The Nuclear Pore Complex as a Flexible and Dynamic Gate

Cell

Volumn 164, Issue 6, 2016, Pages 1162-1171

  Knockenhauer, Kevin E ^a   Schwartz, Thomas U ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEOPORIN;

CELL NUCLEUS MEMBRANE; CELL ULTRASTRUCTURE; HUMAN; NONHUMAN; NUCLEAR PORE COMPLEX; PRIORITY JOURNAL; REVIEW; ANIMAL; CHEMISTRY; GENETICS; MOLECULAR EVOLUTION; MOLECULAR MODEL; NUCLEAR PORE;

ANIMALS; EVOLUTION, MOLECULAR; HUMANS; MODELS, MOLECULAR; NUCLEAR PORE; NUCLEAR PORE COMPLEX PROTEINS;

EID: 84960453991     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2016.01.034     Document Type: Review

References (118)

1. C. Ader, S. Frey, W. Maas, H.B. Schmidt, D. Görlich, and M. Baldus Amyloid-like interactions within nucleoporin FG hydrogels Proc. Natl. Acad. Sci. USA 107 2010 6281 6285
2. F. Alber, S. Dokudovskaya, L.M. Veenhoff, W. Zhang, J. Kipper, D. Devos, A. Suprapto, O. Karni-Schmidt, R. Williams, B.T. Chait, and et al. The molecular architecture of the nuclear pore complex Nature 450 2007 695 701
3. N.P. Allen, L. Huang, A. Burlingame, and M. Rexach Proteomic analysis of nucleoporin interacting proteins J. Biol. Chem. 276 2001 29268 29274
4. T.D. Allen, J.M. Cronshaw, S. Bagley, E. Kiseleva, and M.W. Goldberg The nuclear pore complex: mediator of translocation between nucleus and cytoplasm J. Cell Sci. 113 2000 1651 1659
5. S. Amlacher, P. Sarges, D. Flemming, V. van Noort, R. Kunze, D.P. Devos, M. Arumugam, P. Bork, and E. Hurt Insight into structure and assembly of the nuclear pore complex by utilizing the genome of a eukaryotic thermophile Cell 146 2011 277 289
6. K.R. Andersen, E. Onischenko, J.H. Tang, P. Kumar, J.Z. Chen, A. Ulrich, J.T. Liphardt, K. Weis, and T.U. Schwartz Scaffold nucleoporins Nup188 and Nup192 share structural and functional properties with nuclear transport receptors eLife 2 2013 e00745 10.7554/eLife.00745
7. H. Asakawa, H.-J. Yang, T.G. Yamamoto, C. Ohtsuki, Y. Chikashige, K. Sakata-Sogawa, M. Tokunaga, M. Iwamoto, Y. Hiraoka, and T. Haraguchi Characterization of nuclear pore complex components in fission yeast Schizosaccharomyces pombe Nucleus 5 2014 149 162
8. N. Belgareh, G. Rabut, S.W. Baï, M. van Overbeek, J. Beaudouin, N. Daigle, O.V. Zatsepina, F. Pasteau, V. Labas, M. Fromont-Racine, and et al. An evolutionarily conserved NPC subcomplex, which redistributes in part to kinetochores in mammalian cells J. Cell Biol. 154 2001 1147 1160
9. I.C. Berke, T. Boehmer, G. Blobel, and T.U. Schwartz Structural and functional analysis of Nup133 domains reveals modular building blocks of the nuclear pore complex J. Cell Biol. 167 2004 591 597
10. A. Bestembayeva, A. Kramer, A.A. Labokha, D. Osmanović, I. Liashkovich, E.V. Orlova, I.J. Ford, G. Charras, A. Fassati, and B.W. Hoogenboom Nanoscale stiffness topography reveals structure and mechanics of the transport barrier in intact nuclear pore complexes Nat. Nanotechnol. 10 2015 60 64
11. S. Bilokapic, and T.U. Schwartz 3D ultrastructure of the nuclear pore complex Curr. Opin. Cell Biol. 24 2012 86 91
12. S. Bilokapic, and T.U. Schwartz Molecular basis for Nup37 and ELY5/ELYS recruitment to the nuclear pore complex Proc. Natl. Acad. Sci. USA 109 2012 15241 15246
