Tertiary lymphoid structures are associated with higher tumor grade in primary operable breast cancer patients

BMC Cancer

Volumn 15, Issue 1, 2015, Pages

  Figenschau, Stine L ^a   Fismen, Silje ^b   Fenton, Kristin A ^a   Fenton, Christopher ^a   Mortensen, Elin S ^a,b  

^a UNIVERSITY OF TROMSØ   (Norway)

^b UNIVERSITY HOSPITAL OF NORTH NORWAY   (Norway)

Author keywords

Adaptive immune response; Breast cancer; Immune cell infiltration; Tertiary lymphoid structures; Tumor

Indexed keywords

HORMONE RECEPTOR; TUMOR MARKER;

ADULT; ARTICLE; BREAST CANCER; BREAST CARCINOMA; BREAST SURGERY; CANCER GRADING; CANCER PROGNOSIS; CELL AGGREGATION; CELL INFILTRATION; CELLS BY BODY ANATOMY; CLINICAL FEATURE; CONTROLLED STUDY; DISEASE ASSOCIATION; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; LYMPH NODE METASTASIS; MAJOR CLINICAL STUDY; MIDDLE AGED; MOLECULAR DYNAMICS; OUTCOME ASSESSMENT; PREDICTION; TERTIARY LYMPHOID STRUCTURE; TUMOR VOLUME; AGED; BIOPSY; BREAST NEOPLASMS; CANCER STAGING; FEMALE; IMMUNOLOGY; METASTASIS; PATHOLOGY; TUMOR ASSOCIATED LEUKOCYTE; YOUNG ADULT;

ADULT; AGED; BIOMARKERS, TUMOR; BIOPSY; BREAST NEOPLASMS; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; LYMPHOCYTES, TUMOR-INFILTRATING; MIDDLE AGED; NEOPLASM GRADING; NEOPLASM METASTASIS; NEOPLASM STAGING; TUMOR BURDEN; YOUNG ADULT;

EID: 84928720413     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/s12885-015-1116-1     Document Type: Article

References (53)

