill, M. C.; Rehman, S.; Das, N. et al. Targeting cancer cells with nanotherapeutics and nanodiagnostics: Current status and future perspectives. Semin. Cancer Biol., in press, .
[85]
Wang, S.; Lin, J.; Wang, Z. T.; Zhou, Z. J.; Bai, R. L.; Lu, N.; Liu, Y. J.; Fu, X.; Jacobson, O.; Fan, W. P. et al. Core-satellite polydopamine-gadolinium-metallofullerene nanotheranostics for multimodal imaging guided combination cancer therapy. Adv. Mater. 2017, 29, 1701013.
[86]
Lin, X.; Song, X. F.; Zhang, Y. W.; Cao, Y. B.; Xue, Y. N.; Wu, F. S.; Yu, F. Q.; Wu, M.; Zhu, X. J. Multifunctional theranostic nanosystems enabling photothermal-chemo combination therapy of triple-stimuli- responsive drug release with magnetic resonance imaging. Biomater. Sci. 2020, 8, 1875-1884.
[87]
Yang, Z.; Song, J. B.; Tang, W.; Fan, W. P.; Dai, Y. L.; Shen, Z. Y.; Lin, L. S.; Cheng, S. Y.; Liu, Y. J.; Niu, G. et al. Stimuli-responsive nanotheranostics for real-time monitoring drug release by photoacoustic imaging. Theranostics 2019, 9, 526-536.
[88]
Yang, Z.; Dai, Y. L.; Yin, C.; Fan, Q. L.; Zhang, W. S.; Song, J.; Yu, G. C.; Tang, W.; Fan, W. P.; Yung, B. C. et al. Activatable semiconducting theranostics: Simultaneous generation and ratiometric photoacoustic imaging of reactive oxygen species in vivo. Adv. Mater. 2018, 30, 1707509.
[89]
Sung, Y. C.; Jin, P. R.; Chu, L. A.; Hsu, F. F.; Wang, M. R.; Chang, C. C.; Chiou, S. J.; Qiu, J. T.; Gao, D. Y.; Lin, C. C. et al. Delivery of nitric oxide with a nanocarrier promotes tumour vessel normalization and potentiates anti-cancer therapies. Nat. Nanotechnol. 2019, 14, 1160-1169.
[90]
Truffi, M.; Mazzucchelli, S.; Bonizzi, A.; Sorrentino, L.; Allevi, R.; Vanna, R.; Morasso, C.; Corsi, F. Nano-strategies to target breast cancer-associated fibroblasts: Rearranging the tumor microenvironment to achieve antitumor efficacy. Int. J. Mol. Sci. 2019, 20, 1263.
[91]
Chung, S. J.; Nagaraju, G. P.; Nagalingam, A.; Muniraj, N.; Kuppusamy, P.; Walker, A.; Woo, J.; Győrffy, B.; Gabrielson, E.; Saxena, N. K. et al. ADIPOQ/adiponectin induces cytotoxic autophagy in breast cancer cells through STK11/LKB1-mediated activation of the AMPK-ULK1 axis. Autophagy 2017, 13, 1386-1403.
[92]
Katheder, N. S.; Khezri, R.; O'Farrell, F.; Schultz, S. W.; Jain, A.; Rahman, M. M.; Schink, K. O.; Theodossiou, T. A.; Johansen, T.; Juhász, G. et al. Microenvironmental autophagy promotes tumour growth. Nature 2017, 541, 417-420.
[93]
Chen, Q.; Chen, J. W.; Yang, Z. J.; Xu, J.; Xu, L. G.; Liang, C.; Han, X.; Liu, Z. Nanoparticle-enhanced radiotherapy to trigger robust cancer immunotherapy. Adv. Mater. 2019, 31, 1802228.
[94]
Gao, S.; Zhang, W. Z.; Wang, R. J.; Hopkins, S. P.; Spagnoli, J. C.; Racin, M.; Bai, L.; Li, L.; Jiang, W.; Yang, X. Y. et al. Nanoparticles encapsulating nitrosylated maytansine to enhance radiation therapy. ACS Nano 2020, 14, 1468-1481.
[95]
Sarkar, S.; Levi-Polyachenko, N. Conjugated polymer nano-systems for hyperthermia, imaging and drug delivery. Adv. Drug Deliv. Rev., in press, .
[96]
Hotchkiss, R. D. The quantitative separation of purines, pyrimidines, and nucleosides by paper chromatography. J. Biol. Chem. 1948, 175, 315-332.
[97]
Kubik, T.; Bogunia-Kubik, K.; Sugisaka, M. Nanotechnology on duty in medical applications. Curr. Pharm. Biotechnol. 2005, 6, 17-33.
[98]
Fire, A.; Xu, S. Q.; Montgomery, M. K.; Kostas, S. A.; Driver, S. E.; Mello, C. C. Potent and specific genetic interference by double- stranded rna in Caenorhabditis elegans. Nature 1998, 391, 806-811.
