Tertiary lymphoid structures in cancer and beyond

Trends in Immunology

Volumn 35, Issue 11, 2014, Pages 571-580

  Dieu Nosjean, Marie Caroline ^a,b,c   Goc, Jérémy ^a,b,c   Giraldo, Nicolas A ^a,b,c   Sautès Fridman, Catherine ^a,b,c   Fridman, Wolf Herman ^a,b,c  

^a CENTRE DE RECHERCHE DES CORDELIERS   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Cancer; Immunotherapy; Prognostic biomarker; Tertiary lymphoid structure

Indexed keywords

AUTOIMMUNITY; DISEASE ASSOCIATION; GRAFT REJECTION; HUMAN; IMMUNE RESPONSE; INFECTION; INFLAMMATORY DISEASE; LYMPHOID ORGAN; NEOPLASM; NONHUMAN; PATHOGENICITY; PROGNOSIS; REVIEW; TERTIARY LYMPHOID STRUCTURE; TUMOR MICROENVIRONMENT; ANIMAL; CELLULAR IMMUNITY; GENETICS; IMMUNOLOGY; INFLAMMATION; PATHOLOGY;

BIOLOGICAL MARKER;

ANIMALS; BIOLOGICAL MARKERS; HUMANS; IMMUNITY, CELLULAR; INFECTION; INFLAMMATION; NEOPLASMS; PROGNOSIS; TUMOR MICROENVIRONMENT;

EID: 84923092072     PISSN: 14714906     EISSN: 14714981     Source Type: Journal    
DOI: 10.1016/j.it.2014.09.006     Document Type: Review

References (83)

