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Review | Open Access

Bacterial outer membrane vesicle-based cancer nanovaccines

Xiaoyu Gao1,2Qingqing Feng1Jing Wang3 ( )Xiao Zhao1,2,4 ( )
CAS Key Laboratory for Biomedical Effects of Nanomaterials and Nanosafety & CAS Center for Excellence in Nanoscience, National Center for Nanoscience and Technology of China, Beijing 100190, China
University of Chinese Academy of Sciences, Beijing 100049, China
Center of Drug Evaluation, National Medical Products Administration, Beijing 100022, China
IGDB-NCNST Joint Research Center, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China
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Abstract

Tumor vaccines, a type of personalized tumor immunotherapy, have developed rapidly in recent decades. These vaccines evoke tumor antigen-specific T cells to achieve immune recognition and killing of tumor cells. Because the immunogenicity of tumor antigens alone is insufficient, immune adjuvants and nanocarriers are often required to enhance anti-tumor immune responses. At present, vaccine carrier development often integrates nanocarriers and immune adjuvants. Among them, outer membrane vesicles (OMVs) are receiving increasing attention as a delivery platform for tumor vaccines. OMVs are natural nanovesicles derived from Gram-negative bacteria, which have adjuvant function because they contain pathogen associated molecular patterns. Importantly, OMVs can be functionally modified by genetic engineering of bacteria, thus laying a foundation for applications as a delivery platform for tumor nanovaccines. This review summarizes 5 aspects of recent progress in, and future development of, OMV-based tumor nanovaccines: strain selection, heterogeneity, tumor antigen loading, immunogenicity and safety, and mass production of OMVs.

References

1

Siegel RL, Miller KD, Fuchs HE, Jemal A. Cancer statistics, 2022. CA Cancer J Clin. 2022; 72: 7-33.

2

Sanmamed MF, Chen L. A paradigm shift in cancer immunotherapy: from enhancement to normalization. Cell. 2018; 175: 313-26.

3

Mun EJ, Babiker HM, Weinberg U, Kirson ED, Von Hoff DD. Tumor-treating fields: a fourth modality in cancer treatment. Clin Cancer Res. 2018; 24: 266-75.

4

Weber J, Mandala M, Del Vecchio M, Gogas HJ, Arance AM, Cowey CL, et al. Adjuvant nivolumab versus ipilimumab in resected stage Ⅲ or Ⅳ melanoma. N Engl J Med. 2017; 377: 1824-35.

5

Hellmann MD, Paz-Ares L, Bernabe Caro R, Zurawski B, Kim SW, Carcereny Costa E, et al. Nivolumab plus ipilimumab in advanced non-small-cell lung cancer. N Engl J Med. 2019; 381: 2020-31.

6

Rini BI, Plimack ER, Stus V, Gafanov R, Hawkins R, Nosov D, et al. Pembrolizumab plus axitinib versus sunitinib for advanced renal-cell carcinoma. N Engl J Med. 2019; 380: 1116-27.

7

Kennedy LB, Salama AKS. A review of cancer immunotherapy toxicity. CA Cancer J Clin. 2020; 70: 86-104.

8

Sahin U, Türeci Ö. Personalized vaccines for cancer immunotherapy. Science. 2018; 359: 1355-60.

9

Gerritzen MJH, Martens DE, Wijffels RH, van der Pol L, Stork M. Bioengineering bacterial outer membrane vesicles as vaccine platform. Biotechnol Adv. 2017; 35: 565-74.

10

Kushnir N, Streatfield SJ, Yusibov V. Virus-like particles as a highly efficient vaccine platform: diversity of targets and production systems and advances in clinical development. Vaccine. 2012; 31: 58-83.

11

Sanders H, Feavers IM. Adjuvant properties of meningococcal outer membrane vesicles and the use of adjuvants in Neisseria meningitidis protein vaccines. Expert Rev Vaccines. 2011; 10: 323-34.

12

Schumacher TN, Schreiber RD. Neoantigens in cancer immunotherapy. Science. 2015; 348: 69-74.

