The nuclear pore complex: understanding its function through structural insight (original) (raw)
Doye, V. & Hurt, E. C. From nucleoporins to nuclear pore complexes. Curr. Opin. Cell Biol.9, 401–411 (1997). ArticleCASPubMed Google Scholar
Rout, M. P. et al. The yeast nuclear pore complex: Composition, architecture, and transport mechanism. J. Cell Biol.148, 635–651 (2000). ArticleCASPubMedPubMed Central Google Scholar
Fahrenkrog, B. & Aebi, U. The nuclear pore complex: Nucleocytoplasmic transport and beyond. Nat. Rev. Mol. Cell Biol.4, 757–766 (2003). ArticleCASPubMed Google Scholar
Dickmanns, A., Kehlenbach, R. H. & Fahrenkrog, B. Nuclear pore complexes and nucleocytoplasmic transport: from structure to function to disease. Int. Rev. Cell Mol. Biol.320, 171–233 (2015). ArticleCASPubMed Google Scholar
Hurt, E. & Beck, M. Towards understanding nuclear pore complex architecture and dynamics in the age of integrative structural analysis. Curr. Opin. Cell Biol.34, 31–38 (2015). ArticleCASPubMed Google Scholar
von Appen, A. & Beck, M. Structure determination of the nuclear pore complex with three-dimensional cryo electron microscopy. J. Mol. Biol.428, 2001–2010 (2016). ArticleCASPubMedPubMed Central Google Scholar
Schwartz, T. U. Modularity within the architecture of the nuclear pore complex. Curr. Opin. Struct. Biol.15, 221–226 (2005). ArticleCASPubMed Google Scholar
Siniossoglou, S. et al. A novel complex of nucleoporins, which includes Sec13p and a Sec13p homolog, is essential for normal nuclear pores. Cell84, 265–275 (1996). ArticleCASPubMed Google Scholar
Walther, T. C. et al. The conserved Nup107–160 complex is critical for nuclear pore complex assembly. Cell113, 195–206 (2003). ArticleCASPubMed Google Scholar
Ulrich, A., Partridge, J. R. & Schwartz, T. U. The stoichiometry of the nucleoporin 62 subcomplex of the nuclear pore in solution. Mol. Biol. Cell25, 1484–1492 (2014). This work demonstrates a 1:1:1 stoichiometry of the NUP62 complex, but non-canonical stoichiometries when a coiled-coil partner is absent. ArticlePubMedPubMed Central Google Scholar
Amlacher, S. et al. Insight into structure and assembly of the nuclear pore complex by utilizing the genome of a eukaryotic thermophile. Cell146, 277–286 (2011). This study shows that NUPs from a eukaryotic thermophile have superior properties forin vitroreconstitution. ArticleCASPubMed Google Scholar
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). ArticleCASPubMedPubMed Central Google Scholar
Schellhaus, A. K., De Magistris, P. & Antonin, W. Nuclear reformation at the end of mitosis. J. Mol. Biol.428, 1962–1985 (2015). ArticlePubMedCAS Google Scholar
Gay, S. & Foiani, M. Nuclear envelope and chromatin, lock and key of genome integrity. Int. Rev. Cell Mol. Biol.317, 267–330 (2015). ArticleCASPubMed Google Scholar
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). ArticleCASPubMed Google Scholar
Pascual-Garcia, P. & Capelson, M. Nuclear pores as versatile platforms for gene regulation. Curr. Opin. Genet. Dev.25, 110–117 (2014). ArticleCASPubMed Google Scholar
Sood, V. & Brickner, J. H. Nuclear pore interactions with the genome. Curr. Opin. Genet. Dev.25, 43–49 (2014). ArticleCASPubMed Google Scholar
Light, W. H. & Brickner, J. H. Nuclear pore proteins regulate chromatin structure and transcriptional memory by a conserved mechanism. Nucleus4, 357–360 (2013). ArticlePubMedPubMed Central Google Scholar
Imamoto, N. & Funakoshi, T. Nuclear pore dynamics during the cell cycle. Curr. Opin. Cell Biol.24, 453–459 (2012). ArticleCASPubMed Google Scholar
Van de Vosse, D. W., Wan, Y., Wozniak, R. W. & Aitchison, J. D. Role of the nuclear envelope in genome organization and gene expression. Wiley Interdiscip. Rev. Syst. Biol. Med.3, 147–166 (2011). ArticleCASPubMedPubMed Central Google Scholar
Arib, G. & Akhtar, A. Multiple facets of nuclear periphery in gene expression control. Curr. Opin. Cell Biol.23, 346–353 (2011). ArticleCASPubMed Google Scholar
Liang, Y. & Hetzer, M. W. Functional interactions between nucleoporins and chromatin. Curr. Opin. Cell Biol.23, 65–70 (2011). ArticleCASPubMed Google Scholar
