ATP is released from autophagic vesicles to the extracellular space in a VAMP7-dependent manner

Autophagy

Volumn 8, Issue 12, 2012, Pages 1741-1756

  Fader, Claudio Marcelo ^a   Aguilera, Milton Osmar ^a   Colombo, María Isabel ^a  

^a FACULTAD DE CIENCIAS MÉDICAS   (Argentina)

Author keywords

ATP; Autophagosome; Autophagy; Focal adhesions; LC3; SNAREs; VAMP7

Indexed keywords

ADENOSINE TRIPHOSPHATE; CELL PROTEIN; MEMBRANE PROTEIN; MOLECULAR MOTOR; NUCLEOTIDE; PROTEIN KIF5; PROTEIN LC3; PROTEIN VAMP7; RAB INTERACTING LYSOSOMAL PROTEIN; RAB7 PROTEIN; SNARE PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; AUTOCRINE EFFECT; AUTOPHAGOSOME; AUTOPHAGY; CELL DEATH; CELL FUNCTION; CELL MEMBRANE; CELL VACUOLE; CONTROLLED STUDY; EXTRACELLULAR SPACE; FOCAL ADHESION; HELA CELL; HUMAN; IMMUNOGENICITY; INFLAMMATION; MICROTUBULE; PARACRINE SIGNALING; PROTEIN LOCALIZATION; TUMOR CELL LINE;

EID: 84870858655     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.21858     Document Type: Article

References (65)

