Antigen-delivery through invariant chain (CD74) boosts CD8 and CD4 T cell immunity

References

• Shang N, Figini M, Shangguan J, Wang B, Sun C, Pan L, Ma Q, Zhang Z. Dendritic cells based immunotherapy. Am J Cancer Res. 2017;7(10):2091–2102.
   PubMed Web of Science ®Google Scholar
• Garg AD, Coulie PG, Van Den Eynde BJ, Agostinis P. Integrating next-generation dendritic cell vaccines into the current cancer immunotherapy landscape. Trends Immunol. 2017;38(8):577–593. doi:10.1016/j.it.2017.05.006.
   PubMed Web of Science ®Google Scholar
• Garg AD, Vara Perez M, Schaaf M, Agostinis P, Zitvogel L, Kroemer G, Galluzzi L. Trial watch: dendritic cell-based anticancer immunotherapy. Oncoimmunology. 2017;6(7):e1328341. doi:10.1080/2162402X.2017.1328341.
   PubMed Web of Science ®Google Scholar
• Slingluff CL, Petroni GR, Chianese-Bullock KA, Smolkin ME, Hibbitts S, Murphy C, Johansen N, Grosh WW, Yamshchikov GV, Neese PY, et al. Immunologic and clinical outcomes of a randomized phase II trial of two multipeptide vaccines for melanoma in the adjuvant setting. Clin Cancer Res. 2007;13(21):6386–6395. doi:10.1158/1078-0432.CCR-07-0486.
   PubMed Web of Science ®Google Scholar
• Slingluff CL, Petroni GR, Chianese-Bullock KA, Smolkin ME, Ross MI, Haas NB, von Mehren M, Grosh WW. Randomized multicenter trial of the effects of Melanoma-associated helper peptides and cyclophosphamide on the immunogenicity of a multipeptide Melanoma vaccine. J Clin Oncol. 2011;29(21):2924–2932. doi:10.1200/JCO.2010.33.8053.
   PubMed Web of Science ®Google Scholar
• Kreiter S, Vormehr M, van de Roemer N, Diken M, Lower M, Diekmann J, Boegel S, Schrors 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.
   PubMed Web of Science ®Google Scholar
• Sahin U, Derhovanessian E, Miller M, Kloke BP, Simon P, Lower M, Bukur V, Tadmor AD, Luxemburger U, Schrors B, et al. Personalized RNA mutanome vaccines mobilize poly-specific therapeutic immunity against cancer. Nature. 2017;547(7662):222–226. doi:10.1038/nature23003.
   PubMed Web of Science ®Google Scholar
• Bristol JA, Orsini C, Lindinger P, Thalhamer J, Abrams SI. Identification of a ras oncogene peptide that contains both CD4(+) and CD8(+) T cell epitopes in a nested configuration and elicits both T cell subset responses by peptide or DNA immunization. Cell Immunol. 2000;205(2):73–83. doi:10.1006/cimm.2000.1712.
   PubMed Web of Science ®Google Scholar
• Aubert RD, Kamphorst AO, Sarkar S, Vezys V, Ha SJ, Barber DL, Ye L, Sharpe AH, Freeman GJ, Ahmed R. Antigen-specific CD4 T-cell help rescues exhausted CD8 T cells during chronic viral infection. Proc Natl Acad Sci USA. 2011;108(52):21182–21187. doi:10.1073/pnas.1118450109.
   PubMed Web of Science ®Google Scholar
• Neefjes J, Jongsma MLM, Paul P, Bakke O. Towards a systems understanding of MHC class I and MHC class II antigen presentation. Nat Rev Immunol. 2011;11(12):823–836. doi:10.1038/nri3084.
   PubMed Web of Science ®Google Scholar
• Blum JS, Wearsch PA, Cresswell P. Pathways of antigen processing. Annu Rev Immunol. 2013;31(1):443–473. doi:10.1146/annurev-immunol-032712-095910.
   PubMed Web of Science ®Google Scholar
• Cruz FM, Colbert JD, Merino E, Kriegsman BA, Rock KL. The biology and underlying mechanisms of cross-presentation of exogenous antigens on MHC-I molecules. Annu Rev Immunol. 2017;35:149–176. doi:10.1146/annurev-immunol-041015-055254.
