Anthracyclines potentiate anti-tumor immunity: A new opportunity for chemoimmunotherapy

Cancer Letters

Volumn 369, Issue 2, 2015, Pages 331-335

  Zhang, Zhigang ^a,b   Yu, Xiuyang ^a   Wang, Zhen ^b   Wu, Pin ^b   Huang, Jian ^a,b  

^a ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b THE SECOND AFFILIATED HOSPITAL OF ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Anthracyclines; Anticancer immunity; Chemoimmunotherapy; Doxorubicin; Immunomodulation

Indexed keywords

ANTHRACYCLINE; ANTINEOPLASTIC ANTIBIOTIC; DOXORUBICIN;

ANTINEOPLASTIC ACTIVITY; CANCER IMMUNOTHERAPY; CLINICAL EFFECTIVENESS; DRUG EFFICACY; DRUG MECHANISM; DRUG RESPONSE; FEEDBACK SYSTEM; HUMAN; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOREGULATION; IMMUNOSURVEILLANCE; MALIGNANT NEOPLASTIC DISEASE; MOLECULAR DYNAMICS; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; SHORT SURVEY; TUMOR IMMUNITY; IMMUNOLOGY; IMMUNOTHERAPY; TUMOR MICROENVIRONMENT;

ANTHRACYCLINES; ANTIBIOTICS, ANTINEOPLASTIC; DOXORUBICIN; HUMANS; IMMUNOMODULATION; IMMUNOTHERAPY; TUMOR MICROENVIRONMENT;

EID: 84945314387     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2015.10.002     Document Type: Review

References (46)

