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Dynamic Structures of the Nuclear Pore Complex and Their Roles in Nucleocytoplasmic Transport

  • Martin W. Goldberg
Chapter
Part of the Nucleic Acids and Molecular Biology book series (NUCLEIC, volume 33)

Abstract

The structure of the NPC has been studied for over 60 years. Although we are beginning to understand its structural framework, we do not know how the structure acts as a selective gate and how it facilitates transport in either direction. This may be because the very components that directly facilitate gating are varied, dynamic and possibly amorphous. Here, what we know about the structural organisation of the peripheral and dynamic components, such as the cytoplasmic filaments, the NPC basket and the structures within and protruding from the central channel, is reviewed in relation to their roles in nuclear transport.

Notes

Acknowledgements

Thanks to Christine Richardson for Fig. 3.4. Work was supported by Biotechnology and Biological Sciences Research Council, UK (grant numbers BB/E015735/1 and BB/G011818/1).

References

  1. Akey CW, Goldfarb DS (1989) Protein import through the nuclear pore complex is a multistep process. J Cell Biol 109:971–982CrossRefPubMedGoogle Scholar
  2. Afzelius BA (1955) The ultrastructure of the nuclear membrane of the sea urchin oocyte as studied with the electron microscope. Exp Cell Res 8:147–158CrossRefPubMedGoogle Scholar
  3. Ben-Efraim I, Frosst PD, Gerace L (2009) Karyopherin binding interactions and nuclear import mechanism of nuclear pore complex protein Tpr. BMC Cell Biol. 10:74CrossRefPubMedPubMedCentralGoogle Scholar
  4. Ball JR, Dimaano C, Bilak A, Kurchan E, Zundel MT, Ullman KS (2007) Sequence preference in RNA recognition by the nucleoporin Nup153. J Biol Chem 282:8734–8740CrossRefPubMedGoogle Scholar
  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 306:1387–1390CrossRefPubMedGoogle Scholar
  6. Beck M, Hurt E (2017) The nuclear pore complex: understanding its function through structural insight. Nat Rev Mol Cell Biol 18:73–89CrossRefPubMedGoogle Scholar
  7. Bernad R, van der Velde H, Fornerod M, Pickersgill H (2004) Nup358/RanBP2 attaches to the nuclear pore complex via association with Nup88 and Nup214/CAN and plays a supporting role in CRM1-mediated nuclear protein export. Mol Cell Biol 24:2373–2384CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bui KH, von Appen A, DiGuilio AL, Ori A, Sparks L, Mackmull MT, Bock T, Hagen W, Andrés-Pons A, Glavy JS, Beck M (2013) Integrated structural analysis of the human nuclear pore complex scaffold. Cell 155:1233–1243CrossRefPubMedGoogle Scholar
  9. Byrd DA, Sweet DJ, Panté N, Konstantinov KN, Guan T, Saphire AC, Mitchell PJ, Cooper CS, Aebi U, Gerace L (1994) Tpr, a large coiled coil protein whose amino terminus is involved in activation of oncogenic kinases, is localized to the cytoplasmic surface of the nuclear pore complex. J Cell Biol 127:1515–1526CrossRefPubMedGoogle Scholar
  10. Callan HG, Randall JT, Tomlin SG (1949) An electron microscope study of the nuclear membrane. Nature 163:280CrossRefPubMedGoogle Scholar
  11. Callan HG, Tomlin SG (1950) Experimental studies on amphibian oocyte nuclei. I. Investigation of the structure of the nuclear membrane by means of the electron microscope. Proc R Soc Lond B Biol Sci 137:367–378CrossRefPubMedGoogle Scholar
