Home LiteratureArticle Details
PMID: 20696705 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.

Structure of the Sec13-Sec16 edge element, a template for assembly of the COPII vesicle coat.

The Journal of cell biology ·Vol. 190 ·No. 3 ·2010-08-09 ·Pages 347-61

Whittle JR, Schwartz TU

Abstract

Ancestral coatomer element 1 (ACE1) proteins assemble latticework coats for COPII vesicles and the nuclear pore complex. The ACE1 protein Sec31 and Sec13 make a 2:2 tetramer that forms the edge element of the COPII outer coat. In this study, we report that the COPII accessory protein Sec16 also contains an ACE1. The 165-kD crystal structure of the central domain of Sec16 in complex with Sec13 was solved at 2.7-A resolution. Sec16 and Sec13 also make a 2:2 tetramer, another edge element for the COPII system. Domain swapping at the ACE1-ACE1 interface is observed both in the prior structure of Sec13-Sec31 and in Sec13-Sec16. A Sec31 mutant in which domain swapping is prevented adopts an unprecedented laminated structure, solved at 2.8-A resolution. Our in vivo data suggest that the ACE1 element of Sec31 can functionally replace the ACE1 element of Sec16. Our data support Sec16 as a scaffold for the COPII system and a template for the Sec13-Sec31 coat.

