1932

Abstract

The successful development of prophylactic cancer vaccines targeting oncogenic viruses has demonstrated the potential for vaccination to reduce the global burden of cancer. However, most human cancers are not caused by viruses, and therefore novel approaches are needed for the successful development of prophylactic cancer vaccines for nonviral cancers. In this review, we detail evidence that the human immune system can recognize and eliminate non-virus-caused cancers before they become clinically apparent. We also discuss the design of an ideal prophylactic vaccine with the goal of providing a lasting adaptive immune response against antigen targets that arise early in a cancer's development.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-cancerbio-030617-050558
2018-03-04
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/cancerbio/2/1/annurev-cancerbio-030617-050558.html?itemId=/content/journals/10.1146/annurev-cancerbio-030617-050558&mimeType=html&fmt=ahah

Literature Cited

  1. Azuma M, Ebihara T, Oshiumi H, Matsumoto M, Seya T. 2012. Cross-priming for antitumor CTL induced by soluble Ag+ polyI:C depends on the TICAM-1 pathway in mouse CD11c+/CD8α+ dendritic cells. Oncoimmunology 1:5581–92 [Google Scholar]
  2. Banday AH, Jeelani S, Hruby VJ. 2015. Cancer vaccine adjuvants—recent clinical progress and future perspectives. Immunopharmacol. Immunotoxicol. 37:11–11 [Google Scholar]
  3. Bauer S, Groh V, Wu J, Steinle A, Phillips JH. et al. 1999. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 285:5428727–29 [Google Scholar]
  4. Bautz DJ, Sherpa AT, Threadgill DW. 2016. Prophylactic vaccination targeting ERBB3 decreases polyp burden in a mouse model of human colorectal cancer. Oncoimmunology 6:1e1255395 [Google Scholar]
  5. Beatty P, Ranganathan S, Finn OJ. 2012. Prevention of colitis-associated colon cancer using a vaccine to target abnormal expression of the MUC1 tumor antigen. Oncoimmunology 1:3263–70 [Google Scholar]
  6. Benevides L, da Fonseca DM, Donate PB, Tiezzi DG, De Carvalho DD. et al. 2015. IL17 promotes mammary tumor progression by changing the behavior of tumor cells and eliciting tumorigenic neutrophils recruitment. Cancer Res 75:183788–99 [Google Scholar]
  7. Beutler B. 2000. Tlr4: central component of the sole mammalian LPS sensor. Curr. Opin. Immunol. 12:120–26 [Google Scholar]
  8. Blachere NE, Morris HK, Braun D, Saklani H, Di Santo JP. et al. 2006. IL-2 is required for the activation of memory CD8+ T cells via antigen cross-presentation. J. Immunol. 176:127288–300 [Google Scholar]
  9. Boch C, Kollmeier J, Roth A, Stephan-Falkenau S, Misch D. et al. 2013. The frequency of EGFR and KRAS mutations in non-small cell lung cancer (NSCLC): routine screening data for central Europe from a cohort study. BMJ Open 3:4e002560 [Google Scholar]
  10. Brunham RC, Coombs KM. 1998. In celebration of the 200th anniversary of Edward Jenner's Inquiry into the Causes and Effects of the Variolae vaccinae. Can. J. Infect. Dis. 9:5310–13 [Google Scholar]
  11. Bryant KL, Mancias JD, Kimmelman AC, Der CJ. 2014. KRAS: feeding pancreatic cancer proliferation. Trends Biochem. Sci. 39:291–100 [Google Scholar]
  12. Burdette DL, Monroe KM, Sotelo-Troha K, Iwig JS, Eckert B. et al. 2011. STING is a direct innate immune sensor of cyclic di-GMP. Nature 478:7370515–18 [Google Scholar]