1. Boehm T., et al. Evolution of the immune system in the lower vertebrates. Annu. Rev. Genomics Hum. Genet. 2012, 13:127-149.
2. Moyron-Quiroz J.E., et al. Role of inducible bronchus associated lymphoid tissue (iBALT) in respiratory immunity. Nat. Med. 2004, 10:927-934.
3. Moyron-Quiroz J.E., et al. Persistence and responsiveness of immunologic memory in the absence of secondary lymphoid organs. Immunity 2006, 25:643-654.
4. Baddoura F.K., et al. Lymphoid neogenesis in murine cardiac allografts undergoing chronic rejection. Am. J. Transplant. 2005, 5:510-516.
5. Thaunat O., et al. Lymphoid neogenesis in chronic rejection: evidence for a local humoral alloimmune response. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:14723-14728.
6. Kerjaschki D., et al. Lymphatic neoangiogenesis in human kidney transplants is associated with immunologically active lymphocytic infiltrates. J. Am. Soc. Nephrol. 2004, 15:603-612.
7. Nasr I.W., et al. Tertiary lymphoid tissues generate effector and memory T cells that lead to allograft rejection. Am. J. Transplant. 2007, 7:1071-1079.
8. Deteix C., et al. Intragraft Th17 infiltrate promotes lymphoid neogenesis and hastens clinical chronic rejection. J. Immunol. 2010, 184:5344-5351.
9. Neyt K., et al. Tertiary lymphoid organs in infection and autoimmunity. Trends Immunol. 2012, 33:297-305.
10. Lucchesi D., Bombardieri M. The role of viruses in autoreactive B cell activation within tertiary lymphoid structures in autoimmune diseases. J. Leukoc. Biol. 2013, 94:1191-1199.
11. Takahashi Y., et al. Primary and secondary B-cell responses to pulmonary virus infection. Infect. Disord. Drug Targets 2012, 12:232-240.
12. Maglione P.J., et al. B cells moderate inflammatory progression and enhance bacterial containment upon pulmonary challenge with Mycobacterium tuberculosis. J. Immunol. 2007, 178:7222-7234.
13. Khader S.A., et al. In a murine tuberculosis model, the absence of homeostatic chemokines delays granuloma formation and protective immunity. J. Immunol. 2009, 183:8004-8014.
14. Halle S., et al. Induced bronchus-associated lymphoid tissue serves as a general priming site for T cells and is maintained by dendritic cells. J. Exp. Med. 2009, 206:2593-2601.
15. Winter S., et al. The chemokine receptor CXCR5 is pivotal for ectopic mucosa-associated lymphoid tissue neogenesis in chronic Helicobacter pylori-induced inflammation. J. Mol. Med. 2010, 88:1169-1180.
16. Murakami J., et al. Functional B-cell response in intrahepatic lymphoid follicles in chronic hepatitis C. Hepatology 1999, 30:143-150.
17. Mazzucchelli L., et al. BCA-1 is highly expressed in Helicobacter pylori-induced mucosa-associated lymphoid tissue and gastric lymphoma. J. Clin. Invest. 1999, 104:R49-R54.
18. Minutello M.A., et al. Compartmentalization of T lymphocytes to the site of disease: intrahepatic CD4+ T cells specific for the protein NS4 of hepatitis C virus in patients with chronic hepatitis C. J. Exp. Med. 1993, 178:17-25.
19. Pei G., et al. Renal interstitial infiltration and tertiary lymphoid organ neogenesis in IgA nephropathy. Clin. J. Am. Soc. Nephrol. 2014, 9:255-264.
20. Manzo A., et al. Systematic microanatomical analysis of CXCL13 and CCL21 in situ production and progressive lymphoid organization in rheumatoid synovitis. Eur. J. Immunol. 2005, 35:1347-1359.
21. Page G., et al. Anatomic localization of immature and mature dendritic cells in an ectopic lymphoid organ: correlation with selective chemokine expression in rheumatoid synovium. J. Immunol. 2002, 168:5333-5341.
22. Humby F., et al. Ectopic lymphoid structures support ongoing production of class-switched autoantibodies in rheumatoid synovium. PLoS Med. 2009, 6:e1.
23. Van Der Helm-Van Mil A.H.M., et al. Antibodies to citrullinated proteins and differences in clinical progression of rheumatoid arthritis. Arthritis Res. Ther. 2005, 7:R949-R958.
24. Barone F., et al. Association of CXCL13 and CCL21 expression with the progressive organization of lymphoid-like structures in Sjögren's syndrome. Arthritis Rheum. 2005, 52:1773-1784.
25. Barone F., et al. CXCL13, CCL21, and CXCL12 expression in salivary glands of patients with Sjögren's syndrome and MALT lymphoma: association with reactive and malignant areas of lymphoid organization. J. Immunol. 2008, 180:5130-5140.
