The diverse roles of the Nup93/Nic96 complex proteins – structural scaffolds of the nuclear pore complex with additional cellular functions

References

Adams, R.L. and Wente, S.R. (2013). Uncovering nuclear pore complexity with innovation. Cell 152, 1218–1221.10.1016/j.cell.2013.02.042Suche in Google Scholar PubMed PubMed Central

Ahmed, S., Brickner, D.G., Light, W.H., Cajigas, I., McDonough, M., Froyshteter, A.B., Volpe, T., and Brickner, J.H. (2010). DNA zip codes control an ancient mechanism for gene targeting to the nuclear periphery. Nat. Cell. Biol. 12, 111–118.10.1038/ncb2011Suche in Google Scholar PubMed PubMed Central

Aitchison, J.D., Rout, M.P., Marelli, M., Blobel, G., and Wozniak, R.W. (1995). Two novel related yeast nucleoporins Nup170p and Nup157p: complementation with the vertebrate homologue Nup155p and functional interactions with the yeast nuclear pore-membrane protein Pom152p. J. Cell Biol. 131, 1133–1148.10.1083/jcb.131.5.1133Suche in Google Scholar PubMed PubMed Central

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. (2007a). Determining the architectures of macromolecular assemblies. Nature 450, 683–694.10.1038/nature06404Suche in Google Scholar PubMed

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. (2007b). The molecular architecture of the nuclear pore complex. Nature 450, 695–701.10.1038/nature06405Suche in Google Scholar PubMed

Allende, M.L., Amsterdam, A., Becker, T., Kawakami, K., Gaiano, N., and Hopkins, N. (1996). Insertional mutagenesis in zebrafish identifies two novel genes, pescadillo and dead eye, essential for embryonic development. Genes Dev. 10, 3141–3155.10.1101/gad.10.24.3141Suche in Google Scholar PubMed

Amlacher, S., Sarges, P., Flemming, D., van Noort, V., Kunze, R., Devos, D.P., Arumugam, M., Bork, P., and Hurt, E. (2011). Insight into structure and assembly of the nuclear pore complex by utilizing the genome of a eukaryotic thermophile. Cell 146, 277–289.10.1016/j.cell.2011.06.039Suche in Google Scholar PubMed

Andersen, K.R., Onischenko, E., Tang, J.H., Kumar, P., Chen, J.Z., Ulrich, A., Liphardt, J.T., Weis, K., and Schwartz, T.U. (2013). Scaffold nucleoporins Nup188 and Nup192 share structural and functional properties with nuclear transport receptors. eLife 2, e00745.10.7554/eLife.00745.016Suche in Google Scholar

Antonin, W. (2009). Nuclear envelope: membrane bending for pore formation? Curr. Biol. 19, R410–412.10.1016/j.cub.2009.03.053Suche in Google Scholar PubMed

Antonin, W., Ungricht, R., and Kutay, U. (2011). Traversing the NPC along the pore membrane: Targeting of membrane proteins to the INM. Nucleus 2, 87–91.10.4161/nucl.2.2.14637Suche in Google Scholar PubMed PubMed Central

Bilokapic, S. and Schwartz, T.U. (2012). 3D ultrastructure of the nuclear pore complex. Curr. Opin. Cell. Biol. 24, 86–91.10.1016/j.ceb.2011.12.011Suche in Google Scholar PubMed PubMed Central

Brohawn, S.G., Leksa, N.C., Spear, E.D., Rajashankar, K.R., and Schwartz, T.U. (2008). Structural evidence for common ancestry of the nuclear pore complex and vesicle coats. Science 322, 1369–1373.10.1126/science.1165886Suche in Google Scholar PubMed PubMed Central

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. (2013). Integrated structural analysis of the human nuclear pore complex scaffold. Cell 155, 1233–1243.10.1016/j.cell.2013.10.055Suche in Google Scholar PubMed

