Expression of programmed cell death protein 1 (PD-1) and its ligand PD-L1 in colorectal cancer: Relationship with sidedness and prognosis

References

• Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Cancer J Clin. 2015;65(2):87–108. PMID:25651787.
   PubMed Web of Science ®Google Scholar
• Keir ME, Butte MJ, Freeman GJ, Sharpe AH. PD-1 and its ligands in tolerance and immunity. Annu Rev Immunol. 2008;26:677–704. doi:10.1146/annurev.immunol.26.021607.090331. PMID:18173375.
   PubMed Web of Science ®Google Scholar
• Gordon SR, Maute RL, Dulken BW, Hutter G, George BM, McCracken MN, Gupta R, Tsai JM, Sinha R, Corey D, et al. PD-1 expression by tumour-associated macrophages inhibits phagocytosis and tumour immunity. Nature. 2017;545(7655):495–9. doi:10.1038/nature22396. PMID:28514441.
   PubMed Web of Science ®Google Scholar
• Lim TS, Chew V, Sieow JL, Goh S, Yeong JP, Soon AL, Ricciardi-Castagnoli P. PD-1 expression on dendritic cells suppresses CD8(+) T cell function and antitumor immunity. Oncoimmunology. 2016;5(3):e1085146. doi:10.1080/2162402X.2015.1085146. PMID:27141339.
   PubMed Web of Science ®Google Scholar
• Francisco LM, Sage PT, Sharpe AH. The PD-1 pathway in tolerance and autoimmunity. Immunol Rev. 2010;236:219–42. doi:10.1111/j.1600-065X.2010.00923.x. PMID:20636820.
   PubMed Web of Science ®Google Scholar
• Nomi T, Sho M, Akahori T, Hamada K, Kubo A, Kanehiro H, Nakamura S, Enomoto K, Yagita H, Azuma M, et al. Clinical significance and therapeutic potential of the programmed death-1 ligand/programmed death-1 pathway in human pancreatic cancer. Clinical cancer research : an official journal of the American Association for Cancer Research. 2007;13(7):2151–7. doi:10.1158/1078-0432.CCR-06-2746. PMID:17404099.
   PubMed Web of Science ®Google Scholar
• Muenst S, Schaerli AR, Gao F, Daster S, Trella E, Droeser RA, et al. Expression of programmed death ligand 1 (PD-L1) is associated with poor prognosis in human breast cancer. Breast Cancer Res Treat. 2014;146(1):15–24. doi:10.1007/s10549-014-2988-5. PMID:24842267.
   PubMed Web of Science ®Google Scholar
• Thompson RH, Gillett MD, Cheville JC, Lohse CM, Dong H, Webster WS, Krejci KG, Lobo JR, Sengupta S, Chen L, et al. Costimulatory B7-H1 in renal cell carcinoma patients: Indicator of tumor aggressiveness and potential therapeutic target. PNAS. 2004;101(49):17174–9. doi:10.1073/pnas.0406351101. PMID:15569934.
   PubMed Web of Science ®Google Scholar
• Mellman I, Coukos G, Dranoff G. Cancer immunotherapy comes of age. Nature. 2011;480(7378):480–9. doi:10.1038/nature10673. PMID:22193102.
   PubMed Web of Science ®Google Scholar
• Restifo NP, Dudley ME, Rosenberg SA. Adoptive immunotherapy for cancer: harnessing the T cell response. Nat Rev Immunol. 2012;12(4):269–81. doi:10.1038/nri3191. PMID:22437939.
   PubMed Web of Science ®Google Scholar
• 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(26):2443–54. doi:10.1056/NEJMoa1200690. PMID:22658127.
