Home LiteratureArticle Details
PMID: 11927603 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Sequential tethering of Golgins and catalysis of SNAREpin assembly by the vesicle-tethering protein p115.

The Journal of cell biology ·Vol. 157 ·No. 1 ·2002-04-01 ·Pages 45-62

Shorter J, Beard MB, Seemann J, Dirac-Svejstrup AB, Warren G

Abstract

p115 tethers coat protein (COP)I vesicles to Golgi membranes. The acidic COOH-terminal domain of p115 links the Golgins, Giantin on COPI vesicles, to GM130 on Golgi membranes. We now show that a SNARE motif-related domain within p115 stimulates the specific assembly of endogenous Golgi SNAREpins containing the t-SNARE, syntaxin 5. p115 catalyzes the construction of a cognate GOS-28-syntaxin-5 (v-/t-SNARE) complex by first linking the SNAREs to promote their direct interaction. These events are essential for NSF-catalyzed reassembly of postmitotic Golgi vesicles and tubules into mature cisternae. Staging experiments reveal that the linking of Golgins precedes SNAREpin assembly. Thus, p115 coordinates sequential tethering and docking of COPI vesicles by first using long tethers (Golgins) and then short tethers (SNAREs).

MeSH Terms
Animals Autoantigens COP-Coated Vesicles/metabolism Carrier Proteins/metabolism Detergents Golgi Apparatus/metabolism Golgi Matrix Proteins In Vitro Techniques Membrane Fusion/physiology Membrane Proteins/metabolism Qa-SNARE Proteins Qb-SNARE Proteins Qc-SNARE Proteins R-SNARE Proteins Rats Soluble N-Ethylmaleimide-Sensitive Factor Attachment Proteins Vesicular Transport Proteins
Chemicals
Autoantigens BET1 protein, rat BET1L protein, human Bet1l protein, rat Carrier Proteins Detergents GOSR1 protein, human GOSR2 protein, human Golgi Matrix Proteins Golgin subfamily A member 2 Gosr1 protein, mouse Gosr1 protein, rat Gosr2 protein, rat Membrane Proteins Qa-SNARE Proteins Qb-SNARE Proteins Qc-SNARE Proteins R-SNARE Proteins SEC22A protein, human Sec22a protein, rat Soluble N-Ethylmaleimide-Sensitive Factor Attachment Proteins Vesicular Transport Proteins Ykt6 protein, rat macrogolgin vesicular transport factor p115
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Shorter James
Department of Cell Biology, Ludwig Institute for Cancer Research, Yale University School of Medicine, New Haven, CT 06520, USA.
Beard Matthew B
Seemann Joachim
Dirac-Svejstrup A Barbara
Warren Graham
References (55)
55 references, click to expand
  1. Transport-vesicle targeting: tethers before SNAREs.
    Nat Cell Biol. 1999 May;1(1):E17-22 PMID: 10559876
  2. Membrane traffic: exocyst III--makes a family.
    Curr Biol. 2002 Jan 8;12(1):R18-20 PMID: 11790318
  3. Stacking the cisternae.
    Curr Biol. 1999 Dec 2;9(23):R893-6 PMID: 10607552
  4. The amino-terminal domain of the golgi protein giantin interacts directly with the vesicle-tethering protein p115.
    J Biol Chem. 2000 Jan 28;275(4):2831-6 PMID: 10644749
  5. The role of the tethering proteins p115 and GM130 in transport through the Golgi apparatus in vivo.
    Mol Biol Cell. 2000 Feb;11(2):635-45 PMID: 10679020
  6. SNAREs contribute to the specificity of membrane fusion.
    Neuron. 2000 May;26(2):457-64 PMID: 10839363
  7. Membrane fusion and exocytosis.
    Annu Rev Biochem. 1999;68:863-911 PMID: 10872468
  8. Close is not enough: SNARE-dependent membrane fusion requires an active mechanism that transduces force to membrane anchors.
    J Cell Biol. 2000 Jul 10;150(1):105-17 PMID: 10893260
  9. Rab1 recruitment of p115 into a cis-SNARE complex: programming budding COPII vesicles for fusion.
    Science. 2000 Jul 21;289(5478):444-8 PMID: 10903204