[99]
Yatsunyk, L. A.; Mendoza, O.; Mergny, J. L. “Nano-oddities”: Unusual nucleic acid assemblies for DNA-based nanostructures and nanodevices. Acc. Chem. Res. 2014, 47, 1836-1844.
[100]
Putnam, D. Polymers for gene delivery across length scales. Nat. Mater. 2006, 5, 439-451.
[101]
Xin, Y.; Huang, M.; Guo, W. W.; Huang, Q.; Zhang, L. Z.; Jiang, G. Nano-based delivery of rnai in cancer therapy. Mol. Cancer 2017, 16, 134.
[102]
Liu, Y. J.; Zou, Y.; Feng, C.; Lee, A.; Yin, J. L.; Chung, R.; Park, J. B.; Rizos, H.; Tao, W.; Zheng, M. et al. Charge conversional biomimetic nanocomplexes as a multifunctional platform for boosting orthotopic glioblastoma rnai therapy. Nano Lett. 2020, 20, 1637-1646.
[103]
Yu, T.; Guo, F. F.; Yu, Y. N.; Sun, T. T.; Ma, D.; Han, J. X.; Qian, Y.; Kryczek, I.; Sun, D. F.; Nagarsheth, N. et al. Fusobacterium nucleatum promotes chemoresistance to colorectal cancer by modulating autophagy. Cell 2017, 170, 548-563.e16.
[104]
Eedunuri, V. K.; Rajapakshe, K.; Fiskus, W.; Geng, C. D.; Chew, S. A.; Foley, C.; Shah, S. S.; Shou, J.; Mohamed, J. S.; Coarfa, C. et al. miR-137 targets p160 steroid receptor coactivators SRC1, SRC2, and SRC3 and inhibits cell proliferation. Mol. Endocrinol. 2015, 29, 1170-1183.
[105]
Vodnala, S. K.; Eil, R.; Kishton, R. J.; Sukumar, M.; Yamamoto, T. N.; Ha, N. H.; Lee, P. H.; Shin, M.; Patel, S. J.; Yu, Z. Y. et al. T cell stemness and dysfunction in tumors are triggered by a common mechanism. Science 2019, 363, eaau0135.
[106]
Loginov, V. I.; Burdennyy, A. M.; Pronina, I. V.; Khokonova, V. V.; Kurevljov, S. V.; Kazubskaya, T. P.; Kushlinskii, N. E.; Braga, E. A. Novel miRNA genes hypermethylated in breast cancer. Mol. Biol. 2016, 50, 705-709.
[107]
Zhang, D.; Tang, Z. Y.; Huang, H.; Zhou, G. L.; Cui, C.; Weng, Y. J.; Liu, W. C.; Kim, S.; Lee, S.; Perez-Neut, M. et al. Metabolic regulation of gene expression by histone lactylation. Nature 2019, 574, 575-580.
[108]
Hoos, A. Development of immuno-oncology drugs—from CTLA4 to PD1 to the next generations. Nat. Rev. Drug Discov. 2016, 15, 235-247.
[109]
Dong, H.; Xu, X.; Wang, L. K.; Mo, R. Advances in living cell-based anticancer therapeutics. Biomater. Sci. 2020, 8, 2344-2365.
[110]
Xu, X.; Li, T.; Shen, S. Y.; Wang, J. Q.; Abdou, P.; Gu, Z.; Mo, R. Advances in engineering cells for cancer immunotherapy. Theranostics 2019, 9, 7889-7905.
[111]
Abdou, P.; Wang, Z. J.; Chen, Q.; Chan, A.; Zhou, D. R.; Gunadhi, V.; Gu, Z. Advances in engineering local drug delivery systems for cancer immunotherapy. Wiley Interdiscip. Rev. Nanomedicine. Nanobiotechnol., in press, .
[112]
Sharma, P.; Allison, J. P. The future of immune checkpoint therapy. Science 2015, 348, 56-61.
[113]
Sharma, P.; Allison, J. P. Immune checkpoint targeting in cancer therapy: Toward combination strategies with curative potential. Cell 2015, 161, 205-214.
[114]
Sang, W.; Zhang, Z.; Dai, Y. L.; Chen, X. Y. Recent advances in nanomaterial-based synergistic combination cancer immunotherapy. Chem. Soc. Rev. 2019, 48, 3771-3810.
[115]
Wei, X. X.; Fong, L.; Small, E. J. Prostate cancer immunotherapy with sipuleucel-T: Current standards and future directions. Expert Rev. Vaccines 2015, 14, 1529-1541.
[116]
Van Der Bruggen, P.; Traversari, C.; Chomez, P.; Lurquin, C.; De Plaen, E.; Van den Eynde, B.; Knuth, A.; Boon, T. A gene encoding an antigen recognized by cytolytic T lymphocytes on a human melanoma. Science 1991, 254, 1643-1647.
[117]
Song, Q.; Zhang, C. D.; Wu, X. H. Therapeutic cancer vaccines: From initial findings to prospects. Immunol. Lett. 2018, 196, 11-21.
