Linker Nups connect the nuclear pore complex inner ring with the outer ring and transport channel

Nature Structural and Molecular Biology

Volumn 22, Issue 10, 2015, Pages 774-781

  Fischer, Jessica ^a   Teimer, Roman ^a   Amlacher, Stefan ^a   Kunze, Ruth ^a   Hurt, Ed ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEOPORIN; NUCLEOPORIN 170; NUCLEOPORIN 192; NUCLEOPORIN 82; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CHAETOMIUM; CHAETOMIUM THERMOPHILUM; CHANNEL GATING; COMPLEX FORMATION; CONTROLLED STUDY; HUMAN; IN VITRO STUDY; NONHUMAN; NUCLEAR PORE COMPLEX; NUCLEOCYTOPLASMIC TRANSPORT; PRIORITY JOURNAL; PROTEIN MOTIF; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; AFFINITY CHROMATOGRAPHY; CHEMICAL STRUCTURE; CHEMISTRY; ESCHERICHIA COLI; GENETICS; METABOLISM; MOLECULAR CLONING; NUCLEAR PORE; PLASMID; SIZE EXCLUSION CHROMATOGRAPHY; WESTERN BLOTTING; YEAST;

BLOTTING, WESTERN; CHAETOMIUM; CHROMATOGRAPHY, AFFINITY; CHROMATOGRAPHY, GEL; CLONING, MOLECULAR; ESCHERICHIA COLI; MODELS, MOLECULAR; NUCLEAR PORE; NUCLEAR PORE COMPLEX PROTEINS; PLASMIDS; YEASTS;

EID: 84943457200     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.3084     Document Type: Article

References (55)

