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Tumor infiltrating lymphocytes and PD-L1 expression in pre- and post-treatment
breast cancers in the SWOG S0800 Phase II neoadjuvant chemotherapy trial
Vasiliki Pelekanou1; William E. Barlow2; Zeina A. Nahleh3§; Brad Wasserman1; Ying-
Chun Lo1; Marie-Kristin von Wahlde4¶; Daniel Hayes5; Gabriel N. Hortobagyi6; Julie
Gralow7; Debu Tripathy6; Peggy Porter7; Borbala Szekely4; Christos Hatzis4; David L.
Rimm1 and Lajos Pusztai4*.
1Yale School of Medicine, Pathology, New Haven, CT
2SWOG Statistical Center, Seattle, WA
3Texas Tech University Health Sciences Center, Paul L. Foster School of Medicine, El
Paso, TX
4 Yale School of Medicine, Medical Oncology, New Haven, CT
5 University of Michigan, School of Medicine, Medical Oncology, Ann Arbor, MI
6University of Texas MD Anderson Cancer Center, Houston TX
7Fred Hutchinson Cancer Center Seattle, WA
* Corresponding author
§ Current affiliation: Maroone Cancer Center, Cleveland Clinic Florida
¶ Current affiliation: University Hospital Muenster, Department of Obstetrics and
Gynecology
Running Title: TILs and PD-L1 in neoadjuvant treated breast cancer
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on March 27, 2018; DOI: 10.1158/1535-7163.MCT-17-1005
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on March 27, 2018; DOI: 10.1158/1535-7163.MCT-17-1005
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on March 27, 2018; DOI: 10.1158/1535-7163.MCT-17-1005
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on March 27, 2018; DOI: 10.1158/1535-7163.MCT-17-1005
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on March 27, 2018; DOI: 10.1158/1535-7163.MCT-17-1005
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on March 27, 2018; DOI: 10.1158/1535-7163.MCT-17-1005
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on March 27, 2018; DOI: 10.1158/1535-7163.MCT-17-1005
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on March 27, 2018; DOI: 10.1158/1535-7163.MCT-17-1005
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on March 27, 2018; DOI: 10.1158/1535-7163.MCT-17-1005
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on March 27, 2018; DOI: 10.1158/1535-7163.MCT-17-1005
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on March 27, 2018; DOI: 10.1158/1535-7163.MCT-17-1005
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on March 27, 2018; DOI: 10.1158/1535-7163.MCT-17-1005
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on March 27, 2018; DOI: 10.1158/1535-7163.MCT-17-1005
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on March 27, 2018; DOI: 10.1158/1535-7163.MCT-17-1005
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on March 27, 2018; DOI: 10.1158/1535-7163.MCT-17-1005
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on March 27, 2018; DOI: 10.1158/1535-7163.MCT-17-1005
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on March 27, 2018; DOI: 10.1158/1535-7163.MCT-17-1005
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on March 27, 2018; DOI: 10.1158/1535-7163.MCT-17-1005
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13. Bottai G, Raschioni C, Losurdo A, Di Tommaso L, Tinterri C, Torrisi R, et al. An immune stratification reveals a subset of PD-1/LAG-3 double-positive triple-negative breast cancers. Breast Cancer Res. 2016;18:121. 14. Wimberly H, Brown JR, Schalper K, Haack H, Silver MR, Nixon C, et al. PD-L1 Expression Correlates with Tumor-Infiltrating Lymphocytes and Response to Neoadjuvant Chemotherapy in Breast Cancer. Cancer Immunol Res. 2015;3:326-32. 15. Schalper KA, Velcheti V, Carvajal D, Wimberly H, Brown J, Pusztai L, et al. 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. 16. Liu B, Cui J, Sun J, Li J, Han X, Guo J, et al. Immunolocalization of MMP9 and MMP2 in osteolytic metastasis originating from MDA-MB-231 human breast cancer cells. Mol Med Rep. 2016;14:1099-106. 17. Pusztai L, Karn T, Safonov A, Abu-Khalaf MM, Bianchini G. New Strategies in Breast Cancer: Immunotherapy. Clinical cancer research : an official journal of the American Association for Cancer Research. 2016;22:2105-10. 18. Sistigu A, Yamazaki T, Vacchelli E, Chaba K, Enot DP, Adam J, et al. Cancer cell-autonomous contribution of type I interferon signaling to the efficacy of chemotherapy. Nat Med. 2014;20:1301-9. 19. Vincent J, Mignot G, Chalmin F, Ladoire S, Bruchard M, Chevriaux A, et al. 5-Fluorouracil selectively kills tumor-associated myeloid-derived suppressor cells resulting in enhanced T cell-dependent antitumor immunity. Cancer Res. 2010;70:3052-61. 20. Roselli M, Cereda V, di Bari MG, Formica V, Spila A, Jochems C, et al. Effects of conventional therapeutic interventions on the number and function of regulatory T cells. Oncoimmunology. 2013;2:e27025. 21. Voron T, Colussi O, Marcheteau E, Pernot S, Nizard M, Pointet AL, et al. VEGF-A modulates expression of inhibitory checkpoints on CD8+ T cells in tumors. J Exp Med. 2015;212:139-48. 22. Nahleh ZA, Barlow WE, Hayes DF, Schott AF, Gralow JR, Sikov WM, et al. SWOG S0800 (NCI CDR0000636131): addition of bevacizumab to neoadjuvant nab-paclitaxel with dose-dense doxorubicin and cyclophosphamide improves pathologic complete response (pCR) rates in inflammatory or locally advanced breast cancer. Breast Cancer Res Treat. 2016;158:485-95. 23. Salgado R, Denkert C, Demaria S, Sirtaine N, Klauschen F, Pruneri G, 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. 24. Rimm DL, Han G, Taube JM, Yi ES, Bridge JA, Flieder DB, et al. A Prospective, Multi-institutional, Pathologist-Based Assessment of 4 Immunohistochemistry Assays for PD-L1 Expression in Non-Small Cell Lung Cancer. JAMA Oncol. 2017. 25. Nanda R, Chow LQ, Dees EC, Berger R, Gupta S, Geva R, et al. Pembrolizumab in Patients With Advanced Triple-Negative Breast Cancer: Phase Ib KEYNOTE-012 Study. Journal of clinical oncology : official journal of the American Society of Clinical Oncology. 2016;34:2460-7. 26. McLaughlin J, Han G, Schalper KA, Carvajal-Hausdorf D, Pelekanou V, Rehman J, et al. Quantitative Assessment of the Heterogeneity of PD-L1 Expression in Non-Small-Cell Lung Cancer. JAMA Oncol. 2016;2:46-54. 27. Kluger HM, Zito CR, Barr ML, Baine MK, Chiang VL, Sznol M, et al. Characterization of PD-L1 Expression and Associated T-cell Infiltrates in Metastatic Melanoma Samples from Variable Anatomic Sites. Clinical cancer research : an official journal of the American Association for Cancer Research. 2015;21:3052-60. 28. Cimino-Mathews A, Thompson E, Taube JM, Ye X, Lu Y, Meeker A, et al. PD-L1 (B7-H1) expression and the immune tumor microenvironment in primary and metastatic breast carcinomas. Hum Pathol. 2016;47:52-63.