13. A. Boni, A.Z. Politi, P. Strnad, W. Xiang, M.J. Hossain, and J. Ellenberg Live imaging and modeling of inner nuclear membrane targeting reveals its molecular requirements in mammalian cells J. Cell Biol. 209 2015 705 720
14. S.G. Brohawn, N.C. Leksa, E.D. Spear, K.R. Rajashankar, and T.U. Schwartz Structural evidence for common ancestry of the nuclear pore complex and vesicle coats Science 322 2008 1369 1373
15. S.G. Brohawn, J.R. Partridge, J.R.R. Whittle, and T.U. Schwartz The nuclear pore complex has entered the atomic age Structure 17 2009 1156 1168
16. K.H. Bui, A. von Appen, A.L. DiGuilio, A. Ori, L. Sparks, M.-T. Mackmull, T. Bock, W. Hagen, A. Andrés-Pons, J.S. Glavy, and M. Beck Integrated structural analysis of the human nuclear pore complex scaffold Cell 155 2013 1233 1243
17. H. Chug, S. Trakhanov, B.B. Hülsmann, T. Pleiner, and D. Görlich Crystal structure of the metazoan Nup62•Nup58•Nup54 nucleoporin complex Science 350 2015 106 110
18. A.G. Cook, and E. Conti Nuclear export complexes in the frame Curr. Opin. Struct. Biol. 20 2010 247 252
19. J.M. Cronshaw, A.N. Krutchinsky, W. Zhang, B.T. Chait, and M.J. Matunis Proteomic analysis of the mammalian nuclear pore complex J. Cell Biol. 158 2002 915 927
20. M.A. D'Angelo, M. Raices, S.H. Panowski, and M.W. Hetzer Age-dependent deterioration of nuclear pore complexes causes a loss of nuclear integrity in postmitotic cells Cell 136 2009 284 295
21. M.A. D'Angelo, J.S. Gomez-Cavazos, A. Mei, D.H. Lackner, and M.W. Hetzer A change in nuclear pore complex composition regulates cell differentiation Dev. Cell 22 2012 446 458
22. E.W. Debler, Y. Ma, H.-S. Seo, K.-C. Hsia, T.R. Noriega, G. Blobel, and A. Hoelz A fence-like coat for the nuclear pore membrane Mol. Cell 32 2008 815 826
23. J.A. Degrasse, and D. Devos A functional proteomic study of the Trypanosoma brucei nuclear pore complex: an informatic strategy Methods Mol. Biol. 673 2010 231 238
24. J.A. DeGrasse, K.N. DuBois, D. Devos, T.N. Siegel, A. Sali, M.C. Field, M.P. Rout, and B.T. Chait Evidence for a shared nuclear pore complex architecture that is conserved from the last common eukaryotic ancestor Mol. Cell. Proteomics 8 2009 2119 2130
25. D.P. Denning, S.S. Patel, V. Uversky, A.L. Fink, and M. Rexach Disorder in the nuclear pore complex: the FG repeat regions of nucleoporins are natively unfolded Proc. Natl. Acad. Sci. USA 100 2003 2450 2455
26. D. Devos, S. Dokudovskaya, F. Alber, R. Williams, B.T. Chait, A. Sali, and M.P. Rout Components of coated vesicles and nuclear pore complexes share a common molecular architecture PLoS Biol. 2 2004 e380
27. D. Devos, S. Dokudovskaya, R. Williams, F. Alber, N. Eswar, B.T. Chait, M.P. Rout, and A. Sali Simple fold composition and modular architecture of the nuclear pore complex Proc. Natl. Acad. Sci. USA 103 2006 2172 2177
28. D.P. Devos, R. Gräf, and M.C. Field Evolution of the nucleus Curr. Opin. Cell Biol. 28 2014 8 15
29. C.M. Doucet, and M.W. Hetzer Nuclear pore biogenesis into an intact nuclear envelope Chromosoma 119 2010 469 477
30. E. Dultz, and J. Ellenberg Live imaging of single nuclear pores reveals unique assembly kinetics and mechanism in interphase J. Cell Biol. 191 2010 15 22
31. M. Eibauer, M. Pellanda, Y. Turgay, A. Dubrovsky, A. Wild, and O. Medalia Structure and gating of the nuclear pore complex Nat. Commun. 6 2015 7532