[118]
Zhang, Y.; Lin, S. B.; Wang, X. Y.; Zhu, G. Z. Nanovaccines for cancer immunotherapy. Wiley Interdiscip. Rev. Nanomedicine. Nanobiotechnol. 2019, 11, e1559.
[119]
Palucka, K.; Banchereau, J. Cancer immunotherapy via dendritic cells. Nat. Rev. Cancer 2012, 12, 265-277.
[120]
Zhang, J. X.; Mai, J. H.; Li, F.; Shen, J. L.; Zhang, G. D.; Li, J.; Hinkle, L. E.; Lin, D.; Liu, X. W.; Li, Z. et al. Investigation of parameters that determine nano-DC vaccine transport. Biomed. Microdevices 2019, 21, 39.
[121]
Xia, X. J.; Mai, J. H.; Xu, R.; Perez, J. E. T.; Guevara, M. L.; Shen, Q.; Mu, C. F.; Tung, H. Y.; Corry, D. B.; Evans, S. E. et al. Porous silicon microparticle potentiates anti-tumor immunity by enhancing cross-presentation and inducing type I interferon response. Cell Rep. 2015, 11, 957-966.
[122]
Duong, H. T. T.; Thambi, T.; Yin, Y.; Kim, S. H.; Nguyen, T. L.; Phan, V. H. G.; Kim, J.; Jeong, J. H.; Lee, D. S. Degradation-regulated architecture of injectable smart hydrogels enhances humoral immune response and potentiates antitumor activity in human lung carcinoma. Biomaterials 2020, 230, 119599.
[123]
Milani, A.; Sangiolo, D.; Montemurro, F.; Aglietta, M.; Valabrega, G. Active immunotherapy in HER2 overexpressing breast cancer: Current status and future perspectives. Ann. Oncol. 2013, 24, 1740-1748.
[124]
Yang, Z. G.; Ma, Y. F.; Zhao, H.; Yuan, Y.; Kim, B. Y. S. Nanotechnology platforms for cancer immunotherapy. Wiley Interdiscip. Rev. Nanomedicine. Nanobiotechnol. 2020, 12, e1590.
[125]
Li, A. W.; Sobral, M. C.; Badrinath, S.; Choi, Y.; Graveline, A.; Stafford, A. G.; Weaver, J. C.; Dellacherie, M. O.; Shih, T. Y.; Ali, O. A. et al. A facile approach to enhance antigen response for personalized cancer vaccination. Nat. Mater. 2018, 17, 528-534.
[126]
Wilson, J. T.; Postma, A.; Keller, S.; Convertine, A. J.; Moad, G.; Rizzardo, E.; Meagher, L.; Chiefari, J.; Stayton, P. S. Enhancement of MHC-I antigen presentation via architectural control of pH-responsive, endosomolytic polymer nanoparticles. AAPS J. 2015, 17, 358-369.
[127]
Alspach, E.; Lussier, D. M.; Miceli, A. P.; Kizhvatov, I.; DuPage, M.; Luoma, A. M.; Meng, W.; Lichti, C. F.; Esaulova, E.; Vomund, A. N. et al. MHC-II neoantigens shape tumour immunity and response to immunotherapy. Nature 2019, 574, 696-701.
[128]
Liu, M. A. DNA vaccines: An historical perspective and view to the future. Immunol. Rev. 2011, 239, 62-84.
[129]
Riley, R. S.; June, C. H.; Langer, R.; Mitchell, M. J. Delivery technologies for cancer immunotherapy. Nat. Rev. Drug Discov. 2019, 18, 175-196.
[130]
Lu, Y. X.; Wu, F. P.; Duan, W. H.; Mu, X.; Fang, S.; Lu, N. N.; Zhou, X. F.; Kong, W. Engineering a “PEG-g-PEI/DNA nanoparticle-in- PLGA microsphere” hybrid controlled release system to enhance immunogenicity of DNA vaccine. Mater. Sci. Eng. C 2020, 106, 110294.
[131]
Lee, K.; Kim, M.; Seo, Y.; Lee, H. Development of mRNA vaccines and their prophylactic and therapeutic applications. Nano Res. 2018, 11, 5173-5192.
[132]
Li, J. C.; Zhen, X.; Lyu, Y.; Jiang, Y. Y.; Huang, J. G.; Pu, K. Y. Cell membrane coated semiconducting polymer nanoparticles for enhanced multimodal cancer phototheranostics. ACS Nano 2018, 12, 8520-8530.
[133]
Guo, Y. Y.; Wang, D.; Song, Q. L.; Wu, T. T.; Zhuang, X. T.; Bao, Y. L.; Kong, M.; Qi, Y.; Tan, S. W.; Zhang, Z. P. Erythrocyte membrane-enveloped polymeric nanoparticles as nanovaccine for induction of antitumor immunity against melanoma. ACS Nano 2015, 9, 6918-6933.