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29. Nanda R, Liu MC, Yau C, Asare S, Hylton N, Van't Veer L, et al. Pembrolizumab plus standard neoadjuvant therapy for high-risk breast cancer (BC): Results from I-SPY 2. Journal of clinical oncology : official journal of the American Society of Clinical Oncology. 2017;35 30. Pusztai L, Silber A, Wysong Hofstatter E, Chung GG, Horowitz NR, Lannin DR, et al. Safety of MEDI4736 (anti-PD-L1 antibody) administered concomitant with weekly nab-paclitaxel and dose dense doxorubicin/cyclophosphamide (ddAC) as neoadjuvant chemotherapy for stage I-III triple negative breast cancer (TNBC): A Phase I/II trial. Journal of clinical oncology : official journal of the American Society of Clinical Oncology. 2017;35. 31. Schmid P, Park YH, Muñoz-Couselo E, Kim S-B, Sohn J, Im S-A, et al. Pembrolizumab (pembro) + chemotherapy (chemo) as neoadjuvant treatment for triple negative breast cancer (TNBC): Preliminary results from KEYNOTE-173. Journal of clinical oncology : official journal of the American Society of Clinical Oncology. 2017;35. 32. 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. Clinical cancer research : an official journal of the American Association for Cancer Research. 2001;7:3025-30. 33. Zhang P, Su DM, Liang M, Fu J. Chemopreventive agents induce programmed death-1-ligand 1 (PD-L1) surface expression in breast cancer cells and promote PD-L1-mediated T cell apoptosis. Mol Immunol. 2008;45:1470-6. 34. Garcia-Martinez E, Gil GL, Benito AC, Gonzalez-Billalabeitia E, Conesa MA, Garcia Garcia T, et al. Tumor-infiltrating immune cell profiles and their change after neoadjuvant chemotherapy predict response and prognosis of breast cancer. Breast Cancer Res. 2014;16:488. 35. Gonzalez-Angulo AM, Iwamoto T, Liu S, Chen H, Do KA, Hortobagyi GN, et al. Gene expression, molecular class changes, and pathway analysis after neoadjuvant systemic therapy for breast cancer. Clin Cancer Res. 2012;18:1109-19. 36. Dieci MV, Criscitiello C, Goubar A, Viale G, Conte P, Guarneri V, et al. Prognostic value of tumor-infiltrating lymphocytes on residual disease after primary chemotherapy for triple-negative breast cancer: a retrospective multicenter study. Ann Oncol. 2014;25:611-8. 37. Ladoire S, Arnould L, Apetoh L, Coudert B, Martin F, Chauffert B, et al. Pathologic complete response to neoadjuvant chemotherapy of breast carcinoma is associated with the disappearance of tumor-infiltrating foxp3+ regulatory T cells. Clinical cancer research : an official journal of the American Association for Cancer Research. 2008;14:2413-20. 38. Mani NL, Schalper KA, Hatzis C, Saglam O, Tavassoli F, Butler M, et al. Quantitative assessment of the spatial heterogeneity of tumor-infiltrating lymphocytes in breast cancer. Breast Cancer Res. 2016;18:78.
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on March 27, 2018; DOI: 10.1158/1535-7163.MCT-17-1005
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on March 27, 2018; DOI: 10.1158/1535-7163.MCT-17-1005
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on March 27, 2018; DOI: 10.1158/1535-7163.MCT-17-1005
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on March 27, 2018; DOI: 10.1158/1535-7163.MCT-17-1005
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on March 27, 2018; DOI: 10.1158/1535-7163.MCT-17-1005
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on March 27, 2018; DOI: 10.1158/1535-7163.MCT-17-1005
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on March 27, 2018; DOI: 10.1158/1535-7163.MCT-17-1005
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on March 27, 2018; DOI: 10.1158/1535-7163.MCT-17-1005
Published OnlineFirst March 27, 2018.Mol Cancer Ther Vasiliki Pelekanou, William E. Barlow, Zeina Nahleh, et al. neoadjuvant chemotherapy trialand post-treatment breast cancers in the SWOG S0800 Phase II Tumor infiltrating lymphocytes and PD-L1 expression in pre-
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Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on March 27, 2018; DOI: 10.1158/1535-7163.MCT-17-1005