   PubMed Web of Science ®Google Scholar
• Mellins ED, Stern LJ. HLA-DM and HLA-DO, key regulators of MHC-II processing and presentation. Curr Opin Immunol. 2014;26:115–122. doi:10.1016/j.coi.2013.11.005.
   PubMed Web of Science ®Google Scholar
• Kreiter S, Selmi A, Diken M, Sebastian M, Osterloh P, Schild H, Huber C, Tureci O, Sahin U. Increased antigen presentation efficiency by coupling antigens to MHC class I trafficking signals. J Immunol. 2008;180(1):309–318. doi:10.4049/jimmunol.180.1.309.
   PubMed Web of Science ®Google Scholar
• Holtkamp S, Kreiter S, Selmi A, Simon P, Koslowski M, Huber C, Tureci O, Sahin U. Modification of antigen-encoding RNA increases stability, translational efficacy, and T-cell stimulatory capacity of dendritic cells. Blood. 2006;108(13):4009–4017. doi:10.1182/blood-2006-04-015024.
   PubMed Web of Science ®Google Scholar
• Gregers TF, Fleckenstein B, Vartdal F, Roepstorff P, Bakke O, Sandlie I. MHC class II loading of high or low affinity peptides directed by Ii/peptide fusion constructs: implications for T cell activation. Int Immunol. 2003;15(11):1291–1299.
   PubMed Web of Science ®Google Scholar
• Malcherek G, Wirblich C, Willcox N, Rammensee HG, Trowsdale J, Melms A. MHC class II-associated invariant chain peptide replacement by T cell epitopes: engineered invariant chain as a vehicle for directed and enhanced MHC class II antigen processing and presentation. Eur J Immunol. 1998;28(5):1524–1533. doi:10.1002/(SICI)1521-4141(199805)28:05<1524::AID-IMMU1524>3.0.CO;2-T.
   PubMed Web of Science ®Google Scholar
• Fujii S, Senju S, Chen YZ, Ando M, Matsushita S, Nishimura Y. The CLIP-substituted invariant chain efficiently targets an antigenic peptide to HLA class II pathway in L cells. Hum Immunol. 1998;59(10):607–614.
   PubMed Web of Science ®Google Scholar
• Carstens C, Newman DK, Bohlen H, Konig A, Koch N. Invariant chains with the class II binding site replaced by a sequence from influenza virus matrix protein constrain low-affinity sequences to MHC II presentation. Int Immunol. 2000;12(11):1561–1568.
   PubMed Web of Science ®Google Scholar
• Vigna JL, Smith KD, Lutz CT. Invariant chain association with MHC class I: preference for HLA class I/beta 2-microglobulin heterodimers, specificity, and influence of the MHC peptide-binding groove. J Immunol. 1996;157(10):4503–4510.
   PubMed Web of Science ®Google Scholar
• Powis SJ. CLIP-region mediated interaction of invariant chain with MHC class I molecules. FEBS Lett. 2006;580(13):3112–3116. doi:10.1016/j.febslet.2006.04.060.
   PubMed Web of Science ®Google Scholar
• Basha G, Omilusik K, Chavez-Steenbock A, Reinicke AT, Lack N, Choi KB, Jefferies WA. A CD74-dependent MHC class I endolysosomal cross-presentation pathway. Nat Immunol. 2012;13(3):237–245. doi:10.1038/ni.2225.
   PubMed Web of Science ®Google Scholar
• Walchli S, Kumari S, Fallang L-E-E, Sand KMKM, Yang W, Landsverk OJBJ, Bakke O, Olweus J, Gregers TFF. Invariant chain as a vehicle to load antigenic peptides on human MHC class I for cytotoxic T-cell activation. 2014;44(3):774–784. doi:10.1002/eji.201343671.
   Google Scholar
• Saeterdal I, Gjertsen MK, Straten P, Eriksen JA, Gaudernack G. A TGF betaRII frameshift-mutation-derived CTL epitope recognised by HLA-A2-restricted CD8+ T cells. Cancer Immunol Immunother. 2001;50(9):469–476. doi:10.1007/s002620100222.