[134]
Zhou, J. R.; Kroll, A. V.; Holay, M.; Fang, R. H.; Zhang, L. F. Biomimetic nanotechnology toward personalized vaccines. Adv. Mater. 2020, 32, 1901255.
[135]
Hu, Q. Y.; Sun, W. J.; Qian, C. E.; Wang, C.; Bomba, H. N.; Gu, Z. Anticancer platelet-mimicking nanovehicles. Adv. Mater. 2015, 27, 7043-7050.
[136]
Liu, R.; An, Y.; Jia, W. F.; Wang, Y. S.; Wu, Y.; Zhen, Y. H.; Cao, J.; Gao, H. L. Macrophage-mimic shape changeable nanomedicine retained in tumor for multimodal therapy of breast cancer. J. Control. Release 2020, 321, 589-601.
[137]
Gao, C. Y.; Lin, Z. H.; Wu, Z. G.; Lin, X. K.; He, Q. Stem-cell- membrane camouflaging on near-infrared photoactivated upconversion nanoarchitectures for in vivo remote-controlled photodynamic therapy. ACS Appl. Mater. Interfaces 2016, 8, 34252-34260.
[138]
Zou, S. J.; Wang, B. L.; Wang, C.; Wang, Q. Q.; Zhang, L. M. Cell membrane-coated nanoparticles: Research advances. Nanomedicine 2020, 15, 625-641.
[139]
Chen, M. S.; Ouyang, H. C.; Zhou, S. Y.; Li, J. Y.; Ye, Y. B. PLGA-nanoparticle mediated delivery of anti-OX40 monoclonal antibody enhances anti-tumor cytotoxic t cell responses. Cell. Immunol. 2014, 287, 91-99.
[140]
Chen, Q.; Wang, C.; Zhang, X. D.; Chen, G. J.; Hu, Q. Y.; Li, H. J.; Wang, J. Q.; Wen, D.; Zhang, Y. Q.; Lu, Y. F. et al. In situ sprayed bioresponsive immunotherapeutic gel for post-surgical cancer treatment. Nat. Nanotechnol. 2019, 14, 89-97.
[141]
Ma, L. L.; Zhu, M.; Gai, J. W.; Li, G. H.; Chang, Q.; Qiao, P.; Cao, L. L.; Chen, W. Q.; Zhang, S. Y.; Wan, Y. K. Preclinical development of a novel CD47 nanobody with less toxicity and enhanced anti-cancer therapeutic potential. J. Nanobiotechnol. 2020, 18, 12.
[142]
De Bruijn, H. S.; Mashayekhi, V.; Schreurs, T. J. L.; Van Driel, P. B. A. A.; Strijkers, G. J.; Van Diest, P. J.; Lowik, C. W. G. M.; Seynhaeve, A. L. B.; Ten Hagen, T. L. M.; Prompers, J. J. et al. Acute cellular and vascular responses to photodynamic therapy using egfr-targeted nanobody-photosensitizer conjugates studied with intravital optical imaging and magnetic resonance imaging. Theranostics 2020, 10, 2436-2452.
[143]
Hassani, M.; Hajari Taheri, F.; Sharifzadeh, Z.; Arashkia, A.; Hadjati, J.; Van Weerden, W. M.; Abdoli, S.; Modarressi, M. H.; Abolhassani, M. Engineered jurkat cells for targeting prostate-specific membrane antigen on prostate cancer cells by nanobody-based chimeric antigen receptor. Iran. Biomed. J. 2020, 24, 81-88.
[144]
Huang, Y. H.; Zhu, C.; Kondo, Y.; Anderson, A. C.; Gandhi, A.; Russell, A.; Dougan, S. K.; Petersen, B. S.; Melum, E.; Pertel, T. et al. CEACAM1 regulates TIM-3-mediated tolerance and exhaustion. Nature 2015, 517, 386-390.
[145]
ElTanbouly, M. A.; Zhao, Y. D.; Nowak, E.; Li, J. N.; Schaafsma, E.; Le Mercier, I.; Ceeraz, S.; Lines, J. L.; Peng, C. W.; Carriere, C. et al. VISTA is a checkpoint regulator for naive T cell quiescence and peripheral tolerance. Science 2020, 367, eaay0524.
[146]
Jafari, S.; Molavi, O.; Kahroba, H.; Hejazi, M. S.; Maleki-Dizaji, N.; Barghi, S.; Kiaie, S. H.; Jadidi-Niaragh, F. Clinical application of immune checkpoints in targeted immunotherapy of prostate cancer. Cell. Mol. Life Sci., in press, .
[147]
Greenwald, R. J.; Freeman, G. J.; Sharpe, A. H. The B7 family revisited. Annu. Rev. Immunol. 2005, 23, 515-548.
[148]
Wei, S. C.; Levine, J. H.; Cogdill, A. P.; Zhao, Y.; Anang, N. A. S.; Andrews, M. C.; Sharma, P.; Wang, J.; Wargo, J. A.; Pe'er, D. et al. Distinct cellular mechanisms underlie anti-CTLA-4 and anti-PD-1 checkpoint blockade. Cell 2017, 170, 1120-1133.e17.