13

Yamamoto TN, Kishton RJ, Restifo NP. Developing neoantigen-targeted T cell-based treatments for solid tumors. Nat Med. 2019; 25: 1488-99.

14

Haen SP, Löffler MW, Rammensee HG, Brossart P. Towards new horizons: characterization, classification and implications of the tumour antigenic repertoire. Nat Rev Clin Oncol. 2020; 17: 595-610.

15

Morse MA, Chui S, Hobeika A, Lyerly HK, Clay T. Recent developments in therapeutic cancer vaccines. Nat Clin Pract Oncol. 2005; 2: 108-13.

16

Liu G, Zhu M, Zhao X, Nie G. Nanotechnology-empowered vaccine delivery for enhancing CD8+ T cells-mediated cellular immunity. Adv Drug Deliv Rev. 2021; 176: 113889.

17

Hu Z, Ott PA, Wu CJ. Towards personalized, tumour-specific, therapeutic vaccines for cancer. Nat Rev Immunol. 2018; 18: 168-82.

18

Handy CE, Antonarakis ES. Sipuleucel-T for the treatment of prostate cancer: novel insights and future directions. Future Oncol. 2018; 14: 907-17.

19

Couzin-Frankel J. Breakthrough of the year 2013. Cancer immunotherapy. Science. 2013; 342: 1432-3.

20

Ott PA, Hu Z, Keskin DB, Shukla SA, Sun J, Bozym DJ, et al. An immunogenic personal neoantigen vaccine for patients with melanoma. Nature. 2017; 547: 217-21.

21

Sahin U, Derhovanessian E, Miller M, Kloke BP, Simon P, Löwer M, et al. Personalized RNA mutanome vaccines mobilize poly-specific therapeutic immunity against cancer. Nature. 2017; 547: 222-6.

22

Luo M, Samandi LZ, Wang Z, Chen ZJ, Gao J. Synthetic nanovaccines for immunotherapy. J Control Release. 2017; 263: 200-10.

23

Bowen WS, Svrivastava AK, Batra L, Barsoumian H, Shirwan H. Current challenges for cancer vaccine adjuvant development. Expert Rev Vaccines. 2018; 17: 207-15.

24

Wang S, Cheng K, Chen K, Xu C, Ma P, Dang G, et al. Nanoparticle-based medicines in clinical cancer therapy. Nano Today. 2022; 45: 101512.

25

Kranz LM, Diken M, Haas H, Kreiter S, Loquai C, Reuter KC, et al. Systemic RNA delivery to dendritic cells exploits antiviral defence for cancer immunotherapy. Nature. 2016; 534: 396-401.

26

Van der Jeught K, De Koker S, Bialkowski L, Heirman C, Tjok Joe P, Perche F, et al. Dendritic cell targeting mRNA lipopolyplexes combine strong antitumor T-cell immunity with improved inflammatory safety. ACS Nano. 2018; 12: 9815-29.

27

Huang C, Jin H, Qian Y, Qi S, Luo H, Luo Q, et al. Hybrid melittin cytolytic Peptide-driven ultrasmall lipid nanoparticles block melanoma growth in vivo. ACS Nano. 2013; 7: 5791-800.

28

Li S, Jiang Q, Liu S, Zhang Y, Tian Y, Song C, et al. A DNA nanorobot functions as a cancer therapeutic in response to a molecular trigger in vivo. Nat Biotechnol. 2018; 36: 258-64.

29

Luo M, Wang H, Wang Z, Cai H, Lu Z, Li Y, et al. A STING-activating nanovaccine for cancer immunotherapy. Nat Nanotechnol. 2017; 12: 648-54.

30

Miao L, Li L, Huang Y, Delcassian D, Chahal J, Han J, et al. Delivery of mRNA vaccines with heterocyclic lipids increases anti-tumor efficacy by STING-mediated immune cell activation. Nat Biotechnol. 2019; 37: 1174-85.