Kohler, A. & Hurt, E. Gene regulation by nucleoporins and links to cancer. Mol. Cell38, 6–15 (2010). ArticlePubMedCAS Google Scholar
Capelson, M., Doucet, C. & Hetzer, M. W. Nuclear pore complexes: Guardians of the nuclear genome. Cold Spring Harb. Symp. Quant. Biol.75, 585–597 (2010). ArticleCASPubMed Google Scholar
Callan, H. G., Randall, J. T. & Tomlin, S. G. An electron microscope study of the nuclear membrane. Nature163, 280–281 (1949). ArticleCASPubMed Google Scholar
Callan, H. G. & Tomlin, S. G. 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. B137, 367–378 (1950). ArticleCASPubMed Google Scholar
Afzelius, B. A. The ultrastructure of the nuclear membrane of the sea urchin oocyte as studied with the electron microscope. Exp. Cell Res.8, 147–158 (1955). ArticleCASPubMed Google Scholar
Dwyer, N. & Blobel, G. A modified procedure for isolation of a pore complex-lamina fraction from rat liver nuclei. J. Cell Biol.70, 581–591 (1976). ArticleCASPubMed Google Scholar
Aaronson, R. P. & Blobel, G. Isolation of nuclear pore complexes in association with a lamina. Proc. Natl Acad. Sci. USA72, 1007–1011 (1975). ArticleCASPubMedPubMed Central Google Scholar
Gerace, L., Ottaviano, Y. & Kondor-Koch, C. Identification of a major polypeptide of the nuclear pore complex. J. Cell Biol.95, 826–837 (1982). ArticleCASPubMed Google Scholar
Wozniak, R. W., Bartnik, E. & Blobel, G. Primary structure analysis of an integral membrane glycoprotein of the nuclear pore. J. Cell Biol.108, 2083–2092 (1989). ArticleCASPubMed Google Scholar
Greber, U. F., Senior, A. & Gerace, L. A major glycoprotein of the nuclear pore complex is a membrane-spanning polypeptide with a large luminal domain and a small cytoplasmic tail. EMBO J.9, 1495–1502 (1990). ArticleCASPubMedPubMed Central Google Scholar
Davis, L. I. & Blobel, G. Identification and characterization of a nuclear pore complex protein. Cell45, 699–709 (1986). ArticleCASPubMed Google Scholar
Snow, C. M., Senior, A. & Gerace, L. Monoclonal antibodies identify a group of nuclear pore complex glycoproteins. J. Cell Biol.104, 1143–1156 (1987). ArticleCASPubMed Google Scholar
Szymborska, A. et al. Nuclear pore scaffold structure analyzed by super-resolution microscopy and particle averaging. Science341, 655–658 (2013). ArticleCASPubMed Google Scholar
Uno, S. N. et al. A spontaneously blinking fluorophore based on intramolecular spirocyclization for live-cell super-resolution imaging. Nat. Chem.6, 681–689 (2014). ArticleCASPubMed Google Scholar
Loschberger, A., Franke, C., Krohne, G., van de Linde, S. & Sauer, M. Correlative super-resolution fluorescence and electron microscopy of the nuclear pore complex with molecular resolution. J. Cell Sci.127, 4351–4355 (2014). PubMed Google Scholar
Pleiner, T. et al. Nanobodies: Site-specific labeling for super-resolution imaging, rapid epitope-mapping and native protein complex isolation. eLife4, e11349 (2015). ArticlePubMedPubMed Central Google Scholar
Holt, G. D. & Hart, G. W. The subcellular distribution of terminal _N_-acetylglucosamine moieties. Localization of a novel protein-saccharide linkage, _O_-linked GlcNAc. J. Biol. Chem.261, 8049–8057 (1986). ArticleCASPubMed Google Scholar
Davis, L. I. & Blobel, G. Nuclear pore complex contains a family of glycoproteins that includes p62: Glycosylation through a previously unidentified cellular pathway. Proc. Natl Acad. Sci. USA84, 7552–7556 (1987). ArticleCASPubMedPubMed Central Google Scholar
Hanover, J. A., Cohen, C. K., Willingham, M. C. & Park, M. K. _O_-Linked _N_-acetylglucosamine is attached to proteins of the nuclear pore. Evidence for cytoplasmic and nucleoplasmic glycoproteins. J. Biol. Chem.262, 9887–9894 (1987). ArticleCASPubMed Google Scholar
Park, M. K., D'Onofrio, M., Willingham, M. C. & Hanover, J. A. A monoclonal antibody against a family of nuclear pore proteins (nucleoporins): _O_-linked _N_-acetylglucosamine is part of the immunodeterminant. Proc. Natl Acad. Sci. USA84, 6462–6466 (1987). ArticleCASPubMedPubMed Central Google Scholar
