Functional insights from studies on the structure of the nuclear pore and coat protein complexes

Cold Spring Harbor Perspectives in Biology

Volumn 5, Issue 7, 2013, Pages

  Schwartz, Thomas ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COAT PROTEIN COMPLEX I;

ACTIVE TRANSPORT; ARTICLE; BIOLOGICAL MODEL; CHEMISTRY; NUCLEAR PORE; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; STRUCTURE ACTIVITY RELATION;

ACTIVE TRANSPORT, CELL NUCLEUS; COAT PROTEIN COMPLEX I; MODELS, BIOLOGICAL; NUCLEAR PORE; PROTEIN STRUCTURE, TERTIARY; STRUCTURE-ACTIVITY RELATIONSHIP;

EUKARYOTA;

EID: 84879763996     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a013375     Document Type: Article

References (78)

1. Alber F, Dokudovskaya S, Veenhoff LM, Zhang W, Kipper J, Devos D, Suprapto A, Karni-Schmidt O, Williams R, Chait BT, et al. 2007. The molecular architecture of the nuclear pore complex. Nature 450: 695-701.
2. Amlacher S, Sarges P, Flemming D, van Noort V, Kunze R, Devos DP, Arumugam M, Bork P, Hurt E. 2011. Insight into structure and assembly of the nuclear pore complex by utilizing the genome of a eukaryotic thermophile. Cell 146: 277-289.
3. Antonin W, Mattaj IW. 2005. Nuclear pore complexes: Round the bend? Nat Cell Biol 7: 10-12.
4. Antonin W, Ellenberg J, Dultz E. 2008. Nuclear pore complex assembly through the cell cycle: Regulation and membrane organization. FEBS Lett 582: 2004-2016.
5. Beck M, Förster F, Ecke M, Plitzko JM, Melchior F, Gerisch G, Baumeister W, Medalia O. 2004. Nuclear pore complex structure and dynamics revealed by cryoelectron tomography. Science 306: 1387-1390.
6. Beck M, Lucić V, Förster F, Baumeister W, Medalia O. 2007. Snapshots of nuclear pore complexes in action captured by cryo-electron tomography. Nature 449: 611-615.
7. Berke IC, Boehmer T, Blobel G, Schwartz TU. 2004. Structural and functional analysis of Nup133 domains reveals modular building blocks of the nuclear pore complex. J Cell Biol 167: 591-597.
8. Bilokapic S, Schwartz TU. 2012. Molecular basis for Nup37 and ELY5/ELYS recruitment to the nuclear pore complex. Proc Natl Acad Sci 109: 15241-15246.
9. Brohawn SG, Schwartz TU. 2009. Molecular architecture of the Nup84-Nup145C-Sec13 edge element in the nuclear pore complex lattice. Nat Struct Mol Biol 16: 1173-1177.
10. Brohawn SG, Leksa NC, Spear ED, Rajashankar KR, Schwartz TU. 2008. Structural evidence for common ancestry of the nuclear pore complex and vesicle coats. Science 322: 1369-1373.
11. Brohawn SG, Partridge JR, Whittle JRR, Schwartz TU. 2009. The nuclear pore complex has entered the atomic age. Structure 17: 1156-1168.
12. Chaudhuri I, Söding J, Lupas AN. 2008. Evolution of the b-propeller fold. Proteins 71: 795-803.
13. Collins BM, McCoy AJ, Kent HM, Evans PR, Owen DJ. 2002. Molecular architecture and functional model of the endocytic AP2 complex. Cell 109: 523-535.
14. Connerly PL, Esaki M, Montegna EA, Strongin DE, Levi S, Soderholm J, Glick BS. 2005. Sec16 is a determinant of transitional ER organization. Curr Biol 15: 1439-1447.
15. Cronshaw JM, Krutchinsky AN, Zhang W, Chait BT, Matunis MJ. 2002. Proteomic analysis of the mammalian nuclear pore complex. J Cell Biol 158: 915-927.
16. D'Angelo MA, Raices M, Panowski SH, Hetzer MW. 2009. Age-dependent deterioration of nuclear pore complexes causes a loss of nuclear integrity in postmitotic cells. Cell 136: 284-295.
17. Degrasse JA, DuBois KN, Devos D, Siegel TN, Sali A, Field MC, Rout MP, Chait BT. 2009. Evidence for a shared nuclear pore complex architecture that is conserved from the last common eukaryotic ancestor. Mol Cell Proteomics 8: 2119-2130.