1. Ptak, C., Aitchison, J.D. &Wozniak, R.W. The multifunctional nuclear pore complex: a platform for controlling gene expression. Curr. Opin. Cell Biol. 28, 46-53 (2014).
2. Bilokapic, S. &Schwartz, T.U. 3D ultrastructure of the nuclear pore complex. Curr. Opin. Cell Biol. 24, 86-91 (2012).
3. Wente, S.R. &Rout, M.P. The nuclear pore complex and nuclear transport. Cold Spring Harb. Perspect. Biol. 2, a000562 (2010).
4. Fahrenkrog, B. &Aebi, U. The nuclear pore complex: nucleocytoplasmic transport and beyond. Nat. Rev. Mol. Cell Biol. 4, 757-766 (2003).
5. Frey, S., Richter, R.P. &Gorlich, D. FG-rich repeats of nuclear pore proteins form a three-dimensional meshwork with hydrogel-like properties. Science 314, 815-817 (2006).
6. Lim, R.Y. et al. Nanomechanical basis of selective gating by the nuclear pore complex. Science 318, 640-643 (2007).
7. Rexach, M. &Blobel, G. Protein import into nuclei: association and dissociation reactions involving transport substrate, transport factors, and nucleoporins. Cell 83, 683-692 (1995).
8. Schwartz, T.U. Modularity within the architecture of the nuclear pore complex. Curr. Opin. Struct. Biol. 15, 221-226 (2005).
9. 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).
10. Walther, T.C. et al. The conserved Nup107-160 complex is critical for nuclear pore complex assembly. Cell 113, 195-206 (2003).
11. Stuwe, T. et al. Nuclear pores: architecture of the nuclear pore complex coat. Science 347, 1148-1152 (2015).
12. Kelley, K., Knockenhauer, K.E., Kabachinski, G. &Schwartz, T.U. Atomic structure of the Y complex of the nuclear pore. Nat. Struct. Mol. Biol. 22, 425-431 (2015).
13. Bui, K.H. et al. Integrated structural analysis of the human nuclear pore complex scaffold. Cell 155, 1233-1243 (2013).
14. Belgareh, N. et al. Functional characterization of a Nup159p-containing nuclear pore subcomplex. Mol. Biol. Cell 9, 3475-3492 (1998).
15. Grandi, P. et al. A novel nuclear pore protein Nup82p which specifically binds to a fraction of Nsp1p. J. Cell Biol. 130, 1263-1273 (1995).
16. Tieg, B. &Krebber, H. Dbp5: from nuclear export to translation. Biochim. Biophys. Acta 1829, 791-798 (2013).
17. Weirich, C.S., Erzberger, J.P., Berger, J.M. &Weis, K. The N-terminal domain of Nup159 forms a beta-propeller that functions in mRNA export by tethering the helicase Dbp5 to the nuclear pore. Mol. Cell 16, 749-760 (2004).
18. Gaik, M. et al. Structural basis for assembly and function of the Nup82 complex in the nuclear pore scaffold. J. Cell Biol. 208, 283-297 (2015).
19. Stelter, P. et al. Molecular basis for the functional interaction of dynein light chain with the nuclear-pore complex. Nat. Cell Biol. 9, 788-796 (2007).
20. Grandi, P., Schlaich, N., Tekotte, H. &Hurt, E.C. Functional interaction of Nic96p with a core nucleoporin complex consisting of Nsp1p, Nup49p and a novel protein Nup57p. EMBO J. 14, 76-87 (1995).
21. Amlacher, S. et al. Insight into structure and assembly of the nuclear pore complex by utilizing the genome of a eukaryotic thermophile. Cell 146, 277-289 (2011).
22. 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).
23. Eisenhardt, N., Redolfi, J. &Antonin, W. Interaction of Nup53 with Ndc1 and Nup155 is required for nuclear pore complex assembly. J. Cell Sci. 127, 908-921 (2014).
24. Mansfeld, J. et al. The conserved transmembrane nucleoporin NDC1 is required for nuclear pore complex assembly in vertebrate cells. Mol. Cell 22, 93-103 (2006).
25. Onischenko, E., Stanton, L.H., Madrid, A.S., Kieselbach, T. &Weis, K. Role of the Ndc1 interaction network in yeast nuclear pore complex assembly and maintenance. J. Cell Biol. 185, 475-491 (2009).
26. Rothballer, A. &Kutay, U. Poring over pores: nuclear pore complex insertion into the nuclear envelope. Trends Biochem. Sci. 38, 292-301 (2013).
27. Solmaz, S.R., Chauhan, R., Blobel, G. &Melcak, I. Molecular architecture of the transport channel of the nuclear pore complex. Cell 147, 590-602 (2011).
28. Chatel, G., Desai, S.H., Mattheyses, A.L., Powers, M.A. &Fahrenkrog, B. Domain topology of nucleoporin Nup98 within the nuclear pore complex. J. Struct. Biol. 177, 81-89 (2012).
29. Fabre, E., Boelens, W.C., Wimmer, C., Mattaj, I.W. &Hurt, E.C. Nup145p is required for nuclear export of mRNA and binds homopolymeric RNA in vitro via a novel conserved motif. Cell 78, 275-289 (1994).
