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Original Research

A poly-neoantigen DNA vaccine synergizes with PD-1 blockade to induce T cell-mediated tumor control

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Article: 1652539 | Received 26 Apr 2019, Accepted 31 Jul 2019, Published online: 02 Sep 2019

References

  • Lurquin C, Van Pel A, Mariamé B, De Plaen E, Szikora JP, Janssens C, Reddehase MJ, Lejeune J, Boon T. Structure of the gene of tum- transplantation antigen P91A: the mutated exon encodes a peptide recognized with Ld by cytolytic T cells. Cell. 1989;58(2):1–10. doi:10.1016/0092-8674(89)90844-1.
  • Swann JB, Smyth MJ. Immune surveillance of tumors. J Clin Invest. 2007;117(5):1137–1146. doi:10.1172/JCI31405.
  • Sharma P, Allison JP. Immune checkpoint targeting in cancer therapy: toward combination strategies with curative potential. Cell. 2015;161(2):205–214. doi:10.1016/j.cell.2015.03.030.
  • Seidel JA, Otsuka A, Kabashima K. Anti-PD-1 and anti-CTLA-4 therapies in cancer: mechanisms of action, efficacy, and limitations. Front Oncol. 2018;8:86. doi:10.3389/fonc.2018.00086.
  • Aldous AR, Dong JZ. Personalized neoantigen vaccines: A new approach to cancer immunotherapy. Bioorg Med Chem. 2018;26(10):2842–2849. doi:10.1016/j.bmc.2017.10.021.
  • Heuts J, Varypataki EM, van der Maaden K, Romeijn S, Drijfhout JW, van Scheltinga AT, Ossendorp F, Jiskoot W. Cationic liposomes: A flexible vaccine delivery system for physicochemically diverse antigenic peptides. Pharm Res. 2018;35(11):207. doi:10.1007/s11095-018-2490-6.
  • Yadav M, Jhunjhunwala S, Phung QT, Lupardus P, Tanguay J, Bumbaca S, Franci C, Cheung TK, Fritsche J, Weinschenk T, et al. Predicting immunogenic tumour mutations by combining mass spectrometry and exome sequencing. Nature. 2014;515(7528):572–576. doi:10.1038/nature14001.
  • Bekri S, Uduman M, Gruenstein D, Mei AHC, Tung K, Rodney-Sandy R, Bogen B, Buell J, Stein R, Doherty K, et al. Neoantigen synthetic peptide vaccine for multiple myeloma elicits T cell immunity in a pre-clinical model. Blood. 2017;130(Suppl 1):1868.
  • Kreiter S, Vormehr M, van de Roemer N, Diken M, Löwer M, Diekmann J, Boegel S, Schrörs B, Vascotto F, Castle JC, et al. Mutant MHC class II epitopes drive therapeutic immune responses to cancer. Nature. 2015;520(7549):692–696. doi:10.1038/nature14426.
  • Kranz LM, Diken M, Haas H, Kreiter S, Loquai C, Reuter KC, 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(7607):396–401. doi:10.1038/nature18300.
  • Sahin U, Derhovanessian E, Miller M, Kloke B-P, Simon P, Löwer M, Bukur V, Tadmor AD, Luxemburger U, Schrörs B, et al. Personalized RNA mutanome vaccines mobilize poly-specific therapeutic immunity against cancer. Nature. 2017;547(7662):222–226. doi:10.1038/nature23003.
  • Ott PA, Hu Z, Keskin DB, Shukla SA, Sun J, Bozym DJ, Zhang W, Luoma A, Giobbie-Hurder A, Peter L, et al. An immunogenic personal neoantigen vaccine for patients with melanoma. Nature. 2017;547(7662):217–221. doi:10.1038/nature22991.
  • Tang DC, DeVit M, Johnston SA. Genetic immunization is a simple method for eliciting an immune response. Nature. 1992;356(6365):152–154. doi:10.1038/356152a0.