Finlay, D. R., Newmeyer, D. D., Price, T. M. & Forbes, D. J. Inhibition of in vitro nuclear transport by a lectin that binds to nuclear pores. J. Cell Biol.104, 189–200 (1987). ArticleCASPubMed Google Scholar
Dabauvalle, M. C., Benavente, R. & Chaly, N. Monoclonal antibodies to a Mr 68,000 pore complex glycoprotein interfere with nuclear protein uptake in Xenopus oocytes. Chromosoma97, 193–197 (1988). ArticleCASPubMed Google Scholar
Dabauvalle, M. C., Schulz, B., Scheer, U. & Peters, R. Inhibition of nuclear accumulation of karyophilic proteins in living cells by microinjection of the lectin wheat germ agglutinin. Exp. Cell Res.174, 291–296 (1988). ArticleCASPubMed Google Scholar
Yoneda, Y., Imamoto-Sonobe, N., Yamaizumi, M. & Uchida, T. Reversible inhibition of protein import into the nucleus by wheat germ agglutinin injected into cultured cells. Exp. Cell Res.173, 586–595 (1987). ArticleCASPubMed Google Scholar
Hurt, E. C. A novel nucleoskeletal-like protein located at the nuclear periphery is required for the life cycle of Saccharomyces cerevisiae. EMBO J.7, 4323–4334 (1988). ArticleCASPubMedPubMed Central Google Scholar
Nehrbass, U. et al. NSP1: A yeast nuclear envelope protein localized at the nuclear pores exerts its essential function by its carboxy-terminal domain. Cell61, 979–989 (1990). ArticleCASPubMed Google Scholar
Davis, L. I. & Fink, G. R. The NUP1 gene encodes an essential component of the yeast nuclear pore complex. Cell61, 965–978 (1990). ArticleCASPubMed Google Scholar
Wente, S. R., Rout, M. P. & Blobel, G. A new family of yeast nuclear pore complex proteins. J. Cell Biol.119, 705–723 (1992). ArticleCASPubMed Google Scholar
Wimmer, C., Doye, V., Grandi, P., Nehrbass, U. & Hurt, E. C. A new subclass of nucleoporins that functionally interacts with nuclear pore protein NSP1. EMBO J.11, 5051–5061 (1992). ArticleCASPubMedPubMed Central Google Scholar
Doye, V. & Hurt, E. C. Genetic approaches to nuclear pore structure and function. Trends Genet.11, 235–241 (1995). ArticleCASPubMed Google Scholar
Grandi, P., Doye, V. & Hurt, E. C. Purification of NSP1 reveals complex formation with 'GLFG' nucleoporins and a novel nuclear pore protein NIC96. EMBO J.12, 3061–3071 (1993). ArticleCASPubMedPubMed Central Google Scholar
Miller, B. R., Powers, M., Park, M., Fischer, W. & Forbes, D. J. Identification of a new vertebrate nucleoporin, Nup188, with the use of a novel organelle trap assay. Mol. Biol. Cell11, 3381–3936 (2000). ArticleCASPubMedPubMed Central Google Scholar
Sukegawa, J. C. & Blobel, G. A nuclear pore complex protein that contains zinc finger motifs, binds DNA, and faces the nucleoplasm. Cell72, 29–38 (1993). ArticleCASPubMed Google Scholar
Powers, M. A., Forbes, D. J., Dahlberg, J. E. & Lund, E. The vertebrate GLFG nucleoporin, Nup98, is an essential component of multiple RNA export pathways. J. Cell Biol.136, 241–250 (1997). ArticleCASPubMedPubMed Central Google Scholar
Grandi, P. et al. Nup93, a vertebrate homologue of yeast Nic96p, forms a complex with a novel 205-kDa protein and is required for correct nuclear pore assembly. Mol. Biol. Cell8, 2017–2038 (1997). ArticleCASPubMedPubMed Central Google Scholar
Rout, M. P. & Blobel, G. Isolation of the yeast nuclear pore complex. J. Cell Biol.123, 771–783 (1993). ArticleCASPubMed Google Scholar
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). ArticleCASPubMedPubMed Central Google Scholar
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). ArticleCASPubMed Google Scholar
Finlay, D. R., Meier, E., Bradley, P., Horecka, J. & Forbes, D. J. A complex of nuclear pore proteins required for pore function. J. Cell Biol.114, 169–183 (1991). ArticleCASPubMed Google Scholar
Dabauvalle, M. C., Loos, K. & Scheer, U. Identification of a soluble precursor complex essential for nuclear pore assembly. Chromosoma100, 56–66 (1990). ArticleCASPubMed Google Scholar
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). ArticleCASPubMedPubMed Central Google Scholar
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). ArticleCASPubMedPubMed Central Google Scholar