   PubMed Web of Science ®Google Scholar
• Overman MJ, McDermott R, Leach JL, Lonardi S, Lenz HJ, Morse MA, Desai J, Hill A, Axelson M, Moss RA, et al. Nivolumab in patients with metastatic DNA mismatch repair-deficient or microsatellite instability-high colorectal cancer (CheckMate 142): an open-label, multicentre, phase 2 study. Lancet Oncol. 2017;18(9):1182–91. doi:10.1016/S1470-2045(17)30422-9. PMID:28734759.
   PubMed Web of Science ®Google Scholar
• Le DT, Uram JN, Wang H, Bartlett BR, Kemberling H, Eyring AD, et al. PD-1 Blockade in Tumors with Mismatch-Repair Deficiency. N Engl J Med. 2015;372(26):2509–20. doi:10.1056/NEJMoa1500596. PMID:26028255.
   PubMed Web of Science ®Google Scholar
• Berntsson J, Svensson MC, Leandersson K, Nodin B, Micke P, Larsson AH, Eberhard J, Jirström K. The clinical impact of tumour-infiltrating lymphocytes in colorectal cancer differs by anatomical subsite: A cohort study. Int J Cancer. 2017;141(8):1654–66. doi:10.1002/ijc.30869. PMID:28677162.
   PubMed Web of Science ®Google Scholar
• Berntsson J, Nodin B, Eberhard J, Micke P, Jirstrom K. Prognostic impact of tumour-infiltrating B cells and plasma cells in colorectal cancer. Int J Cancer. 2016;139(5):1129–39. doi:10.1002/ijc.30138. PMID:27074317.
   PubMed Web of Science ®Google Scholar
• Wang L, Ren F, Wang Q, Baldridge LA, Monn MF, Fisher KW, Sheng W, Zhou X, Du X, Cheng L. Significance of Programmed Death Ligand 1 (PD-L1) Immunohistochemical Expression in Colorectal Cancer. Mol Diagn Ther. 2016;20(2):175–81. doi:10.1007/s40291-016-0188-1..
   PubMed Web of Science ®Google Scholar
• Li Y, Liang L, Dai W, Cai G, Xu Y, Li X, Li Q, Cai S. Prognostic impact of programed cell death-1 (PD-1) and PD-ligand 1 (PD-L1) expression in cancer cells and tumor infiltrating lymphocytes in colorectal cancer. Mol Cancer. 2016;15(1):55. doi:10.1186/s12943-016-0539-x. PMID:27552968.
   PubMed Web of Science ®Google Scholar
• Droeser RA, Hirt C, Viehl CT, Frey DM, Nebiker C, Huber X, Zlobec I, Eppenberger-Castori S, Tzankov A, Rosso R, et al. Clinical impact of programmed cell death ligand 1 expression in colorectal cancer. European journal of cancer (Oxford, England : 1990). 2013;49(9):2233–42. doi:10.1016/j.ejca.2013.02.015. PMID:23478000.
   PubMed Web of Science ®Google Scholar
• Lee KS, Kwak Y, Ahn S, Shin E, Oh HK, Kim DW, Kang SB, Choe G, Kim WH, Lee HS. Prognostic implication of CD274 (PD-L1) protein expression in tumor-infiltrating immune cells for microsatellite unstable and stable colorectal cancer. Cancer Immunol Immunother : CII. 2017;66(7):927–39. doi:10.1007/s00262-017-1999-6. PMID:28405764.
   PubMed Web of Science ®Google Scholar
• Lee LH, Cavalcanti MS, Segal NH, Hechtman JF, Weiser MR, Smith JJ, Garcia-Aguilar J, Sadot E, Ntiamoah P, Markowitz AJ, et al. Patterns and prognostic relevance of PD-1 and PD-L1 expression in colorectal carcinoma. Modern pathology : an official journal of the United States and Canadian Academy of Pathology, Inc. 2016;29(11):1433–42. doi:10.1038/modpathol.2016.139. PMID:27443512.
