Atomic structure of the y complex of the nuclear pore

Nature Structural and Molecular Biology

Volumn 22, Issue 5, 2015, Pages 425-431

  Kelley, Kotaro ^a   Knockenhauer, Kevin E ^a   Kabachinski, Greg ^a   Schwartz, Thomas U ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEOPORIN; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; ATOMIC PARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; HUMAN; MOLECULAR DOCKING; MYCELIOPHTHORA THERMOPHILA; NONHUMAN; NUCLEAR PORE COMPLEX; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; SPECIES DIFFERENCE; Y COMPLEX HUB; AMINO ACID SEQUENCE; CELL NUCLEUS; METABOLISM; MOLECULAR MODEL; NUCLEAR PORE; PROTEIN TERTIARY STRUCTURE; SACCHAROMYCES CEREVISIAE; SEQUENCE ALIGNMENT; SORDARIALES; ULTRASTRUCTURE; X RAY CRYSTALLOGRAPHY;

CORYNASCUS HETEROTHALLICUS; EUKARYOTA;

AMINO ACID SEQUENCE; CELL NUCLEUS; CRYSTALLOGRAPHY, X-RAY; HUMANS; MODELS, MOLECULAR; MOLECULAR DOCKING SIMULATION; NUCLEAR PORE; NUCLEAR PORE COMPLEX PROTEINS; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ALIGNMENT; SORDARIALES;

EID: 84929268418     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2998     Document Type: Article

References (59)

