A trs20 mutation that mimics an SEDT-causing mutation blocks selective and non-selective autophagy: A model for TRAPP III organization

Traffic

Volumn 14, Issue 10, 2013, Pages 1091-1104

  Brunet, Stephanie ^a   Shahrzad, Nassim ^a   Saint Dic, Djenann ^a   Dutczak, Hartley ^a   Sacher, Michael ^a,b  

^a Gina Cody School of Engineering and Computer Science   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

Atg9p; Autophagy; Bet3p; SEDT; TRAPP; Trs20p; Trs85p

Indexed keywords

ADAPTOR PROTEIN; ATG9P PROTEIN; BET3P PROTEIN; CARBOXYPEPTIDASE C; CORE PROTEIN; SYNTAXIN; SYNTAXIN 5; TRAPP I PROTEIN; TRAPP II PROTEIN; TRAPP III PROTEIN; TRAPP PROTEIN; TRS130P PROTEIN; TRS20 PROTEIN; TRS20P PROTEIN; TRS85P PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; AUTOPHAGY; CELL VACUOLE; CONTROLLED STUDY; CYTOSOL; ENDOCYTOSIS; GEL PERMEATION CHROMATOGRAPHY; HUMAN; HUMAN CELL; IN VITRO STUDY; MISSENSE MUTATION; MOLECULAR SIZE; NON SELECTIVE AUTOPHAGY; NONHUMAN; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; SECRETORY PATHWAY; SELECTIVE AUTOPHAGY; SIGNAL TRANSDUCTION; SPONDYLOEPIPHYSEAL DYSPLASIA;

ATG9P; AUTOPHAGY; BET3P; SEDT; TRAPP; TRS20P; TRS85P;

AUTOPHAGY; CELL LINE; CELL LINE, TUMOR; CYTOSOL; ENDOCYTOSIS; FUNGAL PROTEINS; GENETIC DISEASES, X-LINKED; HEK293 CELLS; HELA CELLS; HUMANS; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; MUTATION, MISSENSE; OSTEOCHONDRODYSPLASIAS; PROTEIN BINDING; PROTEIN TRANSPORT; QA-SNARE PROTEINS; SNARE PROTEINS; TRANSCRIPTION FACTORS; VACUOLES; VESICULAR TRANSPORT PROTEINS; YEASTS;

EID: 84883652935     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/tra.12095     Document Type: Article

References (56)