1. Knecht E, Aguado C, Cárcel J, Esteban I, Esteve JM, Ghislat G, et al. Intracellular protein degradation in mammalian cells: recent developments. Cell Mol Life Sci 2009; 66:2427-43; PMID:19399586; http://dx.doi.org/10.1007/ s00018-009-0030-6
2. Cuervo AM. The plasma membrane brings autophagosomes to life. Nat Cell Biol 2010; 12:735-7; PMID:20680002; http://dx.doi.org/10.1038/ncb0810-735
3. Hailey DW, Rambold AS, Satpute-Krishnan P, Mitra K, Sougrat R, Kim PK, et al. Mitochondria supply membranes for autophagosome biogenesis during starvation. Cell 2010; 141:656-67; PMID:20478256; http://dx.doi.org/10.1016/j. cell.2010.04.009
4. Hayashi-Nishino M, Fujita N, Noda T, Yamaguchi A, Yoshimori T, Yamamoto A. A subdomain of the endoplasmic reticulum forms a cradle for autophagosome formation. Nat Cell Biol 2009; 11:1433-7; PMID:19898463; http://dx.doi.org/10. 1038/ncb1991
5. Mari M, Griffith J, Rieter E, Krishnappa L, Klionsky DJ, Reggiori F. An Atg9-containing compartment that functions in the early steps of autophagosome biogenesis. J Cell Biol 2010; 190:1005-22; PMID:20855505; http://dx.doi.org/10. 1083/jcb.200912089
6. van der Vaart A, Reggiori F. The Golgi complex as a source for yeast autophagosomal membranes. Autophagy 2010; 6:800-1; PMID:20714226; http://dx.doi.org/10.4161/auto.6.6.12575
7. Yen WL, Shintani T, Nair U, Cao Y, Richardson BC, Li Z, et al. The conserved oligomeric Golgi complex is involved in double-membrane vesicle formation during autophagy. J Cell Biol 2010; 188:101-14; PMID:20065092; http://dx.doi.org/10.1083/jcb.200904075
8. Ylä-Anttila P, Vihinen H, Jokitalo E, Eskelinen EL. 3D tomography reveals connections between the phagophore and endoplasmic reticulum. Autophagy 2009; 5:1180-5; PMID:19855179; http://dx.doi.org/10.4161/auto.5.8.10274
9. Zoppino FC, Militello RD, Slavin I, Alvarez C, Colombo MI. Autophagosome formation depends on the small GTPase Rab1 and functional ER exit sites. Traffic 2010; 11:1246-61; PMID:20545908; http://dx.doi.org/10.1111/j.1600-0854.2010. 01086.x
10. Ravikumar B, Moreau K, Rubinsztein DC. Plasma membrane helps autophagosomes grow. Autophagy 2010; 6:1184-6; PMID:20861674; http://dx.doi.org/10.4161/auto.6.8.13428
11. Berg TO, Fengsrud M, Strømhaug PE, Berg T, Seglen PO. Isolation and characterization of rat liver amphisomes. Evidence for fusion of autophagosomes with both early and late endosomes. J Biol Chem 1998; 273:21883-92; PMID:9705327; http://dx.doi.org/10.1074/jbc.273.34.21883
12. Eskelinen EL. Maturation of autophagic vacuoles in Mammalian cells. Autophagy 2005; 1:1-10; PMID:16874026; http://dx.doi.org/10.4161/auto.1.1.1270
13. Chaineau M, Danglot L, Galli T. Multiple roles of the vesicular-SNARE TI-VAMP in post-Golgi and endosomal trafficking. FEBS Lett 2009; 583:3817-26; PMID:19837067; http://dx.doi.org/10.1016/j.febslet.2009.10.026
14. Brunger AT, Weninger K, Bowen M, Chu S. Single-molecule studies of the neuronal SNARE fusion machinery. Annu Rev Biochem 2009; 78:903-28; PMID:19489736; http://dx.doi.org/10.1146/annurev.biochem.77.070306.103621
15. Galli T, Zahraoui A, Vaidyanathan VV, Raposo G, Tian JM, Karin M, et al. A novel tetanus neurotoxin-insensitive vesicle-associated membrane protein in SNARE complexes of the apical plasma membrane of epithelial cells. Mol Biol Cell 1998; 9:1437-48; PMID:9614185
16. Advani RJ, Bae HR, Bock JB, Chao DS, Doung YC, Prekeris R, et al. Seven novel mammalian SNARE proteins localize to distinct membrane compartments. J Biol Chem 1998; 273:10317-24; PMID:9553086; http://dx.doi.org/10.1074/jbc.273. 17.10317
