Up-regulation of PD-L1, IDO, and Tregs in the melanoma tumor microenvironment is driven by CD8+ T cells

Science Translational Medicine

Volumn 5, Issue 200, 2013, Pages

  Spranger, Stefani ^a   Spaapen, Robbert M ^a   Zha, Yuanyuan ^a   Williams, Jason ^a   Meng, Yuru ^a   Ha, Thanh T ^a   Gajewski, Thomas F ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CHEMOKINE RECEPTOR CCR4; GAMMA INTERFERON; INDOLEAMINE 2,3 DIOXYGENASE; PD L1 PROTEIN; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; CANCER CELL; CANCER IMMUNOTHERAPY; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE DEFICIENCY; IMMUNE SYSTEM; INFLAMMATION; LYMPHOCYTE PROLIFERATION; LYMPHOCYTIC INFILTRATION; MELANOMA; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; REVIEW; T LYMPHOCYTE SUBPOPULATION; TUMOR MICROENVIRONMENT; UPREGULATION;

ANIMALS; ANTIGENS, CD274; CD8-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; CHEMOKINES; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; INTERFERON-GAMMA; LYMPHOCYTE ACTIVATION; MELANOMA; MELANOMA, EXPERIMENTAL; MICE; NEOPLASM METASTASIS; T-LYMPHOCYTES, REGULATORY; TUMOR MICROENVIRONMENT; UP-REGULATION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84883863501     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3006504     Document Type: Review

References (50)