  12. Chakraborty P, Wang Y, Wei JH, van Deursen J, Yu H, Malureanu L, Dasso M, Forbes DJ, Levy DE, Seemann J, Fontoura BM (2008) Nucleoporin levels regulate cell cycle progression and phase-specific gene expression. Dev Cell 15:657–667CrossRefPubMedPubMedCentralGoogle Scholar
  13. Chatel G, Desai SH, Mattheyses AL, Powers MA, Fahrenkrog B (2012) Domain topology of nucleoporin Nup98 within the nuclear pore complex. J Struct Biol 177:81–89CrossRefPubMedGoogle Scholar
  14. Coyle JH, Bor YC, Rekosh D, Hammarskjold ML (2011) The Tpr protein regulates export of mRNAs with retained introns that traffic through the Nxf1 pathway. RNA 17:1344–1356CrossRefPubMedPubMedCentralGoogle Scholar
  15. Cordes VC, Reidenbach S, Rackwitz HR, Franke WW (1997) Identification of protein p270/Tpr as a constitutive component of the nuclear pore complex-attached intranuclear filaments. J Cell Biol 136:515–529CrossRefPubMedPubMedCentralGoogle Scholar
  16. Daigle N, Beaudouin J, Hartnell L, Imreh G, Hallberg E, Lippincott-Schwartz J, Ellenberg J (2001) Nuclear pore complexes form immobile networks and have a very low turnover in live mammalian cells. J Cell Biol 154:71–84CrossRefPubMedPubMedCentralGoogle Scholar
  17. 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 136:284–295CrossRefPubMedPubMedCentralGoogle Scholar
  18. Delphin C, Guan T, Melchior F, Gerace L (1997) RanGTP targets p97 to RanBP2, a filamentous protein localized at the cytoplasmic periphery of the nuclear pore complex. Mol Biol Cell 8:2379–2390CrossRefPubMedPubMedCentralGoogle Scholar
  19. Denning DP, Patel SS, Uversky V, Fink AL, Rexach M (2003) Disorder in the nuclear pore complex: the FG repeat regions of nucleoporins are natively unfolded. Proc Natl Acad Sci U S A 100:2450–2455CrossRefPubMedPubMedCentralGoogle Scholar
  20. Dimaano C, Ball JR, Prunuske AJ, Ullman KS (2001) RNA association defines a functionally conserved domain in the nuclear pore protein Nup153. J Biol Chem 276:45349–45357CrossRefPubMedGoogle Scholar
  21. Doucet CM, Esmery N, de Saint-Jean M, Antonny B (2015) Membrane curvature sensing by amphipathic helices is modulated by the surrounding protein backbone. PLoS One 10:e0137965CrossRefPubMedPubMedCentralGoogle Scholar
  22. Duheron V, Chatel G, Sauder U, Oliveri V, Fahrenkrog B (2014) Structural characterization of altered nucleoporin Nup153 expression in human cells by thin-section electron microscopy. Nucleus 5:601–612CrossRefPubMedPubMedCentralGoogle Scholar
  23. Eisele NB, Labokha AA, Frey S, Görlich D, Richter RP (2013) Cohesiveness tunes assembly and morphology of FG nucleoporin domain meshworks – implications for nuclear pore permeability. Biophys J 105:1860–1870CrossRefPubMedPubMedCentralGoogle Scholar
  24. Fahrenkrog B, Maco B, Fager AM, Köser J, Sauder U, Ullman KS, Aebi U (2002) Domain-specific antibodies reveal multiple-site topology of Nup153 within the nuclear pore complex. J Struct Biol 140:254–267CrossRefPubMedGoogle Scholar
  25. Feldherr CM (1965) The effect of the electron-opaque pore material on exchanges through the nuclear annuli. J Cell Biol 25:43–53CrossRefPubMedPubMedCentralGoogle Scholar
