Different immunogenicity but similar antitumor efficacy of two DNA vaccines coding for an antigen secreted in different membrane vesicle-associated forms

References

• Finn OJ. Cancer vaccines: between the idea and the reality. Nat Rev Immunol. 2003; 3: 630–41. [PubMed Abstract].
   Google Scholar
• Rice J, Ottensmeier CH, Stevenson FK. DNA vaccines: precision tools for activating effective immunity against cancer. Nat Rev Cancer. 2008; 8: 108–20. [PubMed Abstract].
   Google Scholar
• Liu MA. DNA vaccines: an historical perspective and view to the future. Immunol Rev. 2011; 239: 62–84. [PubMed Abstract].
   Google Scholar
• Guermonprez P, Valladeau J, Zitvogel L, Thery C, Amigorena S. Antigen presentation and T cell stimulation by dendritic cells. Annu Rev Immunol. 2002; 20: 621–67. [PubMed Abstract].
   Google Scholar
• Joffre OP, Segura E, Savina A, Amigorena S. Cross-presentation by dendritic cells. Nat Rev Immunol. 2012; 12: 557–69. [PubMed Abstract].
   Google Scholar
• Li M, Davey GM, Sutherland RM, Kurts C, Lew AM, Hirst C et al. Cell-associated ovalbumin is cross-presented much more efficiently than soluble ovalbumin in vivo. J Immunol. 2001; 166: 6099–103. [PubMed Abstract].
   Google Scholar
• Belizaire R, Unanue ER. Targeting proteins to distinct subcellular compartments reveals unique requirements for MHC class I and II presentation. Proc Natl Acad Sci U S A. 2009; 106: 17463–8. [PubMed Abstract] [PubMed CentralFull Text].
   Google Scholar
• Graham DB, Stephenson LM, Lam SK, Brim K, Lee HM, Bautista J et al. An ITAM-signaling pathway controls cross-presentation of particulate but not soluble antigens in dendritic cells. J Exp Med. 2007; 204: 2889–97. [PubMed Abstract] [PubMed CentralFull Text].
   Google Scholar
• Wolfers J, Lozier A, Raposo G, Regnault A, Thery C, Masurier C et al. Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming. Nat Med. 2001; 7: 297–303. [PubMed Abstract].
   Google Scholar
• Qazi KR, Gehrmann U, Domange Jordo E, Karlsson MC, Gabrielsson S. Antigen-loaded exosomes alone induce Th1-type memory through a B-cell-dependent mechanism. Blood. 2009; 113: 2673–83. [PubMed Abstract].
   Google Scholar
• Zeelenberg IS, Ostrowski M, Krumeich S, Bobrie A, Jancic C, Boissonnas A et al. Targeting tumor antigens to secreted membrane vesicles in vivo induces efficient antitumor immune responses. Cancer Res. 2008; 68: 1228–35. [PubMed Abstract].
   Google Scholar
• Thery C, Regnault A, Garin J, Wolfers J, Zitvogel L, Ricciardi-Castagnoli P et al. Molecular characterization of dendritic cell-derived exosomes. Selective accumulation of the heat shock protein hsc73. J Cell Biol. 1999; 147: 599–610. [PubMed Abstract] [PubMed CentralFull Text].
   Google Scholar
• Hanayama R, Tanaka M, Miwa K, Shinohara A, Iwamatsu A, Nagata S. Identification of a factor that links apoptotic cells to phagocytes. Nature. 2002; 417: 182–7. [PubMed Abstract].
   Google Scholar
• Veron P, Segura E, Sugano G, Amigorena S, Thery C. Accumulation of MFG-E8/lactadherin on exosomes from immature dendritic cells. Blood Cells Mol Dis. 2005; 35: 81–8. [PubMed Abstract].
   Google Scholar
• Rountree RB, Mandl SJ, Nachtwey JM, Dalpozzo K, Do L, Lombardo JR et al. Exosome targeting of tumor antigens expressed by cancer vaccines can improve antigen immunogenicity and therapeutic efficacy. Cancer Res. 2011; 71: 5235–44. [PubMed Abstract].
   Google Scholar
• Hartman ZC, Wei J, Glass OK, Guo H, Lei G, Yang XY et al. Increasing vaccine potency through exosome antigen targeting. Vaccine. 2011; 29: 9361–7. [PubMed Abstract] [PubMed CentralFull Text].
   Google Scholar
• Bellier B, Klatzmann D. Virus-like particle-based vaccines against hepatitis C virus infection. Expert Rev Vaccines. 2013; 12: 143–54. [PubMed Abstract].
