Atg27 tyrosine sorting motif is important for its trafficking and Atg9 localization

Traffic

Volumn 16, Issue 4, 2015, Pages 365-378

  Segarra, Verónica A ^a,b   Boettner, Douglas R ^a   Lemmon, Sandra K ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b ROLLINS COLLEGE   (United States)

Author keywords

AP 3; Atg27; Atg9; Autophagy; Cytoplasm to vacuole transport; Endosome; Preautophagosomal structure; Trans Golgi network; Tyrosine sorting motif; Vacuole

Indexed keywords

MEMBRANE PROTEIN; PROTEIN AP 3; PROTEIN ATG27; PROTEIN ATG9; TYROSINE; UNCLASSIFIED DRUG; ATG27 PROTEIN, S CEREVISIAE; ATG9 PROTEIN, S CEREVISIAE; CARRIER PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; VESICULAR TRANSPORT PROTEIN;

ARTICLE; AUTOPHAGY; CONTROLLED STUDY; ENDOSOME; MULTIVESICULAR BODY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; SIGNAL TRANSDUCTION; TONOPLAST; TRANS GOLGI NETWORK; TRANSPORT VESICLE; CELL VACUOLE; GOLGI COMPLEX; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE;

AMINO ACID MOTIFS; AUTOPHAGY; CARRIER PROTEINS; GOLGI APPARATUS; MEMBRANE PROTEINS; MULTIVESICULAR BODIES; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TYROSINE; VACUOLES; VESICULAR TRANSPORT PROTEINS;

EID: 84926076454     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/tra.12253     Document Type: Article

References (49)