  26. Ferreira PA, Nakayama TA, Pak WL, Travis GH (1996) Cyclophilin-related protein RanBP2 acts as chaperone for red/green opsin. Nature 383:637–640CrossRefPubMedGoogle Scholar
  27. Fiserova J, Kiseleva E, Goldberg MW (2009) Nuclear envelope and nuclear pore complex structure and organization in tobacco BY-2 cells. Plant J 59:243–255CrossRefPubMedGoogle Scholar
  28. Fiserova J, Richards SA, Wente SR, Goldberg MW (2010) Facilitated transport and diffusion take distinct spatial routes through the nuclear pore complex. J Cell Sci 123:2773–2780CrossRefPubMedPubMedCentralGoogle Scholar
  29. Fiserova J, Spink M, Richards SA, Saunter C, Goldberg MW (2014) Entry into the nuclear pore complex is controlled by a cytoplasmic exclusion zone containing dynamic GLFG-repeat nucleoporin domains. J Cell Sci 127:124–136CrossRefPubMedGoogle Scholar
  30. Frosst P, Guan T, Subauste C, Hahn K, Gerace L (2002) Tpr is localized within the nuclear basket of the pore complex and has a role in nuclear protein export. J Cell Biol 156:617–630CrossRefPubMedPubMedCentralGoogle Scholar
  31. Galy V, Gadal O, Fromont-Racine M, Romano A, Jacquier A, Nehrbass U (2004) Nuclear retention of unspliced mRNAs in yeast is mediated by perinuclear Mlp1. Cell 116:63–73CrossRefPubMedGoogle Scholar
  32. Goldberg MW, Allen TD (1992) High resolution scanning electron microscopy of the nuclear envelope: demonstration of a new, regular, fibrous lattice attached to the baskets of the nucleoplasmic face of the nuclear pores. J Cell Biol 119:1429–1440CrossRefPubMedGoogle Scholar
  33. Goldberg MW, Allen TD (1993) The nuclear pore complex: three-dimensional surface structure revealed by field emission, in-lens scanning electron microscopy, with underlying structure uncovered by proteolysis. J Cell Sci 106:261–274PubMedGoogle Scholar
  34. 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 257:848–865CrossRefPubMedGoogle Scholar
  35. Goldberg MW, Solovei II, Allen TD (1997) Nuclear pore complex structure in birds. J Struct Biol 119:284–294CrossRefPubMedGoogle Scholar
  36. Goldberg MW, Rutherford SA, Hughes M, Cotter LA, Bagley S, Kiseleva E, Allen TD, Clarke PR (2000) Ran alters nuclear pore complex conformation. J Mol Biol 300:519–529CrossRefPubMedGoogle Scholar
  37. Goldberg MW, Huttenlauch I, Hutchison CJ, Stick R (2008) Filaments made from A- and B-type lamins differ in structure and organization. J Cell Sci 121:215–225CrossRefPubMedGoogle Scholar
  38. Griffis ER, Altan N, Lippincott-Schwartz J, Powers MA (2002) Nup98 is a mobile nucleoporin with transcription-dependent dynamics. Mol Biol Cell 13:1282–1297CrossRefPubMedPubMedCentralGoogle Scholar
  39. Hamada M, Haeger A, Jeganathan KB, van Ree JH, Malureanu L, Wälde S, Joseph J, Kehlenbach RH, van Deursen JM (2011) Ran-dependent docking of importin-beta to RanBP2/Nup358 filaments is essential for protein import and cell viability. J Cell Biol 194:597–612CrossRefPubMedPubMedCentralGoogle Scholar
  40. Hase ME, Kuznetsov NV, Cordes VC (2001) Amino acid substitutions of coiled-coil protein Tpr abrogate anchorage to the nuclear pore complex but not parallel, in-register homodimerization. Mol Biol Cell 12:2433–2452CrossRefPubMedPubMedCentralGoogle Scholar