   PubMed Web of Science ®Google Scholar
• Inderberg EM, Wälchli S, Myhre MR, Trachsel S, Almåsbak H, Kvalheim G, Gaudernack G. T cell therapy targeting a public neoantigen in microsatellite instable colon cancer reduces in vivo tumor growth. Oncoimmunology. 2017;6(4):e1302631. doi:10.1080/2162402X.2017.1302631.
   PubMed Web of Science ®Google Scholar
• Saeterdal I, Bjorheim J, Lislerud K, Gjertsen MK, Bukholm IK, Olsen OC, Nesland JM, Eriksen JA, Moller M, Lindblom A, et al. Frameshift-mutation-derived peptides as tumor-specific antigens in inherited and spontaneous colorectal cancer. Proc Natl Acad Sci USA. 2001;98(23):13255–13260. doi:10.1073/pnas.231326898.
   PubMed Web of Science ®Google Scholar
• Linnebacher M, Gebert J, Rudy W, Woerner S, Yuan YP, Bork P, von Knebel Doeberitz M. Frameshift peptide-derived T-cell epitopes: a source of novel tumor-specific antigens. Int J Cancer. 2001;93(1):6–11. doi:10.1002/(ISSN)1097-0215.
   PubMed Web of Science ®Google Scholar
• Yu YY, Netuschil N, Lybarger L, Connolly JM, Hansen TH. Cutting edge: single-chain trimers of MHC class I molecules form stable structures that potently stimulate antigen-specific T cells and B cells. J Immunol. 2002;168(7):3145–3149. doi:10.4049/jimmunol.168.7.3145.
   PubMed Web of Science ®Google Scholar
• Bremnes B, Madsen T, Gedde-Dahl M, Bakke O. An LI and ML motif in the cytoplasmic tail of the MHC-associated invariant chain mediate rapid internalization. J Cell Sci. 1994;107(Pt 7):2021–2032.
   PubMedGoogle Scholar
• Van Tendeloo VF, Ponsaerts P, Lardon F, Nijs G, Lenjou M, Van Broeckhoven C, Van Bockstaele DR, Berneman ZN. Highly efficient gene delivery by mRNA electroporation in human hematopoietic cells: superiority to lipofection and passive pulsing of mRNA and to electroporation of plasmid cDNA for tumor antigen loading of dendritic cells. Blood. 2001;98(1):49–56.
   PubMed Web of Science ®Google Scholar
• Mahvi DM, Sondel PM, Yang N-S, Albertini MR, Schiller JH, Hank J, Heiner J, Gan J, Swain W, Logrono R. Phase I/IB study of immunization with autologous tumor cells transfected with the GM-CSF gene by particle-mediated transfer in patients with Melanoma or Sarcoma University of Wisconsin, Madison, Wisconsin. Hum Gene Ther. 1997;8(7):875–891. doi:10.1089/hum.1997.8.7-875.
   PubMed Web of Science ®Google Scholar
• Lopes L, Fletcher K, Ikeda Y, Collins M. Lentiviral vector expression of tumour antigens in dendritic cells as an immunotherapeutic strategy. Cancer Immunol Immunother. 2006;55(8):1011–1016. doi:10.1007/s00262-005-0095-5.
   PubMed Web of Science ®Google Scholar
• Aurisicchio L, Fridman A, Bagchi A, Scarselli E, La Monica N, Ciliberto G. A novel minigene scaffold for therapeutic cancer vaccines. Oncoimmunology. 2014;3(1):e27529. doi:10.4161/onci.27529.
   PubMed Web of Science ®Google Scholar
• Wagner CS, Cresswell P. TLR and nucleotide-binding oligomerization domain-like receptor signals differentially regulate exogenous antigen presentation. J Immunol. 2012;188(2):686–693. doi:10.4049/jimmunol.1102214.
   PubMed Web of Science ®Google Scholar
• Gil-Torregrosa BC, Lennon-Duménil AM, Kessler B, Guermonprez P, Ploegh HL, Fruci D, van Endert P, Amigorena S. Control of cross-presentation during dendritic cell maturation. Eur J Immunol. 2004;34(2):398–407. doi:10.1002/eji.200324508.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Borst J, Ahrends T, Bąbała N, Melief CJM, Kastenmüller 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.
