Evaluation of programmed cell death protein 1 (PD-1) expression as a prognostic biomarker in patients with clear cell renal cell carcinoma

References

• Siegel RL, Miller KD, Jemal A. Cancer statistics, 2016. CA Cancer J Clin. 66(1):7–30. doi:10.3322/caac.21332.
   PubMed Web of Science ®Google Scholar
• Janzen NK, Kim HL, Figlin RA, Belldegrun AS. Surveillance after radical or partial nephrectomy for localized renal cell carcinoma and management of recurrent disease. Urol Clin North Am. 2003;30(4):843–852. http://www.ncbi.nlm.nih.gov/pubmed/14680319. doi:10.1016/S0094-0143(03)00056-9.
   PubMed Web of Science ®Google Scholar
• Klapper JA, Downey SG, Smith FO, Yang JC, Hughes MS, Kammula US, Sherry RM, Royal RE, Steinberg SM, Rosenberg S. High-dose interleukin-2 for the treatment of metastatic renal cell carcinoma : a retrospective analysis of response and survival in patients treated in the surgery branch at the National Cancer Institute between 1986 and 2006. Cancer. 2008;113(2):293–301. doi:10.1002/cncr.23552.
   PubMed Web of Science ®Google Scholar
• Jensen HK, Donskov F, Marcussen N, Nordsmark M, Lundbeck F, von der Maase H. Presence of intratumoral neutrophils is an independent prognostic factor in localized renal cell carcinoma. J Clin Oncol. 2009;27(28):4709–4717. doi:10.1200/JCO.2008.18.9498.
   PubMed Web of Science ®Google Scholar
• Donskov F, von der Maase H. Impact of immune parameters on long-term survival in metastatic renal cell carcinoma. J Clin Oncol. 2006;24(13):1997–2005. doi:10.1200/JCO.2005.03.9594.
   PubMed Web of Science ®Google Scholar
• Webster WS, Lohse CM, Thompson RH, Dong H, Frigola X, Dicks DL, Sengupta S, Frank I, Leibovich BC, Blute ML, et al. Mononuclear cell infiltration in clear-cell renal cell carcinoma independently predicts patient survival. Cancer. 2006;107(1):46–53. doi:10.1002/cncr.21951.
   PubMed Web of Science ®Google Scholar
• Igarashi T, Takahashi H, Tobe T, Suzuki H, Mizoguchi K, Nakatsu HO, Ito H.. Effect of tumor-infiltrating lymphocyte subsets on prognosis and susceptibility to interferon therapy in patients with renal cell carcinoma. Urol Int. 2002;69(1):51–56. doi:10.1159/000064361.
   PubMed Web of Science ®Google Scholar
• Bromwich EJ, McArdle PA, Canna K, McMillan DC, McNicol AM, Brown M, Aitchison M. The relationship between T-lymphocyte infiltration, stage, tumour grade and survival in patients undergoing curative surgery for renal cell cancer. Br J Cancer. 2003;89(10):1906–1908. doi:10.1038/sj.bjc.6601400.
   PubMed Web of Science ®Google Scholar
• Wherry EJ. T cell exhaustion. Nat Immunol. 2011;12(6):492–499. doi:10.1038/ni.2035.
   PubMed Web of Science ®Google Scholar
• Wherry EJ, Kurachi M. Molecular and cellular insights into T cell exhaustion. Nat Rev Immunol. 2015;15(8):486–499. doi:10.1038/nri3862.
   PubMed Web of Science ®Google Scholar
• Pauken KE, Wherry EJ. Overcoming T cell exhaustion in infection and cancer. Trends Immunol. 2015;36(4):265–276. doi:10.1016/j.it.2015.02.008.
   PubMed Web of Science ®Google Scholar
• Frankenberger B, Noessner E, Schendel DJ. Immune suppression in renal cell carcinoma. Semin Cancer Biol. 2007;17(4):330–343. doi:10.1016/j.semcancer.2007.06.004.
   PubMed Web of Science ®Google Scholar
• Geissler K, Fornara P, Lautenschläger C, Holzhausen H-J, Seliger B, Riemann D. Immune signature of tumor infiltrating immune cells in renal cancer. Oncoimmunology. 2015;4(1):e985082. doi:10.4161/2162402X.2014.985082.
   PubMed Web of Science ®Google Scholar
• Chen L, Flies DB. Molecular mechanisms of T cell co-stimulation and co-inhibition. Nat Rev Immunol. 2013;13(April):227–242. doi:10.1038/nri3405.
   PubMedGoogle Scholar
• FDA Approves Nivolumab to Treat Advanced Kidney Cancer. The ASCO Post. http://www.ascopost.com/News/34072. Published 2015. Accessed January 1, 2016.
