An autophagy-dependent anticancer immune response determines the efficacy of melanoma chemotherapy

OncoImmunology

Volumn 3, Issue 7, 2014, Pages

  Michaud, Mickaël ^a,b,c   Xie, Xiaoqi ^g   Pedro, José Manuel Bravo San ^a,b,c   Zitvogel, Laurence ^d,e,f   White, Eileen ^g,h,i   Kroemer, Guido ^a,b,c,j  

^a CENTRE DE RECHERCHE DES CORDELIERS   (France)

^b INSTITUT GUSTAVE ROUSSY   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d University Paris XI   (France)

^e UNIVERSITÉ PARIS SACLAY   (France)

^f Center of Clinical Investigations in Biotherapies of Cancer   (France)

^g RUTGERS CANCER INSTITUTE OF NEW JERSEY   (United States)

^h RUTGERS UNIVERSITY   (United States)

ⁱ RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^j HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

more..

Author keywords

Anthracycline; Autophagy; Cancer

Indexed keywords

AFIMOXIFENE; B RAF KINASE; CRE RECOMBINASE; MITOXANTRONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; ATG7 GENE; AUTOPHAGY; CANCER CHEMOTHERAPY; CANCER GRAFT; CANCER INHIBITION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; DRUG EFFICACY; GENE ACTIVATION; GENE INACTIVATION; GENOTYPE; HISTOPATHOLOGY; LYMPHOCYTE DEPLETION; MELANOCYTE; MELANOMA; MOUSE; NONHUMAN; ONCOGENE; ONCOGENE BRAF; PROTEIN EXPRESSION; PTEN GENE; TREATMENT RESPONSE; TUMOR IMMUNITY; TUMOR SUPPRESSOR GENE;

EID: 84911453574     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.4161/21624011.2014.944047     Document Type: Article

References (50)

