An ER-Localized SNARE Protein Is Exported in Specific COPII Vesicles for Autophagosome Biogenesis

Cell Reports

Volumn 14, Issue 7, 2016, Pages 1710-1722

  Lemus, Leticia ^a   Ribas, Juan Luis ^a   Sikorska, Natalia ^a,b   Goder, Veit ^a  

^a UNIVERSITY OF SEVILLE   (Spain)

^b UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ATG8 PROTEIN; ATG9 PROTEIN; COAT PROTEIN COMPLEX II; GREEN FLUORESCENT PROTEIN; MEMBRANE PROTEIN; SNARE PROTEIN; TAP PROTEIN; THROMBOXANE RECEPTOR; UBIQUITIN; UFE1 PROTEIN; UNCLASSIFIED DRUG; ATG8 PROTEIN, S CEREVISIAE; ATG9 PROTEIN, S CEREVISIAE; AUTOPHAGY RELATED PROTEIN; AUTOPHAGY RELATED PROTEIN 8 FAMILY; CULTURE MEDIUM; MICROTUBULE ASSOCIATED PROTEIN; NITROGEN; SACCHAROMYCES CEREVISIAE PROTEIN; SYNTAXIN; UFE1 PROTEIN, S CEREVISIAE;

ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; BIOGENESIS; CELL VACUOLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; STARVATION; YEAST; COP-COATED VESICLE; CULTURE MEDIUM; DEFICIENCY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; LYSOSOME; METABOLISM; ORGANELLE BIOGENESIS; PHAGOSOME; PHARMACOLOGY; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; TEMPERATURE; ULTRASTRUCTURE;

AUTOPHAGY; AUTOPHAGY-RELATED PROTEIN 8 FAMILY; AUTOPHAGY-RELATED PROTEINS; COP-COATED VESICLES; CULTURE MEDIA; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION, FUNGAL; LYSOSOMES; MEMBRANE PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; NITROGEN; ORGANELLE BIOGENESIS; PHAGOSOMES; PROTEIN TRANSPORT; QA-SNARE PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; TEMPERATURE; VACUOLES;

EID: 84959114147     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.01.047     Document Type: Article

References (44)