1. Fridman WH, Pages F, Sautes-Fridman C, Galon J. The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer. 2012;12:298-306.
2. Aloisi F, Pujol-Borrell R. Lymphoid neogenesis in chronic inflammatory diseases. Nat Rev Immunol. 2006;6:205-17.
3. Drayton DL, Liao S, Mounzer RH, Ruddle NH. Lymphoid organ development: from ontogeny to neogenesis. Nat Immunol. 2006;7:344-53.
4. van de Pavert SA, Mebius RE. New insights into the development of lymphoid tissues. Nat Rev Immunol. 2010;10:664-74.
5. DeNardo DG, Coussens LM. Inflammation and breast cancer. Balancing immune response: crosstalk between adaptive and innate immune cells during breast cancer progression. Breast Cancer Res. 2007;9:212.
6. Coronella JA, Spier C, Welch M, Trevor KT, Stopeck AT, Villar H, et al. Antigen-driven oligoclonal expansion of tumor-infiltrating B cells in infiltrating ductal carcinoma of the breast. J Immunol (Baltimore, Md: 1950). 2002;169:1829-36.
7. Coronella JA, Telleman P, Kingsbury GA, Truong TD, Hays S, Junghans RP. Evidence for an antigen-driven humoral immune response in medullary ductal breast cancer. Cancer Res. 2001;61:7889-99.
8. Nzula S, Going JJ, Stott DI. Antigen-driven clonal proliferation, somatic hypermutation, and selection of B lymphocytes infiltrating human ductal breast carcinomas. Cancer Res. 2003;63:3275-80.
9. Coronella-Wood JA, Hersh EM. Naturally occurring B-cell responses to breast cancer. Cancer Immunol Immunother. 2003;52:715-38.
10. Dieu-Nosjean MC, Antoine M, Danel C, Heudes D, Wislez M, Poulot V, et al. Long-term survival for patients with non-small-cell lung cancer with intratumoral lymphoid structures. J Clin Oncol Off J Am Soc Clin Oncol. 2008;26:4410-7.
11. de Chaisemartin L, Goc J, Damotte D, Validire P, Magdeleinat P, Alifano M, et al. Characterization of chemokines and adhesion molecules associated with T cell presence in tertiary lymphoid structures in human lung cancer. Cancer Res. 2011;71:6391-9.
12. Coppola D, Nebozhyn M, Khalil F, Dai H, Yeatman T, Loboda A, 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.
13. Bergomas F, Grizzi F, Doni A, Pesce S, Laghi L, Allavena P, et al. Tertiary intratumor lymphoid tissue in colo-rectal cancer. Cancers. 2011;4:1-10.
14. Cipponi A, Mercier M, Seremet T, Baurain JF, Theate I, van den Oord J, et al. Neogenesis of lymphoid structures and antibody responses occur in human melanoma metastases. Cancer Res. 2012;72:3997-4007.
15. Messina JL, Fenstermacher DA, Eschrich S, Qu X, Berglund AE, Lloyd MC, et al. 12-Chemokine gene signature identifies lymph node-like structures in melanoma: potential for patient selection for immunotherapy? Sci Rep. 2012;2:765.
16. Takemura S, Braun A, Crowson C, Kurtin PJ, Cofield RH, O'Fallon WM, et al. Lymphoid neogenesis in rheumatoid synovitis. J Immunol (Baltimore, Md: 1950). 2001;167:1072-80.
17. Manzo A, Paoletti S, Carulli M, Blades MC, Barone F, Yanni G, et al. Systematic microanatomical analysis of CXCL13 and CCL21 in situ production and progressive lymphoid organization in rheumatoid synovitis. Eur J Immunol. 2005;35:1347-59.
18. Salomonsson S, Jonsson MV, Skarstein K, Brokstad KA, Hjelmstrom P, Wahren-Herlenius M, et al. Cellular basis of ectopic germinal center formation and autoantibody production in the target organ of patients with Sjogren's syndrome. Arthritis Rheum. 2003;48:3187-201.
19. Barone F, Bombardieri M, Manzo A, Blades MC, Morgan PR, Challacombe SJ, et al. Association of CXCL13 and CCL21 expression with the progressive organization of lymphoid-like structures in Sjogren's syndrome. Arthritis Rheum. 2005;52:1773-84.
20. Mazzucchelli L, Blaser A, Kappeler A, Scharli P, Laissue JA, Baggiolini M, et al. BCA-1 is highly expressed in Helicobacter pylori-induced mucosa-associated lymphoid tissue and gastric lymphoma. J Clin Invest. 1999;104:R49-54.
21. Winter S, Loddenkemper C, Aebischer A, Rabel K, Hoffmann K, Meyer TF, et al. The chemokine receptor CXCR5 is pivotal for ectopic mucosa-associated lymphoid tissue neogenesis in chronic Helicobacter pylori-induced inflammation. J Mol Med (Berlin, Germany). 2010;88:1169-80.
22. Gu-Trantien C, Loi S, Garaud S, Equeter C, Libin M, de Wind A, et al. CD4(+) follicular helper T cell infiltration predicts breast cancer survival. J Clin Invest. 2013;123:2873-92.
23. Martinet L, Garrido I, Filleron T, Le Guellec S, Bellard E, Fournie JJ, 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;71:5678-87.
24. Lal P, Tan LK, Chen B. Correlation of HER-2 status with estrogen and progesterone receptors and histologic features in 3,655 invasive breast carcinomas. Am J Clin Pathol. 2005;123:541-6.
25. Lee AH, Gillett CE, Ryder K, Fentiman IS, Miles DW, Millis RR. Different patterns of inflammation and prognosis in invasive carcinoma of the breast. Histopathology. 2006;48:692-701.
