PDL1 expression is a poor-prognosis factor in soft-tissue sarcomas

OncoImmunology

Volumn 6, Issue 3, 2017, Pages

  Bertucci, François ^a,b,c,d   Finetti, Pascal ^a   Perrot, Delphine ^b,d   Leroux, Agnès ^d,e   Collin, Françoise ^d,f   Le Cesne, Axel ^d,g   Coindre, Jean Michel ^d,h   Blay, Jean Yves ^d,i   Birnbaum, Daniel ^a   Mamessier, Emilie ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

^b INSTITUT PAOLI CALMETTES   (France)

^c AIX MARSEILLE UNIVERSITY   (France)

^d French Sarcoma Group   (France)

^e CENTRE ALEXIS VAUTRIN   (France)

^f Centre George Fra ois Leclerc   (France)

^g INSTITUT GUSTAVE ROUSSY   (France)

^h INSTITUT BERGONIÉ   (France)

ⁱ CENTRE LÉON BÉRARD   (France)

Author keywords

DNA microarray; gene expression; immune response; PDL1; prognosis; soft tissue sarcoma

Indexed keywords

ALPHA INTERFERON; GAMMA INTERFERON; PROGRAMMED DEATH 1 LIGAND 1; TUMOR NECROSIS FACTOR;

ADOLESCENT; ADULT; AGED; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER GRADING; CANCER PROGNOSIS; CANCER RECURRENCE; CHILD; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DNA MICROARRAY; FEMALE; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LEIOMYOSARCOMA; LIPOSARCOMA; MAJOR CLINICAL STUDY; MALE; METASTASIS FREE SURVIVAL; PROTEIN EXPRESSION; RECEIVER OPERATING CHARACTERISTIC; SOFT TISSUE SARCOMA; TUMOR VOLUME;

EID: 85014507894     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.1080/2162402X.2016.1278100     Document Type: Article

References (85)

