Tailored Tumor Immunogenicity Reveals Regulation of CD4 and CD8 T Cell Responses against Cancer

Cell Reports

Volumn 17, Issue 9, 2016, Pages 2234-2246

  Knocke, Sarah ^a   Fleischmann Mundt, Bettina ^a   Saborowski, Michael ^a   Manns, Michael P ^a   Kühnel, Florian ^a   Wirth, Thomas C ^a   Woller, Norman ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

cancer immunosurveillance; cancer mouse model; CD4 T cells; CD8 T cells; immune responses to cancer; immunoediting; neoepitopes; oncogenic ras; senescence surveillance; T cell regulation

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; TUMOR ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CANCER SURVIVAL; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; ENZYME LINKED IMMUNOSPOT ASSAY; FLOW CYTOMETRY; HISTOLOGY; IMMUNE SYSTEM; IMMUNOGENICITY; IMMUNOHISTOCHEMISTRY; LIVER CANCER; MOUSE; NONHUMAN; PLASMID; PRIORITY JOURNAL; TRANSPOSON; TUMOR GROWTH; TUMOR IMMUNITY; ANIMAL; C57BL MOUSE; CARCINOGENESIS; CYTOTOXIC T LYMPHOCYTE; CYTOTOXICITY; GENE; IMMUNOLOGY; IMMUNOSURVEILLANCE; NEOPLASM; ONCOGENE RAS; PATHOLOGY; SURVIVAL ANALYSIS; TH1 CELL;

ANIMALS; ANTIGENS, NEOPLASM; CARCINOGENESIS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CYTOTOXICITY, IMMUNOLOGIC; GENES, MHC CLASS I; GENES, RAS; IMMUNOLOGIC SURVEILLANCE; MICE, INBRED C57BL; NEOPLASMS; SURVIVAL ANALYSIS; T-LYMPHOCYTES, CYTOTOXIC; TH1 CELLS;

EID: 84996791595     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.10.086     Document Type: Article

References (33)