26. Mohammed ZM, Going JJ, Edwards J, Elsberger B, Doughty JC, McMillan DC. The relationship between components of tumour inflammatory cell infiltrate and clinicopathological factors and survival in patients with primary operable invasive ductal breast cancer. Br J Cancer. 2012;107:864-73.
27. Mohammed ZM, Going JJ, Edwards J, Elsberger B, McMillan DC. The relationship between lymphocyte subsets and clinico-pathological determinants of survival in patients with primary operable invasive ductal breast cancer. Br J Cancer. 2013;109:1676-84.
28. Mahmoud SM, Paish EC, Powe DG, Macmillan RD, Grainge MJ, Lee AH, et al. Tumor-infiltrating CD8+ lymphocytes predict clinical outcome in breast cancer. J Clin Oncol. 2011;29:1949-55.
29. Mahmoud S, Lee A, Ellis I, Green A. CD8(+) T lymphocytes infiltrating breast cancer: A promising new prognostic marker? Oncoimmunol. 2012;1:364-5.
30. Nelson BH. CD20+ B cells: the other tumor-infiltrating lymphocytes. J Immunol (Baltimore, Md: 1950). 2010;185:4977-82.
31. 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.
32. Schmidt M, Bohm D, von Torne C, Steiner E, Puhl A, Pilch H, et al. The humoral immune system has a key prognostic impact in node-negative breast cancer. Cancer Res. 2008;68:5405-13.
33. Mohammed ZM, Going JJ, Edwards J, McMillan DC. The role of the tumour inflammatory cell infiltrate in predicting recurrence and survival in patients with primary operable breast cancer. Cancer Treat Rev. 2012;38:943-55.
34. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144:646-74.
35. Bell D, Chomarat P, Broyles D, Netto G, Harb GM, Lebecque S, 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;190:1417-26.
36. Gobert M, Treilleux I, Bendriss-Vermare N, Bachelot T, Goddard-Leon S, Arfi V, 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;69:2000-9.
37. Martinet L, Filleron T, Le Guellec S, Rochaix P, Garrido I, Girard JP. High endothelial venule blood vessels for tumor-infiltrating lymphocytes are associated with lymphotoxin beta-producing dendritic cells in human breast cancer. J Immunol (Baltimore, Md: 1950). 2013;191:2001-8.
38. Lakhani SR, Ellis IO, Schnitt SJ, Tan PH, van der Vijver MJ. World Health Organization Classification of Tumours of the breast. 4th ed. Lyon, France: International Agency for Research on Cancer (IARC); 2012.
39. Silverstein MJ, Lagios MD, Craig PH, Waisman JR, Lewinsky BS, Colburn WJ, et al. A prognostic index for ductal carcinoma in situ of the breast. Cancer. 1996;77:2267-74.
40. Elston CW, Ellis IO. Pathological prognostic factors in breast cancer. I The value of histological grade in breast cancer: experience from a large study with long-term follow-up. Histopathology. 1991;19:403-10.
41. Goc J, Fridman WH, Sautes-Fridman C, Dieu-Nosjean MC. Characteristics of tertiary lymphoid structures in primary cancers. Oncoimmunology. 2013;2:e26836.
42. Ben-Hur H, Cohen O, Schneider D, Gurevich P, Halperin R, Bala U, et al. The role of lymphocytes and macrophages in human breast tumorigenesis: an immunohistochemical and morphometric study. Anticancer Res. 2002;22:1231-8.
43. Bilik R, Mor C, Hazaz B, Moroz C. Characterization of T-lymphocyte subpopulations infiltrating primary breast cancer. Cancer Immunol Immunother. 1989;28:143-7.
44. Tesar BM, Chalasani G, Smith-Diggs L, Baddoura FK, Lakkis FG, Goldstein DR. Direct antigen presentation by a xenograft induces immunity independently of secondary lymphoid organs. J Immunol (Baltimore, Md: 1950). 2004;173:4377-86.
45. Kirk CJ, Hartigan-O'Connor D, Mule JJ. The dynamics of the T-cell antitumor response: chemokine-secreting dendritic cells can prime tumor-reactive T cells extranodally. Cancer Res. 2001;61:8794-802.
46. Schrama D, Thor Straten P, Fischer WH, McLellan AD, Brocker EB, Reisfeld RA, et al. Targeting of lymphotoxin-alpha to the tumor elicits an efficient immune response associated with induction of peripheral lymphoid-like tissue. Immunity. 2001;14:111-21.
47. Schrama D, Voigt H, Eggert AO, Xiang R, Zhou H, Schumacher TN, 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.
48. Goc J, Germain C, Vo-Bourgais TK, Lupo A, Klein C, Knockaert S, 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.
49. Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science (New York, NY). 2011;331:1565-70.
50. Dunn GP, Bruce AT, Ikeda H, Old LJ, Schreiber RD. Cancer immunoediting: from immunosurveillance to tumor escape. Nat Immunol. 2002;3:991-8.
51. Shields JD, Kourtis IC, Tomei AA, Roberts JM, Swartz MA. Induction of lymphoidlike stroma and immune escape by tumors that express the chemokine CCL21. Science (New York, NY). 2010;328:749-52.
52. Tan TT, Coussens LM. Humoral immunity, inflammation and cancer. Curr Opin Immunol. 2007;19:209-16.
53. Ciampricotti M, Vrijland K, Hau CS, Pemovska T, Doornebal CW, Speksnijder EN, et al. Development of metastatic HER2(+) breast cancer is independent of the adaptive immune system. J Pathol. 2011;224:56-66.