Immunotherapy for breast cancer: What are we missing?

Clinical Cancer Research

Volumn 23, Issue 11, 2017, Pages 2640-2646

  Vonderheide, Robert H ^a   Domchek, Susan M ^a   Clark, Amy S ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATEZOLIZUMAB; AVELUMAB; CHIMERIC ANTIGEN RECEPTOR; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR VACCINE; PEMBROLIZUMAB; PROGRAMMED DEATH 1 LIGAND 1; PROGRAMMED DEATH 1 RECEPTOR; TICILIMUMAB; CD274 PROTEIN, HUMAN; EPITOPE;

ADOPTIVE TRANSFER; ADVANCED CANCER; ARTICLE; BREAST CANCER; CANCER IMMUNIZATION; CANCER IMMUNOTHERAPY; CANCER SURVIVAL; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL THERAPY; CELLULAR IMMUNITY; COMBINATION DRUG THERAPY; ESTROGEN RECEPTOR POSITIVE BREAST CANCER; HUMAN; IMMUNOBIOLOGY; METASTATIC BREAST CANCER; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROTEIN EXPRESSION; TREATMENT RESPONSE; TRIPLE NEGATIVE BREAST CANCER; TUMOR IMMUNOLOGY; TUMOR MICROENVIRONMENT; BREAST TUMOR; FEMALE; GENETICS; IMMUNOLOGY; IMMUNOTHERAPY; PATHOLOGY; TUMOR ASSOCIATED LEUKOCYTE;

B7-H1 ANTIGEN; BREAST NEOPLASMS; EPITOPES, T-LYMPHOCYTE; FEMALE; HUMANS; IMMUNOTHERAPY; LYMPHOCYTES, TUMOR-INFILTRATING; PROGRAMMED CELL DEATH 1 RECEPTOR; TUMOR MICROENVIRONMENT;

EID: 85020259344     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-16-2569     Document Type: Article

References (64)