31

Zhai Y, Su J, Ran W, Zhang P, Yin Q, Zhang Z, et al. Preparation and application of cell membrane-camouflaged nanoparticles for cancer therapy. Theranostics. 2017; 7: 2575-92.

32

Toyofuku M, Nomura N, Eberl L. Types and origins of bacterial membrane vesicles. Nat Rev Microbiol. 2019; 17: 13-24.

33

Zhao X, Zhao R, Nie G. Nanocarriers based on bacterial membrane materials for cancer vaccine delivery. Nat Protoc. 2022 (in press). https://doi.org/10.1038/s41596-022-00713-7.

34

Chatterjee SN, Das J. Electron microscopic observations on the excretion of cell-wall material by Vibrio cholerae. J Gen Microbiol. 1967; 49: 1-11.

35

Schwechheimer C, Kuehn MJ. Outer-membrane vesicles from Gram-negative bacteria: biogenesis and functions. Nat Rev Microbiol. 2015; 13: 605-19.

36

Xie J, Li Q, Haesebrouck F, van Hoecke L, Vandenbroucke RE. The tremendous biomedical potential of bacterial extracellular vesicles. Trends Biotechnol. 2022. https://doi.org/10.1016/j.tibtech.2022.03.005.

37

Toyofuku M, Cárcamo-Oyarce G, Yamamoto T, Eisenstein F, Hsiao CC, Kurosawa M, et al. Prophage-triggered membrane vesicle formation through peptidoglycan damage in Bacillus subtilis. Nat Commun. 2017; 8: 481.

38

Schwechheimer C, Kulp A, Kuehn MJ. Modulation of bacterial outer membrane vesicle production by envelope structure and content. BMC Microbiol. 2014; 14: 324.

39

Chowdhury C, Jagannadham MV. Virulence factors are released in association with outer membrane vesicles of Pseudomonas syringae pv. tomato T1 during normal growth. Biochim Biophys Acta. 2013; 1834: 231-9.

40

Tashiro Y, Ichikawa S, Nakajima-Kambe T, Uchiyama H, Nomura N. Pseudomonas quinolone signal affects membrane vesicle production in not only gram-negative but also gram-positive bacteria. Microbes Environ. 2010; 25: 120-5.

41

Zingl FG, Kohl P, Cakar F, Leitner DR, Mitterer F, Bonnington KE, et al. Outer membrane vesiculation facilitates surface exchange and in vivo adaptation of Vibrio cholerae. Cell Host Microbe. 2020; 27: 225-37.e8.

42

Kadurugamuwa JL, Beveridge TJ. Virulence factors are released from Pseudomonas aeruginosa in association with membrane vesicles during normal growth and exposure to gentamicin: a novel mechanism of enzyme secretion. J Bacteriol. 1995; 177: 3998-4008.

43

Rumbo C, Fernández-Moreira E, Merino M, Poza M, Mendez JA, Soares NC, et al. Horizontal transfer of the OXA-24 carbapenemase gene via outer membrane vesicles: a new mechanism of dissemination of carbapenem resistance genes in Acinetobacter baumannii. Antimicrob Agents Chemother. 2011; 55: 3084-90.

44

Kaparakis-Liaskos M, Ferrero RL. Immune modulation by bacterial outer membrane vesicles. Nat Rev Immunol. 2015; 15: 375-87.

45

Poltorak A, He X, Smirnova I, Liu MY, Van Huffel C, Du X, et al. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science. 1998; 282: 2085-8.

46

Zariri A, Beskers J, van de Waterbeemd B, Hamstra HJ, Bindels TH, van Riet E, et al. Meningococcal outer membrane vesicle composition-dependent activation of the innate immune response. Infect Immun. 2016; 84: 3024-33.

47

Cheng K, Kang Q, Zhao X. Biogenic nanoparticles as immunomodulator for tumor treatment. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2020; 12: e1646.

48

Kuerban K, Gao X, Zhang H, Liu J, Dong M, Wu L, et al. Doxorubicin-loaded bacterial outer-membrane vesicles exert enhanced anti-tumor efficacy in non-small-cell lung cancer. Acta Pharm Sin B. 2020; 10: 1534-48.