1. Wunder JS, Nielsen TO, Maki RG, O'Sullivan B, Alman BA. Opportunities for improving the therapeutic ratio for patients with sarcoma. Lancet Oncol 2007; 8:513-24; PMID:17540303; http://dx.doi.org/10.1016/S1470-2045(07)70169-9
2. Group ESESNW. Soft tissue and visceral sarcomas:ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol 2014; 25 Suppl 3:iii102-12; PMID:25210080; http://dx.doi.org/10.1093/annonc/mdu254
3. Pang A, Carbini M, Maki RG. Contemporary therapy for advanced soft-tissue sarcomas in adults:a review. JAMA 0ncol 2016; 2:941-7; PMID:27148906; http://dx.doi.org/10.1001/jamaoncol.2016.0241
4. Demetri GD, von Mehren M, Jones RL, Hensley ML, Schuetze SM, Staddon A, Milhem M, Elias A, Ganjoo K, Tawbi H, et al. Efficacy and safety of trabectedin or dacarbazine for metastatic liposarcoma or leiomyosarcoma after failure of conventional chemotherapy:results of a phase III randomized multicenter clinical trial. J Clin Oncol 2016; 34:786-93; PMID:26371143; http://dx.doi.org/10.1200/JCO.2015.62.4734
5. Schoffski P, Chawla S, Maki RG, Italiano A, Gelderblom H, Choy E, Grignani G, Camargo V, Bauer S, Rha SY, et al. Eribulin versus dacarbazine in previously treated patients with advanced liposarcoma or leiomyosarcoma:a randomised, open-label, multicentre, phase 3 trial. Lancet 2016; 387:1629-37; PMID:26874885; http://dx.doi.org/10.1016/S0140-6736(15)01283-0
6. van der Graaf WT, Blay JY, Chawla SP, Kim DW, Bui-Nguyen B, Casali PG, Schoffski P, Aglietta M, Staddon AP, Beppu Y, et al. Pazopanib for metastatic soft-tissue sarcoma (PALETTE):a randomised, double-blind, placebo-controlled phase 3 trial. Lancet 2012; 379:1879-86; PMID:22595799; http://dx.doi.org/10.1016/S0140-6736(12)60651-5
7. Ratan R, Patel SR. Chemotherapy for soft tissue sarcoma. Cancer 2016; 122:2952-60; PMID:27434055; http://dx.doi.org/10.1002/cncr.30191
8. D'Angelo SP, Shoushtari AN, Agaram NP, Kuk D, Qin LX, Carvajal RD, Dickson MA, Gounder M, Keohan ML, Schwartz GK, et al. Prevalence of tumor-infiltrating lymphocytes and PD-L1 expression in the soft tissue sarcoma microenvironment. Hum Pathol 2015; 46:357-65; PMID:25540867; http://dx.doi.org/10.1016/j.humpath.2014.11.001
9. Hu JS, Skeate JG, Kast WM, Wong MK. Immunotherapy in sarcoma:a brief review. Sarcoma Res Int 2014; 1:1-8.
10. Coley WB, II. Contribution to the knowledge of sarcoma. Ann Surg 1891; 14:199-220; PMID:17859590; http://dx.doi.org/10.1097/00000658-189112000-00015
11. Wiemann B, Starnes CO. Coley's toxins, tumor necrosis factor and cancer research:a historical perspective. Pharmacol Ther 1994; 64:529-64; PMID:7724661; http://dx.doi.org/10.1016/0163-7258(94)90023-X
12. Sakamoto A, Shiba E, Hisaoka M. Short-term spontaneous regression of myxofibrosarcoma in the scapular region. Skeletal Radiol 2014; 43:1487-90; PMID:24910124; http://dx.doi.org/10.1007/s00256-014-1914-6
13. Penn I. Sarcomas in organ allograft recipients. Transplantation 1995; 60:1485-91; PMID:8545879; http://dx.doi.org/10.1097/00007890-199560120-00020
14. Fujii H, Arakawa A, Utsumi D, Sumiyoshi S, Yamamoto Y, Kitoh A, Ono M, Matsumura Y, Kato M, Konishi K, et al. CD8(+) tumor-infiltrating lymphocytes at primary sites as a possible prognostic factor of cutaneous angiosarcoma. Int J Cancer 2014; 134:2393-402; PMID:24243586; http://dx.doi.org/10.1002/ijc.28581
15. Kim JR, Moon YJ, Kwon KS, Bae JS, Wagle S, Kim KM, Park HS, Lee H, Moon WS, Chung MJ, et al. Tumor infiltrating PD1-positive lymphocytes and the expression of PD-L1 predict poor prognosis of soft tissue sarcomas. PLoS One 2013; 8:e82870; PMID:24349382; http://dx.doi.org/10.1371/journal.pone.0082870