17. Advani RJ, Yang B, Prekeris R, Lee KC, Klumperman J, Scheller RH. VAMP-7 mediates vesicular transport from endosomes to lysosomes. J Cell Biol 1999; 146:765-76; PMID:10459012; http://dx.doi.org/10.1083/jcb.146.4.765
18. Fader CM, Sánchez DG, Mestre MB, Colombo MI. TI-VAMP/VAMP7 and VAMP3/cellubrevin: two v-SNARE proteins involved in specific steps of the autophagy/multivesicular body pathways. Biochim Biophys Acta 2009; 1793:1901-16; PMID:19781582; http://dx.doi.org/10.1016/j.bbamcr.2009.09.011
19. Oishi Y, Arakawa T, Tanimura A, Itakura M, Takahashi M, Tajima Y, et al. Role of VAMP-2, VAMP-7, and VAMP-8 in constitutive exocytosis from HSY cells. Histochem Cell Biol 2006; 125:273-81; PMID:16195891; http://dx.doi.org/10.1007/ s00418-005-0068-y
20. Moreau K, Ravikumar B, Renna M, Puri C, Rubinsztein DC. Autophagosome precursor maturation requires homotypic fusion. Cell 2011; 146:303-17; PMID:21784250; http://dx.doi.org/10.1016/j.cell.2011.06.023
21. Braun V, Fraisier V, Raposo G, Hurbain I, Sibarita JB, Chavrier P, et al. TI-VAMP/VAMP7 is required for optimal phagocytosis of opsonised particles in macrophages. EMBO J 2004; 23:4166-76; PMID:15470500; http://dx.doi.org/10.1038/ sj.emboj.7600427
22. Pryor PR, Mullock BM, Bright NA, Lindsay MR, Gray SR, Richardson SC, et al. Combinatorial SNARE complexes with VAMP7 or VAMP8 define different late endocytic fusion events. EMBO Rep 2004; 5:590-5; PMID:15133481; http://dx.doi.org/10.1038/sj.embor.7400150
23. Ward DM, Pevsner J, Scullion MA, Vaughn M, Kaplan J. Syntaxin 7 and VAMP-7 are soluble N-ethylmaleimide-sensitive factor attachment protein receptors required for late endosome-lysosome and homotypic lysosome fusion in alveolar macrophages. Mol Biol Cell 2000; 11:2327-33; PMID:10888671
24. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 2000; 19:5720-8; PMID:11060023; http://dx.doi.org/10.1093/emboj/19.21.5720
25. Mauthe M, Jacob A, Freiberger S, Hentschel K, Stierhof YD, Codogno P, et al. Resveratrol-mediated autophagy requires WIPI-1-regulated LC3 lipidation in the absence of induced phagophore formation. Autophagy 2011; 7:1448-61; PMID:22082875; http://dx.doi.org/10.4161/auto.7.12.17802
26. Morselli E, Mariño 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; 192:615-29; PMID:21339330; http://dx.doi.org/10.1083/jcb.201008167
27. Madeo F, Eisenberg T, Büttner S, Ruckenstuhl C, Kroemer G. Spermidine: a novel autophagy inducer and longevity elixir. Autophagy 2010; 6:160-2; PMID:20110777; http://dx.doi.org/10.4161/auto.6.1.10600
28. Berrier AL, Yamada KM. Cell-matrix adhesion. J Cell Physiol 2007; 213:565-73; PMID:17680633; http://dx.doi.org/10.1002/jcp.21237
29. Gutierrez MG, Vázquez CL, Munafó DB, Zoppino FC, Berón W, Rabinovitch M, et al. Autophagy induction favours the generation and maturation of the Coxiella-replicative vacuoles. Cell Microbiol 2005; 7:981-93; PMID:15953030; http://dx.doi.org/10.1111/j.1462-5822.2005.00527.x
30. Jäger S, Bucci C, Tanida I, Ueno T, Kominami E, Saftig P, et al. Role for Rab7 in maturation of late autophagic vacuoles. J Cell Sci 2004; 117:4837-48; PMID:15340014; http://dx.doi.org/10.1242/jcs.01370
31. Progida C, Malerød L, Stuffers S, Brech A, Bucci C, Stenmark H. RILP is required for the proper morphology and function of late endosomes. J Cell Sci 2007; 120:3729-37; PMID:17959629; http://dx.doi.org/10.1242/jcs.017301
32. Xie P. Mechanism of processive movement of monomeric and dimeric kinesin molecules. Int J Biol Sci 2010; 6:665-74; PMID:21060728; http://dx.doi.org/10. 7150/ijbs.6.665
33. Luna C, Li G, Qiu J, Challa P, Epstein DL, Gonzalez P. Extracellular release of ATP mediated by cyclic mechanical stress leads to mobilization of AA in trabecular meshwork cells. Invest Ophthalmol Vis Sci 2009; 50:5805-10; PMID:19608543; http://dx.doi.org/10.1167/iovs.09-3796