1. Aridor M, Hannan LA. Traffic jam: a compendium of human diseases that affect intracellular transport processes. Traffic 2000;1:836-851.
2. Aridor M, Hannan LA. Traffic jams II: an update of diseases of intracellular transport. Traffic 2002;3:781-790.
3. Cai H, Reinisch K, Ferro-Novick S. Coats, tethers, Rabs, and SNAREs work together to mediate the intracellular destination of a transport vesicle. Dev Cell 2007;12:671-682.
4. Cai H, Yu S, Menon S, Cai Y, Lazarova D, Fu C, Reinisch K, Hay JC, Ferro-Novick S. TRAPPI tethers COPII vesicles by binding the coat subunit Sec23. Nature 2007;445:941-944.
5. Lord C, Bhandari D, Menon S, Ghassemian M, Nycz D, Hay J, Ghosh P, Ferro-Novick S. Sequential interactions with Sec23 control the direction of vesicle traffic. Nature 2011;473:181-186.
6. Jones S, Newman C, Liu F, Segev N. The TRAPP complex is a nucleotide exchanger for Ypt1 and Ypt31/32. Mol Biol Cell 2000;11:4403-4411.
7. Wang W, Sacher M, Ferro-Novick S. TRAPP stimulates guanine nucleotide exchange on Ypt1p. J Cell Biol 2000;151:289-296.
8. Rossi G, Kolstad K, Stone S, Palluault F, Ferro-Novick S. BET3 encodes a novel hydrophilic protein that acts in conjunction with yeast SNAREs. Mol Biol Cell 1995;6:1769-1780.
9. Sacher M, Barrowman J, Wang W, Horecka J, Zhang Y, Pypaert M, Ferro-Novick S. TRAPP I implicated in the specificity of tethering in ER-to-Golgi transport. Mol Cell 2001;7:433-442.
10. Lynch-Day MA, Bhandari D, Menon S, Huang J, Cai H, Bartholomew CR, Brumell JH, Ferro-Novick S, Klionsky DJ. Trs85 directs a Ypt1 GEF, TRAPPIII, to the phagophore to promote autophagy. Proc Natl Acad Sci U S A 2010;107:7811-7816.
11. Montpetit B, Conibear E. Identification of the novel TRAPP associated protein Tca17. Traffic 2009;10:713-723.
12. Choi C, Davey M, Schluter C, Pandher P, Fang Y, Foster LJ, Conibear E. Organization and assembly of the TRAPPII complex. Traffic 2011;12:715-725.
13. Cai H, Zhang Y, Pypaert M, Walker L, Ferro-Novick S. Mutants in trs120 disrupt traffic from the early endosome to the late Golgi. J Cell Biol 2005;171:823-833.
14. Zou S, Chen Y, Liu Y, Segev N, Yu S, Liu Y, Min G, Ye M, Zeng Y, Zhu X, Hong B, Bjorn LO, Liang Y, Li S, Xie Z. Trs130 participates in autophagy through GTPases Ypt31/32 in Saccharomyces cerevisiae. Traffic 2013;14:233-246.
15. Meiling-Wesse K, Epple UD, Krick R, Barth H, Appelles A, Voss C, Eskelinen EL, Thumm M. Trs85 (Gsg1), a component of the TRAPP complexes, is required for the organization of the preautophagosomal structure during selective autophagy via the Cvt pathway. J Biol Chem 2005;280:33669-33678.
16. Lipatova Z, Belogortseva N, Zhang XQ, Kim J, Taussig D, Segev N. Regulation of selective autophagy onset by a Ypt/Rab GTPase module. Proc Natl Acad Sci U S A 2012;109:6981-6986.
17. Zou S, Liu Y, Zhang XQ, Chen Y, Ye M, Zhu X, Yang S, Lipatova Z, Liang Y, Segev N. Modular TRAPP complexes regulate intracellular protein trafficking through multiple Ypt/Rab GTPases in Saccharomyces cerevisiae. Genetics 2012;191:451-460.
18. Bacon RA, Salminen A, Ruohola H, Novick P, Ferro-Novick S. The GTP-binding protein Ypt1 is required for transport in vitro: the Golgi apparatus is defective in ypt1 mutants. J Cell Biol 1989;109:1015-1022.
19. Jedd G, Richardson C, Litt R, Segev N. The Ypt1 GTPase is essential for the first two steps of the yeast secretory pathway. J Cell Biol 1995;131:583-590.