  41. Hase ME, Cordes VC (2003) Direct interaction with nup153 mediates binding of Tpr to the periphery of the nuclear pore complex. Mol Biol Cell 14:1923–1940CrossRefPubMedPubMedCentralGoogle Scholar
  42. Higa MM, Alam SL, Sundquist WI, Ullman KS (2007) Molecular characterization of the Ran-binding zinc finger domain of Nup153. J Biol Chem 282:17090–17100CrossRefPubMedGoogle Scholar
  43. Hoelz A, Debler EW, Blobel G (2011) The structure of the nuclear pore complex. Annu Rev Biochem 80:613–643CrossRefPubMedGoogle Scholar
  44. Jarnik M, Aebi U (1991) Toward a more complete 3-D structure of the nuclear pore complex. J Struct Biol 107:291–308CrossRefPubMedGoogle Scholar
  45. Kapinos LE, Schoch RL, Wagner RS, Schleicher KD, Lim RY (2014) Karyopherin-centric control of nuclear pores based on molecular occupancy and kinetic analysis of multivalent binding with FG nucleoporins. Biophys J 106:1751–1762CrossRefPubMedPubMedCentralGoogle Scholar
  46. Kim SJ, Fernandez-Martinez J, Sampathkumar P, Martel A, Matsui T, Tsuruta H, Weiss TM, Shi Y, Markina-Inarrairaegui A, Bonanno JB, Sauder JM, Burley SK, Chait BT, Almo SC, Rout MP, Sali A (2014) Integrative structure-function mapping of the nucleoporin Nup133 suggests a conserved mechanism for membrane anchoring of the nuclear pore complex. Mol Cell Proteomics 13:2911–2926CrossRefPubMedPubMedCentralGoogle Scholar
  47. Kiseleva E, Allen TD, Rutherford S, Bucci M, Wente SR, Goldberg MW (2004) Yeast nuclear pore complexes have a cytoplasmic ring and internal filaments. J Struct Biol 145:272–288CrossRefPubMedGoogle Scholar
  48. Kiseleva E, Goldberg MW, Daneholt B, Allen TD (1996) RNP export is mediated by structural reorganization of the nuclear pore basket. J Mol Biol 260:304–311CrossRefPubMedGoogle Scholar
  49. Kosinski J, Mosalaganti S, von Appen A, Teimer R, DiGuilio AL, Wan W, Bui KH, Hagen WJ, Briggs JA, Glavy JS, Hurt E, Beck M (2016) Molecular architecture of the inner ring scaffold of the human nuclear pore complex. Science 352:363–365CrossRefPubMedGoogle Scholar
  50. Krull S, Dörries J, Boysen B, Reidenbach S, Magnius L, Norder H, Thyberg J, Cordes VC (2010) Protein Tpr is required for establishing nuclear pore-associated zones of heterochromatin exclusion. EMBO J 29:1659–1673CrossRefPubMedPubMedCentralGoogle Scholar
  51. Labokha AA, Gradmann S, Frey S, Hülsmann BB, Urlaub H, Baldus M, Görlich D (2013) Systematic analysis of barrier-forming FG hydrogels from Xenopus nuclear pore complexes. EMBO J 32:204–218CrossRefPubMedGoogle Scholar
  52. Lemaître C, Bickmore WA (2015) Chromatin at the nuclear periphery and the regulation of genome functions. Histochem Cell Biol 144:111–122CrossRefPubMedGoogle Scholar
  53. Lemke EA (2016) The multiple faces of disordered nucleoporins. J Mol Biol 428:2011–2024CrossRefPubMedGoogle Scholar
  54. Li B, Kohler JJ (2014) Glycosylation of the nuclear pore. Traffic 15:347–361CrossRefPubMedPubMedCentralGoogle Scholar
  55. Lim RY, Köser J, Huang NP, Schwarz-Herion K, Aebi U (2007a) Nanomechanical interactions of phenylalanine-glycine nucleoporins studied by single molecule force-volume spectroscopy. J Struct Biol 159:277–289CrossRefPubMedGoogle Scholar
  56. Lim RY, Fahrenkrog B, Köser J, Schwarz-Herion K, Deng J, Aebi U (2007b) Nanomechanical basis of selective gating by the nuclear pore complex. Science 318:640–643CrossRefPubMedGoogle Scholar
