Histological analysis of γδ Tlymphocytes infiltrating human triple-negative breast carcinomas

Frontiers in Immunology

Volumn 5, Issue DEC, 2014, Pages

  Hidalgo, Jose Villacorta ^a,b,c   Bronsert, Peter ^a,b   Orlowska Volk, Marzenna ^a   Díaz, Liliana B ^c   Stickeler, Elmar ^a,b   Werner, Martin ^a,b   Schmitt Graeff, Annette ^a   Kayser, Gian ^a   Malkovsky, Miroslav ^d   Fisch, Paul ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c HOSPITAL DE CLÍNICAS JOSÉ DE SAN MARTÍN   (Argentina)

^d UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

breast cancer; Histology; Paraffin material; Triple negative breast cancer; T cells

Indexed keywords

CASPASE ACTIVATED DEOXYRIBONUCLEASE; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTROGEN RECEPTOR; PROGESTERONE RECEPTOR;

ADULT; AGED; ARTICLE; BREAST FIBROADENOMA; CANCER PROGNOSIS; CELL HETEROGENEITY; CELLULAR DISTRIBUTION; CLINICAL ARTICLE; CONTROLLED STUDY; GAMMA DELTA T LYMPHOCYTE; HISTOLOGY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LYMPHOCYTIC INFILTRATION; MEDULLARY CARCINOMA; MICROSCOPY; PROTEIN EXPRESSION; TREATMENT OUTCOME; TRIPLE NEGATIVE BREAST CANCER; TUMOR MICROENVIRONMENT; TUMOR VOLUME;

EID: 84919492923     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2014.00632     Document Type: Article

References (50)