20. Sclafani A, Chen S, Rivera-Molina F, Reinisch K, Novick P, Ferro-Novick S. Establishing a role for the GTPase Ypt1p at the late Golgi. Traffic 2010;11:520-532.
21. Segev N, Mulholland J, Botstein D. The yeast GTP-binding YPT1 protein and a mammalian counterpart are associated with the secretion machinery. Cell 1988;52:915-924.
22. Shaw MA, Brunetti-Pierri N, Kadasi L, Kovacova V, Van ML, De BD, Salerno M, Gecz J. Identification of three novel SEDL mutations, including mutation in the rare, non-canonical splice site of exon 4. Clin Genet 2003;64:235-242.
23. Tiller GE, Hannig VL, Dozier D, Carrel L, Trevarthen KC, Wilcox WR, Mundlos S, Haines JL, Gedeon AK, Gecz J. A recurrent RNA-splicing mutation in the SEDL gene causes X-linked spondyloepiphyseal dysplasia tarda. Am J Hum Genet 2001;68:1398-1407.
24. Venditti R, Scanu T, Santoro M, Di TG, Spaar A, Gaibisso R, Beznoussenko GV, Mironov AA, Mironov A, Jr., Zelante L, Piemontese MR, Notarangelo A, Malhotra V, Vertel BM, Wilson C. Sedlin controls the ER export of procollagen by regulating the Sar1 cycle. Science 2012;337:1668-1672.
25. Scrivens PJ, Shahrzad N, Moores A, Morin A, Brunet S, Sacher M. TRAPPC2L is a novel, highly conserved TRAPP-interacting protein. Traffic 2009;10:724-736.
26. Gecz J, Shaw MA, Bellon JR, de Barros LM. Human wild-type SEDL protein functionally complements yeast Trs20p but some naturally occurring SEDL mutants do not. Gene 2003;320:137-144.
27. Gonzalez LC Jr, Weis WI, Scheller RH. A novel snare N-terminal domain revealed by the crystal structure of Sec22b. J Biol Chem 2001;276:24203-24211.
28. Jang SB, Kim YG, Cho YS, Suh PG, Kim KH, Oh BH. Crystal structure of SEDL and its implications for a genetic disease spondyloepiphyseal dysplasia tarda. J Biol Chem 2002;277:49863-49869.
29. Tochio H, Tsui MM, Banfield DK, Zhang M. An autoinhibitory mechanism for nonsyntaxin SNARE proteins revealed by the structure of Ykt6p. Science 2001;293:698-702.
30. Williams AL, Ehm S, Jacobson NC, Xu D, Hay JC. rsly1 binding to syntaxin 5 is required for endoplasmic reticulum-to-Golgi transport but does not promote SNARE motif accessibility. Mol Biol Cell 2004;15:162-175.
31. Stevens T, Esmon B, Schekman R. Early stages in the yeast secretory pathway are required for transport of carboxypeptidase Y to the vacuole. Cell 1982;30:439-448.
32. Ben-Aroya S, Coombes C, Kwok T, O'Donnell KA, Boeke JD, Hieter P. Toward a comprehensive temperature-sensitive mutant repository of the essential genes of Saccharomyces cerevisiae. Mol Cell 2008;30:248-258.
33. Cai Y, Chin HF, Lazarova D, Menon S, Fu C, Cai H, Sclafani A, Rodgers DW, De La Cruz EM, Ferro-Novick S, Reinisch KM. The structural basis for activation of the Rab Ypt1p by the TRAPP membrane-tethering complexes. Cell 2008;133:1202-1213.
34. Kim YG, Raunser S, Munger C, Wagner J, Song YL, Cygler M, Walz T, Oh BH, Sacher M. The architecture of the multisubunit TRAPP I complex suggests a model for vesicle tethering. Cell 2006;127:817-830.
35. Zong M, Wu XG, Chan CW, Choi MY, Chan HC, Tanner JA, Yu S. The adaptor function of TRAPPC2 in mammalian TRAPPs explains TRAPPC2-associated SEDT and TRAPPC9-associated congenital intellectual disability. PLoS One 2011;6:e23350.
36. Valdivia RH, Baggott D, Chuang JS, Schekman RW. The yeast clathrin adaptor protein complex 1 is required for the efficient retention of a subset of late Golgi membrane proteins. Dev Cell 2002;2:283-294.
