Melanoma lesions independently acquire t-cell resistance during metastatic latency

Cancer Research

Volumn 76, Issue 15, 2016, Pages 4347-4358

  Zhao, Fang ^a   Sucker, Antje ^a   Horn, Susanne ^a   Heeke, Christina ^a   Bielefeld, Nicola ^a   Schrörs, Barbara ^b   Bicker, Anne ^b   Lindemann, Monika ^a   Roesch, Alexander ^a   Gaudernack, Gustav ^c   Stiller, Mathias ^a   Becker, Jürgen C ^a   Lennerz, Volker ^b   Wölfel, Thomas ^b   Schadendorf, Dirk ^a   Griewank, Klaus ^a   Paschen, Annette ^a  

^a UNIVERSITY HOSPITAL ESSEN   (Germany)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

^c OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIGEN; CD8 ANTIGEN; HLA ANTIGEN CLASS 1; MICROPHTHALMIA ASSOCIATED TRANSCRIPTION FACTOR; PROTEIN C JUN; TUMOR ANTIGEN; TUMOR PROTEIN;

ANTIGEN EXPRESSION; ANTIGEN SPECIFICITY; ARTICLE; B2M GENE; CANCER RECURRENCE; CANCER RESISTANCE; CANCER STAGING; CD8+ T LYMPHOCYTE; CELL DEDIFFERENTIATION; CHROMOSOME 15Q; CHROMOSOME ABERRATION; CONTROLLED STUDY; EVOLUTION; GENE; GENE DELETION; HAPLOTYPE; HUMAN; HUMAN CELL; IMMUNE DEFICIENCY; IMMUNOGENICITY; IMMUNOPHENOTYPING; MELANOMA CELL; MELANOMA METASTASIS; METASTATIC MELANOMA; MULTIPLE CANCER; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; TUMOR ESCAPE; GENETICS; IMMUNOLOGY; MELANOMA; METASTASIS; PATHOLOGY;

ANTIGENS, NEOPLASM; CD8-POSITIVE T-LYMPHOCYTES; HUMANS; MELANOMA; NEOPLASM METASTASIS; NEOPLASM PROTEINS;

EID: 84982686580     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-16-0008     Document Type: Article

References (50)

