Tertiary Lymphoid Tissue in the Tumor Microenvironment: From Its Occurrence to Immunotherapeutic Implications

REFERENCES

• Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011;144:646–674.
   PubMed Web of Science ®Google Scholar
• Balkwill F, Mantovani A. Inflammation and cancer: back to Virchow? Lancet 2001;357:539–545.
   PubMed Web of Science ®Google Scholar
• Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature 2008;454:436–444.
   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;29:235–271.
   PubMed Web of Science ®Google Scholar
• Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science 2011;331:1565–1570.
   PubMed Web of Science ®Google Scholar
• Di Caro G, Marchesi F, Laghi L, Grizzi F. Immune cells: plastic players along colorectal cancer progression. J Cell Mol Med 2013;17:1088–1095.
   PubMed Web of Science ®Google Scholar
• Galon J, Pages F, Marincola FM, et al. Cancer classification using the Immunoscore: a worldwide task force. J Transl Med 2012;10:205.
   PubMed Web of Science ®Google Scholar
• Restifo NP. A “big data” view of the tumor “immunome”. Immunity 2013;39:631–632.
   PubMed Web of Science ®Google Scholar
• Bindea G, Mlecnik B, Tosolini M, et al. Spatiotemporal dynamics of intratumoral immune cells reveal the immune landscape in human cancer. Immunity 2013;39:782–795.
   PubMed Web of Science ®Google Scholar
• Pages F, Kirilovsky A, Mlecnik B, et al. In situ cytotoxic and memory T cells predict outcome in patients with early-stage colorectal cancer. J Clin Oncol 2009;27:5944–5951.
   PubMed Web of Science ®Google Scholar
• Di Caro G, Marchesi F. Tertiary lymphoid tissue: a gateway for T cells in the tumor microenvironment. Oncoimmunology 2014;3:e28850.
   Google Scholar
• Mellman I, Coukos G, Dranoff G. Cancer immunotherapy comes of age. Nature 2011;480:480–489.
   PubMed Web of Science ®Google Scholar
• Mueller SN, Gebhardt T, Carbone FR, Heath WR. Memory T cell subsets, migration patterns, and tissue residence. Annu Rev Immunol 2013;31:137–161.
   PubMed Web of Science ®Google Scholar
• Aloisi F, Pujol-Borrell R. Lymphoid neogenesis in chronic inflammatory diseases. Nat Rev Immunol 2006;6:205–217.
   PubMed Web of Science ®Google Scholar
• Carragher DM, Rangel-Moreno J, Randall TD. Ectopic lymphoid tissues and local immunity. Semin Immunol 2008;20:26–42.
   PubMedGoogle Scholar
• Neyt K, Perros F, GeurtsvanKessel CH, et al. Tertiary lymphoid organs in infection and autoimmunity. Trends Immunol 2012;33:297–305.
   PubMed Web of Science ®Google Scholar
• de Chaisemartin L, Goc J, Damotte D, et al. Characterization of chemokines and adhesion molecules associated with T cell presence in tertiary lymphoid structures in human lung cancer. Cancer Res 2011;71:6391–6399.
   PubMed Web of Science ®Google Scholar
• Di Caro G, Bergomas F, Grizzi F, et al. 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.
   PubMed Web of Science ®Google Scholar
• Lutz ER, Wu AA, Bigelow E, et al. Immunotherapy converts nonimmunogenic pancreatic tumors into immunogenic foci of immune regulation. Cancer Immunol Res 2014;2:616–631.
   PubMed Web of Science ®Google Scholar
• Futterer A, Mink K, Luz A, et al. The lymphotoxin beta receptor controls organogenesis and affinity maturation in peripheral lymphoid tissues. Immunity 1998;9:59–70.
   PubMedGoogle Scholar
• Randall TD, Carragher DM, Rangel-Moreno J. Development of secondary lymphoid organs. Annu Rev Immunol 2008;26:627–650.
   PubMed Web of Science ®Google Scholar
• Cupedo T, Vondenhoff MF, Heeregrave EJ, et al. Presumptive lymph node organizers are differentially represented in developing mesenteric and peripheral nodes. J Immunol 2004;173:2968–2975.
   PubMed Web of Science ®Google Scholar
• Roozendaal R, Mebius RE. Stromal cell-immune cell interactions. Annu Rev Immunol 2011;29:23–43.
   Google Scholar
• Peduto L, Dulauroy S, Lochner M, et al. Inflammation recapitulates the ontogeny of lymphoid stromal cells. J Immunol 2009;182:5789–5799.
   Google Scholar
• Kratz A, Campos-Neto A, Hanson MS, Ruddle NH. Chronic inflammation caused by lymphotoxin is lymphoid neogenesis. J Exp Med 1996;183:1461–1472.
   PubMed Web of Science ®Google Scholar
• Hjelmstrom P, Fjell J, Nakagawa T, et al. Lymphoid tissue homing chemokines are expressed in chronic inflammation. Am J Pathol 2000;156:1133–1138.