16. Feng Y, Shen J, Gao Y, Liao Y, Cote G, Choy E, Chebib I, Mankin H, Hornicek F, Duan Z. Expression of programmed cell death ligand 1 (PD-L1) and prevalence of tumor-infiltrating lymphocytes (TILs) in chordoma. Oncotarget 2015; 6:11139-49; PMID:25871477; http://dx.doi.org/10.18632/oncotarget.3576
17. Sorbye SW, Kilvaer T, Valkov A, Donnem T, Smeland E, Al-Shibli K, Bremnes RM, Busund LT. Prognostic impact of lymphocytes in soft tissue sarcomas. PLoS One 2011; 6:e14611; PMID:21298041; http://dx.doi.org/10.1371/journal.pone.0014611
18. Sorbye SW, Kilvaer TK, Valkov A, Donnem T, Smeland E, Al-Shibli K, Bremnes RM, Busund LT. Prognostic impact of peritumoral lymphocyte infiltration in soft tissue sarcomas. BMC Clin Pathol 2012; 12:5; PMID:22375962; http://dx.doi.org/10.1186/1472-6890-12-5
19. Tseng WW, Malu S, Zhang M, Chen J, Sim GC, Wei W, Ingram D, Somaiah N, Lev DC, Pollock RE, et al. Analysis of the intratumoral adaptive immune response in well differentiated and dedifferentiated retroperitoneal liposarcoma. Sarcoma 2015; 2015:547460; PMID:25705114; http://dx.doi.org/10.1155/2015/547460
20. Shurell E, Singh AS, Crompton JG, Jensen S, Li Y, Dry S, Nelson S, Chmielowski B, Bernthal N, Federman N, et al. Characterizing the immune microenvironment of malignant peripheral nerve sheath tumor by PD-L1 expression and presence of CD8+ tumor infiltrating lymphocytes. Oncotarget 2016; 7(39):64300-8; PMID:27588404; http://dx.doi.org/10.18632/oncotarget.11734
21. Lee CH, Espinosa I, Vrijaldenhoven S, Subramanian S, Montgomery KD, Zhu S, Marinelli RJ, Peterse JL, Poulin N, Nielsen TO, et al. Prognostic significance of macrophage infiltration in leiomyosarcomas. Clin Cancer Res 2008; 14:1423-30; PMID:18316565; http://dx.doi.org/10.1158/1078-0432.CCR-07-1712
22. Nabeshima A, Matsumoto Y, Fukushi J, Iura K, Matsunobu T, Endo M, Fujiwara T, Iida K, Fujiwara Y, Hatano M, et al. Tumour-associated macrophages correlate with poor prognosis in myxoid liposarcoma and promote cell motility and invasion via the HB-EGF-EGFR-PI3K/Akt pathways. Br J Cancer 2015; 112:547-55; PMID:25562433; http://dx.doi.org/10.1038/bjc.2014.637
23. Meyers PA, Schwartz CL, Krailo MD, Healey JH, Bernstein ML, Betcher D, Ferguson WS, Gebhardt MC, Goorin AM, Harris M, et al. Osteosarcoma:the addition of muramyl tripeptide to chemotherapy improves overall survival–a report from the children's oncology group. J Clin Oncol 2008; 26:633-8; PMID:18235123; http://dx.doi.org/10.1200/JCO.2008.14.0095
24. Lai JP, Rosenberg AZ, Miettinen MM, Lee CC. NY-ESO-1 expression in sarcomas:A diagnostic marker and immunotherapy target. Oncoimmunology 2012; 1:1409-10; PMID:23243610; http://dx.doi.org/10.4161/onci.21059
25. Robbins PF, Kassim SH, Tran TL, Crystal JS, Morgan RA, Feldman SA, Yang JC, Dudley ME, Wunderlich JR, Sherry RM, et al. A pilot trial using lymphocytes genetically engineered with an NY-ESO-1-reactive T-cell receptor:long-term follow-up and correlates with response. Clin Cancer Res 2015; 21:1019-27; PMID:25538264; http://dx.doi.org/10.1158/1078-0432.CCR-14-2708
26. Robbins PF, Morgan RA, Feldman SA, Yang JC, Sherry RM, Dudley ME, Wunderlich JR, Nahvi AV, Helman LJ, Mackall CL, et al. Tumor regression in patients with metastatic synovial cell sarcoma and melanoma using genetically engineered lymphocytes reactive with NY-ESO-1. J Clin Oncol 2011; 29:917-24; PMID:21282551; http://dx.doi.org/10.1200/JCO.2010.32.2537
27. Bucklein V, Adunka T, Mendler AN, Issels R, Subklewe M, Schmollinger JC, Noessner E. Progressive natural killer cell dysfunction associated with alterations in subset proportions and receptor expression in soft-tissue sarcoma patients. Oncoimmunology 2016; 5:e1178421; PMID:27622032; http://dx.doi.org/10.1080/2162402X.2016.1178421