MeSH Terms
COP-Coated Vesicles/chemistry,metabolism DNA-Binding Proteins/chemistry,metabolism Endoplasmic Reticulum/chemistry,metabolism Membrane Proteins/chemistry,genetics,metabolism Models, Molecular Mutation Nuclear Pore Complex Proteins/chemistry,genetics,metabolism Protein Structure, Secondary Saccharomyces cerevisiae Proteins/chemistry,genetics,metabolism Transcription Factors/chemistry,metabolism
Chemicals
CUP2 protein, S cerevisiae DNA-Binding Proteins Membrane Proteins Nuclear Pore Complex Proteins SEC13 protein, S cerevisiae SEC16 protein, S cerevisiae Saccharomyces cerevisiae Proteins Transcription Factors
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Whittle James R R
Department of Biology, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
Schwartz Thomas U
References (59)
59 references, click to expand
  1. A fence-like coat for the nuclear pore membrane.
    Mol Cell. 2008 Dec 26;32(6):815-26 PMID: 19111661
  2. Organisation of human ER-exit sites: requirements for the localisation of Sec16 to transitional ER.
    J Cell Sci. 2009 Aug 15;122(Pt 16):2924-34 PMID: 19638414
  3. Components of coated vesicles and nuclear pore complexes share a common molecular architecture.
    PLoS Biol. 2004 Dec;2(12):e380 PMID: 15523559
  4. 3D domain swapping: a mechanism for oligomer assembly.
    Protein Sci. 1995 Dec;4(12):2455-68 PMID: 8580836
  5. Structure and organization of coat proteins in the COPII cage.
    Cell. 2007 Jun 29;129(7):1325-36 PMID: 17604721
  6. ALINE: a WYSIWYG protein-sequence alignment editor for publication-quality alignments.
    Acta Crystallogr D Biol Crystallogr. 2009 May;65(Pt 5):510-2 PMID: 19390156
  7. Determination of molecular weights and frictional ratios of proteins in impure systems by use of gel filtration and density gradient centrifugation. Application to crude preparations of sulfite and hydroxylamine reductases.
    Biochim Biophys Acta. 1966 Feb 7;112(2):346-62 PMID: 5329026
  8. Drosophila Sec16 mediates the biogenesis of tER sites upstream of Sar1 through an arginine-rich motif.
    Mol Biol Cell. 2008 Oct;19(10):4352-65 PMID: 18614796
  9. The CCP4 suite: programs for protein crystallography.
    Acta Crystallogr D Biol Crystallogr. 1994 Sep 1;50(Pt 5):760-3 PMID: 15299374
  10. Structural design of cage and coat scaffolds that direct membrane traffic.
    Curr Opin Struct Biol. 2007 Apr;17(2):221-8 PMID: 17395454
  11. The COPII cage: unifying principles of vesicle coat assembly.
    Nat Rev Mol Cell Biol. 2006 Oct;7(10):727-38 PMID: 16990852
  12. Structure of the Sec13/31 COPII coat cage.
    Nature. 2006 Jan 12;439(7073):234-8 PMID: 16407955
  13. Structural basis of the nic96 subcomplex organization in the nuclear pore channel.
    Mol Cell. 2008 Jan 18;29(1):46-55 PMID: 18206968
  14. Mechanism of scaffolding-assisted viral assembly.
    Adv Protein Chem. 2003;64:259-99 PMID: 13677050
  15. Structural evidence for common ancestry of the nuclear pore complex and vesicle coats.
    Science. 2008 Nov 28;322(5906):1369-73 PMID: 18974315
  16. Structural basis for cargo regulation of COPII coat assembly.
    Cell. 2008 Aug 8;134(3):474-84 PMID: 18692470
  17. Evolution of the beta-propeller fold.
    Proteins. 2008 May 1;71(2):795-803 PMID: 17979191
  18. COPII subunit interactions in the assembly of the vesicle coat.
    J Biol Chem. 1997 Oct 10;272(41):25413-6 PMID: 9325247
  19. SED4 encodes a yeast endoplasmic reticulum protein that binds Sec16p and participates in vesicle formation.
    J Cell Biol. 1995 Oct;131(2):325-38 PMID: 7593162
  20. Refinement of macromolecular structures by the maximum-likelihood method.
    Acta Crystallogr D Biol Crystallogr. 1997 May 1;53(Pt 3):240-55 PMID: 15299926
  21. COPII: a membrane coat formed by Sec proteins that drive vesicle budding from the endoplasmic reticulum.
    Cell. 1994 Jun 17;77(6):895-907 PMID: 8004676
  22. COPII and exit from the endoplasmic reticulum.
    Biochim Biophys Acta. 2005 Jul 10;1744(3):293-303 PMID: 15979503
  23. Protein acrobatics in pairs--dimerization via domain swapping.
    Curr Opin Struct Biol. 2009 Feb;19(1):39-49 PMID: 19162470
  24. COPII-coated vesicles: flexible enough for large cargo?
    Curr Opin Cell Biol. 2005 Aug;17(4):345-52 PMID: 15975775
  25. Sec16 is a determinant of transitional ER organization.
    Curr Biol. 2005 Aug 23;15(16):1439-47 PMID: 16111939
  26. Sec16 defines endoplasmic reticulum exit sites and is required for secretory cargo export in mammalian cells.
    Traffic. 2006 Dec;7(12):1678-87 PMID: 17005010
  27. [20] Processing of X-ray diffraction data collected in oscillation mode.
    Methods Enzymol. 1997;276:307-326 PMID: 27799103
  28. Reconstitution of coat protein complex II (COPII) vesicle formation from cargo-reconstituted proteoliposomes reveals the potential role of GTP hydrolysis by Sar1p in protein sorting.
    J Biol Chem. 2004 Jan 9;279(2):1330-5 PMID: 14627716
