p115-SNARE Interactions: A Dynamic Cycle of p115 Binding Monomeric SNARE Motifs and Releasing Assembled Bundles

Traffic

Volumn 16, Issue 2, 2015, Pages 148-171

  Wang, Ting ^a   Grabski, Robert ^b   Sztul, Elizabeth ^b   Hay, Jesse C ^a  

^a UNIVERSITY OF MONTANA   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

Bet1; Endoplasmic reticulum to Golgi transport; Membrane fusion; Membrane tethers; P115; Sec22; Secretion; SNARE; Syntaxin 5; Vesicle transport

Indexed keywords

P115 PROTEIN; PROTEIN; SNARE PROTEIN; UNCLASSIFIED DRUG; BET1 PROTEIN, RAT; PROTEIN BINDING; QC SNARE PROTEIN; SEC22 HOMOLOG PROTEIN, RAT; SYNAPTOBREVIN; VESICULAR TRANSPORT FACTOR P115; VESICULAR TRANSPORT PROTEIN;

ANIMAL CELL; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GEL FILTRATION; LIVER CYTOSOL; MEMBRANE FUSION; MEMBRANE VESICLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN TRANSPORT; RAT; ANIMAL; BINDING SITE; CHEMISTRY; CHO CELL LINE; COP-COATED VESICLE; CRICETULUS; HAMSTER; METABOLISM; PROTEIN MULTIMERIZATION;

ANIMALS; BINDING SITES; CHO CELLS; COP-COATED VESICLES; CRICETINAE; CRICETULUS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN TRANSPORT; QC-SNARE PROTEINS; R-SNARE PROTEINS; RATS; VESICULAR TRANSPORT PROTEINS;

EID: 84921438038     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/tra.12242     Document Type: Article

References (77)