28. Zitvogel L, Kroemer G. Targeting PD-1/PD-L1 interactions for cancer immunotherapy. Oncoimmunology 2012; 1:1223-5; PMID:23243584; http://dx.doi.org/10.4161/onci.21335
29. Gatalica Z, Snyder C, Maney T, Ghazalpour A, Holterman DA, Xiao N, Overberg P, Rose I, Basu GD, Vranic S, et al. Programmed cell death 1 (PD-1) and its ligand (PD-L1) in common cancers and their correlation with molecular cancer type. Cancer Epidemiol Biomarkers Prev 2014; 23(12):2965-70; PMID:25392179; http://dx.doi.org/10.1158/1055-9965.EPI-14-0654
30. Amarnath S, Mangus CW, Wang JC, Wei F, He A, Kapoor V, Foley JE, Massey PR, Felizardo TC, Riley JL, et al. The PDL1-PD1 axis converts human TH1 cells into regulatory T cells. Science Transl Med 2011; 3:111ra20; PMID:22133721; http://dx.doi.org/10.1126/scitranslmed.3003130
31. Brahmer JR, Tykodi SS, Chow LQ, Hwu WJ, Topalian SL, Hwu P, Drake CG, Camacho LH, Kauh J, Odunsi K, et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 2012; 366:2455-65; PMID:22658128; http://dx.doi.org/10.1056/NEJMoa1200694
32. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, Powderly JD, Carvajal RD, Sosman JA, Atkins MB, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012; 366:2443-54; PMID:22658127; http://dx.doi.org/10.1056/NEJMoa1200690
33. 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. Clin Cancer Res 2014; 20:5064-74; PMID:24714771; http://dx.doi.org/10.1158/1078-0432.CCR-13-3271
34. Herbst RS, Baas P, Kim DW, Felip E, Perez-Gracia JL, Han JY, Molina J, Kim JH, Arvis CD, Ahn MJ, et al. Pembrolizumab versus docetaxel for previously treated, PD-L1-positive, advanced non-small-cell lung cancer (KEYNOTE-010):a randomised controlled trial. Lancet 2016; 387:1540-50; PMID:26712084; http://dx.doi.org/10.1016/S0140-6736(15)01281-7
35. 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; 515:563-7; PMID:25428504; http://dx.doi.org/10.1038/nature14011
36. Powles T, Eder JP, Fine GD, Braiteh FS, Loriot Y, Cruz C, Bellmunt J, Burris HA, Petrylak DP, Teng SL, et al. MPDL3280A (anti-PD-L1) treatment leads to clinical activity in metastatic bladder cancer. Nature 2014; 515:558-62; PMID:25428503; http://dx.doi.org/10.1038/nature13904
37. Bertucci F, Finetti P, Birnbaum D, Mamessier E. The PD1/PDL1 axis, a promising therapeutic target in aggressive breast cancers. Oncoimmunology 2016; 5:e1085148; PMID:27141340; http://dx.doi.org/10.1080/2162402X.2015.1085148
38. Zou W, Wolchok JD, Chen L. PD-L1 (B7-H1) and PD-1 pathway blockade for cancer therapy:Mechanisms, response biomarkers, and combinations. Science Transl Med 2016; 8:328rv4; PMID:26936508; http://dx.doi.org/10.1126/scitranslmed.aad7118
39. George S, Barysauskas CM, Solomon S, Tahlil K, Malley R, Hohos M, Polson K, Loucks M, Wagner AJ, Merriam P, et al. Phase 2 study of nivolumab in metastatic leiomyosarcoma of the uterus. J Clin Oncol 2016; 34:(suppl; abstr 11007).
40. Paoluzzi L, Ghesani MV, Cacavio A, Rapkiewicz A, Rosen G. Anti-PD1 therapy with nivolumab in sarcoma. J Clin Oncol 2016; 34 (suppl; abstr 11047).
41. Tawbi HA, Burgess MA, Crowley J, Van Tine BA, Hu J, Schuetze S, D'Angelo SP, Attia S, Priebat DA, Okuno SH, et al. Safety and efficacy of PD-1 blockade using pembrolizumab in patients with advanced soft tissue (STS) and bone sarcomas (BS):results of SARC028—A multicenter phase II study. J Clin Oncol 2016; 34 (suppl; abstr 11006).
42. Kim C, Kim EK, Jung H, Chon HJ, Han JW, Shin KH, Hu H, Kim KS, Choi YD, Kim S, et al. Prognostic implications of PD-L1 expression in patients with soft tissue sarcoma. BMC Cancer 2016; 16:434; PMID:27393385; http://dx.doi.org/10.1186/s12885-016-2451-6