1. Anwar K., Klemm R.W., Condon A., Severin K.N., Zhang M., Ghirlando R., Hu J., Rapoport T.A., Prinz W.A. The dynamin-like GTPase Sey1p mediates homotypic ER fusion in S. cerevisiae. J. Cell Biol. 2012, 197:209-217.
2. Bernales S., Schuck S., Walter P. ER-phagy: selective autophagy of the endoplasmic reticulum. Autophagy 2007, 3:285-287.
3. Biazik J., Ylä-Anttila P., Vihinen H., Jokitalo E., Eskelinen E.L. Ultrastructural relationship of the phagophore with surrounding organelles. Autophagy 2015, 11:439-451.
4. Braun S., Jentsch S. SM-protein-controlled ER-associated degradation discriminates between different SNAREs. EMBO Rep. 2007, 8:1176-1182.
5. Chen Y., Klionsky D.J. The regulation of autophagy - unanswered questions. J. Cell Sci. 2011, 124:161-170.
6. Cheong H., Klionsky D.J. Biochemical methods to monitor autophagy-related processes in yeast. Methods Enzymol. 2008, 451:1-26.
7. Dilcher M., Veith B., Chidambaram S., Hartmann E., Schmitt H.D., Fischer von Mollard G. Use1p is a yeast SNARE protein required for retrograde traffic to the ER. EMBO J. 2003, 22:3664-3674.
8. Ge L., Melville D., Zhang M., Schekman R. The ER-Golgi intermediate compartment is a key membrane source for the LC3 lipidation step of autophagosome biogenesis. eLife 2013, 2:e00947.
9. Graef M., Friedman J.R., Graham C., Babu M., Nunnari J. ER exit sites are physical and functional core autophagosome biogenesis components. Mol. Biol. Cell 2013, 24:2918-2931.
10. Hamasaki M., Noda T., Ohsumi Y. The early secretory pathway contributes to autophagy in yeast. Cell Struct. Funct. 2003, 28:49-54.
11. Hamasaki M., Noda T., Baba M., Ohsumi Y. Starvation triggers the delivery of the endoplasmic reticulum to the vacuole via autophagy in yeast. Traffic 2005, 6:56-65.
12. Hamasaki M., Furuta N., Matsuda A., Nezu A., Yamamoto A., Fujita N., Oomori H., Noda T., Haraguchi T., Hiraoka Y., et al. Autophagosomes form at ER-mitochondria contact sites. Nature 2013, 495:389-393.
13. 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, 11:1433-1437.
14. Hu J., Shibata Y., Zhu P.P., Voss C., Rismanchi N., Prinz W.A., Rapoport T.A., Blackstone C. A class of dynamin-like GTPases involved in the generation of the tubular ER network. Cell 2009, 138:549-561.
15. Ishihara N., Hamasaki M., Yokota S., Suzuki K., Kamada Y., Kihara A., Yoshimori T., Noda T., Ohsumi Y. Autophagosome requires specific early Sec proteins for its formation and NSF/SNARE for vacuolar fusion. Mol. Biol. Cell 2001, 12:3690-3702.
16. Itakura E., Kishi-Itakura C., Mizushima N. The hairpin-type tail-anchored SNARE syntaxin 17 targets to autophagosomes for fusion with endosomes/lysosomes. Cell 2012, 151:1256-1269.
17. Jin M., Klionsky D.J. Regulation of autophagy: modulation of the size and number of autophagosomes. FEBS Lett. 2014, 588:2457-2463.
18. Jin M., He D., Backues S.K., Freeberg M.A., Liu X., Kim J.K., Klionsky D.J. Transcriptional regulation by Pho23 modulates the frequency of autophagosome formation. Curr. Biol. 2014, 24:1314-1322.
19. Kirisako T., Baba M., Ishihara N., Miyazawa K., Ohsumi M., Yoshimori T., Noda T., Ohsumi Y. Formation process of autophagosome is traced with Apg8/Aut7p in yeast. J. Cell Biol. 1999, 147:435-446.
20. Klionsky D.J. Autophagy: from phenomenology to molecular understanding in less than a decade. Nat. Rev. Mol. Cell Biol. 2007, 8:931-937.
21. Kushnirov V.V. Rapid and reliable protein extraction from yeast. Yeast 2000, 16:857-860.
22. Lewis M.J., Rayner J.C., Pelham H.R. A novel SNARE complex implicated in vesicle fusion with the endoplasmic reticulum. EMBO J. 1997, 16:3017-3024.
23. Lipatova Z., Segev N. A role for macro-ER-phagy in ER quality control. PLoS Genet. 2015, 11:e1005390.
24. Mari M., Griffith J., Rieter E., Krishnappa L., Klionsky D.J., Reggiori F. An Atg9-containing compartment that functions in the early steps of autophagosome biogenesis. J. Cell Biol. 2010, 190:1005-1022.
