Tumor infiltration by Tbet+ effector T cells and CD20+ B cells is associated with survival in gastric cancer patients

References

• Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F. Cancer incidence and mortality worldwide: Sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 2015; 136(5):E359-86; PMID:25220842
   PubMed Web of Science ®Google Scholar
• Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin 2011; 61:69-90; PMID:21296855
   PubMed Web of Science ®Google Scholar
• Lauren P. The two histological main types of gastric carcinoma: diffuse and so-called intestinal-type carcinoma. An attempt at a histo-clinical classification. Acta Pathol Microbiol Scand 1965; 64:31-49; PMID:14320675
   PubMedGoogle Scholar
• Bouvier AM, Sant M, Verdecchia A, Forman D, Damhuis R, Willem Coebergh J, Crocetti E, Crosignani P, Gafa L, Launoy G, et al. What reasons lie behind long-term survival differences for gastric cancer within Europe? Eur J Cancer 2010; 46:1086-92; PMID:20163952; http://dx.doi.org/10.1016/j.ejca.2010.01.019
   PubMed Web of Science ®Google Scholar
• Vesely MD, Kershaw MH, Schreiber RD, Smyth MJ. Natural innate and adaptive immunity to cancer. Annu Rev Immunol 2011; 29:235-71; PMID:21219185; http://dx.doi.org/10.1146/annurev-immunol-031210-101324
   PubMed Web of Science ®Google Scholar
• Polk DB, Peek RM, Jr. Helicobacter pylori: gastric cancer and beyond. Nat Rev Cancer 2010; 10:403-14; PMID:20495574; http://dx.doi.org/10.1038/nrc2857
   PubMed Web of Science ®Google Scholar
• Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pages C, Tosolini M, Camus M, Berger A, Wind P, et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 2006; 313:1960-4; PMID:17008531; http://dx.doi.org/10.1126/science.1129139
   PubMed Web of Science ®Google Scholar
• Zhang L, Conejo-Garcia JR, Katsaros D, Gimotty PA, Massobrio M, Regnani G, Makrigiannakis A, Gray H, Schlienger K, Liebman MN, et al. Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N Engl J Med 2003; 348:203-13; PMID:12529460; http://dx.doi.org/10.1056/NEJMoa020177
   PubMed Web of Science ®Google Scholar
• Roepman P, Jassem J, Smit EF, Muley T, Niklinski J, van de Velde T, Witteveen AT, Rzyman W, Floore A, Burgers S, et al. An immune response enriched 72-gene prognostic profile for early-stage non-small-cell lung cancer. Clin Cancer Res 2009; 15:284-90; PMID:19118056; http://dx.doi.org/10.1158/1078-0432.CCR-08-1258
   PubMed Web of Science ®Google Scholar
• Tartour E, Gey A, Sastre-Garau X, Lombard Surin I, Mosseri V, Fridman WH. Prognostic value of intratumoral interferon gamma messenger RNA expression in invasive cervical carcinomas. J Natl Cancer Inst 1998; 90:287-94; PMID:9486814; http://dx.doi.org/10.1093/jnci/90.4.287
   PubMed Web of Science ®Google Scholar
• Marth C, Fiegl H, Zeimet AG, Muller-Holzner E, Deibl M, Doppler W, Daxenbichler G. Interferon-gamma expression is an independent prognostic factor in ovarian cancer. Am J Obstet Gynecol 2004; 191:1598-605; PMID:15547530; http://dx.doi.org/10.1016/j.ajog.2004.05.007
   PubMed Web of Science ®Google Scholar
• Mullen AC, High FA, Hutchins AS, Lee HW, Villarino AV, Livingston DM, Kung AL, Cereb N, Yao TP, Yang SY, Reiner SL. Role of T-bet in commitment of TH1 cells before IL-12-dependent selection. Science 2001; 292:1907-10; PMID:11397944; http://dx.doi.org/10.1126/science.1059835
   PubMed Web of Science ®Google Scholar
• Chen LJ, Zheng X, Shen YP, Zhu YB, Li Q, Chen J, Xia R, Zhou SM, Wu CP, Zhang XG, Lu BF, Jiang JT. Higher numbers of T-bet(+) intratumoral lymphoid cells correlate with better survival in gastric cancer. Cancer Immunol Immunother 2013; 62:553-61; PMID:23090288; http://dx.doi.org/10.1007/s00262-012-1358-6
   PubMed Web of Science ®Google Scholar
• Glimcher LH. Trawling for treasure: tales of T-bet. Nat Immunol 2007; 8:448-50; PMID:17440449; http://dx.doi.org/10.1038/ni0507-448
   PubMed Web of Science ®Google Scholar