1. Galluzzi L, Senovilla L, Zitvogel L, Kroemer G. The secret ally: immunostimulation by anticancer drugs. Nat Rev Drug Discov 2012; 11:215-33; PMID: 22301798; http://dx.doi.org/10.1038/nrd3626
2. Krysko DV, Garg AD, Kaczmarek A, Krysko O, Agostinis P, Vandenabeele P. Immunogenic cell death and DAMPs in cancer therapy. Nat Rev Cancer 2012; 12:860-75; PMID: 23151605; http://dx.doi. org/10.1038/nrc3380
3. Zitvogel L, Galluzzi L, Smyth MJ, Kroemer G. Mechanism of action of conventional and targeted anticancer therapies: reinstating immunosurveillance. Immunity 2013; 39:74-88; PMID: 23890065; http://dx.doi.org/10.1016/j.immuni.2013.06.014
4. Zitvogel L, Kepp O, Kroemer G. Immune parameters affecting the efficacy of chemotherapeutic regimens. Nat Rev Clin Oncol 2011; 8:151-60; PMID: 21364688; http://dx.doi.org/10.1038/nrclinonc.2010.223
5. Casares N, Pequignot MO, Tesniere A, Ghiringhelli F, Roux S, Chaput N, Schmitt E, Hamai A, Hervas-Stubbs S, Obeid M, et al. Caspase-dependent immunogenicity of doxorubicin-induced tumor cell death. J Exp Med 2005; 202:1691-701; PMID: 16365148; http://dx.doi.org/10.1084/jem.20050915
6. Michaud M, Martins I, Sukkurwala AQ, Adjemian S, Ma Y, Pellegatti P, Shen S, Kepp O, Scoazec M, Mignot G, et al. Autophagy-dependent anticancer immune responses induced by chemotherapeutic agents in mice. Science 2011; 334:1573-7; PMID: 22174255; http://dx.doi.org/10.1126/science.1208347
7. Obeid M, Tesniere A, Ghiringhelli F, Fimia GM, Apetoh L, Perfettini JL, Castedo M, Mignot G, Panaretakis T, Casares N, et al. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat Med 2007; 13:54-61; PMID: 17187072; http://dx. doi.org/10.1038/nm1523
8. Apetoh L, Ghiringhelli F, Tesniere A, Obeid M, Ortiz C, Criollo A, Mignot G, Maiuri MC, Ullrich E, Saulnier P, et al. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med 2007; 13:1050-9; PMID: 17704786; http://dx.doi.org/10.1038/nm1622
9. Tesniere A, Schlemmer F, Boige V, Kepp O, Martins I, Ghiringhelli F, Aymeric L, Michaud M, Apetoh L, Barault L, et al. Immunogenic death of colon cancer cells treated with oxaliplatin. Oncogene 2009; 29:482-91; PMID: 19881547; http://dx.doi.org/10.1038/onc.2009.356
10. Schiavoni G, Sistigu A, Valentini M, Mattei F, Sestili P, Spadaro F, Sanchez M, Lorenzi S, D'Urso MT, Belardelli F, et al. Cyclophosphamide synergizes with type I interferons through systemic dendritic cell reactivation and induction of immunogenic tumor apoptosis. Cancer Res 2010; 71:768-78; PMID: 21156650; http://dx.doi.org/10.1158/0008-5472. CAN-10-2788
11. Viaud S, Saccheri F, Mignot G, Yamazaki T, Daillere R, Hannani D, Enot DP, Pfirschke C, Engblom C, Pittet MJ, et al. The intestinal microbiota modulates the anticancer immune effects of cyclophosphamide. Science 2013; 342:971-6; PMID: 24264990; http://dx.doi.org/10.1126/science.1240537
12. Menger L, Vacchelli E, Adjemian S, Martins I, Ma Y, Shen S, Yamazaki T, Sukkurwala AQ, Michaud M, Mignot G, et al. Cardiac glycosides exert anticancer effects by inducing immunogenic cell death. Sci Transl Med 2012; 4:143ra99; PMID: 22814852; http://dx.doi.org/10.1126/scitranslmed.3003807
13. Menger L, Vacchelli E, Kepp O, Eggermont A, Tartour E, Zitvogel L, Kroemer G, Galluzzi L. Trial watch: cardiac glycosides and cancer therapy. Oncoimmunology 2013; 2:e23082; PMID: 23525565; http://dx.doi.org/10.4161/onci.23082
14. Senovilla L, Vitale I, Martins I, Tailler M, Pailleret C, Michaud M, Galluzzi L, Adjemian S, Kepp O, Niso-Santano M, et al. An immunosurveillance mechanism controls cancer cell ploidy. Science 2012; 337:1678-84; PMID: 23019653; http://dx.doi.org/10.1126/science.1224922
15. Kepp O, Galluzzi L, Kroemer G. Immune effectors required for the therapeutic activity of vorinostat. Oncoimmunology 2014; 2:e27157; http://dx.doi. org/10.4161/onci.27157
16. West AC, Mattarollo SR, Shortt J, Cluse LA, Christiansen AJ, Smyth MJ, Johnstone RW. An intact immune system is required for the anticancer activities of histone deacetylase inhibitors. Cancer Res 2013; 73:7265-76; PMID: 24158093; http://dx.doi. org/10.1158/0008-5472.CAN-13-0890
17. Galluzzi L, Kepp O, Kroemer G. Immunogenic cell death in radiation therapy. Oncoimmunology 2014; 2:e26536; http://dx.doi.org/10.4161/onci.26536