25. McNew J.A., Parlati F., Fukuda R., Johnston R.J., Paz K., Paumet F., Söllner T.H., Rothman J.E. Compartmental specificity of cellular membrane fusion encoded in SNARE proteins. Nature 2000, 407:153-159.
26. Miller E.A., Schekman R. COPII - a flexible vesicle formation system. Curr. Opin. Cell Biol. 2013, 25:420-427.
27. Mochida K., Oikawa Y., Kimura Y., Kirisako H., Hirano H., Ohsumi Y., Nakatogawa H. Receptor-mediated selective autophagy degrades the endoplasmic reticulum and the nucleus. Nature 2015, 522:359-362.
28. Moreau K., Ravikumar B., Renna M., Puri C., Rubinsztein D.C. Autophagosome precursor maturation requires homotypic fusion. Cell 2011, 146:303-317.
29. Müller V.S., Jungblut P.R., Meyer T.F., Hunke S. Membrane-SPINE: an improved method to identify protein-protein interaction partners of membrane proteins in vivo. Proteomics 2011, 11:2124-2128.
30. Müller M., Schmidt O., Angelova M., Faserl K., Weys S., Kremser L., Pfaffenwimmer T., Dalik T., Kraft C., Trajanoski Z., et al. The coordinated action of the MVB pathway and autophagy ensures cell survival during starvation. eLife 2015, 4:e07736.
31. Nair U., Jotwani A., Geng J., Gammoh N., Richerson D., Yen W.L., Griffith J., Nag S., Wang K., Moss T., et al. SNARE proteins are required for macroautophagy. Cell 2011, 146:290-302.
32. Newman A.P., Shim J., Ferro-Novick S. BET1, BOS1, and SEC22 are members of a group of interacting yeast genes required for transport from the endoplasmic reticulum to the Golgi complex. Mol. Cell. Biol. 1990, 10:3405-3414.
33. Ohashi Y., Munro S. Membrane delivery to the yeast autophagosome from the Golgi-endosomal system. Mol. Biol. Cell 2010, 21:3998-4008.
34. Ohsumi Y. Molecular dissection of autophagy: two ubiquitin-like systems. Nat. Rev. Mol. Cell Biol. 2001, 2:211-216.
35. Patel S.K., Indig F.E., Olivieri N., Levine N.D., Latterich M. Organelle membrane fusion: a novel function for the syntaxin homolog Ufe1p in ER membrane fusion. Cell 1998, 92:611-620.
36. Piper R.C., Cooper A.A., Yang H., Stevens T.H. VPS27 controls vacuolar and endocytic traffic through a prevacuolar compartment in Saccharomyces cerevisiae. J. Cell Biol. 1995, 131:603-617.
37. Popovic D., Akutsu M., Novak I., Harper J.W., Behrends C., Dikic I. Rab GTPase-activating proteins in autophagy: regulation of endocytic and autophagy pathways by direct binding to human ATG8 modifiers. Mol. Cell. Biol. 2012, 32:1733-1744.
38. Puri C., Renna M., Bento C.F., Moreau K., Rubinsztein D.C. Diverse autophagosome membrane sources coalesce in recycling endosomes. Cell 2013, 154:1285-1299.
39. Reggiori F., Wang C.W., Nair U., Shintani T., Abeliovich H., Klionsky D.J. Early stages of the secretory pathway, but not endosomes, are required for Cvt vesicle and autophagosome assembly in Saccharomyces cerevisiae. Mol. Biol. Cell 2004, 15:2189-2204.
40. Tan D., Cai Y., Wang J., Zhang J., Menon S., Chou H.T., Ferro-Novick S., Reinisch K.M., Walz T. The EM structure of the TRAPPIII complex leads to the identification of a requirement for COPII vesicles on the macroautophagy pathway. Proc. Natl. Acad. Sci. USA 2013, 110:19432-19437.
41. Tsukada M., Ohsumi Y. Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett. 1993, 333:169-174.
42. Voeltz G.K., Prinz W.A., Shibata Y., Rist J.M., Rapoport T.A. A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell 2006, 124:573-586.
43. Yamamoto H., Kakuta S., Watanabe T.M., Kitamura A., Sekito T., Kondo-Kakuta C., Ichikawa R., Kinjo M., Ohsumi Y. Atg9 vesicles are an important membrane source during early steps of autophagosome formation. J. Cell Biol. 2012, 198:219-233.
44. Ylä-Anttila P., Vihinen H., Jokitalo E., Eskelinen E.L. 3D tomography reveals connections between the phagophore and endoplasmic reticulum. Autophagy 2009, 5:1180-1185.