  29. Dynamics of the COPII coat with GTP and stable analogues.
    Nat Cell Biol. 2001 Jun;3(6):531-7 PMID: 11389436
  30. Yeast SEC16 gene encodes a multidomain vesicle coat protein that interacts with Sec23p.
    J Cell Biol. 1995 Oct;131(2):311-24 PMID: 7593161
  31. COPII-coated vesicle formation reconstituted with purified coat proteins and chemically defined liposomes.
    Cell. 1998 Apr 17;93(2):263-75 PMID: 9568718
  32. 3D domain swapping: as domains continue to swap.
    Protein Sci. 2002 Jun;11(6):1285-99 PMID: 12021428
  33. The mechanisms of vesicle budding and fusion.
    Cell. 2004 Jan 23;116(2):153-66 PMID: 14744428
  34. Homodimerization of the G protein SRbeta in the nucleotide-free state involves proline cis/trans isomerization in the switch II region.
    Proc Natl Acad Sci U S A. 2006 May 2;103(18):6823-8 PMID: 16627619
  35. Role of the scaffolding protein in P22 procapsid size determination suggested by T = 4 and T = 7 procapsid structures.
    Biophys J. 1998 Jan;74(1):559-68 PMID: 9449356
  36. The nuclear pore complex has entered the atomic age.
    Structure. 2009 Sep 9;17(9):1156-68 PMID: 19748337
  37. PHENIX: building new software for automated crystallographic structure determination.
    Acta Crystallogr D Biol Crystallogr. 2002 Nov;58(Pt 11):1948-54 PMID: 12393927
  38. Self-assembly of minimal COPII cages.
    EMBO Rep. 2003 Apr;4(4):419-24 PMID: 12671686
  39. Jalview Version 2--a multiple sequence alignment editor and analysis workbench.
    Bioinformatics. 2009 May 1;25(9):1189-91 PMID: 19151095
  40. The unfolding story of three-dimensional domain swapping.
    Structure. 2003 Mar;11(3):243-51 PMID: 12623012
  41. XDS.
    Acta Crystallogr D Biol Crystallogr. 2010 Feb;66(Pt 2):125-32 PMID: 20124692
  42. Two mammalian Sec16 homologues have nonredundant functions in endoplasmic reticulum (ER) export and transitional ER organization.
    Mol Biol Cell. 2007 Mar;18(3):839-49 PMID: 17192411
  43. Spherically averaged phased translation function and its application to the search for molecules and fragments in electron-density maps.
    Acta Crystallogr D Biol Crystallogr. 2001 Oct;57(Pt 10):1451-6 PMID: 11567159
  44. Protein crystallography for non-crystallographers, or how to get the best (but not more) from published macromolecular structures.
    FEBS J. 2008 Jan;275(1):1-21 PMID: 18034855
  45. Architecture of a coat for the nuclear pore membrane.
    Cell. 2007 Dec 28;131(7):1313-26 PMID: 18160040
  46. The Sec13p complex and reconstitution of vesicle budding from the ER with purified cytosolic proteins.
    EMBO J. 1993 Nov;12(11):4073-82 PMID: 8223424
  47. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae.
    Genetics. 1989 May;122(1):19-27 PMID: 2659436
  48. Distinct sets of SEC genes govern transport vesicle formation and fusion early in the secretory pathway.
    Cell. 1990 May 18;61(4):723-33 PMID: 2188733
  49. Molecular architecture of the Nup84-Nup145C-Sec13 edge element in the nuclear pore complex lattice.
    Nat Struct Mol Biol. 2009 Nov;16(11):1173-7 PMID: 19855394
  50. Crystal structure of nucleoporin Nic96 reveals a novel, intricate helical domain architecture.
    J Biol Chem. 2007 Nov 30;282(48):34904-12 PMID: 17897938
  51. A novel complex of nucleoporins, which includes Sec13p and a Sec13p homolog, is essential for normal nuclear pores.
    Cell. 1996 Jan 26;84(2):265-75 PMID: 8565072
  52. Sec16p potentiates the action of COPII proteins to bud transport vesicles.
    J Cell Biol. 2002 Sep 16;158(6):1029-38 PMID: 12235121
  53. Phaser crystallographic software.
    J Appl Crystallogr. 2007 Aug 1;40(Pt 4):658-674 PMID: 19461840
  54. Exiting the endoplasmic reticulum.
    Traffic. 2005 Apr;6(4):278-85 PMID: 15752134
  55. Assembly, organization, and function of the COPII coat.
    Histochem Cell Biol. 2008 Feb;129(2):129-51 PMID: 18060556
  56. COPII coat subunit interactions: Sec24p and Sec23p bind to adjacent regions of Sec16p.
    Mol Biol Cell. 1996 Nov;7(11):1815-23 PMID: 8930902
  57. Rapid and reliable protein extraction from yeast.
    Yeast. 2000 Jun 30;16(9):857-60 PMID: 10861908
  58. Calculation of hydrodynamic properties of globular proteins from their atomic-level structure.
    Biophys J. 2000 Feb;78(2):719-30 PMID: 10653785
  59. ER export: public transportation by the COPII coach.
    Curr Opin Cell Biol. 2001 Aug;13(4):438-43 PMID: 11454450
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
1540-8140
DOI
10.1083/jcb.201003092
Published
2010-08-09
Pages
347-61
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2922654
Subset
IM
Grants
NCRR NIH HHS · P41 RR015301 · United States
NIGMS NIH HHS · P50 GM068762 · United States
NIGMS NIH HHS · R01 GM077537 · United States
NCRR NIH HHS · RR-15301 · United States
External Links
PubMed source DOI: 10.1083/jcb.201003092 PMC Full Text View journal details
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: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2