1. Rosenberg SA, Yang JC, Sherry RM, Kammula US, Hughes MS, Phan GQ, et al. Durable complete responses in heavily pretreated patients with metastatic melanoma using t-cell transfer immunotherapy. Clin Cancer Res 2011;17:4550-7.
2. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010;363:711-23.
3. Topalian SL, Sznol M, McDermott DF, Kluger HM, Carvajal RD, Sharfman WH, et al. Survival, durable tumor remission, and long-term safety in patients with advanced melanoma receiving nivolumab. J Clin Oncol 2014;32:1020-30.
4. Larkin J, Chiarion-Sileni V, Gonzalez R, Grob JJ, Cowey CL, Lao CD, et al. Combined nivolumab and ipilimumab or monotherapy in untreated melanoma. N Engl J Med 2015;373:23-34.
5. Coulie PG, Van den Eynde BJ, van der Bruggen P, Boon T. Tumour antigens recognized by T lymphocytes: at the core of cancer immunotherapy. Nat Rev Cancer 2014;14:135-46.
6. DuPage M, Cheung AF, Mazumdar C, Winslow MM, Bronson R, Schmidt LM, et al. Endogenous T cell responses to antigens expressed in lung adenocarcinomas delay malignant tumor progression. Cancer Cell 2011;19:72-85.
7. DuPage M, Mazumdar C, Schmidt LM, Cheung AF, Jacks T. Expression of tumour-specific antigens underlies cancer immunoediting. Nature 2012;482:405-9.
8. Matsushita H, Vesely MD, Koboldt DC, Rickert CG, Uppaluri R, Magrini VJ, et al. Cancer exome analysis reveals a T-cell-dependent mechanism of cancer immunoediting. Nature 2012;482:400-4.
9. Mittal D, Gubin MM, Schreiber RD, Smyth MJ. New insights into cancer immunoediting and its three component phases-elimination, equilibrium and escape. Curr Opin Immunol 2014;27:16-25.
10. Eyles J, Puaux AL, Wang X, Toh B, Prakash C, Hong M, et al. Tumor cells disseminate early, but immunosurveillance limits metastatic outgrowth, in a mouse model of melanoma. J Clin Invest 2010;120:2030-9.
11. Koebel CM, Vermi W, Swann JB, Zerafa N, Rodig SJ, Old LJ, et al. Adaptive immunity maintains occult cancer in an equilibrium state. Nature 2007;450:903-7.
12. Ikeda H, Lethe B, Lehmann F, van Baren N, Baurain JF, de Smet C, et al. Characterization of an antigen that is recognized on a melanoma showing partial HLA loss by CTL expressing an NK inhibitory receptor. Immunity 1997;6:199-208.
13. Yamshchikov GV, Mullins DW, Chang CC, Ogino T, Thompson L, Presley J, et al. Sequential immune escape and shifting of T cell responses in a long-term survivor of melanoma. J Immunol 2005;174:6863-71.
14. van de Nes J, Gessi M, Sucker A, Möller I, Stiller M, Horn S, et al. Targeted next generation sequencing reveals unique mutation profile of primary melanocytic tumors of the central nervous system. J Neurooncol 2016;127:435-44.
15. Sucker A, Zhao F, Real B, Heeke C, Bielefeld N, Maßen S, et al. Genetic evolution of T-cell resistance in the course of melanoma progression. Clin Cancer Res 2014;20:6593-604.
16. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 2013;30:2725-9.
17. Robins HS, Campregher PV, Srivastava SK, Wacher A, Turtle CJ, Kahsai O, et al. Comprehensive assessment of T-cell receptor beta-chain diversity in alphabeta T cells. Blood 2009;114:4099-107.
18. Carlson CS, Emerson RO, Sherwood AM, Desmarais C, Chung MW, Parsons JM, et al. Using synthetic templates to design an unbiased multiplex PCR assay. Nat Commun 2013;4:2680.
19. Schwinn N, Vokhminova D, Sucker A, Textor S, Striegel S, Moll I, et al. Interferon-gamma down-regulates NKG2D ligand expression and impairs the NKG2D-mediated cytolysis of MHC class I-deficient melanoma by natural killer cells. Int J Cancer 2009;124:1594-604.
20. Konieczkowski DJ, Johannessen CM, Abudayyeh O, Kim JW, Cooper ZA, Piris A, et al. A melanoma cell state distinction influences sensitivity to MAPK pathway inhibitors. Cancer Discov 2014;4:816-27.
21. Riesenberg S, Groetchen A, Siddaway R, Bald T, Reinhardt J, Smorra D, et al. MITF and c-Jun antagonism interconnects melanoma dedifferentiation with pro-inflammatory cytokine responsiveness and myeloid cell recruitment. Nat Commun 2015;6:8755.
22. Paschen A, Arens N, Sucker A, Greulich-Bode KM, Fonsatti E, Gloghini A, et al. The coincidence of chromosome 15 aberrations and beta2-microglobulin gene mutations is causative for the total loss of human leukocyte antigen class I expression in melanoma. Clin Cancer Res 2006;12:3297-305.
23. Paschen A, Mendez RM, Jimenez P, Sucker A, Ruiz-Cabello F, Song M, et al. Complete loss of HLA class I antigen expression on melanoma cells: a result of successive mutational events. Int J Cancer 2003;103:759-67.
24. Wei F, Zhong S, Ma Z, Kong H, Medvec A, Ahmed R, et al. Strength of PD-1 signaling differentially affects T-cell effector functions. Proc Natl Acad Sci U S A 2013;110:E2480-9.
25. Marzec M, Zhang Q, Goradia A, Raghunath PN, Liu X, Paessler M, et al. Oncogenic kinase NPM/ALK induces through STAT3 expression of immunosuppressive protein CD274 (PD-L1, B7-H1). Proc Natl Acad Sci U S A 2008;105:20852-7.