[149]
Ordikhani, F.; Uehara, M.; Kasinath, V.; Dai, L.; Eskandari, S. K.; Bahmani, B.; Yonar, M.; Azzi, J. R.; Haik, Y.; Sage, P. T. et al. Targeting antigen-presenting cells by anti-PD-1 nanoparticles augments antitumor immunity. JCI Insight 2018, 3, 122700.
[150]
Hu, Q. Y.; Sun, W. J.; Wang, J. Q.; Ruan, H. T.; Zhang, X. D.; Ye, Y. Q.; Shen, S.; Wang, C.; Lu, W. Y.; Cheng, K. et al. Conjugation of haematopoietic stem cells and platelets decorated with anti-pd-1 antibodies augments anti-leukaemia efficacy. Nat. Biomed. Eng. 2018, 2, 831-840.
[151]
Zhu, Y. Y.; An, X.; Zhang, X.; Qiao, Y.; Zheng, T. S.; Li, X. B. STING: A master regulator in the cancer-immunity cycle. Mol. Cancer 2019, 18, 152.
[152]
Luo, M.; Wang, H.; Wang, Z. H.; Cai, H. C.; Lu, Z. G.; Li, Y.; Du, M. J.; Huang, G.; Wang, C. S.; Chen, X. et al. A STING-activating nanovaccine for cancer immunotherapy. Nat. Nanotechnol. 2017, 12, 648-654.
[153]
Ruan, H. T.; Hu, Q. Y.; Wen, D.; Chen, Q.; Chen, G. J.; Lu, Y. F.; Wang, J. Q.; Cheng, H.; Lu, W. Y.; Gu, Z. A dual-bioresponsive drug-delivery depot for combination of epigenetic modulation and immune checkpoint blockade. Adv. Mater. 2019, 31, 1806957.
[154]
Chen, Q.; Wang, C.; Chen, G. J.; Hu, Q. Y.; Gu, Z. Delivery strategies for immune checkpoint blockade. Adv. Healthc. Mater. 2018, 7, 1800424.
[155]
Schmid, P.; Adams, S.; Rugo, H. S.; Schneeweiss, A.; Barrios, C. H.; Iwata, H.; Diéras, V.; Hegg, R.; Im, S. A.; Shaw Wright, G. et al. Atezolizumab and Nab-paclitaxel in advanced triple-negative breast cancer. N. Engl. J. Med. 2018, 379, 2108-2121.
[156]
Larkin, J.; Chiarion-Sileni, V.; Gonzalez, R.; Grob, J. J.; Cowey, C. L.; Lao, C. D.; Schadendorf, D.; Dummer, R.; Smylie, M.; Rutkowski, P. et al. Combined nivolumab and ipilimumab or monotherapy in untreated melanoma. N. Engl. J. Med. 2015, 373, 23-34.
[157]
Wang, C.; Ye, Y. Q.; Hochu, G. M.; Sadeghifar, H.; Gu, Z. Enhanced cancer immunotherapy by microneedle patch-assisted delivery of anti-PD1 antibody. Nano Lett. 2016, 16, 2334-2340.
[158]
Kuai, R.; Ochyl, L. J.; Bahjat, K. S.; Schwendeman, A.; Moon, J. J. Designer vaccine nanodiscs for personalized cancer immunotherapy. Nat. Mater. 2017, 16, 489-496.
[159]
June, C. H.; Sadelain, M. Chimeric antigen receptor therapy. N. Engl. J. Med. 2018, 379, 64-73.
[160]
Brown, C. E.; Mackall, C. L. CAR T cell therapy: Inroads to response and resistance. Nat. Rev. Immunol. 2019, 19, 73-74.
[161]
Tang, J.; Hubbard-Lucey, V. M.; Pearce, L.; O'Donnell-Tormey, J.; Shalabi, A. The global landscape of cancer cell therapy. Nat. Rev. Drug Discov. 2018, 17, 465-466.
[162]
June, C. H.; O'Connor, R. S.; Kawalekar, O. U.; Ghassemi, S.; Milone, M. C. CAR T cell immunotherapy for human cancer. Science 2018, 359, 1361-1365.
[163]
Hinrichs, C. S.; Rosenberg, S. A. Exploiting the curative potential of adoptive T-cell therapy for cancer. Immunol. Rev. 2014, 257, 56-71.
[164]
Zhao, L. J.; Cao, Y. J. Engineered T cell therapy for cancer in the clinic. Front. Immunol. 2019, 10, 2250.
[165]
Cheung, A. S.; Zhang, D. K. Y.; Koshy, S. T.; Mooney, D. J. Scaffolds that mimic antigen-presenting cells enable ex vivo expansion of primary T cells. Nat. Biotechnol. 2018, 36, 160-169.
[166]
Rhodes, K. R.; Green, J. J. Nanoscale artificial antigen presenting cells for cancer immunotherapy. Mol. Immunol. 2018, 98, 13-18.
