Doxorubicin eliminates myeloid-derived suppressor cells and enhances the efficacy of adoptive T-cell transfer in breast cancer

Cancer Research

Volumn 74, Issue 1, 2014, Pages 104-118

  Alizadeh, Darya ^a,c   Trad, Malika ^e   Hanke, Neale T ^b   Larmonier, Claire B ^c   Janikashvili, Nona ^e   Bonnotte, Bernard ^e,f   Katsanis, Emmanuel ^a,b,c,d   Larmonier, Nicolas ^a,b,c,d  

^a Cancer Biology Graduate Program   (United Kingdom)

^b UNIVERSITY OF ARIZONA   (United States)

^c Veterinary and Life Sciences   (United Kingdom)

^d UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^e France   (France)

^f HÔPITAL DU BOCAGE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOPHOSPHAMIDE; DOXORUBICIN; ETOPOSIDE; FLUDARABINE; GAMMA INTERFERON; GRANZYME B; MELPHALAN; PERFORIN; VINCRISTINE;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD; BONE MARROW CELL; BREAST CANCER; CANCER CLASSIFICATION; CANCER COMBINATION CHEMOTHERAPY; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ISOLATION; CLINICAL ARTICLE; COLON CANCER; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DRUG CYTOTOXICITY; DRUG EFFICACY; DRUG POTENCY; DRUG SENSITIVITY; EFFECTOR CELL; HUMAN; IMMUNOSUPPRESSIVE TREATMENT; IN VITRO STUDY; IN VIVO STUDY; KIDNEY CANCER; LUNG CANCER; LYMPHOCYTE; METASTASIS INHIBITION; MONOTHERAPY; MOUSE; MYELOID DERIVED SUPPRESSOR CELL; NATURAL KILLER CELL; NEOPLASM; NONHUMAN; OUTCOME ASSESSMENT; OVARY CANCER; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPLEEN; STOMACH CANCER; SUPPRESSOR CELL; T LYMPHOCYTE; TH1 CELL; TH2 CELL;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; BREAST NEOPLASMS; CELL LINE, TUMOR; DOXORUBICIN; FEMALE; HUMANS; IMMUNOTHERAPY, ADOPTIVE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MYELOID CELLS; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84892686102     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-13-1545     Document Type: Article

References (49)

1. Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 2009;9:162-74.
2. Ostrand-Rosenberg S, Sinha P. Myeloid-derived suppressor cells: linking inflammation and cancer. J Immunol 2009;182:4499-506.
3. Serafini P, De Santo C, Marigo I, Cingarlini S, Dolcetti L, Gallina G, et al. Derangement of immune responses by myeloid suppressor cells. Cancer Immunol Immunother 2004;53:64-72.
4. Bunt SK, Sinha P, Clements VK, Leips J, Ostrand-Rosenberg S. Inflammation induces myeloid-derived suppressor cells that facilitate tumor progression. J Immunol 2006;176:284-90.
5. Youn JI, Nagaraj S, Collazo M, Gabrilovich DI. Subsets of myeloidderived suppressor cells in tumor-bearing mice. J Immunol 2008;181: 5791-802.
6. Peranzoni E, Zilio S, Marigo I, Dolcetti L, Zanovello P, Mandruzzato S, et al. Myeloid-derived suppressor cell heterogeneity and subset definition. Curr Opin Immunol 2010;22: 238-44.
7. Ochoa AC, Zea AH, Hernandez C, Rodriguez PC. Arginase, prostaglandins, and myeloid-derived suppressor cells in renal cell carcinoma. Clin Cancer Res 2007;13:721s-6s.
8. Beck BH, Kim HG, Kim H, Samuel S, Liu Z, Shrestha R, et al. Adoptively transferred ex vivo expanded gammadelta-T cells mediate in vivo antitumor activity in preclinical mouse models of breast cancer. Breast Cancer Res Treat 2010;122:135-44.
9. Younos I, Donkor M, Hoke T, Dafferner A, Samson H, Westphal S, et al. Tumor- and organ-dependent infiltration bymyeloid-derived suppressor cells. Int Immunopharmacol 2011;11:816-26.
10. Almand B, Clark JI, Nikitina E, van Beynen J, English NR, Knight SC, et al. Increased production of immature myeloid cells in cancer patients: a mechanism of immunosuppression in cancer. J Immunol 2001;166:678-89.
11. Ostrand-Rosenberg S. Myeloid-derived suppressor cells: more mechanisms for inhibiting antitumor immunity. Cancer Immunol Immunother 2010;59:1593-600.
12. Gabrilovich DI, Ostrand-Rosenberg S, Bronte V. Coordinated regulation of myeloid cells by tumours. Nat Rev Immunol 2012;12:253-68.
13. Bronte V, Serafini P, Apolloni E, Zanovello P. Tumor-induced immune dysfunctions caused by myeloid suppressor cells. J Immunother 2001;24:431-46.
14. Kusmartsev S, Cheng F, Yu B, Nefedova Y, Sotomayor E, Lush R, et al. All-trans-retinoic acid eliminates immature myeloid cells from tumorbearing mice and improves the effect of vaccination. Cancer Res 2003; 63:4441-9.
15. Nefedova Y, Fishman M, Sherman S, Wang X, Beg AA, Gabrilovich DI. Mechanism of all-trans retinoic acid effect on tumor-associated myeloid-derived suppressor cells. Cancer Res 2007;67: 11021-8.
16. Mirza N, Fishman M, Fricke I, Dunn M, Neuger AM, Frost TJ, et al. All-trans-retinoic acid improves differentiation of myeloid cells and immune response in cancer patients. Cancer Res 2006;66: 9299-307.
17. Suzuki E, Kapoor V, Jassar AS, Kaiser LR, Albelda SM. Gemcitabine selectively eliminates splenic Gr-1+/CD11b+ myeloid suppressor cells in tumor-bearing animals and enhances antitumor immune activity. Clin Cancer Res 2005;11:6713-21.
18. Bunt SK, Mohr AM, Bailey JM, Grandgenett PM, Hollingsworth MA. Rosiglitazone and Gemcitabine in combination reduces immune suppression and modulates T cell populations in pancreatic cancer. Cancer Immunol Immunother 2013;62:225-36.
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. Kodumudi KN, Woan K, Gilvary DL, Sahakian E, Wei S, Djeu JY. Anovel chemoimmunomodulating property of docetaxel: suppression of myeloid-derived suppressor cells in tumor bearers. Clin Cancer Res 2010; 16:4583-94.
21. Tacar O, Sriamornsak P, Dass CR. Doxorubicin: an update on anticancer molecular action, toxicity and novel drug delivery systems. J Pharm Pharmacol 2013;65:157-70.
22. Bandyopadhyay A, Wang L, Agyin J, Tang Y, Lin S, Yeh IT, et al. Doxorubicin in combination with a small TGF-β inhibitor: a potential novel therapy for metastatic breast cancer in mouse models. PLoS One 2010;5:e10365.
23. Casares N, Pequignot MO, Tesniere A, Ghiringhelli F, Roux S, Chaput N, et al. Caspase-dependent immunogenicity of doxorubicin-induced tumor cell death. J Exp Med 2005;202:1691-701.
24. Eralp Y, Wang X, Wang JP, Maughan MF, Polo JM, Lachman LB. Doxorubicin and paclitaxel enhance the antitumor efficacy of vaccines directed against HER 2/neu in a murine mammary carcinoma model. Breast Cancer Res 2004;6:R275-83.
25. Panis C, Lemos LG, Victorino VJ, Herrera AC, Campos FC, Colado Simao AN, et al. Immunological effects of taxol and adryamicin in breast cancer patients. Cancer Immunol Immunother 2012;61:481-8.