32. N. Eisenhardt, J. Redolfi, and W. Antonin Interaction of Nup53 with Ndc1 and Nup155 is required for nuclear pore complex assembly J. Cell Sci. 127 2014 908 921
33. N. Fay, and N. Panté Nuclear entry of DNA viruses Front Microbiol 6 2015 467
34. M.C. Field, L. Koreny, and M.P. Rout Enriching the pore: splendid complexity from humble origins Traffic 15 2014 141 156
35. J. Fischer, R. Teimer, S. Amlacher, R. Kunze, and E. Hurt Linker Nups connect the nuclear pore complex inner ring with the outer ring and transport channel Nat. Struct. Mol. Biol. 22 2015 774 781
36. J. Fiserova, E. Kiseleva, and M.W. Goldberg Nuclear envelope and nuclear pore complex structure and organization in tobacco BY-2 cells Plant J. 59 2009 243 255
37. D. Flemming, D.P. Devos, J. Schwarz, S. Amlacher, M. Lutzmann, and E. Hurt Analysis of the yeast nucleoporin Nup188 reveals a conserved S-like structure with similarity to karyopherins J. Struct. Biol. 177 2012 99 105
38. C. Franz, R. Walczak, S. Yavuz, R. Santarella, M. Gentzel, P. Askjaer, V. Galy, M. Hetzer, I.W. Mattaj, and W. Antonin MEL-28/ELYS is required for the recruitment of nucleoporins to chromatin and postmitotic nuclear pore complex assembly EMBO Rep. 8 2007 165 172
39. V. Galy, I.W. Mattaj, and P. Askjaer Caenorhabditis elegans nucleoporins Nup93 and Nup205 determine the limit of nuclear pore complex size exclusion in vivo Mol. Biol. Cell 14 2003 5104 5115
40. J.S. Gomez-Cavazos, and M.W. Hetzer The nucleoporin gp210/Nup210 controls muscle differentiation by regulating nuclear envelope/ER homeostasis J. Cell Biol. 208 2015 671 681
41. P. Grandi, V. Doye, and E.C. Hurt Purification of NSP1 reveals complex formation with 'GLFG' nucleoporins and a novel nuclear pore protein NIC96 EMBO J. 12 1993 3061 3071
42. E. Grossman, O. Medalia, and M. Zwerger Functional architecture of the nuclear pore complex Annu. Rev. Biophys. 41 2012 557 584
43. N. Handa, M. Kukimoto-Niino, R. Akasaka, S. Kishishita, K. Murayama, T. Terada, M. Inoue, T. Kigawa, S. Kose, N. Imamoto, and et al. The crystal structure of mouse Nup35 reveals atypical RNP motifs and novel homodimerization of the RRM domain J. Mol. Biol. 363 2006 114 124
44. A. Harel, A.V. Orjalo, T. Vincent, A. Lachish-Zalait, S. Vasu, S. Shah, E. Zimmerman, M. Elbaum, and D.J. Forbes Removal of a single pore subcomplex results in vertebrate nuclei devoid of nuclear pores Mol. Cell 11 2003 853 864
45. M.W. Hetzer, and S.R. Wente Border control at the nucleus: biogenesis and organization of the nuclear membrane and pore complexes Dev. Cell 17 2009 606 616
46. L.E. Hough, K. Dutta, S. Sparks, D.B. Temel, A. Kamal, J. Tetenbaum-Novatt, M.P. Rout, and D. Cowburn The molecular mechanism of nuclear transport revealed by atomic-scale measurements eLife 4 2015 635
47. E. Hurt, and M. Beck Towards understanding nuclear pore complex architecture and dynamics in the age of integrative structural analysis Curr. Opin. Cell Biol. 34 2015 31 38
48. B.B. Hülsmann, A.A. Labokha, and D. Görlich The permeability of reconstituted nuclear pores provides direct evidence for the selective phase model Cell 150 2012 738 751
