Molecular mechanisms of ATP secretion during immunogenic cell death

Cell Death and Differentiation

Volumn 21, Issue 1, 2014, Pages 79-91

  Martins, I ^a,b   Wang, Y ^a,b   Michaud, M ^a,b   Ma, Y ^a,b   Sukkurwala, A Q ^a,b   Shen, S ^a,b   Kepp, O ^a,b   Metivier D ^a,b   Galluzzi, L ^a,c,d   Perfettini, J L ^a,b   Zitvogel, L ^a,b,e   Kroemer, G ^a,c,d,f  

^a INSTITUT GUSTAVE ROUSSY   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d CENTRE DE RECHERCHE DES CORDELIERS   (France)

^e INSERM   (France)

^f HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

Author keywords

apoptosis; Beclin 1; caspases; endoplasmic reticulum stress; quinacrine; U2OS cells

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; 4,4' DIISOTHIOCYANATOSTILBENE 2,2' DISULFONIC ACID; ADENOSINE TRIPHOSPHATE; ANTIMYCIN A1; BETA,GAMMA DIBROMOMETHYLENE 6 N,N DIETHYLADENOSINE TRIPHOSPHATE; BLEBBISTATIN; CALRETICULIN; CASPASE; DEOXYGLUCOSE; HIGH MOBILITY GROUP B1 PROTEIN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MEMBRANE PROTEIN; MEPACRINE; METHOTREXATE; MITOXANTRONE; MONENSIN; MYOSIN II; OXALIPLATIN; PANNEXIN 1; PROTEIN KINASE; RAPAMYCIN; RESVERATROL; RHO ASSOCIATED COILED COIL CONTAINING PROTEIN KINASE 1; SPERMIDINE; SYNAPTOBREVIN 1; UNCLASSIFIED DRUG;

ARTICLE; AUTOLYSOSOME; AUTOPHAGOSOME; AUTOPHAGY; CANCER CELL; CANCER CHEMOTHERAPY; CANCER IMMUNIZATION; CARCINOMA CELL; CELL DEATH; CELL MEMBRANE; CELL SURFACE; CELLULAR DISTRIBUTION; COLON CARCINOMA; CONTROLLED STUDY; ENZYME ACTIVATION; EXOCYTOSIS; EXTRACELLULAR SPACE; FIBROSARCOMA; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOGENIC CELL DEATH; LYSOSOME; MEMBRANE PERMEABILITY; MEMBRANE POTENTIAL; MITOCHONDRION; OSTEOSARCOMA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TRANSPORT;

ADENOSINE TRIPHOSPHATE; ANIMALS; ANTINEOPLASTIC AGENTS; CELL DEATH; CELL LINE, TUMOR; CELL MEMBRANE; CONNEXINS; DNA-BINDING PROTEINS; HMGB1 PROTEIN; HUMANS; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 1; LYSOSOMES; MICE; MICROTUBULE-ASSOCIATED PROTEINS; MYOSIN TYPE II; NERVE TISSUE PROTEINS; RHO-ASSOCIATED KINASES; RNA INTERFERENCE; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS;

EID: 84890103572     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2013.75     Document Type: Article

References (60)

