Towards understanding nuclear pore complex architecture and dynamics in the age of integrative structural analysis

Current Opinion in Cell Biology

Volumn 34, Issue , 2015, Pages 31-38

  Hurt, Ed ^a   Beck, Martin ^b  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DYNAMICS; HUMAN; IN VITRO STUDY; NONHUMAN; NUCLEAR PORE; NUCLEAR PORE COMPLEX; NUCLEOCYTOPLASMIC TRANSPORT; PRIORITY JOURNAL; REVIEW; STOICHIOMETRY; ACTIVE TRANSPORT; ANIMAL; BIOCHEMISTRY; METABOLISM;

NUCLEOPORIN;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; BIOCHEMICAL PHENOMENA; HUMANS; NUCLEAR PORE; NUCLEAR PORE COMPLEX PROTEINS;

EID: 84928783218     PISSN: 09550674     EISSN: 18790410     Source Type: Journal    
DOI: 10.1016/j.ceb.2015.04.009     Document Type: Review

References (58)

1. Hoelz A., Debler E.W., Blobel G. The structure of the nuclear pore complex. Annual Rev Biochem 2011, 80:613-643.
2. Russel D., Lasker K., Phillips J., Schneidman-Duhovny D., Velazquez-Muriel J.A., Sali A. The structural dynamics of macromolecular processes. Curr Opin Cell Biol 2009, 21:97-108.
3. Alber F., Dokudovskaya S., Veenhoff L.M., Zhang W., Kipper J., Devos D., Suprapto A., Karni-Schmidt O., Williams R., Chait B.T., et al. The molecular architecture of the nuclear pore complex. Nature 2007, 450:695-701.
4. 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 2008, 322:1369-1373.
5. Debler E.W., Ma Y., Seo H.S., Hsia K.C., Noriega T.R., Blobel G., Hoelz A. A fence-like coat for the nuclear pore membrane. Mol Cell 2008, 32:815-826.
6. Berman H.M., Burley S.K., Chiu W., Sali A., Adzhubei A., Bourne P.E., Bryant S.H., Dunbrack R.L., Fidelis K., Frank J., et al. Outcome of a workshop on archiving structural models of biological macromolecules. Structure 2006, 14:1211-1217.
7. Rout M.P., Aitchison J.D., Suprapto A., Hjertaas K., Zhao Y., Chait B.T. The yeast nuclear pore complex: composition, architecture, and transport mechanism. J Cell Biol 2000, 148:635-651.
8. 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 2002, 158:915-927.
9. Ori A., Andres-Pons A., Beck M. The use of targeted proteomics to determine the stoichiometry of large macromolecular assemblies. Methods Cell Biol 2014, 122:117-146.
10. Ulrich A., Partridge J.R., Schwartz T.U. The stoichiometry of the nucleoporin 62 subcomplex of the nuclear pore in solution. Mol Biol Cell 2014, 25:1484-1492.
11. Gaik M., Flemming D., Appen Av, Kastritis P., Mücke N., Fischer J., Stelter P., Ori A., Bui K.H., Bassler J., et al. Structural basis for assembly and function of the Nup82 complex in the nuclear pore scaffold. J Cell Biol 2015, 208:283-297. 10.1083/jcb.201411003.
12. Rabut G., Doye V., Ellenberg J. Mapping the dynamic organization of the nuclear pore complex inside single living cells. Nat Cell Biol 2004, 6:1114-1121.
13. Asakawa H., Yang H.J., Yamamoto T.G., Ohtsuki C., Chikashige Y., Sakata-Sogawa K., Tokunaga M., Iwamoto M., Hiraoka Y., Haraguchi T. Characterization of nuclear pore complex components in fission yeast Schizosaccharomyces pombe. Nucleus 2014, 5:149-162.
14. Ori A., Banterle N., Iskar M., Andres-Pons A., Escher C., Khanh Bui H., Sparks L., Solis-Mezarino V., Rinner O., Bork P., et al. Cell type-specific nuclear pores: a case in point for context-dependent stoichiometry of molecular machines. Mol Syst Biol 2013, 9:648.
15. Bui K.H., von Appen A., DiGuilio A.L., Ori A., Sparks L., Mackmull M.T., Bock T., Hagen W., Andres-Pons A., Glavy J.S., et al. Integrated structural analysis of the human nuclear pore complex scaffold. Cell 2013, 155:1233-1243.
16. Shi Y., Fernandez-Martinez J., Tjioe E., Pellarin R., Kim S.J., Williams R., Schneidman-Duhovny D., Sali A., Rout M.P., Chait B.T. Structural characterization by cross-linking reveals the detailed architecture of a coatomer-related heptameric module from the nuclear pore complex. Mol Cell Proteomics 2014, 13:2927-2943.