49. S. Jeudy, and T.U. Schwartz Crystal structure of nucleoporin Nic96 reveals a novel, intricate helical domain architecture J. Biol. Chem. 282 2007 34904 34912
50. M. Kampmann, and G. Blobel Three-dimensional structure and flexibility of a membrane-coating module of the nuclear pore complex Nat. Struct. Mol. Biol. 16 2009 782 788
51. K. Kelley, K.E. Knockenhauer, G. Kabachinski, and T.U. Schwartz Atomic structure of the Y complex of the nuclear pore Nat. Struct. Mol. Biol. 22 2015 425 431
52. D.I. Kim, K.C. Birendra, W. Zhu, K. Motamedchaboki, V. Doye, and K.J. Roux Probing nuclear pore complex architecture with proximity-dependent biotinylation Proc. Natl. Acad. Sci. USA 111 2014 E2453 E2461
53. S.J. Kim, J. Fernandez-Martinez, P. Sampathkumar, A. Martel, T. Matsui, H. Tsuruta, T.M. Weiss, Y. Shi, A. Markina-Inarrairaegui, J.B. Bonanno, and 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 2014 2911 2926
54. M.C. King, C.P. Lusk, and G. Blobel Karyopherin-mediated import of integral inner nuclear membrane proteins Nature 442 2006 1003 1007
55. T. Kirchhausen, D. Owen, and S.C. Harrison Molecular structure, function, and dynamics of clathrin-mediated membrane traffic Cold Spring Harb. Perspect. Biol. 6 2014 a016725-a016725
56. B. Kobe, and A.V. Kajava When protein folding is simplified to protein coiling: the continuum of solenoid protein structures Trends Biochem. Sci. 25 2000 509 515
57. J. Koh, and G. Blobel Allosteric regulation in gating the central channel of the nuclear pore complex Cell 161 2015 1361 1373
58. V.L. Koumandou, B. Wickstead, M.L. Ginger, M. van der Giezen, J.B. Dacks, and M.C. Field Molecular paleontology and complexity in the last eukaryotic common ancestor Crit. Rev. Biochem. Mol. Biol. 48 2013 373 396
59. A. Kralt, N.B. Jagalur, V. van den Boom, R.K. Lokareddy, A. Steen, G. Cingolani, M. Fornerod, and L.M. Veenhoff Conservation of inner nuclear membrane targeting sequences in mammalian Pom121 and yeast Heh2 membrane proteins Mol. Biol. Cell 26 2015 3301 3312
60. U. Kubitscheck, P. Wedekind, O. Zeidler, M. Grote, and R. Peters Single nuclear pores visualized by confocal microscopy and image processing Biophys. J. 70 1996 2067 2077
61. A.A. Labokha, S. Gradmann, S. Frey, B.B. Hülsmann, H. Urlaub, M. Baldus, and D. Görlich Systematic analysis of barrier-forming FG hydrogels from Xenopus nuclear pore complexes EMBO J. 32 2013 204 218
62. R.Y.H. Lim, B. Fahrenkrog, J. Köser, K. Schwarz-Herion, J. Deng, and U. Aebi Nanomechanical basis of selective gating by the nuclear pore complex Science 318 2007 640 643
63. X. Liu, J.M. Mitchell, R.W. Wozniak, G. Blobel, J. Fan, J. Fan, and J. Fan Structural evolution of the membrane-coating module of the nuclear pore complex Proc. Natl. Acad. Sci. USA 109 2012 16498 16503
64. I. Loïodice, A. Alves, G. Rabut, M. Van Overbeek, J. Ellenberg, J.-B. Sibarita, and V. Doye The entire Nup107-160 complex, including three new members, is targeted as one entity to kinetochores in mitosis Mol. Biol. Cell 15 2004 3333 3344
65. A.R. Lowe, J.H. Tang, J. Yassif, M. Graf, W.Y.C. Huang, J.T. Groves, K. Weis, and J.T. Liphardt Importin-β modulates the permeability of the nuclear pore complex in a Ran-dependent manner eLife 4 2015 10.7554/eLife.04052