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). This investigation reveals the crystal structure of the central hub of theMyceliophthora thermophilaY-complex. ArticleCASPubMedPubMed Central Google Scholar
Stuwe, T. et al. Architecture of the nuclear pore complex coat. Science347, 1148–1152 (2015). This study reports the crystal structure of the yeastS. cerevisiaehexameric Y-complex. ArticleCASPubMedPubMed Central Google Scholar
Goldberg, M. W., Wiese, C., Allen, T. D. & Wilson, K. L. Dimples, pores, star-rings, and thin rings on growing nuclear envelopes: Evidence for structural intermediates in nuclear pore complex assembly. J. Cell Sci.110, 409–420 (1997). ArticleCASPubMed Google Scholar
Goldberg, M. W. & Allen, T. D. 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, 1429–1440 (1992). ArticleCASPubMed Google Scholar
Jarnik, M. & Aebi, U. Toward a more complete 3D structure of the nuclear pore complex. J. Struct. Biol.107, 291–308 (1991). ArticleCASPubMed Google Scholar
Ris, H. & Malecki, M. 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, 148–157 (1993). ArticleCASPubMed Google Scholar
Reichelt, R. et al. Correlation between structure and mass distribution of nuclear pore complex components. J. Cell Biol.110, 883–894 (1990). ArticleCASPubMed Google Scholar
Hinshaw, J. E., Carragher, B. O. & Milligan, R. A. Architecture and design of the nuclear pore complex. Cell69, 1133–1141 (1992). ArticleCASPubMed Google Scholar
Pante, N., Bastos, R., McMorrow, I., Burke, B. & Aebi, U. Interactions and three-dimensional localization of a group of nuclear pore complex proteins. J. Cell Biol.126, 603–617 (1994). ArticleCASPubMed Google Scholar
Alber, F. et al. The molecular architecture of the nuclear pore complex. Nature450, 695–701 (2007). ArticleCASPubMed Google Scholar
Unwin, P. N. & Milligan, R. A. A large particle associated with the perimeter of the nuclear pore complex. J. Cell Biol.93, 63–75 (1982). ArticleCASPubMed Google Scholar
Akey, C. W. & Radermacher, M. Architecture of the Xenopus nuclear pore complex revealed by three-dimensional cryo-electron microscopy. J. Cell Biol.122, 1–19 (1993). ArticleCASPubMed Google Scholar
Akey, C. W. Structural plasticity of the nuclear pore complex. J. Mol. Biol.248, 273–293 (1995). CASPubMed Google Scholar
Stoffler, D. et al. Cryo-electron tomography provides novel insights into nuclear pore architecture: implications for nucleocytoplasmic transport. J. Mol. Biol.328, 119–130 (2003). ArticleCASPubMed Google Scholar
Beck, M. et al. Nuclear pore complex structure and dynamics revealed by cryoelectron tomography. Science306, 1387–1390 (2004). ArticleCASPubMed Google Scholar
Beck, M., Lucic, V., Forster, F., Baumeister, W. & Medalia, O. Snapshots of nuclear pore complexes in action captured by cryo-electron tomography. Nature449, 611–615 (2007). ArticleCASPubMed Google Scholar
Maimon, T., Elad, N., Dahan, I. & Medalia, O. The human nuclear pore complex as revealed by cryo-electron tomography. Structure20, 998–1006 (2012). ArticleCASPubMed Google Scholar
Hodel, A. et al. The three-dimensional structure of the autoproteolytic, nuclear pore-targeting domain of the human nucleoporin Nup98. Mol. Cell10, 347–358 (2002). ArticleCASPubMed Google Scholar
Hoelz, A., Debler, E. W. & Blobel, G. The structure of the nuclear pore complex. Annu. Rev. Biochem.80, 613–643 (2011). ArticleCASPubMed Google Scholar
Berka, R. M. et al. Comparative genomic analysis of the thermophilic biomass-degrading fungi Myceliophthora thermophila and Thielavia terrestris. Nat. Biotechnol.29, 922–927 (2011). ArticleCASPubMed Google Scholar
Andersen, K. R. et al. Scaffold nucleoporins Nup188 and Nup192 share structural and functional properties with nuclear transport receptors. eLife2, e00745 (2013). This paper shows that large scaffold NUPs, whose crystal structures could be obtained, can bind to FG-NUPs and translocate through NPCs by facilitated diffusion. ArticlePubMedPubMed CentralCAS Google Scholar