17. Thierbach K., von Appen A., Thoms M., Beck M., Flemming D., Hurt E. Protein interfaces of the conserved Nup84 complex from Chaetomium thermophilum shown by crosslinking mass spectrometry and electron microscopy. Structure 2013, 21:1672-1682. 10.1016/j.str.2013.07.004.
18. Jani D., Valkov E., Stewart M. Structural basis for binding the TREX2 complex to nuclear pores, GAL1 localisation and mRNA export. Nucleic Acids Res 2014, 42:6686-6697.
19. Kassube S.A., Stuwe T., Lin D.H., Antonuk C.D., Napetschnig J., Blobel G., Hoelz A. Crystal structure of the N-terminal domain of Nup358/RanBP2. J Mol Biol 2012, 423:752-765.
20. Lin D.H., Zimmermann S., Stuwe T., Stuwe E., Hoelz A. Structural and functional analysis of the C-terminal domain of Nup358/RanBP2. J Mol Biol 2013, 425:1318-1329.
21. 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 2012, 419:330-346.
22. Solmaz S.R., Blobel G., Melcak I. Ring cycle for dilating and constricting the nuclear pore. Proc Natl Acad Sci U S A 2013, 110:5858-5863.
23. Amlacher S., Sarges P., Flemming D., van Noort V., Kunze R., Devos D.P., Arumugam M., Bork P., Hurt E. Insight into structure and assembly of the nuclear pore complex by utilizing the genome of a eukaryotic thermophile. Cell 2011, 146:277-289.
24. Andersen K.R., Onischenko E., Tang J.H., Kumar P., Chen J.Z., Ulrich A., Liphardt J.T., Weis K., Schwartz T.U. Scaffold nucleoporins Nup188 and Nup192 share structural and functional properties with nuclear transport receptors. Elife 2013, 2:e00745.
25. Stuwe T., Lin D.H., Collins L.N., Hurt E., Hoelz A. Evidence for an evolutionary relationship between the large adaptor nucleoporin Nup192 and karyopherins. Proc Natl Acad Sci U S A 2014, 111:2530-2535.
26. Sampathkumar P., Kim S.J., Upla P., Rice W.J., Phillips J., Timney B.L., Pieper U., Bonanno J.B., Fernandez-Martinez J., Hakhverdyan Z., et al. Structure, dynamics, evolution, and function of a major scaffold component in the nuclear pore complex. Structure 2013, 21:560-571.
27. Flemming D., Devos D.P., Schwarz J., Amlacher S., Lutzmann M., Hurt E. Analysis of the yeast nucleoporin Nup188 reveals a conserved S-like structure with similarity to karyopherins. J Struct Biol 2012, 177:99-105.
28. Schrader N., Stelter P., Flemming D., Kunze R., Hurt E., Vetter I.R. Structural basis of the nic96 subcomplex organization in the nuclear pore channel. Mol Cell 2008, 29:46-55.
29. Xu S., Powers M.A. In vivo analysis of human nucleoporin repeat domain interactions. Mol Biol Cell 2013, 24:1222-1231.
30. Hulsmann B.B., Labokha A.A., Gorlich D. The permeability of reconstituted nuclear pores provides direct evidence for the selective phase model. Cell 2012, 150:738-751.
31. Van de Vosse D.W., Wan Y., Lapetina D.L., Chen W.M., Chiang J.H., Aitchison J.D., Wozniak R.W. A role for the nucleoporin Nup170p in chromatin structure and gene silencing. Cell 2013, 152:969-983.
32. Seo H.S., Blus B.J., Jankovic N.Z., Blobel G. Structure and nucleic acid binding activity of the nucleoporin Nup157. Proc Natl Acad Sci U S A 2013, 110:16450-16455.
33. Whittle J.R., Schwartz T.U. Architectural nucleoporins Nup157/170 and Nup133 are structurally related and descend from a second ancestral element. J Biol Chem 2009, 284:28442-28452.
34. Vollmer B., Schooley A., Sachdev R., Eisenhardt N., Schneider A.M., Sieverding C., Madlung J., Gerken U., Macek B., Antonin W. Dimerization and direct membrane interaction of Nup53 contribute to nuclear pore complex assembly. EMBO J 2012, 31:4072-4084.
35. Eisenhardt N., Redolfi J., Antonin W. Interaction of Nup53 with Ndc1 and Nup155 is required for nuclear pore complex assembly. J Cell Sci 2014, 127:908-921.
36. 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 1995, 14:76-87.
37. Sachdev R., Sieverding C., Flotenmeyer M., Antonin W. The C-terminal domain of Nup93 is essential for assembly of the structural backbone of nuclear pore complexes. Mol Biol Cell 2012, 23:740-749.