43. Palmer C, Diehn M, Alizadeh AA, Brown PO. Cell-type specific gene expression profiles of leukocytes in human peripheral blood. BMC Genomics 2006; 7:115; PMID:16704732; http://dx.doi.org/10.1186/1471-2164-7-115
44. Bindea G, Mlecnik B, Tosolini M, Kirilovsky A, Waldner M, Obenauf AC, Angell H, Fredriksen T, Lafontaine L, Berger A, et al. Spatiotemporal dynamics of intratumoral immune cells reveal the immune landscape in human cancer. Immunity 2013; 39:782-95; PMID:24138885; http://dx.doi.org/10.1016/j.immuni.2013.10.003
45. Rody A, Holtrich U, Pusztai L, Liedtke C, Gaetje R, Ruckhaeberle E, Solbach C, Hanker L, Ahr A, Metzler D, et al. T-cell metagene predicts a favorable prognosis in estrogen receptor-negative and HER2-positive breast cancers. Breast Cancer Res 2009; 11:R15; PMID:19272155; http://dx.doi.org/10.1186/bcr2234
46. Sabatier R, Finetti P, Mamessier E, Raynaud S, Cervera N, Lambaudie E, Jacquemier J, Viens P, Birnbaum D, Bertucci F. Kinome expression profiling and prognosis of basal breast cancers. Mol Cancer 2011; 10:86; PMID:21777462; http://dx.doi.org/10.1186/1476-4598-10-86
47. Gatza ML, Lucas JE, Barry WT, Kim JW, Wang Q, Crawford MD, Datto MB, Kelley M, Mathey-Prevot B, Potti A, et al. A pathway-based classification of human breast cancer. Proc Natl Acad Sci U S A 2010; 107:6994-9; PMID:20335537; http://dx.doi.org/10.1073/pnas.0912708107
48. Chakravarti N, Prieto VG. Predictive factors of activity of anti-programmed death-1/programmed death ligand-1 drugs:immunohistochemistry analysis. Transl Lung Cancer Res 2015; 4:743-51; PMID:26798583; http://dx.doi.org/10.3978/j.issn.2218-6751.2015.12.10
49. Rimm D, Schalper K, Pusztai L. Unvalidated antibodies and misleading results. Breast Cancer Res Treat 2014; 147:457-8; PMID:25086631; http://dx.doi.org/10.1007/s10549-014-3061-0
50. Velcheti V, Schalper KA, Carvajal DE, Anagnostou VK, Syrigos KN, Sznol M, Herbst RS, Gettinger SN, Chen L, Rimm DL. Programmed death ligand-1 expression in non-small cell lung cancer. Lab Invest 2014; 94:107-16; PMID:24217091; http://dx.doi.org/10.1038/labinvest.2013.130
51. Gadiot J, Hooijkaas AI, Kaiser AD, van Tinteren H, van Boven H, Blank C. Overall survival and PD-L1 expression in metastasized malignant melanoma. Cancer 2011; 117:2192-201; PMID:21523733; http://dx.doi.org/10.1002/cncr.25747
52. McLaughlin J, Han G, Schalper KA, Carvajal-Hausdorf D, Pelekanou V, Rehman J, Velcheti V, Herbst R, LoRusso P, Rimm DL. Quantitative assessment of the heterogeneity of PD-L1 expression in non-small-cell lung cancer. JAMA Oncol 2016; 2:46-54; PMID:26562159; http://dx.doi.org/10.1001/jamaoncol.2015.3638
53. Ilie M, Hofman V, Dietel M, Soria JC, Hofman P. Assessment of the PD-L1 status by immunohistochemistry:challenges and perspectives for therapeutic strategies in lung cancer patients. Virchows Arch 2016; 468:511-25; PMID:26915032; http://dx.doi.org/10.1007/s00428-016-1910-4
54. Sholl LM, Aisner DL, Allen TC, Beasley MB, Borczuk AC, Cagle PT, Capelozzi V, Dacic S, Hariri L, Kerr KM, et al. Programmed death ligand-1 immunohistochemistry–a new challenge for pathologists:a perspective from members of the pulmonary pathology society. Arch Pathol Lab Med 2016; 140:341-4; PMID:26780537; http://dx.doi.org/10.5858/arpa.2015-0506-SA
55. Schalper KA, Velcheti V, Carvajal D, Wimberly H, Brown J, Pusztai L, Rimm DL. In situ tumor PD-L1 mRNA expression is associated with increased TILs and better outcome in breast carcinomas. Clin Cancer Res 2014; 20:2773-82; PMID:24647569; http://dx.doi.org/10.1158/1078-0432.CCR-13-2702
56. Soliman H, Khalil F, Antonia S. PD-L1 expression is increased in a subset of basal type breast cancer cells. PLoS One 2014; 9:e88557; PMID:24551119; http://dx.doi.org/10.1371/journal.pone.0088557
