SNARE proteins are required for macroautophagy

Cell

Volumn 146, Issue 2, 2011, Pages 290-302

  Nair, Usha ^a   Jotwani, Anjali ^b   Geng, Jiefei ^a   Gammoh, Noor ^c   Richerson, Diana ^d   Yen, Wei Lien ^a   Griffith, Janice ^e   Nag, Shanta ^b   Wang, Ke ^a   Moss, Tyler ^f   Baba, Misuzu ^g   McNew, James A ^f   Jiang, Xuejun ^c   Reggiori, Fulvio ^e   Melia, Thomas J ^d   Klionsky, Daniel J ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b YALE UNIVERSITY   (United States)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^f RICE UNIVERSITY   (United States)

^g KOGAKUIN UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ATG8 PROTEIN; ATG9 PROTEIN; PHOSPHATIDYLETHANOLAMINE BINDING PROTEIN; SNARE PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; BIOGENESIS; CLUSTER ANALYSIS; CONTROLLED STUDY; EXOCYTOSIS; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT;

EID: 79960798816     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2011.06.022     Document Type: Article

References (58)

1. M.K. Aalto, H. Ronne, and S. Keränen Yeast syntaxins Sso1p and Sso2p belong to a family of related membrane proteins that function in vesicular transport EMBO J. 12 1993 4095 4104 (Pubitemid 23302023)
2. H. Abeliovich, T. Darsow, and S.D. Emr Cytoplasm to vacuole trafficking of aminopeptidase I requires a t-SNARE-Sec1p complex composed of Tlg2p and Vps45p EMBO J. 18 1999 6005 6016 (Pubitemid 29515677)
3. P. Brennwald, B. Kearns, K. Champion, S. Keränen, V. Bankaitis, and P. Novick Sec9 is a SNAP-25-like component of a yeast SNARE complex that may be the effector of Sec4 function in exocytosis Cell 79 1994 245 258 (Pubitemid 24324915)
4. B. Brügger, W. Nickel, T. Weber, F. Parlati, J.A. McNew, J.E. Rothman, and T. Söllner Putative fusogenic activity of NSF is restricted to a lipid mixture whose coalescence is also triggered by other factors EMBO J. 19 2000 1272 1278 (Pubitemid 30151023)
5. C.M. Carr, E. Grote, M. Munson, F.M. Hughson, and P.J. Novick Sec1p binds to SNARE complexes and concentrates at sites of secretion J. Cell Biol. 146 1999 333 344 (Pubitemid 29369771)
6. L.V. Chernomordik, and M.M. Kozlov Protein-lipid interplay in fusion and fission of biological membranes Annu. Rev. Biochem. 72 2003 175 207 (Pubitemid 36930445)
7. M. Fukasawa, O. Varlamov, W.S. Eng, T.H. Söllner, and J.E. Rothman Localization and activity of the SNARE Ykt6 determined by its regulatory domain and palmitoylation Proc. Natl. Acad. Sci. USA 101 2004 4815 4820 (Pubitemid 38469160)
8. J. Geng, U. Nair, K. Yasumura-Yorimitsu, and D.J. Klionsky Post-Golgi Sec proteins are required for autophagy in Saccharomyces cerevisiae Mol. Biol. Cell 21 2010 2257 2269
9. E. Grote, C.M. Carr, and P.J. Novick Ordering the final events in yeast exocytosis J. Cell Biol. 151 2000 439 452
10. D.W. Hailey, A.S. Rambold, P. Satpute-Krishnan, K. Mitra, R. Sougrat, P.K. Kim, and J. Lippincott-Schwartz Mitochondria supply membranes for autophagosome biogenesis during starvation Cell 141 2010 656 667
11. E. Harsay, and A. Bretscher Parallel secretory pathways to the cell surface in yeast J. Cell Biol. 131 1995 297 310
12. J.C. Holthuis, B.J. Nichols, S. Dhruvakumar, and H.R.B. Pelham Two syntaxin homologues in the TGN/endosomal system of yeast EMBO J. 17 1998 113 126 (Pubitemid 28041053)