Busayavalasa, K., Chen, X., Farrants, A.K., Wagner, N., and Sabri, N. (2012). The Nup155-mediated organisation of inner nuclear membrane proteins is independent of Nup155 anchoring to the metazoan nuclear pore complex. J. Cell Sci. 125, 4214–4218.Suche in Google Scholar

Cairo, L.V., Ptak, C., and Wozniak, R.W. (2013). Mitosis-specific regulation of nuclear transport by the spindle assembly checkpoint protein Mad1p. Mol. Cell 49, 109–120.10.1016/j.molcel.2012.10.017Suche in Google Scholar PubMed

Chen, X. and Xu, L. (2010). Specific nucleoporin requirement for Smad nuclear translocation. Mol. Cell Biol. 30, 4022–4034.10.1128/MCB.00124-10Suche in Google Scholar PubMed PubMed Central

Chen, X.Q., Du, X., Liu, J., Balasubramanian, M.K., and Balasundaram, D. (2004). Identification of genes encoding putative nucleoporins and transport factors in the fission yeast Schizosaccharomyces pombe: a deletion analysis. Yeast 21, 495–509.10.1002/yea.1115Suche in Google Scholar PubMed

Dawson, T.R., Lazarus, M.D., Hetzer, M.W., and Wente, S.R. (2009). E.R. membrane-bending proteins are necessary for de novo nuclear pore formation. J. Cell. Biol. 184, 659–675.10.1083/jcb.200806174Suche in Google Scholar PubMed PubMed Central

DeGrasse, J.A., DuBois, K.N., Devos, D., Siegel, T.N., Sali, A., Field, M.C., Rout, M.P., and Chait, B.T. (2009). Evidence for a shared nuclear pore complex architecture that is conserved from the last common eukaryotic ancestor. Mol. Cell. Proteomics 8, 2119–2130.10.1074/mcp.M900038-MCP200Suche in Google Scholar PubMed PubMed Central

Deng, M. and Hochstrasser, M. (2006). Spatially regulated ubiquitin ligation by an ER/nuclear membrane ligase. Nature 443, 827–831.10.1038/nature05170Suche in Google Scholar PubMed

Dephoure, N., Zhou, C., Villen, J., Beausoleil, S.A., Bakalarski, C.E., Elledge, S.J., and Gygi, S.P. (2008). A quantitative atlas of mitotic phosphorylation. Proc. Natl. Acad. Sci. USA 105, 10762–10767.10.1073/pnas.0805139105Suche in Google Scholar PubMed PubMed Central

Devos, D., Dokudovskaya, S., Alber, F., Williams, R., Chait, B.T., Sali, A., and Rout, M.P. (2004). Components of coated vesicles and nuclear pore complexes share a common molecular architecture. PLoS Biol 2, e380.10.1371/journal.pbio.0020380Suche in Google Scholar PubMed PubMed Central

Doucet, C.M., Talamas, J.A., and Hetzer, M.W. (2010). Cell cycle-dependent differences in nuclear pore complex assembly in metazoa. Cell 141, 1030–1041.10.1016/j.cell.2010.04.036Suche in Google Scholar PubMed PubMed Central

Dultz, E., Zanin, E., Wurzenberger, C., Braun, M., Rabut, G., Sironi, L., and Ellenberg, J. (2008). Systematic kinetic analysis of mitotic dis- and reassembly of the nuclear pore in living cells. J. Cell. Biol. 180, 857–865.10.1083/jcb.200707026Suche in Google Scholar PubMed PubMed Central

Eisenhardt, N., Redolfi, J., and Antonin, W. (2014). Interaction of Nup53 with Ndc1 and Nup155 is required for nuclear pore complex assembly. J. Cell Sci. 127, 908–921.Suche in Google Scholar

Fahrenkrog, B., Hubner, W., Mandinova, A., Pante, N., Keller, W., and Aebi, U. (2000). The yeast nucleoporin Nup53p specifically interacts with Nic96p and is directly involved in nuclear protein import. Mol. Biol. Cell 11, 3885–3896.10.1091/mbc.11.11.3885Suche in Google Scholar PubMed PubMed Central