1. Alvarez R.D., Morgan R.J., Armstrong D.K., Burger R.A., Chen L.M., Copeland L., et al. Ovarian cancer, version 1.2015. J. Natl Compr. Canc. Netw 2015, 20:1339-1349.
2. Anderson B.O., Gradishar W.J., Balassanian R., Blair S.L., Burstein H.J., Cyr A., et al. Breast cancer version 2.2015. J. Natl Compr. Canc. Netw 2015, 13:448-475.
3. Brown P.A., Alvarnas J.C., Aoun P., Ballen K.K., Bellam N., Blum W., et al. Acute lymphoblastic leukemia. Version 1.2015. J. Natl Compr. Canc. Netw 2015.
4. Rabbani A., Finn R.M., Ausio J. The anthracycline antibiotics: antitumor drugs that alter chromatin structure. Bioessays 2005, 27:50-56.
5. Casares N., Pequignot M.O., Tesniere A., Ghiringhelli F., Roux S., Chaput N., et al. Caspase-dependent immunogenicity of doxorubicin-induced tumor cell death. J. Exp. Med 2005, 202:1691-1701.
6. Galluzzi L., Senovilla L., Zitvogel L., Kroemer G. The secret ally: immunostimulation by anticancer drugs. Nat. Rev. Drug Discov 2012, 11:215-233.
7. Ruffell B., Au A., Rugo H.S., Esserman L.J., Hwang E.S., Coussens L.M. Leukocyte composition of human breast cancer. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:2796-2801.
8. Dieci M.V., 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, 25:611-618.
9. West N.R., Milne K., Truong P.T., Macpherson N., Nelson B.H., Watson P.H. Tumor-infiltrating lymphocytes predict response to anthracycline-based chemotherapy in estrogen receptor-negative breast cancer. Breast Cancer Res 2011, 13:R126.
10. Bossuyt V., Provenzano E., Symmans W.F., Boughey J.C., Coles C., Curigliano G., et al. Recommendations for standardized pathological characterization of residual disease for neoadjuvant clinical trials of breast cancer by the BIG-NABCG collaboration. Ann. Oncol 2015, 26:1280-1291.
11. Steele T.A. Chemotherapy-induced immunosuppression and reconstitution of immune function. Leuk. Res 2002, 26:411-414.
12. Apetoh L., Mignot G., Panaretakis T., Kroemer G., Zitvogel L. Immunogenicity of anthracyclines: moving towards more personalized medicine. Trends Mol. Med 2008, 14:141-151.
13. Obeid M., Tesniere A., Ghiringhelli F., Fimia G.M., Apetoh L., Perfettini J.L., et al. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat. Med 2007, 13:54-61.
14. Zitvogel L., Kepp O., Senovilla L., Menger L., Chaput N., Kroemer G. Immunogenic tumor cell death for optimal anticancer therapy: the calreticulin exposure pathway. Clin. Cancer Res 2010, 16:3100-3104.
15. Ghiringhelli F., Apetoh L., Tesniere A., Aymeric L., Ma Y., Ortiz C., et al. Activation of the NLRP3 inflammasome in dendritic cells induces IL-1beta-dependent adaptive immunity against tumors. Nat. Med 2009, 15:1170-1178.
16. Sistigu A., Yamazaki T., Vacchelli E., Chaba K., Enot D.P., Adam J., et al. Cancer cell-autonomous contribution of type I interferon signaling to the efficacy of chemotherapy. Nat. Med 2014, 20:1301-1309.
17. Niiya M., Niiya K., Kiguchi T., Shibakura M., Asaumi N., Shinagawa K., et al. Induction of TNF-alpha, uPA, IL-8 and MCP-1 by doxorubicin in human lung carcinoma cells. Cancer Chemother. Pharmacol 2003, 52:391-398.
18. Qian D.Z., Rademacher B.L., Pittsenbarger J., Huang C.Y., Myrthue A., Higano C.S., et al. CCL2 is induced by chemotherapy and protects prostate cancer cells from docetaxel-induced cytotoxicity. Prostate 2010, 70:433-442.
19. Ma Y., Mattarollo S.R., Adjemian S., Yang H., Aymeric L., Hannani D., et al. CCL2/CCR2-dependent recruitment of functional antigen-presenting cells into tumors upon chemotherapy. Cancer Res 2014, 74:436-445.
20. Antonopoulos C., Dubyak G.R. Chemotherapy engages multiple pathways leading to IL-1beta production by myeloid leukocytes. Oncoimmunology 2014, 3:e27499.
21. Hu J., Zhu S., Xia X., Zhang L., Kleinerman E.S., Li S. CD8+T cell-specific induction of NKG2D receptor by doxorubicin plus interleukin-12 and its contribution to CD8+T cell accumulation in tumors. Mol. Cancer 2014, 13:34.
22. Ma Y., Aymeric L., Locher C., Mattarollo S.R., Delahaye N.F., Pereira P., et al. Contribution of IL-17-producing gamma delta T cells to the efficacy of anticancer chemotherapy. J. Exp. Med 2011, 208:491-503.
23. Alizadeh D., Trad M., Hanke N.T., Larmonier C.B., Janikashvili N., Bonnotte B., et al. Doxorubicin eliminates myeloid-derived suppressor cells and enhances the efficacy of adoptive T-cell transfer in breast cancer. Cancer Res 2014, 74:104-118.