1. M. B. Atkins, L. Kunkel, M. Sznol, S. A. Rosenberg, High-dose recombinant interleukin-2 therapy in patients with metastatic melanoma: Long-term survival update. Cancer J. Sci. Am. 6 (Suppl. 1), S11-S14 (2000).
2. A. C. Peterson, H. Harlin, T. F. Gajewski, Immunization with Melan-A peptide-pulsed peripheral blood mononuclear cells plus recombinant human interleukin-12 induces clinical activity and T-cell responses in advanced melanoma. J. Clin. Oncol. 21, 2342-2348 (2003).
3. T. Tanimoto, A. Hori, M. Kami, Sipuleucel-T immunotherapy for castration-resistant prostate cancer. N. Engl. J. Med. 363, 1966 (2010).
4. F. S. Hodi, S. J. O'Day, D. F. McDermott, R. W. Weber, J. A. Sosman, J. B. Haanen, R. Gonzalez, C. Robert, D. Schadendorf, J. C. Hassel, W. Akerley, A. J. van den Eertwegh, J. Lutzky, P. Lorigan, J.M. Vaubel, G. P. Linette, D. Hogg, C. H. Ottensmeier, C. Lebbé, C. Peschel, I. Quirt, J. I. Clark, J. D. Wolchok, J. S. Weber, J. Tian, M. J. Yellin, G. M. Nichol, A. Hoos, W. J. Urba, Improved survival with ipilimumab in patients with metastatic melanoma. N. Engl. J. Med. 363, 711-723 (2010).
5. T. F. Gajewski, Y. Meng, H. Harlin, Immune suppression in the tumor microenvironment. J. Immunother. 29, 233-240 (2006).
6. J. Kline, I. E. Brown, Y. Y. Zha, C. Blank, J. Strickler, H. Wouters, L. Zhang, T. F. Gajewski, Homeostatic proliferation plus regulatory T-cell depletion promotes potent rejection of B16 melanoma. Clin. Cancer Res. 14, 3156-3167 (2008).
7. C. Uyttenhove, L. Pilotte, I. Théate, V. Stroobant, D. Colau, N. Parmentier, T. Boon, B. J. Van den Eynde, Evidence for a tumoral immune resistance mechanism based on tryptophan degradation by indoleamine 2,3-dioxygenase. Nat. Med. 9, 1269-1274 (2003).
8. H. Dong, L. Chen, B7-H1 pathway and its role in the evasion of tumor immunity. J. Mol. Med. 81, 281-287 (2003).
9. + T cells. Cancer Res. 64, 1140-1145 (2004).
10. J. R. Brahmer, C. G. Drake, I. Wollner, J. D. Powderly, J. Picus, W. H. Sharfman, E. Stankevich, A. Pons, T. M. Salay, T. L. McMiller, M. M. Gilson, C. Wang, M. Selby, J. M. Taube, R. Anders, L. Chen, A. J. Korman, D. M. Pardoll, I. Lowy, S. L. Topalian, Phase I study of single-agent anti-programmed death-1 (MDX-1106) in refractory solid tumors: Safety, clinical activity, pharmacodynamics, and immunologic correlates. J. Clin. Oncol. 28, 3167-3175 (2010).
11. S. L. Topalian, F. S. Hodi, J. R. Brahmer, S. N. Gettinger, D. C. Smith, D. F. McDermott, J. D. Powderly, R. D. Carvajal, J. A. Sosman, M. B. Atkins, P. D. Leming, D. R. Spigel, S. J. Antonia, L. Horn, C. G. Drake, D. M. Pardoll, L. Chen, W. H. Sharfman, R. A. Anders, J. M. Taube, T. L. McMiller, H. Xu, A. J. Korman, M. Jure-Kunkel, S. Agrawal, D. McDonald, G. D. Kollia, A. Gupta, J. M. Wigginton, M. Sznol, Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N. Engl. J. Med. 366, 2443-2454 (2012).
12. M. A. Rasku, A. L. Clem, S. Telang, B. Taft, K. Gettings, H. Gragg, D. Cramer, S. C. Lear, K. M. McMasters, D. M. Miller, J. Chesney, Transient T cell depletion causes regression of melanoma metastases. J. Transl. Med. 6, 12 (2008).
13. + T-cell recruitment. Cancer Res. 69, 3077-3085 (2009).
14. T. F. Gajewski, J. Louahed, V. G. Brichard, Gene signature in melanoma associated with clinical activity: A potential clue to unlock cancer immunotherapy. Cancer J. 16, 399-403 (2010).
15. J. L. Messina, D. A. Fenstermacher, S. Eschrich, X. Qu, A. E. Berglund, M. C. Lloyd, M. J. Schell, V. K. Sondak, J. S. Weber, J. J. Mulé, 12-Chemokine gene signature identifies lymph nodelike structures in melanoma: Potential for patient selection for immunotherapy? Sci. Rep. 2, 765 (2012).
16. G. Erdag, J. T. Schaefer, M. E. Smolkin, D. H. Deacon, S. M. Shea, L. T. Dengel, J. W. Patterson, C. L. Slingluff Jr., Immunotype and immunohistologic characteristics of tumor-infiltrating immune cells are associated with clinical outcome in metastatic melanoma. Cancer Res. 72, 1070-1080 (2012).
17. P. P. Lee, C. Yee, P. A. Savage, L. Fong, D. Brockstedt, J. S. Weber, D. Johnson, S. Swetter, J. Thompson, P. D. Greenberg, M. Roederer, M. M. Davis, Characterization of circulating T cells specific for tumor-associated antigens in melanoma patients. Nat. Med. 5, 677-685 (1999).
18. 254-262 in melanoma. Cancer Res. 61, 509-512 (2001).
19. + dendritic cells. J. Exp. Med. 208, 2005-2016 (2011).
20. M. S. Diamond, M. Kinder, H. Matsushita, M. Mashayekhi, G. P. Dunn, J. M. Archambault, H. Lee, C. D. Arthur, J. M. White, U. Kalinke, K. M. Murphy, R. D. Schreiber, Type I interferon is selectively required by dendritic cells for immune rejection of tumors. J. Exp. Med. 208, 1989-2003 (2011).
21. R. R. Ji, S. D. Chasalow, L. Wang, O. Hamid, H. Schmidt, J. Cogswell, S. Alaparthy, D. Berman, M. Jure-Kunkel, N. O. Siemers, J. R. Jackson, V. Shahabi, An immune-active tumor microenvironment favors clinical response to ipilimumab. Cancer Immunol. Immunother. 61, 1019-1031 (2012).
22. + T cells in a patient with malignant melanoma ascites. Cancer. Immunol. Immunother. 55, 1185-1197 (2006).
23. + T cells at tumor site in spite of antitumor immunity to self-antigens in human metastatic melanoma. Cancer Res. 63, 2535-2545 (2003).