1. Hetzer, M.W. & Wente, S.R. Border control at the nucleus: biogenesis and organization of the nuclear membrane and pore complexes. Dev. Cell 17, 606-616 (2009).
2. Strambio-De-Castillia, C., Niepel, M. & Rout, M.P. The nuclear pore complex: bridging nuclear transport and gene regulation. Nat. Rev. Mol. Cell Biol. 11, 490-501 (2010).
3. Brohawn, S.G., Partridge, J.R., Whittle, J.R.R. & Schwartz, T.U. The nuclear pore complex has entered the atomic age. Structure 17, 1156-1168 (2009).
4. Reichelt, R. et al. Correlation between structure and mass distribution of the nuclear pore complex and of distinct pore complex components. J. Cell Biol. 110, 883-894 (1990).
5. Yang, Q., Rout, M.P. & Akey, C.W. Three-dimensional architecture of the isolated yeast nuclear pore complex: functional and evolutionary implications. Mol. Cell 1, 223-234 (1998).
6. Rout, M.P. et al. The yeast nuclear pore complex: composition, architecture, and transport mechanism. J. Cell Biol. 148, 635-651 (2000).
7. Walther, T.C. et al. The conserved Nup107-160 complex is critical for nuclear pore complex assembly. Cell 113, 195-206 (2003).
8. Harel, A. et al. Removal of a single pore subcomplex results in vertebrate nuclei devoid of nuclear pores. Mol. Cell 11, 853-864 (2003).
9. Lutzmann, M., Kunze, R., Buerer, A., Aebi, U. & Hurt, E. Modular self-assembly of a Y-shaped multiprotein complex from seven nucleoporins. EMBO J. 21, 387-397 (2002).
10. Belgareh, N. et al. An evolutionarily conserved NPC subcomplex, which redistributes in part to kinetochores in mammalian cells. J. Cell Biol. 154, 1147-1160 (2001).
11. Vasu, S. et al. Novel vertebrate nucleoporins Nup133 and Nup160 play a role in mRNA export. J. Cell Biol. 155, 339-354 (2001).
12. Neumann, N., Lundin, D. & Poole, A.M. Comparative genomic evidence for a complete nuclear pore complex in the last eukaryotic common ancestor. PLoS ONE 5, e13241 (2010).
13. Vollmer, B. & Antonin, W. The diverse roles of the Nup93/Nic96 complex proteins: structural scaffolds of the nuclear pore complex with additional cellular functions. Biol. Chem. 395, 515-528 (2014).
14. Alber, F. et al. The molecular architecture of the nuclear pore complex. Nature 450, 695-701 (2007).
15. Bui, K.H. et al. Integrated structural analysis of the human nuclear pore complex scaffold. Cell 155, 1233-1243 (2013).
16. Berke, I.C., Boehmer, T., Blobel, G. & Schwartz, T.U. Structural and functional analysis of Nup133 domains reveals modular building blocks of the nuclear pore complex. J. Cell Biol. 167, 591-597 (2004).
17. Boehmer, T., Jeudy, S., Berke, I.C. & Schwartz, T.U. Structural and functional studies of Nup107/Nup133 interaction and its implications for the architecture of the nuclear pore complex. Mol. Cell 30, 721-731 (2008).
18. Brohawn, S.G., Leksa, N.C., Spear, E.D., Rajashankar, K.R. & Schwartz, T.U. Structural evidence for common ancestry of the nuclear pore complex and vesicle coats. Science 322, 1369-1373 (2008).
19. Brohawn, S.G. & Schwartz, T.U. Molecular architecture of the Nup84-Nup145C- Sec13 edge element in the nuclear pore complex lattice. Nat. Struct. Mol. Biol. 16, 1173-1177 (2009).
20. Leksa, N.C., Brohawn, S.G. & Schwartz, T.U. The structure of the scaffold nucleoporin Nup120 reveals a new and unexpected domain architecture. Structure 17, 1082-1091 (2009).
21. Whittle, J.R.R. & Schwartz, T.U. Architectural nucleoporins Nup157/170 and Nup133 are structurally related and descend from a second ancestral element. J. Biol. Chem. 284, 28442-28452 (2009).
22. Bilokapic, S. & Schwartz, T.U. Molecular basis for Nup37 and ELY5/ELYS recruitment to the nuclear pore complex. Proc. Natl. Acad. Sci. USA 109, 15241-15246 (2012).
23. Hsia, K.-C., Stavropoulos, P., Blobel, G. & Hoelz, A. Architecture of a coat for the nuclear pore membrane. Cell 131, 1313-1326 (2007).
24. Debler, E.W. et al. A fence-like coat for the nuclear pore membrane. Mol. Cell 32, 815-826 (2008).
25. Nagy, V. et al. Structure of a trimeric nucleoporin complex reveals alternate oligomerization states. Proc. Natl. Acad. Sci. USA 106, 17693-17698 (2009).
26. Seo, H.-S. et al. Structural and functional analysis of Nup120 suggests ring formation of the Nup84 complex. Proc. Natl. Acad. Sci. USA 106, 14281-14286 (2009).
27. Sampathkumar, P. et al. Structure of the C-terminal domain of Saccharomyces cerevisiae Nup133, a component of the nuclear pore complex. Proteins 79, 1672-1677 (2011).
