Tumour-infiltrating CD8+ lymphocytes as an independent predictive factor for pathological complete response to primary systemic therapy in breast cancer

British Journal of Cancer

Volumn 109, Issue 10, 2013, Pages 2705-2713

  Seo, A N ^a,b   Lee, H J ^c   Kim, E J ^a   Kim, H J ^a   Jang, M H ^d   Lee, H E ^d   Kim, Y J ^a,d   Kim, J H ^a,d   Park, S Y ^a,d  

^a Seoul National University Bundang Hospital   (South Korea)

^b Kyungpook National University School of Medicine   (South Korea)

^c Asan Medical Center   (South Korea)

^d Seoul National University College of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE DEHYDROGENASE; ALDEHYDE DEHYDROGENASE ISOENZYME 1; CD24 ANTIGEN; CYCLOPHOSPHAMIDE; DOCETAXEL; DOXORUBICIN; HERMES ANTIGEN; NERVE CELL ADHESION MOLECULE; OSTEONECTIN; SMOOTH MUSCLE ACTIN; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG; UVOMORULIN; VIMENTIN;

ADULT; ARTICLE; BREAST CARCINOMA; CANCER COMBINATION CHEMOTHERAPY; CANCER STEM CELL; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CYTOTOXIC T LYMPHOCYTE; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; HUMAN; HUMAN TISSUE; LYMPHOCYTIC INFILTRATION; MAJOR CLINICAL STUDY; MULTIPLE CYCLE TREATMENT; OUTCOME ASSESSMENT; PHENOTYPE; PREDICTIVE VALUE; PRIORITY JOURNAL; SYSTEMIC THERAPY; T LYMPHOCYTE SUBPOPULATION; TREATMENT RESPONSE; TUMOR ASSOCIATED LEUKOCYTE;

ADULT; ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CD8-POSITIVE T-LYMPHOCYTES; COMBINED MODALITY THERAPY; FEMALE; HUMANS; LYMPHOCYTES, TUMOR-INFILTRATING; MIDDLE AGED; NEOADJUVANT THERAPY; PROGNOSIS; REMISSION INDUCTION; RETROSPECTIVE STUDIES; TREATMENT OUTCOME; TUMOR MARKERS, BIOLOGICAL;

EID: 84887851057     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2013.634     Document Type: Article

References (47)