30. Fontoura, B.M., Blobel, G. &Matunis, M.J. A conserved biogenesis pathway for nucleoporins: proteolytic processing of a 186-kilodalton precursor generates Nup98 and the novel nucleoporin, Nup96. J. Cell Biol. 144, 1097-1112 (1999).
31. Rosenblum, J.S. &Blobel, G. Autoproteolysis in nucleoporin biogenesis. Proc. Natl. Acad. Sci. USA 96, 11370-11375 (1999).
32. Teixeira, M.T. et al. Two functionally distinct domains generated by in vivo cleavage of Nup145p: a novel biogenesis pathway for nucleoporins. EMBO J. 16, 5086-5097 (1997).
33. Stelter, P. et al. Monitoring spatiotemporal biogenesis of macromolecular assemblies by pulse-chase epitope labeling. Mol. Cell 47, 788-796 (2012).
34. Wente, S.R. &Blobel, G. NUP145 encodes a novel yeast glycine-leucine-phenylalanine-glycine (GLFG) nucleoporin required for nuclear envelope structure. J. Cell Biol. 125, 955-969 (1994).
35. Wente, S.R., Rout, M.P. &Blobel, G. A new family of yeast nuclear pore complex proteins. J. Cell Biol. 119, 705-723 (1992).
36. Bailer, S.M. et al. Nup116p and nup100p are interchangeable through a conserved motif which constitutes a docking site for the mRNA transport factor gle2p. EMBO J. 17, 1107-1119 (1998).
37. Bailer, S.M. et al. Nup116p associates with the Nup82p-Nsp1p-Nup159p nucleoporin complex. J. Biol. Chem. 275, 23540-23548 (2000).
38. Ho, A.K. et al. Assembly and preferential localization of Nup116p on the cytoplasmic face of the nuclear pore complex by interaction with Nup82p. Mol. Cell. Biol. 20, 5736-5748 (2000).
39. Yoshida, K., Seo, H.S., Debler, E.W., Blobel, G. &Hoelz, A. Structural and functional analysis of an essential nucleoporin heterotrimer on the cytoplasmic face of the nuclear pore complex. Proc. Natl. Acad. Sci. USA 108, 16571-16576 (2011).
40. Stuwe, T., von Borzyskowski, L.S., Davenport, A.M. &Hoelz, A. Molecular basis for the anchoring of proto-oncoprotein Nup98 to the cytoplasmic face of the nuclear pore complex. J. Mol. Biol. 419, 330-346 (2012).
41. Lutzmann, M. et al. Reconstitution of Nup157 and Nup145N into the Nup84 complex. J. Biol. Chem. 280, 18442-18451 (2005).
42. Laurell, E. et al. Phosphorylation of Nup98 by multiple kinases is crucial for NPC disassembly during mitotic entry. Cell 144, 539-550 (2011).
43. Schlaich, N.L., Haner, M., Lustig, A., Aebi, U. &Hurt, E.C. In vitro reconstitution of a heterotrimeric nucleoporin complex consisting of recombinant Nsp1p, Nup49p, and Nup57p. Mol. Biol. Cell 8, 33-46 (1997).
44. Ulrich, A., Partridge, J.R. &Schwartz, T.U. The stoichiometry of the nucleoporin 62 subcomplex of the nuclear pore in solution. Mol. Biol. Cell 25, 1484-1492 (2014).
45. Schlaich, N.L., Häner, M., Lustig, A., Aebi, U. &Hurt, E.C. In vitro reconstitution of a heterotrimeric nucleoporin complex consisting of recombinant Nsp1p, Nup49p and Nup57p. Mol. Biol. Cell 8, 33-46 (1997).
46. Bailer, S.M., Balduf, C. &Hurt, E. The Nsp1p carboxy-terminal domain is organized into functionally distinct coiled-coil regions required for assembly of nucleoporin subcomplexes and nucleocytoplasmic transport. Mol. Cell. Biol. 21, 7944-7955 (2001).
47. Andersen, K.R. et al. Scaffold nucleoporins Nup188 and Nup192 share structural and functional properties with nuclear transport receptors. eLife 2, e00745 (2013).
48. Schrader, N. et al. Structural basis of the nic96 subcomplex organization in the nuclear pore channel. Mol. Cell 29, 46-55 (2008).
49. Rabut, G., Doye, V. &Ellenberg, J. Mapping the dynamic organization of the nuclear pore complex inside single living cells. Nat. Cell Biol. 6, 1114-1121 (2004).
50. Rout, M.P. et al. The yeast nuclear pore complex: composition, architecture, and transport mechanism. J. Cell Biol. 148, 635-651 (2000).
51. Bock, T. et al. An integrated approach for genome annotation of the eukaryotic thermophile Chaetomium thermophilum. Nucleic Acids Res. 42, 13525-13533 (2014).
52. Nissan, T.A., Bassler, J., Petfalski, E., Tollervey, D. &Hurt, E. 60S pre-ribosome formation viewed from assembly in the nucleolus until export to the cytoplasm. EMBO J. 21, 5539-5547 (2002).
53. 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).
54. Waterhouse, A.M., Procter, J.B., Martin, D.M., Clamp, M. &Barton, G.J. Jalview Version 2: a multiple sequence alignment editor and analysis workbench. Bioinformatics 25, 1189-1191 (2009).
55. Cole, C., Barber, J.D. &Barton, G.J. The Jpred 3 secondary structure prediction server. Nucleic Acids Res. 36, W197-W201 (2008).