18. Devos D, Dokudovskaya S, Alber F, Williams R, Chait BT, Sali A, Rout MP. 2004. Components of coated vesicles and nuclear pore complexes share a common molecular architecture. PLoS Biol 2: e380.
19. Devos D, Dokudovskaya S, Williams R, Alber F, Eswar N, Chait BT, Rout MP, Sali A. 2006. Simple fold composition and modular architecture of the nuclear pore complex. Proc Natl Acad Sci 103: 2172-2177.
20. Dultz E, Ellenberg J. 2010. Live imaging of single nuclear pores reveals unique assembly kinetics and mechanism in interphase. J Cell Biol 191: 15-22.
21. Edeling MA, Smith C, Owen D. 2006. Life of a clathrin coat: Insights from clathrin and AP structures. Nat Rev Mol Cell Biol 7: 32-44.
22. Elad N, Maimon T, Frenkiel-Krispin D, Lim RYH, Medalia O. 2009. Structural analysis of the nuclear pore complex by integrated approaches. Curr Opin Struct Biol 19: 226-232.
23. Faini M, Prinz S, Beck R, Schorb M, Riches JD, Bacia K, Brügger B, Wieland FT, Briggs JAG. 2012. The structures of COPI-coated vesicles reveal alternate coatomer conformations and interactions. Science 336: 1451-1454.
24. Fath S, Mancias JD, Bi X, Goldberg J. 2007. Structure and organization of coat proteins in the COPII cage. Cell 129: 1325-1336.
25. Fernandez-Martinez J, Phillips J, Sekedat MD, Diaz-Avalos R, Velazquez-Muriel J, Franke JD, Williams R, Stokes DL, Chait BT, Sali A, et al. 2012. Structure-function mapping of a heptameric module in the nuclear pore complex. J Cell Biol 196: 419-434.
26. Flemming D, Devos DP, Schwarz J, Amlacher S, Lutzmann M, Hurt E. 2011. Analysis of the yeast nucleoporin Nup188 reveals a conserved S-like structure with similarity to karyopherins. J Struct Biol 177: 99-105.
27. Fotin A, Cheng Y, Sliz P, Grigorieff N, Harrison SC, Kirchhausen T, Walz T. 2004. Molecular model for a complete clathrin lattice from electron cryomicroscopy. Nature 432: 573-579.
28. Franz C, Askjaer P, Antonin W, Iglesias CL, Haselmann U, Schelder M, de Marco A, Wilm M, Antony C, Mattaj IW. 2005. Nup155 regulates nuclear envelope and nuclear pore complex formation in nematodes and vertebrates. EMBO J 24: 3519-3531.
29. Goldberg MW, Allen TD. 1996. The nuclear pore complex and lamina: Three-dimensional structures and interactions determined by field emission in-lens scanning electron microscopy. J Mol Biol 257: 848-865.
30. Görlich D, Kutay U. 1999. Transport between the cell nucleus and the cytoplasm. Annu Rev Cell Dev Biol 15: 607-660.
31. Grossman E, Medalia O, Zwerger M. 2012. Functional architecture of the nuclear pore complex. Annu Rev Biophys 41: 557-584.
32. Handa N, Kukimotoniino M, Akasaka R, Kishishita S, Murayama K, Terada T, Inoue M, Kigawa T, Kose S, Imamoto N. 2006. The crystal structure of mouse Nup35 reveals atypical RNP motifs and novel homodimerization of theRRMdomain. JMol Biol 363: 114-124.
33. Hawryluk-Gara LA, Platani M, Santarella R, Wozniak RW, Mattaj IW. 2008. Nup53 is required for nuclear envelope and nuclear pore complex assembly. Mol Biol Cell 19: 1753-1762.
34. Heldwein EE, Macia E, Wang J, Yin HL, Kirchhausen T, Harrison SC. 2004. Crystal structure of the clathrin adaptor protein 1 core. Proc Natl Acad Sci 101: 14108-14113.
35. Hetzer MW, Wente SR. 2009. Border control at the nucleus: Biogenesis and organization of the nuclear membrane and pore complexes. Dev Cell 17: 606-616.
36. Hsia K-C, Hoelz A. 2010. Crystal structure of a-COP in complex with 1-COP provides insight into the architecture of the COPI vesicular coat. Proc Natl Acad Sci 107: 11271-11276.