1. Bannykh SI, Rowe T, Balch WE. The organization of endoplasmic reticulum export complexes. J Cell Biol 1996;135:19-35.
2. Scales SJ, Pepperkok R, Kreis TE. Visualization of ER-to-Golgi transport in living cells reveals a sequential mode of action for COPII and COPI. Cell 1997;90:1137-1148.
3. Ungar D, Hughson FM. SNARE protein structure and function. Annu Rev Cell Dev Biol 2003;19:493-517.
4. Weber T, Zemelman BV, McNew JA, Westermann B, Gmachl M, Parlati F, Sollner TH, Rothman JE. SNAREpins: minimal machinery for membrane fusion. Cell 1998;92:759-772.
5. Waters MG, Pfeffer SR. Membrane tethering in intracellular transport. Curr Opin Cell Biol 1999;11:453-459.
6. Linstedt AD, Hauri HP. Giantin, a novel conserved Golgi membrane protein containing a cytoplasmic domain of at least 350 kDa. Mol Biol Cell 1993;4:679-693.
7. Mu FT, Callaghan JM, Steele-Mortimer O, Stenmark H, Parton RG, Campbell PL, McCluskey J, Yeo JP, Tock EP, Toh BH. EEA1, an early endosome-associated protein. EEA1 is a conserved alpha-helical peripheral membrane protein flanked by cysteine "fingers" and contains a calmodulin-binding IQ motif. J Biol Chem 1995;270:13503-13511.
8. Nakamura N, Rabouille C, Watson R, Nilsson T, Hui N, Slusarewicz P, Kreis TE, Warren G. Characterization of a cis-Golgi matrix protein, GM130. J Cell Biol 1995;131:1715-1726.
9. TerBush DR, Maurice T, Roth D, Novick P. The exocyst is a multiprotein complex required for exocytosis in Saccharomyces cerevisiae. EMBO J 1996;15:6483-6494.
10. Sacher M, Jiang Y, Barrowman J, Scarpa A, Burston J, Zhang L, Schieltz D, Yates JR III, Abeliovich H, Ferro-Novick S. TRAPP, a highly conserved novel complex on the cis-Golgi that mediates vesicle docking and fusion. EMBO J 1998;17:2494-2503.
11. Conibear E, Stevens TH. Vps52p, Vps53p, and Vps54p form a novel multisubunit complex required for protein sorting at the yeast late Golgi. Mol Biol Cell 2000;11:305-323.
12. Seals DF, Eitzen G, Margolis N, Wickner WT, Price A. A Ypt/Rab effector complex containing the Sec1 homolog Vps33p is required for homotypic vacuole fusion. Proc Natl Acad Sci U S A 2000;97:9402-9407.
13. Ungar D, Oka T, Brittle EE, Vasile E, Lupashin VV, Chatterton JE, Heuser JE, Krieger M, Waters MG. Characterization of a mammalian Golgi-localized protein complex, COG, that is required for normal Golgi morphology and function. J Cell Biol 2002;157:405-415.
14. Kraynack BA, Chan A, Rosenthal E, Essid M, Umansky B, Waters MG, Schmitt HD. Dsl1p, Tip20p, and the novel Dsl3(Sec39) protein are required for the stability of the Q/t-SNARE complex at the endoplasmic reticulum in yeast. Mol Biol Cell 2005;16:3963-3977.
15. Barr FA, Puype M, Vandekerckhove J, Warren G. GRASP65, a protein involved in the stacking of Golgi cisternae. Cell 1997;91:253-262.
16. Nelson DS, Alvarez C, Gao YS, Garcia-Mata R, Fialkowski E, Sztul E. The membrane transport factor TAP/p115 cycles between the Golgi and earlier secretory compartments and contains distinct domains required for its localization and function. J Cell Biol 1998;143:319-331.
17. Shorter J, Warren G. A role for the vesicle tethering protein, p115, in the post-mitotic stacking of reassembling Golgi cisternae in a cell-free system. J Cell Biol 1999;146:57-70.
18. Zolov SN, Lupashin VV. Cog3p depletion blocks vesicle-mediated Golgi retrograde trafficking in HeLa cells. J Cell Biol 2005;168:747-759.
19. Orci L, Perrelet A, Rothman JE. Vesicles on strings: morphological evidence for processive transport within the Golgi stack. Proc Natl Acad Sci U S A 1998;95:2279-2283.
20. Walter DM, Paul KS, Waters MG. Purification and characterization of a novel 13S hetero-oligomeric protein complex that stimulates in vitro Golgi transport. J Biol Chem 1998;273:29565-29576.
21. Ren Y, Yip CK, Tripathi A, Huie D, Jeffrey PD, Walz T, Hughson FM. A structure-based mechanism for vesicle capture by the multisubunit tethering complex Dsl1. Cell 2009;139:1119-1129.
22. Lupashin V, Sztul E. Golgi tethering factors. Biochim Biophys Acta 2005;1744:325-339.
23. Waters MG, Clary DO, Rothman JE. A novel 115-kD peripheral membrane protein is required for intercisternal transport in the Golgi stack. J Cell Biol 1992;118:1015-1026.
24. Nakajima H, Hirata A, Ogawa Y, Yonehara T, Yoda K, Yamasaki M. A cytoskeleton-related gene, uso1, is required for intracellular protein transport in Saccharomyces cerevisiae. J Cell Biol 1991;113:245-260.
25. Barroso M, Nelson DS, Sztul E. Transcytosis-associated protein (TAP)/p115 is a general fusion factor required for binding of vesicles to acceptor membranes. Proc Natl Acad Sci U S A 1995;92:527-531.