24. + T cells in the circulation but not in the tumor site. J. Immunol. 177, 1670-1678 (2006).
25. D. H. Munn, M. Zhou, J. T. Attwood, I. Bondarev, S. J. Conway, B. Marshall, C. Brown, A. L. Mellor, Prevention of allogeneic fetal rejection by tryptophan catabolism. Science 281, 1191-1193 (1998).
26. + regulatory T cells in tumor immunity. Curr. Top. Microbiol. Immunol. 293, 287-302 (2005).
27. D. H. Munn, A. L. Mellor, IDO and tolerance to tumors. Trends Mol. Med. 10, 15-18 (2004).
28. + regulatory T cells. J. Exp. Med. 194, 847-853 (2001).
29. + T cell subsets requires cell cycle progression. J. Immunol. 177, 1981-1987 (2006).
30. T. Gajewski, Y. Zha, B. Thurner, G. Schuler, Association of gene expression profile in melanoma and survival to a dendritic cell-based vaccine. J. Clin. Oncol. 27, 9002 (2009).
31. A. T. Parsa, J. S. Waldron, A. Panner, C. A. Crane, I. F. Parney, J. J. Barry, K. E. Cachola, J. C. Murray, T. Tihan, M. C. Jensen, P. S. Mischel, D. Stokoe, R. O. Pieper, Loss of tumor suppressor PTEN function increases B7-H1 expression and immunoresistance in glioma. Nat. Med. 13, 84-88 (2007).
32. J. M. Taube, R. A. Anders, G. D. Young, H. Xu, R. Sharma, T. L. McMiller, S. Chen, A. P. Klein, D. M. Pardoll, S. L. Topalian, L. Chen, Colocalization of inflammatory response with B7-H1 expression in human melanocytic lesions supports an adaptive resistance mechanism of immune escape. Sci. Transl. Med. 4, 127ra37 (2012).
33. + T regulatory cells mediating allograft tolerance depends on the CCR4 chemokine receptor. J. Exp. Med. 201, 1037-1044 (2005).
34. T. J. Curiel, G. Coukos, L. Zou, X. Alvarez, P. Cheng, P. Mottram, M. Evdemon-Hogan, J. R. Conejo-Garcia, L. Zhang, M. Burow, Y. Zhu, S. Wei, I. Kryczek, B. Daniel, A. Gordon, L. Myers, A. Lackner, M. L. Disis, K. L. Knutson, L. Chen, W. Zou, Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat. Med. 10, 942-949 (2004).
35. D. B. Hoelzinger, S. E. Smith, N. Mirza, A. L. Dominguez, S. Z. Manrique, J. Lustgarten, Blockade of CCL1 inhibits T regulatory cell suppressive function enhancing tumor immunity without affecting T effector responses. J. Immunol. 184, 6833-6842 (2010).
36. R. H. Schwartz, T cell clonal anergy. Curr. Opin. Immunol. 9, 351-357 (1997).
37. S. K. Watkins, Z. Zhu, E. Riboldi, K. A. Shafer-Weaver, K. E. Stagliano, M. M. Sklavos, S. Ambs, H. Yagita, A. A. Hurwitz, FOXO3 programs tumor-associated DCs to become tolerogenic in human and murine prostate cancer. J. Clin. Invest. 121, 1361-1372 (2011).
38. + T cells resulting in a failure to lyse tumor cells. Blood 93, 1634-1642 (1999).
39. + T cell anergy and promotes tumor rejection. J. Immunol. 177, 4521-4529 (2006).
40. L. Chen, S. Ashe, W. A. Brady, I. Hellström, K. E. Hellström, J. A. Ledbetter, P. McGowan, P. S. Linsley, Costimulation of antitumor immunity by the B7 counterreceptor for the T lymphocyte molecules CD28 and CTLA-4. Cell 71, 1093-1102 (1992).
41. + T cells by B7-transfected melanoma cells. Science 259, 368-370 (1993).
42. M. Sznol, J. D. Powderly, D. C. Smith, J. R. Brahmer, C. G. Drake, D. F. McDermott, D. P. Lawrence, J. D. Wolchok, S. L. Topalian, I. Lowy, Safety and antitumor activity of biweekly MDX-1106 (anti-PD-1, BMS-936558/ONO-4538) in patients with advanced refractory malignancies. J. Clin. Oncol. 28, 15s (2010).
43. J. R. Brahmer, S. S. Tykodi, L. Q. Chow, W. J. Hwu, S. L. Topalian, P. Hwu, C. G. Drake, L. H. Camacho, J. Kauh, K. Odunsi, H. C. Pitot, O. Hamid, S. Bhatia, R. Martins, K. Eaton, S. Chen, T. M. Salay, S. Alaparthy, J. F. Grosso, A. J. Korman, S. M. Parker, S. Agrawal, S. M. Goldberg, D. M. Pardoll, A. Gupta, J. M. Wigginton, Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N. Engl. J. Med. 366, 2455-2465 (2012).
44. X. Liu, N. Shin, H. K. Koblish, G. Yang, Q. Wang, K. Wang, L. Leffet, M. J. Hansbury, B. Thomas, M. Rupar, P. Waeltz, K. J. Bowman, P. Polam, R. B. Sparks, E. W. Yue, Y. Li, R. Wynn, J. S. Fridman, T. C. Burn, A. P. Combs, R. C. Newton, P. A. Scherle, Selective inhibition of IDO1 effectively regulates mediators of antitumor immunity. Blood 115, 3520-3530 (2010).
45. S. H. Chen, K. B. Pham-Nguyen, O. Martinet, Y. Huang, W. Yang, S. N. Thung, L. Chen, R. Mittler, S. L. Woo, Rejection of disseminated metastases of colon carcinoma by synergism of IL-12 gene therapy and 4-1BB costimulation. Mol. Ther. 2, 39-46 (2000).
46. M. A. Curran, W. Montalvo, H. Yagita, J. P. Allison, PD-1 and CTLA-4 combination blockade expands infiltrating T cells and reduces regulatory T and myeloid cells within B16 melanoma tumors. Proc. Natl. Acad. Sci. U.S.A. 107, 4275-4280 (2010).
47. + T cell-mediated tumor rejection in vivo. J. Immunol. 174, 3416-3420 (2005).
48. L. Zhang, T. F. Gajewski, J. Kline, PD-1/PD-L1 interactions inhibit antitumor immune responses in a murine acute myeloid leukemia model. Blood 114, 1545-1552 (2009).
49. J. D. Fontenot, J. P. Rasmussen, M. A. Gavin, A. Y. Rudensky, A function for interleukin 2 in Foxp3-expressing regulatory T cells. Nat. Immunol. 6, 1142-1151 (2005).
50. + T cells. Sci. Transl. Med. 5, 200ra116 (2013).