26. Bombardieri M., et al. Activation-induced cytidine deaminase expression in follicular dendritic cell networks and interfollicular large B cells supports functionality of ectopic lymphoid neogenesis in autoimmune sialoadenitis and MALT lymphoma in Sjögren's syndrome. J. Immunol. 2007, 179:4929-4938.
27. Theander E., et al. Lymphoid organisation in labial salivary gland biopsies is a possible predictor for the development of malignant lymphoma in primary Sjögren's syndrome. Ann. Rheum. Dis. 2011, 70:1363-1368.
28. Magliozzi R., et al. Meningeal B-cell follicles in secondary progressive multiple sclerosis associate with early onset of disease and severe cortical pathology. Brain 2007, 130:1089-1104.
29. Takemura S., et al. Lymphoid neogenesis in rheumatoid synovitis. J. Immunol. 2001, 167:1072-1080.
30. Timmer T.C.G., et al. Inflammation and ectopic lymphoid structures in rheumatoid arthritis synovial tissues dissected by genomics technology: identification of the interleukin-7 signaling pathway in tissues with lymphoid neogenesis. Arthritis Rheum. 2007, 56:2492-2502.
31. Amft N., et al. Ectopic expression of the B cell-attracting chemokine BCA-1 (CXCL13) on endothelial cells and within lymphoid follicles contributes to the establishment of germinal center-like structures in Sjögren's syndrome. Arthritis Rheum. 2001, 44:2633-2641.
32. Serafini B., et al. Detection of ectopic B-cell follicles with germinal centers in the meninges of patients with secondary progressive multiple sclerosis. Brain Pathol. 2004, 14:164-174.
33. Armengol M-P., et al. Chemokines determine local lymphoneogenesis and a reduction of circulating CXCR4+ T and CCR7 B and T lymphocytes in thyroid autoimmune diseases. J. Immunol. 2003, 170:6320-6328.
34. Schreiber R.D., et al. Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science 2011, 331:1565-1570.
35. Fridman W.H., et al. The immune microenvironment: a major player in human cancers. Int. Arch. Allergy Immunol. 2014, 164:13-26.
36. Fridman W.H., et al. The immune contexture in human tumours: impact on clinical outcome. Nat. Rev. Cancer 2012, 12:298-306.
37. Ladányi A., 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.
38. Dieu-Nosjean M-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.
39. Germain C., 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.
40. De Chaisemartin L., 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.
41. Girard J-P., et al. HEVs, lymphatics and homeostatic immune cell trafficking in lymph nodes. Nat. Rev. Immunol. 2012, 12:762-773.
42. Goc J., 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.
43. Goc J., et al. Characteristics of tertiary lymphoid structures in primary cancers. OncoImmunology 2013, 2:e26836.
44. Bergomas F., et al. Tertiary intratumor lymphoid tissue in colo-rectal cancer. Cancers 2011, 4:1-10.
45. McMullen T.P.W., et al. Survival in rectal cancer is predicted by T cell infiltration of tumour-associated lymphoid nodules. Clin. Exp. Immunol. 2010, 161:81-88.
46. Suzuki A., et al. Mature dendritic cells make clusters with T cells in the invasive margin of colorectal carcinoma. J. Pathol. 2002, 196:37-43.
47. Coppola D., 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.
48. Martinet L., 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.
49. Di Caro G., et al. Occurrence of tertiary lymphoid tissue is associated to T cell infiltration and predicts better prognosis in early stage colorectal cancers. Clin. Cancer Res. 2014, 10.1158/1078-0432.CCR-13-2590.
50. Bell D., et al. In breast carcinoma tissue, immature dendritic cells reside within the tumor, whereas mature dendritic cells are located in peritumoral areas. J. Exp. Med. 1999, 190:1417-1426.
51. Coronella J.A., et al. Antigen-driven oligoclonal expansion of tumor-infiltrating B cells in infiltrating ductal carcinoma of the breast. J. Immunol. 2002, 169:1829-1836.
52. Gu-Trantien C., et al. CD4+ follicular helper T cell infiltration predicts breast cancer survival. J. Clin. Invest. 2013, 123:2873-2892.
53. Nzula S., et al. Antigen-driven clonal proliferation, somatic hypermutation, and selection of B lymphocytes infiltrating human ductal breast carcinomas. Cancer Res. 2003, 63:3275-3280.
54. Gobert M., 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.
55. Martinet L., et al. High endothelial venule blood vessels for tumor-infiltrating lymphocytes are associated with lymphotoxin β-producing dendritic cells in human breast cancer. J. Immunol. 2013, 191:2001-2008.