   PubMed Web of Science ®Google Scholar
• Kollmann D, Schweiger T, Schwarz S, Ignatova D, Chang YT, Lewik G, Schoppmann SF, Hoetzenecker W, Klepetko W, Guenova E, et al. PD1-positive tumor-infiltrating lymphocytes are associated with poor clinical outcome after pulmonary metastasectomy for colorectal cancer. Oncoimmunology. 2017;6(9):e1331194. doi:10.1080/2162402X.2017.1331194. PMID:28932634.
   PubMed Web of Science ®Google Scholar
• Hecht M, Buttner-Herold M, Erlenbach-Wunsch K, Haderlein M, Croner R, Grutzmann R, Hartmann A, Fietkau R, Distel LV. PD-L1 is upregulated by radiochemotherapy in rectal adenocarcinoma patients and associated with a favourable prognosis. European journal of cancer (Oxford, England : 1990). 2016;65:52–60. doi:10.1016/j.ejca.2016.06.015. PMID:27468145.
   PubMed Web of Science ®Google Scholar
• Lee GH, Malietzis G, Askari A, Bernardo D, Al-Hassi HO, Clark SK. Is right-sided colon cancer different to left-sided colorectal cancer? – a systematic review. European journal of surgical oncology : the journal of the European Society of Surgical Oncology and the British Association of Surgical Oncology. 2015;41(3):300–8. doi:10.1016/j.ejso.2014.11.001. PMID:25468456.
   PubMed Web of Science ®Google Scholar
• Gervaz P, Bucher P, Morel P. Two colons-two cancers: paradigm shift and clinical implications. J Surg Oncol. 2004;88(4):261–6. doi:10.1002/jso.20156. PMID:15565587.
   PubMed Web of Science ®Google Scholar
• Hansen IO, Jess P. Possible better long-term survival in left versus right-sided colon cancer – a systematic review. Dan Med J. 2012;59(6):A4444. PMID:22677242.
   PubMed Web of Science ®Google Scholar
• Holch JW, Ricard I, Stintzing S, Modest DP, Heinemann V. The relevance of primary tumour location in patients with metastatic colorectal cancer: A meta-analysis of first-line clinical trials. European journal of cancer (Oxford, England : 1990). 2017;70:87–98. doi:10.1016/j.ejca.2016.10.007. PMID:27907852.
   PubMed Web of Science ®Google Scholar
• Sunakawa Y, Ichikawa W, Tsuji A, Denda T, Segawa Y, Negoro Y, Shimada K, Kochi M, Nakamura M, Kotaka M, et al. Prognostic Impact of Primary Tumor Location on Clinical Outcomes of Metastatic Colorectal Cancer Treated With Cetuximab Plus Oxaliplatin-Based Chemotherapy: A Subgroup Analysis of the JACCRO CC-05/06 Trials. Clin Colorectal Cancer. 2017;16(3):e171−e80. doi:10.1016/j.clcc.2016.09.010. PMID:27856123.
   PubMed Web of Science ®Google Scholar
• Boeckx N, Koukakis R, Op de Beeck K, Rolfo C, Van Camp G, Siena S, Tabernero J, Douillard JY, André T, Peeters M. Primary tumor sidedness has an impact on prognosis and treatment outcome in metastatic colorectal cancer: results from two randomized first-line panitumumab studies. Annals of oncology : official journal of the European Society for Medical Oncology. 2017;28(8):1862–8. doi:10.1093/annonc/mdx119. PMID:28449055.
   PubMed Web of Science ®Google Scholar
• Arnold D, Lueza B, Douillard JY, Peeters M, Lenz HJ, Venook A, Heinemann V, Van Cutsem E, Pignon JP, Tabernero J, et al. Prognostic and predictive value of primary tumour side in patients with RAS wild-type metastatic colorectal cancer treated with chemotherapy and EGFR directed antibodies in six randomized trials. Annals of oncology : official journal of the European Society for Medical Oncology. 2017;28(8):1713–29. doi:10.1093/annonc/mdx175. PMID:28407110.