Flemming, D., Sarges, P., Stelter, P., Hellwig, A., Bottcher, B., and Hurt, E. (2009). Two structurally distinct domains of the nucleoporin Nup170 cooperate to tether a subset of nucleoporins to nuclear pores. J. Cell Biol. 185, 387–395.10.1083/jcb.200810016Suche in Google Scholar PubMed PubMed Central

Flemming, D., Devos, D.P., Schwarz, J., Amlacher, S., Lutzmann, M., and Hurt, E. (2012). Analysis of the yeast nucleoporin Nup188 reveals a conserved S-like structure with similarity to karyopherins. J. Struct. Biol. 177, 99–105.10.1016/j.jsb.2011.11.008Suche in Google Scholar PubMed

Franz, C., Askjaer, P., Antonin, W., Iglesias, C.L., Haselmann, U., Schelder, M., de Marco, A., Wilm, M., Antony, C., and Mattaj, I.W. (2005). Nup155 regulates nuclear envelope and nuclear pore complex formation in nematodes and vertebrates. EMBO J. 24, 3519–3531.10.1038/sj.emboj.7600825Suche in Google Scholar PubMed PubMed Central

Fried, H. and Kutay, U. (2003). Nucleocytoplasmic transport: taking an inventory. Cell. Mol. Life Sci. 60, 1659–1688.10.1007/s00018-003-3070-3Suche in Google Scholar PubMed

Galy, V., Mattaj, I.W., and Askjaer, P. (2003). Caenorhabditis elegans nucleoporins Nup93 and Nup205 determine the limit of nuclear pore complex size exclusion in vivo. Mol. Biol. Cell 14, 5104–5115.10.1091/mbc.e03-04-0237Suche in Google Scholar PubMed PubMed Central

Gant, T.M. and Wilson, K.L. (1997). Nuclear assembly. Annu. Rev. Cell. Dev. Biol. 13, 669–695.10.1146/annurev.cellbio.13.1.669Suche in Google Scholar PubMed

Gigliotti, S., Callaini, G., Andone, S., Riparbelli, M.G., Pernas-Alonso, R., Hoffmann, G., Graziani, F., and Malva, C. (1998). Nup154, a new Drosophila gene essential for male and female gametogenesis is related to the nup155 vertebrate nucleoporin gene. J. Cell Biol. 142, 1195–1207.10.1083/jcb.142.5.1195Suche in Google Scholar PubMed PubMed Central

Gomez-Ospina, N., Morgan, G., Giddings, T.H., Jr., Kosova, B., Hurt, E., and Winey, M. (2000). Yeast nuclear pore complex assembly defects determined by nuclear envelope reconstruction. J. Struct. Biol. 132, 1–5.10.1006/jsbi.2000.4305Suche in Google Scholar PubMed

Grandi, P., Doye, V., and Hurt, E.C. (1993). Purification of NSP1 reveals complex formation with ‘GLFG’ nucleoporins and a novel nuclear pore protein NIC96. EMBO J. 12, 3061–3071.10.1002/j.1460-2075.1993.tb05975.xSuche in Google Scholar PubMed PubMed Central

Grandi, P., Schlaich, N., Tekotte, H., and Hurt, E.C. (1995). Functional interaction of Nic96p with a core nucleoporin complex consisting of Nsp1p, Nup49p and a novel protein Nup57p. EMBO J. 14, 76–87.10.1002/j.1460-2075.1995.tb06977.xSuche in Google Scholar PubMed PubMed Central

Grandi, P., Dang, T., Pane, N., Shevchenko, A., Mann, M., Forbes, D., and Hurt, E. (1997). 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. Cell 8, 2017–2038.10.1091/mbc.8.10.2017Suche in Google Scholar PubMed PubMed Central

Grossman, E., Medalia, O., and Zwerger, M. (2012). Functional architecture of the nuclear pore complex. Annu. Rev. Biophys. 41, 557–584.10.1146/annurev-biophys-050511-102328Suche in Google Scholar PubMed