  13. Carreno BM, Magrini V, Becker-Hapak M, Kaabinejadian S, Hundal J. et al. 2015. A dendritic cell vaccine increases the breadth and diversity of melanoma neoantigen-specific T cells. Science 348:6236803–8 [Google Scholar]
  14. Chang M-H, Chen C-J, Lai M-S, Hsu H-M, Wu T-C. et al. 1997. Universal hepatitis B vaccination in Taiwan and the incidence of hepatocellular carcinoma in children. N. Engl. J. Med. 336:261855–59 [Google Scholar]
  15. Chassaing B, Aitken JD, Malleshappa M, Vijay-Kumar M. 2014. Dextran sulfate sodium (DSS)-induced colitis in mice. Curr. Protoc. Immunol. 104:15.25 [Google Scholar]
  16. Chen H-M, Tanaka N, Mitani Y, Oda E, Nozawa H. et al. 2009. Critical role for constitutive type I interferon signaling in the prevention of cellular transformation. Cancer Sci 100:3449–56 [Google Scholar]
  17. Cho JH, Lee H-J, Ko H-J, Yoon B-I, Choe J. et al. 2017. The TLR7 agonist imiquimod induces anti-cancer effects via autophagic cell death and enhances anti-tumoral and systemic immunity during radiotherapy for melanoma. Oncotarget 8:24932–48 [Google Scholar]
  18. Chu NJ, Armstrong TD, Jaffee EM. 2015. Nonviral oncogenic antigens and the inflammatory signals driving early cancer development as targets for cancer immunoprevention. Clin. Cancer Res. 21:71549–57 [Google Scholar]
  19. Coler RN, Bertholet S, Moutaftsi M, Guderian JA, Windish HP. et al. 2011. Development and characterization of synthetic glucopyranosyl lipid adjuvant system as a vaccine adjuvant. PLOS ONE 6:1e16333 [Google Scholar]
  20. Colotta F, Allavena P, Sica A, Garlanda C, Mantovani A. 2009. Cancer-related inflammation, the seventh hallmark of cancer: links to genetic instability. Carcinogenesis 30:71073–81 [Google Scholar]
  21. Corrales L, Glickman LH, McWhirter SM, Kanne DB, Sivick KE. et al. 2015. Direct activation of STING in the tumor microenvironment leads to potent and systemic tumor regression and immunity. Cell Rep 11:71018–30 [Google Scholar]
  22. Çuburu N, Graham BS, Buck CB, Kines RC, Pang Y-YS. et al. 2012. Intravaginal immunization with HPV vectors induces tissue-resident CD8+ T cell responses. J. Clin. Investig. 122:124606–20 [Google Scholar]
  23. Danilchanka O, Mekalanos JJ. 2013. Cyclic dinucleotides and the innate immune response. Cell 154:5962–70 [Google Scholar]
  24. De Gregorio E, Caproni E, Ulmer JB. 2013. Vaccine adjuvants: mode of action. Front. Immunol. 4:214 [Google Scholar]
  25. Di Pasquale A, Preiss S, Tavares Da Silva F, Garçon N. 2015. Vaccine adjuvants: from 1920 to 2015 and beyond. Vaccines 3:2320–43 [Google Scholar]
  26. Ding L, Ley TJ, Larson DE, Miller CA, Koboldt DC. et al. 2012. Clonal evolution in relapsed acute myeloid leukaemia revealed by whole-genome sequencing. Nature 481:7382506–10 [Google Scholar]
  27. Dowling JK, Mansell A. 2016. Toll-like receptors: the swiss army knife of immunity and vaccine development. Clin. Transl. Immunol. 5:5e85 [Google Scholar]
  28. Dubensky TW, Kanne DB, Leong ML. 2013. Rationale, progress and development of vaccines utilizing STING-activating cyclic dinucleotide adjuvants. Ther. Adv. Vaccines 1:4131–43 [Google Scholar]
  29. Dunn GP, Bruce AT, Ikeda H, Old LJ. 2002. Cancer immunoediting: from immunosurveillance to tumor escape. Nat. Immunol. 3:11991–98 [Google Scholar]