   Google Scholar
• Bellier B, Dalba C, Clerc B, Desjardins D, Drury R, Cosset FL et al. DNA vaccines encoding retrovirus-based virus-like particles induce efficient immune responses without adjuvant. Vaccine. 2006; 24: 2643–55. [PubMed Abstract].
   Google Scholar
• Huret C, Desjardins D, Miyalou M, Levacher B, Amadoudji Zin M, Bonduelle O et al. Recombinant retrovirus-derived virus-like particle-based vaccines induce hepatitis C virus-specific cellular and neutralizing immune responses in mice. Vaccine. 2013; 31: 1540–7. [PubMed Abstract].
   Google Scholar
• Bellier B, Huret C, Miyalou M, Desjardins D, Frenkiel MP, Despres P et al. DNA vaccines expressing retrovirus-like particles are efficient immunogens to induce neutralizing antibodies. Vaccine. 2009; 27: 5772–80. [PubMed Abstract].
   Google Scholar
• Lescaille G, Pitoiset F, Macedo R, Baillou C, Huret C, Klatzmann D et al. Efficacy of DNA vaccines forming e7 recombinant retroviral virus-like particles for the treatment of human papillomavirus-induced cancers. Hum Gene Ther. 2013; 24: 533–44. [PubMed Abstract].
   Google Scholar
• Thery C, Amigorena S, Raposo G, Clayton A. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol. 2006; Chapter 3: Unit 3 22. [PubMed Abstract].
   Google Scholar
• Thery C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol. 2009; 9: 581–93. [PubMed Abstract].
   Google Scholar
• Chiarella P, Fazio VM, Signori E. Electroporation in DNA vaccination protocols against cancer. Curr Drug Metab. 2013; 14: 291–9. [PubMed Abstract].
   Google Scholar
• Zeelenberg IS, van Maren WW, Boissonnas A, Van Hout-Kuijer MA, Den Brok MH, Wagenaars JA et al. Antigen localization controls T cell-mediated tumor immunity. J Immunol. 2011; 187: 1281–8. [PubMed Abstract].
   Google Scholar
• Ahlén G, Söderholm J, Tjelle T, Kjeken R, Frelin L, Höglund U et al. In vivo electroporation enhances the immunogenicity of hepatitis C virus nonstructural 3/4A DNA by increased local DNA uptake, protein expression, inflammation, and infiltration of CD3+ T cells. J Immunol. 2007; 179: 4741–53.
   PubMed Web of Science ®Google Scholar
• Widera G, Austin M, Rabussay D, Goldbeck C, Barnett SW, Chen M et al. Increased DNA vaccine delivery and immunogenicity by electroporation in vivo. J Immunol. 2000; 164: 4635–40. [PubMed Abstract].
   Google Scholar
• Daud AI, DeConti RC, Andrews S, Urbas P, Riker AI, Sondak VK et al. Phase I trial of interleukin-12 plasmid electroporation in patients with metastatic melanoma. J Clin Oncol. 2008; 26: 5896–903. [PubMed Abstract] [PubMed CentralFull Text].
   Google Scholar
• Tjelle T, Rabussay D, Ottensmeier C, Mathiesen I, Kjeken R. Taking electroporation-based delivery of DNA vaccination into humans: a generic clinical protocol. Methods Mol. Biol. 2008; 423: 497–507.
   Google Scholar
• Senovilla L, Vacchelli E, Garcia P, Eggermont A, Fridman WH, Galon J et al. Trial watch: DNA vaccines for cancer therapy. Oncoimmunology. 2013; 2: e23803. [PubMed Abstract] [PubMed CentralFull Text].
   Google Scholar
• Crescitelli R, Lasser C, Szabo TG, Kittel A, Eldh M, Dianzani I. Distinct RNA profiles in subpopulations of extracellular vesicles: apoptotic bodies, microvesicles and exosomes. J Extracell Vesicles. 2013; 2: 20677.
   PubMedGoogle Scholar
• Manolova V, Flace A, Bauer M, Schwarz K, Saudan P, Bachmann MF. Nanoparticles target distinct dendritic cell populations according to their size. Eur J Immunol. 2008; 38: 1404–13. [PubMed Abstract].
   Google Scholar
• Lattanzi L, Federico M. A strategy of antigen incorporation into exosomes: comparing cross-presentation levels of antigens delivered by engineered exosomes and by lentiviral virus-like particles. Vaccine. 2012; 30: 7229–37. [PubMed Abstract].
   Google Scholar