   PubMed Web of Science ®Google Scholar
• Frey DM, Droeser RA, Viehl CT, Zlobec I, Lugli A, Zingg U, Oertli D, Kettelhack C, Terracciano L, Tornillo L. High frequency of tumor-infiltrating FOXP3(+) regulatory T cells predicts improved survival in mismatch repair-proficient colorectal cancer patients. Int J Cancer. 2010;126(11):2635–43. PMID:19856313.
   PubMed Web of Science ®Google Scholar
• Salama P, Phillips M, Grieu F, Morris M, Zeps N, Joseph D, Platell C, Iacopetta B. Tumor-infiltrating FOXP3+ T regulatory cells show strong prognostic significance in colorectal cancer. Journal of clinical oncology : official journal of the American Society of Clinical Oncology. 2009;27(2):186–92. doi:10.1200/JCO.2008.18.7229. PMID:19064967.
   PubMed Web of Science ®Google Scholar
• Kim HR, Ha SJ, Hong MH, Heo SJ, Koh YW, Choi EC, et al. PD-L1 expression on immune cells, but not on tumor cells, is a favorable prognostic factor for head and neck cancer patients. Sci Rep. 2016;6:36956. doi:10.1038/srep36956. PMID:27841362.
   PubMed Web of Science ®Google Scholar
• Webb JR, Milne K, Kroeger DR, Nelson BH. PD-L1 expression is associated with tumor-infiltrating T cells and favorable prognosis in high-grade serous ovarian cancer. Gynecol Oncol. 2016;141(2):293–302. doi:10.1016/j.ygyno.2016.03.008. PMID:26972336.
   PubMed Web of Science ®Google Scholar
• Cho J, Lee J, Bang H, Kim ST, Park SH, An JY, Choi MG, Lee JH, Sohn TS, Bae JM, et al. Programmed cell death-ligand 1 expression predicts survival in patients with gastric carcinoma with microsatellite instability. Oncotarget. 2017;8(8):13320–8. doi:10.18632/oncotarget.14519. PMID:28076847.
   PubMedGoogle Scholar
• Thompson RH, Dong H, Lohse CM, Leibovich BC, Blute ML, Cheville JC, et al. PD-1 is expressed by tumor-infiltrating immune cells and is associated with poor outcome for patients with renal cell carcinoma. Clinical cancer research : an official journal of the American Association for Cancer Research. 2007;13(6):1757–61. doi:10.1158/1078-0432.CCR-06-2599. PMID:17363529.
   PubMed Web of Science ®Google Scholar
• Hirano F, Kaneko K, Tamura H, Dong H, Wang S, Ichikawa M, Rietz C, Flies DB, Lau JS, Zhu G, et al. Blockade of B7-H1 and PD-1 by monoclonal antibodies potentiates cancer therapeutic immunity. Cancer Res. 2005;65(3):1089–96. PMID:15705911.
   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. PNAS. 2002;99(19):12293–7. doi:10.1073/pnas.192461099. PMID:12218188.
   PubMed Web of Science ®Google Scholar
• Herbst RS, Soria JC, Kowanetz M, Fine GD, Hamid O, Gordon MS, Sosman JA, McDermott DF, Powderly JD, Gettinger SN, et al. Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients. Nature. 2014;515(7528):563–7. doi:10.1038/nature14011. PMID:25428504.
   PubMed Web of Science ®Google Scholar
• Taube JM, Klein A, Brahmer JR, Xu H, Pan X, Kim JH, Chen L, Pardoll DM, Topalian SL, Anders RA. 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 : an official journal of the American Association for Cancer Research. 2014;20(19):5064–74. doi:10.1158/1078-0432.CCR-13-3271. PMID:24714771.