26. Jiang X, Zhou J, Giobbie-Hurder A, Wargo J, Hodi FS. The activation of MAPK in melanoma cells resistant to BRAF inhibition promotes PD-L1 expression that is reversible by MEK and PI3K inhibition. Clin Cancer Res 2013;19:598-609.
27. Simon S, Vignard V, Florenceau L, Dreno B, Khammari A, Lang F, et al. PD-1 expression conditions T cell avidity within an antigen-specific repertoire. Oncoimmunology 2016;5:e1104448.
28. Taube JM, Anders RA, Young GD, Xu H, Sharma R, McMiller TL, et al. Colocalization of inflammatory response with B7-h1 expression in human melanocytic lesions supports an adaptive resistance mechanism of immune escape. Sci Transl Med 2012;4:127ra137.
29. Paez D, Labonte MJ, Bohanes P, Zhang W, Benhanim L, Ning Y, et al. Cancer dormancy: a model of early dissemination and late cancer recurrence. Clin Cancer Res 2012;18:645-53.
30. Matsushita H, Hosoi A, Ueha S, Abe J, Fujieda N, Tomura M, et al. Cytotoxic T lymphocytes block tumor growth both by lytic activity and IFNgamma-dependent cell-cycle arrest. Cancer Immunol Res 2015;3:26-36.
31. Donia M, Andersen R, Kjeldsen JW, Fagone P, Munir S, Nicoletti F, et al. Aberrant expression of MHC class II in melanoma attracts inflammatory tumor-specific CD4+ T- cells, which dampen CD8+ T-cell antitumor reactivity. Cancer Res 2015;75:3747-59.
32. Kitano S, Tsuji T, Liu C, Hirschhorn-Cymerman D, Kyi C, Mu Z, et al. Enhancement of tumor-reactive cytotoxic CD4+ T cell responses after ipilimumab treatment in four advanced melanoma patients. Cancer Immunol Res 2013;1:235-44.
33. Quezada SA, Simpson TR, Peggs KS, Merghoub T, Vider J, Fan X, et al. Tumor-reactive CD4(+) T cells develop cytotoxic activity and eradicate large established melanoma after transfer into lymphopenic hosts. J Exp Med 2010;207:637-50.
34. Qin Z, Blankenstein T. CD4+ T cell-mediated tumor rejection involves inhibition of angiogenesis that is dependent on IFN gamma receptor expression by nonhematopoietic cells. Immunity 2000;12:677-86.
35. Braumuller H, Wieder T, Brenner E, Aßmann S, Hahn M, Alkhaled M, et al. T-helper-1-cell cytokines drive cancer into senescence. Nature 2013;494:361-365.
36. Knight DA, Ngiow SF, Li M, Parmenter T, Mok S, Cass A, et al. Host immunity contributes to the anti-melanoma activity of BRAF inhibitors. J Clin Invest 2013;123:1371-81.
37. Ferrari de Andrade L, Ngiow SF, Stannard K, Rusakiewicz S, Kalimutho M, Khanna KK, et al. Natural killer cells are essential for the ability of BRAF inhibitors to control BRAFV600E-mutant metastatic melanoma. Cancer Res 2014;74:7298-308.
38. Ni J, Miller M, Stojanovic A, Garbi N, Cerwenka A. Sustained effector function of IL-12/15/18-preactivated NK cells against established tumors. J Exp Med 2012;209:2351-65.
39. Zamarin D, Holmgaard RB, Subudhi SK, Park JS, Mansour M, Palese P, et al. Localized oncolytic virotherapy overcomes systemic tumor resistance to immune checkpoint blockade immunotherapy. Sci Transl Med 2014;6:226ra232.
40. Spiotto MT, Rowley DA, Schreiber H. Bystander elimination of antigen loss variants in established tumors. Nat Med 2004;10:294-8.
41. Zhang B, Bowerman NA, Salama JK, Schmidt H, Spiotto MT, Schietinger A, et al. Induced sensitization of tumor stroma leads to eradication of established cancer by T cells. J Exp Med 2007;204:49-55.
42. Zhang B, Karrison T, Rowley DA, Schreiber H. IFN-gamma- and TNF-dependent bystander eradication of antigen-loss variants in established mouse cancers. J Clin Invest 2008;118:1398-404.
43. Gotter J, Brors B, Hergenhahn M, Kyewski B. Medullary epithelial cells of the human thymus express a highly diverse selection of tissue-specific genes colocalized in chromosomal clusters. J Exp Med 2004;199:155-66.
44. Duan F, Lin Y, Liu C, Engelhorn ME, Cohen AD, Curran M, et al. Immune rejection of mouse tumors expressing mutated self. Cancer Res 2009;69:3545-53.
45. Mendez R, Serrano A, Jager E, Maleno I, Ruiz-Cabello F, Knuth A, et al. Analysis of HLA class I expression in different metastases from two melanoma patients undergoing peptide immunotherapy. Tissue Antigens 2001;57:508-19.
46. Mendez R, Ruiz-Cabello F, Rodriguez T, Del Campo A, Paschen A, Schadendorf D, et al. Identification of different tumor escape mechanisms in several metastases from a melanoma patient undergoing immunotherapy. Cancer Immunol Immunother 2007;56:88-94.
47. Rooney MS, Shukla SA, Wu CJ, Getz G, Hacohen N. Molecular and genetic properties of tumors associated with local immune cytolytic activity. Cell 2015;160:48-61.
48. Sensi M, Catani M, Castellano G, Nicolini G, Alciato F, Tragni G, et al. Human cutaneous melanomas lacking MITF and melanocyte differentiation antigens express a functional Axl receptor kinase. J Invest Dermatol 2011;131:2448-57.
49. Zhang J, Patel L, Pienta KJ. Targeting chemokine (C-C motif) ligand 2 (CCL2) as an example of translation of cancer molecular biology to the clinic. Prog Mol Biol Transl Sci 2010;95:31-53.
50. Hugo W, Zaretsky JM, Sun L, Song C, Moreno BH, Hu-Lieskovan S, et al. Genomic and transcriptomic features of response to anti-PD-1 therapy in metastatic melanoma. Cell 2016;165:35-44.