1. Ferlay J, Soerjomataram I, Ervik M, Dikshit R, Eser S, Mathers C, et al. GLOBOCAN 2012 v1.0, Cancer Incidence and Mortality Worldwide: IARC Cancer Base No. 11 [Internet]. Lyon: International Agency for Research on Cancer (2013). Available from: http://globocan.iarc.fr
2. Metzger-Filho O, Tutt A, de Azambuja E, Saini KS, Viale G, Loi S, et al. Dissecting the heterogeneity of triple-negative breast cancer. J Clin Oncol (2012) 15:1879-87. doi:10.1200/JCO.2011.38.2010
3. Loi S, Michiels S, Salgado R, Sirtaine N, Jose V, Fumagalli D, et al. Tumor infiltrating lymphocytes are prognostic in triple negative breast cancer and predictive for trastuzumab benefit in early breast cancer: results from the FinHER trial. Ann Oncol (2014) 25:1544-50. doi:10.1093/annonc/mdu112
4. Adams S, Gray R, Demaria S, Goldstein LJ, Perez EA, Shulman LN, et al. Prognostic value of tumor-infiltrating lymphocytes in triple-negative breast cancers from two phase III randomized adjuvant breast cancer trials: ECOG 2197 and ECOG 1199. J Clin Oncol (2014) 32:2959-66. doi:10.1200/JCO.2013.55.0491
5. Dent R, Trudeau M, Pritchard KI, Hanna WM, Kahn HK, Sawka CA, et al. Triple-negative breast cancer: clinical features and patterns of recurrence. Clin Cancer Res (2007) 15(Pt 1):4429-34. doi:10.1158/1078-0432.CCR-06-3045
6. Reis-Filho JS, Tutt AN. Triple negative tumours: a critical review. Histopathology (2008) 52:108-18. doi:10.1111/j.1365-2559.2007.02889.x
7. Ridolfi RL, Rosen PP, Port A, Kinne D, Miké V. Medullary carcinoma of the breast: a clinicopathologic study with 10 year follow-up. Cancer (1977) 40:1365-85. doi:10.1002/1097-0142(197710)40:4<1365::AID-CNCR2820400402>3.0.CO;2-N
8. Huober J, Gelber S, Goldhirsch A, Coates AS, Viale G, öhlschlegel C, et al. Prognosis of medullary breast cancer: analysis of 13 International Breast Cancer Study Group (IBCSG) trials. Ann Oncol (2012) 23(11):2843-51. doi:10.1093/annonc/mds105
9. Rosen PP. Rosen's Breast Pathology. 3rd ed. (Vol. 15). Dover: Lippincott Williams & Wilkins (2008). p. 449-67.
10. Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pages C, et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science (2006) 313:1960-4. doi:10.1126/science.1129139
11. Zhang L, Conejo-Garcia JR, Katsaros D, Gimotty PA, Massobrio M, Regnani G, et al. Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N Engl J Med (2003) 348:203-13. doi:10.1056/NEJMoa020177
12. Kawai O, Ishii G, Kubota K, Murata Y, Naito Y, Mizuno T, et al. Predominant infiltration of macrophages and CD8+ T Cells in cancer nests is a significant predictor of survival in stage IV non-small cell lung cancer. Cancer (2008) 113:1387-95. doi:10.1002/cncr.23712
13. Aaltomaa S, Lipponen P, Eskelinen M, Kosma VM, Marin S, Alhava E, et al. Lymphocyte infiltrates as a prognostic variable in female breast cancer. Eur J Cancer (1992) 28A:859-64. doi:10.1016/0959-8049(92)90134-N
14. Pagès F, Galon J, Dieu-Nosjean MC, Tartour E, Sautès-Fridman C, Fridman WH. Immune infiltration in human tumors: a prognostic factor that should not be ignored. Oncogene (2010) 29(8):1093-102. doi:10.1038/onc.2009.416
15. Fukunaga A, Miyamoto M, Cho Y, Murakami S, Kawarada Y, Oshikiri T, et al. CD8+ tumor-infiltrating lymphocytes together with CD4+ tumor-infiltrating lymphocytes and dendritic cells improve the prognosis of patients with pancreatic adenocarcinoma. Pancreas (2004) 28:e26-31. doi:10.1097/00006676-200401000-00023
16. Clemente CG, Mihm MC Jr, Bufalino R, Zurrida S, Collini P, Cascinelli N. Prognostic value of tumor infiltrating lymphocytes in the vertical growth phase of primary cutaneous melanoma. Cancer (1996) 77(7):1303-10. doi:10.1002/(SICI)1097-0142(19960401)77:7<1303::AID-CNCR12>3.0.CO;2-5
17. Schumacher K, Haensch W, Roefzaad C, Schlag PM. Prognostic significance of activated CD8+ T cell infiltrations within esophageal carcinomas. Cancer Res (2001) 61:3932-6.
18. Seo AN, Lee HJ, Kim EJ, Kim HJ, Jang MH, Lee HE, et al. Tumour-infiltrating CD8+ lymphocytes as an independent predictive factor for pathological complete response to primary systemic therapy in breast cancer. Br J Cancer (2013) 109(10):2705-13. doi:10.1038/bjc.2013.634
19. 3+ tumor-infiltrating lymphocytes in breast cancer depends on estrogen receptor and human epidermal growth factor receptor-2 expression status and concurrent cytotoxic T-cell infiltration. Breast Cancer Res (2014) 16(5):432. doi:10.1186/s13058-014-0432-8
20. 4+ cytotoxic T cells predicts poor survival and high recurrence rates in patients with hepatocellular carcinoma. Hepatology (2013) 58(1):139-49. doi:10.1002/hep.26054
21. Groh V, Rhinehart R, Secrist H, Bauer S, Grabstein KH, Spies T. Broad tumor-associated expression and recognition by tumor-derived γδ T cells of MICA and MICB. Proc Natl Acad Sci U S A (1999) 96:6879-84. doi:10.1073/pnas.96.12.6879
22. Vetter CS, Groh V, thor Straten P, Spies T, Bröcker EB, Becker JC. Expression of stress-induced MHC class I related chain molecules on human melanoma. J Invest Dermatol (2002) 118(4):600-5. doi:10.1046/j.1523-1747.2002.01700.x
23. Todaro M, D'Asaro M, Caccamo N, Iovino F, Francipane MG, Meraviglia S, et al. Efficient killing of human colon cancer stem cells by γδ T lymphocytes. J Immunol (2009) 182:7287-96. doi:10.4049/jimmunol.0804288
24. Viey E, Fromont G, Escudier B, Morel Y, Da Rocha S, Chouaib S, et al. Phosphostim-activated γδ T cells kill autologous metastatic renal cell carcinoma. J Immunol (2005) 174(3):1338-47. doi:10.4049/jimmunol.174.3.1338