  • Ulmer JB, Donnelly JJ, Parker SE, Rhodes GH, Felgner PL, Dwarki VJ, Gromkowski SH, Deck RR, DeWitt CM, Friedman A. Heterologous protection against influenza by injection of DNA encoding a viral protein. Science. 1993;259(5102):1745–1749. doi:10.1126/science.8456302.
  • Wang B, Ugen KE, Srikantan V, Agadjanyan MG, Dang K, Refaeli Y, Sato AI, Boyer J, Williams WV, Weiner DB. Gene inoculation generates immune responses against human immunodeficiency virus type 1. Proc Natl Acad Sci U S A. 1993;90(9):4156–4160. doi:10.1073/pnas.90.9.4156.
  • Fioretti D, Iurescia S, Fazio VM, Rinaldi M. DNA vaccines: developing new strategies against cancer. J Biomed Biotechnol. 2010;2010:174378. doi:10.1155/2010/174378.
  • Raz E, Carson DA, Parker SE, Parr TB, Abai AM, Aichinger G, Gromkowski SH, Singh M, Lew D, Yankauckas MA. Intradermal gene immunization: the possible role of DNA uptake in the induction of cellular immunity to viruses. Proc Natl Acad Sci U S A. 1994;91(20):9519–9523. doi:10.1073/pnas.91.20.9519.
  • Williams BB, Wall M, Miao RY, Williams B, Bertoncello I, Kershaw MH, Mantamadiotis T, Haber M, Norris MD, Gautam A, et al. Induction of T cell-mediated immunity using a c-Myb DNA vaccine in a mouse model of colon cancer. Cancer Immunol Immunother. 2008;57(11):1635–1645. doi:10.1007/s00262-008-0497-2.
  • Porgador A, Irvine KR, Iwasaki A, Barber BH, Restifo NP, Germain RN. Predominant role for directly transfected dendritic cells in antigen presentation to CD8+ T cells after gene gun immunization. J Exp Med. 1998;188(6):1075–1082. doi:10.1084/jem.188.6.1075.
  • Luxembourg A, Hannaman D, Ellefsen B, Nakamura G, Bernard R. Enhancement of immune responses to an HBV DNA vaccine by electroporation. Vaccine. 2006;24(21):4490–4493. doi:10.1016/j.vaccine.2005.08.014.
  • Bins AD, Jorritsma A, Wolkers MC, Hung C-F, Wu T-C, Schumacher TNM, Haanen JBAG. A rapid and potent DNA vaccination strategy defined by in vivo monitoring of antigen expression. Nat Med. 2005;11(8):899–904. doi:10.1038/nm1264.
  • Duperret EK, Perales-Puchalt A, Stoltz R, G H H, Mandloi N, Barlow J, Chaudhuri A, Sardesai NY, Weiner DB. A synthetic DNA, multi-neoantigen vaccine drives predominately MHC class I CD8+ T-cell responses, impacting tumor challenge. Cancer Immunol Res. 2019;7(2):174–182. doi:10.1158/2326-6066.CIR-18-0283.
  • Falo LD Jr., Kovacsovics-Bankowski M, Thompson K, Rock KL. Targeting antigen into the phagocytic pathway in vivo induces protective tumour immunity. Nat Med. 1995;1:649–653.
  • Winzler C, Rovere P, Rescigno M, Granucci F, Penna G, Adorini L, Zimmermann VS, Davoust J, Ricciardi-Castagnoli P. Maturation stages of mouse dendritic cells in growth factor-dependent long-term cultures. J Exp Med. 1997;185(2):317–328. doi:10.1084/jem.185.2.317.
  • Porgador A, Yewdell JW, Deng Y, Bennink JR, Germain RN. Localization, quantitation, and in situ detection of specific peptide-MHC class I complexes using a monoclonal antibody. Immunity. 1997;6:715–726.
  • Endmann A, Baden M, Weisermann E, Kapp K, Schroff M, Kleuss C, Wittig B, Juhls C. Immune response induced by a linear DNA vector: influence of dose, formulation and route of injection. Vaccine. 2010;28(21):3642–3649. doi:10.1016/j.vaccine.2010.03.034.