  30. Duthie MS, Windish HP, Fox CB, Reed SG. 2011. Use of defined TLR ligands as adjuvants within human vaccines. Immunol. Rev. 239:1178–96 [Google Scholar]
  31. Facciponte JG, Ugel S, De Sanctis F, Li C, Wang L. et al. 2014. Tumor endothelial marker 1–specific DNA vaccination targets tumor vasculature. J. Clin. Investig. 124:41497–511 [Google Scholar]
  32. Fearon ER, Vogelstein B. 1990. A genetic model for colorectal tumorigenesis. Cell 61:5759–67 [Google Scholar]
  33. Frazer IH, Lowy DR, Schiller JT. 2007. Prevention of cancer through immunization: prospects and challenges for the 21st century. Eur. J. Immunol. 37:Suppl. 1S148–55 [Google Scholar]
  34. Fu J, Kanne DB, Leong M, Glickman LH, McWhirter SM. et al. 2015. STING agonist formulated cancer vaccines can cure established tumors resistant to PD-1 blockade. Sci. Transl. Med. 7:283283ra52 [Google Scholar]
  35. Gao Y, Whitaker-Dowling P, Bergman I. 2015. Memory antitumor T-cells resist inhibition by immune suppressor cells. Anticancer Res 35:94593–97 [Google Scholar]
  36. Gebhardt T, Wakim LM, Eidsmo L, Reading PC, Heath WR, Carbone FR. 2009. Memory T cells in nonlymphoid tissue that provide enhanced local immunity during infection with herpes simplex virus. Nat. Immunol. 10:5524–30 [Google Scholar]
  37. Geijtenbeek TBH, Gringhuis SI. 2016. C-type lectin receptors in the control of T helper cell differentiation. Nat. Rev. Immunol. 16:7433–48 [Google Scholar]
  38. Gnjatic S, Sawhney NB, Bhardwaj N. 2010. Toll-like receptor agonists: Are they good adjuvants?. Cancer J 16:4382–91 [Google Scholar]
  39. Gross L. 1943. Intradermal immunization of C3H mice against a sarcoma that originated in an animal of the same line. Cancer Res 3:5326–33 [Google Scholar]
  40. Gubin MM, Artyomov MN, Mardis ER, Schreiber RD. 2015. Tumor neoantigens: building a framework for personalized cancer immunotherapy. J. Clin. Investig. 125:93413–21 [Google Scholar]
  41. Gupta AK, Cherman AM, Tyring SK. 2004. Viral and nonviral uses of imiquimod: a review. J. Cutan. Med. 8:338–52 [Google Scholar]
  42. Hanson MC, Crespo MP, Abraham W, Moynihan KD, Szeto GL. et al. 2015. Nanoparticulate STING agonists are potent lymph node-targeted vaccine adjuvants. J. Clin. Investig. 125:62532–46 [Google Scholar]
  43. Haworth KB, Leddon JL, Chen C-Y, Horwitz EM, Mackall CL, Cripe TP. 2015. Going back to class I: MHC and immunotherapies for childhood cancer. Pediatr. Blood Cancer 62:4571–76 [Google Scholar]
  44. He D, Li H, Yusuf N, Elmets CA, Athar M. et al. 2012. IL-17 mediated inflammation promotes tumor growth and progression in the skin. PLOS ONE 7:2e32126 [Google Scholar]
  45. Huijbers EJM, Griffioen AW. 2017. The revival of cancer vaccines—the eminent need to activate humoral immunity. Hum. Vaccines Immunother. 13:1112–14 [Google Scholar]
  46. Ingale S, Wolfert MA, Gaekwad J, Buskas T, Boons G-J. 2007. Robust immune responses elicited by a fully synthetic three-component vaccine. Nat. Chem. Biol. 3:10663–67 [Google Scholar]
  47. Ishizaka ST, Hawkins LD. 2007. E6020: a synthetic Toll-like receptor 4 agonist as a vaccine adjuvant. Expert Rev. Vaccines 6:5773–84 [Google Scholar]
  48. Jobsri J, Allen A, Rajagopal D, Shipton M, Kanyuka K. et al. 2015. Plant virus particles carrying tumour antigen activate TLR7 and induce high levels of protective antibody. PLOS ONE 10:2e0118096 [Google Scholar]