25. Maeurer MJ, Martin D, Walter W, Liu K, Zitvogel L, Halusczcak K, et al. Human intestinal Vδ+ lymphocytes recognize tumor cells of epithelial origin. J Exp Med (1996) 183(4):1681-96. doi:10.1084/jem.183.4.1681
26. Chien YH, Bonneville M.γδ T cell receptors. Cell Mol Life Sci (2006) 63(18):2089-94. doi:10.1007/s00018-006-6020-z
27. Viney J, MacDonald TT, Spencer J. γδ T cells in the gut epithelium. Gut (1990) 31(8):841-4. doi:10.1136/gut.31.8.841
28. Hohlfeld R, Engel AG, Ii K, Harper MC. Polymyositis mediated by T lymphocytes that express the γδ receptor. N Engl J Med (1991) 324(13):877-81. doi:10.1056/NEJM199103283241303
29. Vantourout P, Hayday A. Six-of-the-best: unique contributions of γδ T cells to immunology. Nat Rev Immunol (2013) 13(2):88-100. doi:10.1038/nri3384
30. Hayday A, Tigelaar R. Immunoregulation in the tissues by γδ T cells. Nat Rev Immunol (2003) 3(3):233-42. doi:10.1038/nri1030
31. Behr C, Poupot R, Peyrat MA, Poquet Y, Constant P, Dubois P, et al. Plasmodium falciparum stimuli for human γδ T cells are related to phosphorylated antigens of mycobacteria. Infect Immun (1996) 64(8):2892-6.
32. Sandstrom A, Peigné CM, Léger A, Crooks JE, Konczak F, Gesnel MC, et al. The intracellular B30.2 domain of butyrophilin 3A1 binds phosphoantigens to mediate activation of human Vγ9Vδ2 T cells. Immunity (2014) 40(4):490-500. doi:10.1016/j.immuni.2014.03.003
33. Poggi A, Venturino C, Catellani S, Clavio M, Miglino M, Gobbi M, et al. Vd1 T lymphocytes from B-CLL patients recognize ULBP3 expressed on leukemic B cells and up-regulated by trans-retinoic acid. Cancer Res (2004) 64(24):9172-9. doi:10.1158/0008-5472.CAN-04-2417
34. 7 breast carcinoma cell line and can be detected among the T cells that infiltrate breast tumors. Clin Immunol Immunopathol (1993) 67(1):17-24. doi:10.1006/clin.1993.1040
35. Loi S. Host antitumor immunity plays a role in the survival of patients with newly diagnosed triple-negative breast cancer. J Clin Oncol (2014) 32(27):2935-7. doi:10.1200/JCO.2014.56.7677
36. 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(5):403-10. doi:10.1111/j.1365-2559.1991.tb00229.x
37. Roullet M, Gheith SM, Mauger J, Junkins-Hopkins JM, Choi JK. Percentage of γδ T cells in panniculitis by paraffin immunohistochemical analysis. Am J Clin Pathol (2009) 131(6):820-6. doi:10.1309/AJCPMG37MXKYPUBE
38. Denkert C, Loibl S, Noske A, Roller M, Müller BM, Komor M, et al. Tumor-associated lymphocytes as an independent predictor of response to neoadjuvant chemotherapy in breast cancer. J Clin Oncol (2010) 28(1):105-13. doi:10.1200/JCO.2009.23.7370
39. Duan WR, Garner DS, Williams SD, Funckes-Shippy CL, Spath IS, Blomme EA. Comparison of immunohistochemistry for activated caspase-3 and cleaved cytokeratin 18 with the TUNEL method for quantification of apoptosis in histological sections of PC-3 subcutaneous xenografts. J Pathol (2003) 199(2):221-8. doi:10.1002/path.1289
40. 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(15):1949-55. doi:10.1200/JCO.2010.30.5037
41. 4 are selectively activated in lymphoid infiltrates surrounding primary breast tumors and lead to an adverse clinical outcome. Cancer Res (2009) 69:2000-9. doi:10.1158/0008-5472.CAN-08-2360
42. Badve S, Dabbs DJ, Schnitt SJ, Baehner FL, Decker T, Eusebi V, et al. Basal-like and triple-negative breast cancers: a critical review with an emphasis on the implications for pathologists and oncologists. Mod Pathol (2011) 24(2):157-67. doi:10.1038/modpathol.2010.200
43. Ma C, Zhang Q, Ye J, Wang F, Zhang Y, Wevers E, et al. Tumor-infiltrating γδ T lymphocytes predict clinical outcome in human breast cancer. J Immunol (2012) 189(10):5029-36. doi:10.4049/jimmunol.1201892
44. Flucke U, Flucke MT, Hoy L, Breuer E, Goebbels R, Rhiem K, et al. Distinguishing medullary carcinoma of the breast from high-grade hormone receptor-negative invasive ductal carcinoma: an immunohistochemical approach. Histopathology (2010) 56(7):852-9. doi:10.1111/j.1365-2559.2010.03555.x
45. Kostianets O, Antoniuk S, Filonenko V, Kiyamova R. Immunohistochemical analysis of medullary breast carcinoma autoantigens in different histological types of breast carcinomas. Diagn Pathol (2012) 7:161. doi:10.1186/1746-1596-7-161
46. 2 chemokine pathway through recruitment of type 1 cytotoxic γδ T lymphocytes to tumor beds. J Immunol (2013) 190(12):6673-80. doi:10.4049/jimmunol.1300434
47. Kajiwara M, Toyoshima S, Yao T, Tanaka M, Tsuneyoshi M. Apoptosis and cell proliferation in medullary carcinoma of the breast: a comparative study between medullary and non-medullary carcinoma using the TUNEL method and immunohistochemistry. J Surg Oncol (1999) 70(4):209-16. doi:10.1002/(SICI)1096-9098(199904)70:4<209::AID-JSO2>3.0.CO;2-6
48. 95)/Fas ligand expression in medullary carcinoma of the breast. J Pathol (2000) 192(2):166-73. doi:10.1002/1096-9896(2000)9999:9999<::AID-PATH689>3.3.CO;2-1
49. Vincent-Salomon A, Gruel N, Lucchesi C, MacGrogan G, Dendale R, Sigal-Zafrani B, et al. Identification of typical medullary breast carcinoma as a genomic sub-group of basal-like carcinomas, a heterogeneous new molecular entity. Breast Cancer Res (2007) 9(2):R24. doi:10.1186/bcr1666
50. Ye J, Ma C, Hsueh EC, Eickhoff CS, Zhang Y, Varvares MA, et al. Tumor-derived γδ regulatory T cells suppress innate and adaptive immunity through the induction of immunosenescence. J Immunol (2013) 190(5):2403-14. doi:10.4049/jimmunol.1202369