1. Brinkhoff, B., Ostroumov, D., Heemcke, J., Woller, N., Gürlevik, E., Manns, M.P., Longerich, T., Zender, L., Harty, J.T., Kubicka, S., et al. Microsphere priming facilitates induction of potent therapeutic T-cell immune responses against autochthonous liver cancers. Eur. J. Immunol. 44 (2014), 1213–1224.
2. Carlson, C.M., Frandsen, J.L., Kirchhof, N., McIvor, R.S., Largaespada, D.A., Somatic integration of an oncogene-harboring Sleeping Beauty transposon models liver tumor development in the mouse. Proc. Natl. Acad. Sci. USA 102 (2005), 17059–17064.
3. Castle, J.C., Kreiter, S., Diekmann, J., Löwer, 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. 72 (2012), 1081–1091.
4. Chang, E.H., Furth, M.E., Scolnick, E.M., Lowy, D.R., Tumorigenic transformation of mammalian cells induced by a normal human gene homologous to the oncogene of Harvey murine sarcoma virus. Nature 297 (1982), 479–483.
5. Dunn, G.P., Old, L.J., Schreiber, R.D., The three Es of cancer immunoediting. Annu. Rev. Immunol. 22 (2004), 329–360.
6. DuPage, M., Mazumdar, C., Schmidt, L.M., Cheung, A.F., Jacks, T., Expression of tumour-specific antigens underlies cancer immunoediting. Nature 482 (2012), 405–409.
7. Friedman, K.M., Prieto, P.A., Devillier, L.E., Gross, C.A., Yang, J.C., Wunderlich, J.R., Rosenberg, S.A., Dudley, M.E., Tumor-specific CD4+ melanoma tumor-infiltrating lymphocytes. J. Immunother. 35 (2012), 400–408.
8. Galon, J., Costes, A., Sanchez-Cabo, F., Kirilovsky, A., Mlecnik, B., Lagorce-Pagès, C., Tosolini, M., Camus, M., Berger, A., Wind, P., et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 313 (2006), 1960–1964.
9. Gubin, M.M., Zhang, X., Schuster, H., Caron, E., Ward, J.P., Noguchi, T., Ivanova, Y., Hundal, J., Arthur, C.D., Krebber, W.J., et al. Checkpoint blockade cancer immunotherapy targets tumour-specific mutant antigens. Nature 515 (2014), 577–581.
10. Kamijo, T., Zindy, F., Roussel, M.F., Quelle, D.E., Downing, J.R., Ashmun, R.A., Grosveld, G., Sherr, C.J., Tumor suppression at the mouse INK4a locus mediated by the alternative reading frame product p19ARF. Cell 91 (1997), 649–659.
11. Kang, T.W., Yevsa, T., Woller, N., Hoenicke, L., Wuestefeld, T., Dauch, D., Hohmeyer, A., Gereke, M., Rudalska, R., Potapova, A., et al. Senescence surveillance of pre-malignant hepatocytes limits liver cancer development. Nature 479 (2011), 547–551.
12. Koebel, C.M., Vermi, W., Swann, J.B., Zerafa, N., Rodig, S.J., Old, L.J., Smyth, M.J., Schreiber, R.D., Adaptive immunity maintains occult cancer in an equilibrium state. Nature 450 (2007), 903–907.
13. Kreiter, S., Vormehr, M., van de Roemer, N., Diken, M., Löwer, M., Diekmann, J., Boegel, S., Schrörs, B., Vascotto, F., Castle, J.C., et al. Mutant MHC class II epitopes drive therapeutic immune responses to cancer. Nature 520 (2015), 692–696.
14. Kuilman, T., Michaloglou, C., Vredeveld, L.C., Douma, S., van Doorn, R., Desmet, C.J., Aarden, L.A., Mooi, W.J., Peeper, D.S., Oncogene-induced senescence relayed by an interleukin-dependent inflammatory network. Cell 133 (2008), 1019–1031.
15. Lennerz, V., Fatho, M., Gentilini, C., Frye, R.A., Lifke, A., Ferel, D., Wölfel, C., Huber, C., Wölfel, T., The response of autologous T cells to a human melanoma is dominated by mutated neoantigens. Proc. Natl. Acad. Sci. USA 102 (2005), 16013–16018.
16. Linnemann, C., van Buuren, M.M., Bies, L., Verdegaal, E.M., Schotte, R., Calis, J.J., Behjati, S., Velds, A., Hilkmann, H., Atmioui, D.E., et al. High-throughput epitope discovery reveals frequent recognition of neo-antigens by CD4+ T cells in human melanoma. Nat. Med. 21 (2015), 81–85.
17. Lowe, S.W., Cepero, E., Evan, G., Intrinsic tumour suppression. Nature 432 (2004), 307–315.