1. Galluzzi L, Senovilla L, Zitvogel L, Kroemer G. The secret al.ly: Immunostimulation by anticancer drugs. Nat Rev Drug Discov 2012; 11: 215-233.
2. Kroemer G, Galluzzi L, Kepp O, Zitvogel L. Immunogenic cell death in cancer therapy. Annu Rev Immunol 2013; 31: 51-72.
3. 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: 860-875.
4. Vanneman M, Dranoff G. Combining immunotherapy and targeted therapies in cancer treatment. Nat Rev Cancer 2012; 12: 237-251.
5. Galluzzi L, Vitale I, Abrams JM, Alnemri ES, Baehrecke EH, Blagosklonny MV et al. Molecular definitions of cell death subroutines: Recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death Differ 2012; 19: 107-120.
6. Kroemer G, Galluzzi L, Vandenabeele P, Abrams J, Alnemri ES, Baehrecke EH et al. Classification of cell death: Recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ 2009; 16: 3-11.
7. 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: 1691-1701.
8. Obeid M, Panaretakis T, Joza N, Tufi R, Tesniere A, van Endert P et al. Calreticulin exposure is required for the immunogenicity of gamma-irradiation and UVC light-induced apoptosis. Cell Death Differ 2007; 14: 1848-1850.
9. Tanaka H, Matsushima H, Nishibu A, Clausen BE, Takashima A. Dual therapeutic efficacy of vinblastine as a unique chemotherapeutic agent capable of inducing dendritic cell maturation. Cancer Res 2009; 69: 6987-6994.
10. 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: 641-648.
11. Green DR, Ferguson T, Zitvogel L, Kroemer G. Immunogenic and tolerogenic cell death. Nat Rev Immunol 2009; 9: 353-363.
12. Galluzzi L, Kepp O, Kroemer G. Mitochondria: Master regulators of danger signalling. Nat Rev Mol Cell Biol 2012; 13: 780-788.
13. Ferguson TA, Choi J, Green DR. Armed response: How dying cells influence T-cell functions. Immunol Rev 2011; 241: 77-88.
14. Tesniere A, Schlemmer F, Boige V, Kepp O, Martins I, Ghiringhelli F et al. Immunogenic death of colon cancer cells treated with oxaliplatin. Oncogene 2010; 29: 482-491.
15. Schiavoni G, Sistigu A, Valentini M, Mattei F, Sestili P, Spadaro F et al. Cyclophosphamide synergizes with type I interferons through systemic dendritic cell reactivation and induction of immunogenic tumor apoptosis. Cancer Res 2011; 71: 768-778.
16. Senovilla L, Vitale I, Martins I, Tailler M, Pailleret C, Michaud M et al. An immunosurveillance mechanism controls cancer cell ploidy. Science 2012; 337: 1678-1684.
17. Menger L, Vacchelli E, Adjemian S, Martins I, Ma Y, Shen S et al. Cardiac glycosides exert anticancer effects by inducing immunogenic cell death. Sci Transl Med 2012; 4: 143ra199.
18. Kepp O, Menger L, Vacchelli E, Adjemian S, Martins I, Ma Y et al. Anticancer activity of cardiac glycosides: At the frontier between cell-Autonomous and immunological effects. Oncoimmunology 2012; 1: 1640-1642.
19. Menger L, Vacchelli E, Kepp O, Eggermont A, Tartour E, Zitvogel L et al. Trial watch: Cardiac glycosides and cancer therapy. Oncoimmunology 2013; 2: E23082.
20. Vacchelli E, Galluzzi L, Fridman WH, Galon J, Sautes-Fridman C, Tartour E et al. Trial Watch: Chemotherapy with immunogenic cell death inducers. Oncoimmunology 2012; 1: 179-188.
21. Vacchelli E, Senovilla L, Eggermont A, Fridman WH, Galon J, Zitvogel L et al. Trial Watch: Chemotherapy with immunogenic cell death inducers. Oncoimmunology 2013; 2: E23510.
22. 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.
23. Michaud M, Martins I, Sukkurwala AQ, Adjemian S, Ma Y, Pellegatti P et al. Autophagydependent anticancer immune responses induced by chemotherapeutic agents in mice. Science 2011; 334: 1573-1577.
