Tumor-infiltrating lymphocyte composition, organization and PD-1/PD-l1 expression are linked in breast cancer

OncoImmunology

Volumn 6, Issue 1, 2017, Pages

  Buisseret, Laurence ^a   Garaud, Soizic ^a   De Wind, Alexandre ^a   Van den Eynden, Gert ^b   Boisson, Anais ^a   Solinas, Cinzia ^a   Gu Trantien, Chunyan ^a,d   Naveaux, Céline ^a   Lodewyckx, Jean Nicolas ^a   Duvillier, Hugues ^a   Craciun, Ligia ^a   Veys, Isabelle ^a   Larsimont, Denis ^a   Piccart Gebhart, Martine ^a   Stagg, John ^c   Sotiriou, Christos ^a   Willard Gallo, Karen ^a  

^a JULES BORDET INSTITUTE   (Belgium)

^b Institut Jules Bordet ^*  (Belgium)

^c CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^d UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

Breast cancer; Lymphocytes; PD 1; PD L1; Tertiary lymphoid structures; Tumor infiltrating

Indexed keywords

CD19 ANTIGEN; CD27 ANTIGEN; CD45RO ANTIGEN; PROGRAMMED DEATH 1 LIGAND 1; PROGRAMMED DEATH 1 RECEPTOR;

ADULT; ARTICLE; B LYMPHOCYTE; BREAST CANCER; BREAST TISSUE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; FLOW CYTOMETRY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LYMPHOCYTE SUBPOPULATION; MAJOR CLINICAL STUDY; MEMORY CELL; PHENOTYPE; PROTEIN EXPRESSION; TERTIARY LYMPHOID STRUCTURE; TUMOR ASSOCIATED LEUKOCYTE;

EID: 85019477463     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.1080/2162402X.2016.1257452     Document Type: Article

References (59)