1. Aaltomaa S, Lipponen P, Eskelinen M, Kosma VM, Marin S, Alhava E, Syrjanen K (1992) Lymphocyte infiltrates as a prognostic variable in female breast cancer. Eur J Cancer 28A: 859-864.
2. Bear HD, Anderson S, Brown A, Smith R, Mamounas EP, Fisher B, Margolese R, Theoret H, Soran A, Wickerham DL, Wolmark N (2003) The effect on tumor response of adding sequential preoperative docetaxel to preoperative doxorubicin and cyclophosphamide: preliminary results from National Surgical Adjuvant Breast and Bowel Project Protocol B-27. J Clin Oncol 21: 4165-4174.
3. Bhargava R, Beriwal S, Dabbs DJ, Ozbek U, Soran A, Johnson RR, Brufsky AM, Lembersky BC, Ahrendt GM (2010) Immunohistochemical surrogate markers of breast cancer molecular classes predicts response to neoadjuvant chemotherapy: a single institutional experience with 359 cases. Cancer 116: 1431-1439.
4. Buzdar AU, Ibrahim NK, Francis D, Booser DJ, Thomas ES, Theriault RL, Pusztai L, Green MC, Arun BK, Giordano SH, Cristofanilli M, Frye DK, Smith TL, Hunt KK, Singletary SE, Sahin AA, Ewer MS, Buchholz TA, Berry D, Hortobagyi GN (2005) Significantly higher pathologic complete remission rate after neoadjuvant therapy with trastuzumab, paclitaxel, and epirubicin chemotherapy: results of a randomized trial in human epidermal growth factor receptor 2-positive operable breast cancer. J Clin Oncol 23: 3676-3685.
5. Capietto AH, Martinet L, Fournie JJ (2011) Stimulated gammadelta T cells increase the in vivo efficacy of trastuzumab in HER-2+ breast cancer. J Immunol 187: 1031-1038.
6. Carey LA, Dees EC, Sawyer L, Gatti L, Moore DT, Collichio F, Ollila DW, Sartor CI, Graham ML, Perou CM (2007) The triple negative paradox: primary tumor chemosensitivity of breast cancer subtypes. Clin Cancer Res 13: 2329-2334.
7. Carson 3rd WE, Shapiro CL, Crespin TR, Thornton LM, Andersen BL (2004) Cellular immunity in breast cancer patients completing taxane treatment. Clin Cancer Res 10: 3401-3409.
8. Casares N, Pequignot MO, Tesniere A, Ghiringhelli F, Roux S, Chaput N, Schmitt E, Hamai A, Hervas-Stubbs S, Obeid M, Coutant F, Metivier D, Pichard E, Aucouturier P, Pierron G, Garrido C, Zitvogel L, Kroemer G (2005) Caspase-dependent immunogenicity of doxorubicin-induced tumor cell death. J Exp Med 202: 1691-1701.
9. Chollet P, Amat S, Cure H, de Latour M, Le Bouedec G, Mouret-Reynier MA, Ferriere JP, Achard JL, Dauplat J, Penault-Llorca F (2002) Prognostic significance of a complete pathological response after induction chemotherapy in operable breast cancer. Br J Cancer 86: 1041-1046.
10. Creighton CJ, Li X, Landis M, Dixon JM, Neumeister VM, Sjolund A, Rimm DL, Wong H, Rodriguez A, Herschkowitz JI, Fan C, Zhang X, He X, Pavlick A, Gutierrez MC, Renshaw L, Larionov AA, Faratian D, Hilsenbeck SG, Perou CM, Lewis MT, Rosen JM, Chang JC (2009) Residual breast cancers after conventional therapy display mesenchymal as well as tumor-initiating features. Proc Natl Acad Sci USA 106: 13820-13825.
11. DeNardo DG, Brennan DJ, Rexhepaj E, Ruffell B, Shiao SL, Madden SF, Gallagher WM, Wadhwani N, Keil SD, Junaid SA, Rugo HS, Hwang ES, Jirstrom K, West BL, Coussens LM (2011) Leukocyte complexity predicts breast cancer survival and functionally regulates response to chemotherapy. Cancer Discov 1: 54-67.
12. DeNardo DG, Coussens LM (2007) Inflammation and breast cancer. Balancing immune response: crosstalk between adaptive and innate immune cells during breast cancer progression. Breast Cancer Res 9: 212.
13. Denkert C, Loibl S, Noske A, Roller M, Muller BM, Komor M, Budczies J, Darb-Esfahani S, Kronenwett R, Hanusch C, von Torne C, Weichert W, Engels K, Solbach C, Schrader I, Dietel M, von Minckwitz G (2010) Tumor-associated lymphocytes as an independent predictor of response to neoadjuvant chemotherapy in breast cancer. J Clin Oncol 28: 105-113.
14. Ding ZC, Zhou G (2012) Cytotoxic chemotherapy and CD4+ effector T cells: an emerging alliance for durable antitumor effects. Clin Dev Immunol 2012: 890178.
