Association of PD-1, PD-1 ligands, and other features of the tumor immune microenvironment with response to anti-PD-1 therapy

Clinical Cancer Research

Volumn 20, Issue 19, 2014, Pages 5064-5074

  Taube, Janis M ^a   Klein, Alison ^a,b   Brahmer, Julie R ^a   Xu, Haiying ^a   Pan, Xiaoyu ^a   Kim, Jung H ^a   Chen, Lieping ^c   Pardoll, Drew M ^a   Topalian, Suzanne L ^a   Anders, Robert A ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NIVOLUMAB; PROGRAMMED DEATH 1 LIGAND 1; PROGRAMMED DEATH 1 LIGAND 2; PROGRAMMED DEATH 1 RECEPTOR; ANTINEOPLASTIC AGENT; MONOCLONAL ANTIBODY; PDCD1LG2 PROTEIN, HUMAN;

ARTICLE; B LYMPHOCYTE; CANCER IMMUNOTHERAPY; CASTRATION RESISTANT PROSTATE CANCER; CD4 CD8 RATIO; CELL INFILTRATION; CELL SURFACE; CLINICAL ARTICLE; CLINICAL TRIAL (TOPIC); COLORECTAL CANCER; CONTROLLED STUDY; HUMAN; HUMAN TISSUE; IMMUNOCOMPETENT CELL; KIDNEY CANCER; KIDNEY CARCINOMA; LYMPHOCYTE; MALE; MELANOMA; NON SMALL CELL LUNG CANCER; PROTEIN EXPRESSION; TREATMENT RESPONSE; TUMOR ASSOCIATED LEUKOCYTE; TUMOR CELL; TUMOR MICROENVIRONMENT; ANTAGONISTS AND INHIBITORS; BIOPSY; CANCER STAGING; CLINICAL TRIAL; GENE EXPRESSION; GENETICS; IMMUNOLOGY; METABOLISM; METASTASIS; MOLECULARLY TARGETED THERAPY; MULTICENTER STUDY; NEOPLASMS; TREATMENT OUTCOME;

ANTIBODIES, MONOCLONAL; ANTIGENS, CD274; ANTINEOPLASTIC AGENTS; BIOPSY; GENE EXPRESSION; HUMANS; LYMPHOCYTES, TUMOR-INFILTRATING; MOLECULAR TARGETED THERAPY; NEOPLASM METASTASIS; NEOPLASM STAGING; NEOPLASMS; PROGRAMMED CELL DEATH 1 LIGAND 2 PROTEIN; PROGRAMMED CELL DEATH 1 RECEPTOR; TREATMENT OUTCOME; TUMOR MICROENVIRONMENT;

EID: 84904024273     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-13-3271     Document Type: Article

References (45)