26. Mattarollo SR, Loi S, Duret H, Ma Y, Zitvogel L, Smyth MJ. Pivotal role of innate and adaptive immunity in anthracycline chemotherapy of established tumors. Cancer Res 2011;71:4809-20.
27. Obeid M, Tesniere A, Ghiringhelli F, Fimia GM, Apetoh L, Perfettini JL, et al. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat Med 2007;13:54-61.
28. Ramakrishnan R, Assudani D, Nagaraj S, Hunter T, Cho HI, Antonia S, et al. Chemotherapy enhances tumor cell susceptibility to CTL-mediated killing during cancer immunotherapy in mice. J Clin Invest 2010; 120:1111-24.
29. Eruslanov E, Kusmartsev S. Identification of ROS using oxidized DCFDA and flow-cytometry. Methods Mol Biol 2010;594:57-72.
30. DuPre SA, Redelman D, Hunter KW Jr. The mouse mammary carcinoma 4T1: characterization of the cellular landscape of primary tumours and metastatic tumour foci. Int J Exp Pathol 2007;88:351-60.
31. Tao K, Fang M, Alroy J, Sahagian GG. Imagable 4T1 model for the study of late stage breast cancer. BMC Cancer 2008;8:228.
32. Centuori SM, Trad M, LaCasse CJ, Alizadeh D, Larmonier CB, Hanke NT, et al. Myeloid-derived suppressor cells from tumor-bearing mice impair TGF-β-induced differentiation of CD4+CD25+FoxP3+ Tregs from CD4+CD25-FoxP3-T cells. J Leukoc Biol 2012;92: 987-97.
33. Corzo CA, Cotter MJ, Cheng P, Cheng F, Kusmartsev S, Sotomayor E, et al. Mechanism regulating reactive oxygen species in tumorinduced myeloid-derived suppressor cells. J Immunol 2009;182: 5693-701.
34. Martin-Orozco N, Muranski P, Chung Y, Yang XO, Yamazaki T, Lu S, et al. T helper 17 cells promote cytotoxic T cell activation in tumor immunity. Immunity 2009;31:787-98.
35. Janikashvili N, LaCasse CJ, Larmonier C, Trad M, Herrell A, Bustamante S, et al. Allogeneic effector/memory Th-1 cells impair FoxP3+ regulatory T lymphocytes and synergize with chaperone-rich cell lysate vaccine to treat leukemia. Blood 2011;117:1555-64.
36. Filipazzi P, Huber V, Rivoltini L. Phenotype, function and clinical implications of myeloid-derived suppressor cells in cancer patients. Cancer Immunol Immunother 2012;61:255-63.
37. Galluzzi L, Senovilla L, Zitvogel L, Kroemer G. The secret ally: immunostimulation by anticancer drugs. Nat Rev Drug Discov 2012;11: 215-33.
38. Ghiringhelli F, Larmonier N, Schmitt E, Parcellier A, Cathelin D, Garrido C, et al. CD4+CD25+ regulatory T cells suppress tumor immunity but are sensitive to cyclophosphamide which allows immunotherapy of established tumors to be curative. Eur J Immunol 2004;34:336-44.
39. Ghiringhelli F, Menard C, Puig PE, Ladoire S, Roux S, Martin F, et al. Metronomic cyclophosphamide regimen selectively depletes CD4+CD25+ regulatory T cells and restores T and NK effector functions in end stage cancer patients. Cancer Immunol Immunother 2007; 56:641-8.
40. Wang S, Konorev EA, Kotamraju S, Joseph J, Kalivendi S, Kalyanaraman B. Doxorubicin induces apoptosis in normal and tumor cells via distinctly different mechanisms. intermediacy of H(2)O(2)- and p53-dependent pathways. J Biol Chem 2004;279:25535-43.
41. Bettelli E, Korn T, Kuchroo VK. Th17: the third member of the effector T cell trilogy. Curr Opin Immunol 2007;19:652-7.
42. Korn T, Bettelli E, Oukka M, Kuchroo VK. IL-17 and Th17 Cells. Annu Rev Immunol 2009;27:485-517.
43. Muranski P, Boni A, Antony PA, Cassard L, Irvine KR, Kaiser A, et al. Tumor-specific Th17-polarized cells eradicate large established melanoma. Blood 2008;112:362-73.
44. Muranski P, Borman ZA, Kerkar SP, Klebanoff CA, Ji Y, Sanchez-Perez L, et al. Th17 cells are long lived and retain a stem cell-like molecular signature. Immunity 2011;35: 972-85.
45. Wei S, Zhao E, Kryczek I, Zou W. Th17 cells have stem cell-like features and promote long-term immunity. Oncoimmunology 2012; 1:516-9.
46. Chalmin F, Mignot G, Bruchard M, Chevriaux A, Vegran F, Hichami A, et al. Stat3 and Gfi-1 transcription factors control Th17 cell immunosuppressive activity via the regulation of ectonucleotidase expression. Immunity 2012;36:362-73.
47. Martin F, Apetoh L, Ghiringhelli F. Controversies on the role of Th17 in cancer: a TGF-β-dependent immunosuppressive activity? Trends Mol Med 2012;18:742-9.
48. Muranski P, Restifo NP. Essentials of Th17 cell commitment and plasticity. Blood 2013;121:2402-14.
49. Zou W, Restifo NP. T(H)17 cells in tumour immunity and immunotherapy. Nat Rev Immunol 2010;10:248-56.