37. Brunet S, Noueihed B, Shahrzad N, Saint-Dic D, Hasaj B, Guan TL, Moores A, Barlowe C, Sacher M. The SMS domain of Trs23p is responsible for the in vitro appearance of the TRAPP I complex in Saccharomyces cerevisiae. Cell Logist 2012;2:28-42.
38. Scott SV, Hefner-Gravink A, Morano KA, Noda T, Ohsumi Y, Klionsky DJ. Cytoplasm-to-vacuole targeting and autophagy employ the same machinery to deliver proteins to the yeast vacuole. Proc Natl Acad Sci U S A 1996;93:12304-12308.
39. 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.
40. Sekito T, Kawamata T, Ichikawa R, Suzuki K, Ohsumi Y. Atg17 recruits Atg9 to organize the pre-autophagosomal structure. Genes Cells 2009;14:525-538.
41. Kim YG, Sohn EJ, Seo J, Lee KJ, Lee HS, Hwang I, Whiteway M, Sacher M. Crystal structure of bet3 reveals a novel mechanism for Golgi localization of tethering factor TRAPP. Nat Struct Mol Biol 2005;12:38-45.
42. Turnbull AP, Kummel D, Prinz B, Holz C, Schultchen J, Lang C, Niesen FH, Hofmann KP, Delbruck H, Behlke J, Muller EC, Jarosch E, Sommer T, Heinemann U. Structure of palmitoylated BET3: insights into TRAPP complex assembly and membrane localization. EMBO J 2005;24:875-884.
43. Kummel D, Heinemann U, Veit M. Unique self-palmitoylation activity of the transport protein particle component Bet3: a mechanism required for protein stability. Proc Natl Acad Sci U S A 2006;103:12701-12706.
44. 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.
45. Boyd C, Hughes T, Pypaert M, Novick P. Vesicles carry most exocyst subunits to exocytic sites marked by the remaining two subunits, Sec3p and Exo70p. J Cell Biol 2004;167:889-901.
46. Cheong H, Yorimitsu T, Reggiori F, Legakis JE, Wang CW, Klionsky DJ. Atg17 regulates the magnitude of the autophagic response. Mol Biol Cell 2005;16:3438-3453.
47. Munro S. The Golgi apparatus: defining the identity of Golgi membranes. Curr Opin Cell Biol 2005;17:395-401.
48. Roskoski R Jr. Protein prenylation: a pivotal posttranslational process. Biochem Biophys Res Commun 2003;303:1-7.
49. Kummel D, Walter J, Heck M, Heinemann U, Veit M. Characterization of the self-palmitoylation activity of the transport protein particle component Bet3. Cell Mol Life Sci 2010;67:2653-2664.
50. Yip CK, Berscheminski J, Walz T. Molecular architecture of the TRAPPII complex and implications for vesicle tethering. Nat Struct Mol Biol 2010;17:1298-1304.
51. Tai G, Lu L, Wang TL, Tang BL, Goud B, Johannes L, Hong W. Participation of the syntaxin 5/Ykt6/GS28/GS15 SNARE complex in transport from the early/recycling endosome to the trans-Golgi network. Mol Biol Cell 2004;15:4011-4022.
52. Xu Y, Martin S, James DE, Hong W. GS15 forms a SNARE complex with syntaxin 5, GS28, and Ykt6 and is implicated in traffic in the early cisternae of the Golgi apparatus. Mol Biol Cell 2002;13:3493-3507.
53. Scrivens PJ, Noueihed B, Shahrzad N, Hul S, Brunet S, Sacher M. C4orf41 and TTC-15 are mammalian TRAPP components with a role at an early stage in ER-to-Golgi trafficking. Mol Biol Cell 2011;22:2083-2093.
54. Klionsky DJ, Cueva R, Yaver DS. Aminopeptidase I of Saccharomyces cerevisiae is localized to the vacuole independent of the secretory pathway. J Cell Biol 1992;119:287-299.
55. Hou H, Subramanian K, LaGrassa TJ, Markgraf D, Dietrich LE, Urban J, Decker N, Ungermann C. The DHHC protein Pfa3 affects vacuole-associated palmitoylation of the fusion factor Vac8. Proc Natl Acad Sci U S A 2005;102:17366-17371.
56. Wan J, Roth AF, Bailey AO, Davis NG. Palmitoylated proteins: purification and identification. Nat Protoc 2007;2:1573-1584.