57. Shen JK, Cote GM, Choy E, Yang P, Harmon D, Schwab J, Nielsen GP, Chebib I, Ferrone S, Wang X, et al. Programmed cell death ligand 1 expression in osteosarcoma. Cancer Immunol Res 2014; 2:690-8; PMID:24866169; http://dx.doi.org/10.1158/2326-6066.CIR-13-0224
58. Ohigashi Y, Sho M, Yamada Y, Tsurui Y, Hamada K, Ikeda N, Mizuno T, Yoriki R, Kashizuka H, Yane K, et al. Clinical significance of programmed death-1 ligand-1 and programmed death-1 ligand-2 expression in human esophageal cancer. Clin Cancer Res 2005; 11:2947-53; PMID:15837746; http://dx.doi.org/10.1158/1078-0432.CCR-04-1469
59. Sabatier R, Finetti P, Mamessier E, Adelaide J, Chaffanet M, Ali HR, Viens P, Caldas C, Birnbaum D, Bertucci F. Prognostic and predictive value of PDL1 expression in breast cancer. Oncotarget 2015; 6:5449-64; PMID:25669979; http://dx.doi.org/10.18632/oncotarget.3216
60. Ottaiano A, De Chiara A, Fazioli F, Talamanca AA, Mori S, Botti G, Milano A, Apice G. Biological prognostic factors in adult soft tissue sarcomas. Anticancer Res 2005; 25:4519-26; PMID:16334136
61. Chibon F, Lagarde P, Salas S, Perot G, Brouste V, Tirode F, Lucchesi C, de Reynies A, Kauffmann A, Bui B, et al. Validated prediction of clinical outcome in sarcomas and multiple types of cancer on the basis of a gene expression signature related to genome complexity. Nat Med 2010; 16:781-87; PMID:20581836; http://dx.doi.org/10.1038/nm.2174
62. 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; 25:2178-84; PMID:25193987; http://dx.doi.org/10.1093/annonc/mdu445
63. Kiyasu J, Miyoshi H, Hirata A, Arakawa F, Ichikawa A, Niino D, Sugita Y, Yufu Y, Choi I, Abe Y, et al. Expression of programmed cell death ligand 1 is associated with poor overall survival in patients with diffuse large B-cell lymphoma. Blood 2015; 126:2193-201; PMID:26239088; http://dx.doi.org/10.1182/blood-2015-02-629600
64. Massi D, Brusa D, Merelli B, Ciano M, Audrito V, Serra S, Buonincontri R, Baroni G, Nassini R, Minocci D, et al. PD-L1 marks a subset of melanomas with a shorter overall survival and distinct genetic and morphological characteristics. Ann Oncol 2014; 25:2433-42; PMID:25223485; http://dx.doi.org/10.1093/annonc/mdu452
65. 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; 66:3381-5; PMID:16585157; http://dx.doi.org/10.1158/0008-5472.CAN-05-4303
66. Birnbaum DJ, Finetti P, Lopresti A, Gilabert M, Poizat F, Turrini O, Raoul JL, Delpero JR, Moutardier V, Birnbaum D, et al. Prognostic value of PDL1 expression in pancreatic cancer. Oncotarget 2016; PMID:27589570; http://dx.doi.org/10.18632/oncotarget.11685
67. 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. Eur J Cancer 2013; 49:2233-42; PMID:23478000; http://dx.doi.org/10.1016/j.ejca.2013.02.015
68. Bertucci F, Finetti P, Mamessier E, Pantaleo MA, Astolfi A, Ostrowski J, Birnbaum D. PDL1 expression is an independent prognostic factor in localized GIST. Oncoimmunology 2015; 4(5):e1002729; PMID:26155391; http://dx.doi.org/10.1080/2162402X.2014.1002729
69. Lipson EJ, Vincent JG, Loyo M, Kagohara LT, Luber BS, Wang H, Xu H, Nayar SK, Wang TS, Sidransky D, 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; PMID:24416729; http://dx.doi.org/10.1158/2326-6066.CIR-13-0034
70. Toulmonde M, Adam J, Bessede A, Ranchere-Vince D, Velasco V, Brouste V, Blay JY, Mir O, Italiano A. Integrative assessment of expression and prognostic value of PDL1, IDO, and kynurenine in 371 primary soft tissue sarcomas with genomic complexity. J Clin Oncol 2016; 34:(suppl; abstr 11008) 2016 ASCO Annual Meeting.
