Helper T cell-dominant tertiary lymphoid structures are associated with disease relapse of advanced colorectal cancer

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:E359–11. doi:10.1002/ijc.29210.
   PubMed Web of Science ®Google Scholar
• André T, Boni C, Navarro M, Tabernero J, Hickish T, Topham C, Bonetti A, Clingan P, Bridgewater J, Rivera F, et al. Improved overall survival with oxaliplatin, fluorouracil, and leucovorin as adjuvant treatment in stage II or III colon cancer in the MOSAIC trial. J Clin Oncol. 2009;27:3109–3116. doi:10.1200/JCO.2008.20.6771.
   PubMed Web of Science ®Google Scholar
• Chen DS, Mellman I. Oncology meets immunology: the cancer-immunity cycle. Immunity. 2013;39:1–10. doi:10.1016/j.immuni.2013.07.012.
   PubMed Web of Science ®Google Scholar
• Dieu-Nosjean MC, Goc J, Giraldo NA, Sautès-Fridman C, Fridman WH. Tertiary lymphoid structures in cancer and beyond. Trends Immunol. 2014;35:571–580. doi:10.1016/j.it.2014.09.006.
   PubMed Web of Science ®Google Scholar
• Pitzalis C, Jones GW, Bombardieri M, Jones SA. Ectopic lymphoid-like structures in infection, cancer and autoimmunity. Nat Rev Immunol. 2014;14:447–462. doi:10.1038/nri3700.
   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;74:705–715. doi:10.1158/0008-5472.
   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;189:832–844. doi:10.1164/rccm.201309-1611OC.
   PubMed Web of Science ®Google Scholar
• Hiraoka N, Ino Y, Yamazaki-Itoh R, Kanai Y, Kosuge T, Shimada K. Intratumoral tertiary lymphoid organ is a favourable prognosticator in patients with pancreatic cancer. Br J Cancer. 2015;112:1782–1790. doi:10.1038/bjc.2015.145.
   PubMed Web of Science ®Google Scholar
• Väyrynen JP, Sajanti SA, Klintrup K, Mäkelä J, Herzig KH, Karttunen TJ, Tuomisto A, Mäkinen MJ. Characteristics and significance of colorectal cancer associated lymphoid reaction. Int J Cancer. 2014;134:2126–2135. doi:10.1002/ijc.28533.
   PubMed Web of Science ®Google Scholar
• Goeppert B, Frauenschuh L, Zucknick M, Stenzinger A, Andrulis M, Klauschen F, Joehrens K, Warth A, Renner M, Mehrabi A, et al. Prognostic impact of tumour-infiltrating immune cells on biliary tract cancer. Br J Cancer. 2013;109:2665–2674. doi:10.1038/bjc.2013.610.
   PubMed Web of Science ®Google Scholar
• Di Caro G, Bergomas F, Grizzi F, Doni A, Bianchi P, Malesci A, Laghi L, Allavena P, Mantovani A, Marchesi F. Occurrence of tertiary lymphoid tissue is associated with T-cell infiltration and predicts better prognosis in early-stage colorectal cancers. Clin Cancer Res. 2014;20:2147–2158. doi:10.1158/1078-0432.
   PubMed Web of Science ®Google Scholar
• Posch F, Silina K, Leibl S, Mündlein A, Moch H, Siebenhüner A, Samaras P, Riedl J, Stotz M, Szkandera J, et al. Maturation of tertiary lymphoid structures and recurrence of stage II and III colorectal cancer. Oncoimmunology. 2017;7:e1378844. doi:10.1080/2162402X.2017.1378844.
   PubMed Web of Science ®Google Scholar
• McMullen TP, Lai R, Dabbagh L, Wallace TM, de Gara CJ. Survival in rectal cancer is predicted by T cell infiltration of tumour-associated lymphoid nodules. Clin Exp Immunol. 2010;161:81–88. doi:10.1111/j.1365-2249.2010.04147.x.
   PubMed Web of Science ®Google Scholar
• 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;39:782–795. doi:10.1016/j.immuni.2013.10.003.
   PubMed Web of Science ®Google Scholar
• Sakimura C, Tanaka H, Okuno T, Hiramatsu S, Muguruma K, Hirakawa K, Wanibuchi H, Ohira M. B cells in tertiary lymphoid structures are associated with favorable prognosis in gastric cancer. J Surg Res. 2017;215:74–82. doi:10.1016/j.jss.2017.03.033.