  57. Lin DH, Zimmermann S, Stuwe T, Stuwe E, Hoelz A (2013) Structural and functional analysis of the C-terminal domain of Nup358/RanBP2. J Mol Biol 425:1318–1329CrossRefPubMedPubMedCentralGoogle Scholar
  58. Loïodice I, Alves A, Rabut G, Van Overbeek M, Ellenberg J, Sibarita JB, Doye V (2004) The entire Nup107-160 complex, including three new members, is targeted as one entity to kinetochores in mitosis. Mol Biol Cell 15:3333–3344CrossRefPubMedPubMedCentralGoogle Scholar
  59. Ma J, Yang W (2010) Three-dimensional distribution of transient interactions in the nuclear pore complex obtained from single-molecule snapshots. Proc Natl Acad Sci USA 107:7305–7310CrossRefPubMedGoogle Scholar
  60. Ma J, Goryaynov A, Sarma A, Yang W (2012) Self-regulated viscous channel in the nuclear pore complex. Proc Natl Acad Sci USA 109:7326–7331CrossRefPubMedGoogle Scholar
  61. Ma J, Liu Z, Michelotti N, Pitchiaya S, Veerapaneni R, Androsavich JR, Walter NG, Yang W (2013) High-resolution three-dimensional mapping of mRNA export through the nuclear pore. Nat Commun 4:2414CrossRefPubMedPubMedCentralGoogle Scholar
  62. Ma J, Goryaynov A, Yang W (2016) Super-resolution 3D tomography of interactions and competition in the nuclear pore complex. Nat Struct Mol Biol 23:239–247CrossRefPubMedPubMedCentralGoogle Scholar
  63. Mehlin H, Daneholt B, Skoglund U (1995) Structural interaction between the nuclear pore complex and a specific translocating RNP particle. J Cell Biol 129:1205–1216CrossRefPubMedGoogle Scholar
  64. Merriam RW (1961) On the fine structure and composition of the nuclear envelope. J Biophys Biochem Cytol 11:559–570CrossRefPubMedPubMedCentralGoogle Scholar
  65. Milles S, Mercadante D, Aramburu IV, Jensen MR, Banterle N, Koehler C, Tyagi S, Clarke J, Shammas SL, Blackledge M, Gräter F, Lemke EA (2015) Plasticity of an ultrafast interaction between nucleoporins and nuclear transport receptors. Cell 163:734–745CrossRefPubMedPubMedCentralGoogle Scholar
  66. Murawala P, Tripathi MM, Vyas P, Salunke A, Joseph J (2009) Nup358 interacts with APC and plays a role in cell polarization. J Cell Sci 122:3113–3122CrossRefPubMedGoogle Scholar
  67. Oates ME, Romero P, Ishida T, Ghalwash M, Mizianty MJ, Xue B, Dosztányi S, Uversky VN, Obradovic Z, Kurgan L, Dunker AK, Gough J (2013) D2P2: database of disordered protein predictions. Nucleic Acids Res 41(D1):D508–D516CrossRefPubMedGoogle Scholar
  68. Palancade B, Zuccolo M, Loeillet S, Nicolas A, Doye V (2005) Pml39, a novel protein of the nuclear periphery required for nuclear retention of improper messenger ribonucleoparticles. Mol Biol Cell 16:5258–5268CrossRefPubMedPubMedCentralGoogle Scholar
  69. Panté N, Aebi U (1996) Sequential binding of import ligands to distinct nucleopore regions during their nuclear import. Science 273:1729–1732CrossRefPubMedGoogle Scholar
  70. Park N, Schweers NJ, Gustin KE (2015) Selective removal of FG repeat domains from the nuclear pore complex by enterovirus 2A(pro). J Virol 89:11069–11079CrossRefPubMedPubMedCentralGoogle Scholar
  71. Paulillo SM, Powers MA, Ullman KS, Fahrenkrog B (2006) Changes in nucleoporin domain topology in response to chemical effectors. J Mol Biol 363:39–50CrossRefPubMedGoogle Scholar