1. 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 19;363:711-23.
2. Agata Y, Kawasaki A, Nishimura H, Ishida Y, Tsubata T, Yagita H, et al. Expression of the PD-1 antigen on the surface of stimulated mouse T and B lymphocytes. Int Immunol 1996;8:765-72.
3. Dong H, Zhu G, Tamada K, Chen L. B7-H1, a third member of the B7 family, co-stimulates T-cell proliferation and interleukin-10 secretion. Nat Med 1999;5:1365-9.
4. Dong H, Strome SE, Salomao DR, Tamura H, Hirano F, Flies DB, et al. Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat Med 2002;8:793-800.
5. Mazanet MM, Hughes CC. B7-H1 is expressed by human endothelial cells and suppresses T cell cytokine synthesis. J Immunol 2002;169:3581-8.
6. Petroff MG, Chen L, Phillips TA, Azzola D, Sedlmayr P, Hunt JS. B7 family molecules are favorably positioned at the human maternal-fetal interface. Biol Reprod 2003;68:1496-504.
7. Ishida M, Iwai Y, Tanaka Y, Okazaki T, Freeman GJ, Minato N, et al. Differential expression of PD-L1 and PD-L2, ligands for an inhibitory receptor PD-1, in the cells of lymphohematopoietic tissues. Immunol Lett 2002;84:57-62.
8. Yamazaki T, Akiba H, Iwai H, Matsuda H, Aoki M, Tanno Y, et al. Expression of programmed death 1 ligands by murine T cells and APC. J Immunol 2002;169:5538-45.
9. Tseng SY, Otsuji M, Gorski K, Huang X, Slansky JE, Pai SI, et al. B7-DC, a new dendritic cell molecule with potent costimulatory properties for T cells. J Exp Med 2001;193:839-46.
10. Flies DB, Chen L. The new B7s: playing a pivotal role in tumor immunity. J Immunother 2007;30:251-60.
11. Zou W, Chen L. Inhibitory B7-family molecules in the tumour micro-environment. Nat Rev Immunol 2008;8:467-77.
12. Taube JM, Anders RA, Young GD, Xu H, Sharma R, McMiller TL, et al. Colocalization of in flammatory response with B7-h1 expression in human melanocytic lesions supports an adaptive resistance mechanism of immune escape. Sci Transl Med 2012;4:127ra37.
13. Lipson EJ, Vincent JG, Loyo M, Kagohara LT, Luber BS, Wang H, et al. PD-L1 expression in the merkel cell carcinoma microenvironment: association with inflammation, merkel cell polyomavirus and overall survival. Cancer Immunol Res 2013;1:54-63.
14. Nishimura H, Nose M, Hiai H, Minato N, Honjo T. Development of lupus-like autoimmune diseases by disruption of the PD-1 gene encoding an ITIM motif-carrying immunoreceptor. Immunity 1999;11:141-51.
15. Nishimura H, Okazaki T, Tanaka Y, Nakatani K, Hara M, Matsumori A, et al. Autoimmune dilated cardiomyopathy in PD-1 receptor-deficient mice. Science 2001;291:319-22.
16. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012;366:2443-54.
17. Brahmer JR, Drake CG, Wollner I, Powderly JD, Picus J, Sharfman WH, et al. 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 2010;28:3167-75.
18. Brahmer JR, Tykodi SS, Chow LQ, Hwu WJ, Topalian SL, Hwu P, et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 2012;366:2455-65.
19. Hamid O, Robert C, Daud A, Hodi FS, Hwu WJ, Kefford R, et al. Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma. N Engl J Med 2013;369:134-44.
20. Therasse P, Arbuck SG, Eisenhauer EA, Wanders J, Kaplan RS, Rubinstein L, et al. New guidelines to evaluate the response to treatment in solid tumors. European organization for research and treatment of cancer, national cancer institute of the United States, national cancer institute of Canada. J Natl Cancer Inst 2000;92:205-16.
21. Lipson EJ, Sharfman WH, Drake CG, Wollner I, Taube JM, Anders RA, et al. Durable cancer regression off-treatment and effective reinduction therapy with an anti-PD-1 antibody. Clin Cancer Res 2013;19:462-8.
22. Blansfield JA, Beck KE, Tran K, Yang JC, Hughes MS, Kammula US, et al. Cytotoxic T-lymphocyte-associated antigen-4 blockage can induce autoimmune hypophysitis in patients with metastatic melanoma and renal cancer. J Immunother 2005;28:593-8.
23. Downey SG, Klapper JA, Smith FO, Yang JC, Sherry RM, Royal RE, et al. Prognostic factors related to clinical response in patients with metastatic melanoma treated by CTL-associated antigen-4 blockade. Clin Cancer Res 2007;13:6681-8.
24. Beck KE, Blans field JA, Tran KQ, Feldman AL, Hughes MS, Royal RE, et al. Enterocolitis in patients with cancer after antibody blockade of cytotoxic T-lymphocyte-associated antigen 4. J Clin Oncol 2006;24:2283-9.
25. Gajewski TF, Fuertes M, Spaapen R, Zheng Y, Kline J. Molecular pro filing to identify relevant immune resistance mechanisms in the tumor microenvironment. Curr Opin Immunol 2011;23:286-92.