24. Ma Y, Adjemian S, Mattarollo SR, Yamazaki T, Aymeric L, Yang H et al. Anticancer chemotherapy-induced intratumoral recruitment and differentiation of antigen-presenting cells. Immunity 2013; 38: 729-741.
25. Ayna G, Krysko DV, Kaczmarek A, Petrovski G, Vandenabeele P, Fesus L. ATP release from dying autophagic cells and their phagocytosis are crucial for inflammasome activation in macrophages. PLoS One 2012; 7: E40069.
26. Zitvogel L, Kepp O, Galluzzi L, Kroemer G. Inflammasomes in carcinogenesis and anticancer immune responses. Nat Immunol 2012; 13: 343-351.
27. Vacchelli E, Galluzzi L, Rousseau V, Rigoni A, Tesniere A, Delahaye N et al. Loss-of-function alleles of P2RX7 and TLR4 fail to affect the response to chemotherapy in non-small cell lung cancer. Oncoimmunology 2012; 1: 271-278.
28. 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: 393-395.
29. Martins I, Tesniere A, Kepp O, Michaud M, Schlemmer F, Senovilla L et al. Chemotherapy induces ATP release from tumor cells. Cell Cycle 2009; 8: 3723-3728.
30. Fader CM, Aguilera MO, Colombo MI. ATP is released from autophagic vesicles to the extracellular space in a VAMP7-dependent manner. Autophagy 2012; 8: 1741-1756.
31. Sandilos JK, Chiu YH, Chekeni FB, Armstrong AJ, Walk SF, Ravichandran KS et al. Pannexin 1, an ATP release channel, is activated by caspase cleavage of its pore-Associated C-Terminal autoinhibitory region. J Biol Chem 2012; 287: 11303-11311.
32. Elliott MR, Chekeni FB, Trampont PC, Lazarowski ER, Kadl A, Walk SF et al. Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature 2009; 461: 282-286.
33. Chekeni FB, Elliott MR, Sandilos JK, Walk SF, Kinchen JM, Lazarowski ER et al. Pannexin 1 channels mediate 'find-me' signal release and membrane permeability during apoptosis. Nature 2010; 467: 863-867.
34. Qu Y, Misaghi S, Newton K, Gilmour LL, Louie S, Cupp JE et al. Pannexin-1 is required for ATP release during apoptosis but not for inflammasome activation. J Immunol 2011; 186: 6553-6561.
35. Zhang Z, Chen G, Zhou W, Song A, Xu T, Luo Q et al. Regulated ATP release from astrocytes through lysosome exocytosis. Nat Cell Biol 2007; 9: 945-953.
36. Pangrsic T, Potokar M, Stenovec M, Kreft M, Fabbretti E, Nistri A et al. Exocytotic release of ATP from cultured astrocytes. J Biol Chem 2007; 282: 28749-28758.
37. Martins I, Michaud M, Sukkurwala AQ, Adjemian S, Ma Y, Shen S et al. Premortem autophagy determines the immunogenicity of chemotherapy-induced cancer cell death. Autophagy 2012; 8: 413-415.
38. Akopova I, Tatur S, Grygorczyk M, Luchowski R, Gryczynski I, Gryczynski Z et al. Imaging exocytosis of ATP-containing vesicles with TIRF microscopy in lung epithelial A549 cells. Purinergic Signal 2012; 8: 59-70.
39. Straight AF, Cheung A, Limouze J, Chen I, Westwood NJ, Sellers JR et al. Dissecting temporal and spatial control of cytokinesis with a myosin II Inhibitor. Science 2003; 299: 1743-1747.
40. Uehata M, Ishizaki T, Satoh H, Ono T, Kawahara T, Morishita T et al. Calcium sensitization of smooth muscle mediated by a Rho-Associated protein kinase in hypertension. Nature 1997; 389: 990-994.
41. Coleman ML, Sahai EA, Yeo M, Bosch M, Dewar A, Olson MF. Membrane blebbing during apoptosis results from caspase-mediated activation of ROCK I. Nat Cell Biol 2001; 3: 339-345.
42. Sebbagh M, Renvoize C, Hamelin J, Riche N, Bertoglio J, Breard J. Caspase-3-mediated cleavage of ROCK I induces MLC phosphorylation and apoptotic membrane blebbing. Nat Cell Biol 2001; 3: 346-352.