   Google Scholar
• Motzer RJ, Escudier B, McDermott DF, George S, Hammers HJ, Srinivas S, Tykodi SS, Sosman JA, Procopio G, Plimack ER, et al. Nivolumab versus Everolimus in Advanced Renal-Cell Carcinoma. N Engl J Med. 2015:1803–1813. doi:10.1056/NEJMoa1510665.
   PubMed Web of Science ®Google Scholar
• Quinn DI, Lara PN, Ph D, Lara PN. Renal-Cell Cancer – Targeting an Immune Checkpoint or Multiple Kinases. N Engl J Med. 2015;373(19):1–3. doi:10.1056/NEJMe1511252.
   PubMed Web of Science ®Google Scholar
• McDermott DF, Motzer RJ, Atkins MB, et al. Long-term overall survival (OS) with nivolumab in previously treated patients with advanced renal cell carcinoma (aRCC) from phase I and II studies. J Clin Oncol. 2016;34:suppl:abstr 4507. http://meetinglibrary.asco.org/content/162949-176.
   Google Scholar
• Thompson RH, Gillett MD, Cheville JC, Lohse CM, Dong H, Webster WS, Chen L, Zincke H, Blute ML, Leibovich BC, et al. Costimulatory molecule B7-H1 in primary and metastatic clear cell renal cell carcinoma. Cancer. 2005;104(10):2084–2091. doi:10.1002/cncr.21470.
   PubMed Web of Science ®Google Scholar
• Thompson RH, Kuntz SM, Leibovich BC, Dong H, Lohse CM, Webster WS, Sengupta S, Frank I, Parker AS, Zincke H, et al. Tumor B7-H1 is associated with poor prognosis in renal cell carcinoma patients with long-term follow-up. Cancer Res. 2006;66(7):3381–3385. doi:10.1158/0008-5472.CAN-05-4303.
   PubMed Web of Science ®Google Scholar
• Thompson RH, Dong H, Lohse CM, Leibovich BC, Blute ML, Cheville JC, Kwon ED. PD-1 is expressed by tumor-infiltrating immune cells and is associated with poor outcome for patients with renal cell carcinoma. Clin Cancer Res. 2007;13(6):1757–1761. doi:10.1158/1078-0432.CCR-06-2599.
   PubMed Web of Science ®Google Scholar
• Kang MJ, Kim KM, Bae JS, Park HS, Lee H, Chung MJ, Moon WS, Lee DG, Jang KY. Tumor-infiltrating PD1-Positive Lymphocytes and FoxP3-Positive Regulatory T Cells Predict Distant Metastatic Relapse and Survival of Clear Cell Renal Cell Carcinoma. Transl Oncol. 2013;6(3):282–289. doi:10.1593/tlo.13256.
   PubMed Web of Science ®Google Scholar
• Choueiri TK, Fay AP, Gray KP, Callea M, Ho TH, Albiges L, Bellmunt J, Song J, Carvo I, Lampron M, et al. PD-L1 expression in nonclear-cell renal cell carcinoma. Ann Oncol. 2014;25(11):2178–2184. doi:10.1093/annonc/mdu445.
   PubMed Web of Science ®Google Scholar
• Choueiri TK, Figueroa DJ, Fay AP, Signoretti S, Liu Y, Gagnon R, Deen K, Carpenter C, Benson P, Ho TH, et al. Correlation of PD-L1 tumor expression and treatment outcomes in patients with renal cell carcinoma receiving sunitinib or pazopanib: Results from COMPARZ, a randomized controlled trial. Clin Cancer Res. 2015;21(5):1071–1077. doi:10.1158/1078-0432.CCR-14-1993.
   PubMed Web of Science ®Google Scholar
• Giraldo NA, Becht E, Pag??s F, Skliris G, Verkarre V, Vano Y, Mejean A, Saint-Aubert N, Lacroix L, Natario I, et al. Orchestration and prognostic significance of immune checkpoints in the microenvironment of primary and metastatic renal cell cancer. Clin Cancer Res. 2015;21(13):3031–3040. doi:10.1158/1078-0432.CCR-14-2926.
   PubMed Web of Science ®Google Scholar
• Shin SJ, Jeon YK, Kim PJ, Cho YM, Koh J, Chung DH, Go H.. Clinicopathologic Analysis of PD-L1 and PD-L2 Expression in Renal Cell Carcinoma: Association with Oncogenic Proteins Status. Ann Surg Oncol. 2015:694–702. doi:10.1245/s10434-015-4903-7.