Frey, S., Richter, R. P. & Gorlich, D. FG-rich repeats of nuclear pore proteins form a three-dimensional meshwork with hydrogel-like properties. Science314, 815–817 (2006). ArticleCASPubMed Google Scholar
Lim, R. Y. et al. Nanomechanical basis of selective gating by the nuclear pore complex. Science318, 640–643 (2007). ArticleCASPubMed Google Scholar
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). ArticleCASPubMedPubMed Central Google Scholar
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. USA108, 16571–16576 (2011). The authors report the crystal structure of a cytoplasmically oriented NUP complex, clarifying the mode of NUP interactions. ArticleCASPubMedPubMed Central Google Scholar
Matsuura, Y., Lange, A., Harreman, M. T., Corbett, A. H. & Stewart, M. Structural basis for Nup2p function in cargo release and karyopherin recycling in nuclear import. EMBO J.22, 5358–5369 (2003). ArticleCASPubMedPubMed Central Google Scholar
Schrader, N. et al. The crystal structure of the Ran–Nup153ZnF2 complex: A general Ran docking site at the nuclear pore complex. Structure16, 1116–1125 (2008). ArticleCASPubMed Google Scholar
Görlich, D., Prehn, S., Laskey, R. A. & Hartmann, E. Isolation of a protein that is essential for the first step of nuclear protein import. Cell79, 767–778 (1994). ArticlePubMed Google Scholar
Imamoto, N., Tachibana, T., Matsubae, M. & Yoneda, Y. A karyophilic protein forms a stable complex with cytoplasmic components prior to nuclear pore binding. J. Biol. Chem.270, 8559–8565 (1995). ArticleCASPubMed Google Scholar
Radu, A., Blobel, G. & Moore, M. S. Identification of a protein complex that is required for nuclear protein import and mediates docking of import substrate to distinct nucleoporins. Proc. Natl Acad. Sci. USA92, 1769–1773 (1995). ArticleCASPubMedPubMed Central Google Scholar
Moore, M. S. & Blobel, G. The GTP-binding protein Ran/TC4 is required for protein import into the nucleus. Nature365, 661–663 (1993). ArticleCASPubMed Google Scholar
Melchior, F., Paschal, B., Evans, J. & Gerace, L. Inhibition of nuclear protein import by nonhydrolyzable analogues of GTP and identification of the small GTPase Ran/TC4 as an essential transport factor. J. Cell Biol.123, 1649–1659 (1993). ArticleCASPubMed Google Scholar
Kutay, U., Bischoff, F. R., Kostka, S., Kraft, R. & Görlich, D. Export of importin α from the nucleus is mediated by a specific nuclear transport factor. Cell90, 1061–1071 (1997). ArticleCASPubMed Google Scholar
Gorlich, D. & Kutay, U. Transport between the cell nucleus and the cytoplasm. Annu. Rev. Cell Dev. Biol.15, 607–660 (1999). ArticleCASPubMed Google Scholar
Rexach, M. & Blobel, G. Protein import into nuclei: Association and dissociation reactions involving transport substrate, transport factors, and nucleoporins. Cell83, 683–692 (1995). ArticleCASPubMed Google Scholar
Schmidt, H. B. & Gorlich, D. Transport selectivity of nuclear pores, phase separation, and membraneless organelles. Trends Biochem. Sci.41, 46–61 (2016). ArticleCASPubMed Google Scholar
Rout, M. P., Aitchison, J. D., Magnasco, M. O. & Chait, B. T. Virtual gating and nuclear transport: The hole picture. Trends Cell Biol.13, 622–628 (2003). ArticleCASPubMed Google Scholar
Sakiyama, Y., Mazur, A., Kapinos, L. E. & Lim, R. Y. Spatiotemporal dynamics of the nuclear pore complex transport barrier resolved by high-speed atomic force microscopy. Nat. Nanotechnol.11, 719–723 (2016). ArticleCASPubMed Google Scholar
Hyman, A. A., Weber, C. A. & Julicher, F. Liquid–liquid phase separation in biology. Annu. Rev. Cell Dev. Biol.30, 39–58 (2014). ArticleCASPubMed Google Scholar
Milles, S. et al. Plasticity of an ultrafast interaction between nucleoporins and nuclear transport receptors. Cell163, 734–745 (2015). ArticleCASPubMedPubMed Central Google Scholar
Raveh, B. et al. Slide-and-exchange mechanism for rapid and selective transport through the nuclear pore complex. Proc. Natl Acad. Sci. USA113, E2489–E2497 (2016). ArticleCASPubMedPubMed Central Google Scholar