   PubMed Web of Science ®Google Scholar
• Juneja VR, McGuire KA, Manguso RT, LaFleur MW, Collins N, Haining WN, Freeman GJ, Sharpe AH. PD-L1 on tumor cells is sufficient for immune evasion in immunogenic tumors and inhibits CD8 T cell cytotoxicity. J Exp Med. 2017;214(4):895–904. doi:10.1084/jem.20160801. PMID:28302645.
   PubMed Web of Science ®Google Scholar
• Kleinovink JW, Marijt KA, Schoonderwoerd MJA, van Hall T, Ossendorp F, Fransen MF. PD-L1 expression on malignant cells is no prerequisite for checkpoint therapy. Oncoimmunology. 2017;6(4):e1294299. doi:10.1080/2162402X.2017.1294299. PMID:28507803.
   PubMed Web of Science ®Google Scholar
• Noguchi T, Ward JP, Gubin MM, Arthur CD, Lee SH, Hundal J, Selby MJ, Graziano RF, Mardis ER, Korman AJ, et al. Temporally Distinct PD-L1 Expression by Tumor and Host Cells Contributes to Immune Escape. Cancer Immunol Res. 2017;5(2):106–17. doi:10.1158/2326-6066.CIR-16-0391. PMID:28073774.
   PubMed Web of Science ®Google Scholar
• Powles T, Eder JP, Fine GD, Braiteh FS, Loriot Y, Cruz C, et al. MPDL3280A (anti-PD-L1) treatment leads to clinical activity in metastatic bladder cancer. Nature. 2014;515(7528):558–62. doi:10.1038/nature13904. PMID:25428503.
   PubMed Web of Science ®Google Scholar
• Masugi Y, Nishihara R, Yang J, Mima K, da Silva A, Shi Y, Inamura K, Cao Y, Song M, Nowak JA, et al. Tumour CD274 (PD-L1) expression and T cells in colorectal cancer. Gut. 2017;66(8):1463–73. doi:10.1136/gutjnl-2016-311421. PMID:27196573.
   PubMed Web of Science ®Google Scholar
• Rosenbaum MW, Bledsoe JR, Morales-Oyarvide V, Huynh TG, Mino-Kenudson M. PD-L1 expression in colorectal cancer is associated with microsatellite instability, BRAF mutation, medullary morphology and cytotoxic tumor-infiltrating lymphocytes. Modern pathology : an official journal of the United States and Canadian Academy of Pathology, Inc. 2016;29(9):1104–12. doi:10.1038/modpathol.2016.95. PMID:27198569.
   PubMed Web of Science ®Google Scholar
• Brunnstrom H, Johansson A, Westbom-Fremer S, Backman M, Djureinovic D, Patthey A, Isaksson-Mettävainio M, Gulyas M, Micke P. PD-L1 immunohistochemistry in clinical diagnostics of lung cancer: inter-pathologist variability is higher than assay variability. Modern pathology : an official journal of the United States and Canadian Academy of Pathology, Inc. 2017;30(10):1411–21. doi:10.1038/modpathol.2017.59. PMID:28664936.
   PubMed Web of Science ®Google Scholar
• Wu Y, Cao D, Qu L, Cao X, Jia Z, Zhao T, Wang Q, Jiang J. PD-1 and PD-L1 co-expression predicts favorable prognosis in gastric cancer. Oncotarget. 2017;8(38):64066–82. doi:10.18632/oncotarget.19318. PMID:28969052.
   PubMedGoogle Scholar
• Darb-Esfahani S, Kunze CA, Kulbe H, Sehouli J, Wienert S, Lindner J, Budczies J, Bockmayr M, Dietel M, Denkert C, et al. Prognostic impact of programmed cell death-1 (PD-1) and PD-ligand 1 (PD-L1) expression in cancer cells and tumor-infiltrating lymphocytes in ovarian high grade serous carcinoma. Oncotarget. 2016;7(2):1486–99. doi:10.18632/oncotarget.6429. PMID:26625204.