18. Maker, A.V., Phan, G.Q., Attia, P., Yang, J.C., Sherry, R.M., Topalian, S.L., Kammula, U.S., Royal, R.E., Haworth, L.R., Levy, C., et al. Tumor regression and autoimmunity in patients treated with cytotoxic T lymphocyte-associated antigen 4 blockade and interleukin 2: a phase I/II study. Ann. Surg. Oncol. 12 (2005), 1005–1016.
19. Matsushita, H., Vesely, M.D., Koboldt, D.C., Rickert, C.G., Uppaluri, R., Magrini, V.J., Arthur, C.D., White, J.M., Chen, Y.S., Shea, L.K., et al. Cancer exome analysis reveals a T-cell-dependent mechanism of cancer immunoediting. Nature 482 (2012), 400–404.
20. McKelvey, T., Tang, A., Bett, A.J., Casimiro, D.R., Chastain, M., T-cell response to adenovirus hexon and DNA-binding protein in mice. Gene Ther. 11 (2004), 791–796.
21. Mittal, D., Gubin, M.M., Schreiber, R.D., Smyth, M.J., New insights into cancer immunoediting and its three component phases–elimination, equilibrium and escape. Curr. Opin. Immunol. 27 (2014), 16–25.
22. O'Sullivan, T., Saddawi-Konefka, R., Vermi, W., Koebel, C.M., Arthur, C., White, J.M., Uppaluri, R., Andrews, D.M., Ngiow, S.F., Teng, M.W., et al. Cancer immunoediting by the innate immune system in the absence of adaptive immunity. J. Exp. Med. 209 (2012), 1869–1882.
23. Ossendorp, F., Mengedé, E., Camps, M., Filius, R., Melief, C.J., Specific T helper cell requirement for optimal induction of cytotoxic T lymphocytes against major histocompatibility complex class II negative tumors. J. Exp. Med. 187 (1998), 693–702.
24. Penaloza-MacMaster, P., Barber, D.L., Wherry, E.J., Provine, N.M., Teigler, J.E., Parenteau, L., Blackmore, S., Borducchi, E.N., Larocca, R.A., Yates, K.B., et al. Vaccine-elicited CD4 T cells induce immunopathology after chronic LCMV infection. Science 347 (2015), 278–282.
25. Pomerantz, J., Schreiber-Agus, N., Liégeois, N.J., Silverman, A., Alland, L., Chin, L., Potes, J., Chen, K., Orlow, I., Lee, H.W., et al. The Ink4a tumor suppressor gene product, p19Arf, interacts with MDM2 and neutralizes MDM2's inhibition of p53. Cell 92 (1998), 713–723.
26. Schreiber, R.D., Old, L.J., Smyth, M.J., Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science 331 (2011), 1565–1570.
27. Shankaran, V., Ikeda, H., Bruce, A.T., White, J.M., Swanson, P.E., Old, L.J., Schreiber, R.D., IFNgamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 410 (2001), 1107–1111.
28. Topalian, S.L., Hodi, F.S., Brahmer, J.R., Gettinger, S.N., Smith, D.C., McDermott, D.F., Powderly, J.D., Carvajal, R.D., Sosman, J.A., Atkins, M.B., et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N. Engl. J. Med. 366 (2012), 2443–2454.
29. Tran, E., Turcotte, S., Gros, A., Robbins, P.F., Lu, Y.C., Dudley, M.E., Wunderlich, J.R., Somerville, R.P., Hogan, K., Hinrichs, C.S., et al. Cancer immunotherapy based on mutation-specific CD4+ T cells in a patient with epithelial cancer. Science 344 (2014), 641–645.
30. van Rooij, N., van Buuren, M.M., Philips, D., Velds, A., Toebes, M., Heemskerk, B., van Dijk, L.J., Behjati, S., Hilkmann, H., El Atmioui, D., et al. Tumor exome analysis reveals neoantigen-specific T-cell reactivity in an ipilimumab-responsive melanoma. J. Clin. Oncol. 31 (2013), e439–e442.
31. Warne, P.H., Viciana, P.R., Downward, J., Direct interaction of Ras and the amino-terminal region of Raf-1 in vitro. Nature 364 (1993), 352–355.
32. Woller, N., Knocke, S., Mundt, B., Gürlevik, E., Strüver, N., Kloos, A., Boozari, B., Schache, P., Manns, M.P., Malek, N.P., et al. Virus-induced tumor inflammation facilitates effective DC cancer immunotherapy in a Treg-dependent manner in mice. J. Clin. Invest. 121 (2011), 2570–2582.
33. Woller, N., Gürlevik, E., Fleischmann-Mundt, B., Schumacher, A., Knocke, S., Kloos, A.M., Saborowski, M., Geffers, R., Manns, M.P., Wirth, T.C., et al. Viral infection of tumors overcomes resistance to PD-1-immunotherapy by broadening neoantigenome-directed T-cell responses. Mol. Ther. 23 (2015), 1630–1640.