26. Sapperstein SK, Lupashin VV, Schmitt HD, Waters MG. Assembly of the ER to Golgi SNARE complex requires Uso1p. J Cell Biol 1996;132:755-767.
27. Barlowe C. Coupled ER to Golgi transport reconstituted with purified cytosolic proteins. J Cell Biol 1997;139:1097-1108.
28. Cao X, Ballew N, Barlowe C. Initial docking of ER-derived vesicles requires Uso1p and Ypt1p but is independent of SNARE proteins. EMBO J 1998;17:2156-2165.
29. Alvarez C, Fujita H, Hubbard A, Sztul E. ER to Golgi transport: requirement for p115 at a pre-Golgi VTC stage. J Cell Biol 1999;147:1205-1222.
30. Allan BB, Moyer BD, Balch WE. Rab1 recruitment of p115 into a cis-SNARE complex: programming budding COPII vesicles for fusion. Science 2000;289:444-448.
31. Brandon E, Szul T, Alvarez C, Grabski R, Benjamin R, Kawai R, Sztul E. On and off membrane dynamics of the endoplasmic reticulum-Golgi tethering factor p115 in vivo. Mol Biol Cell 2006;17:2996-3008.
32. Lupashin VV, Hamamoto S, Schekman RW. Biochemical requirements for the targeting and fusion of ER-derived transport vesicles with purified yeast Golgi membranes. J Cell Biol 1996;132:277-289.
33. Gmachl MJ, Wimmer C. Sequential involvement of p115, SNAREs, and Rab proteins in intra-Golgi protein transport. J Biol Chem 2001;276:18178-18184.
34. Nakamura N, Lowe M, Levine TP, Rabouille C, Warren G. The vesicle docking protein p115 binds GM130, a cis-Golgi matrix protein, in a mitotically regulated manner. Cell 1997;89:445-455.
35. Sohda M, Misumi Y, Yano A, Takami N, Ikehara Y. Phosphorylation of the vesicle docking protein p115 regulates its association with the Golgi membrane. J Biol Chem 1998;273:5385-5388.
36. Dirac-Svejstrup AB, Shorter J, Waters MG, Warren G. Phosphorylation of the vesicle-tethering protein p115 by a casein kinase II-like enzyme is required for Golgi reassembly from isolated mitotic fragments. J Cell Biol 2000;150:475-488.
37. 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.
38. Wuestehube LJ, Duden R, Eun A, Hamamoto S, Korn P, Ram R, Schekman R. New mutants of Saccharomyces cerevisiae affected in the transport of proteins from the endoplasmic reticulum to the Golgi complex. Genetics 1996;142:393-406.
39. VanRheenen SM, Cao X, Lupashin VV, Barlowe C, Waters MG. Sec35p, a novel peripheral membrane protein, is required for ER to Golgi vesicle docking. J Cell Biol 1998;141:1107-1119.
40. Sapperstein SK, Walter DM, Grosvenor AR, Heuser JE, Waters MG. p115 is a general vesicular transport factor related to the yeast endoplasmic reticulum to Golgi transport factor Uso1p. Proc Natl Acad Sci U S A 1995;92:522-526.
41. Yamakawa H, Seog DH, Yoda K, Yamasaki M, Wakabayashi T. Uso1 protein is a dimer with two globular heads and a long coiled-coil tail. J Struct Biol 1996;116:356-365.
42. An Y, Chen CY, Moyer B, Rotkiewicz P, Elsliger MA, Godzik A, Wilson IA, Balch WE. Structural and functional analysis of the globular head domain of p115 provides insight into membrane tethering. J Mol Biol 2009;391:26-41.
43. Striegl H, Roske Y, Kummel D, Heinemann U. Unusual armadillo fold in the human general vesicular transport factor p115. PLoS One 2009;4:e4656.
44. Beard M, Satoh A, Shorter J, Warren G. A cryptic Rab1-binding site in the p115 tethering protein. J Biol Chem 2005;280:25840-25848.
45. Sonnichsen B, Lowe M, Levine T, Jamsa E, Dirac-Svejstrup B, Warren G. A role for giantin in docking COPI vesicles to Golgi membranes. J Cell Biol 1998;140:1013-1021.
46. Lesa GM, Seemann J, Shorter J, Vandekerckhove J, Warren G. The amino-terminal domain of the Golgi protein giantin interacts directly with the vesicle-tethering protein p115. J Biol Chem 2000;275:2831-2836.
47. Linstedt AD, Jesch SA, Mehta A, Lee TH, Garcia-Mata R, Nelson DS, Sztul E. Binding relationships of membrane tethering components. The giantin N terminus and the GM130 N terminus compete for binding to the p115 C terminus. J Biol Chem 2000;275:10196-10201.
48. Puthenveedu MA, Linstedt AD. Evidence that Golgi structure depends on a p115 activity that is independent of the vesicle tether components giantin and GM130. J Cell Biol 2001;155:227-238.
49. Satoh A, Warren G. In situ cleavage of the acidic domain from the p115 tether inhibits exocytic transport. Traffic 2008;9:1522-1529.
50. Grabski R, Balklava Z, Wyrozumska P, Szul T, Brandon E, Alvarez C, Holloway ZG, Sztul E. Identification of a functional domain within the p115 tethering factor that is required for Golgi ribbon assembly and membrane trafficking. J Cell Sci 2012;125(Pt 8):1896-1909.