1. Weiss SA, Hanniford D, Hernando E, Osman I. Revisiting determinants of prognosis in cutaneous melanoma. Cancer 2015; 121:4108-23; PMID:26308244; http://dx.doi.org/10.1002/cncr.29634
2. Reissfelder C, Stamova S, Gossmann C, Braun M, Bonertz A, Walliczek U, Grimm M, Rahbari NN, Koch M, Saadati M et al. Tumor-specific cytotoxic T lymphocyte activity determines colorectal cancer patient prognosis. J Clin Invest 2015; 125:739-51; PMID:25562322; http://dx.doi.org/10.1172/JCI74894
3. Brambilla E, Le Teuff G, Marguet S, Lantuejoul S, Dunant A, Graziano S, Pirker R, Douillard JY, Le Chevalier T, Filipits M et al. Prognostic effect of tumor lymphocytic infiltration in Resectable Non-small-cell lung cancer. J Clin Oncol 2016; 34:1223-30; PMID:26834066; http://dx.doi.org/10.1200/JCO.2015.63.0970
4. Salgado R, Denkert C, Demaria S, Sirtaine N, Klauschen F, Pruneri G, Wienert S, Van den Eynden G, Baehner FL, Penault-Llorca F et al. The evaluation of tumor-infiltrating lymphocytes (TILs) in breast cancer: recommendations by an International TILs Working Group 2014. Ann Oncol 2015; 26:259-71; PMID:25214542; http://dx.doi.org/10.1093/annonc/mdu450
5. Savas P, Salgado R, Denkert C, Sotiriou C, Darcy PK, Smyth MJ, Loi S. Clinical relevance of host immunity in breast cancer: from TILs to the clinic. Nat Rev Clin Oncol 2016; 13:228-41; PMID:26667975; http://dx.doi.org/10.1038/nrclinonc.2015.215
6. Gu-Trantien C, Loi S, Garaud S, Equeter C, Libin M, de Wind A, Ravoet M, Le Buanec H, Sibille C, Manfouo-Foutsop G et al. CD4(+) follicular helper T cell infiltration predicts breast cancer survival. J Clin Invest 2013; 123:2873-92; PMID:23778140; http://dx.doi.org/10.1172/JCI67428
7. Palucka AK, Coussens LM. The basis of oncoimmunology. Cell 2016; 164:1233-47; PMID:26967289; http://dx.doi.org/10.1016/j.cell.2016.01.049
8. Ali HR, Provenzano E, Dawson SJ, Blows FM, Liu B, Shah M, Earl HM, Poole CJ, Hiller L, Dunn JA et al. Association between CD8+ T-cell infiltration and breast cancer survival in 12,439 patients. Ann Oncol 2014; 25:1536-43; PMID:24915873; http://dx.doi.org/10.1093/annonc/mdu191
9. Bates GJ, Fox SB, Han C, Leek RD, Garcia JF, Harris AL, Banham AH. Quantification of regulatory T cells enables the identification of high-risk breast cancer patients and those at risk of late relapse. J Clin Oncol 2006; 24:5373-80; PMID:17135638; http://dx.doi.org/10.1200/JCO.2006.05.9584
10. Lindau D, Gielen P, Kroesen M, Wesseling P, Adema GJ. The immunosuppressive tumour network: myeloid-derived suppressor cells, regulatory T cells and natural killer T cells. Immunology 2013; 138:105-15; PMID:23216602; http://dx.doi.org/10.1111/imm.12036
11. Dieu-Nosjean MC, Giraldo NA, Kaplon H, Germain C, Fridman WH, Sautes-Fridman C. Tertiary lymphoid structures, drivers of the anti-tumor responses in human cancers. Immunol Rev 2016; 271:260-75; PMID:27088920; http://dx.doi.org/10.1111/imr.12405
12. Jones GW, Jones SA. Ectopic lymphoid follicles: inducible centres for generating antigen-specific immune responses within tissues. Immunology 2016; 147:141-51; PMID:26551738; http://dx.doi.org/10.1111/imm.12554
13. Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pages C, Tosolini M, Camus M, Berger A, Wind P et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 2006; 313:1960-4; PMID:17008531; http://dx.doi.org/10.1126/science.1129139
14. Dieu-Nosjean MC, Antoine M, Danel C, Heudes D, Wislez M, Poulot V, Rabbe N, Laurans L, Tartour E, de Chaisemartin L et al. Long-term survival for patients with non-small-cell lung cancer with intratumoral lymphoid structures. J Clin Oncol 2008; 26:4410-7; PMID:18802153; http://dx.doi.org/10.1200/JCO.2007.15.0284
15. Ruffell B, Au A, Rugo HS, Esserman LJ, Hwang ES, Coussens LM. Leukocyte composition of human breast cancer. Proc Natl Acad Sci U S A 2012; 109:2796-801; PMID:21825174; http://dx.doi.org/10.1073/pnas.1104303108