24. Mattarollo S.R., Loi S., Duret H., Ma Y., Zitvogel L., Smyth M.J. Pivotal role of innate and adaptive immunity in anthracycline chemotherapy of established tumors. Cancer Res 2011, 71:4809-4820.
25. Alizadeh D., Larmonier N. Chemotherapeutic targeting of cancer-induced immunosuppressive cells. Cancer Res 2014, 74:2663-2668.
26. Lesterhuis W.J., Haanen J.B., Punt C.J. Cancer immunotherapy - revisited. Nat. Rev. Drug Discov 2011, 10:591-600.
27. Emens L.A. Chemoimmunotherapy. Cancer J. 2010, 16:295-303.
28. Kirkwood J.M., Butterfield L.H., Tarhini A.A., Zarour H., Kalinski P., Ferrone S. Immunotherapy of cancer in 2012. CA Cancer J. Clin 2012, 62:309-335.
29. Ewens A., Luo L., Berleth E., Alderfer J., Wollman R., Hafeez B.B., et al. Doxorubicin plus interleukin-2 chemoimmunotherapy against breast cancer in mice. Cancer Res 2006, 66:5419-5426.
30. Ehrke M.J., Verstovsek S., Maccubbin D.L., Ujházy P., Zaleskis G., Berleth E., et al. Protective specific immunity induced by doxorubicin plus TNF-alpha combination treatment of EL4 lymphoma-bearing C57BL/6 mice. Int. J. Cancer 2000, 87:101-109.
31. Buter J., Pinedo H.M. Neoadjuvant chemoimmunotherapy in locally advanced breast cancer: a new avenue to be explored. Curr. Oncol. Rep 2003, 5:171-176.
32. Honkoop A.H., Luykx-de Bakker S.A., Hoekman K., Meyer S., Meyer O.W., van Groeningen C.J., et al. Prolonged neoadjuvant chemotherapy with GM-CSF in locally advanced breast cancer. Oncologist 1999, 4:106-111.
33. Parra H.S., Tixi L., Latteri F., Bretti S., Alloisio M., Gravina A., et al. Combined regimen of cisplatin, doxorubicin, and alpha-2b interferon in the treatment of advanced malignant pleural mesothelioma: a phase II multicenter trial of the Italian Group on Rare Tumors (GITR) and the Italian Lung Cancer Task Force (FONICAP). Cancer 2001, 92:650-656.
34. Simpkins F., Flores A., Chu C., Berek J.S., Lucci J., Murray S., et al. Chemoimmunotherapy using pegylated liposomal Doxorubicin and interleukin-18 in recurrent ovarian cancer: a phase I dose-escalation study. Cancer Immunol. Res 2013, 1:168-178.
35. Eralp Y., Wang X., Wang J.P., Maughan M.F., Polo J.M., Lachman L.B. 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-R283.
36. Machiels J.P., Reilly R.T., Emens L.A., Ercolini A.M., Lei R.Y., Weintraub D., et al. Cyclophosphamide, doxorubicin, and paclitaxel enhance the antitumor immune response of granulocyte/macrophage-colony stimulating factor-secreting whole-cell vaccines in HER-2/neu tolerized mice. Cancer Res 2001, 61:3689-3697.
37. Marconato L., Frayssinet P., Rouquet N., Comazzi S., Leone V.F., Laganga P., et al. Randomized, placebo-controlled, double-blinded chemoimmunotherapy clinical trial in a pet dog model of diffuse large B-cell lymphoma. Clin. Cancer Res 2014, 20:668-677.
38. Ding Z.C., Munn D.H., Zhou G. Chemotherapy-induced myeloid suppressor cells and antitumor immunity: the Janus face of chemotherapy in immunomodulation. Oncoimmunology 2014, 3:e954471.
39. Zhu S., Waguespack M., Barker S.A., Li S. Doxorubicin directs the accumulation of interleukin-12 induced IFN gamma into tumors for enhancing STAT1 dependent antitumor effect. Clin. Cancer Res 2007, 13:4252-4260.
40. Mattarollo S.R., Kenna T., Nieda M., Nicol A.J. Chemotherapy and zoledronate sensitize solid tumour cells to Vgamma9Vdelta2 T cell cytotoxicity. Cancer Immunol. Immunother 2007, 56:1285-1297.
41. Todaro M., Orlando V., Cicero G., Caccamo N., Meraviglia S., Stassi G., et al. Chemotherapy sensitizes colon cancer initiating cells to Vgamma9Vdelta2 T cell-mediated cytotoxicity. PLoS ONE 2013, 8:e65145.
42. Todaro M., Meraviglia S., Caccamo N., Stassi G., Dieli F. Combining conventional chemotherapy and γδ T cell-based immunotherapy to target cancer-initiating cells. Oncoimmunology 2013, 2:e25821.
43. Chen D.S., Mellman I. Oncology meets immunology: the cancer-immunity cycle. Immunity 2013, 39:1-10.
44. Couzin-Frankel J. Breakthrough of the year 2013. Cancer immunotherapy. Science 2013, 342:1432-1433.
45. Ikeda S., Hansel D.E., Kurzrock R. Beyond conventional chemotherapy: emerging molecular targeted and immunotherapy strategies in urothelial carcinoma. Cancer Treat. Rev 2015, 41:699-706.
46. Wayteck L., Breckpot K., Demeester J., De Smedt S.C., Raemdonck K. A personalized view on cancer immunotherapy. Cancer Lett 2014, 352:113-125.