  • Fransen MF, Schoonderwoerd M, Knopf P, Camps MG, Hawinkels LJ, Kneilling M,van Hall T, Ossendorp F. Tumor-draining lymph nodes are pivotal in PD-1/PD-L1 checkpoint therapy. JCI Insight. 2018;3:23. doi:10.1172/jci.insight.97941.
  • McCluskie MJ, Brazolot Millan CL, Gramzinski RA, Robinson HL, Santoro JC, Fuller JT, Widera G, Haynes JR, Purcell RH, Davis HL. Route and method of delivery of DNA vaccine influence immune responses in mice and non-human primates. Mol Med. 1999;5:287–300.
  • Kleinovink JW, Marijt KA, Schoonderwoerd MJA, van Hall T, Ossendorp F, Fransen MF. PD-L1 expression on malignant cells is no prerequisite for checkpoint therapy. Oncoimmunology. 2017;6(4):e1294299. doi:10.1080/2162402X.2017.1294299.
  • Sato Y, Roman M, Tighe H, Lee D, Corr M, Nguyen MD, Silverman GJ, Lotz M, Carson DA, Raz E. Immunostimulatory DNA sequences necessary for effective intradermal gene immunization. Science. 1996;273(5273):352–354. doi:10.1126/science.273.5273.352.
  • Klinman DM, Yamshchikov G, Ishigatsubo Y. Contribution of CpG motifs to the immunogenicity of DNA vaccines. J Immunol. 1997;158:3635–3639.
  • Suschak JJ, Wang S, Fitzgerald KA, Lu S. A cGAS-independent STING/IRF7 pathway mediates the immunogenicity of DNA vaccines. J Immunol. 2016;196(1):310–316. doi:10.4049/jimmunol.1501836.
  • Jalah R, Patel V, Kulkarni V, Rosati M, Alicea C, Ganneru B, von Gegerfelt A, Huang W, Guan Y, Broderick KE, et al. IL-12 DNA as molecular vaccine adjuvant increases the cytotoxic T cell responses and breadth of humoral immune responses in SIV DNA vaccinated macaques. Hum Vaccin Immunother. 2012;8(11):1620–1629. doi:10.4161/hv.21407.
  • Leachman SA, Tigelaar RE, Shlyankevich M, Slade MD, Irwin M, Chang E, Wu TC, Xiao W, Pazhani S, Zelterman D, et al. Granulocyte-macrophage colony-stimulating factor priming plus papillomavirus E6 DNA vaccination: effects on papilloma formation and regression in the cottontail rabbit papillomavirus–rabbit model. J Virol. 2000;74(18):8700–8708. doi:10.1128/jvi.74.18.8700-8708.2000.
  • Qing Y, Chen M, Zhao J, Hu H, Xu H, Ling N, Peng M, Ren H. Construction of an HBV DNA vaccine by fusion of the GM-CSF gene to the HBV-S gene and examination of its immune effects in normal and HBV-transgenic mice. Vaccine. 2010;28(26):4301–4307. doi:10.1016/j.vaccine.2010.04.023.
  • Lindencrona JA, Preiss S, Kammertoens T, Schüler T, Piechocki M, Wei W-Z, Seliger B, Blankenstein T, Kiessling R. CD4+ T cell-mediated HER-2/neu-specific tumor rejection in the absence of B cells. Int J Cancer. 2004;109(2):259–264. doi:10.1002/ijc.11654.
  • Kim JJ, Bagarazzi ML, Trivedi N, Hu Y, Kazahaya K, Wilson DM, Ciccarelli R, Chattergoon MA, Dang K, Mahalingam S, et al. Engineering of in vivo immune responses to DNA immunization via codelivery of costimulatory molecule genes. Nat Biotechnol. 1997;15(7):641–646. doi:10.1038/nbt0797-641.
  • Agadjanyan MG, Kim JJ, Trivedi N, Wilson DM, Monzavi-Karbassi B, Morrison LD, Nottingham LK, Dentchev T, Tsai A, Dang K, et al. CD86 (B7-2) can function to drive MHC-restricted antigen-specific CTL responses in vivo. J Immunol. 1999;162:3417–3427.