51. Kondylis V, Rabouille C. A novel role for dp115 in the organization of tER sites in Drosophila. J Cell Biol 2003;162:185-198.
52. Puthenveedu MA, Linstedt AD. Gene replacement reveals that p115/SNARE interactions are essential for Golgi biogenesis. Proc Natl Acad Sci U S A 2004;101:1253-1256.
53. Levine TP, Rabouille C, Kieckbusch RH, Warren G. Binding of the vesicle docking protein p115 to Golgi membranes is inhibited under mitotic conditions. J Biol Chem 1996;271:17304-17311.
54. Diao A, Frost L, Morohashi Y, Lowe M. Coordination of Golgin tethering and SNARE assembly: GM130 binds syntaxin 5 in a p115-regulated manner. J Biol Chem 2008;283:6957-6967.
55. Bentley M, Liang Y, Mullen K, Xu D, Sztul E, Hay JC. SNARE status regulates tether recruitment and function in homotypic COPII vesicle fusion. J Biol Chem 2006;281:38825-38833.
56. Shorter J, Beard MB, Seemann J, Dirac-Svejstrup AB, Warren G. Sequential tethering of Golgins and catalysis of SNAREpin assembly by the vesicle-tethering protein p115. J Cell Biol 2002;157:45-62.
57. Xu D, Joglekar AP, Williams AL, Hay JC. Subunit structure of a mammalian ER/Golgi SNARE complex. J Biol Chem 2000;275:39631-39639.
58. Conibear E, Cleck JN, Stevens TH. Vps51p mediates the association of the GARP (Vps52/53/54) complex with the late Golgi t-SNARE Tlg1p. Mol Biol Cell 2003;14:1610-1623.
59. Siniossoglou S, Pelham HR. An effector of Ypt6p binds the SNARE Tlg1p and mediates selective fusion of vesicles with late Golgi membranes. EMBO J 2001;20:5991-5998.
60. Stroupe C, Collins KM, Fratti RA, Wickner W. Purification of active HOPS complex reveals its affinities for phosphoinositides and the SNARE Vam7p. EMBO J 2006;25:1579-1589.
61. Laage R, Ungermann C. The N-terminal domain of the t-SNARE Vam3p coordinates priming and docking in yeast vacuole fusion. Mol Biol Cell 2001;12:3375-3385.
62. Shestakova A, Suvorova E, Pavliv O, Khaidakova G, Lupashin V. Interaction of the conserved oligomeric Golgi complex with t-SNARE Syntaxin5a/Sed5 enhances intra-Golgi SNARE complex stability. J Cell Biol 2007;179:1179-1192.
63. Weimbs T, Low SH, Chapin SJ, Mostov KE, Bucher P, Hofmann K. A conserved domain is present in different families of vesicular fusion proteins: a new superfamily. Proc Natl Acad Sci U S A 1997;94:3046-3051.
64. 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.
65. 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.
66. Martinez-Arca S, Alberts P, Zahraoui A, Louvard D, Galli T. Role of tetanus neurotoxin insensitive vesicle-associated membrane protein (TI-VAMP) in vesicular transport mediating neurite outgrowth. J Cell Biol 2000;149:889-900.
67. Martinez-Arca S, Rudge R, Vacca M, Raposo G, Camonis J, Proux-Gillardeaux V, Daviet L, Formstecher E, Hamburger A, Filippini F, D'Esposito M, Galli T. A dual mechanism controlling the localization and function of exocytic v-SNAREs. Proc Natl Acad Sci U S A 2003;100:9011-9016.
68. Hasegawa H, Zinsser S, Rhee Y, Vik-Mo EO, Davanger S, Hay JC. Mammalian ykt6 is a neuronal SNARE targeted to a specialized compartment by its profilin-like amino terminal domain. Mol Biol Cell 2003;14:698-720.
69. Antonin W, Dulubova I, Arac D, Pabst S, Plitzner J, Rizo J, Jahn R. The N-terminal domains of syntaxin 7 and vti1b form three-helix bundles that differ in their ability to regulate SNARE complex assembly. J Biol Chem 2002;277:36449-36456.
70. Mossessova E, Bickford LC, Goldberg J. SNARE selectivity of the COPII coat. Cell 2003;114:483-495.
71. Bentley M, Nycz DC, Joglekar A, Fertschai I, Malli R, Graier WF, Hay JC. Vesicular calcium regulates coat retention, fusogenicity, and size of pre-Golgi intermediates. Mol Biol Cell 2010;21:1033-1046.
72. Seemann J, Jokitalo EJ, Warren G. The role of the tethering proteins p115 and GM130 in transport through the Golgi apparatus in vivo. Mol Biol Cell 2000;11:635-645.
73. Xu D, Hay JC. Reconstitution of COPII vesicle fusion to generate a pre-Golgi intermediate compartment. J Cell Biol 2004;167:997-1003.
74. Zagouras P, Rose JK. Dynamic equilibrium between vesicular stomatitis virus glycoprotein monomers and trimers in the Golgi and at the cell surface. J Virol 1993;67:7533-7538.
75. Moyer BD, Allan BB, Balch WE. Rab1 interaction with a GM130 effector complex regulates COPII vesicle cis--Golgi tethering. Traffic 2001;2:268-276.
76. Schwaninger R, Beckers CJ, Balch WE. Sequential transport of protein between the endoplasmic reticulum and successive Golgi compartments in semi-intact cells. J Biol Chem 1991;266:13055-13063.
77. 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.