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PMID: 18692470 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Structural basis for cargo regulation of COPII coat assembly.

Cell ·Vol. 134 ·No. 3 ·2008-08-08 ·Pages 474-84

Stagg SM, LaPointe P, Razvi A, Gürkan C, Potter CS, Carragher B, Balch WE

Abstract

Using cryo-electron microscopy, we have solved the structure of an icosidodecahedral COPII coat involved in cargo export from the endoplasmic reticulum (ER) coassembled from purified cargo adaptor Sec23-24 and Sec13-31 lattice-forming complexes. The coat structure shows a tetrameric assembly of the Sec23-24 adaptor layer that is well positioned beneath the vertices and edges of the Sec13-31 lattice. Fitting the known crystal structures of the COPII proteins into the density map reveals a flexible hinge region stemming from interactions between WD40 beta-propeller domains present in Sec13 and Sec31 at the vertices. The structure shows that the hinge region can direct geometric cage expansion to accommodate a wide range of bulky cargo, including procollagen and chylomicrons, that is sensitive to adaptor function in inherited disease. The COPII coat structure leads us to propose a mechanism by which cargo drives cage assembly and membrane curvature for budding from the ER.

MeSH Terms
Carrier Proteins/chemistry,metabolism Cryoelectron Microscopy Endoplasmic Reticulum/chemistry,metabolism Humans Models, Molecular Protein Transport Vesicular Transport Proteins/chemistry,metabolism
Chemicals
Carrier Proteins SEC13 protein, human SEC23A protein, human SEC24C protein, human SEC31A protein, human Vesicular Transport Proteins
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Stagg Scott M
National Resource for Automated Molecular Microscopy, The Scripps Research Institute, 10550 North Torrey Pines Road, La Jolla, CA 92037, USA.
LaPointe Paul
Razvi Abbas
Gürkan Cemal
Potter Clinton S
Carragher Bridget
Balch William E
References (37)
37 references, click to expand
  1. The genetic basis of a craniofacial disease provides insight into COPII coat assembly.
    Dev Cell. 2007 Nov;13(5):623-634 PMID: 17981132
  2. Structure of the Sec13/31 COPII coat cage.
    Nature. 2006 Jan 12;439(7073):234-8 PMID: 16407955
  3. Regulation of Sar1 NH2 terminus by GTP binding and hydrolysis promotes membrane deformation to control COPII vesicle fission.
    J Cell Biol. 2005 Dec 19;171(6):919-24 PMID: 16344311
  4. Cargo selection into COPII vesicles is driven by the Sec24p subunit.
    EMBO J. 2002 Nov 15;21(22):6105-13 PMID: 12426382
  5. Requirement for a GTPase-activating protein in vesicle budding from the endoplasmic reticulum.
    Science. 1993 Mar 5;259(5100):1466-8 PMID: 8451644
  6. Sar1p N-terminal helix initiates membrane curvature and completes the fission of a COPII vesicle.
    Cell. 2005 Aug 26;122(4):605-17 PMID: 16122427
  7. Endocytosis: clathrin-mediated membrane budding.
    Curr Opin Cell Biol. 2007 Aug;19(4):417-25 PMID: 17631994
  8. Cranio-lenticulo-sutural dysplasia is caused by a SEC23A mutation leading to abnormal endoplasmic-reticulum-to-Golgi trafficking.
    Nat Genet. 2006 Oct;38(10):1192-7 PMID: 16980979
  9. Self-assembly of minimal COPII cages.
    EMBO Rep. 2003 Apr;4(4):419-24 PMID: 12671686
  10. Bi-directional protein transport between the ER and Golgi.
    Annu Rev Cell Dev Biol. 2004;20:87-123 PMID: 15473836
  11. SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields.
    J Struct Biol. 1996 Jan-Feb;116(1):190-9 PMID: 8742743
  12. Structure and organization of coat proteins in the COPII cage.
    Cell. 2007 Jun 29;129(7):1325-36 PMID: 17604721
  13. COPII proteins are required for Golgi fusion but not for endoplasmic reticulum budding of the pre-chylomicron transport vesicle.
    J Cell Sci. 2003 Jan 15;116(Pt 2):415-27 PMID: 12482926
  14. Automated molecular microscopy: the new Leginon system.
    J Struct Biol. 2005 Jul;151(1):41-60 PMID: 15890530