  • Mendoza RB, Cantwell MJ, Kipps TJ. Immunostimulatory effects of a plasmid expressing CD40 ligand (CD154) on gene immunization. J Immunol. 1997;159:5777–5781.
  • Ossendorp F, Mengede E, Camps M, Filius R, Melief CJ. Specific T helper cell requirement for optimal induction of cytotoxic T lymphocytes against major histocompatibility complex class II negative tumors. J Exp Med. 1998;187(5):693–702. doi:10.1084/jem.187.5.693.
  • Borst J, Ahrends T, Babala N, Melief CJM, Kastenmuller W. CD4(+) T cell help in cancer immunology and immunotherapy. Nat Rev Immunol. 2018;18(10):635–647. doi:10.1038/s41577-018-0044-0.
  • Perez-Diez A, Joncker NT, Choi K, Chan WFN, Anderson CC, Lantz O, Matzinger P. CD4 cells can be more efficient at tumor rejection than CD8 cells. Blood. 2007;109(12):5346–5354. doi:10.1182/blood-2006-10-051318.
  • Xie Y, Akpinarli A, Maris C, Hipkiss EL, Lane M, Kwon E-KM, Muranski P, Restifo NP, Antony PA. Naive tumor-specific CD4(+) T cells differentiated in vivo eradicate established melanoma. J Exp Med. 2010;207(3):651–667. doi:10.1084/jem.20091921.
  • Elnekave M, Furmanov K, Nudel I, Arizon M, Clausen BE, Hovav AH. Directly transfected langerin+ dermal dendritic cells potentiate CD8+ T cell responses following intradermal plasmid DNA immunization. J Immunol. 2010;185(6):3463–3471. doi:10.4049/jimmunol.1001825.
  • Bedoui S, Davey GM, Lew AM, Heath WR. Equivalent stimulation of naive and memory CD8 T cells by DNA vaccination: a dendritic cell-dependent process. Immunol Cell Biol. 2009;87(3):255–259. doi:10.1038/icb.2008.105.
  • Gurunathan S, Klinman DM, Seder RA. DNA vaccines: immunology, application, and optimization*. Annu Rev Immunol. 2000;18:927–974. doi:10.1146/annurev.immunol.18.1.927.
  • Xiong H, Mittman S, Rodriguez R, Pacheco-Sanchez P, Moskalenko M, Yang Y, Elstrott J, Ritter AT, Müller S, Nickles D, et al. Coexpression of inhibitory receptors enriches for activated and functional CD8+ T cells in murine syngeneic tumor models. Cancer Immunol Res. 2019;7(6):963–976. doi:10.1158/2326-6066.CIR-18-0750.
  • Castle JC, Kreiter S, Diekmann J, Lower M, van de Roemer N, de Graaf J, Selmi A, Diken M, Boegel S, Paret C, et al. Exploiting the mutanome for tumor vaccination. Cancer Res. 2012;72(5):1081–1091. doi:10.1158/0008-5472.CAN-11-3722.
  • Carreno BM, Magrini V, Becker-Hapak M, Kaabinejadian S, Hundal J, Petti AA, Ly A, Lie W-R, Hildebrand WH, Mardis ER, et al. Cancer immunotherapy. A dendritic cell vaccine increases the breadth and diversity of melanoma neoantigen-specific T cells. Science. 2015;348(6236):803–808. doi:10.1126/science.aaa3828.
  • Rajasagi M, Shukla SA, Fritsch EF, Keskin DB, DeLuca D, Carmona E, Zhang W, Sougnez C, Cibulskis K, Sidney J, et al. Systematic identification of personal tumor-specific neoantigens in chronic lymphocytic leukemia. Blood. 2014;124(3):453–462. doi:10.1182/blood-2014-04-567933.
  • Vormehr M, Reinhard K, Blatnik R, Josef K, Beck JD, Salomon N, Suchan M, Selmi A, Vascotto F, Zerweck J, et al. A non-functional neoepitope specific CD8 + T-cell response induced by tumor derived antigen exposure in vivo. Oncoimmunology. 2019;8(3):1553478. doi:10.1080/2162402X.2018.1553478.