15. Dunn GP, Bruce AT, Ikeda H, Old LJ, Schreiber RD (2002) Cancer immunoediting: from immunosurveillance to tumor escape. Nat Immunol 3: 991-998.
16. Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pages C, Tosolini M, Camus M, Berger A, Wind P, Zinzindohoue F, Bruneval P, Cugnenc PH, Trajanoski Z, Fridman WH, Pages F (2006) Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 313: 1960-1964.
17. Gianni L, Eiermann W, Semiglazov V, Manikhas A, Lluch A, Tjulandin S, Zambetti M, Vazquez F, Byakhow M, Lichinitser M, Climent MA, Ciruelos E, Ojeda B, Mansutti M, Bozhok A, Baronio R, Feyereislova A, Barton C, Valagussa P, Baselga J (2010) Neoadjuvant chemotherapy with trastuzumab followed by adjuvant trastuzumab versus neoadjuvant chemotherapy alone, in patients with HER2-positive locally advanced breast cancer (the NOAH trial): a randomised controlled superiority trial with a parallel HER2-negative cohort. Lancet 375: 377-384.
18. Goldhirsch A, Wood WC, Coates AS, Gelber RD, Thurlimann B, Senn HJ, Panel M (2011) Strategies for subtypes-dealing with the diversity of breast cancer: highlights of the St. Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer 2011. Ann Oncol 22: 1736-1747.
19. Hornychova H, Melichar B, Tomsova M, Mergancova J, Urminska H, Ryska A (2008) Tumor-infiltrating lymphocytes predict response to neoadjuvant chemotherapy in patients with breast carcinoma. Cancer Invest 26: 1024-1031.
20. Ismael G, Hegg R, Muehlbauer S, Heinzmann D, Lum B, Kim SB, Pienkowski T, Lichinitser M, Semiglazov V, Melichar B, Jackisch C (2012) Subcutaneous versus intravenous administration of (neo)adjuvant trastuzumab in patients with HER2-positive, clinical stage I-III breast cancer (HannaH study): a phase 3, open-label, multicentre, randomised trial. Lancet Oncol 13: 869-878.
21. Javeed A, Ashraf M, Riaz A, Ghafoor A, Afzal S, Mukhtar MM (2009) Paclitaxel and immune system. Eur J Pharm Sci 38: 283-290.
22. Knutson KL, Lu H, Stone B, Reiman JM, Behrens MD, Prosperi CM, Gad EA, Smorlesi A, Disis ML (2006) Immunoediting of cancers may lead to epithelial to mesenchymal transition. J Immunol 177: 1526-1533.
23. Ladoire S, Arnould L, Apetoh L, Coudert B, Martin F, Chauffert B, Fumoleau P, Ghiringhelli F (2008) Pathologic complete response to neoadjuvant chemotherapy of breast carcinoma is associated with the disappearance of tumor-infiltrating foxp3+ regulatory T cells. Clin Cancer Res 14: 2413-2420.
24. Lee HJ, Seo JY, Ahn JH, Ahn SH, Gong G (2013) Tumor-associated lymphocytes predict response to neoadjuvant chemotherapy in breast cancer patients. J Breast Cancer 16: 32-39.
25. Li X, Lewis MT, Huang J, Gutierrez C, Osborne CK, Wu MF, Hilsenbeck SG, Pavlick A, Zhang X, Chamness GC, Wong H, Rosen J, Chang JC (2008) Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. J Natl Cancer Inst 100: 672-679.
26. Liedtke C, Mazouni C, Hess KR, Andre F, Tordai A, Mejia JA, Symmans WF, Gonzalez-Angulo AM, Hennessy B, Green M, Cristofanilli M, Hortobagyi GN, Pusztai L (2008) Response to neoadjuvant therapy and long-term survival in patients with triple-negative breast cancer. J Clin Oncol 26: 1275-1281.
27. Liu S, Lachapelle J, Leung S, Gao D, Foulkes WD, Nielsen TO (2012) CD8+ lymphocyte infiltration is an independent favorable prognostic indicator in basal-like breast cancer. Breast Cancer Res 14: R48.
28. Mahmoud SM, Paish EC, Powe DG, Macmillan RD, Grainge MJ, Lee AH, Ellis IO, Green AR (2011) Tumor-infiltrating CD8+ lymphocytes predict clinical outcome in breast cancer. J Clin Oncol 29: 1949-1955.
29. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, Campbell LL, Polyak K, Brisken C, Yang J, Weinberg RA (2008) The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133: 704-715.
30. Mattarollo SR, Loi S, Duret H, Ma Y, Zitvogel L, Smyth MJ (2011) Pivotal role of innate and adaptive immunity in anthracycline chemotherapy of established tumors. Cancer Res 71: 4809-4820.