34. Miller DS, Villalobos AR, Pritchard JB. Organic cation transport in rat choroid plexus cells studied by fluorescence microscopy. Am J Physiol 1999; 276:C955-68; PMID:10199828
35. Coco S, Calegari F, Pravettoni E, Pozzi D, Taverna E, Rosa P, et al. Storage and release of ATP from astrocytes in culture. J Biol Chem 2003; 278:1354-62; PMID:12414798; http://dx.doi.org/10.1074/jbc. M209454200
36. Bodin P, Burnstock G. Evidence that release of adenosine triphosphate from endothelial cells during increased shear stress is vesicular. J Cardiovasc Pharmacol 2001; 38:900-8; PMID:11707694; http://dx.doi.org/10.1097/00005344- 200112000-00012
37. 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; 282:28749-58; PMID:17627942; http://dx.doi.org/10.1074/jbc. M700290200
38. Martins RM, Alves RM, Macedo S, Yoshida N. Starvation and rapamycin differentially regulate host cell lysosome exocytosis and invasion by Trypanosoma cruzi metacyclic forms. Cell Microbiol 2011; 13:943-54; PMID:21501360; http://dx.doi.org/10.1111/j.1462-5822.2011.01590.x
39. Steffen A, Le Dez G, Poincloux R, Recchi C, Nassoy P, Rottner K, et al. MT1-MMP-dependent invasion is regulated by TI-VAMP/VAMP7. Curr Biol 2008; 18:926-31; PMID:18571410; http://dx.doi.org/10.1016/j.cub.2008.05.044
40. Mili S, Moissoglu K, Macara IG. Genome-wide screen reveals APC-associated RNAs enriched in cell protrusions. Nature 2008; 453:115-9; PMID:18451862; http://dx.doi.org/10.1038/nature06888
41. Tuloup-Minguez V, Greffard A, Codogno P, Botti J. Regulation of autophagy by extracellular matrix glycoproteins in HeLa cells. Autophagy 2011; 7:27-39; PMID:20980830; http://dx.doi.org/10.4161/auto.7.1.13851
42. Martinez-Arca S, Arold S, Rudge R, Laroche F, Galli T. A mutant impaired in SNARE complex dissociation identifies the plasma membrane as first target of synaptobrevin 2. Traffic 2004; 5:371-82; PMID:15086786; http://dx.doi.org/10. 1111/j.1398-9219.2004.00180.x
43. Korolchuk VI, Saiki S, Lichtenberg M, Siddiqi FH, Roberts EA, Imarisio S, et al. Lysosomal positioning coordinates cellular nutrient responses. Nat Cell Biol 2011; 13:453-60; PMID:21394080; http://dx.doi.org/10.1038/ncb2204
44. Cantalupo G, Alifano P, Roberti V, Bruni CB, Bucci C. Rab-interacting lysosomal protein (RILP): the Rab7 effector required for transport to lysosomes. EMBO J 2001; 20:683-93; PMID:11179213; http://dx.doi.org/10.1093/emboj/20.4.683
45. Wang T, Ming Z, Xiaochun W, Hong W. Rab7: role of its protein interaction cascades in endo-lysosomal traffic. Cell Signal 2011; 23:516-21; PMID:20851765; http://dx.doi.org/10.1016/j.cellsig.2010.09.012
46. Harrison RE, Bucci C, Vieira OV, Schroer TA, Grinstein S. Phagosomes fuse with late endosomes and/ or lysosomes by extension of membrane protrusions along microtubules: role of Rab7 and RILP. Mol Cell Biol 2003; 23:6494-506; PMID:12944476; http://dx.doi.org/10.1128/MCB.23.18.6494-6506.2003
47. Jordens I, Fernandez-Borja M, Marsman M, Dusseljee S, Janssen L, Calafat J, et al. The Rab7 effector protein RILP controls lysosomal transport by inducing the recruitment of dynein-dynactin motors. Curr Biol 2001; 11:1680-5; PMID:11696325; http://dx.doi.org/10.1016/S0960-9822(01)00531-0
48. Santama N, Krijnse-Locker J, Griffiths G, Noda Y, Hirokawa N, Dotti CG. KIF2beta, a new kinesin superfamily protein in non-neuronal cells, is associated with lysosomes and may be implicated in their centrifugal translocation. EMBO J 1998; 17:5855-67; PMID:9774330; http://dx.doi.org/10.1093/emboj/17.20.5855