  72. Radu A, Moore MS, Blobel G (1995) The peptide repeat domain of nucleoporin Nup98 functions as a docking site in transport across the nuclear pore complex. Cell 81:215–222CrossRefPubMedGoogle Scholar
  73. Raices M, D’Angelo MA (2017) Nuclear pore complexes and regulation of gene expression. Curr Opin Cell Biol 46:26–32CrossRefPubMedPubMedCentralGoogle Scholar
  74. Rajanala K, Nandicoori VK (2012) Localization of nucleoporin Tpr to the nuclear pore complex is essential or Tpr mediated regulation of the export of unspliced RNA. PLoS One 7:e29921CrossRefPubMedPubMedCentralGoogle Scholar
  75. Ribbeck K, Görlich D (2002) The permeability barrier of nuclear pore complexes appears to operate via hydrophobic exclusion. EMBO J 21:2664–2671CrossRefPubMedPubMedCentralGoogle Scholar
  76. Ris H (1989) Three-dimensional imaging of cell ultrastructure with high resolution low voltage SEM. Inst Phys Conf Ser 98:657–662Google Scholar
  77. Ris H, Malecki M (1993) High-resolution field emission scanning electron microscope imaging of internal cell structures after Epon extraction from sections: a new approach to correlative ultrastructural and immunocytochemical studies. J Struct Biol 111:148–157CrossRefPubMedGoogle Scholar
  78. Ritterhoff T, Das H, Hofhaus G, Schröder RR, Flotho A, Melchior F (2016) The RanBP2/RanGAP1*SUMO1/Ubc9 SUMO E3 ligase is a disassembly machine for Crm1-dependent nuclear export complexes. Nat Commun 7:11482CrossRefPubMedPubMedCentralGoogle Scholar
  79. Rout MP, Aitchison JD, Magnasco MO, Chait BT (2003) Virtual gating and nuclear transport: the hole picture. Trends Cell Biol 13:622–628CrossRefPubMedGoogle Scholar
  80. Rutherford SA, Goldberg MW, Allen TD (1997) Three-dimensional visualization of the route of protein import: the role of nuclear pore complex substructures. Exp Cell Res 232:146–160CrossRefPubMedGoogle Scholar
  81. Sakiyama Y, Mazur A, Kapinos LE, Lim RY (2016) Spatiotemporal dynamics of the nuclear pore complex transport barrier resolved by high-speed atomic force microscopy. Nat Nanotechnol 11:719–723CrossRefPubMedGoogle Scholar
  82. Salina D, Enarson P, Rattner JB, Burke B (2003) Nup358 integrates nuclear envelope breakdown with kinetochore assembly. J Cell Biol 162:991–1001CrossRefPubMedPubMedCentralGoogle Scholar
  83. Schäpe J, Prausse S, Radmacher M, Stick R (2009) Influence of lamin A on the mechanical properties of amphibian oocyte nuclei measured by atomic force microscopy. Biophys J 96:4319–4325CrossRefPubMedPubMedCentralGoogle Scholar
  84. Schoch RL, Kapinos LE, Lim RY (2012) Nuclear transport receptor binding avidity triggers a self-healing collapse transition in FG-nucleoporin molecular brushes. Proc Natl Acad Sci U S A 109:16911–16916CrossRefPubMedPubMedCentralGoogle Scholar
  85. Schrader N, Koerner C, Koessmeier K, Bangert JA, Wittinghofer A, Stoll R, Vetter IR (2008) The crystal structure of the Ran-Nup153ZnF2 complex: a general Ran docking site at the nuclear pore complex. Structure 16:1116–1125CrossRefPubMedGoogle Scholar
  86. Schwarz-Herion K, Maco B, Sauder U, Fahrenkrog B (2007) Domain topology of the p62 complex within the 3-D architecture of the nuclear pore complex. J Mol Biol 370:796–806CrossRefPubMedGoogle Scholar