66. F. Lupu, A. Alves, K. Anderson, V. Doye, and E. Lacy Nuclear pore composition regulates neural stem/progenitor cell differentiation in the mouse embryo Dev. Cell 14 2008 831 842
67. T. Maimon, N. Elad, I. Dahan, and O. Medalia The human nuclear pore complex as revealed by cryo-electron tomography Structure 20 2012 998 1006
68. B.J. Mans, V. Anantharaman, L. Aravind, and E.V. Koonin Comparative genomics, evolution and origins of the nuclear envelope and nuclear pore complex Cell Cycle 3 2004 1612 1637
69. K.A. Matreyek, and A. Engelman Viral and cellular requirements for the nuclear entry of retroviral preintegration nucleoprotein complexes Viruses 5 2013 2483 2511
70. A.C. Meinema, J.K. Laba, R.A. Hapsari, R. Otten, F.A.A. Mulder, A. Kralt, G. van den Bogaart, C.P. Lusk, B. Poolman, and L.M. Veenhoff Long unfolded linkers facilitate membrane protein import through the nuclear pore complex Science 333 2011 90 93
71. I. Melcák, A. Hoelz, and G. Blobel Structure of Nup58/45 suggests flexible nuclear pore diameter by intermolecular sliding Science 315 2007 1729 1732
72. E.A. Miller, and R. Schekman COPII - a flexible vesicle formation system Curr. Opin. Cell Biol. 25 2013 420 427
73. S. Milles, D. Mercadante, I.V. Aramburu, M.R. Jensen, N. Banterle, C. Koehler, S. Tyagi, J. Clarke, S.L. Shammas, M. Blackledge, and et al. Plasticity of an ultrafast interaction between nucleoporins and nuclear transport receptors Cell 163 2015 734 745
74. D. Mohr, S. Frey, T. Fischer, T. Güttler, and D. Görlich Characterisation of the passive permeability barrier of nuclear pore complexes EMBO J. 28 2009 2541 2553
75. S. Morchoisne-Bolhy, M.-C. Geoffroy, I.B. Bouhlel, A. Alves, N. Audugé, X. Baudin, K. Van Bortle, M.A. Powers, and V. Doye Intranuclear dynamics of the Nup107-160 complex Mol. Biol. Cell 26 2015 2343 2356
76. N. Neumann, D. Lundin, and A.M. Poole Comparative genomic evidence for a complete nuclear pore complex in the last eukaryotic common ancestor PLoS ONE 5 2010 e13241
77. E. Onischenko, L.H. Stanton, A.S. Madrid, T. Kieselbach, and K. Weis Role of the Ndc1 interaction network in yeast nuclear pore complex assembly and maintenance J. Cell Biol. 185 2009 475 491
78. A. Ori, N. Banterle, M. Iskar, A. Andrés-Pons, C. Escher, H. Khanh Bui, L. Sparks, V. Solis-Mezarino, O. Rinner, P. Bork, and et al. Cell type-specific nuclear pores: a case in point for context-dependent stoichiometry of molecular machines Mol. Syst. Biol. 9 2013 648-648
79. N. Panté, and M. Kann Nuclear pore complex is able to transport macromolecules with diameters of about 39 nm Mol. Biol. Cell 13 2002 425 434
80. S.S. Patel, B.J. Belmont, J.M. Sante, and M.F. Rexach Natively unfolded nucleoporins gate protein diffusion across the nuclear pore complex Cell 129 2007 83 96
81. O. Peleg, and R.Y.H. Lim Converging on the function of intrinsically disordered nucleoporins in the nuclear pore complex Biol. Chem. 391 2010 719 730
82. G. Rabut, V. Doye, and J. Ellenberg Mapping the dynamic organization of the nuclear pore complex inside single living cells Nat. Cell Biol. 6 2004 1114 1121
83. B.A. Rasala, A.V. Orjalo, Z. Shen, S. Briggs, and D.J. Forbes ELYS is a dual nucleoporin/kinetochore protein required for nuclear pore assembly and proper cell division Proc. Natl. Acad. Sci. USA 103 2006 17801 17806
