Concordance of immune checkpoints within tumor immune contexture and their prognostic significance in gastric cancer

Molecular Oncology

Volumn 10, Issue 10, 2016, Pages 1551-

  Dai, Congqi ^a   Geng, Ruixuan ^b   Wang, Chenchen ^c   Wong, Angela ^d   Qing, Min ^d   Hu, Jianjun ^d   Sun, Yu ^d   Lo, A W I ^e   Li, Jin ^a  

^a TONGJI UNIVERSITY   (China)

^b PEKING UNION MEDICAL COLLEGE HOSPITAL   (China)

^c FUDAN UNIVERSITY SHANGHAI CANCER CENTER   (China)

^d Merck Serono   (China)

^e QUEEN MARY HOSPITAL   (Hong Kong)

Author keywords

Gastric carcinoma; Immune checkpoint; Prognosis; Programmed cell death 1 ligand 1; Tumor infiltrating lymphocytes

Indexed keywords

ANTINEOPLASTIC AGENT; GAMMA INTERFERON; MESSENGER RNA; PROGRAMMED DEATH 1 LIGAND 1;

ADJUVANT CHEMOTHERAPY; ADULT; ARTICLE; CANCER PATIENT; CANCER PROGNOSIS; CANCER STAGING; CANCER SURGERY; CANCER TISSUE; CELL DENSITY; CELL INFILTRATION; CLINICAL OUTCOME; COHORT ANALYSIS; CONTROLLED STUDY; CORRELATIONAL STUDY; EPSTEIN BARR VIRUS; FEMALE; GASTRECTOMY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; OVERALL SURVIVAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; STOMACH CANCER; SURVIVAL RATE; TISSUE SECTION; TUMOR ASSOCIATED LEUKOCYTE; TUMOR IMMUNITY; TUMOR IMMUNOLOGY; VIRUS DETECTION; COMPLICATION; EPSTEIN-BARR VIRUS INFECTIONS; IMMUNOLOGY; ISOLATION AND PURIFICATION; PATHOLOGY; PROGNOSIS; STOMACH; STOMACH NEOPLASMS; SURVIVAL ANALYSIS; VIROLOGY;

ANTIGENS, CD274; EPSTEIN-BARR VIRUS INFECTIONS; FEMALE; HERPESVIRUS 4, HUMAN; HUMANS; IMMUNOHISTOCHEMISTRY; LYMPHOCYTES, TUMOR-INFILTRATING; MALE; MIDDLE AGED; PROGNOSIS; STOMACH; STOMACH NEOPLASMS; SURVIVAL ANALYSIS;

EID: 84991780897     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1016/j.molonc.2016.09.004     Document Type: Article

References (31)