13. K. Isahara, Y. Ohsawa, S. Kanamori, M. Shibata, S. Waguri, N. Sato, T. Gotow, T. Watanabe, T. Momoi, and K. Urase Regulation of a novel pathway for cell death by lysosomal aspartic and cysteine proteinases Neuroscience 91 1999 233 249 (Pubitemid 29170462)
14. N. Ishihara, M. Hamasaki, S. Yokota, K. Suzuki, Y. Kamada, A. Kihara, T. Yoshimori, T. Noda, and Y. Ohsumi Autophagosome requires specific early Sec proteins for its formation and NSF/SNARE for vacuolar fusion Mol. Biol. Cell 12 2001 3690 3702 (Pubitemid 33108497)
15. J. Jäntti, M.K. Aalto, M. Oyen, L. Sundqvist, S. Keränen, and H. Ronne Characterization of temperature-sensitive mutations in the yeast syntaxin 1 homologues Sso1p and Sso2p, and evidence of a distinct function for Sso1p in sporulation J. Cell Sci. 115 2002 409 420 (Pubitemid 34145189)
16. Y. Liu, and C. Barlowe Analysis of Sec22p in endoplasmic reticulum/Golgi transport reveals cellular redundancy in SNARE protein function Mol. Biol. Cell 13 2002 3314 3324 (Pubitemid 35034265)
17. Y. Liu, J.J. Flanagan, and C. Barlowe Sec22p export from the endoplasmic reticulum is independent of SNARE pairing J. Biol. Chem. 279 2004 27225 27232 (Pubitemid 38812560)
18. M.A. Lynch-Day, D. Bhandari, S. Menon, J. Huang, H. Cai, C.R. Bartholomew, J.H. Brumell, S. Ferro-Novick, and D.J. Klionsky Trs85 directs a Ypt1 GEF, TRAPPIII, to the phagophore to promote autophagy Proc. Natl. Acad. Sci. USA 107 2010 7811 7816
19. M. Mari, J. Griffith, E. Rieter, L. Krishnappa, D.J. Klionsky, and F. Reggiori An Atg9-containing compartment that functions in the early steps of autophagosome biogenesis J. Cell Biol. 190 2010 1005 1022
20. A. Mayer, W. Wickner, and A. Haas Sec18p (NSF)-driven release of Sec17p (α-SNAP) can precede docking and fusion of yeast vacuoles Cell 85 1996 83 94 (Pubitemid 26116809)
21. J.A. McNew, M. Sogaard, N.M. Lampen, S. Machida, R.R. Ye, L. Lacomis, P. Tempst, J.E. Rothman, and T.H. Söllner Ykt6p, a prenylated SNARE essential for endoplasmic reticulum-Golgi transport J. Biol. Chem. 272 1997 17776 17783 (Pubitemid 27311217)
22. J.A. McNew, F. Parlati, R. Fukuda, R.J. Johnston, K. Paz, F. Paumet, T.H. Söllner, and J.E. Rothman Compartmental specificity of cellular membrane fusion encoded in SNARE proteins Nature 407 2000 153 159
23. H. Nakatogawa, Y. Ichimura, and Y. Ohsumi Atg8, a ubiquitin-like protein required for autophagosome formation, mediates membrane tethering and hemifusion Cell 130 2007 165 178 (Pubitemid 47031316)
24. T. Noda, J. Kim, W.-P. Huang, M. Baba, C. Tokunaga, Y. Ohsumi, and D.J. Klionsky Apg9p/Cvt7p is an integral membrane protein required for transport vesicle formation in the Cvt and autophagy pathways J. Cell Biol. 148 2000 465 480
25. F. Paumet, B. Brügger, F. Parlati, J.A. McNew, T.H. Söllner, and J.E. Rothman A t-SNARE of the endocytic pathway must be activated for fusion J. Cell Biol. 155 2001 961 968 (Pubitemid 34286247)
26. V. Protopopov, B. Govindan, P. Novick, and J.E. Gerst Homologs of the synaptobrevin/VAMP family of synaptic vesicle proteins function on the late secretory pathway in S. cerevisiae Cell 74 1993 855 861 (Pubitemid 23270605)
27. B. Ravikumar, K. Moreau, L. Jahreiss, C. Puri, and D.C. Rubinsztein Plasma membrane contributes to the formation of pre-autophagosomal structures Nat. Cell Biol. 12 2010 747 757
28. F. Reggiori, K.A. Tucker, P.E. Stromhaug, and D.J. Klionsky The Atg1-Atg13 complex regulates Atg9 and Atg23 retrieval transport from the pre-autophagosomal structure Dev. Cell 6 2004 79 90 (Pubitemid 38089207)