31. Melichar B, Hornychova H, Kalabova H, Basova H, Mergancova J, Urminska H, Jandik P, Cervinka V, Laco J, Ryska A (2012) Increased efficacy of a dose-dense regimen of neoadjuvant chemotherapy in breast carcinoma: a retrospective analysis. Med Oncol 29: 2577-2585.
32. Menard C, Martin F, Apetoh L, Bouyer F, Ghiringhelli F (2008) Cancer chemotherapy: not only a direct cytotoxic effect, but also an adjuvant for antitumor immunity. Cancer Immunol Immunother 57: 1579-1587.
33. Milani A, Sangiolo D, Montemurro F, Aglietta M, Valabrega G (2013) Active immunotherapy in HER2 overexpressing breast cancer: current status and future perspectives. Ann Oncol 24: 1740-1748.
34. Oda N, Shimazu K, Naoi Y, Morimoto K, Shimomura A, Shimoda M, Kagara N, Maruyama N, Kim SJ, Noguchi S (2012) Intratumoral regulatory T cells as an independent predictive factor for pathological complete response to neoadjuvant paclitaxel followed by 5-FU/epirubicin/cyclophosphamide in breast cancer patients. Breast Cancer Res Treat 136: 107-116.
35. Ono M, Tsuda H, Shimizu C, Yamamoto S, Shibata T, Yamamoto H, Hirata T, Yonemori K, Ando M, Tamura K, Katsumata N, Kinoshita T, Takiguchi Y, Tanzawa H, Fujiwara Y (2012) Tumor-infiltrating lymphocytes are correlated with response to neoadjuvant chemotherapy in triple-negative breast cancer. Breast Cancer Res Treat 132: 793-805.
36. Pages F, Kirilovsky A, Mlecnik B, Asslaber M, Tosolini M, Bindea G, Lagorce C, Wind P, Marliot F, Bruneval P, Zatloukal K, Trajanoski Z, Berger A, Fridman WH, Galon J (2009) In situ cytotoxic and memory T cells predict outcome in patients with early-stage colorectal cancer. J Clin Oncol 27: 5944-5951.
37. Park SY, Lee HE, Li H, Shipitsin M, Gelman R, Polyak K (2010) Heterogeneity for stem cell-related markers according to tumor subtype and histologic stage in breast cancer. Clin Cancer Res 16: 876-887.
38. Reiman JM, Knutson KL, Radisky DC (2010) Immune promotion of epithelial-mesenchymal transition and generation of breast cancer stem cells. Cancer Res 70: 3005-3008.
39. Reis-Filho JS, Tutt AN (2008) Triple negative tumours: a critical review. Histopathology 52: 108-118.
40. Santisteban M, Reiman JM, Asiedu MK, Behrens MD, Nassar A, Kalli KR, Haluska P, Ingle JN, Hartmann LC, Manjili MH, Radisky DC, Ferrone S, Knutson KL (2009) Immune-induced epithelial to mesenchymal transition in vivo generates breast cancer stem cells. Cancer Res 69: 2887-2895.
41. Sato E, Olson SH, Ahn J, Bundy B, Nishikawa H, Qian F, Jungbluth AA, Frosina D, Gnjatic S, Ambrosone C, Kepner J, Odunsi T, Ritter G, Lele S, Chen YT, Ohtani H, Old LJ, Odunsi K (2005) Intraepithelial CD8+ tumor-infiltrating lymphocytes and a high CD8+/regulatory T cell ratio are associated with favorable prognosis in ovarian cancer. Proc Natl Acad Sci USA 102: 18538-18543.
42. Schmidt M, Bohm D, von Torne C, Steiner E, Puhl A, Pilch H, Lehr HA, Hengstler JG, Kolbl H, Gehrmann M (2008) The humoral immune system has a key prognostic impact in node-negative breast cancer. Cancer Res 68: 5405-5413.
43. Singh A, Settleman J (2010) EMT, cancer stem cells and drug resistance: an emerging axis of evil in the war on cancer. Oncogene 29: 4741-4751.
44. Swann JB, Smyth MJ (2007) Immune surveillance of tumors. J Clin Invest 117: 1137-1146.
45. Tanei T, Morimoto K, Shimazu K, Kim SJ, Tanji Y, Taguchi T, Tamaki Y, Noguchi S (2009) Association of breast cancer stem cells identified by aldehyde dehydrogenase 1 expression with resistance to sequential Paclitaxel and epirubicin-based chemotherapy for breast cancers. Clin Cancer Res 15: 4234-4241.
46. West NR, Milne K, Truong PT, Macpherson N, Nelson BH, Watson PH (2011) Tumor-infiltrating lymphocytes predict response to anthracycline-based chemotherapy in estrogen receptor-negative breast cancer. Breast Cancer Res 13: R126.
47. Zitvogel L, Apetoh L, Ghiringhelli F, Andre F, Tesniere A, Kroemer G (2008) The anticancer immune response: indispensable for therapeutic success? J Clin Invest 118: 1991-2001.