[167]
Meyer, R. A.; Sunshine, J. C.; Perica, K.; Kosmides, A. K.; Aje, K.; Schneck, J. P.; Green, J. J. Biodegradable nanoellipsoidal artificial antigen presenting cells for antigen specific T-cell activation. Small 2015, 11, 1519-1525.
[168]
Olden, B. R.; Perez, C. R.; Wilson, A. L.; Cardle, I. I.; Lin, Y. S.; Kaehr, B.; Gustafson, J. A.; Jensen, M. C.; Pun, S. H. Cell-templated silica microparticles with supported lipid bilayers as artificial antigen-presenting cells for T cell activation. Adv. Healthc. Mater. 2019, 8, 1801188.
[169]
Stephan, M. T.; Moon, J. J.; Um, S. H.; Bershteyn, A.; Irvine, D. J. Therapeutic cell engineering with surface-conjugated synthetic nanoparticles. Nat. Med. 2010, 16, 1035-1041.
[170]
Stephan, M. T.; Stephan, S. B.; Bak, P.; Chen, J. Z.; Irvine, D. J. Synapse-directed delivery of immunomodulators using T-cell- conjugated nanoparticles. Biomaterials 2012, 33, 5776-5787.
[171]
Huang, B.; Abraham, W. D.; Zheng, Y. R.; Bustamante López, S. C.; Luo, S. S.; Irvine, D. J. Active targeting of chemotherapy to disseminated tumors using nanoparticle-carrying T cells. Sci. Transl. Med. 2015, 7, 291ra94.
[172]
Ma, L. Y.; Dichwalkar, T.; Chang, J. Y. H.; Cossette, B.; Garafola, D.; Zhang, A. Q.; Fichter, M.; Wang, C. S.; Liang, S.; Silva, M. et al. Enhanced CAR-T cell activity against solid tumors by vaccine boosting through the chimeric receptor. Science 2019, 365, 162-168.
[173]
Chen, Q.; Hu, Q. Y.; Dukhovlinova, E.; Chen, G. J.; Ahn, S.; Wang, C.; Ogunnaike, E. A.; Ligler, F. S.; Dotti, G.; Gu, Z. Photothermal therapy promotes tumor infiltration and antitumor activity of CAR T cells. Adv. Mater. 2019, 31, 1900192.
[174]
Beatty, G. L.; O'Hara, M. H.; Lacey, S. F.; Torigian, D. A.; Nazimuddin, F.; Chen, F.; Kulikovskaya, I. M.; Soulen, M. C.; McGarvey, M.; Nelson, A. M. et al. Activity of mesothelin- specific chimeric antigen receptor t cells against pancreatic carcinoma metastases in a phase 1 trial. Gastroenterology 2018, 155, 29-32.
[175]
Lim, W. A.; June, C. H. The principles of engineering immune cells to treat cancer. Cell 2017, 168, 724-740.
[176]
Millar, D. G.; Ramjiawan, R. R.; Kawaguchi, K.; Gupta, N.; Chen, J.; Zhang, S. F.; Nojiri, T.; Ho, W. W.; Aoki, S.; Jung, K. et al. Antibody-mediated delivery of viral epitopes to tumors harnesses CMV-specific T cells for cancer therapy. Nat. Biotechnol. 2020, 38, 420-425.
[177]
Thakkar, S.; Sharma, D.; Kalia, K.; Tekade, R. K. Tumor microenvironment targeted nanotherapeutics for cancer therapy and diagnosis: A review. Acta Biomater. 2020, 101, 43-68.
[178]
Chen, Q.; Liu, G. X.; Liu, S.; Su, H. Y.; Wang, Y.; Li, J. Y.; Luo, C. Remodeling the tumor microenvironment with emerging nanotherapeutics. Trends Pharmacol. Sci. 2018, 39, 59-74.
[179]
Sahai, E.; Astsaturov, I.; Cukierman, E.; DeNardo, D. G.; Egeblad, M.; Evans, R. M.; Fearon, D.; Greten, F. R.; Hingorani, S. R.; Hunter, T. et al. A framework for advancing our understanding of cancer-associated fibroblasts. Nat. Rev. Cancer 2020, 20, 174-186.
[180]
Fukumura, D.; Xavier, R.; Sugiura, T.; Chen, Y.; Park, E. C.; Lu, N. F.; Selig, M.; Nielsen, G.; Taksir, T.; Jain, R. K. et al. Tumor induction of VEGF promoter activity in stromal cells. Cell 1998, 94, 715-725.
[181]
Bhome, R.; Goh, R. W.; Bullock, M. D.; Pillar, N.; Thirdborough, S. M.; Mellone, M.; Mirnezami, R.; Galea, D.; Veselkov, K.; Gu, Q. et al. Exosomal microRNAs derived from colorectal cancer- associated fibroblasts: Role in driving cancer progression. Aging 2017, 9, 2666-2694.