Strawn, L. A., Shen, T., Shulga, N., Goldfarb, D. S. & Wente, S. R. Minimal nuclear pore complexes define FG repeat domains essential for transport. Nat. Cell Biol.6, 197–206 (2004). ArticleCASPubMed Google Scholar
Schrader, N. et al. Structural basis of the Nic96 subcomplex organization in the nuclear pore channel. Mol. Cell29, 46–55 (2008). ArticleCASPubMed Google Scholar
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). ArticleCASPubMedPubMed Central Google Scholar
Devos, D. et al. Components of coated vesicles and nuclear pore complexes share a common molecular architecture. PLoS Biol.2, e380 (2004). ArticlePubMedPubMed CentralCAS Google Scholar
Chug, H., Trakhanov, S., Hulsmann, B. B., Pleiner, T. & Gorlich, D. Crystal structure of the metazoan Nup62–Nup58–Nup54 nucleoporin complex. Science350, 106–110 (2015). ArticleCASPubMed Google Scholar
Stuwe, T. et al. Architecture of the fungal nuclear pore inner ring complex. Science350, 56–64 (2015). References 122 and 123 reveal the crystal structures of the NUP62 and Nsp1 channel complexes fromX. laevisandC thermophilum, respectively. ArticleCASPubMedPubMed Central Google Scholar
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). The authors develop an integrated 3D structural model of the Nup82 complex and propose how it embeds into the NPC scaffold, showing that it projects towards the central channel in agreement with reference 125. ArticlePubMedPubMed CentralCAS Google Scholar
Bui, K. H. et al. Integrated structural analysis of the human nuclear pore complex scaffold. Cell155, 1233–1243 (2013). ArticleCASPubMed Google Scholar
Marelli, M., Lusk, C. P., Chan, H., Aitchison, J. D. & Wozniak, R. W. A link between the synthesis of nucleoporins and the biogenesis of the nuclear envelope. J. Cell Biol.153, 709–724 (2001). ArticleCASPubMedPubMed Central Google Scholar
Drin, G. et al. A general amphipathic α-helical motif for sensing membrane curvature. Nat. Struct. Mol. Biol.14, 138–146 (2007). ArticleCASPubMed Google Scholar
Doucet, C. M., Esmery, N., de Saint-Jean, M. & Antonny, B. Membrane curvature sensing by amphipathic helices is modulated by the surrounding protein backbone. PLoS ONE10, e0137965 (2015). ArticlePubMedPubMed CentralCAS Google Scholar
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. Proteomics13, 2911–2926 (2014). ArticleCASPubMedPubMed Central Google Scholar
Meszaros, N. et al. Nuclear pore basket proteins are tethered to the nuclear envelope and can regulate membrane curvature. Dev. Cell33, 285–298 (2015). ArticleCASPubMedPubMed Central Google Scholar
Vollmer, B. et al. Nup153 recruits the Nup107–160 complex to the inner nuclear membrane for interphasic nuclear pore complex assembly. Dev. Cell33, 717–728 (2015). ArticleCASPubMed Google Scholar
Vollmer, B. et al. Dimerization and direct membrane interaction of Nup53 contribute to nuclear pore complex assembly. EMBO J.31, 4072–4084 (2012). References 130–132 report the membrane anchoring of NUPs and NUP complexes to the nuclear envelope and the role of this anchoring in the regulation of membrane curvature. ArticleCASPubMedPubMed Central Google Scholar
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). ArticleCASPubMedPubMed Central Google Scholar
Madrid, A. S., Mancuso, J., Cande, W. Z. & Weis, K. The role of the integral membrane nucleoporins Ndc1p and Pom152p in nuclear pore complex assembly and function. J. Cell Biol.173, 361–371 (2006). ArticleCASPubMedPubMed Central Google Scholar
Liu, H. L., De Souza, C. P., Osmani, A. H. & Osmani, S. A. The three fungal transmembrane nuclear pore complex proteins of Aspergillus nidulans are dispensable in the presence of an intact An-Nup84–120 complex. Mol. Biol. Cell20, 616–630 (2009). ArticlePubMedPubMed Central Google Scholar
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). ArticleCASPubMedPubMed Central Google Scholar
Miao, M., Ryan, K. J. & Wente, S. R. The integral membrane protein Pom34p functionally links nucleoporin subcomplexes. Genetics172, 1441–1457 (2006). ArticleCASPubMedPubMed Central Google Scholar