1. Bass, A.J., Thorsson, V., Shmulevich, I., et al., Cancer Genome Atlas Research Network. Comprehensive molecular characterization of gastric adenocarcinoma. Nature 513 (2014), 202–209.
2. Brahmer, J.R., Tykodi, S.S., Chow, L.Q., Hwu, W.J., Topalian, S.L., Hwu, P., Drake, C.G., Camacho, L.H., Kauh, J., Odunsi, K., Pitot, H.C., Hamid, O., Bhatia, S., Martins, R., Eaton, K., Chen, S., Salay, T.M., Alaparthy, S., Grosso, J.F., Korman, A.J., Parker, S.M., Agrawal, S., Goldberg, S.M., Pardoll, D.M., Gupta, A., Wigginton, J.M., Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N. Engl. J. Med. 366 (2012), 2455–2465.
3. Busse, A., Asemissen, A., Nonnenmacher, A., Ochsenreither, S., Fusi, A., Braun, F., Stather, D., Schmittel, A., Miller, K., Thiel, E., Keilholz, U., Systemic immune tuning in renal cell carcinoma: favorable prognostic impact of TGF-beta1 mRNA expression in peripheral blood mononuclear cells. J. Immunother. 34 (2011), 113–119.
4. Droeser, R.A., Hirt, C., Viehl, C.T., Frey, D.M., Nebiker, C., Huber, X., Zlobec, I., Eppenberger-Castori, S., Tzankov, A., Rosso, R., Zuber, M., Muraro, M.G., Amicarella, F., Cremonesi, E., Heberer, M., Iezzi, G., Lugli, A., Terracciano, L., Sconocchia, G., Oertli, D., Spagnoli, G.C., Tornillo, L., Clinical impact of programmed cell death ligand 1 expression in colorectal cancer. Eur. J. Cancer 49 (2013), 2233–2242.
5. Eto, S., Yoshikawa, K., Nishi, M., Higashijima, J., Tokunaga, T., Nakao, T., Kashihara, H., Takasu, C., Iwata, T., Shimada, M., Programmed cell death protein 1 expression is an independent prognostic factor in gastric cancer after curative resection. Gastric Cancer 19 (2016), 466–471.
6. Fridman, W.H., Pagès, F., Sautès-Fridman, C., Galon, J., The immune contexture in human tumours: impact on clinical outcome. Nat. Rev. Cancer 12 (2012), 298–306.
7. Gao, Q., Wang, X.Y., Qiu, S.J., Yamato, I., Sho, M., Nakajima, Y., Zhou, J., Li, B.Z., Shi, Y.H., Xiao, Y.S., Xu, Y., Fan, J., Overexpression of PD-L1 significantly associates with tumor aggressiveness and postoperative recurrence in human hepatocellular carcinoma. Clin. Cancer Res. 15 (2009), 971–979.
8. Gao, Y.F., Peng, R.Q., Li, J., Ding, Y., Zhang, X., Wu, X.J., Pan, Z.Z., Wan, D.S., Zeng, Y.X., Zhang, X.S., The paradoxical patterns of expression of indoleamine 2,3-dioxygenase in colon cancer. J. Transl. Med., 7, 2009, 71, 10.1186/1479-5876-7-71.
9. Giraldo, N.A., Becht, E., Pagès, F., Skliris, G., Verkarre, V., Vano, Y., Mejean, A., Saint-Aubert, N., Lacroix, L., Natario, I., Lupo, A., Alifano, M., Damotte, D., Cazes, A., Triebel, F., Freeman, G.J., Dieu-Nosjean, M.C., Oudard, S., Fridman, W.H., Sautès-Fridman, C., Orchestration and prognostic significance of immune checkpoints in the microenvironment of primary and metastatic renal cell cancer. Clin. Cancer Res. 21 (2015), 3031–3040.
10. Hamanishi, J., Mandai, M., Iwasaki, M., Okazaki, T., Tanaka, Y., Yamaguchi, K., Higuchi, T., Yagi, H., Takakura, K., Minato, N., Honjo, T., Fujii, S., Programmed cell death 1 ligand 1 and tumor-infiltrating CD8+ T lymphocytes are prognostic factors of human ovarian cancer. Proc. Natl. Acad. Sci. U. S. A. 104 (2007), 3360–3365.
11. Hino, R., Kabashima, K., Kato, Y., Yagi, H., Nakamura, M., Honjo, T., Okazaki, T., Tokura, Y., Tumor cell expression of programmed cell death-1 ligand 1 is a prognostic factor for malignant melanoma. Cancer 116 (2010), 1757–1766.
12. Jacquemier, J., Bertucci, F., Finetti, P., Esterni, B., Charafe-Jauffret, E., Thibult, M.L., Houvenaeghel, G., Van den Eynde, B., Birnbaum, D., Olive, D., Xerri, L., High expression of indoleamine 2,3-dioxygenase in the tumour is associated with medullary features and favourable outcome in basal-like breast carcinoma. Int. J. Cancer 130 (2012), 96–104.
13. Jie, H.B., Schuler, P.J., Lee, S.C., Srivastava, R.M., Argiris, A., Ferrone, S., Whiteside, T.L., Ferris, R.L., CTLA-4+ regulatory T cells increased in cetuximab-treated head and neck cancer patients suppress NK cell cytotoxicity and correlate with poor prognosis. Cancer Res. 75 (2015), 2200–2210.
14. Joshi, A.D., Hegde, G.V., Dickinson, J.D., Mittal, A.K., Lynch, J.C., Eudy, J.D., Armitage, J.O., Bierman, P.J., Bociek, R.G., Devetten, M.P., Vose, J.M., Joshi, S.S., ATM, CTLA4, MNDA, and HEM1 in high versus low CD38 expressing B-cell chronic lymphocytic leukemia. Clin. Cancer Res. 13 (2007), 5295–5304.
15. June, C.H., Adoptive T cell therapy for cancer in the clinic. J. Clin. Invest. 117 (2007), 1466–1476.