  49. Joura EA, Giuliano AR, Iversen O-E, Bouchard C, Mao C. et al. 2015. A 9-valent HPV vaccine against infection and intraepithelial neoplasia in women. N. Engl. J. Med. 372:8711–23 [Google Scholar]
  50. Kanneganti T-D, Lamkanfi M, Núñez G. 2007. Intracellular NOD-like receptors in host defense and disease. Immunity 27:4549–59 [Google Scholar]
  51. Kantoff PW, Higano CS, Shore ND, Berger ER, Small EJ. et al. 2010. Sipuleucel-T immunotherapy for castration-resistant prostate cancer. N. Engl. J. Med. 363:5411–22 [Google Scholar]
  52. Keenan BP, Saenger Y, Kafrouni MI, Leubner A, Lauer P. et al. 2014. A Listeria vaccine and depletion of T-regulatory cells activate immunity against early stage pancreatic intraepithelial neoplasms and prolong survival of mice. Gastroenterology 146:71784–86 [Google Scholar]
  53. Khan N, Vidyarthi A, Pahari S, Negi S, Aqdas M. et al. 2016. Signaling through NOD-2 and TLR-4 bolsters the T cell priming capability of dendritic cells by inducing autophagy. Sci. Rep. 6:19084 [Google Scholar]
  54. Kiani A, Tschiersch A, Gaboriau E, Otto F, Seiz A. et al. 1997. Downregulation of the proinflammatory cytokine response to endotoxin by pretreatment with the nontoxic lipid A analog SDZ MRL 953 in cancer patients. Blood 90:41673–83 [Google Scholar]
  55. Kim MT, Kurup SP, Starbeck-Miller GR, Harty JT. 2016. Manipulating memory CD8 T cell numbers by timed enhancement of IL-2 signals. J. Immunol. 197:51754–61 [Google Scholar]
  56. Kool M, Fierens K, Lambrecht BN. 2012. Alum adjuvant: some of the tricks of the oldest adjuvant. J. Med. Microbiol. 61:Pt. 7927–34 [Google Scholar]
  57. Lamrani M, Sassi N, Paul C, Yousfi N, Boucher J-L. et al. 2016. TLR4/IFNγ pathways induce tumor regression via NOS II-dependent NO and ROS production in murine breast cancer models. Oncoimmunology 5:5e1123369 [Google Scholar]
  58. Libanova R, Ebensen T, Schulze K, Bruhn D, Nörder M. et al. 2010. The member of the cyclic di-nucleotide family bis-(3′, 5′)-cyclic dimeric inosine monophosphate exerts potent activity as mucosal adjuvant. Vaccine 28:102249–58 [Google Scholar]
  59. Loo Y-M, Gale M. 2011. Immune signaling by RIG-I-like receptors. Immunity 34:5680–92 [Google Scholar]
  60. Macallan DC, Borghans JAM, Asquith B. 2017. Human T cell memory: a dynamic view. Vaccines 5:15 [Google Scholar]
  61. Mantovani A, Allavena P, Sica A, Balkwill F. 2008. Cancer-related inflammation. Nature 454:7203436–44 [Google Scholar]
  62. Markowitz LE, Liu G, Hariri S, Steinau M, Dunne EF, Unger ER. 2016. Prevalence of HPV after introduction of the vaccination program in the United States. Pediatrics 137:e20151968 [Google Scholar]
  63. Melero I, Gaudernack G, Gerritsen W, Huber C, Parmiani G. et al. 2014. Therapeutic vaccines for cancer: an overview of clinical trials. Nat. Rev. Clin. Oncol. 11:9509–24 [Google Scholar]
  64. Michie CA, McLean A, Alcock C, Beverley PC. 1992. Lifespan of human lymphocyte subsets defined by CD45 isoforms. Nature 360:6401264–65 [Google Scholar]
  65. Miller DG. 1980. On the nature of susceptibility to cancer. The presidential address. Cancer 46:61307–18 [Google Scholar]
  66. NCI SEER (Natl. Cancer Inst. Surveill. Epidemiol. End Results Program). 2016. Cancer stat facts: cancer of any site Natl. Cancer Inst., Bethesda, MD. https://seer.cancer.gov/statfacts/html/all.html
  67. Parkin DM. 2006. The global health burden of infection-associated cancers in the year 2002. Int. J. Cancer 118:123030–44 [Google Scholar]