18. Ko A, Kanehisa A, Martins I, Senovilla L, Chargari C, Dugue D, Marino G, Kepp O, Michaud M, Perfettini JL, et al. Autophagy inhibition radiosensitizes in vitro, yet reduces radioresponses in vivo due to deficient immunogenic signalling. Cell Death Differ 2013; 21:92-9; PMID: 24037090; http://dx.doi.org/10.1038/cdd.2013.124
19. Obeid M, Panaretakis T, Joza N, TufiR, Tesniere A, van Endert P, Zitvogel L, Kroemer G. Calreticulin exposure is required for the immunogenicity of gamma-irradiation and UVC light-induced apoptosis. Cell Death Differ 2007; 14:1848-50; PMID: 17657249; http://dx.doi.org/10.1038/sj. cdd.4402201
20. Garg AD, Krysko DV, Vandenabeele P, Agostinis P. The emergence of phox-ER stress induced immunogenic apoptosis. Oncoimmunology 2012; 1:786-8; PMID: 22934283; http://dx.doi.org/10.4161/onci.19750
21. Garg AD, Krysko DV, Verfaillie T, Kaczmarek A, Ferreira GB, Marysael T, Rubio N, Firczuk M, Mathieu C, Roebroek AJ, et al. A novel pathway combining calreticulin exposure and ATP secretion in immunogenic cancer cell death. EMBO J 2012; 31:1062-79; PMID: 22252128; http://dx.doi.org/10.1038/emboj.2011.497
22. Martins I, Kepp O, Schlemmer F, Adjemian S, Tailler M, Shen S, Michaud M, Menger L, Gdoura A, Tajeddine N, et al. Restoration of the immunogenicity of cisplatin-induced cancer cell death by endoplasmic reticulum stress. Oncogene 2010; 30:1147-58; PMID: 21151176; http://dx.doi.org/10.1038/onc.2010.500
23. Martins I, Wang Y, Michaud M, Ma Y, Sukkurwala AQ, Shen S, Kepp O, Metivier D, Galluzzi L, Perfettini JL, et al. Molecular mechanisms of ATP secretion during immunogenic cell death. Cell Death Differ 2013; 21:79-91; PMID: 23852373; http://dx. doi.org/10.1038/cdd.2013.75
24. Panaretakis T, Joza N, Modjtahedi N, Tesniere A, Vitale I, Durchschlag M, Fimia GM, Kepp O, Piacentini M, Froehlich KU, et al. The co-translocation of ERp57 and calreticulin determines the immunogenicity of cell death. Cell Death Differ 2008; 15:1499-509; PMID: 18464797; http://dx.doi.org/10.1038/cdd.2008.67
25. Panaretakis T, Kepp O, Brockmeier U, Tesniere A, Bjorklund AC, Chapman DC, Durchschlag M, Joza N, Pierron G, van Endert P, et al. Mechanisms of pre-apoptotic calreticulin exposure in immunogenic cell death. EMBO J 2009; 28:578-90; PMID: 19165151; http://dx.doi.org/10.1038/emboj.2009.1
26. Yamazaki T, Hannani D, Poirier-Colame V, Ladoire S, Locher C, Sistigu A, Prada N, Adjemian S, Catani JP, Freudenberg M, et al. Defective immunogenic cell death of HMGB1-deficient tumors: compensatory therapy with TLR4 agonists. Cell Death Differ 2013; 21:69-78; PMID: 23811849; http://dx.doi. org/10.1038/cdd.2013.72
27. Kroemer G, Galluzzi L, Kepp O, Zitvogel L. Immunogenic cell death in cancer therapy. Annu Rev Immunol 2012; 31:51-72; PMID: 23157435; http://dx.doi.org/10.1146/annurev-immunol-032712-100008
28. Tesniere A, Apetoh L, Ghiringhelli F, Joza N, Panaretakis T, Kepp O, Schlemmer F, Zitvogel L, Kroemer G. Immunogenic cancer cell death: a key-lock paradigm. Curr Opin Immunol 2008; 20:504-11; PMID: 18573340; http://dx.doi.org/10.1016/j. coi.2008.05.007
29. Ma Y, Adjemian S, Mattarollo SR, Yamazaki T, Aymeric L, Yang H, Portela Catani JP, Hannani D, Duret H, Steegh K, et al. Anticancer chemotherapyinduced intratumoral recruitment and differentiation of antigen-presenting cells. Immunity 2013; 38:729-41.
30. Ma Y, Mattarollo SR, Adjemian S, Yang H, Aymeric L, Hannani D, Portela Catani JP, Duret H, Teng MW, Kepp O, et al. CCL2/CCR2-dependent recruitment of functional antigen-presenting cells into tumors upon chemotherapy. Cancer Res 2013; 74:436-45; PMID: 24302580; http://dx.doi.org/10.1158/0008-5472.CAN-13-1265
31. Michaud M, Sukkurwala AQ, Martins I, Shen S, Zitvogel L, Kroemer G. Subversion of the chemotherapy-induced anticancer immune response by the ecto-ATPase CD39. Oncoimmunology 2012; 1:393-5; PMID: 22737627; http://dx.doi.org/10.4161/onci.19070
32. Wang Y, Martins I, Ma Y, Kepp O, Galluzzi L, Kroemer G. Autophagy-dependent ATP release from dying cells via lysosomal exocytosis. Autophagy 2013; 9:1624-5.
33. Ma Y, Galluzzi L, Zitvogel L, Kroemer G. Autophagy and cellular immune responses. Immunity 2013; 39:211-27; PMID: 23973220; http://dx.doi.org/10.1016/j.immuni.2013.07.017