56. Cipponi A., et al. Neogenesis of lymphoid structures and antibody responses occur in human melanoma metastases. Cancer Res. 2012, 72:3997-4007.
57. Martinet L., et al. High endothelial venules (HEVs) in human melanoma lesions: major gateways for tumor-infiltrating lymphocytes. Oncoimmunology 2012, 1:829-839.
58. Messina J.L., et al. 12-Chemokine gene signature identifies lymph node-like structures in melanoma: potential for patient selection for immunotherapy?. Sci. Rep. 2012, 2:765.
59. Nielsen J.S., et al. 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, 18:3281-3292.
60. Willis S.N., et al. The microenvironment of germ cell tumors harbors a prominent antigen-driven humoral response. J. Immunol. 2009, 182:3310-3317.
61. Platonova S., et al. Profound coordinated alterations of intratumoral NK cell phenotype and function in lung carcinoma. Cancer Res. 2011, 71:5412-5422.
62. Remark R., et al. Characteristics and clinical impacts of the immune environments in colorectal and renal cell carcinoma lung metastases: influence of tumor origin. Clin. Cancer Res. 2013, 19:4079-4091.
63. Becht E., et al. Shaping of an effective immune microenvironment to and by cancer cells. Cancer Immunol. Immunother. 2014, 63:991-997.
64. Martinet L., et al. Tumor high endothelial venules (HEVs) predict lymphocyte infiltration and favorable prognosis in breast cancer. Oncoimmunology 2012, 1:789-790.
65. Kirk C.J., et al. The dynamics of the T-cell antitumor response chemokine-secreting dendritic cells can prime tumor-reactive T cells extranodally. Cancer Res. 2001, 61:8794-8802.
66. Schrama D., et al. Immunological tumor destruction in a murine melanoma model by targeted LTalpha independent of secondary lymphoid tissue. Cancer Immunol. Immunother. 2008, 57:85-95.
67. Schrama D., et al. Targeting of lymphotoxin-alpha to the tumor elicits an efficient immune response associated with induction of peripheral lymphoid-like tissue. Immunity 2001, 14:111-121.
68. Bindea G., et al. Spatiotemporal dynamics of intratumoral immune cells reveal the immune landscape in human cancer. Immunity 2013, 39:782-795.
69. Väyrynen J.P., et al. Characteristics and significance of colorectal cancer associated lymphoid reaction. Int. J. Cancer 2014, 134:2126-2135.
70. Schultz K.R., et al. The role of B cells for in vivo T cell responses to a Friend virus-induced leukemia. Science 1990, 249:921-923.
71. Andreu P., et al. FcRgamma activation regulates inflammation-associated squamous carcinogenesis. Cancer Cell 2010, 17:121-134.
72. De Visser K.E., et al. De novo carcinogenesis promoted by chronic inflammation is B lymphocyte dependent. Cancer Cell 2005, 7:411-423.
73. Erdag G., et al. Immunotype and immunohistologic characteristics of tumor-infiltrating immune cells are associated with clinical outcome in metastatic melanoma. Cancer Res. 2012, 72:1070-1080.
74. Galon J., et al. Cancer classification using the Immunoscore: a worldwide task force. J. Transl. Med. 2012, 10:205.
75. Maldonado L., et al. Intramuscular therapeutic vaccination targeting HPV16 induces T cell responses that localize in mucosal lesions. Sci. Transl. Med. 2014, 6:221ra13.
76. Taube J.M., et al. 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, 10.1158/1078-0432.CCR-13-3271.
77. Frederick D.T., et al. BRAF inhibition is associated with enhanced melanoma antigen expression and a more favorable tumor microenvironment in patients with metastatic melanoma. Clin. Cancer Res. 2013, 19:1225-1231.
78. Bargou R., et al. Tumor regression in cancer patients by very low doses of a T cell-engaging antibody. Science 2008, 321:974-977.
79. Pitzalis C., et al. Ectopic lymphoid-like structures in infection, cancer and autoimmunity. Nat. Rev. Immunol. 2014, 14:447-462.
80. Drayton D.L., et al. Ectopic LTαβ directs lymphoid organ neogenesis with concomitant expression of peripheral node addressin and a HEV-restricted sulfotransferase. J. Exp. Med. 2003, 197:1153-1163.
81. Miyagawa S., et al. Prognostic significance of mature dendritic cells and factors associated with their accumulation in metastatic liver tumors from colorectal cancer. Hum. Pathol. 2004, 35:1392-1396.
82. Cherrier M., et al. Notch, Id2, and RORγt sequentially orchestrate the fetal development of lymphoid tissue inducer cells. J. Exp. Med. 2012, 209:729-740.
83. Lutz E.R., et al. Immunotherapy converts nonimmunogenic pancreatic tumors into immunogenic foci of immune regulation. Cancer Immunol. Res. 2014, 2:616-631.