• Dieu-Nosjean MC, Antoine M, Danel C, Heudes D, Wislez M, Poulot V, Rabbe N, Laurans L, Tartour E, de Chaisemartin L, et al. Long-term survival for patients with non-small-cell lung cancer with intratumoral lymphoid structures. J Clin Oncol 2008; 26:4410-7; PMID:18802153; http://dx.doi.org/10.1200/JCO.2007.15.0284
   PubMed Web of Science ®Google Scholar
• Goc J, Germain C, Vo-Bourgais TK, Lupo A, Klein C, Knockaert S, de Chaisemartin L, Ouakrim H, Becht E, Alifano M, et al. Dendritic cells in tumor-associated tertiary lymphoid structures signal a Th1 cytotoxic immune contexture and license the positive prognostic value of infiltrating CD8+ T cells. Cancer Res 2014; 74:705-15; PMID:24366885; http://dx.doi.org/10.1158/0008-5472.CAN-13-1342
   PubMed Web of Science ®Google Scholar
• Goc J, Fridman WH, Sautes-Fridman C, Dieu-Nosjean MC. Characteristics of tertiary lymphoid structures in primary cancers. Oncoimmunology 2013; 2:e26836; PMID:24498556; http://dx.doi.org/10.4161/onci.26836
   PubMed Web of Science ®Google Scholar
• Ishigami S, Ueno S, Matsumoto M, Okumura H, Arigami T, Uchikado Y, Setoyama T, Arima H, Sasaki K, Kitazono M, et al. Prognostic value of CD208-positive cell infiltration in gastric cancer. Cancer Immunol Immunother 2010; 59:389-95; PMID:19760221; http://dx.doi.org/10.1007/s00262-009-0758-8
   PubMed Web of Science ®Google Scholar
• Bouaziz JD, Yanaba K, Venturi GM, Wang Y, Tisch RM, Poe JC, Tedder TF. Therapeutic B cell depletion impairs adaptive and autoreactive CD4+ T cell activation in mice. Proc Natl Acad Sci U S A 2007; 104:20878-83; PMID:18093919; http://dx.doi.org/10.1073/pnas.0709205105
   PubMed Web of Science ®Google Scholar
• Crawford A, Macleod M, Schumacher T, Corlett L, Gray D. Primary T cell expansion and differentiation in vivo requires antigen presentation by B cells. J Immunol 2006; 176:3498-506; PMID:16517718; http://dx.doi.org/10.4049/jimmunol.176.6.3498
   PubMed Web of Science ®Google Scholar
• Ladanyi A, Kiss J, Mohos A, Somlai B, Liszkay G, Gilde K, Fejos Z, Gaudi I, Dobos J, Timar J. Prognostic impact of B-cell density in cutaneous melanoma. Cancer Immunol Immunother 2011; 60:1729-38; PMID:21779876; http://dx.doi.org/10.1007/s00262-011-1071-x
   PubMed Web of Science ®Google Scholar
• Mahmoud SM, Lee AH, Paish EC, Macmillan RD, Ellis IO, Green AR. The prognostic significance of B lymphocytes in invasive carcinoma of the breast. Breast Cancer Res Treat 2012; 132:545-53; PMID:21671016; http://dx.doi.org/10.1007/s10549-011-1620-1
   PubMed Web of Science ®Google Scholar
• Nielsen JS, Sahota RA, Milne K, Kost SE, Nesslinger NJ, Watson PH, Nelson BH. CD20+ tumor-infiltrating lymphocytes have an atypical CD27- memory phenotype and together with CD8+ T cells promote favorable prognosis in ovarian cancer. Clin Cancer Res 2012; 18:3281-92; PMID:22553348; http://dx.doi.org/10.1158/1078-0432.CCR-12-0234
   PubMed Web of Science ®Google Scholar
• Germain C, Gnjatic S, Tamzalit F, Knockaert S, Remark R, Goc J, Lepelley A, Becht E, Katsahian S, Bizouard G, et al. Presence of B cells in tertiary lymphoid structures is associated with a protective immunity in patients with lung cancer. Am J Respir Crit Care Med 2014; 189:832-44; PMID:24484236; http://dx.doi.org/10.1164/rccm.201309-1611OC
   PubMed Web of Science ®Google Scholar
• Curiel TJ, Coukos G, Zou L, Alvarez X, Cheng P, Mottram P, Evdemon-Hogan M, Conejo-Garcia JR, Zhang L, Burow M, et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 2004; 10:942-9; PMID:15322536; http://dx.doi.org/10.1038/nm1093
   PubMed Web of Science ®Google Scholar
• Wolf D, Wolf AM, Rumpold H, Fiegl H, Zeimet AG, Muller-Holzner E, Deibl M, Gastl G, Gunsilius E, Marth C. The expression of the regulatory T cell-specific forkhead box transcription factor FoxP3 is associated with poor prognosis in ovarian cancer. Clin Cancer Res 2005; 11:8326-31; PMID:16322292; http://dx.doi.org/10.1158/1078-0432.CCR-05-1244
   PubMed Web of Science ®Google Scholar
• Xu L, Xu W, Qiu S, Xiong S. Enrichment of CCR6+Foxp3+ regulatory T cells in the tumor mass correlates with impaired CD8+ T cell function and poor prognosis of breast cancer. Clin Immunol 2010; 135:466-75; PMID:20181533; http://dx.doi.org/10.1016/j.clim.2010.01.014