34. Ciampricotti M, Hau CS, Doornebal CW, Jonkers J, de Visser KE. Chemotherapy response of spontaneous mammary tumors is independent of the adaptive immune system. Nat Med 2012; 18:344-6; author reply 6; PMID: 22395693; http://dx.doi.org/10.1038/nm.2652
35. Kroemer G, Galluzzi L, Zitvogel L. Immunological effects of chemotherapy in spontaneous breast cancers. Oncoimmunology 2014; 2:e27158; http://dx. doi.org/10.4161/onci.27158
36. 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; PMID: 21646474; http://dx.doi.org/10.1158/0008-5472. CAN-11-0753
37. Hannesdottir L, Tymoszuk P, Parajuli N, Wasmer MH, Philipp S, Daschil N, Datta S, Koller JB, Tripp CH, Stoitzner P, et al. Lapatinib and doxorubicin enhance the Stat1-dependent antitumor immune response. Eur J Immunol 2013; 43:2718-29; PMID: 23843024; http://dx.doi.org/10.1002/eji.201242505
38. Fridman WH, Galon J, Pages F, Tartour E, Sautes-Fridman C, Kroemer G. Prognostic and predictive impact of intra- and peritumoral immune infiltrates. Cancer Res 2011; 71:5601-5; PMID: 21846822; http://dx.doi.org/10.1158/0008-5472.CAN-11-1316
39. Galon J, Angell HK, Bedognetti D, Marincola FM. The continuum of cancer immunosurveillance: prognostic, predictive, and mechanistic signatures. Immunity 2013; 39:11-26; PMID: 23890060; http://dx. doi.org/10.1016/j.immuni.2013.07.008
40. Senovilla L, Vacchelli E, Galon J, Adjemian S, Eggermont A, Fridman WH, Sautes-Fridman C, Ma Y, Tartour E, Zitvogel L, et al. Trial watch: Prognostic and predictive value of the immune infiltrate in cancer. Oncoimmunology 2012; 1:1323-43; PMID: 23243596; http://dx.doi.org/10.4161/onci.22009
41. Denkert C, Loibl S, Noske A, Roller M, Muller BM, Komor M, Budczies J, Darb-Esfahani S, Kronenwett R, Hanusch C, et al. Tumor-associated lymphocytes as an independent predictor of response to neoadjuvant chemotherapy in breast cancer. J Clin Oncol 2009; 28:105-13; PMID: 19917869; http://dx.doi. org/10.1200/JCO.2009.23.7370
42. Ladoire S, Mignot G, Dabakuyo S, Arnould L, Apetoh L, Rebe C, Coudert B, Martin F, Bizollon MH, Vanoli A, et al. In situ immune response after neoadjuvant chemotherapy for breast cancer predicts survival. J Pathol 2011; 224:389-400; PMID: 21437909; http://dx.doi.org/10.1002/path.2866
43. Loi S. Tumor-infiltrating lymphocytes, breast cancer subtypes and therapeutic efficacy. Oncoimmunology 2013; 2:e24720; PMID: 24073365; http://dx.doi. org/10.4161/onci.24720
44. Loi S, Sirtaine N, Piette F, Salgado R, Viale G, Van Eenoo F, Rouas G, Francis P, Crown JP, Hitre E, 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; PMID: 23341518; http://dx.doi.org/10.1200/JCO.2011.41.0902
45. Rao S, Yang H, Penninger JM, Kroemer G. Autophagy in non-small cell lung carcinogenesis: A positive regulator of antitumor immunosurveillance. Autophagy 2014; 10:529-31.
46. Maiuri MC, Tasdemir E, Criollo A, Morselli E, Vicencio JM, Carnuccio R, Kroemer G. Control of autophagy by oncogenes and tumor suppressor genes. Cell Death Differ 2009; 16:87-93; PMID: 18806760; http://dx.doi.org/10.1038/cdd.2008.131
47. Morselli E, Shen S, Ruckenstuhl C, Bauer MA, Marino G, Galluzzi L, Criollo A, Michaud M, Maiuri MC, Chano T, et al. p53 inhibits autophagy by interacting with the human ortholog of yeast Atg17, RB1CC1/FIP200. Cell Cycle 2011; 10:2763-9; PMID: 21775823; http://dx.doi.org/10.4161/cc.10.16.16868
48. Shen S, Niso-Santano M, Adjemian S, Takehara T, Malik SA, Minoux H, Souquere S, Marino G, Lachkar S, Senovilla L, et al. Cytoplasmic STAT3 represses autophagy by inhibiting PKR activity. Mol Cell 2012; 48:667-80; PMID: 23084476; http://dx. doi.org/10.1016/j.molcel.2012.09.013
49. Cartlidge RA, Thomas GR, Cagnol S, Jong KA, Molton SA, Finch AJ, McMahon M. Oncogenic BRAF (V600E) inhibits BIM expression to promote melanoma cell survival. Pigment Cell Melanoma Res 2008; 21:534-44; PMID: 18715233; http://dx.doi. org/10.1111/j.1755-148X.2008.00491.x
50. Komatsu M, Waguri S, Ueno T, Iwata J, Murata S, Tanida I, Ezaki J, Mizushima N, Ohsumi Y, Uchiyama Y, et al. Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J Cell Biol 2005; 169:425-34; PMID: 15866887; http://dx.doi.org/10.1083/jcb.200412022