Fischer, J., Teimer, R., Amlacher, S., Kunze, R. & Hurt, E. Linker Nups connect the nuclear pore complex inner ring with the outer ring and transport channel. Nat. Struct. Mol. Biol.22, 774–781 (2015). This work describes thein vitroreconstitution of a large part of the NPC protomer, a process that depended on SLMs within linker NUPs. ArticleCASPubMed Google Scholar
Lin, D. H. et al. Architecture of the symmetric core of the nuclear pore. Science352, aaf1015 (2016). This study reports the X-ray structure of scaffold NUPs with bound SLMs from linker NUPs and the docking of these structures into the tomographic map of the human NPC. ArticlePubMedPubMed CentralCAS Google Scholar
Laurell, E. et al. Phosphorylation of Nup98 by multiple kinases is crucial for NPC disassembly during mitotic entry. Cell144, 539–550 (2011). This study demonstrates that mitotic phosphorylation of the linker NUP NUP98 in human cells induces disintegration of the NPC during prophase. ArticleCASPubMed Google Scholar
Onischenko, E. A., Gubanova, N. V., Kiseleva, E. V. & Hallberg, E. Cdk1 and okadaic acid-sensitive phosphatases control assembly of nuclear pore complexes in Drosophila embryos. Mol. Biol. Cell16, 5152–5162 (2005). ArticleCASPubMedPubMed Central Google Scholar
Hattersley, N. et al. A nucleoporin docks protein phosphatase 1 to direct meiotic chromosome segregation and nuclear assembly. Dev. Cell38, 463–477 (2016). ArticleCASPubMedPubMed Central Google Scholar
Raab, M. et al. ESCRT III repairs nuclear envelope ruptures during cell migration to limit DNA damage and cell death. Science352, 359–362 (2016). ArticleCASPubMed Google Scholar
Kim, D. I. et al. Probing nuclear pore complex architecture with proximity-dependent biotinylation. Proc. Natl Acad. Sci. USA111, E2453–E2461 (2014). ArticleCASPubMedPubMed Central Google Scholar
Damelin, M. & Silver, P. A. In situ analysis of spatial relationships between proteins of the nuclear pore complex. Biophys. J.83, 3626–3636 (2002). ArticleCASPubMedPubMed Central Google Scholar
Krull, S., Thyberg, J., Bjorkroth, B., Rackwitz, H. R. & Cordes, V. C. Nucleoporins as components of the nuclear pore complex core structure and Tpr as the architectural element of the nuclear basket. Mol. Biol. Cell15, 4261–4277 (2004). ArticleCASPubMedPubMed Central Google Scholar
Fahrenkrog, B. et al. Domain-specific antibodies reveal multiple-site topology of Nup153 within the nuclear pore complex. J. Struct. Biol.140, 254–267 (2002). ArticleCASPubMed Google Scholar
Otsuka, S., Szymborska, A. & Ellenberg, J. Imaging the assembly, structure, and function of the nuclear pore inside cells. Methods Cell Biol.122, 219–238 (2014). ArticleCASPubMed Google Scholar
Krull, S. et al. Protein Tpr is required for establishing nuclear pore-associated zones of heterochromatin exclusion. EMBO J.29, 1659–1673 (2010). ArticleCASPubMedPubMed Central Google Scholar
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.18, 643–649 (2011). ArticleCASPubMedPubMed Central Google Scholar
Ori, A., Andres-Pons, A. & Beck, M. The use of targeted proteomics to determine the stoichiometry of large macromolecular assemblies. Methods Cell Biol.122, 117–146 (2014). ArticleCASPubMed Google Scholar
Olinares, P. D. et al. A robust workflow for native mass spectrometric analysis of affinity-isolated endogenous protein assemblies. Anal. Chem.88, 2799–2807 (2016). ArticleCASPubMedPubMed Central Google Scholar
Mi, L., Goryaynov, A., Lindquist, A., Rexach, M. & Yang, W. Quantifying nucleoporin stoichiometry inside single nuclear pore complexes in vivo. Sci. Rep.5, 9372 (2015). ArticleCASPubMedPubMed Central Google Scholar
Asakawa, H. et al. Characterization of nuclear pore complex components in fission yeast Schizosaccharomyces pombe. Nucleus5, 149–162 (2014). ArticlePubMedPubMed Central Google Scholar
Eibauer, M. et al. Structure and gating of the nuclear pore complex. Nat. Commun.6, 7532 (2015). ArticleCASPubMed Google Scholar
Alber, F. et al. Determining the architectures of macromolecular assemblies. Nature450, 683–694 (2007). ArticleCASPubMed Google Scholar