   PubMed Web of Science ®Google Scholar
• Ladoire S, Martin F, Ghiringhelli F. Prognostic role of FOXP3+ regulatory T cells infiltrating human carcinomas: the paradox of colorectal cancer. Cancer Immunol Immunother 2011; 60:909-18; PMID:21644034; http://dx.doi.org/10.1007/s00262-011-1046-y
   PubMed Web of Science ®Google Scholar
• Shen Z, Zhou S, Wang Y, Li RL, Zhong C, Liang C, Sun Y. Higher intratumoral infiltrated Foxp3+ Treg numbers and Foxp3+/CD8+ ratio are associated with adverse prognosis in resectable gastric cancer. J Cancer Res Clin Oncol 2010; 136:1585-95; PMID:20221835; http://dx.doi.org/10.1007/s00432-010-0816-9
   PubMed Web of Science ®Google Scholar
• Lu X, Liu J, Li H, Li W, Wang X, Ma J, Tong Q, Wu K, Wang G. Conversion of intratumoral regulatory T cells by human gastric cancer cells is dependent on transforming growth factor-beta1. J Surg Oncol 2011; 104:571-7; PMID:21695703; http://dx.doi.org/10.1002/jso.22005
   PubMed Web of Science ®Google Scholar
• Ishigami S, Arigami T, Uenosono Y, Matsumoto M, Okumura H, Uchikado Y, Kita Y, Nishizono Y, Maemura K, Kijima Y, et al. Cancerous HLA class I expression and regulatory T cell infiltration in gastric cancer. Cancer Immunol Immunothera 2012; 61:1663-9; PMID:22374482; http://dx.doi.org/10.1007/s00262-012-1225-5
   PubMed Web of Science ®Google Scholar
• Li Q, Li Q, Chen J, Liu Y, Zhao X, Tan B, Ai J, Zhang Z, Song J, Shan B. Prevalence of Th17 and Treg cells in gastric cancer patients and its correlation with clinical parameters. Oncol Rep 2013; 30:1215-22; PMID:23807713
   PubMed Web of Science ®Google Scholar
• Haas M, Dimmler A, Hohenberger W, Grabenbauer GG, Niedobitek G, Distel LV. Stromal regulatory T-cells are associated with a favourable prognosis in gastric cancer of the cardia. BMC Gastroenterol 2009; 9:65; PMID:19732435; http://dx.doi.org/10.1186/1471-230X-9-65
   PubMed Web of Science ®Google Scholar
• Lee HE, Chae SW, Lee YJ, Kim MA, Lee HS, Lee BL, Kim WH. Prognostic implications of type and density of tumour-infiltrating lymphocytes in gastric cancer. Br J Cancer 2008; 99:1704-11; PMID:18941457; http://dx.doi.org/10.1038/sj.bjc.6604738
   PubMed Web of Science ®Google Scholar
• Giraldo NA, Becht E, Remark R, Damotte D, Sautes-Fridman C, Fridman WH. The immune contexture of primary and metastatic human tumours. Curr Opin Immunol 2014; 27:8-15; PMID:24487185; http://dx.doi.org/10.1016/j.coi.2014.01.001
   PubMed Web of Science ®Google Scholar
• Yamada Y, Saito H, Ikeguchi M. Prevalence and clinical relevance of Th17 cells in patients with gastric cancer. J Surg Res 2012; 178:685-91; PMID:22940035; http://dx.doi.org/10.1016/j.jss.2012.07.055
   PubMed Web of Science ®Google Scholar
• Martin F, Apetoh L, Ghiringhelli F. Controversies on the role of Th17 in cancer: a TGF-beta-dependent immunosuppressive activity? Trends Mol Med 2012; 18:742-9; PMID:23083809; http://dx.doi.org/10.1016/j.molmed.2012.09.007
   PubMed Web of Science ®Google Scholar
• Zhuang Y, Peng LS, Zhao YL, Shi Y, Mao XH, Chen W, Pang KC, Liu XF, Liu T, Zhang JY, et al. CD8(+) T cells that produce interleukin-17 regulate myeloid-derived suppressor cells and are associated with survival time of patients with gastric cancer. Gastroenterology 2012; 143:951-62.e8; PMID:22710190; http://dx.doi.org/10.1053/j.gastro.2012.06.010
   PubMed Web of Science ®Google Scholar
• Lee J, Sohn I, Do IG, Kim KM, Park SH, Park JO, Park YS, Lim HY, Sohn TS, Bae JM, et al. Nanostring-based multigene assay to predict recurrence for gastric cancer patients after surgery. PLoS One 2014; 9:e90133; PMID:24598828; http://dx.doi.org/10.1371/journal.pone.0090133
   PubMed Web of Science ®Google Scholar
• Bindea G, Mlecnik B, Hackl H, Charoentong P, Tosolini M, Kirilovsky A, Fridman WH, Pages F, Trajanoski Z, Galon J. ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics 2009; 25:1091-3; PMID:19237447; http://dx.doi.org/10.1093/bioinformatics/btp101
   PubMed Web of Science ®Google Scholar