[182]
Kojima, Y.; Acar, A.; Eaton, E. N.; Mellody, K. T.; Scheel, C.; Ben-Porath, I.; Onder, T. T.; Wang, Z. C.; Richardson, A. L.; Weinberg, R. A. et al. Autocrine TGF-β and stromal cell-derived factor-1 (SDF-1) signaling drives the evolution of tumor-promoting mammary stromal myofibroblasts. Proc. Natl. Acad. Sci. USA 2010, 107, 20009-20014.
[183]
Hou, L.; Liu, Q.; Shen, L. M.; Liu, Y.; Zhang, X. Q.; Chen, F. Q.; Huang, L. Nano-delivery of fraxinellone remodels tumor microenvironment and facilitates therapeutic vaccination in desmoplastic melanoma. Theranostics 2018, 8, 3781-3796.
[184]
Hu, C. H.; Liu, X. Y.; Ran, W.; Meng, J.; Zhai, Y. H.; Zhang, P. C.; Yin, Q.; Yu, H. J.; Zhang, Z. W.; Li, Y. P. Regulating cancer associated fibroblasts with losartan-loaded injectable peptide hydrogel to potentiate chemotherapy in inhibiting growth and lung metastasis of triple negative breast cancer. Biomaterials 2017, 144, 60-72.
[185]
Zhang, B.; Jin, K.; Jiang, T.; Wang, L. T.; Shen, S.; Luo, Z. M.; Tuo, Y. Y.; Liu, X. P.; Hu, Y.; Pang, Z. Q. Celecoxib normalizes the tumor microenvironment and enhances small nanotherapeutics delivery to A549 tumors in nude mice. Sci. Rep. 2017, 7, 10071.
[186]
Li, W.; Zhao, X. X.; Du, B.; Li, X.; Liu, S. H.; Yang, X. Y.; Ding, H.; Yang, W. D.; Pan, F.; Wu, X. B. et al. Gold nanoparticle-mediated targeted delivery of recombinant human endostatin normalizes tumour vasculature and improves cancer therapy. Sci. Rep. 2016, 6, 30619.
[187]
Lewis, C. E.; Pollard, J. W. Distinct role of macrophages in different tumor microenvironments. Cancer Res. 2006, 66, 605-612.
[188]
Ngambenjawong, C.; Gustafson, H. H.; Pun, S. H. Progress in tumor-associated macrophage (TAM)-targeted therapeutics. Adv. Drug Deliv. Rev. 2017, 114, 206-221.
[189]
Okabe, Y.; Medzhitov, R. Tissue-specific signals control reversible program of localization and functional polarization of macrophages. Cell 2014, 157, 832-844.
[190]
Gordon, S.; Martinez, F. O. Alternative activation of macrophages: Mechanism and functions. Immunity 2010, 32, 593-604.
[191]
Rodell, C. B.; Arlauckas, S. P.; Cuccarese, M. F.; Garris, C. S.; Li, R.; Ahmed, M. S.; Kohler, R. H.; Pittet, M. J.; Weissleder, R. TLR7/8-agonist-loaded nanoparticles promote the polarization of tumour-associated macrophages to enhance cancer immunotherapy. Nat. Biomed. Eng. 2018, 2, 578-588.
[192]
Chen, L.; Zhou, L. L.; Wang, C. H.; Han, Y.; Lu, Y. L.; Liu, J.; Hu, X. C.; Yao, T. M.; Lin, Y.; Liang, S. J. et al. Tumor-targeted drug and CpG delivery system for phototherapy and docetaxel-enhanced immunotherapy with polarization toward M1-type macrophages on triple negative breast cancers. Adv. Mater. 2019, 31, 1904997.
[193]
Tsai, S. J.; Andorko, J. I.; Zeng, X. B.; Gammon, J. M.; Jewell, C. M. Polyplex interaction strength as a driver of potency during cancer immunotherapy. Nano Res. 2018, 11, 5642-5656.
[194]
Kim, S. Y.; Kim, S.; Kim, J. E.; Lee, S. N.; Shin, I. W.; Shin, H. S.; Jin, S. M.; Noh, Y. W.; Kang, Y. J.; Kim, Y. S. et al. Lyophilizable and multifaceted toll-like receptor 7/8 agonist-loaded nanoemulsion for the reprogramming of tumor microenvironments and enhanced cancer immunotherapy. ACS Nano 2019, 13, 12671-12686.
[195]
Cheng, N.; Watkins-Schulz, R.; Junkins, R. D.; David, C. N.; Johnson, B. M.; Montgomery, S. A.; Peine, K. J.; Darr, D. B.; Yuan, H.; McKinnon, K. P. et al. A nanoparticle-incorporated STING activator enhances antitumor immunity in PD-L1-insensitive models of triple-negative breast cancer. JCI Insight 2018, 3, e120638.