Seo, H. S. et al. Structural and functional analysis of Nup120 suggests ring formation of the Nup84 complex. Proc. Natl Acad. Sci. USA106, 14281–14286 (2009). ArticleCASPubMedPubMed Central Google Scholar
Dodonova, S. O. et al. A structure of the COPI coat and the role of coat proteins in membrane vesicle assembly. Science349, 195–198 (2015). ArticleCASPubMed Google Scholar
Sharma, A., Solmaz, S. R., Blobel, G. & Melcak, I. Ordered regions of channel nucleoporins NUP62, NUP54, and NUP58 form dynamic complexes in solution. J. Biol. Chem.290, 18370–18378 (2015). ArticleCASPubMedPubMed Central Google Scholar
Solmaz, S. R., Chauhan, R., Blobel, G. & Melcak, I. Molecular architecture of the transport channel of the nuclear pore complex. Cell147, 590–602 (2011). ArticleCASPubMedPubMed Central Google Scholar
Koh, J. & Blobel, G. Allosteric regulation in gating the central channel of the nuclear pore complex. Cell161, 1361–1373 (2015). ArticleCASPubMed Google Scholar
Debler, E. W. et al. A fence-like coat for the nuclear pore membrane. Mol. Cell32, 815–826 (2008). ArticleCASPubMed Google Scholar
Colombi, P., Webster, B. M., Frohlich, F. & Lusk, C. P. The transmission of nuclear pore complexes to daughter cells requires a cytoplasmic pool of Nsp1. J. Cell Biol.203, 215–232 (2013). ArticleCASPubMedPubMed Central Google Scholar
Kubitscheck, U. et al. Nuclear transport of single molecules: dwell times at the nuclear pore complex. J. Cell Biol.168, 233–243 (2005). ArticlePubMedPubMed CentralCAS Google Scholar
Musser, S. M. & Grunwald, D. Deciphering the structure and function of nuclear pores using single-molecule fluorescence approaches. J. Mol. Biol.428, 2091–2119 (2016). ArticleCASPubMedPubMed Central Google Scholar
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. USA110, 16450–16455 (2013). ArticleCASPubMedPubMed Central Google Scholar
Kerscher, O., Hieter, P., Winey, M. & Basrai, M. A. Novel role for a Saccharomyces cerevisiae nucleoporin, Nup170p, in chromosome segregation. Genetics157, 1543–1553 (2001). ArticleCASPubMedPubMed Central Google Scholar
Mor, A., White, M. A. & Fontoura, B. M. Nuclear trafficking in health and disease. Curr. Opin. Cell Biol.28, 28–35 (2014). ArticleCASPubMed Google Scholar
Miyake, N. et al. Biallelic mutations in nuclear pore complex subunit NUP107 cause early-childhood-onset steroid-resistant nephrotic syndrome. Am. J. Hum. Genet.97, 555–566 (2015). ArticleCASPubMedPubMed Central Google Scholar
Braun, D. A. et al. Mutations in nuclear pore genes NUP93, NUP205 and XPO5 cause steroid-resistant nephrotic syndrome. Nat. Genet.48, 457–465 (2016). ArticleCASPubMedPubMed Central Google Scholar
Doucet, C. M., Talamas, J. A. & Hetzer, M. W. Cell cycle-dependent differences in nuclear pore complex assembly in metazoa. Cell141, 1030–1041 (2010). ArticleCASPubMedPubMed Central Google Scholar
Weinberg-Shukron, A. et al. A mutation in the nucleoporin-107 gene causes XX gonadal dysgenesis. J. Clin. Invest.125, 4295–4304 (2015). References 175, 176 and 178 show that point mutations in housekeeping NUPs can cause specific human diseases. ArticlePubMedPubMed Central Google Scholar
DeGrasse, J. A. et al. Evidence for a shared nuclear pore complex architecture that is conserved from the last common eukaryotic ancestor. Mol. Cell. Proteomics8, 2119–2130 (2009). ArticleCASPubMedPubMed Central Google Scholar
Marsh, J. A. & Teichmann, S. A. Structure, dynamics, assembly, and evolution of protein complexes. Annu. Rev. Biochem.84, 551–575 (2015). ArticleCASPubMed Google Scholar
Tamura, K., Fukao, Y., Iwamoto, M., Haraguchi, T. & Hara-Nishimura, I. Identification and characterization of nuclear pore complex components in Arabidopsis thaliana. Plant Cell22, 4084–4097 (2010). ArticleCASPubMedPubMed Central Google Scholar
Asakawa, H. et al. Uncleavable Nup98–Nup96 is functional in the fission yeast Schizosaccharomyces pombe. FEBS Open Bio5, 508–514 (2015). ArticleCASPubMedPubMed Central Google Scholar
Wong, C. C., Traynor, D., Basse, N., Kay, R. R. & Warren, A. J. Defective ribosome assembly in Shwachman–Diamond syndrome. Blood118, 4305–4312 (2011). ArticleCASPubMed Google Scholar