   PubMed Web of Science ®Google Scholar
• Schietinger A, Philip M, Liu RB, Schreiber K, Schreiber H. Bystander killing of cancer requires the cooperation of CD4 + and CD8 + T cells during the effector phase. J Exp Med. 2010;207(11):2469–2477. doi:10.1084/jem.20092450.
   PubMed Web of Science ®Google Scholar
• Di Genova G, Savelyeva N, Suchacki A, Thirdborough SM, Stevenson FK. Bystander stimulation of activated CD4 + T cells of unrelated specificity following a booster vaccination with tetanus toxoid. Eur J Immunol. 2010;40(4):976–985. doi:10.1002/eji.200940017.
   PubMed Web of Science ®Google Scholar
• Bos R, Sherman LA. CD4+ T-cell help in the tumor milieu is required for recruitment and cytolytic function of CD8+ T lymphocytes. Cancer Res. 2010;70(21):8368–8377. doi:10.1158/0008-5472.CAN-10-1322.
   PubMed Web of Science ®Google Scholar
• Mathur D, Prakash S, Anand P, Kaur H, Agrawal P, Mehta A, Kumar R, Singh S, Raghava GPS. PEPlife: a repository of the half-life of peptides. Sci Rep. 2016;6(1):36617. doi:10.1038/srep36617.
   PubMedGoogle Scholar
• Moynihan KD, Holden RL, Mehta NK, Wang C, Karver MR, Dinter J, Liang S, Abraham W, Melo MB, Zhang AQ, et al. Enhancement of peptide vaccine immunogenicity by increasing lymphatic drainage and boosting serum stability. Cancer Immunol Res. 2018 Jun 18:canimm.0607.2017. doi:10.1158/2326-6066.CIR-17-0607.
   PubMed Web of Science ®Google Scholar
• Roche PA, Teletski CL, Stang E, Bakke O, Long EO. Cell surface HLA-DR-invariant chain complexes are targeted to endosomes by rapid internalization. Proc Natl Acad Sci USA. 1993;90(18):8581–8585. doi:10.1073/pnas.90.18.8581.
   PubMed Web of Science ®Google Scholar
• Armstrong TD, Clements VK, Martin BK, Ting JP, Ostrand-Rosenberg S. Major histocompatibility complex class II-transfected tumor cells present endogenous antigen and are potent inducers of tumor-specific immunity. Proc Natl Acad Sci USA. 1997;94(13):6886–6891. doi:10.1073/PNAS.94.13.6886.
   PubMed Web of Science ®Google Scholar
• Dasari V, Rehan S, Tey S-K, Smyth MJ, Smith C, Khanna R. Autophagy and proteasome interconnect to coordinate cross-presentation through MHC class I pathway in B cells. Immunol Cell Biol. 2016;94(10):964–974. doi:10.1038/icb.2016.59.
   PubMed Web of Science ®Google Scholar
• Walseng E, Wälchli S, Fallang L-E, Yang W, Vefferstad A, Areffard A, Olweus J. Soluble T-cell receptors produced in human cells for targeted delivery. PLoS One. 2015;10(4). doi:10.1371/journal.pone.0119559.
   PubMed Web of Science ®Google Scholar
• Parkhurst MR, Joo J, Riley JP, Yu Z, Li Y, Robbins PF, Rosenberg SA. Characterization of genetically modified T-cell receptors that recognize the CEA:691-699 peptide in the context of HLA-A2.1 on human colorectal cancer cells. Clin Cancer Res. 2009;15(1):169–180. doi:10.1158/1078-0432.CCR-08-1638.
   PubMed Web of Science ®Google Scholar
• Walchli S, Loset GA, Kumari S, Johansen JN, Yang W, Sandlie I, Olweus J. A practical approach to T-cell receptor cloning and expression. PLoS One. 2011;6(11):e27930. doi:10.1371/journal.pone.0027930.
   PubMed Web of Science ®Google Scholar