28. Fernandez-Martinez, J. et al. Structure-function mapping of a heptameric module in the nuclear pore complex. J. Cell Biol. 196, 419-434 (2012).
29. Whittle, J.R.R. & Schwartz, T.U. Structure of the Sec13-Sec16 edge element, a template for assembly of the COPII vesicle coat. J. Cell Biol. 190, 347-361 (2010).
30. Thierbach, K. et al. Protein interfaces of the conserved Nup84 complex from Chaetomium thermophilum shown by crosslinking mass spectrometry and electron microscopy. Structure 21, 1672-1682 (2013).
31. Bar-Peled, L. et al. A tumor suppressor complex with GAP activity for the Rag GTPases that signal amino acid sufficiency to mTORC1. Science 340, 1100-1106 (2013).
32. Algret, R. et al. Molecular architecture and function of the SEA complex, a modulator of the TORC1 pathway. Mol. Cell. Proteomics 13, 2855-2870 (2014).
33. Siniossoglou, S. et al. A novel complex of nucleoporins, which includes Sec13p and a Sec13p homolog, is essential for normal nuclear pores. Cell 84, 265-275 (1996).
34. Stuwe, T. et al. Architecture of the nuclear pore complex coat. Science 347, 1148-1152 (2015).
35. Kim, S.J. et al. Integrative structure-function mapping of the nucleoporin Nup133 suggests a conserved mechanism for membrane anchoring of the nuclear pore complex. Mol. Cell. Proteomics 13, 2911-2926 (2014).
36. Liu, X., Mitchell, J.M., Wozniak, R.W., Blobel, G. & Fan, J. Structural evolution of the membrane-coating module of the nuclear pore complex. Proc. Natl. Acad. Sci. USA 109, 16498-16503 (2012).
37. Kampmann, M. & Blobel, G. Three-dimensional structure and flexibility of a membrane-coating module of the nuclear pore complex. Nat. Struct. Mol. Biol. 16, 782-788 (2009).
38. Süel, K.E., Cansizoglu, A.E. & Chook, Y.M. Atomic resolution structures in nuclear transport. Methods 39, 342-355 (2006).
39. Cook, A., Bono, F., Jinek, M. & Conti, E. Structural biology of nucleocytoplasmic transport. Annu. Rev. Biochem. 76, 647-671 (2007).
40. Szymborska, A. et al. Nuclear pore scaffold structure analyzed by super-resolution microscopy and particle averaging. Science 341, 655-658 (2013).
41. Ori, A. et al. Cell type-specific nuclear pores: a case in point for context-dependent stoichiometry of molecular machines. Mol. Syst. Biol. 9, 648 (2013).
42. Cronshaw, J.M., Krutchinsky, A.N., Zhang, W., Chait, B.T. & Matunis, M.J. Proteomic analysis of the mammalian nuclear pore complex. J. Cell Biol. 158, 915-927 (2002).
43. Ries, J., Kaplan, C., Platonova, E., Eghlidi, H. & Ewers, H. A simple, versatile method for GFP-based super-resolution microscopy via nanobodies. Nat. Methods 9, 582-584 (2012).
44. Andersen, K.R., Leksa, N.C. & Schwartz, T.U. Optimized E. coli expression strain LOBSTR eliminates common contaminants from His-tag purification. Proteins 81, 1857-1861 (2013).
45. Morin, A. et al. Collaboration gets the most out of software. eLife 2, e01456 (2013).
46. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997).
47. Adams, P.D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 (2010).
48. Winn, M.D. et al. Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67, 235-242 (2011).
49. Terwilliger, T.C. et al. phenix.mr-rosetta: molecular replacement and model rebuilding with Phenix and Rosetta. J. Struct. Funct. Genomics 13, 81-90 (2012).
50. Emsley, P., Lohkamp, B., Scott, W.G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501 (2010).
51. Chen, V.B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21 (2010).
52. Jeudy, S. & Schwartz, T.U. Crystal structure of nucleoporin Nic96 reveals a novel, intricate helical domain architecture. J. Biol. Chem. 282, 34904-34912 (2007).
53. Schrader, N. et al. Structural basis of the nic96 subcomplex organization in the nuclear pore channel. Mol. Cell 29, 46-55 (2008).
54. Kelley, L.A. & Sternberg, M.J.E. Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 4, 363-371 (2009).
55. Pettersen, E.F. et al. UCSF Chimera: a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).
56. Ciccarelli, F.D. et al. Toward automatic reconstruction of a highly resolved tree of life. Science 311, 1283-1287 (2006).
57. Fritz-Laylin, L.K. et al. The genome of Naegleria gruberi illuminates early eukaryotic versatility. Cell 140, 631-642 (2010).
58. Waterhouse, A.M. et al. Jalview Version 2: a multiple sequence alignment editor and analysis workbench. Bioinformatics 25, 1189-1191 (2009).
59. Gibson, D.G. et al. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat. Methods 6, 343-345 (2009).