   PubMed Web of Science ®Google Scholar
• Badoual C, Hans S, Merillon N, Van Ryswick C, Ravel P, Benhamouda N, Levionnois E, Nizard M, Si-Mohamed A, Besnier N, et al. PD-1-expressing tumor-infiltrating T cells are a favorable prognostic biomarker in HPV-associated head and neck cancer. Cancer Res. 2013;73(1):128–38. doi:10.1158/0008-5472.CAN-12-2606. PMID:23135914.
   PubMed Web of Science ®Google Scholar
• Yamauchi M, Morikawa T, Kuchiba A, Imamura Y, Qian ZR, Nishihara R, Liao X, Waldron L, Hoshida Y, Huttenhower C, et al. Assessment of colorectal cancer molecular features along bowel subsites challenges the conception of distinct dichotomy of proximal versus distal colorectum. Gut. 2012;61(6):847–54. doi:10.1136/gutjnl-2011-300865. PMID:22427238.
   PubMed Web of Science ®Google Scholar
• Li FY, Lai MD. Colorectal cancer, one entity or three. Journal of Zhejiang University Science B. 2009;10(3):219–29. doi:10.1631/jzus.B0820273. PMID:19283877.
   PubMed Web of Science ®Google Scholar
• Sheng J, Fang W, Yu J, Chen N, Zhan J, Ma Y, et al. Expression of programmed death ligand-1 on tumor cells varies pre and post chemotherapy in non-small cell lung cancer. Sci Rep. 2016;6:20090. doi:10.1038/srep20090. PMID:26822379.
   PubMed Web of Science ®Google Scholar
• Zhang P, Su DM, Liang M, Fu J. Chemopreventive agents induce programmed death-1-ligand 1 (PD-L1) surface expression in breast cancer cells and promote PD-L1-mediated T cell apoptosis. Mol Immunol. 2008;45(5):1470–6. doi:10.1016/j.molimm.2007.08.013. PMID:17920123.
   PubMed Web of Science ®Google Scholar
• Larsson A, Johansson ME, Wangefjord S, Gaber A, Nodin B, Kucharzewska P, Welinder C, Belting M, Eberhard J, Johnsson A, et al. Overexpression of podocalyxin-like protein is an independent factor of poor prognosis in colorectal cancer. Br J Cancer. 2011;105(5):666–72. doi:10.1038/bjc.2011.295. PMID:21829192.
   PubMed Web of Science ®Google Scholar
• Eberhard J, Gaber A, Wangefjord S, Nodin B, Uhlen M, Ericson Lindquist K, Jirström K. A cohort study of the prognostic and treatment predictive value of SATB2 expression in colorectal cancer. Br J Cancer. 2012;106(5):931–8. doi:10.1038/bjc.2012.34. PMID:22333599.
   PubMed Web of Science ®Google Scholar
• Berglund G, Elmstahl S, Janzon L, Larsson SA. The Malmo Diet and Cancer Study. Design and feasibility. J Intern Med. 1993;233(1):45–51. doi:10.1111/j.1365-2796.1993.tb00647.x. PMID:8429286.
   PubMed Web of Science ®Google Scholar
• Wangefjord S, Brandstedt J, Lindquist KE, Nodin B, Jirstrom K, Eberhard J. Associations of beta-catenin alterations and MSI screening status with expression of key cell cycle regulating proteins and survival from colorectal cancer. Diagn Pathol. 2013;8:10. doi:10.1186/1746-1596-8-10. PMID:23337059.
   PubMed Web of Science ®Google Scholar
• Wangefjord S, Sundstrom M, Zendehrokh N, Lindquist KE, Nodin B, Jirstrom K, Eberhard J. Sex differences in the prognostic significance of KRAS codons 12 and 13, and BRAF mutations in colorectal cancer: a cohort study. Biol Sex Differ. 2013;4(1):17. doi:10.1186/2042-6410-4-17. PMID:24020794.
   PubMedGoogle Scholar