49

Zhang J, Li Z, Liu L, Li L, Zhang L, Wang Y, et al. Self-assembly catalase nanocomplex conveyed by bacterial vesicles for oxygenated photodynamic therapy and tumor immunotherapy. Int J Nanomedicine. 2022; 17: 1971-85.

50

Zhuang Q, Xu J, Deng D, Chao T, Li J, Zhang R, et al. Bacteria-derived membrane vesicles to advance targeted photothermal tumor ablation. Biomaterials. 2021; 268: 120550.

51

Li Y, Zhang K, Wu Y, Yue Y, Cheng K, Feng Q, et al. Antigen capture and immune modulation by bacterial outer membrane vesicles as in situ vaccine for cancer immunotherapy post-photothermal therapy. Small. 2022; 18: e2107461.

52

Yue Y, Xu J, Li Y, Cheng K, Feng Q, Ma X, et al. Antigen-bearing outer membrane vesicles as tumour vaccines produced in situ by ingested genetically engineered bacteria. Nat Biomed Eng. 2022; 6: 898-909.

53
Sierra GV, Campa HC, Varcacel NM, Garcia IL, Izquierdo PL, Sotolongo PF, et al. Vaccine against group B neisseria meningitidis: protection trial and mass vaccination results in Cuba. NIPH Ann. 1991; 14: 195-207; discussion 208-10.
54

Arnold R, Galloway Y, McNicholas A, O’Hallahan J. Effectiveness of a vaccination programme for an epidemic of meningococcal B in New Zealand. Vaccine. 2011; 29: 7100-6.

55

O’Ryan M, Stoddard J, Toneatto D, Wassil J, Dull PM. A multi-component meningococcal serogroup B vaccine (4CMenB): the clinical development program. Drugs. 2014; 74: 15-30.

56

Hoekstra D, van der Laan JW, de Leij L, Witholt B. Release of outer membrane fragments from normally growing Escherichia coli. Biochim Biophys Acta. 1976; 455: 889-99.

57

Olofsson A, Vallström A, Petzold K, Tegtmeyer N, Schleucher J, Carlsson S, et al. Biochemical and functional characterization of Helicobacter pylori vesicles. Mol Microbiol. 2010; 77: 1539-55.

58

Lee EY, Bang JY, Park GW, Choi DS, Kang JS, Kim HJ, et al. Global proteomic profiling of native outer membrane vesicles derived from Escherichia coli. Proteomics. 2007; 7: 3143-53.

59

Vaughan TE, Skipp PJ, O’Connor CD, Hudson MJ, Vipond R, Elmore MJ, et al. Proteomic analysis of Neisseria lactamica and N eisseria meningitidis outer membrane vesicle vaccine antigens. Vaccine. 2006; 24: 5277-93.

60

Hong J, Dauros-Singorenko P, Whitcombe A, Payne L, Blenkiron C, Phillips A, et al. Analysis of the Escherichia coli extracellular vesicle proteome identifies markers of purity and culture conditions. J Extracell Vesicles. 2019; 8: 1632099.

61

Zavan L, Bitto NJ, Johnston EL, Greening DW, Kaparakis-Liaskos M. Helicobacter pylori growth stage determines the size, protein composition, and preferential cargo packaging of outer membrane vesicles. Proteomics. 2019; 19: e1800209.

62

Pan J, Li X, Shao B, Xu F, Huang X, Guo X, et al. Self-blockade of pd-l1 with bacteria-derived outer-membrane vesicle for enhanced cancer immunotherapy. Adv Mater. 2022; 34: e2106307.

63

Grandi A, Tomasi M, Zanella I, Ganfini L, Caproni E, Fantappiè L, et al. Synergistic protective activity of tumor-specific epitopes engineered in bacterial outer membrane vesicles. Front Oncol. 2017; 7: 253.

64

Liang J, Zhao X. Nanomaterial-based delivery vehicles for therapeutic cancer vaccine development. Cancer Biol Med. 2021; 18: 352-71.