84. R. Reichelt, A. Holzenburg, E.L. Buhle Jr., M. Jarnik, A. Engel, and U. Aebi Correlation between structure and mass distribution of the nuclear pore complex and of distinct pore complex components J. Cell Biol. 110 1990 883 894
85. K. Ribbeck, and D. Görlich Kinetic analysis of translocation through nuclear pore complexes EMBO J. 20 2001 1320 1330
86. A. Rothballer, and U. Kutay Poring over pores: nuclear pore complex insertion into the nuclear envelope Trends Biochem. Sci. 38 2013 292 301
87. M.P. Rout, J.D. Aitchison, A. Suprapto, K. Hjertaas, Y. Zhao, and B.T. Chait The yeast nuclear pore complex: composition, architecture, and transport mechanism J. Cell Biol. 148 2000 635 651
88. M.P. Rout, J.D. Aitchison, M.O. Magnasco, and B.T. Chait Virtual gating and nuclear transport: the hole picture Trends Cell Biol. 13 2003 622 628
89. P. Sampathkumar, S.J. Kim, P. Upla, W.J. Rice, J. Phillips, B.L. Timney, U. Pieper, J.B. Bonanno, J. Fernandez-Martinez, Z. Hakhverdyan, and et al. Structure, dynamics, evolution, and function of a major scaffold component in the nuclear pore complex Structure 21 2013 560 571
90. J.N. Savas, B.H. Toyama, T. Xu, J.R. Yates 3rd, and M.W. Hetzer Extremely long-lived nuclear pore proteins in the rat brain Science 335 2012 942
91. H.B. Schmidt, and D. Görlich Nup98 FG domains from diverse species spontaneously phase-separate into particles with nuclear pore-like permselectivity eLife 4 2015 e04251
92. A. Schooley, B. Vollmer, and W. Antonin Building a nuclear envelope at the end of mitosis: coordinating membrane reorganization, nuclear pore complex assembly, and chromatin de-condensation Chromosoma 121 2012 539 554
93. N. Schrader, P. Stelter, D. Flemming, R. Kunze, E. Hurt, and I.R. Vetter Structural basis of the nic96 subcomplex organization in the nuclear pore channel Mol. Cell 29 2008 46 55
94. T.U. Schwartz Modularity within the architecture of the nuclear pore complex Curr. Opin. Struct. Biol. 15 2005 221 226
95. H.-S. Seo, B.J. Blus, N.Z. Jankovic, and G. Blobel Structure and nucleic acid binding activity of the nucleoporin Nup157 Proc. Natl. Acad. Sci. USA 110 2013 16450 16455
96. S. Siniossoglou, M. Lutzmann, H. Santos-Rosa, K. Leonard, S. Mueller, U. Aebi, and E. Hurt Structure and assembly of the Nup84p complex J. Cell Biol. 149 2000 41 54
97. S.R. Solmaz, R. Chauhan, G. Blobel, and I. Melčák Molecular architecture of the transport channel of the nuclear pore complex Cell 147 2011 590 602
98. B. Soullam, and H.J. Worman Signals and structural features involved in integral membrane protein targeting to the inner nuclear membrane J. Cell Biol. 130 1995 15 27
99. F. Stavru, B.B. Hülsmann, A. Spang, E. Hartmann, V.C. Cordes, and D. Görlich NDC1: a crucial membrane-integral nucleoporin of metazoan nuclear pore complexes J. Cell Biol. 173 2006 509 519
100. L.A. Strawn, T. Shen, N. Shulga, D.S. Goldfarb, and S.R. Wente Minimal nuclear pore complexes define FG repeat domains essential for transport Nat. Cell Biol. 6 2004 197 206
101. T. Stuwe, D.H. Lin, L.N. Collins, E. Hurt, and A. Hoelz Evidence for an evolutionary relationship between the large adaptor nucleoporin Nup192 and karyopherins Proc. Natl. Acad. Sci. USA 111 2014 2530 2535