   Google Scholar
• Leite KRM, Reis ST, Junior JP, Zerati M, Gomes Dde O, Camara-Lopes LH, Srougi M.. PD-L1 expression in renal cell carcinoma clear cell type is related to unfavorable prognosis. Diagn Pathol. 2015;10(1):189. doi:10.1186/s13000-015-0414-x.
   PubMedGoogle Scholar
• Abbas M, Steffens S, Bellut M, Becker JU, Großhennig A, Eggers H, Wegener G, Kuczyk MA, Kreipe HH, Grünwald V, et al. Do programmed death 1 (PD-1) and its ligand (PD-L1) play a role in patients with non-clear cell renal cell carcinoma? Med Oncol. 2016;33(6):1–7. doi:10.1007/s12032-016-0770-8.
   PubMed Web of Science ®Google Scholar
• Abbas M, Steffens S, Bellut M, Eggers H, Großhennig A, Becker JU, Wegener G, Schrader AJ, Grünwald V, Ivanyi P. Intratumoral expression of programmed death ligand 1 (PD-L1) in patients with clear cell renal cell carcinoma (ccRCC). Med Oncol. 2016;33(7):1–7. doi:10.1007/s12032-016-0794-0.
   PubMed Web of Science ®Google Scholar
• Erlmeier F, Hartmann A, Autenrieth M, Wiedemann M, Ivanyi P, Steffens S, Weichert W. PD-1/PD-L1 expression in chromophobe renal cell carcinoma: An immunological exception? Med Oncol. 2016;33(11):1–6. doi:10.1007/s12032-016-0833-x.
   PubMed Web of Science ®Google Scholar
• Crispin H, Agarwal AM, Salama ME, Tantravahi SK, Merriman J, Straubhar AM, Poole A, Nussenzveig R, Stenehjem DD, Agarwal N. Correlation of tumor programmed death ligand-1 (PD-L1) expression and response to treatment with high-dose interleukin-2 (HD IL-2) in clear cell metastatic renal cell carcinoma (ccmRCC). J Clin Oncol. 2014;32: suppl; abstr e15584.
   Web of Science ®Google Scholar
• McDermott DF, Sosman JA, Sznol M, Massard C, Gordon MS, Hamid O, Powderly JD, Infante JR, Fassò M, Wang YV, et al. Atezolizumab, an anti-programmed death-ligand 1 antibody, in metastatic renal cell carcinoma: Long-term safety, clinical activity, and immune correlates from a phase Ia study. J Clin Oncol. 2016;34(8):833–842. doi:10.1200/JCO.2015.63.7421.
   PubMed Web of Science ®Google Scholar
• Ishida Y, Agata Y, Shibahara K, Honjo T. Induced expression of PD-1, a novel member of the immunoglobulin gene superfamily, upon programmed cell death. EMBO J. 1992;11(11):3887–3895. http://www.ncbi.nlm.nih.gov/pubmed/1396582.
   PubMed Web of Science ®Google Scholar
• Blank C, Brown I, Marks R, Nishimura H, Honjo T, Gajewski TF. Absence of programmed death receptor 1 alters thymic development and enhances generation of CD4/CD8 double-negative TCR-transgenic T cells. J Immunol. 2003;171(9):4574–4581. http://www.ncbi.nlm.nih.gov/pubmed/14568931. doi:10.4049/jimmunol.171.9.4574.
   PubMed Web of Science ®Google Scholar
• Agata Y, Kawasaki A, Nishimura H, Ishida Y, Tsubata T, Yagita H, Honjo T.. Expression of the PD-1 antigen on the surface of stimulated mouse T and B lymphocytes. Int Immunol. 1996;8(5):765–772. http://www.ncbi.nlm.nih.gov/pubmed/8671665. doi:10.1093/intimm/8.5.765.
   PubMed Web of Science ®Google Scholar
• Nishimura H, Honjo T. PD-1: an inhibitory immunoreceptor involved in peripheral tolerance. Trends Immunol. 2001;22(5):265–268. http://www.ncbi.nlm.nih.gov/pubmed/11323285. doi:10.1016/S1471-4906(01)01888-9.
   PubMed Web of Science ®Google Scholar
• Nishimura H, Minato N, Nakano T, Honjo T. Immunological studies on PD-1 deficient mice: implication of PD-1 as a negative regulator for B cell responses. Int Immunol. 1998;10(10):1563–1572. http://www.ncbi.nlm.nih.gov/pubmed/9796923. doi:10.1093/intimm/10.10.1563.
   PubMed Web of Science ®Google Scholar
• 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(2):141–151. http://www.ncbi.nlm.nih.gov/pubmed/10485649. doi:10.1016/S1074-7613(00)80089-8.