  87. Singh BB, Patel HH, Roepman R, Schick D, Ferreira PA (1999) The zinc finger cluster domain of RanBP2 is a specific docking site for the nuclear export factor, exportin-1. J Biol Chem 274:37370–37378CrossRefPubMedGoogle Scholar
  88. Soop T, Ivarsson B, Björkroth B, Fomproix N, Masich S, Cordes VC, Daneholt B (2005) Nup153 affects entry of messenger and ribosomal ribonucleoproteins into the nuclear basket during export. Mol Biol Cell 16:5610–5620CrossRefPubMedPubMedCentralGoogle Scholar
  89. Strambio-de-Castillia C, Blobel G, Rout MP (1999) Proteins connecting the nuclear pore complex with the nuclear interior. J Cell Biol 144:839–855CrossRefPubMedPubMedCentralGoogle Scholar
  90. Stevens BJ, Swift H (1966) RNA transport from nucleus to cytoplasm in Chironomus salivary glands. J Cell Biol. 31:55–77CrossRefPubMedPubMedCentralGoogle Scholar
  91. Tamura K, Fukao Y, Iwamoto M, Haraguchi T, Hara-Nishimura I (2010) Identification and characterization of nuclear pore complex components in Arabidopsis thaliana. Plant Cell 22:4084–4097CrossRefPubMedPubMedCentralGoogle Scholar
  92. Walther TC, Pickersgill HS, Cordes VC, Goldberg MW, Allen TD, Mattaj IW, Fornerod M (2002) The cytoplasmic filaments of the nuclear pore complex are dispensable for selective nuclear protein import. J Cell Biol 158:63–77CrossRefPubMedPubMedCentralGoogle Scholar
  93. Watson ML (1959) Further observations on the nuclear envelope of the animal cell. J Biophys Biochem Cytol 6:147–156CrossRefPubMedPubMedCentralGoogle Scholar
  94. Werner A, Flotho A, Melchior F (2012) The RanBP2/RanGAP1*SUMO1/Ubc9 complex is a multisubunit SUMO E3 ligase. Mol Cell 46:287–298CrossRefPubMedGoogle Scholar
  95. Wu J, Matunis MJ, Kraemer D, Blobel G, Coutavas E (1995) Nup358, a cytoplasmically exposed nucleoporin with peptide repeats, Ran-GTP binding sites, zinc fingers, a cyclophilin A homologous domain, and a leucine-rich region. J Biol Chem 270:14209–14213CrossRefPubMedGoogle Scholar
  96. Xu XM, Meulia T, Meier I (2007) Anchorage of plant RanGAP to the nuclear envelope involves novel nuclear-pore-associated proteins. Curr Biol 17:1157–1163CrossRefPubMedGoogle Scholar
  97. Yamada J, Phillips JL, Patel S, Goldfien G, Calestagne-Morelli A, Huang H, Reza R, Acheson J, Krishnan VV, Newsam S, Gopinathan A, Lau EY, Colvin ME, Uversky VN, Rexach MF (2010) A bimodal distribution of two distinct categories of intrinsically disordered structures with separate functions in FG nucleoporins. Mol Cell Proteomics 9:2205–2224CrossRefPubMedPubMedCentralGoogle Scholar
  98. Yang W (2013) Distinct, but not completely separate spatial transport routes in the nuclear pore complex. Nucleus 4:166–175CrossRefPubMedPubMedCentralGoogle Scholar
  99. Zhao CL, Mahboobi SH, Moussavi-Baygi R, Mofrad MR (2014) The interaction of CRM1 and the nuclear pore protein Tpr. PLoS One 9:e93709CrossRefPubMedPubMedCentralGoogle Scholar
  100. Zhou X, Graumann K, Evans DE, Meier I (2012) Novel plant SUN-KASH bridges are involved in RanGAP anchoring and nuclear shape determination. J Cell Biol 196:203–211CrossRefPubMedPubMedCentralGoogle Scholar

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© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of BiosciencesDurham UniversityDurhamUK

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