26. Ji RR, Chasalow SD, Wang L, Hamid O, Schmidt H, Cogswell J, et al. An immune-active tumor microenvironment favors clinical response to ipilimumab. Cancer Immunol Immunother 2012;61:1019-31.
27. Droeser RA, Hirt C, Viehl CT, Frey DM, Nebiker C, Huber X, et al. Clinical impact of programmed cell death ligand 1 expression in colorectal cancer. Eur J Cancer 2013;49:2233-42.
28. Velcheti V, Schalper KA, Carvajal DE, Anagnostou VK, Syrigos KN, Sznol M, et al. Programmed death ligand-1 expression in non-small cell lung cancer. Lab Invest 2014;94:107-16.
29. Lyford-Pike S, Peng S, Young GD, Taube JM, Westra WH, Akpeng B, et al. Evidence for a role of the PD-1:PD-L1 pathway in immune resistance of HPV-associated head and neck squamous cell carcinoma. Cancer Res 2013;73:1733-41.
30. Parsa AT, Waldron JS, Panner A, Crane CA, Parney IF, Barry JJ, et al. Loss of tumor suppressor PTEN function increases B7-H1 expression and immunoresistance in glioma. Nat Med 2007;13:84-8.
31. 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.
32. Azimi F, Scolyer RA, Rumcheva P, Moncrieff M, Murali R, McCarthy SW, et al. Tumor-infiltrating lymphocyte grade is an independent predictor of sentinel lymph node status and survival in patients with cutaneous melanoma. J Clin Oncol 2012;30:2678-83.
33. Ogino S, Nosho K, Irahara N, Meyerhardt JA, Baba Y, Shima K, et al. Lymphocytic reaction to colorectal cancer is associated with longer survival, independent of lymph node count, microsatellite instability, and CpG island methylator phenotype. Clin Cancer Res 2009;15:6412-20.
34. Erdag G, Schaefer JT, Smolkin ME, Deacon DH, Shea SM, Dengel LT, et al. Immunotype and immunohistologic characteristics of tumor-infiltrating immune cells are associated with clinical outcome in metastatic melanoma. Cancer Res 2012;72:1070-80.
35. Thomas NE, Busam KJ, From L, Kricker A, Armstrong BK, Anton-Culver H, et al. Tumor-infiltrating lymphocyte grade in primary melanomas is independently associated with melanoma-specific survival in the population-based genes, environment and melanoma study. J Clin Oncol 2013;31:4252-9.
36. Loi S, Sirtaine N, Piette F, Salgado R, Viale G, Van Eenoo F, et al. Prognostic and predictive value of tumor-in filtrating lymphocytes in a phase III randomized adjuvant breast cancer trial in node-positive breast cancer comparing the addition of docetaxel to doxorubicin with doxorubicin-based chemotherapy: BIG 02-98. J Clin Oncol 2013;31:860-7.
37. Hamid O, Schmidt H, Nissan A, Ridolfi L, Aamdal S, Hansson J, et al. A prospective phase II trial exploring the association between tumor microenvironment biomarkers and clinical activity of ipilimumab in advanced melanoma. J Transl Med 2011;9:204-19.
38. Velu V, Titanji K, Zhu B, Husain S, Pladevega A, Lai L, et al. Enhancing SIV-specific immunity in vivo by PD-1 blockade. Nature 2009;458:206-10.
39. Mohos A, Sebestyen T, Liszkay G, Plotar V, Horvath S, Gaudi I, et al. Immune cell profile of sentinel lymph nodes in patients with malignant melanoma - FOXP3+ cell density in cases with positive sentinel node status is associated with unfavorable clinical outcome. J Transl Med 2013;11:43-53.
40. Taube JM. Emerging immunologic biomarkers: setting the [TNM-immune] stage. Clin Cancer Res 2014;20:2023-5.
41. Grosso J, Horak C, Inzunza D, Cardona D, Simon J, Gupta A, et al. Association of tumor PD-L1 expression and immune biomarkers with clinical activity in patients with advanced solid tumors treated with nivolumab. J Clin Oncol 31, 2013 (suppl; abstr 3016).
42. Herbst R, Gordon M, Fine G, Sosman J, Charles J, Hamid O, et al. A study of MPDL3280A, an engineered PD-L1 antibody in patients with locally advanced or metastatic tumors. J Clin Oncol 31, 2013 (suppl; abstr 3000).
43. Gerlinger M, Rowan AJ, Horswell S, Larkin J, Endesfelder D, Gronroos E, et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med 2012;366:883-92.
44. Latchman Y, Wood CR, Chernova T, Chaudhary D, Borde M, Chernova I, et al. PD-L2 is a second ligand for PD-1 and inhibits T cell activation. Nat Immunol 2001;2:261-8.
45. Hodi FS, Powles T, Cassier P, Kowanetz M, Herbst RS, Soria JC, et al. MPDL3280A (anti-PDL1): clinical activity, safety and biomarkers of an engineered PD-L1 antibody in patients with locally advanced or metastatic tumors. Eur Cancer Congr 2013;abstr 879.