  68. Poltorak A, Smirnova I, He X, Liu MY, Van Huffel C. et al. 1998. Genetic and physical mapping of the Lps locus: identification of the Toll-4 receptor as a candidate gene in the critical region. Blood Cells Mol. Dis. 24:3340–55 [Google Scholar]
  69. Reed SG, Hsu F-C, Carter D, Orr MT. 2016. The science of vaccine adjuvants: advances in TLR4 ligand adjuvants. Curr. Opin. Immunol. 41:85–90 [Google Scholar]
  70. Remakus S, Sigal LJ. 2013. Memory CD8+ T cell protection. Adv. Exp. Med. Biol. 785:77–86 [Google Scholar]
  71. Rosenberg SA, Yang JC, Restifo NP. 2004. Cancer immunotherapy: moving beyond current vaccines. Nat. Med. 10:9909–15 [Google Scholar]
  72. Samadder NJ, Neklason DW, Boucher KM, Byrne KR, Kanth P. et al. 2016. Effect of sulindac and erlotinib versus placebo on duodenal neoplasia in familial adenomatous polyposis: a randomized clinical trial. JAMA 315:121266–75 [Google Scholar]
  73. Schinzel AC, Hahn WC. 2008. Oncogenic transformation and experimental models of human cancer. Front. Biosci. 13:71–84 [Google Scholar]
  74. Schreiber RD, Old LJ, Smyth MJ. 2011. Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science 331:60241565–70 [Google Scholar]
  75. Seya T, Shime H, Takeda Y, Tatematsu M, Takashima K, Matsumoto M. 2015. Adjuvant for vaccine immunotherapy of cancer—focusing on Toll-like receptor 2 and 3 agonists for safely enhancing antitumor immunity. Cancer Sci 106:121659–68 [Google Scholar]
  76. Shankaran V, Ikeda H, Bruce AT, White JM, Swanson PE. et al. 2001. IFNγ and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 410:68321107–11 [Google Scholar]
  77. Škrnjug I, Guzmán CA, Rueckert C, Ruecker C. 2014. Cyclic GMP-AMP displays mucosal adjuvant activity in mice. PLOS ONE 9:10e110150 [Google Scholar]
  78. Smyth K, Garcia K, Sun Z, Tuo W, Xiao Z. 2013. TLR agonists are highly effective at eliciting functional memory CTLs of effector memory phenotype in peptide immunization. Int. Immunopharmacol. 15:167–72 [Google Scholar]
  79. Spira A, Disis ML, Schiller JT, Vilar E, Rebbeck TR. et al. 2016. Leveraging premalignant biology for immune-based cancer prevention. PNAS 113:3910750–58 [Google Scholar]
  80. Spira A, Yurgelun MB, Alexandrov L, Rao A, Bejar R. et al. 2017. Precancer atlas to drive precision prevention trials. Cancer Res 77:71510–41 [Google Scholar]
  81. Stratton MR, Campbell PJ, Futreal PA. 2009. The cancer genome. Nature 458:7239719–24 [Google Scholar]
  82. Sun L, Wu J, Du F, Chen X, Chen ZJ. 2013. Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science 339:6121786–91 [Google Scholar]
  83. Takeda Y, Azuma M, Matsumoto M, Seya T. 2016. Tumoricidal efficacy coincides with CD11c up-regulation in antigen-specific CD8+ T cells during vaccine immunotherapy. J. Exp. Clin. Cancer Res. 35:1143 [Google Scholar]
  84. Takeuchi O, Akira S. 2010. Pattern recognition receptors and inflammation. Cell 140:6805–20 [Google Scholar]
  85. Tao J, Zhou X, Jiang Z. 2016. cGAS-cGAMP-STING: the three musketeers of cytosolic DNA sensing and signaling. IUBMB Life 68:11858–70 [Google Scholar]
  86. Temizoz B, Kuroda E, Ishii KJ. 2016. Vaccine adjuvants as potential cancer immunotherapeutics. Int. Immunol. 28:7329–38 [Google Scholar]
  87. Tough DF, Sprent J. 1995. Life span of naive and memory T cells. Stem Cells 13:3242–49 [Google Scholar]