49. Matsushita M, Tanaka S, Nakamura N, Inoue H, Kanazawa H. A novel kinesin-like protein, KIF1Bbeta3 is involved in the movement of lysosomes to the cell periphery in non-neuronal cells. Traffic 2004; 5:140-51; PMID:15086790; http://dx.doi.org/10.1111/j.1600-0854.2003.00165.x
50. Pankiv S, Alemu EA, Brech A, Bruun JA, Lamark T, Overvatn A, et al. FYCO1 is a Rab7 effector that binds to LC3 and PI3P to mediate microtubule plus end-directed vesicle transport. J Cell Biol 2010; 188:253-69; PMID:20100911; http://dx.doi.org/10.1083/jcb.200907015
51. Cardoso CM, Groth-Pedersen L, Høyer-Hansen M, Kirkegaard T, Corcelle E, Andersen JS, et al. Depletion of kinesin 5B affects lysosomal distribution and stability and induces peri-nuclear accumulation of autophagosomes in cancer cells. PLoS One 2009; 4:e4424; PMID:19242560; http://dx.doi.org/10.1371/journal.pone.0004424
52. Ravikumar B, Moreau K, Jahreiss L, Puri C, Rubinsztein DC. Plasma membrane contributes to the formation of pre-autophagosomal structures. Nat Cell Biol 2010; 12:747-57; PMID:20639872; http://dx.doi.org/10.1038/ncb2078
53. Bal-Price A, Moneer Z, Brown GC. Nitric oxide induces rapid, calcium-dependent release of vesicular glutamate and ATP from cultured rat astrocytes. Glia 2002; 40:312-23; PMID:12420311; http://dx.doi.org/10.1002/glia. 10124
54. Di Virgilio F. Liaisons dangereuses: P2X(7) and the inflammasome. Trends Pharmacol Sci 2007; 28:465-72; PMID:17692395; http://dx.doi.org/10.1016/j.tips. 2007.07.002
55. 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; 15:1170-8; PMID:19767732; http://dx.doi.org/10.1038/nm.2028
56. Aymeric L, Apetoh L, Ghiringhelli F, Tesniere A, Martins I, Kroemer G, et al. Tumor cell death and ATP release prime dendritic cells and efficient anticancer immunity. Cancer Res 2010; 70:855-8; PMID:20086177; http://dx.doi.org/10.1158/0008-5472.CAN-09-3566
57. Kreda SM, Okada SF, van Heusden CA, O'Neal W, Gabriel S, Abdullah L, et al. Coordinated release of nucleotides and mucin from human airway epithelial Calu-3 cells. J Physiol 2007; 584:245-59; PMID:17656429; http://dx.doi.org/10. 1113/jphysiol.2007.139840
58. Rieg T, Vallon V. ATP and adenosine in the local regulation of water transport and homeostasis by the kidney. Am J Physiol Regul Integr Comp Physiol 2009; 296:R419-27; PMID:19020292; http://dx.doi.org/10.1152/ajpregu.90784.2008
59. Hovater MB, Olteanu D, Welty EA, Schwiebert EM. Purinergic signaling in the lumen of a normal nephron and in remodeled PKD encapsulated cysts. Purinergic Signal 2008; 4:109-24; PMID:18438719; http://dx.doi.org/10.1007/ s11302-008-9102-6
60. Lee JH, Marcus DC. Purinergic signaling in the inner ear. Hear Res 2008; 235:1-7; PMID:17980525; http://dx.doi.org/10.1016/j.heares.2007.09.006
61. Oury C, Toth-Zsamboki E, Vermylen J, Hoylaerts MF. The platelet ATP and ADP receptors. Curr Pharm Des 2006; 12:859-75; PMID:16515502; http://dx.doi.org/10.2174/138161206776056029
62. Martins I, Tesniere A, Kepp O, Michaud M, Schlemmer F, Senovilla L, et al. Chemotherapy induces ATP release from tumor cells. Cell Cycle 2009; 8:3723-8; PMID:19855167; http://dx.doi.org/10.4161/cc.8.22.10026
63. Michaud M, Martins I, Sukkurwala AQ, Adjemian S, Ma Y, Pellegatti P, 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
64. Martinez-Arca S, Alberts P, Galli T. Clostridial neurotoxin-insensitive vesicular SNAREs in exocytosis and endocytosis. Biol Cell 2000; 92:449-53; PMID:11132707; http://dx.doi.org/10.1016/S0248-4900(00)01096-0
65. Edelstein A, Amodaj N, Hoover K, Vale R, Stuurman N. Computer control of microscopes using microManager. Curr Protoc Mol Biol 2010; Chapter 14:Unit14