37. Hughes H, Budnik A, Schmidt K, Palmer KJ, Mantell J, Noakes C, Johnson A, Carter DA, Verkade P, Watson P, et al. 2009. Organisation of human ER-exit sites: Requirements for the localisation of Sec16 to transitional ER. J Cell Sci 122: 2924-2934.
38. Hülsmann BB, Labokha AA, Görlich D. 2012. The permeability of reconstituted nuclear pores provides direct evidence for the selective phase model. Cell 150: 738-751.
39. Jékely G, Arendt D. 2006. Evolution of intraflagellar transport from coated vesicles and autogenous origin of the eukaryotic cilium. Bioessays 28: 191-198.
40. Jeudy S, Schwartz TU. 2007. Crystal structure of nucleoporin Nic96 reveals a novel, intricate helical domain architecture. J Biol Chem 282: 34904-34912.
41. Jin L, Pahuja KB, Wickliffe KE, Gorur A, Baumgärtel C, Schekman R, Rape M. 2012. Ubiquitin-dependent regulation of COPII coat size and function. Nature 482: 495-500.
42. Kampmann M, Blobel G. 2009. Three-dimensional structure and flexibility of a membrane-coating module of the nuclear pore complex. Nat Struct Mol Biol 16: 782-788.
43. Kutay U, Hetzer MW. 2008. Reorganization of the nuclear envelope during open mitosis. Curr Opin Cell Biol 20: 669-677.
44. Lee C, Goldberg J. 2010. Structure of coatomer cage proteins and the relationship among COPI, COPII, and clathrin vesicle coats. Cell 142: 123-132.
45. Leksa NC, Brohawn SG, Schwartz TU. 2009. The structure of the scaffold nucleoporin Nup120 reveals a new and unexpected domain architecture. Structure 17: 1082-1091.
46. Liu J, Prunuske AJ, Fager AM, Ullman KS. 2003. The COPI complex functions in nuclear envelope breakdown and is recruited by the nucleoporin Nup153. Dev Cell 5: 487-498.
47. Lord C, Ferro-Novick S, Miller EA. 2013. The highly conserved COPII coat complex sorts cargo from the endoplasmic reticulum and targets it to the Golgi. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a013367.
48. Lutzmann M, Kunze R, Buerer A, Aebi U, Hurt E. 2002. Modular self-assembly of a Y-shaped multiprotein complex from seven nucleoporins. EMBO J 21: 387-397.
49. Maimon T, Elad N, Dahan I, Medalia O. 2012. The human nuclear pore complex as revealed by cryo-electron tomography. Structure 20: 998-1006.
50. Makio T, Stanton LH, Lin C-C, Goldfarb DS, Weis K, Wozniak RW. 2009. The nucleoporins Nup170p and Nup157p are essential for nuclear pore complex assembly. J Cell Biol 185: 459-473.
51. Mans BJ, Anantharaman V, Aravind L, Koonin EV. 2004. Comparative genomics, evolution and origins of the nuclear envelope and nuclear pore complex. Cell Cycle 3: 1612-1637.
52. Marelli M, Lusk CP, Chan H, Aitchison JD, Wozniak RW. 2001. A link between the synthesis of nucleoporins and the biogenesis of the nuclear envelope. J Cell Biol 153: 709-724.
53. Mekhail K, Moazed D. 2010. The nuclear envelope in genome organization, expression and stability. Nat Rev Mol Cell Biol 11: 317-328.
54. Nagy V, Hsia K-C, Debler EW, Kampmann M, Davenport AM, Blobel G, Hoelz A. 2009. Structure of a trimeric nucleoporin complex reveals alternate oligomerization states. Proc Natl Acad Sci 106: 17693-17698.
55. Nehrbass U, Rout MP, Maguire S, Blobel G, Wozniak RW. 1996. The yeast nucleoporin Nup188p interacts genetically and physicallywith the core structures of the nuclear pore complex. J Cell Biol 133: 1153-1162.
56. Neumann N, Lundin D, Poole AM. 2010. Comparative genomic evidence for a complete nuclear pore complex in the last eukaryotic common ancestor. PLoS ONE 5: e13241.