   PubMed Web of Science ®Google Scholar
• Martin AP, Coronel EC, Sano G, et al. A novel model for lymphocytic infiltration of the thyroid gland generated by transgenic expression of the CC chemokine CCL21. J Immunol 2004;173:4791–4798.
   PubMed Web of Science ®Google Scholar
• Furtado GC, Marinkovic T, Martin AP, et al. Lymphotoxin beta receptor signaling is required for inflammatory lymphangiogenesis in the thyroid. Proc Natl Acad Sci USA 2007;104:5026–5031.
   PubMed Web of Science ®Google Scholar
• Marchesi F, Martin AP, Thirunarayanan N, et al. CXCL13 expression in the gut promotes accumulation of IL-22-producing lymphoid tissue-inducer cells, and formation of isolated lymphoid follicles. Mucosal Immunol 2009;2:486–494.
   PubMed Web of Science ®Google Scholar
• Rangel-Moreno J, Moyron-Quiroz JE, Hartson L, et al. Pulmonary expression of CXC chemokine ligand 13, CC chemokine ligand 19, and CC chemokine ligand 21 is essential for local immunity to influenza. Proc Natl Acad Sci USA 2007;104:10577–10582.
   PubMed Web of Science ®Google Scholar
• Furtado GC, Marinkovic T, Martin AP, et al. Lymphotoxin beta receptor signaling is required for inflammatory lymphangiogenesis in the thyroid. Proc Natl Acad Sci USA 2007;104:5026–5031.
   PubMed Web of Science ®Google Scholar
• Ruddle NH. Lymphatic vessels and tertiary lymphoid organs. J Clin Invest 2014;124:953–959.
   PubMed Web of Science ®Google Scholar
• von Andrian UH, Mackay CR. T-cell function and migration. Two sides of the same coin. N Engl J Med 2000;343:1020–1034.
   PubMed Web of Science ®Google Scholar
• Vondenhoff MF, Greuter M, Goverse G, et al. LTbetaR signaling induces cytokine expression and up-regulates lymphangiogenic factors in lymph node anlagen. J Immunol 2009;182:5439–5445.
   Google Scholar
• Tammela T, Alitalo K. Lymphangiogenesis: molecular mechanisms and future promise. Cell 2010;140:460–476.
   PubMed Web of Science ®Google Scholar
• Muniz LR, Pacer ME, Lira SA, Furtado GC. A critical role for dendritic cells in the formation of lymphatic vessels within tertiary lymphoid structures. J Immunol 2011;187:828–834.
   Google Scholar
• Liao S, Ruddle NH. Synchrony of high endothelial venules and lymphatic vessels revealed by immunization. J Immunol 2006;177:3369–3379.
   PubMed Web of Science ®Google Scholar
• Martinet L, Garrido I, Filleron T, et al. Human solid tumors contain high endothelial venules: association with T- and B-lymphocyte infiltration and favorable prognosis in breast cancer. Cancer Res 2011;71:5678–5687.
   PubMed Web of Science ®Google Scholar
• Dieu-Nosjean MC, Goc J, Giraldo NA, et al. Tertiary lymphoid structures in cancer and beyond. Trends Immunol 2014;35(11):571–580.
   PubMed Web of Science ®Google Scholar
• Junt T, Scandella E, Ludewig B. Form follows function: lymphoid tissue microarchitecture in antimicrobial immune defence. Nat Rev Immunol 2008;8:764–775.
   Google Scholar
• Gajewski TF, Woo SR, Zha Y, et al. Cancer immunotherapy strategies based on overcoming barriers within the tumor microenvironment. Curr Opin Immunol 2013;25:268–276.
   PubMed Web of Science ®Google Scholar
• Yu P, Lee Y, Liu W, et al. Priming of naive T cells inside tumors leads to eradication of established tumors. Nat Immunol 2004;5:141–149.
   PubMed Web of Science ®Google Scholar
• Tamada K, Shimozaki K, Chapoval AI, et al. Modulation of T-cell-mediated immunity in tumor and graft-versus-host disease models through the LIGHT co-stimulatory pathway. Nat Med 2000;6:283–289.
   PubMedGoogle Scholar
• Mlecnik B, Bindea G, Pages F, Galon J. Tumor immunosurveillance in human cancers. Cancer Metastasis Rev 2011;30:5–12.
   PubMed Web of Science ®Google Scholar
• Spratt JSJ, Spjut HJ. Prevalence and prognosis of individual clinical and pathologic variables associated with colorectal carcinoma. Cancer 1967;20:1976–1985.
   PubMed Web of Science ®Google Scholar
• Jass JR, Love SB, Northover JM. A new prognostic classification of rectal cancer. Lancet 1987;1:1303–1306.
   PubMed Web of Science ®Google Scholar
• Graham DM, Appelman HD. Crohn's-like lymphoid reaction and colorectal carcinoma: a potential histologic prognosticator. Mod Pathol 1990;3:332–335.
   PubMed Web of Science ®Google Scholar
• Ogino S, Nosho K, Irahara N, et al. Lymphocytic reaction to colorectal cancer is associated with longer survival, independent of lymph node count, microsatellite instability, and CpG island methylator phenotype. Clin Cancer Res 2009;15:6412–6420.