Hachet, V., Busso, C., Toya, M., Sugimoto, A., Askjaer, P., and Gonczy, P. (2012). The nucleoporin Nup205/NPP-3 is lost near centrosomes at mitotic onset and can modulate the timing of this process in Caenorhabditis elegans embryos. Mol. Biol. Cell 23, 3111–3121.10.1091/mbc.e12-03-0204Suche in Google Scholar

Handa, N., Kukimoto-Niino, M., Akasaka, R., Kishishita, S., Murayama, K., Terada, T., Inoue, M., Kigawa, T., Kose, S., Imamoto, N., et al. (2006). The crystal structure of mouse Nup35 reveals atypical RNP motifs and novel homodimerization of the RRM domain. J. Mol. Biol. 363, 114–124.10.1016/j.jmb.2006.07.089Suche in Google Scholar PubMed

Hawryluk-Gara, L.A., Shibuya, E.K., and Wozniak, R.W. (2005). Vertebrate Nup53 interacts with the nuclear lamina and is required for the assembly of a Nup93-containing complex. Mol. Biol. Cell 16, 2382–2394.10.1091/mbc.e04-10-0857Suche in Google Scholar PubMed PubMed Central

Hawryluk-Gara, L.A., Platani, M., Santarella, R., Wozniak, R.W., and Mattaj, I.W. (2008). Nup53 is required for nuclear envelope and nuclear pore complex assembly. Mol. Biol. Cell 19, 1753–1762.10.1091/mbc.e07-08-0820Suche in Google Scholar PubMed PubMed Central

Hulsmann, B.B., Labokha, A.A., and Gorlich, D. (2012). The permeability of reconstituted nuclear pores provides direct evidence for the selective phase model. Cell 150, 738–751.10.1016/j.cell.2012.07.019Suche in Google Scholar PubMed

Ikegami, K. and Lieb, J.D. (2013). Integral nuclear pore proteins bind to Pol III-transcribed genes and are required for Pol III transcript processing in C. elegans. Mol. Cell 51, 840–849.10.1016/j.molcel.2013.08.001Suche in Google Scholar PubMed PubMed Central

Iouk, T., Kerscher, O., Scott, R.J., Basrai, M.A., and Wozniak, R.W. (2002). The yeast nuclear pore complex functionally interacts with components of the spindle assembly checkpoint. J. Cell Biol. 159, 807–819.10.1083/jcb.200205068Suche in Google Scholar PubMed PubMed Central

Itoh, G., Sugino, S., Ikeda, M., Mizuguchi, M., Kanno, S., Amin, M.A., Iemura, K., Yasui, A., Hirota, T., and Tanaka, K. (2013). Nucleoporin Nup188 is required for chromosome alignment in mitosis. Cancer Sci. 104, 871–879.10.1111/cas.12159Suche in Google Scholar PubMed PubMed Central

Jeudy, S. and Schwartz, T.U. (2007). Crystal structure of nucleoporin nic96 reveals a novel, intricate helical domain architecture. J. Biol. Chem. 282, 34904–34912.10.1074/jbc.M705479200Suche in Google Scholar PubMed

Kehat, I., Accornero, F., Aronow, B.J., and Molkentin, J.D. (2011). Modulation of chromatin position and gene expression by HDAC4 interaction with nucleoporins. J. Cell Biol. 193, 21–29.10.1083/jcb.201101046Suche in Google Scholar PubMed PubMed Central

Kenna, M.A., Petranka, J.G., Reilly, J.L., and Davis, L.I. (1996). Yeast N1e3p/Nup170p is required for normal stoichiometry of F.G. nucleoporins within the nuclear pore complex. Mol. Cell. Biol. 16, 2025–2036.10.1128/MCB.16.5.2025Suche in Google Scholar PubMed PubMed Central

Kerscher, O., Hieter, P., Winey, M., and Basrai, M.A. (2001). Novel role for a Saccharomyces cerevisiae nucleoporin, Nup170p, in chromosome segregation. Genetics 157, 1543–1553.10.1093/genetics/157.4.1543Suche in Google Scholar PubMed PubMed Central