[196]
Conde, J.; Bao, C. C.; Tan, Y. Q.; Cui, D. X.; Edelman, E. R.; Azevedo, H. S.; Byrne, H. J.; Artzi, N.; Tian, F. R. Dual targeted immunotherapy via in vivo delivery of biohybrid RNAi-peptide nanoparticles to tumor-associated macrophages and cancer cells. Adv. Funct. Mater. 2015, 25, 4183-4194.
[197]
Ma, S.; Song, W. T.; Xu, Y. D.; Si, X. H.; Zhang, D. W.; Lv, S. X.; Yang, C. G.; Ma, L. L.; Tang, Z. H.; Chen, X. S. Neutralizing tumor-promoting inflammation with polypeptide-dexamethasone conjugate for microenvironment modulation and colorectal cancer therapy. Biomaterials 2020, 232, 119676.
[198]
Colegio, O. R.; Chu, N. Q.; Szabo, A. L.; Chu, T.; Rhebergen, A. M.; Jairam, V.; Cyrus, N.; Brokowski, C. E.; Eisenbarth, S. C.; Phillips, G. M. et al. Functional polarization of tumour-associated macrophages by tumour-derived lactic acid. Nature 2014, 513, 559-563.
[199]
Saeed, M.; Gao, J.; Shi, Y.; Lammers, T.; Yu, H. J. Engineering nanoparticles to reprogram the tumor immune microenvironment for improved cancer immunotherapy. Theranostics 2019, 9, 7981-8000.
[200]
Takikawa, O. Biochemical and medical aspects of the indoleamine 2,3-dioxygenase-initiated L-tryptophan metabolism. Biochem. Biophys. Res. Commun. 2005, 338, 12-19.
[201]
Guzik, K.; Tomala, M.; Muszak, D.; Konieczny, M.; Hec, A.; Blaszkiewicz, U.; Pustula, M.; Butera, R.; Dömling, A.; Holak, T. A. Development of the inhibitors that target the PD-1/PD-L1 interaction—a brief look at progress on small molecules, peptides and macrocycles. Molecules 2019, 24, 2071.
[202]
Shi, D. F.; An, X. L.; Bai, Q. F.; Bing, Z. T.; Zhou, S. Y.; Liu, H. X.; Yao, X. J. Computational insight into the small molecule intervening PD-L1 dimerization and the potential structure-activity relationship. Front. Chem. 2019, 7, 764.
[203]
Skalniak, L.; Zak, K. M.; Guzik, K.; Magiera, K.; Musielak, B.; Pachota, M.; Szelazek, B.; Kocik, J.; Grudnik, P.; Tomala, M. et al. Small-molecule inhibitors of PD-1/PD-L1 immune checkpoint alleviate the PD-L1-induced exhaustion of T-cells. Oncotarget 2017, 8, 72167-72181.
[204]
Sasikumar, P. G.; Ramachandra, R. K.; Adurthi, S.; Dhudashiya, A. A.; Vadlamani, S.; Vemula, K.; Vunnum, S.; Satyam, L. K.; Samiulla, D. S.; Subbarao, K. et al. A rationally designed peptide antagonist of the PD-1 signaling pathway as an immunomodulatory agent for cancer therapy. Mol. Cancer Ther. 2019, 18, 1081-1091.
[205]
Musielak, B.; Kocik, J.; Skalniak, L.; Magiera-Mularz, K.; Sala, D.; Czub, M.; Stec, M.; Siedlar, M.; Holak, T. A.; Plewka, J. CA-170-a potent small-molecule PD-L1 inhibitor or not? Molecules 2019, 24, 2804.
[206]
Li, C. L.; Zhang, N. P.; Zhou, J. D.; Ding, C.; Jin, Y. Q.; Cui, X. Y.; Pu, K. F.; Zhu, Y. M. Peptide blocking of PD-1/PD-L1 interaction for cancer immunotherapy. Cancer Immunol. Res. 2018, 6, 178-188.
[207]
Qian, Y.; Qiao, S.; Dai, Y. F.; Xu, G. Q.; Dai, B. L.; Lu, L. S.; Yu, X.; Luo, Q. M.; Zhang, Z. H. Molecular-targeted immunotherapeutic strategy for melanoma via dual-targeting nanoparticles delivering small interfering RNA to tumor-associated macrophages. ACS Nano 2017, 11, 9536-9549.
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Publication history
Copyright
Acknowledgements

Publication history

Received: 27 April 2020
Revised: 24 May 2020
Accepted: 27 May 2020
Published: 26 June 2020
Issue date: October 2020

Copyright

© Tsinghua University Press and Springer-Verlag GmbH Germany, part of Springer Nature 2020

Acknowledgements

This work was supported by the National Natural Science Foundation of China (Nos. 81860547, 81573008, 21671150, 21877084, 81171646, 31170776, and 21472139), the Science and Technology Commission of Shanghai Municipality (Nos. 14DZ2261100 and 15DZ1940106), the Fundamental Research Funds for the Central Universities (No. kx0150720173382) and the Joint Project of Health and Family Planning Committee of Pudong New Area (No. PW2017D-10).

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