   PubMed Web of Science ®Google Scholar
• Galon J, Costes A, Sanchez-Cabo F, et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 2006;313:1960–1964.
   PubMed Web of Science ®Google Scholar
• Dieu-Nosjean MC, Antoine M, Danel C, et al. Long-term survival for patients with non-small-cell lung cancer with intratumoral lymphoid structures. J Clin Oncol 2008;26:4410–4417.
   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(12):e26836.
   PubMed Web of Science ®Google Scholar
• Germain C, Gnjatic S, Tamzalit F, et al. Presence of B Cells in tertiary lymphoid structures is associated with a protective immunity in lung cancer patients. Am J Respir Crit Care Med 2014;189:832–844.
   Google Scholar
• Goc J, Germain C, Vo-Bourgais TK, et al. Dendritic cells in tumor-associated tertiary lymphoid structures signal a Th1 cytotoxic immune contexture and license the good positive prognostic value of infiltrating CD8+ T Cells. Cancer Res 2014;74:705–715.
   Google Scholar
• Coppola D, Nebozhyn M, Khalil F, et al. Unique ectopic lymph node-like structures present in human primary colorectal carcinoma are identified by immune gene array profiling. Am J Pathol 2011;179:37–45.
   PubMed Web of Science ®Google Scholar
• Messina JL, Fenstermacher DA, Eschrich S, et al. 12-Chemokine gene signature identifies lymph node-like structures in melanoma: potential for patient selection for immunotherapy? Sci Rep 2012;2:765.
   PubMed Web of Science ®Google Scholar
• Sharma P, Wagner K, Wolchok JD, Allison JP. Novel cancer immunotherapy agents with survival benefit: recent successes and next steps. Nat Rev Cancer 2011;11:805–812.
   PubMed Web of Science ®Google Scholar
• Galon J, Angell HK, Bedognetti D, Marincola FM. The continuum of cancer immunosurveillance: prognostic, predictive, and mechanistic signatures. Immunity 2013;39:11–26.
   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;12:269–281.
   PubMed Web of Science ®Google Scholar
• Gajewski TF, Schreiber H, Fu YX. Innate and adaptive immune cells in the tumor microenvironment. Nat Immunol 2013;14:1014–1022.
   PubMed Web of Science ®Google Scholar
• Chen L, Taylor JL, Sabins NC, et al. Extranodal induction of therapeutic immunity in the tumor microenvironment after intratumoral delivery of Tbet gene-modified dendritic cells. Cancer Gene Ther 2013;20:469–477.
   PubMed Web of Science ®Google Scholar
• GeurtsvanKessel CH, Willart MA, Bergen IM, et al. Dendritic cells are crucial for maintenance of tertiary lymphoid structures in the lung of influenza virus-infected mice. J Exp Med 2009;206:2339–2349.
   PubMed Web of Science ®Google Scholar
• Mac Keon S, Gazzaniga S, Mallerman J, et al. Vaccination with dendritic cells charged with apoptotic/necrotic B16 melanoma induces the formation of subcutaneous lymphoid tissue. Vaccine 2010;28:8162–8168.
   Google Scholar
• Veiga-Fernandes H, Coles MC, Foster KE, et al. Tyrosine kinase receptor RET is a key regulator of Peyer's patch organogenesis. Nature 2007;446:547–551.
   PubMedGoogle Scholar
• Finn OJ. Cancer immunology. N Engl J Med 2008;358:2704–2715.
   PubMed Web of Science ®Google Scholar
• Gobert M, Treilleux I, Bendriss-Vermare N, et al. Regulatory T cells recruited through CCL22/CCR4 are selectively activated in lymphoid infiltrates surrounding primary breast tumors and lead to an adverse clinical outcome. Cancer Res 2009;69:2000–2009.
   PubMed Web of Science ®Google Scholar
• Gu-Trantien C, Loi S, Garaud S, et al. CD4(+) follicular helper T cell infiltration predicts breast cancer survival. J Clin Invest 2013;123:2873–2892.
   PubMed Web of Science ®Google Scholar
• Martinet L, Filleron T, Le Guellec S, et al. High endothelial venule blood vessels for tumor-infiltrating lymphocytes are associated with lymphotoxin beta-producing dendritic cells in human breast cancer. J Immunol 2013;191:2001–2008.
   Google Scholar
• McMullen TP, Lai R, Dabbagh L, et al. Survival in rectal cancer is predicted by T cell infiltration of tumour-associated lymphoid nodules. Clin Exp Immunol 2010;161:81–88.
   PubMed Web of Science ®Google Scholar
• Vayrynen JP, Sajanti SA, Klintrup K, et al. Characteristics and significance of colorectal cancer associated lymphoid reaction. Int J Cancer 2014;134:2126–2135.
   PubMed Web of Science ®Google Scholar
• Ladanyi A, Kiss J, Somlai B, et al. Density of DC-LAMP(+) mature dendritic cells in combination with activated T lymphocytes infiltrating primary cutaneous melanoma is a strong independent prognostic factor. Cancer Immunol Immunother 2007;56:1459–1469.
   PubMed Web of Science ®Google Scholar