65

Liang J, Cheng K, Li Y, Xu J, Chen Y, Ma N, et al. Personalized cancer vaccines from bacteria-derived outer membrane vesicles with antibody-mediated persistent uptake by dendritic cells. Fundam Res. 2022; 2: 23-36.

66

Cheng K, Zhao R, Li Y, Qi Y, Wang Y, Zhang Y, et al. Bioengineered bacteria-derived outer membrane vesicles as a versatile antigen display platform for tumor vaccination via Plug-and-Display technology. Nat Commun. 2021; 12: 2041.

67

Li Y, Ma X, Yue Y, Zhang K, Cheng K, Feng Q, et al. Rapid surface display of mRNA antigens by bacteria-derived outer membrane vesicles for a personalized tumor vaccine. Adv Mater. 2022; 34: e2109984.

68

van der Pol L, Stork M, van der Ley P. Outer membrane vesicles as platform vaccine technology. Biotechnol J. 2015; 10: 1689-706.

69

Li M, Zhou H, Yang C, Wu Y, Zhou X, Liu H, et al. Bacterial outer membrane vesicles as a platform for biomedical applications: An update. J Control Release. 2020; 323: 253-68.

70

Bos MP, Tefsen B, Geurtsen J, Tommassen J. Identification of an outer membrane protein required for the transport of lipopolysaccharide to the bacterial cell surface. Proc Natl Acad Sci U S A. 2004; 101: 9417-22.

71

Arenas J, van Dijken H, Kuipers B, Hamstra HJ, Tommassen J, van der Ley P. Coincorporation of LpxL1 and PagL mutant lipopolysaccharides into liposomes with Neisseria meningitidis opacity protein: influence on endotoxic and adjuvant activity. Clin Vaccine Immunol. 2010; 17: 487-95.

72

Qing S, Lyu C, Zhu L, Pan C, Wang S, Li F, et al. Biomineralized bacterial outer membrane vesicles potentiate safe and efficient tumor microenvironment reprogramming for anticancer therapy. Adv Mater. 2020; 32: e2002085.

73

Zheng B, Xu J, Chen G, Zhang S, Xiao Z, Lu W. Bacterium-mimicking vector with enhanced adjuvanticity for cancer immunotherapy and minimized toxicity. Adv Funct. 2019; 29: 1901437.

74

van de Waterbeemd B, Streefland M, van der Ley P, Zomer B, van Dijken H, Martens D, et al. Improved OMV vaccine against Neisseria meningitidis using genetically engineered strains and a detergent-free purification process. Vaccine. 2010; 28: 4810-6.

75

Grizot S, Buchanan SK. Structure of the OmpA-like domain of RmpM from Neisseria meningitidis. Mol Microbiol. 2004; 51: 1027-37.

76

Gerritzen MJH, Maas RHW, van den Ijssel J, van Keulen L, Martens DE, Wijffels RH, et al. High dissolved oxygen tension triggers outer membrane vesicle formation by Neisseria meningitidis. Microb Cell Fact. 2018; 17: 157.

77

van de Waterbeemd B, Zomer G, Kaaijk P, Ruiterkamp N, Wijffels RH, van den Dobbelsteen GP, et al. Improved production process for native outer membrane vesicle vaccine against Neisseria meningitidis. PLoS One. 2013; 8: e65157.

78

Gerritzen MJH, Stangowez L, van de Waterbeemd B, Martens DE, Wijffels RH, Stork M. Continuous production of Neisseria meningitidis outer membrane vesicles. Appl Microbiol Biotechnol. 2019; 103: 9401-10.

Cancer Biology & Medicine
Pages 1290-1300
Cite this article:
Gao X, Feng Q, Wang J, et al. Bacterial outer membrane vesicle-based cancer nanovaccines. Cancer Biology & Medicine, 2022, 19(9): 1290-1300. https://doi.org/10.20892/j.issn.2095-3941.2022.0452

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Received: 28 July 2022
Accepted: 24 August 2022
Published: 22 September 2022
©2022 Cancer Biology & Medicine.

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