   PubMed Web of Science ®Google Scholar
• Nishimura H, Okazaki T, Tanaka Y, Nakatani K, Hara M, Matsumori A, Sasayama S, Mizoguchi A, Hiai H, Minato N, et al. Autoimmune dilated cardiomyopathy in PD-1 receptor-deficient mice. Science. 2001;291(5502):319–322. doi:10.1126/science.291.5502.319.
   PubMed Web of Science ®Google Scholar
• McKinney EF, Lee JC, Jayne DR, Lyons PA, Smith KG. T-cell exhaustion, co-stimulation and clinical outcome in autoimmunity and infection. Nature. 2015;523(7562):612–616. doi:10.1038/nature14468.
   PubMed Web of Science ®Google Scholar
• Dong H, Strome SE, Salomao DR, Tamura H, Hirano F, Flies DB, Roche PC, Lu J, Zhu G, Tamada K, et al. Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat Med. 2002;8(8):793–800. doi:10.1038/nm730.
   PubMed Web of Science ®Google Scholar
• Iwai Y, Ishida M, Tanaka Y, Okazaki T, Honjo T, Minato N. Involvement of PD-L1 on tumor cells in the escape from host immune system and tumor immunotherapy by PD-L1 blockade. Proc Natl Acad Sci U S A. 2002;99(19):12293–12297. doi:10.1073/pnas.192461099.
   PubMed Web of Science ®Google Scholar
• Blank C, Gajewski TF, Mackensen A. Interaction of PD-L1 on tumor cells with PD-1 on tumor-specific T cells as a mechanism of immune evasion: Implications for tumor immunotherapy. Cancer Immunol Immunother. 2005;54(4):307–314. doi:10.1007/s00262-004-0593-x.
   PubMed Web of Science ®Google Scholar
• Lee C-H, Motzer RJ. Immune Checkpoint Therapy in Renal Cell Carcinoma. Cancer J. 22(2):92–95. doi:10.1097/PPO.0000000000000177.
   PubMed Web of Science ®Google Scholar
• Gerlinger M, Rowan AJ, Horswell S, Math M, Larkin J, Endesfelder D, Gronroos E, Martinez P, Matthews N, et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med. 2012;366(10):883–892. doi:10.1056/NEJMoa1113205.
   PubMed Web of Science ®Google Scholar
• Jilaveanu LB, Shuch B, Zito CR, Parisi F, Barr M, Kluger Y, Chen L, Kluger HM, et al. PD-L1 expression in clear cell renal cell carcinoma: An analysis of nephrectomy and sites of metastases. J Cancer. 2014;5(3):166–172. doi:10.7150/jca.8167.
   PubMed Web of Science ®Google Scholar
• Callea M, Albiges L, Gupta M, Cheng SC, Genega EM, Fay AP, Song J, Carvo I, Bhatt RS, Atkins MB, et al. Differential Expression of PD-L1 between Primary and Metastatic Sites in Clear-Cell Renal Cell Carcinoma. Cancer Immunol Res. 2015;3(10):1158–1164. doi:10.1158/2326-6066.CIR-15-0043.
   PubMed Web of Science ®Google Scholar
• Frigola X, Inman BA, Lohse CM, Krco CJ, Cheville JC, Thompson RH, Leibovich B, Blute ML, Dong H, Kwon ED. Identification of a soluble form of B7-H1 that retains immunosuppressive activity and is associated with aggressive renal cell carcinoma. Clin Cancer Res. 2011;17(7):1915–1923. doi:10.1158/1078-0432.CCR-10-0250.
   PubMed Web of Science ®Google Scholar
• Blackburn SD, Shin H, Freeman GJ, Wherry EJ. Selective expansion of a subset of exhausted CD8 T cells by alphaPD-L1 blockade. Proc Natl Acad Sci U S A. 2008;105(39):15016–15021. doi:10.1073/pnas.0801497105.
   PubMed Web of Science ®Google Scholar
• Messai Y, Gad S, Noman MZ, Le Teuff G Couve S, Janji B, Kammerer SF, Rioux-Leclerc N, Hasmim M, Ferlicot S, et al. Renal Cell Carcinoma Programmed Death-ligand 1, a New Direct Target of Hypoxia-inducible Factor-2 Alpha, is Regulated by von Hippel-Lindau Gene Mutation Status. Eur Urol. 2016;70(4):623–632. doi:10.1016/j.eururo.2015.11.029.
   PubMed Web of Science ®Google Scholar
• Hirayama Y, Gi M, Yamano S, Tachibana H, Okuno T, Tamada S, Nakatani T, Wanibuchi H. Anti-PD-L1 treatment enhances antitumor effect of everolimus in a mouse model of renal cell carcinoma. Cancer Sci. 2016;107(12):1736–1744. doi:10.1111/cas.13099.
   PubMed Web of Science ®Google Scholar