29. F. Reggiori, C.-W. Wang, U. Nair, T. Shintani, H. Abeliovich, and D.J. Klionsky Early stages of the secretory pathway, but not endosomes, are required for Cvt vesicle and autophagosome assembly in Saccharomyces cerevisiae Mol. Biol. Cell 15 2004 2189 2204 (Pubitemid 38580638)
30. F. Reggiori, T. Shintani, U. Nair, and D.J. Klionsky Atg9 cycles between mitochondria and the pre-autophagosomal structure in yeasts Autophagy 1 2005 101 109
31. B.L. Scott, J.S. Van Komen, H. Irshad, S. Liu, K.A. Wilson, and J.A. McNew Sec1p directly stimulates SNARE-mediated membrane fusion in vitro J. Cell Biol. 167 2004 75 85 (Pubitemid 39363416)
32. C. Ungermann, G.F. von Mollard, O.N. Jensen, N. Margolis, T.H. Stevens, and W. Wickner Three v-SNAREs and two t-SNAREs, present in a pentameric cis-SNARE complex on isolated vacuoles, are essential for homotypic fusion J. Cell Biol. 145 1999 1435 1442 (Pubitemid 29310001)
33. G. van Meer, D.R. Voelker, and G.W. Feigenson Membrane lipids: where they are and how they behave Nat. Rev. Mol. Cell Biol. 9 2008 112 124 (Pubitemid 351158912)
34. H. Weidberg, T. Shpilka, E. Shvets, A. Abada, F. Shimron, and Z. Elazar LC3 and GATE-16 N termini mediate membrane fusion processes required for autophagosome biogenesis Dev. Cell 20 2011 444 454
35. Z. Xie, U. Nair, and D.J. Klionsky Atg8 controls phagophore expansion during autophagosome formation Mol. Biol. Cell 19 2008 3290 3298
36. W.-L. Yen, T. Shintani, U. Nair, Y. Cao, B.C. Richardson, Z. Li, F.M. Hughson, M. Baba, and D.J. Klionsky The conserved oligomeric Golgi complex is involved in double-membrane vesicle formation during autophagy J. Cell Biol. 188 2010 101 114
37. Ames, P., Studdert, C.A., Reiser, R.H., and Parkinson, J.S. (2002). Collaborative signaling by mixed chemoreceptor teams in Escherichia coli. Proc. Natl. Acad. Sci. USA 99, 7060-7065. (Pubitemid 34526255)
38. Cheong, H., Nair, U., Geng, J., and Klionsky, D.J. (2008). The Atg1 kinase complex is involved in the regulation of protein recruitment to initiate sequestering vesicle formation for nonspecific autophagy in Saccharomyces cerevisiae. Mol. Biol. Cell 19, 668-681. (Pubitemid 351272154)
39. Griffith, J., Mari, M., De Mazire, A., and Reggiori, F. (2008). A cryosectioning procedure for the ultrastructural analysis and the immunogold labelling of yeast S. cerevisiae. Traffic 9, 1060-1072. (Pubitemid 351916883)
40. He, C., Song, H., Yorimitsu, T., Monastyrska, I., Yen, W.-L., Legakis, J.E., and Klionsky, D.J. (2006). Recruitment of Atg9 to the preautophagosomal structure by Atg11 is essential for selective autophagy in budding yeast. J. Cell Biol. 175, 925-935. (Pubitemid 44969198)
41. Huang, W.-P., Scott, S.V., Kim, J., and Klionsky, D.J. (2000). The itinerary of a vesicle component, Aut7p/Cvt5p, terminates in the yeast vacuole via the autophagy/Cvt pathways. J. Biol. Chem. 275, 5845-5851. (Pubitemid 30115231)
42. Jäntti, J., Aalto, M.K., Oyen, M., Sundqvist, L., Keränen, S., and Ronne, H. (2002). Characterization of temperature-sensitive mutations in the yeast syntaxin 1 homologues Sso1p and Sso2p, and evidence of a distinct function for Sso1p in sporulation. J. Cell Sci. 115, 409-420. (Pubitemid 34145189)
43. Kim, J., Huang, W.-P., Stromhaug, P.E., and Klionsky, D.J. (2002). Convergence of multiple autophagy and cytoplasm to vacuole targeting components to a perivacuolar membrane compartment prior to de novo vesicle formation. J. Biol. Chem. 277, 763-773. (Pubitemid 34952117)