1. Mizushima N, Yoshimori T, Ohsumi Y. The role of Atg proteins in autophagosome formation. Annu Rev Cell Dev Biol 2011;27:107-132.
2. Xie Z, Klionsky DJ. Autophagosome formation: core machinery and adaptations. Nat Cell Biol 2007;9:1102-1109.
3. Reggiori F, Klionsky DJ. Autophagic processes in yeast: mechanism, machinery and regulation. Genetics 2013;194:341-361.
4. Lamb CA, Yoshimori T, Tooze SA. The autophagosome: origins unknown, biogenesis complex. Nat Rev Mol Cell Biol 2013;14:759-774.
5. Yamamoto H, Kakuta S, Watanabe TM, 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.
6. Yen WL, Klionsky DJ. Atg27 is a second transmembrane cycling protein. Autophagy 2007;3:254-256.
7. Webber JL, Tooze SA. New insights into the function of Atg9. FEBS Lett 2010;584:1319-1326.
8. 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;190:1005-1022.
9. Reggiori F, Tooze SA. Autophagy regulation through Atg9 traffic. J Cell Biol 2012;198:151-153.
10. Shirahama-Noda K, Kira S, Yoshimori T, Noda T. TRAPPIII is responsible for vesicular transport from early endosomes to Golgi, facilitating Atg9 cycling in autophagy. J Cell Sci 2013;126:4963-4973.
11. Ohashi Y, Munro S. Membrane delivery to the yeast autophagosome from the Golgi-endosomal system. Mol Biol Cell 2010;21:3998-4008.
12. Orsi A, Razi M, Dooley HC, Robinson D, Weston AE, Collinson LM, Tooze SA. Dynamic and transient interactions of Atg9 with autophagosomes, but not membrane integration, are required for autophagy. Mol Biol Cell 2012;23:1860-1873.
13. Young AR, Chan EY, Hu XW, Kochl R, Crawshaw SG, High S, Hailey DW, Lippincott-Schwartz J, Tooze SA. Starvation and ULK1-dependent cycling of mammalian Atg9 between the TGN and endosomes. J Cell Sci 2006;119:3888-3900.
14. Puri C, Renna M, Bento CF, Moreau K, Rubinsztein DC. Diverse autophagosome membrane sources coalesce in recycling endosomes. Cell 2013;154:1285-1299.
15. Yen WL, Legakis JE, Nair U, Klionsky DJ. Atg27 is required for autophagy-dependent cycling of Atg9. Mol Biol Cell 2007;18:581-593.
16. Legakis JE, Yen WL, Klionsky DJ. A cycling protein complex required for selective autophagy. Autophagy 2007;3:422-432.
17. Kakuta S, Yamamoto H, Negishi L, Kondo-Kakuta C, Hayashi N, Ohsumi Y. Atg9 vesicles recruit vesicle-tethering proteins Trs85 and Ypt1 to the autophagosome formation site. J Biol Chem 2012;287:44261-44269.
18. Longtine MS, McKenzie A, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P, Pringle JR. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 1998;14:953-961.
19. Ayscough KR, Stryker J, Pokala N, Sanders M, Crews P, Drubin DG. High rates of actin filament turnover in budding yeast and roles for actin in establishment and maintenance of cell polarity revealed using the actin inhibitor latrunculin-A. J Cell Biol 1997;137:399-416.
20. Burston HE, Maldonado-Baez L, Davey M, Montpetit B, Schluter C, Wendland B, Conibear E. Regulators of yeast endocytosis identified by systematic quantitative analysis. J Cell Biol 2009;185:1097-1110.
21. Bowers K, Stevens TH. Protein transport from the late Golgi to the vacuole in the yeast Saccharomyces cerevisiae. Biochim Biophys Acta 2005;1744:438-454.
22. Stepp JD, Huang K, Lemmon SK. The yeast adaptor protein complex, AP-3, is essential for the efficient delivery of alkaline phosphatase by the alternate pathway to the vacuole. J Cell Biol 1997;139:1761-1774.
23. Cowles CR, Odorizzi G, Payne GS, Emr SD. The AP-3 adaptor complex is essential for cargo-selective transport to the yeast vacuole. Cell 1997;91:109-118.
24. Raymond CK, Howald-Stevenson I, Vater CA, Stevens TH. Morphological classification of the yeast vacuolar protein sorting mutants: evidence for a prevacuolar compartment in class E vps mutants. Mol Biol Cell 1992;3:1389-1402.
25. Bonifacino JS, Traub LM. Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu Rev Biochem 2003;72:395-447.
26. Rossanese OW, Reinke CA, Bevis BJ, Hammond AT, Sears IB, O'Connor J, Glick BS. A role for actin, Cdc1p, and Myo2p in the inheritance of late Golgi elements in Saccharomyces cerevisiae. J Cell Biol 2001;153:47-62.
27. Franzusoff A, Redding K, Crosby J, Fuller RS, Schekman R. Localization of components involved in protein transport and processing through the yeast Golgi apparatus. J Cell Biol 1991;112:27-37.
28. Holthuis JC, Nichols BJ, Dhruvakumar S, Pelham HR. Two syntaxin homologues in the TGN/endosomal system of yeast. EMBO J 1998;17:113-126.
29. Abeliovich H, Grote E, Novick P, Ferro-Novick S. Tlg2p, a yeast syntaxin homolog that resides on the Golgi and endocytic structures. J Biol Chem 1998;273:11719-11727.
30. Seron K, Tieaho V, Prescianotto-Baschong C, Aust T, Blondel MO, Guillaud P, Devilliers G, Rossanese OW, Glick BS, Riezman H, Keranen S, Haguenauer-Tsapis R. A yeast t-SNARE involved in endocytosis. Mol Biol Cell 1998;9:2873-2889.
31. Lewis MJ, Nichols BJ, Prescianotto-Baschong C, Riezman H, Pelham HR. Specific retrieval of the exocytic SNARE Snc1p from early yeast endosomes. Mol Biol Cell 2000;11:23-38.
32. Stromhaug PE, Reggiori F, Guan J, Wang CW, Klionsky DJ. Atg21 is a phosphoinositide binding protein required for efficient lipidation and localization of Atg8 during uptake of aminopeptidase I by selective autophagy. Mol Biol Cell 2004;15:3553-3566.
33. Legakis JE, Klionsky DJ. Analysis of autophagosome membrane cycling by fluorescence microscopy. Methods Mol Biol 2008;445:135-145.
34. Klionsky DJ, Cuervo AM, Seglen PO. Methods for monitoring autophagy from yeast to human. Autophagy 2007;3:181-206.
35. Huang WP, Scott SV, Kim J, Klionsky DJ. The itinerary of a vesicle component, Aut7p/Cvt5p, terminates in the yeast vacuole via the autophagy/Cvt pathways. J Biol Chem 2000;275:5845-5851.
36. Shintani T, Klionsky DJ. Cargo proteins facilitate the formation of transport vesicles in the cytoplasm to vacuole targeting pathway. J Biol Chem 2004;279:29889-29894.
37. Wiederhold E, Gandhi T, Permentier HP, Breitling R, Poolman B, Slotboom DJ. The yeast vacuolar membrane proteome. Mol Cell Proteomics 2009;8:380-392.
38. Yen WL, Shintani T, Nair U, Cao Y, Richardson BC, Li Z, Hughson FM, Baba M, Klionsky DJ. The conserved oligomeric Golgi complex is involved in double-membrane vesicle formation during autophagy. J Cell Biol 2010;188:101-114.
39. Muthusamy BP, Natarajan P, Zhou X, Graham TR. Linking phospholipid flippases to vesicle-mediated protein transport. Biochim Biophys Acta 2009;1791:612-619.
40. Guo Y, Chang C, Huang R, Liu B, Bao L, Liu W. AP1 is essential for generation of autophagosomes from trans-Golgi network. J Cell Sci 2012;125:1706-1715.
41. Odorizzi G, Katzmann DJ, Babst M, Audhya A, Emr SD. Bro1 is an endosome-associated protein that functions in the MVB pathway in Saccharomyces cerevisiae. J Cell Sci 2003;116:1893-1903.
42. Castonguay AC, Olson LJ, Dahms NM. Mannose 6-phosphate receptor homology (MRH) domain-containing lectins in the secretory pathway. Biochim Biophys Acta 2011;1810:815-826.
43. Kelley LA, Sternberg MJ. Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 2009;4:363-371.
44. Guthrie C, Fink GR. Guide to yeast genetics and molecular biology. Methods Enzymol 1991;194:1-863.
45. Shintani T, Huang WP, Stromhaug PE, Klionsky DJ. Mechanism of cargo selection in the cytoplasm to vacuole targeting pathway. Dev Cell 2002;3:825-837.
46. Ma J, Bharucha N, Dobry CJ, Frisch RL, Lawson S, Kumar A. Localization of autophagy-related proteins in yeast using a versatile plasmid-based resource of fluorescent protein fusions. Autophagy 2008;4:792-800.
47. Ayscough K. Use of latrunculin-A, an actin monomer-binding drug. Methods Enzymol 1998;298:18-25.
48. Huang KM, D'Hondt K, Riezman H, Lemmon SK. Clathrin functions in the absence of heterotetrameric adaptors and AP180-related proteins in yeast. EMBO J 1999;18:3897-3908.
49. Stepp JD, Pellicena-Palle A, Hamilton S, Kirchhausen T, Lemmon SK. A late Golgi sorting function for Saccharomyces cerevisiae Apm1p, but not for Apm2p, a second yeast clathrin AP medium chain-related protein. Mol Biol Cell 1995;6:41-58.