16. Kim, J.W., Nam, K.H., Ahn, S.H., Park, D.J., Kim, H.H., Kim, S.H., Chang, H., Lee, J.O., Kim, Y.J., Lee, H.S., Kim, J.H., Bang, S.M., Lee, J.S., Lee, K.W., Prognostic implications of immunosuppressive protein expression in tumors as well as immune cell infiltration within the tumor microenvironment in gastric cancer. Gastric Cancer 19 (2016), 42–52.
17. Kim, S.Y., Park, C., Kim, H.J., Park, J., Hwang, J., Kim, J.I., Choi, M.G., Kim, S., Kim, K.M., Kang, M.S., Deregulation of immune response genes in patients with Epstein-Barr virus-associated gastric cancer and outcomes. Gastroenterology 148 (2015), 137–147.
18. Komohara, Y., Morita, T., Annan, D.A., Horlad, H., Ohnishi, K., Yamada, S., Nakayama, T., Kitada, S., Suzu, S., Kinoshita, I., Dosaka-Akita, H., Akashi, K., Takeya, M., Jinushi, M., The coordinated actions of TIM-3 on cancer and myeloid cells in the regulation of tumorigenicity and clinical prognosis in clear cell renal cell carcinomas. Cancer Immunol. Res. 3 (2015), 999–1007.
19. Nomi, T., Sho, M., Akahori, T., Hamada, K., Kubo, A., Kanehiro, H., Nakamura, S., Enomoto, K., Yagita, H., Azuma, M., Nakajima, Y., Clinical significance and therapeutic potential of the programmed death-1 ligand/programmed death-1 pathway in human pancreatic cancer. Clin. Cancer Res. 13 (2007), 2151–2157.
20. Ohigashi, Y., Sho, M., Yamada, Y., Tsurui, Y., Hamada, K., Ikeda, N., Mizuno, T., Yoriki, R., Kashizuka, H., Yane, K., Tsushima, F., Otsuki, N., Yagita, H., Azuma, M., Nakajima, Y., Clinical significance of programmed death-1 ligand-1 and programmed death-1 ligand-2 expression in human esophageal cancer. Clin. Cancer Res. 11 (2005), 2947–2953.
21. Pan, Z.K., Ye, F., Wu, X., An, H.X., Wu, J.X., Clinicopathological and prognostic significance of programmed cell death ligand1 (PD-L1) expression in patients with non-small cell lung cancer: a meta-analysis. J. Thorac. Dis. 7 (2015), 462–470.
22. Qing, Y., Li, Q., Ren, T., Xia, W., Peng, Y., Liu, G.L., Luo, H., Yang, Y.X., Dai, X.Y., Zhou, S.F., Wang, D., Upregulation of PD-L1 and APE1 is associated with tumorigenesis and poor prognosis of gastric cancer. Drug Des. Devel. Ther. 9 (2015), 901–909.
23. Quereux, G., Pandolfino, M.C., Knol, A.C., Khammari, A., Volteau, C., Nguyen, J.M., Dreno, B., Tissue prognostic markers for adoptive immunotherapy in melanoma. Eur. J. Dermatol. 17 (2007), 295–301.
24. 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. J. Clin. Oncol. 27 (2009), 186–192.
25. Schalper, K.A., Velcheti, V., Carvajal, D., Wimberly, H., Brown, J., Pusztai, L., Rimm, D.L., In situ tumor PD-L1 mRNA expression is associated with increased TILs and better outcome in breast carcinomas. Clin. Cancer Res. 20 (2014), 2773–2782.
26. Spranger, S., Spaapen, R.M., Zha, Y., Williams, J., Meng, Y., Ha, T.T., Gajewski, T.F., Upregulation of PD-L1, IDO, and tregs in the melanoma tumor microenvironment is driven by CD8+ T cells. Sci. Transl. Med., 5, 2013 200ra116.
27. Thompson, R.H., Gillett, M.D., Cheville, J.C., Lohse, C.M., Dong, H., Webster, W.S., Krejci, K.G., Lobo, J.R., Sengupta, S., Chen, L., Zincke, H., Blute, M.L., Strome, S.E., Leibovich, B.C., Kwon, E.D., Costimulatory B7-H1 in renal cell carcinoma patients: indicator of tumor aggressiveness and potential therapeutic target. Proc. Natl. Acad. Sci. U. S. A. 101 (2004), 17174–17179.
28. Topalian, S.L., Hodi, F.S., Brahmer, J.R., Gettinger, S.N., Smith, D.C., McDermott, D.F., Powderly, J.D., Carvajal, R.D., Sosman, J.A., Atkins, M.B., Leming, P.D., Spigel, D.R., Antonia, S.J., Horn, L., Drake, C.G., Pardoll, D.M., Chen, L., Sharfman, W.H., Anders, R.A., Taube, J.M., McMiller, T.L., Xu, H., Korman, A.J., Jure-Kunkel, M., Agrawal, S., McDonald, D., Kollia, G.D., Gupta, A., Wigginton, J.M., Sznol, M., Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N. Engl. J. Med. 366 (2012), 2443–2454.
29. Velcheti, V., Schalper, K.A., Carvajal, D.E., Anagnostou, V.K., Syrigos, K.N., Sznol, M., Herbst, R.S., Gettinger, S.N., Chen, L., Rimm, D.L., Programmed death ligand-1 expression in non-small cell lung cancer. Lab. Invest. 94 (2014), 107–116.
30. Wainwright, D.A., Balyasnikova, I.V., Chang, A.L., Ahmed, A.U., Moon, K.S., Auffinger, B., Tobias, A.L., Han, Y., Lesniak, M.S., IDO expression in brain tumors increases the recruitment of regulatory T cells and negatively impacts survival. Clin. Cancer Res. 18 (2012), 6110–6121.
31. Wu, C., Zhu, Y., Jiang, J., Zhao, J., Zhang, X.G., Xu, N., Immunohistochemical localization of programmed death-1 ligand-1 (PD-L1) in gastric carcinoma and its clinical significance. Acta Histochem. 108 (2006), 19–24.