1. Nanda R, Chow LQ, Dees EC, Berger R, Gupta S, Geva R, et al. Pembro-lizumab in patients with advanced triple-negative breast cancer: Phase Ib KEYNOTE-012 Study. J Clin Oncol 2016;34:2460-7.
2. Emens LA, Kok M, Ojalvo LS. Targeting the programmed cell death-1 pathway in breast and ovarian cancer. Curr Opin Obstet Gynecol 2016;28:142-7.
3. Rugo H, DeLord J-P, Im S-A, Ott PA, Piha-Paul SA, Bedard PL, et al. Preliminary efficacy and safety of pembrolizumab (MK-3475) in patients with PD-L1-positive, estrogen receptor (ER)-positive (ER+)/HER-2 negative breast cancer enrolled in KEYNOTE-028 [abstract]. In: Proceedings of the Thirty-Eighth Annual CTRC-AACR San Antonio Breast Cancer Symposium; 2015 Dec. 8-12; San Antonio, TX. Philadelphia (PA): AACR; Cancer Res 2016;76(4 Suppl):Abstract nr S5-07.
4. Vonderheide RH, LoRusso PM, Khalil M, Gartner EM, Khaira D Soulieres D, et al. Tremelimumab in combination with exemestane in patients with advanced breast cancer and treatment-associated modulation of inducible costimulator expression on patient T cells. Clin Cancer Res 2010;16:3485-94.
5. Mittendorf EA, Clifton GT, Holmes JP, Schneble E, van Echo D, Ponniah S, et al. Final report of the phase I/II clinical trial of the E75 (nelipepimut-S) vaccine with booster inoculations to prevent disease recurrence in high-risk breast cancer patients. Ann Oncol 2014;25:1735-42.
6. Miles D, Roche H, Martin M, Perren TJ, Cameron DA, Glaspy J, et al. Phase III multicenter clinical trial of the sialyl-TN (STn)-keyhole limpet hemo-cyanin (KLH) vaccine for metastatic breast cancer. Oncologist 2011;16:1092-100.
7. Yates LR, Desmedt C. Translational genomics: practical applications of the genomic revolution in breast cancer. Clin Cancer Res 2017;23:2630-9.
8. Freedman RA, Partridge AH. Emerging data and current challenges for young, old, obese, or male patients with breast cancer. Clin Cancer Res 2017;23:2647-54.
9. Nik-Zainal S, Morganella S. Mutational signatures in breast cancer: the problem at the DNA level. Clin Cancer Res 2017;23:2617-29.
10. Reeder-Hayes KE, Anderson BO. Breast cancer disparities at home and abroad: a review of the challenges and opportunities for system-level change. Clin Cancer Res 2017;23:2655-64.
11. 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.
12. Emens LA. Breast cancer immunobiology driving immunotherapy: vaccines and immune checkpoint blockade. Expert Rev Anticancer Ther 2012;12:1597-611.
13. Stanton SE, Adams S, Disis ML. Variation in the incidence and magnitude of tumor-infiltrating lymphocytes in breast cancer subtypes: a systematic review. JAMA Oncol 2016;2:1354-60.
14. Desmedt C, Haibe-Kains B, Wirapati P, Buyse M, Larsimont D, Bon-tempi G, et al. Biological processes associated with breast cancer clinical outcome depend on the molecular subtypes. Clin Cancer Res 2008;14:5158-65.
15. Loi S, Sirtaine N, Piette F, Salgado R, Viale G, Van Eenoo F, 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.
16. Liu S, Lachapelle J, Leung S, Gao D, Foulkes WD, Nielsen TO. CD8+ lymphocyte infiltration is an independent favorable prognostic indicator in basal-like breast cancer. Breast Cancer Res 2012;14:R48.
17. Adams S, Gray RJ, Demaria S, Goldstein L, Perez EA, Shulman LN, et al. Prognostic value of tumor-infiltrating lymphocytes intriple-negative breast cancers from two phase III randomized adjuvantbreast cancer trials: ECOG 2197 and ECOG 1199. J Clin Oncol 2014;32:2959-66.
18. Gu-Trantien C, Loi S, Garaud S, Equeter C, Libin M, de Wind A, et al. CD4 (+) follicular helper T cell infiltration predicts breast cancer survival. J Clin Invest 2013;123:2873-92.
19. Martinet L, Garrido I, Filleron T, Le Guellec S, Bellard E, Fournie JJ, et al. Human solid tumors contain high endothelial venules: association with T- and B-lymphocyte infiltration and favorable prognosis in breast cancer. Cancer Res 2011;71:5678-87.
20. Stanton SE, Disis ML. Clinical significance of tumor-infiltrating lymphocytes in breast cancer. J Immunother Cancer 2016;4:59.
21. Luen SJ, Salgado R, Fox S, Savas P, Eng-Wong J, Clark E, et al. Tumour-infiltrating lymphocytes in advanced HER2-positive breast cancer treated with pertuzumab or placebo in addition to trastuzumab and docetaxel: a retrospective analysis of the CLEOPATRA study. Lancet Oncol 2017;18:52-62.