43. Iglesias R, Locovei S, Roque A, Alberto AP, Dahl G, Spray DC et al. P2-7 receptor-Pannexin1 complex: Pharmacology and signaling. Am J Physiol Cell Physiol 2008; 295: C752-C760.
44. Sathe MN, Woo K, Kresge C, Bugde A, Luby-Phelps K, Lewis MA et al. Regulation of purinergic signaling in biliary epithelial cells by exocytosis of SLC17A9-dependent ATPenriched vesicles. J Biol Chem 2011; 286: 25363-25376.
45. Mullick A, Xu Y, Warren R, Koutroumanis M, Guilbault C, Broussau S et al. The cumate gene-switch: A system for regulated expression in mammalian cells. BMC Biotechnol 2006; 6: 43.
46. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012; 8: 445-544.
47. Berg TO, Stromhaug E, Lovdal T, Seglen O, Berg T. Use of glycyl-L-phenylalanine 2-naphthylamide, a lysosome-disrupting cathepsin C substrate, to distinguish between lysosomes and prelysosomal endocytic vacuoles. Biochem J 1994; 300(Pt 1): 229-236.
48. Sherer NM, Lehmann MJ, Jimenez-Soto LF, Ingmundson A, Horner SM, Cicchetti G et al. Visualization of retroviral replication in living cells reveals budding into multivesicular bodies. Traffic 2003; 4: 785-801.
49. Morselli E, Marino G, Bennetzen MV, Eisenberg T, Megalou E, Schroeder S et al. Spermidine and resveratrol induce autophagy by distinct pathways converging on the acetylproteome. J Cell Biol 2011; 192: 615-629.
50. Gonzalez-Polo RA, Boya P, Pauleau AL, Jalil A, Larochette N, Souquere S et al. The apoptosis/autophagy paradox: Autophagic vacuolization before apoptotic death. J Cell Sci 2005; 118: 3091-3102.
51. Liu Y, Sugiura Y, Lin W. The role of synaptobrevin1/VAMP1 in Ca2+-Triggered neurotransmitter release at the mouse neuromuscular junction. J Physiol 2011; 589: 1603-1618.
52. Ainscow EK, Mirshamsi S, Tang T, Ashford ML, Rutter GA. Dynamic imaging of free cytosolic ATP concentration during fuel sensing by rat hypothalamic neurones: Evidence for ATP-independent control of ATP-sensitive K(+) channels. J Physiol 2002; 544: 429-445.
53. Li A, Banerjee J, Leung CT, Peterson-Yantorno K, Stamer WD, Civan MM. Mechanisms of ATP release, the enabling step in purinergic dynamics. Cell Physiol Biochem 2011; 28: 1135-1144.
54. Gonzales E, Julien B, Serriere-Lanneau V, Nicou A, Doignon I, Lagoudakis L et al. ATP release after partial hepatectomy regulates liver regeneration in the rat. J Hepatol 2010; 52: 54-62.
55. Franz S, Herrmann K, Furnrohr BG, Sheriff A, Frey B, Gaipl US et al. After shrinkage apoptotic cells expose internal membrane-derived epitopes on their plasma membranes. Cell Death Differ 2007; 14: 733-742.
56. Martins I, Kepp O, Schlemmer F, Adjemian S, Tailler M, Shen S et al. Restoration of the immunogenicity of cisplatin-induced cancer cell death by endoplasmic reticulum stress. Oncogene 2011; 30: 1147-1158.
57. de La Motte Rouge T, Galluzzi L, Olaussen KA, Zermati Y, Tasdemir E, Robert T et al. A novel epidermal growth factor receptor inhibitor promotes apoptosis in non-small cell lung cancer cells resistant to erlotinib. Cancer Res 2007; 67: 6253-6262.
58. Galluzzi L, Morselli E, Vitale I, Kepp O, Senovilla L, Criollo A et al. miR-181a and miR-630 regulate cisplatin-induced cancer cell death. Cancer Res 2010; 70: 1793-1803.
59. Kepp O, Galluzzi L, Lipinski M, Yuan J, Kroemer G. Cell death assays for drug discovery. Nat Rev Drug Discov 2011; 10: 221-237.
60. Galluzzi L, Zamzami N, de La Motte Rouge T, Lemaire C, Brenner C, Kroemer G. Methods for the assessment of mitochondrial membrane permeabilization in apoptosis. Apoptosis 2007; 12: 803-813.