Treatment regimen, surgical outcome, and t-cell differentiation influence prognostic benefit of tumor-infiltrating lymphocytes in high-grade serous ovarian cancer

Clinical Cancer Research

Volumn 22, Issue 3, 2016, Pages 714-724

  Wouters, Maartje C A ^a   Komdeur, Fenne L ^a   Workel, Hagma H ^a   Klip, Harry G ^a   Plat, Annechien ^a   Kooi, Neeltje M ^a   Wisman, G Bea A ^a   Mourits, Marian J E ^a   Arts, Henriette J G ^a   Oonk, Maaike H M ^a   Yigit, Refika ^a   De Jong, Steven ^a   Melief, Cornelis J M ^b,c   Hollema, Harry ^a   Duiker, Evelien W ^a   Daemen, Toos ^a   De Bruyn, Marco ^a   Nijman, Hans W ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c ISA Pharmaceuticals   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; BIOLOGICAL MARKER; LEUKOCYTE ANTIGEN;

ADULT; ADVANCED CANCER; ARTICLE; CANCER GRADING; CANCER PROGNOSIS; CANCER STAGING; CANCER SURVIVAL; CD8+ T LYMPHOCYTE; COHORT ANALYSIS; CONTROLLED STUDY; CYTOREDUCTIVE SURGERY; DISEASE FREE SURVIVAL; FEMALE; FLOW CYTOMETRY; FOLLOW UP; HUMAN; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; LYMPHOCYTE DIFFERENTIATION; MAJOR CLINICAL STUDY; MALE; OUTCOME ASSESSMENT; OVARY CANCER; PRIORITY JOURNAL; SURVIVAL TIME; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; TISSUE MICROARRAY; TUMOR ASSOCIATED LEUKOCYTE; AGED; CELL DIFFERENTIATION; CYSTADENOCARCINOMA, SEROUS; IMMUNOLOGY; IMMUNOPHENOTYPING; KAPLAN MEIER METHOD; METABOLISM; MIDDLE AGED; MORTALITY; MULTIMODALITY CANCER THERAPY; OVARIAN NEOPLASMS; PATHOLOGY; PHENOTYPE; PROGNOSIS; PROPORTIONAL HAZARDS MODEL; TREATMENT OUTCOME;

AGED; ANTIGENS, CD; BIOMARKERS; CELL DIFFERENTIATION; COMBINED MODALITY THERAPY; CYSTADENOCARCINOMA, SEROUS; FEMALE; HUMANS; IMMUNOPHENOTYPING; KAPLAN-MEIER ESTIMATE; LYMPHOCYTES, TUMOR-INFILTRATING; MIDDLE AGED; NEOPLASM GRADING; NEOPLASM STAGING; OVARIAN NEOPLASMS; PHENOTYPE; PROGNOSIS; PROPORTIONAL HAZARDS MODELS; T-LYMPHOCYTE SUBSETS; TREATMENT OUTCOME;

EID: 84959017008     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-15-1617     Document Type: Article

References (29)