16. Leong PP, Mohammad R, Ibrahim N, Ithnin H, Abdullah M, Davis WC, Seow HF. Phenotyping of lymphocytes expressing regulatory and effector markers in infiltrating ductal carcinoma of the breast. Immunol Letters 2006; 102:229-36; PMID:16246429; http://dx.doi.org/10.1016/j.imlet.2005.09.006
17. Pauken KE, Wherry EJ. SnapShot: T cell exhaustion. Cell 2015; 163:1038-e1; PMID:26544946; http://dx.doi.org/2246164110.1016/j.cell.2015.10.054
18. Taube JM, Anders RA, Young GD, Xu H, Sharma R, McMiller TL, Chen S, Klein AP, Pardoll DM, Topalian SL et al. Colocalization of inflammatory response with B7-h1 expression in human melanocytic lesions supports an adaptive resistance mechanism of immune escape. Sci Transl Med 2012; 4:127ra37; PMID:22461641; http://dx.doi.org/10.1126/scitranslmed.3003689
19. Teng MW, Ngiow SF, Ribas A, Smyth MJ. Classifying cancers based on T-cell infiltration and PD-L1. Cancer Res 2015; 75:2139-45; PMID:25977340; http://dx.doi.org/10.1158/0008-5472.CAN-15-0255
20. Sharma P, Allison JP. The future of immune checkpoint therapy. Science 2015; 348:56-61; PMID:25838373; http://dx.doi.org/10.1126/science.aaa8172
21. Motzer RJ, Escudier B, McDermott DF, George S, Hammers HJ, Srinivas S et al. Nivolumab versus Everolimus in advanced Renal-Cell Carcinoma. N Engl J Med 2015; 373:1803-13; PMID:26406148; http://dx.doi.org/10.1056/NEJMoa1510665
22. Nanda R, Chow LQ, Dees EC, Berger R, Gupta S, Geva R, Pusztai L, Pathiraja K, Aktan G, Cheng JD et al. Pembrolizumab in patients with advanced triple-negative breast cancer: Phase 1b KEYNOTE-012 study. J CLin Oncol 2016; 34(21):2460-7, PMID:27138582; http://dx.doi.org/10.1200/JCO.2015.64.8931
23. Tumeh PC, Harview CL, Yearley JH, Shintaku IP, Taylor EJ, Robert L, Chmielowski B, Spasic M, Henry G, Ciobanu V et al. PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature 2014; 515:568-71; PMID:25428505; http://dx.doi.org/10.1038/nature13954
24. Cimino-Mathews A, Thompson E, Taube JM, Ye X, Lu Y, Meeker A, Xu H, Sharma R, Lecksell K, Cornish TC et al. PD-L1 (B7-H1) expression and the immune tumor microenvironment in primary and metastatic breast carcinomas. Hum Pathol 2016; 47:52-63; PMID:26527522; http://dx.doi.org/10.1016/j.humpath.2015.09.003
25. Ali HR, Glont SE, Blows FM, Provenzano E, Dawson SJ, Liu B, Hiller L, Dunn J, Poole CJ, Bowden S et al. PD-L1 protein expression in breast cancer is rare, enriched in basal-like tumours and associated with infiltrating lymphocytes. Ann Oncol 2015; 26:1488-93; PMID:25897014; http://dx.doi.org/10.1093/annonc/mdv518.22
26. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, Powderly JD, Carvajal RD, Sosman JA, Atkins MB et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012; 366:2443-54; PMID:22658127; http://dx.doi.org/10.1056/NEJMoa1200690
27. Herbst RS, Soria JC, Kowanetz M, Fine GD, Hamid O, Gordon MS, Sosman JA, McDermott DF, Powderly JD, Gettinger SN et al. Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients. Nature 2014; 515:563-7; PMID:25428504; http://dx.doi.org/10.1038/nature14011
28. Bhatia S, Margolin K. Disparate clinical activity of PD-1 blockade in melanoma subtypes: Know thy enemy!. Cancer 2016; 122:3263-6; PMID:27533794; http://dx.doi.org/10.1002/cncr.30260
29. Algazi AP, Tsai KK, Shoushtari AN, Munhoz RR, Eroglu Z, Piulats JM, Ott PA, Johnson DB, Hwang J, Daud AI et al. Clinical outcomes in metastatic uveal melanoma treated with PD-1 and PD-L1 antibodies. Cancer 2016; 122:3344-53; PMID:27533448; http://dx.doi.org/10.1002/cncr.30258
30. Shoushtari AN, Munhoz RR, Kuk D, Ott PA, Johnson DB, Tsai KK, Rapisuwon S, Eroglu Z, Sullivan RJ, Luke JJ et al. The efficacy of anti-PD-1 agents in acral and mucosal melanoma. Cancer 2016; 122:3354-62; PMID:27533633; http://dx.doi.org/10.1002/cncr.30259
31. Cipponi A, Mercier M, Seremet T, Baurain JF, Theate I, van den Oord J, Stas M, Boon T, Coulie PG, van Baren N. Neogenesis of lymphoid structures and antibody responses occur in human melanoma metastases. Cancer Res 2012; 72:3997-4007; PMID:22850419; http://dx.doi.org/10.1158/0008-5472.CAN-12-1377