38. Fernandez-Martinez J., Phillips J., Sekedat M.D., Diaz-Avalos R., Velazquez-Muriel J., Franke J.D., Williams R., Stokes D.L., Chait B.T., Sali A., et al. Structure-function mapping of a heptameric module in the nuclear pore complex. J Cell Biol 2012, 196:419-434.
39. Kim S.J., Fernandez-Martinez J., Sampathkumar P., Martel A., Matsui T., Tsuruta H., Weiss T.M., Shi Y., Markina-Inarrairaegui A., Bonanno J.B., 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 2014, 13:2911-2926.
40. Franz C., Walczak R., Yavuz S., Santarella R., Gentzel M., Askjaer P., Galy V., Hetzer M., Mattaj I.W., Antonin W. MEL-28/ELYS is required for the recruitment of nucleoporins to chromatin and postmitotic nuclear pore complex assembly. Embo Reports 2007, 8:165-172.
41. Walther T.C., Askjaer P., Gentzel M., Habermann A., Griffiths G., Wilm M., Mattaj I.W., Hetzer M. RanGTP mediates nuclear pore complex assembly. Nature 2003, 424:689-694.
42. Walther T.C., Alves A., Pickersgill H., Loiodice I., Hetzer M., Galy V., Hulsmann B.B., Kocher T., Wilm M., Allen T., et al. The conserved Nup107-160 complex is critical for nuclear pore complex assembly. Cell 2003, 113:195-206.
43. Bilokapic S., Schwartz T.U. Molecular basis for Nup37 and ELY5/ELYS recruitment to the nuclear pore complex. Proc Natl Acad Sci U S A 2012, 109:15241-15246.
44. 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 U S A 2012, 109:16498-16503.
45. Bilokapic S., Schwartz T.U. Structural and functional studies of the 252 kDa nucleoporin ELYS reveal distinct roles for its three tethered domains. Structure 2013, 21:572-580. 10.1016/j.str.2013.02.006.
46. Doucet C.M., Talamas J.A., Hetzer M.W. Cell cycle-dependent differences in nuclear pore complex assembly in metazoa. Cell 2010, 141:1030-1041.
47. Szymborska A., de Marco A., Daigle N., Cordes V.C., Briggs J.A., Ellenberg J. Nuclear pore scaffold structure analyzed by super-resolution microscopy and particle averaging. Science 2013, 341:655-658.
48. Seo H.S., Ma Y., Debler E.W., Wacker D., Kutik S., Blobel G., Hoelz A. Structural and functional analysis of Nup120 suggests ring formation of the Nup84 complex. Proc Natl Acad Sci U S A 2009, 106:14281-14286.
49. Kampmann M., Atkinson C.E., Mattheyses A.L., Simon S.M. Mapping the orientation of nuclear pore proteins in living cells with polarized fluorescence microscopy. Nat Struct Mol Biol 2011, 18:643-649.
50. Kim D.I., Birendra K.C., Zhu W., Motamedchaboki K., Doye V., Roux K.J. Probing nuclear pore complex architecture with proximity-dependent biotinylation. Proc Natl Acad Sci U S A 2014, 111:E2453-E2461.
51. Banterle N., Bui K.H., Lemke E.A., Beck M. Fourier ring correlation as a resolution criterion for super-resolution microscopy. J Struct Biol 2013, 183:363-367.
52. Toyama B.H., Savas J.N., Park S.K., Harris M.S., Ingolia N.T., Yates J.R., Hetzer M.W. Identification of long-lived proteins reveals exceptional stability of essential cellular structures. Cell 2013, 154:971-982.
53. Raices M., D'Angelo M.A. Nuclear pore complex composition: a new regulator of tissue-specific and developmental functions. Nat Rev Mol Cell Biol 2012, 13:687-699.
54. Culjkovic-Kraljacic B., Baguet A., Volpon L., Amri A., Borden K.L. The oncogene eIF4E reprograms the nuclear pore complex to promote mRNA export and oncogenic transformation. Cell Rep 2012, 2:207-215.
55. Hansson J., Rafiee M.R., Reiland S., Polo J.M., Gehring J., Okawa S., Huber W., Hochedlinger K., Krijgsveld J. Highly coordinated proteome dynamics during reprogramming of somatic cells to pluripotency. Cell Rep 2012, 2:1579-1592.
56. D'Angelo M.A., Gomez-Cavazos J.S., Mei A., Lackner D.H., Hetzer M.W. A change in nuclear pore complex composition regulates cell differentiation. Dev Cell 2012, 22:446-458.
57. Beck M., Glavy J.S. Toward understanding the structure of the vertebrate nuclear pore complex. Nucleus 2014, 5:119-123.
58. Light W.H., Freaney J., Sood V., Thompson A., D'Urso A., Horvath C.M., Brickner J.H. A conserved role for human Nup98 in altering chromatin structure and promoting epigenetic transcriptional memory. PLoS Biol 2013, 11:e1001524.