  10. 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 Aug 7;150(3):475-88 PMID: 10931861
  11. Sec1/Munc18 proteins: mediators of membrane fusion moving to center stage.
    Neuron. 2000 Aug;27(2):201-4 PMID: 10985341
  12. Anterograde flow of cargo across the golgi stack potentially mediated via bidirectional "percolating" COPI vesicles.
    Proc Natl Acad Sci U S A. 2000 Sep 12;97(19):10400-5 PMID: 10962035
  13. Compartmental specificity of cellular membrane fusion encoded in SNARE proteins.
    Nature. 2000 Sep 14;407(6801):153-9 PMID: 11001046
  14. Topological restriction of SNARE-dependent membrane fusion.
    Nature. 2000 Sep 14;407(6801):194-8 PMID: 11001058
  15. Matrix proteins can generate the higher order architecture of the Golgi apparatus.
    Nature. 2000 Oct 26;407(6807):1022-6 PMID: 11069184
  16. Subunit structure of a mammalian ER/Golgi SNARE complex.
    J Biol Chem. 2000 Dec 15;275(50):39631-9 PMID: 11035026
  17. Trans-complex formation by proteolipid channels in the terminal phase of membrane fusion.
    Nature. 2001 Feb 1;409(6820):581-8 PMID: 11214310
  18. SNARE complex oligomerization by synaphin/complexin is essential for synaptic vesicle exocytosis.
    Cell. 2001 Feb 9;104(3):421-32 PMID: 11239399
  19. Rab proteins as membrane organizers.
    Nat Rev Mol Cell Biol. 2001 Feb;2(2):107-17 PMID: 11252952
  20. Rab1 interaction with a GM130 effector complex regulates COPII vesicle cis--Golgi tethering.
    Traffic. 2001 Apr;2(4):268-76 PMID: 11285137
  21. SNAREs and the specificity of membrane fusion.
    Trends Cell Biol. 2001 Mar;11(3):99-101 PMID: 11306253
  22. The Golgi matrix protein GM130: a specific interacting partner of the small GTPase rab1b.
    EMBO Rep. 2001 Apr;2(4):336-41 PMID: 11306556
  23. Sequential SNARE assembly underlies priming and triggering of exocytosis.
    Neuron. 2001 Apr;30(1):161-70 PMID: 11343652
  24. Kinetics versus thermodynamics in protein folding.
    Biochemistry. 1994 Jun 21;33(24):7505-9 PMID: 8011615
  25. 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 Jan 17;92(2):522-6 PMID: 7831323
  26. Characterization of a cis-Golgi matrix protein, GM130.
    J Cell Biol. 1995 Dec;131(6 Pt 2):1715-26 PMID: 8557739
  27. Assembly of the ER to Golgi SNARE complex requires Uso1p.
    J Cell Biol. 1996 Mar;132(5):755-67 PMID: 8603910
  28. A v-SNARE implicated in intra-Golgi transport.
    J Cell Biol. 1996 May;133(3):507-16 PMID: 8636227
  29. Protein interactions regulating vesicle transport between the endoplasmic reticulum and Golgi apparatus in mammalian cells.
    Cell. 1997 Apr 4;89(1):149-58 PMID: 9094723
  30. A conserved domain is present in different families of vesicular fusion proteins: a new superfamily.
    Proc Natl Acad Sci U S A. 1997 Apr 1;94(7):3046-51 PMID: 9096343
  31. The vesicle docking protein p115 binds GM130, a cis-Golgi matrix protein, in a mitotically regulated manner.
    Cell. 1997 May 2;89(3):445-55 PMID: 9150144
  32. Assembly and disassembly of a ternary complex of synaptobrevin, syntaxin, and SNAP-25 in the membrane of synaptic vesicles.
    Proc Natl Acad Sci U S A. 1997 Jun 10;94(12):6197-201 PMID: 9177194
  33. GS15, a 15-kilodalton Golgi soluble N-ethylmaleimide-sensitive factor attachment protein receptor (SNARE) homologous to rbet1.
    J Biol Chem. 1997 Aug 8;272(32):20162-6 PMID: 9242691
  34. SNARE assembly and disassembly exhibit a pronounced hysteresis.
    Nat Struct Biol. 2002 Feb;9(2):144-51 PMID: 11786917
  35. Irreversible assembly of membrane fusion machines.
    Nat Struct Biol. 2002 Feb;9(2):78-80 PMID: 11813007