   PubMed Web of Science ®Google Scholar
• Joshi NS, Akama-Garren EH, Lu Y, Lee DY, Chang GP, Li A, DuPage M, Tammela T, Kerper NR, Farago AF, et al. Regulatory T cells in tumor-associated tertiary lymphoid structures suppress anti-tumor T cell responses. Immunity. 2015;43:579–590. doi:10.1016/j.immuni.2015.08.006.
   PubMed Web of Science ®Google Scholar
• Luckheeram RV, Zhou R, Verma AD, Xia B. CD4⁺T cells: differentiation and functions. Clin Dev Immunol. 2012;2012:925135. doi:10.1155/2012/925135.
   PubMedGoogle Scholar
• Via CS, Soloviova K, Puliaiev M, Puliav R, Puliaeva I, Morris SC, Finkelman FD. In vivo IL-4 prevents allo-antigen driven CD8(+) CTL development. Clin Immunol. 2017;180:11–24. doi:10.1016/j.clim.2017.03.008.
   PubMed Web of Science ®Google Scholar
• Poh AR, Ernst M. Targeting macrophages in cancer: from bench to bedside. Front Oncol. 2018;8:49. doi:10.3389/fonc.2018.00049.
   PubMed Web of Science ®Google Scholar
• Sawa S, Cherrier M, Lochner M, Satoh-Takayama N, Fehling HJ, Langa F, Di Santo JP, Eberl G. Lineage relationship analysis of RORgammat+ innate lymphoid cells. Science. 2010;330:665–669. doi:10.1126/science.1194597.
   PubMed Web of Science ®Google Scholar
• Schmutz S, Bosco N, Chappaz S, Boyman O, Acha-Orbea H, Ceredig R, Rolink AG, Finke D. Cutting edge: IL-7 regulates the peripheral pool of adult ROR gamma+ lymphoid tissue inducer cells. J Immunol. 2009;183:2217–2221. doi:10.4049/jimmunol.0802911.
   PubMed Web of Science ®Google Scholar
• Drayton DL, Ying X, Lee J, Lesslauer W, Ruddle NH. Ectopic LT alpha beta directs lymphoid organ neogenesis with concomitant expression of peripheral node addressin and a HEV-restricted sulfotransferase. J Exp Med. 2003;197:1153–1163. doi:10.1084/jem.20021761.
   PubMed Web of Science ®Google Scholar
• Teillaud JL, Dieu-Nosjean MC. Tertiary lymphoid structures: an anti-tumor school for adaptive immune cells and an antibody factory to fight cancer? Front Immunol. 2017;8:830. doi:10.3389/fimmu.2017.00830.
   PubMed Web of Science ®Google Scholar
• Smith JP, Burton GF, Tew JG, Szakal AK. Tingible body macrophages in regulation of germinal center reactions. Dev Immunol. 1998;6:285–294. doi:10.1155/1998/38923.
   PubMedGoogle Scholar
• Kroeger DR, Milne K, Nelson BH. Tumor-infiltrating plasma cells are associated with tertiary lymphoid structures, cytolytic T-cell responses, and superior prognosis in ovarian cancer. Clin Cancer Res. 2016;22:3005–3015. doi:10.1158/1078-0432.CCR-15-2762.
   PubMed Web of Science ®Google Scholar
• Siliņa K, Soltermann A, Attar FM, Casanova R, Uckeley ZM, Thut H, Wandres M, Isajevs S, Cheng P, Curioni-Fontecedro A, et al. Germinal centers determine the prognostic relevance of tertiary lymphoid structures and are impaired by corticosteroids in lung squamous cell carcinoma. Cancer Res. 2018;78:1308–1320. doi:10.1158/0008-5472.CAN-17-1987.
   PubMed Web of Science ®Google Scholar
• Pagès F, Mlecnik B, Marliot F, Bindea G, Ou FS, Bifulco C, Lugli A, Zlobec I, Rau TT, Berger MD, et al. International validation of the consensus immunoscore for the classification of colon cancer: a prognostic and accuracy study. Lancet. 2018;391:2128–2139. doi:10.1016/S0140-6736(18)30789-X.
   PubMed Web of Science ®Google Scholar