57. Nickel W, Brügger B, Wieland FT. 2002. Vesicular transport: The core machinery of COPI recruitment and budding. J Cell Sci 115: 3235-3240.
58. Onischenko E, Stanton LH, Madrid AS, Kieselbach T, Weis K. 2009. Role of the Ndc1 interaction network in yeast nuclear pore complex assembly and maintenance. J Cell Biol 185: 475-491.
59. Owen DJ, Collins BM, Evans PR. 2004. Adaptors for clathrin coats: Structure and function. Annu Rev Cell Dev Biol 20: 153-191.
60. Pante N, Kann M. 2002. Nuclear pore complex is able to transport macromolecules with diameters of about 39 nm. Mol Biol Cell 13: 425-434.
61. Pryer NK, Salama NR, Schekman R, Kaiser CA. 1993. Cytosolic Sec13p complex is required for vesicle formation from the endoplasmic reticulum in vitro. J Cell Biol 120: 865-875.
62. Rabut G, Doye V, Ellenberg J. 2004. Mapping the dynamic organization of the nuclear pore complex inside single living cells. Nat Cell Biol 6: 1114-1121.
63. Rout MP, Aitchison JD, Suprapto A, Hjertaas K, Zhao Y, Chait BT. 2000. The yeast nuclear pore complex: Composition, architecture, and transport mechanism. J Cell Biol 148: 635-651.
64. Sahlmüller MC, Strating JRPM, Beck R, Eckert P, Popoff V, Haag M, Hellwig A, Berger I, Brügger B, Wieland FT. 2011. Recombinant heptameric coatomer complexes: Novel tools to study isoform-specific functions. Traffic 12: 682-692.
65. Savas JN, Toyama BH, Xu T, Yates JR, Hetzer MW. 2012. Extremely long-lived nuclear pore proteins in the rat brain. Science 335: 942.
66. Siniossoglou S, Wimmer C, Rieger M, Doye V, Tekotte H, Weise C, Emig S, Segref A, Hurt EC. 1996. A novel complex of nucleoporins, which includes Sec13p and a Sec13p homolog, is essential for normal nuclear pores. Cell 84: 265-275.
67. Stagg SM, Gürkan C, Fowler DM, LaPointe P, Foss TR, Potter CS, Carragher B, Balch WE. 2006. Structure of the Sec13/31 COPII coat cage. Nature 439: 234-238.
68. Stagg SM, LaPointe P, Razvi A, Gürkan C, Potter CS, Carragher B, Balch WE. 2008. Structural basis for cargo regulation of COPII coat assembly. Cell 134: 474-484.
69. Stewart CL, Roux KJ, Burke B. 2007. Blurring the boundary: The nuclear envelope extends its reach. Science 318: 1408-1412.
70. Stirnimann CU, Petsalaki E, Russell RB, Müller CW. 2010. WD40 proteins propel cellular networks. Trends Biochem Sci 35: 565-574.
71. Theerthagiri G, Eisenhardt N, Schwarz H, Antonin W. 2010. The nucleoporin Nup188 controls passage of membrane proteins across the nuclear pore complex. J Cell Biol 189: 1129-1142.
72. Wente SR, Rout MP. 2010. The nuclear pore complex and nuclear transport. Cold Spring Harb Perspect Biol 2: a000562.
73. Whittle JRR, Schwartz TU. 2009. Architectural nucleoporins Nup157/170 and Nup133 are structurally related and descend from a second ancestral element. J Biol Chem 284: 28442-28452.
74. Whittle JRR, Schwartz TU. 2010. Structure of the Sec13-Sec16 edge element, a template for assembly of the COPII vesicle coat. J Cell Biol 190: 347-361.
75. Yu X, Breitman M, Goldberg J. 2012. A structure-based mechanism for Arf1-dependent recruitment of coatomer to membranes. Cell 148: 530-542.
76. Zabel U, Doye V, Tekotte H, Wepf R, Grandi P, Hurt EC. 1996. Nic96p is required for nuclear pore formation and functionally interacts with a novel nucleoporin, Nup188p. J Cell Biol 133: 1141-1152.
77. Zanetti G, Pahuja KB, Studer S, Shim S, Schekman R. 2012. COPII and the regulation of protein sorting inmammals. Nat Cell Biol 14: 20-28.
78. Zuleger N, Kerr ARW, Schirmer EC. 2012. Many mechanisms, one entrance: Membrane protein translocation into the nucleus. Cell Mol Life Sci 69: 2205-2216.