  36. A novel 115-kD peripheral membrane protein is required for intercisternal transport in the Golgi stack.
    J Cell Biol. 1992 Sep;118(5):1015-26 PMID: 1512287
  37. Identification and preliminary characterization of a protein motif related to the zinc finger.
    Proc Natl Acad Sci U S A. 1993 Mar 15;90(6):2112-6 PMID: 7681583
  38. Giantin, a novel conserved Golgi membrane protein containing a cytoplasmic domain of at least 350 kDa.
    Mol Biol Cell. 1993 Jul;4(7):679-93 PMID: 7691276
  39. A role for giantin in docking COPI vesicles to Golgi membranes.
    J Cell Biol. 1998 Mar 9;140(5):1013-21 PMID: 9490716
  40. Syntaxin 5 is a common component of the NSF- and p97-mediated reassembly pathways of Golgi cisternae from mitotic Golgi fragments in vitro.
    Cell. 1998 Mar 6;92(5):603-10 PMID: 9506515
  41. Initial docking of ER-derived vesicles requires Uso1p and Ypt1p but is independent of SNARE proteins.
    EMBO J. 1998 Apr 15;17(8):2156-65 PMID: 9545229
  42. Localization, dynamics, and protein interactions reveal distinct roles for ER and Golgi SNAREs.
    J Cell Biol. 1998 Jun 29;141(7):1489-502 PMID: 9647643
  43. A model for structural similarity between different SNARE complexes based on sequence relationships.
    Trends Cell Biol. 1998 Jul;8(7):260-2 PMID: 9714596
  44. A 29-kilodalton Golgi soluble N-ethylmaleimide-sensitive factor attachment protein receptor (Vti1-rp2) implicated in protein trafficking in the secretory pathway.
    J Biol Chem. 1998 Aug 21;273(34):21783-9 PMID: 9705316
  45. Cdc2 kinase directly phosphorylates the cis-Golgi matrix protein GM130 and is required for Golgi fragmentation in mitosis.
    Cell. 1998 Sep 18;94(6):783-93 PMID: 9753325
  46. Defining the functions of trans-SNARE pairs.
    Nature. 1998 Dec 10;396(6711):543-8 PMID: 9859990
  47. SNARE complex formation is triggered by Ca2+ and drives membrane fusion.
    Cell. 1999 Apr 16;97(2):165-74 PMID: 10219238
  48. The Saccharomyces cerevisiae v-SNARE Vti1p is required for multiple membrane transport pathways to the vacuole.
    Mol Biol Cell. 1999 Jun;10(6):1719-32 PMID: 10359592
  49. 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 Jul 12;146(1):57-70 PMID: 10402460
  50. Oligomeric complexes link Rab5 effectors with NSF and drive membrane fusion via interactions between EEA1 and syntaxin 13.
    Cell. 1999 Aug 6;98(3):377-86 PMID: 10458612
  51. Ykt6 forms a SNARE complex with syntaxin 5, GS28, and Bet1 and participates in a late stage in endoplasmic reticulum-Golgi transport.
    J Biol Chem. 2001 Jul 20;276(29):27480-7 PMID: 11323436
  52. Evidence that Golgi structure depends on a p115 activity that is independent of the vesicle tether components giantin and GM130.
    J Cell Biol. 2001 Oct 15;155(2):227-38 PMID: 11591729
  53. Identification of rabaptin-5, rabex-5, and GM130 as putative effectors of rab33b, a regulator of retrograde traffic between the Golgi apparatus and ER.
    FEBS Lett. 2001 Nov 16;508(2):201-9 PMID: 11718716
  54. A GRASP55-rab2 effector complex linking Golgi structure to membrane traffic.
    J Cell Biol. 2001 Dec 10;155(6):877-83 PMID: 11739401
  55. Peri-Golgi vesicles contain retrograde but not anterograde proteins consistent with the cisternal progression model of intra-Golgi transport.
    J Cell Biol. 2001 Dec 24;155(7):1213-24 PMID: 11748250
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
2002-04-01
Epub
2002-00-01
Pages
45-62
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2173270
Subset
IM
Grants
NIGMS NIH HHS · R01 GM060478 · United States
NIGMS NIH HHS · GM60478-01 · United States
Corrections
CommentIn
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]