  88. Toussi DN, Massari P. 2014. Immune adjuvant effect of molecularly-defined Toll-like receptor ligands. Vaccines 2:2323–53 [Google Scholar]
  89. van Aalst S, Ludwig IS, van Kooten PJS, van der Zee R, van Eden W, Broere F. 2017. Dynamics of APC recruitment at the site of injection following injection of vaccine adjuvants. Vaccine 35:121622–29 [Google Scholar]
  90. Varthaman A, Moreau HD, Maurin M, Benaroch P. 2016. TLR3-induced maturation of murine dendritic cells regulates CTL responses by modulating PD-L1 trafficking. PLOS ONE 11:12e0167057 [Google Scholar]
  91. Vaughn CP, ZoBell SD, Furtado LV, Baker CL, Samowitz WS. 2011. Frequency of KRAS, BRAF, and NRAS mutations in colorectal cancer. Genes Chromosomes Cancer 50:5307–12 [Google Scholar]
  92. Vetter CS, Groh V, thor Straten P, Spies T, Bröcker E-B, Becker JC. 2002. Expression of stress-induced MHC class I related chain molecules on human melanoma. J. Investig. Dermatol. 118:4600–5 [Google Scholar]
  93. Vogelstein B, Papadopoulos N, Velculescu VE, Zhou S, Diaz LA, Kinzler KW. 2013. Cancer genome landscapes. Science 339:61271546–58 [Google Scholar]
  94. Vosika GJ, Barr C, Gilbertson D. 1984. Phase-I study of intravenous modified lipid A. Cancer Immunol. Immunother. 18:2107–12 [Google Scholar]
  95. Wheeler CM, Castellsagué X, Garland SM, Szarewski A, Paavonen J. et al. 2012. Cross-protective efficacy of HPV-16/18 AS04-adjuvanted vaccine against cervical infection and precancer caused by non-vaccine oncogenic HPV types: 4-year end-of-study analysis of the randomised, double-blind PATRICIA trial. Lancet Oncol 13:1100–10 [Google Scholar]
  96. Willimsky G, Czéh M, Loddenkemper C, Gellermann J, Schmidt K. et al. 2008. Immunogenicity of premalignant lesions is the primary cause of general cytotoxic T lymphocyte unresponsiveness. J. Exp. Med. 205:71687–700 [Google Scholar]
  97. Woo S-R, Fuertes MB, Corrales L, Spranger S, Furdyna MJ. et al. 2014. STING-dependent cytosolic DNA sensing mediates innate immune recognition of immunogenic tumors. Immunity 41:5830–42 [Google Scholar]
  98. Yadav M, Jhunjhunwala S, Phung QT, Lupardus P, Tanguay J. et al. 2014. Predicting immunogenic tumour mutations by combining mass spectrometry and exome sequencing. Nature 515:7528572–76 [Google Scholar]
  99. Yang RB, Mark MR, Gray A, Huang A, Xie MH. et al. 1998. Toll-like receptor-2 mediates lipopolysaccharide-induced cellular signalling. Nature 395:6699284–88 [Google Scholar]
  100. Yarchoan M, Johnson BA, Lutz ER, Laheru DA, Jaffee EM. 2017. Targeting neoantigens to augment antitumour immunity. Nat. Rev. Cancer 17:4209–22 [Google Scholar]
  101. Yokoyama WM, Plougastel BFM. 2003. Immune functions encoded by the natural killer gene complex. Nat. Rev. Immunol. 3:4304–16 [Google Scholar]
  102. Zheng JH, Nguyen VH, Jiang S-N, Park S-H, Tan W. et al. 2017. Two-step enhanced cancer immunotherapy with engineered Salmonella typhimurium secreting heterologous flagellin. Sci. Transl. Med. 9:376eaak9537 [Google Scholar]
  103. Zitvogel L, Galluzzi L, Kepp O, Smyth MJ, Kroemer G. 2015. Type I interferons in anticancer immunity. Nat. Rev. Immunol. 15:7405–14 [Google Scholar]
/content/journals/10.1146/annurev-cancerbio-030617-050558
Loading
/content/journals/10.1146/annurev-cancerbio-030617-050558
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error