32. Denkert C, von Minckwitz G, Brase JC, Sinn BV, Gade S, Kronenwett R, Pfitzner BM, Salat C, Loi S, Schmitt WD et al. Tumor-infiltrating lymphocytes and response to neoadjuvant chemotherapy with or without carboplatin in human epidermal growth factor receptor 2-positive and triple-negative primary breast cancers. J Clin Oncol 2015; 33:983-91; PMID:25534375; http://dx.doi.org/10.1200/JCO.2014.58.1967
33. Loi S, Sirtaine N, Piette F, Salgado R, Viale G, Van Eenoo F, Rouas G, Francis P, Crown JP, Hitre E et al. Prognostic and predictive value of tumor-infiltrating lymphocytes in a phase III randomized adjuvant breast cancer trial in node-positive breast cancer comparing the addition of docetaxel to doxorubicin with doxorubicin-based chemotherapy: BIG 02-98. J Clin Oncol 2013; 31:860-7; PMID:23341518; http://dx.doi.org/10.1200/JCO.2011.41.0902
34. Adams S, Gray RJ, Demaria S, Goldstein L, Perez EA, Shulman LN, Martino S, Wang M, Jones VE, Saphner TJ 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(27):2959-66; PMID:25071121; http://dx.doi.org/2774839710.1200/JCO.2013.55.0491
35. Galluzzi L, Buque A, Kepp O, Zitvogel L, Kroemer G. Immunogenic cell death in cancer and infectious disease. Nat Rev Immunol 2016; PMID:27748397; http://dx.doi.org/10.1038/nri.2016.107
36. Denkert C, Loibl S, Noske A, Roller M, Muller BM, Komor M, Budczies J, Darb-Esfahani S, Kronenwett R, Hanusch C et al. Tumor-associated lymphocytes as an independent predictor of response to neoadjuvant chemotherapy in breast cancer. J Clin Oncol 2010; 28:105-13; PMID:19917869; http://dx.doi.org/10.1200/JCO.2009.23.7370
37. Ignatiadis M, Singhal SK, Desmedt C, Haibe-Kains B, Criscitiello C, Andre F, Loi S, Piccart M, Michiels S, Sotiriou C. Gene modules and response to neoadjuvant chemotherapy in breast cancer subtypes: a pooled analysis. J Clin Oncol 2012; 30:1996-2004; PMID:22508827; http://dx.doi.org/10.1200/JCO.2011.39.5624
38. Datta J, Fracol M, McMillan MT, Berk E, Xu S, Goodman N, Lewis DA, DeMichele A, Czerniecki BJ. Association of depressed Anti-HER2 T-Helper Type 1 response with recurrence in patients with completely treated her2-positive breast cancer: Role for immune monitoring. JAMA Oncol 2016; 2:242-6; PMID:26719971; http://dx.doi.org/10.1001/jamaoncol.2015.5482
39. 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; 189:832-44; PMID:24484236; http://dx.doi.org/10.1164/rccm.201309-1611OC
40. Liu S, Foulkes WD, Leung S, Gao D, Lau S, Kos Z, Nielsen TO. Prognostic significance of FOXP3+ 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; 16:432; PMID:25193543; http://dx.doi.org/10.1186/s13058-014-0432-8
41. Bodogai M, Lee Chang C, Wejksza K, Lai J, Merino M, Wersto RP, Gress RE, Chan AC, Hesdorffer C, Biragyn A. Anti-CD20 antibody promotes cancer escape via enrichment of tumor-evoked regulatory B cells expressing low levels of CD20 and CD137L. Cancer Res 2013; 73:2127-38; PMID:23365136; http://dx.doi.org/10.1158/0008-5472.CAN-12-4184
42. Schumacher TN, Schreiber RD. Neoantigens in cancer immunotherapy. Science 2015; 348:69-74; PMID:25838375; http://dx.doi.org/10.1126/science.aaa4971
43. Sautes-Fridman C, Lawand M, Giraldo NA, Kaplon H, Germain C, Fridman WH, Dieu-Nosjean MC. Tertiary lymphoid structures in cancers: Prognostic value, regulation, and manipulation for therapeutic intervention. Front Immunol 2016; 7:407; PMID:27752258; http://dx.doi.org/10.3389/fimmu.2016.00407
44. Joshi Nikhil S, Akama-Garren Elliot H, Lu Y, Lee DY, Chang Gregory P, 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; 43:579-90; PMID:26341400; http://dx.doi.org/10.1016/j.immuni.2015.08.006
45. Figenschau SL, Fismen S, Fenton KA, Fenton C, Mortensen ES. Tertiary lymphoid structures are associated with higher tumor grade in primary operable breast cancer patients. BMC Cancer 2015; 15:101; PMID:25884667; http://dx.doi.org/10.1186/s12885-015-1116-1