22. Denkert C, Loibl S, Noske A, Roller M, Muller BM, Komor M, et al. Tumor-associated lymphocytes asan independent predictor of responseto neoad-juvant chemotherapy in breast cancer. J Clin Oncol 2010;28:105-13.
23. Ono M, Tsuda H, Shimizu C, Yamamoto S, Shibata T, Yamamoto H, et al. Tumor-infiltrating lymphocytes are correlated with response to neoadju-vant chemotherapy in triple-negative breast cancer. Breast Cancer Res Treat 2012;132:793-805.
24. Denkert C, von Minckwitz G, Brase JC, Sinn BV, Gade S, Kronenwett R, 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.
25. 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.
26. 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.
27. 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.
28. 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.
29. Rooney MS, Shukla SA, Wu CJ, Getz G, Hacohen N. Molecular and genetic properties of tumors associated with local immune cytolytic activity. Cell 2015;160:48-61.
30. Haricharan S, Bainbridge MN, Scheet P, Brown PH. Somatic mutation load of estrogen receptor-positive breast tumors predicts overall survival: an analysis of genome sequence data. Breast Cancer Res Treat 2014;146:211-20.
31. Snyder A, Makarov V, Merghoub T, Yuan J, Zaretsky JM, Desrichard A, et al. Genetic basis for clinical response to CTLA-4 blockade in melanoma. N Engl J Med 2014;371:2189-99.
32. Rizvi NA, Hellmann MD, Snyder A, Kvistborg P, Makarov V, Havel JJ, et al. Cancer immunology. Mutational landscape determines sensitivity toPD-1 blockade in non-small cell lung cancer. Science 2015;348:124-8.
33. Schumacher TN, Schreiber RD. Neoantigens in cancer immunotherapy. Science 2015;348:69-74.
34. Lawrence MS, Stojanov P, Polak P, Kryukov GV, Cibulskis K, Sivachenko A, et al. Mutational heterogeneity in cancer and the search for new cancer-associated genes. Nature 2013;499:214-8.
35. Segal NH, Parsons DW, Peggs KS, Velculescu V, Kinzler KW, Vogelstein B, et al. Epitope landscape in breast and colorectal cancer. Cancer Res 2008;68:889-92.
36. Tran E, Turcotte S, Gros A, Robbins PF, Lu YC, Dudley ME, et al. Cancer immunotherapy basedon mutation-specific CD4+ T cells ina patient with epithelial cancer. Science 2014;344:641-5.
37. Vonderheide RH, Nathanson KL. Immunotherapy at large: the road to personalized cancer vaccines. Nat Med 2013;19:1098-100.
38. Carreno BM, Magrini V, Becker-Hapak M, Kaabinejadian S, Hundal J, Petti AA, et al. Cancer immunotherapy. A dendritic cell vaccine increases the breadth and diversity of melanoma neoantigen-specific T cells. Science 2015;348:803-8.
39. Thompson E, Taube JM, Elwood H, Sharma R, Meeker A, Warzecha HN, et al. The immune microenvironment of breast ductal carcinoma in situ. Mod Pathol 2016;29:249-58.
40. Reck M, Rodriguez-Abreu D, Robinson AG, Hui R, Csoszi T, Fulop A, et al. Pembrolizumab versus chemotherapy for PD-L1-positive non-small-cell lung cancer. N Engl J Med 2016;375:1823-33.
41. Gangadhar TC, Vonderheide RH. Mitigating the toxic effects of anticancer immunotherapy. Nat Rev Clin Oncol 2014;11:91-9.
42. Dirix L, Takacs I, Nikolinskos P, Jerusalem G, Arkenau H-T, Hamilton EP, et al. Avelumab (MSB0010718C), an anti-PD-L1 antibody, in patients with locally advanced or metastatic breast cancer: a phase 1b JAVELIN solid tumor trial [abstract]. In: Proceedings of the Thirty-Eighth Annual CTRC-AACR San Antonio Breast Cancer Symposium; 2015 Dec. 8-12; San Antonio, TX. Philadelphia (PA): AACR; Cancer Res 2016;76(4 Suppl):Abstract nr S1-04.
43. McArthur HL, Diab A, Page DB, Yuan J, Solomon SB, Sacchini V, et al. A pilot study of preoperative single-dose ipilimumab and/or cryoablation in women with early-stage breast cancer with comprehensive immune profiling. Clin Cancer Res 2016;22:5729-37.
44. Coveler AL, Bates NE, Disis ML. Progress in the development of a therapeutic vaccine for breast cancer. Breast Cancer 2010;2:25-36.
45. Davis-Sproul JM, Harris MP, Davidson NE, Kobrin BJ, Jaffee EM, Emens LA. Cost-effective manufacture of an allogeneic GM-CSF-secreting breast tumor vaccine in an academic cGMP facility. Cytotherapy 2005;7:46-56.