1. Allemani C, Weir HK, Carreira H, Harewood R, Spika D, Wang X-S, et al. Global surveillance of cancer survival 1995-2009: analysis of individual data for 25 676 887 patients from 279 population-based registries in 67 countries (CONCORD-2). Lancet 2015;385:997-1010.
2. Vaughan S, Coward JI, Bast RC, Berchuck A, Berek JS, Brenton JD, et al. Rethinking ovarian cancer: recommendations for improving outcomes. Nat Rev Cancer 2011;11:719-25.
3. Winter WE, Maxwell GL, Tian C, Sundborg MJ, Rose GS, Rose PG, et al. Tumor residual after surgical cytoreduction in prediction of clinical outcome in stage IV epithelial ovarian cancer: a Gynecologic Oncology Group Study. J Clin Oncol 2008;26:83-9.
4. Bristow RE, Tomacruz RS, Armstrong DK, Trimble EL, Montz FJ. Survival effect of maximal cytoreductive surgery for advanced ovarian carcinoma during the platinum era: a meta-analysis. J Clin Oncol 2002;20:1248-59.
5. Vergote I, Trope CG, Amant F, Kristensen GB, Ehlen T, Johnson N, et al. Neoadjuvant chemotherapy or primary surgery in stage IIIC or IV ovarian cancer. N Engl J Med 2010;363:943-53.
6. 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.
7. Sato E, Olson SH, Ahn J, Bundy B, NishikawaH,Qian F, et al. 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 U S A 2005;102:18538-43.
8. Milne K,KobelM, Kalloger SE, Barnes RO, GaoD,Gilks CB, et al. Systematic analysis of immune infiltrates in high-grade serous ovarian cancer reveals CD20, FoxP3 and TIA-1 as positive prognostic factors. PLoS One 2009;4: e6412.
9. Leffers N, Gooden MJM, de Jong RA, Hoogeboom B-N, ten Hoor KA, Hollema H, et al. Prognostic significance of tumor-infiltrating T-lymphocytes in primary and metastatic lesions of advanced stage ovarian cancer. Cancer Immunol Immunother 2009;58:449-59.
10. Cui TX, Kryczek I, Zhao L, Zhao E, Kuick R, Roh MH, et al. Myeloid-derived suppressor cells enhance stemness of cancer cells by inducing micro-RNA101 and suppressing the corepressor CtBP2. Immunity 2013;39: 611-21.
11. Demaria S, Volm MD, Shapiro RL, Yee HT, Oratz R, Formenti SC, et al. Development of tumor-infiltrating lymphocytes in breast cancer after neoadjuvant paclitaxel chemotherapy. Clin Cancer Res 2001;7:3025-30.
12. Denkert C, Loibl S, Noske A, Roller M,Muller BM, Komor M, et al. Tumorassociated lymphocytes as an independent predictor of response to neoadjuvant chemotherapy in breast cancer. J Clin Oncol 2010;28:105-13.
13. Ono M, Tsuda H, Shimizu C, Yamamoto S, Shibata T, Yamamoto H, et al. Tumor-infiltrating lymphocytes are correlated with response to neoadjuvant chemotherapy in triple-negative breast cancer. Breast Cancer Res Treat 2012;132:793-805.
14. West NR, Milne K, Truong PT, Macpherson N, Nelson BH, Watson PH. Tumor-infiltrating lymphocytes predict response to anthracycline-based chemotherapy in estrogen receptor-negative breast cancer. Breast Cancer Res 2011;13:R126.
15. 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.
16. Besser MJ, Shapira-Frommer R, Treves AJ, Zippel D, Itzhaki O, Hershkovitz L, et al. Clinical responses in a phase II study using adoptive transfer of short-term cultured tumor infiltration lymphocytes in metastatic melanoma patients. Clin Cancer Res 2010;16:2646-55.
17. Gattinoni L, Klebanoff CA, Palmer DC, Wrzesinski C, Kerstann K, Yu Z, et al. Acquisition of full effector function in vitro paradoxically impairs the in vivo antitumor efficacy of adoptively transferred CD8+ T cells. J Clin Invest 2005;115:1616-26.
18. Diaz Y, Tundidor Y, Lopez A, Leon K. Concomitant combination of active immunotherapy and carboplatin-or paclitaxel-based chemotherapy improves anti-tumor response. Cancer Immunol Immunother 2013;62: 455-69.
19. Rosen B, Laframboise S, Ferguson S, Dodge J, BernardiniM, Murphy J, et al. The impacts of neoadjuvant chemotherapy and of debulking surgery on survival from advanced ovarian cancer. Gynecol Oncol 2014;134:462-7.
20. Riester M, Wei W, Waldron L, Culhane AC, Trippa L, Oliva E, et al. Risk prediction for late-stage ovarian cancer by meta-analysis of 1525 patient samples. J Natl Cancer Inst 2014;106:dju048.
21. Huang J, Khong HT, Dudley ME, El-Gamil M, Li YF, Rosenberg SA, et al. Survival, persistence, and progressive differentiation of adoptively transferred tumor-reactive T cells associated with tumor regression. J Immunother 2005;28:258-67.
22. Rosenberg SA, Yang JC, Sherry RM, Kammula US, Hughes MS, Phan GQ, et al. Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin Cancer Res 2011;17:4550-7.
23. Song D-G, Ye Q, Poussin M, Harms GM, Figini M, Powell DJ. CD27 costimulation augments the survival and antitumor activity of redirected human T cells in vivo. Blood 2012;119:696-706.
24. Ye Q, Song D-G, Poussin M, Yamamoto T, Best A, Li C, et al. CD137 accurately identifies and enriches for naturally occurring tumor-reactive T cells in tumor. Clin Cancer Res 2014;20:44-55.
25. Restifo NP, Gattinoni L. Lineage relationship of effector and memory T cells. Curr Opin Immunol 2013;25:556-63.
26. Vitale LA, He L-Z, Thomas LJ, Widger J, Weidlick J, Crocker A, et al. Development of a human monoclonal antibody for potential therapy of CD27-expressing lymphoma and leukemia. Clin Cancer Res 2012;18: 3812-21.
27. He L-Z, Prostak N, Thomas LJ, Vitale L, Weidlick J, Crocker A, et al. Agonist anti-human CD27 monoclonal antibody induces T cell activation and tumor immunity in human CD27-transgenic mice. J Immunol 2013;191: 4174-83.
28. Buchan SL, Manzo T, Flutter B, Rogel A, Edwards N, Zhang L, et al. OX40-and CD27-mediated costimulation synergizes with anti-PD-L1 blockade by forcing exhausted CD8+ T cells to exit quiescence. J Immunol 2015;194: 125-33.
29. Kandalaft LE, Powell DJ, Chiang CL, Tanyi J, Kim S, Bosch M, et al. Autologous lysate-pulsed dendritic cell vaccination followed by adoptive transfer of vaccine-primed ex vivo co-stimulated T cells in recurrent ovarian cancer. Oncoimmunology 2013;2:e22664.