46. Lee HJ, Park IA, Song IH, Shin S-J, Kim JY, Yu JH, Gong G. Tertiary lymphoid structures: prognostic significance and relationship with tumour-infiltrating lymphocytes in triple-negative breast cancer. J Clin Pathol 2016; 69(5):422-30; PMID:26475777; http://dx.doi.org/10.1136/jclinpath-2015-203089
47. Lee HJ, Kim JY, Park IA, Song IH, Yu JH, Ahn J-H et al. Prognostic significance of tumor-infiltrating lymphocytes and the tertiary lymphoid structures in HER2-positive breast cancer treated with Adjuvant Trastuzumab. Am J Clin Pathol 2015; 144:278-88; PMID:26185313; http://dx.doi.org/10.1309/AJCPIXUYDVZ0RZ3G
48. Silina K, Rulle U, Kalnina Z, Line A. Manipulation of tumour-infiltrating B cells and tertiary lymphoid structures: a novel anti-cancer treatment avenue? Cancer Immunol Immunother 2014; 63:643-62; PMID:24695950; http://dx.doi.org/10.1007/s00262-014-1544-9
49. Smyth MJ, Ngiow SF, Ribas A, Teng MW. Combination cancer immunotherapies tailored to the tumour microenvironment. Nat Rev Clin Oncol 2016; 13:143-58; PMID:26598942; http://dx.doi.org/10.1038/nrclinonc.2015.209
50. Callahan MK, Postow MA, Wolchok JD. Targeting T cell co-receptors for cancer therapy. Immunity 2016; 44:1069-78; PMID:27192570; http://dx.doi.org/10.1016/j.immuni.2016.04.023
51. Muenst S, Schaerli AR, Gao F, Daster S, Trella E, Droeser RA, Muraro MG, Zajac P, Zanetti R, Gillanders WE et al. Expression of programmed death ligand 1 (PD-L1) is associated with poor prognosis in human breast cancer. Breast Cancer Res Treat 2014; 146:15-24; PMID:24842267; http://dx.doi.org/10.1007/s10549-014-2988-5
52. Baptista MZ, Sarian LO, Derchain SF, Pinto GA, Vassallo J. Prognostic significance of PD-L1 and PD-L2 in breast cancer. Hum Pathol 2016; 47:78-84; PMID:26541326; http://dx.doi.org/10.1016/j.humpath.2015.09.006
53. Wimberly H, Brown JR, Schalper K, Haack H, Silver MR, Nixon C, Bossuyt V, Pusztai L, Lannin DR, Rimm DL. PD-L1 expression correlates with Tumor-Infiltrating Lymphocytes and response to neoadjuvant chemotherapy in breast cancer. Cancer Immunol Res 2015; 3:326-32; PMID:25527356; http://dx.doi.org/10.1158/2326-6066.CIR-14-0133
54. Schalper KA, Velcheti V, Carvajal D, Wimberly H, Brown J, Pusztai L, Rimm DL. In situ tumor PD-L1 mRNA expression is associated with increased TILs and better outcome in breast carcinomas. Clin Cancer Res 2014; 20:2773-82; PMID:24647569; http://dx.doi.org/10.1158/1078-0432.CCR-13-2702
55. Webb JR, Milne K, Kroeger DR, Nelson BH. PD-L1 expression is associated with tumor-infiltrating T cells and favorable prognosis in high-grade serous ovarian cancer. Gynecol Oncol 2016; 141:293-302; PMID:26972336; http://dx.doi.org/10.1016/j.ygyno.2016.03.008
56. Zou W, Wolchok JD, Chen L. PD-L1 (B7-H1) and PD-1 pathway blockade for cancer therapy: Mechanisms, response biomarkers, and combinations. Sci Transl Med 2016; 8:328rv4; PMID:26936508; http://dx.doi.org/10.1126/scitranslmed.aad7118
57. Garaud S, Gu-Trantien C, Lodewyckx JN, Boisson A, De Silva P, Buisseret L, Migliori E, Libin M, Naveaux C, Duvillier H et al. A simple and rapid protocol to non-enzymatically dissociate fresh human tissues for the analysis of infiltrating lymphocytes. J Vis Exp 2014; PMID:25548995; http://dx.doi.org/10.3791/52392
58. Adams H, Liebisch P, Schmid P, Dirnhofer S, Tzankov A. Diagnostic utility of the B-cell lineage markers CD20, CD79a, PAX5, and CD19 in paraffin-embedded tissues from lymphoid neoplasms. Appl Immunohistochem Mol Morphol 2009; 17:96-101; PMID:18838917; http://dx.doi.org/10.1097/PAI.0b013e3181845ef4
59. Bigelow E, Bever KM, Xu H, Yager A, Wu A, Taube J, Chen L, Jaffee EM, Anders RA, Zheng L. Immunohistochemical staining of B7-H1 (PD-L1) on paraffin-embedded slides of pancreatic adenocarcinoma tissue. J Vis Exp 2013; PMID:23328703; http://dx.doi.org/10.3791/4059