  15. Structure of the Sec23/24-Sar1 pre-budding complex of the COPII vesicle coat.
    Nature. 2002 Sep 19;419(6904):271-7 PMID: 12239560
  16. Structural design of cage and coat scaffolds that direct membrane traffic.
    Curr Opin Struct Biol. 2007 Apr;17(2):221-8 PMID: 17395454
  17. The COPII cage: unifying principles of vesicle coat assembly.
    Nat Rev Mol Cell Biol. 2006 Oct;7(10):727-38 PMID: 16990852
  18. Structural insights into the clathrin coat.
    Semin Cell Dev Biol. 2007 Aug;18(4):448-58 PMID: 17702618
  19. Surface structure of the COPII-coated vesicle.
    Proc Natl Acad Sci U S A. 2001 Nov 20;98(24):13705-9 PMID: 11717432
  20. Molecular mechanisms of COPII vesicle formation.
    Semin Cell Dev Biol. 2007 Aug;18(4):424-34 PMID: 17686639
  21. EMAN: semiautomated software for high-resolution single-particle reconstructions.
    J Struct Biol. 1999 Dec 1;128(1):82-97 PMID: 10600563
  22. The Sar1 GTPase coordinates biosynthetic cargo selection with endoplasmic reticulum export site assembly.
    J Cell Biol. 2001 Jan 8;152(1):213-29 PMID: 11149932
  23. Sec16 is a determinant of transitional ER organization.
    Curr Biol. 2005 Aug 23;15(16):1439-47 PMID: 16111939
  24. Membrane curvature and the control of GTP hydrolysis in Arf1 during COPI vesicle formation.
    Biochem Soc Trans. 2005 Aug;33(Pt 4):619-22 PMID: 16042557
  25. TRAPPI tethers COPII vesicles by binding the coat subunit Sec23.
    Nature. 2007 Feb 22;445(7130):941-4 PMID: 17287728
  26. The intracellular transport of chylomicrons requires the small GTPase, Sar1b.
    Curr Opin Lipidol. 2004 Apr;15(2):191-7 PMID: 15017362
  27. Cargo selection by the COPII budding machinery during export from the ER.
    J Cell Biol. 1998 Apr 6;141(1):61-70 PMID: 9531548
  28. COPII-coated vesicle formation reconstituted with purified coat proteins and chemically defined liposomes.
    Cell. 1998 Apr 17;93(2):263-75 PMID: 9568718
  29. COPI-mediated transport.
    J Membr Biol. 2006;211(2):65-79 PMID: 17041781
  30. Normal mode based flexible fitting of high-resolution structure into low-resolution experimental data from cryo-EM.
    J Struct Biol. 2004 Sep;147(3):315-26 PMID: 15450300
  31. Coat proteins and vesicle budding.
    Science. 1996 Mar 15;271(5255):1526-33 PMID: 8599108
  32. Sec16p potentiates the action of COPII proteins to bud transport vesicles.
    J Cell Biol. 2002 Sep 16;158(6):1029-38 PMID: 12235121
  33. ACE: automated CTF estimation.
    Ultramicroscopy. 2005 Aug;104(1):8-29 PMID: 15935913
  34. Potassium-dependent assembly of coated pits: new coated pits form as planar clathrin lattices.
    J Cell Biol. 1986 Dec;103(6 Pt 2):2619-27 PMID: 2878930
  35. Cargo can modulate COPII vesicle formation from the endoplasmic reticulum.
    J Biol Chem. 1999 Feb 12;274(7):4389-99 PMID: 9933643
  36. Sar1 promotes vesicle budding from the endoplasmic reticulum but not Golgi compartments.
    J Cell Biol. 1994 Apr;125(1):51-65 PMID: 8138575
  37. Insights into COPII coat nucleation from the structure of Sec23.Sar1 complexed with the active fragment of Sec31.
    Dev Cell. 2007 Nov;13(5):635-645 PMID: 17981133
Article Info
Journal
Cell
Abbr.
Cell
ISSN
1097-4172
Published
2008-08-08
Pages
474-84
Language
English
Region
United States
NLM ID
0413066
PMCID
PMC2649882
Subset
IM
Grants
NIGMS NIH HHS · R01 GM042336 · United States
NCRR NIH HHS · P41 RR017573 · United States
NIGMS NIH HHS · GM42336 · United States
NIGMS NIH HHS · F32 GM073509 · United States
NCRR NIH HHS · P41 RR017573-07 · United States
NIBIB NIH HHS · R33 EB000798-04 · United States
NIBIB NIH HHS · R33 EB000798 · United States
NIGMS NIH HHS · R01 GM042336-17S1 · United States
NIGMS NIH HHS · GM073509 · United States
NCRR NIH HHS · RR17573 · United States
NIGMS NIH HHS · F32 GM073509-02 · United States
NIBIB NIH HHS · R33EB00798 · United States
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