44. Kim, J., Huang, W.-P., and Klionsky, D.J. (2001). Membrane recruitment of Aut7p in the autophagy and cytoplasm to vacuole targeting pathways requires Aut1p, Aut2p, and the autophagy conjugation complex. J. Cell Biol. 152, 51-64. (Pubitemid 32102436)
45. Kirisako, T., Baba, M., Ishihara, N., Miyazawa, K., Ohsumi, M., Yoshimori, T., Noda, T., and Ohsumi, Y. (1999). Formation process of autophagosome is traced with Apg8/Aut7p in yeast. J. Cell Biol. 147, 435-446. (Pubitemid 29496349)
46. Krick, R., Bremer, S., Welter, E., Schlotterhose, P., Muehe, Y., Eskelinen, E.L., and Thumm, M. (2010). Cdc48/p97 and Shp1/p47 regulate autophagosome biogenesis in concert with ubiquitin-like Atg8. J. Cell Biol. 190, 965-973.
47. McNew, J.A., Weber, T., Parlati, F., Johnston, R.J., Melia, T.J., Söllner, T.H., and Rothman, J.E. (2000). Close is not enough: SNARE-dependent membrane fusion requires an active mechanism that transduces force to membrane anchors. J. Cell Biol. 150, 105-117. (Pubitemid 30480230)
48. Melia, T.J., Weber, T., McNew, J.A., Fisher, L.E., Johnston, R.J., Parlati, F., Mahal, L.K., Sollner, T.H., and Rothman, J.E. (2002). Regulation of membrane fusion by the membrane-proximal coil of the t-SNARE during zippering of SNAREpins. J. Cell Biol. 158, 929-940. (Pubitemid 35001083)
49. Monastyrska, I., He, C., Geng, J., Hoppe, A.D., Li, Z., and Klionsky, D.J. (2008). Arp2 links autophagic machinery with the actin cytoskeleton. Mol. Biol. Cell 19, 1962-1975.
50. Noda, T., Matsuura, A., Wada, Y., and Ohsumi, Y. (1995). Novel system for monitoring autophagy in the yeast Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 210, 126-132.
51. Paumet, F., Rahimian, V., Di Liberto, M., and Rothman, J.E. (2005). Concerted auto-regulation in yeast endosomal t-SNAREs. J. Biol. Chem. 280, 21137-21143. (Pubitemid 40805674)
52. Shen, J., Tareste, D.C., Paumet, F., Rothman, J.E., and Melia, T.J. (2007). Selective activation of cognate SNAREpins by Sec1/Munc18 proteins. Cell 128, 183-195. (Pubitemid 46048894)
53. Snyder, W.B., Koller, A., Choy, A.J., and Subramani, S. (2000). The peroxin Pex19p interacts with multiple, integral membrane proteins at the peroxisomal membrane. J. Cell Biol. 149, 1171-1178.
54. Struck, D.K., Hoekstra, D., and Pagano, R.E. (1981). Use of resonance energy transfer to monitor membrane fusion. Biochemistry 20, 4093-4099.
55. Wallis, J.W., Chrebet, G., Brodsky, G., Rolfe, M., and Rothstein, R. (1989). A hyper-recombination mutation in S. cerevisiae identifies a novel eukaryotic topoisomerase. Cell 58, 409-419. (Pubitemid 19191422)
56. Yang, Z., Geng, J., Yen, W.-L., Wang, K., and Klionsky, D.J. (2010). Positive or negative roles of different cyclin-dependent kinase Pho85-cyclin complexes orchestrate induction of autophagy in Saccharomyces cerevisiae. Mol. Cell 38, 250-264.
57. Yen, W.-L., Shintani, T., Nair, U., Cao, Y., Richardson, B.C., Li, Z., Hughson, F.M., Baba, M., and Klionsky, D.J. (2010). The conserved oligomeric Golgi complex is involved in double-membrane vesicle formation during autophagy. J. Cell Biol. 188, 101-114.
58. Yorimitsu, T., Zaman, S., Broach, J.R., and Klionsky, D.J. (2007). Protein kinase A and Sch9 cooperatively regulate induction of autophagy in Saccharomyces cerevisiae. Mol. Biol. Cell 18, 4180-4189. (Pubitemid 47519506)