71. Shen JK, Cote GM, Choy E, Hornicek FJ, Duan Z. Targeting programmed cell death ligand 1 in osteosarcoma:an auto-commentary on therapeutic potential. Oncoimmunology 2014; 3:e954467; PMID:25610746; http://dx.doi.org/10.4161/21624011.2014.954467
72. Vacchelli E, Aranda F, Eggermont A, Sautes-Fridman C, Tartour E, Kennedy EP, Platten M, Zitvogel L, Kroemer G, Galluzzi L. Trial watch:IDO inhibitors in cancer therapy. Oncoimmunology 2014; 3:e957994; PMID:25941578; http://dx.doi.org/10.4161/21624011.2014.957994
73. He Y, Rivard CJ, Rozeboom L, Yu H, Ellison K, Kowalewski A, Zhou C, Hirsch FR. Lymphocyte-activation gene-3, an important immune checkpoint in cancer. Cancer Sci 2016; 107:1193-7; PMID:27297395; http://dx.doi.org/10.1111/cas.12986
74. Anderson AC, Joller N, Kuchroo VK. Lag-3, Tim-3, and TIGIT:Co-inhibitory receptors with specialized functions in immune regulation. Immunity 2016; 44:989-1004; PMID:27192565; http://dx.doi.org/10.1016/j.immuni.2016.05.001
75. Kurtulus S, Sakuishi K, Ngiow SF, Joller N, Tan DJ, Teng MW, Smyth MJ, Kuchroo VK, Anderson AC. TIGIT predominantly regulates the immune response via regulatory T cells. J Clin Invest 2015; 125:4053-62; PMID:26413872; http://dx.doi.org/10.1172/JCI81187
76. Nielsen TO, West RB, Linn SC, Alter O, Knowling MA, O'Connell JX, Zhu S, Fero M, Sherlock G, Pollack JR, et al. Molecular characterisation of soft tissue tumours:a gene expression study. Lancet 2002; 359:1301-7; PMID:11965276; http://dx.doi.org/10.1016/S0140-6736(02)08270-3
77. West RB, Nuyten DS, Subramanian S, Nielsen TO, Corless CL, Rubin BP, Montgomery K, Zhu S, Patel R, Hernandez-Boussard T, et al. Determination of stromal signatures in breast carcinoma. PLoS Biol 2005; 3:e187; PMID:15869330; http://dx.doi.org/10.1371/journal.pbio.0030187
78. Beck AH, Lee CH, Witten DM, Gleason BC, Edris B, Espinosa I, Zhu S, Li R, Montgomery KD, Marinelli RJ, et al. Discovery of molecular subtypes in leiomyosarcoma through integrative molecular profiling. Oncogene 2010; 29:845-54; PMID:19901961; http://dx.doi.org/10.1038/onc.2009.381
79. Ylipaa A, Hunt KK, Yang J, Lazar AJ, Torres KE, Lev DC, Nykter M, Pollock RE, Trent J, Zhang W. Integrative genomic characterization and a genomic staging system for gastrointestinal stromal tumors. Cancer 2011; 117:380-9; PMID:20818650; http://dx.doi.org/10.1002/cncr.25594
80. Gibault L, Perot G, Chibon F, Bonnin S, Lagarde P, Terrier P, Coindre JM, Aurias A. New insights in sarcoma oncogenesis:a comprehensive analysis of a large series of 160 soft tissue sarcomas with complex genomics. J Pathol 2011; 223:64-71; PMID:21125665; http://dx.doi.org/10.1002/path.2787
81. Renner M, Wolf T, Meyer H, Hartmann W, Penzel R, Ulrich A, Lehner B, Hovestadt V, Czwan E, Egerer G, et al. Integrative DNA methylation and gene expression analysis in high-grade soft tissue sarcomas. Genome Biol 2013; 14:r137; PMID:24345474; http://dx.doi.org/10.1186/gb-2013-14-12-r137
82. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003; 4:249-64; PMID:12925520; http://dx.doi.org/10.1093/biostatistics/4.2.249
83. Bertucci F, Finetti P, Viens P, Birnbaum D. EndoPredict predicts for the response to neoadjuvant chemotherapy in ER-positive, HER2-negative breast cancer. Cancer Lett 2014; 355:70-5; PMID:25218596; http://dx.doi.org/10.1016/j.canlet.2014.09.014
84. Hochberg Y, Benjamini Y. More powerful procedures for multiple significance testing. Stat Med 1990; 9:811-8; PMID:2218183; http://dx.doi.org/10.1002/sim.4780090710
85. McShane LM, Altman DG, Sauerbrei W, Taube SE, Gion M, Clark GM, Statistics Subcommittee of the NCIEWGoCD. Reporting recommendations for tumour marker prognostic studies (REMARK). Br J Cancer 2005; 93:387-91; PMID:16106245; http://dx.doi.org/10.1038/sj.bjc.6602678