46. Laheru D, Lutz E, Burke J, Biedrzycki B, Solt S, Onners B, et al. Allogeneic granulocyte macrophagecolony-stimulating factor-secreting tumor immu-notherapy alone or in sequence with cyclophosphamide for metastatic pancreatic cancer: a pilot study of safety, feasibility, and immune activation. Clin Cancer Res 2008;14:1455-63.
47. Domchek SM, Recio A, Mick R, Clark CE, Carpenter EL, Fox KR, et al. Telomerase-specific T-cell immunity in breast cancer: effect of vaccination on tumor immunosurveillance. Cancer Res 2007;67:10546-55.
48. Vonderheide RH, Hahn WC, Schultze JL, Nadler LM. The telomerase catalytic subunit isa widely expressed tumor-associated antigen recognized by cytotoxic T lymphocytes. Immunity 1999;10:673-9.
49. Emens LA, Asquith JM, Leatherman JM, Kobrin BJ, Petrik S, Laiko M, et al. Timed sequential treatment with cyclophosphamide, doxorubicin, and an allogeneic granulocyte-macrophage colony-stimulating factor-secreting breast tumor vaccine: a chemotherapy dose-ranging factorial study of safety and immune activation. J Clin Oncol 2009;27:5911-8.
50. Chen G, Gupta R, Petrik S, Laiko M, Leatherman JM, Asquith JM, et al. A feasibility study of cyclophosphamide, trastuzumab, and an allogeneic GM-CSF-secreting breast tumor vaccine for HER2+ metastatic breast cancer. Cancer Immunol Res 2014;2:949-61.
51. Rech AJ, Mick R, Martin S, Recio A, Aqui NA, Powell DJ Jr, et al. CD25 blockade depletes and selectively reprograms regulatory T cells in concert with immunotherapy in cancer patients. Sci Transl Med 2012;4:1324ra62.
52. DeNardo DG, Brennan DJ, Rexhepaj E, Ruffell B, Shiao SL, Madden SF, et al. Leukocyte complexity predicts breast cancer survival and functionally regulates response to chemotherapy. Cancer Discov 2011;1:54-67.
53. De Henau O, Rausch M, Winkler D, Campesato LF, Liu C, Cymerman DH, et al. Overcoming resistance to checkpoint blockade therapy by targeting PI3Kgamma in myeloid cells. Nature 2016;539:443-7.
54. Gill S, June CH. Going viral: chimeric antigen receptor T-cell therapy for hematological malignancies. Immunol Rev 2015;263:68-89.
55. Disis ML, Salazar LG, Coveler A, Waisman J, Higgins D, Childs J, et al. Phase I study of infusion of HER2/neu (HER2) specific T cells in patients with advanced-stage HER2 overexpressing cancers who have received a HER2 vaccine. J Clin Oncol 27:15s, 2009 (suppl; abstr 3000).
56. Morgan RA, Yang JC, Kitano M, Dudley ME, Laurencot CM, Rosenberg SA. Case report of a serious adverse event following the administration of T cells transduced with a chimeric antigen receptor recognizing ERBB2. Mol Ther 2010;18:843-51.
57. Sharma P, Allison JP. The future of immune checkpoint therapy. Science 2015;348:56-61.
58. Spranger S, Luke JJ, Bao R, Zha Y, Hernandez KM, Li Y, et al. Density of immunogenic antigens does not explain the presence or absence of the T-cell-inflamed tumor microenvironment in melanoma. Proc Natl Acad Sci U S A 2016;113:E7759-E68.
59. Balli D, Rech AJ, Stanger BZ, Vonderheide RH. Immune cytolytic activity stratifies molecular subsets of human pancreatic cancer. Clin Cancer Res 2016 Dec. 22. [Epub ahead of print].
60. Pylayeva-Gupta Y, Lee KE, Hajdu CH, Miller G, Bar-Sagi D. Oncogenic Kras-induced GM-CSF production promotes the development of pancreatic neoplasia. Cancer Cell 2012;21:836-47.
61. Bayne LJ, Beatty GL, Jhala N, Clark CE, Rhim AD, Stanger BZ, et al. Tumor-derived granulocyte-macrophage colony-stimulating factor regulates mye-loid inflammation and T cell immunity in pancreatic cancer. Cancer Cell 2012;21:822-35.
62. Akbay EA, Koyama S, Carretero J, Altabef A, Tchaicha JH, Christensen CL, et al. Activation of the PD-1 pathway contributes to immune escape in EGFR-driven lung tumors. Cancer Discov 2013;3:1355-63.
63. Blue Ribbon Panel for the National Cancer Moonshot Initiative. Cancer Moonshot Blue Ribbon Panel Report [PDF on the Internet]. Bethesda (MD): National Cancer Institute; 2016 [cited 2017 May 15]. Available from: https://www.cancer.gov/research/key-initiatives/moonshot-cancer-initiative/blue-ribbon-panel/blue-ribbon-panel-report-2016.pdf.
64. Yan J, Pankhong P, Shin TH, Obeng-Adjei N, Morrow MP, Walters JN, et al. Highly optimized DNA vaccine targeting human telomerase reverse tran-scriptase stimulates potent antitumor immunity. Cancer Immunol Res 2013;1:179-89.