102. T. Stuwe, C.J. Bley, K. Thierbach, S. Petrovic, S. Schilbach, D.J. Mayo, T. Perriches, E.J. Rundlet, Y.E. Jeon, L.N. Collins, and et al. Architecture of the fungal nuclear pore inner ring complex Science 350 2015 56 64
103. T. Stuwe, A.R. Correia, D.H. Lin, M. Paduch, V.T. Lu, A.A. Kossiakoff, and A. Hoelz Nuclear pores. Architecture of the nuclear pore complex coat Science 347 2015 1148 1152
104. K. Tamura, Y. Fukao, M. Iwamoto, T. Haraguchi, and I. Hara-Nishimura Identification and characterization of nuclear pore complex components in Arabidopsis thaliana Plant Cell 22 2010 4084 4097
105. L.J. Terry, and S.R. Wente Flexible gates: dynamic topologies and functions for FG nucleoporins in nucleocytoplasmic transport Eukaryot. Cell 8 2009 1814 1827
106. G. Theerthagiri, N. Eisenhardt, H. Schwarz, and W. Antonin The nucleoporin Nup188 controls passage of membrane proteins across the nuclear pore complex J. Cell Biol. 189 2010 1129 1142
107. B.H. Toyama, J.N. Savas, S.K. Park, M.S. Harris, N.T. Ingolia, J.R. Yates 3rd, and M.W. Hetzer Identification of long-lived proteins reveals exceptional stability of essential cellular structures Cell 154 2013 971 982
108. A. Ulrich, J.R. Partridge, and T.U. Schwartz The stoichiometry of the nucleoporin 62 subcomplex of the nuclear pore in solution Mol. Biol. Cell 25 2014 1484 1492
109. R. Ungricht, and U. Kutay Establishment of NE asymmetry - targeting of membrane proteins to the inner nuclear membrane Curr. Opin. Cell Biol. 34 2015 135 141
110. R. Ungricht, M. Klann, P. Horvath, and U. Kutay Diffusion and retention are major determinants of protein targeting to the inner nuclear membrane J. Cell Biol. 209 2015 687 703
111. B. Vollmer, and W. Antonin The diverse roles of the Nup93/Nic96 complex proteins - structural scaffolds of the nuclear pore complex with additional cellular functions Biol. Chem. 395 2014 515 528
112. A. von Appen, J. Kosinski, L. Sparks, A. Ori, A.L. DiGuilio, B. Vollmer, M.-T. Mackmull, N. Banterle, L. Parca, P. Kastritis, and et al. In situ structural analysis of the human nuclear pore complex Nature 526 2015 140 143
113. T.C. Walther, A. Alves, H. Pickersgill, I. Loïodice, M. Hetzer, V. Galy, B.B. Hülsmann, T. Köcher, M. Wilm, T. Allen, and et al. The conserved Nup107-160 complex is critical for nuclear pore complex assembly Cell 113 2003 195 206
114. J.R.R. Whittle, and T.U. Schwartz Architectural nucleoporins Nup157/170 and Nup133 are structurally related and descend from a second ancestral element J. Biol. Chem. 284 2009 28442 28452
115. P. Wild, C. Senn, C.L. Manera, E. Sutter, E.M. Schraner, K. Tobler, M. Ackermann, U. Ziegler, M.S. Lucas, and A. Kaech Exploring the nuclear envelope of herpes simplex virus 1-infected cells by high-resolution microscopy J. Virol. 83 2009 408 419
116. C. Xu, Z. Li, H. He, A. Wernimont, Y. Li, P. Loppnau, and J. Min Crystal structure of human nuclear pore complex component NUP43 FEBS Lett. 589 2015 3247 3253
117. Q. Yang, M.P. Rout, and C.W. Akey Three-dimensional architecture of the isolated yeast nuclear pore complex: functional and evolutionary implications Mol. Cell 1 1998 223 234
118. G. Zanetti, K.B. Pahuja, S. Studer, S. Shim, and R. Schekman COPII and the regulation of protein sorting in mammals Nat. Cell Biol. 14 2012 20 28