Kim, D.U., Hayles, J., Kim, D., Wood, V., Park, H.O., Won, M., Yoo, H.S., Duhig, T., Nam, M., Palmer, G., et al. (2010). Analysis of a genome-wide set of gene deletions in the fission yeast Schizosaccharomyces pombe. Nat. Biotechnol. 28, 617–623.10.1038/nbt.1628Suche in Google Scholar PubMed PubMed Central

King, M.C., Lusk, C.P., and Blobel, G. (2006). Karyopherin-mediated import of integral inner nuclear membrane proteins. Nature 442, 1003–1007.10.1038/nature05075Suche in Google Scholar PubMed

Kosova, B., Pante, N., Rollenhagen, C., and Hurt, E. (1999). Nup192p is a conserved nucleoporin with a preferential location at the inner site of the nuclear membrane. J. Biol. Chem. 274, 22646–22651.10.1074/jbc.274.32.22646Suche in Google Scholar PubMed

Krull, S., Thyberg, J., Bjorkroth, B., Rackwitz, H.R., and Cordes, V.C. (2004). Nucleoporins as components of the nuclear pore complex core structure and Tpr as the architectural element of the nuclear basket. Mol. Biol. Cell 15, 4261–4277.10.1091/mbc.e04-03-0165Suche in Google Scholar PubMed PubMed Central

Laurell, E., Beck, K., Krupina, K., Theerthagiri, G., Bodenmiller, B., Horvath, P., Aebersold, R., Antonin, W., and Kutay, U. (2011). Phosphorylation of Nup98 by multiple kinases is crucial for NPC disassembly during mitotic entry. Cell 144, 539–550.10.1016/j.cell.2011.01.012Suche in Google Scholar PubMed

Leksa, N.C. and Schwartz, T.U. (2010). Membrane-coating lattice scaffolds in the nuclear pore and vesicle coats: commonalities, differences, challenges. Nucleus 1, 314–318.10.4161/nucl.1.4.11798Suche in Google Scholar PubMed PubMed Central

Liang, Y. and Hetzer, M.W. (2011). Functional interactions between nucleoporins and chromatin. Curr. Opin. Cell Biol. 23, 65–70.10.1016/j.ceb.2010.09.008Suche in Google Scholar PubMed PubMed Central

Liu, H.L., De Souza, C.P., Osmani, A.H., and Osmani, S.A. (2009). 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. Cell 20, 616–630.10.1091/mbc.e08-06-0628Suche in Google Scholar PubMed PubMed Central

Lusk, C.P., Makhnevych, T., Marelli, M., Aitchison, J.D., and Wozniak, R.W. (2002). Karyopherins in nuclear pore biogenesis: a role for Kap121p in the assembly of Nup53p into nuclear pore complexes. J. Cell Biol. 159, 267–278.10.1083/jcb.200203079Suche in Google Scholar PubMed PubMed Central

Lusk, C.P., Blobel, G., and King, M.C. (2007a). Highway to the inner nuclear membrane: rules for the road. Nat. Rev. Mol. Cell. Biol. 8, 414–420.10.1038/nrm2165Suche in Google Scholar PubMed

Lusk, C.P., Waller, D.D., Makhnevych, T., Dienemann, A., Whiteway, M., Thomas, D.Y., and Wozniak, R.W. (2007b). Nup53p is a target of two mitotic kinases, Cdk1p and Hrr25p. Traffic 8, 647–660.10.1111/j.1600-0854.2007.00559.xSuche in Google Scholar PubMed

Lutzmann, M., Kunze, R., Buerer, A., Aebi, U., and Hurt, E. (2002). Modular self-assembly of a Y-shaped multiprotein complex from seven nucleoporins. EMBO J. 21, 387–397.10.1093/emboj/21.3.387Suche in Google Scholar PubMed PubMed Central

Lutzmann, M., Kunze, R., Stangl, K., Stelter, P., Toth, K.F., Bottcher, B., and Hurt, E. (2005). Reconstitution of Nup157 and Nup145N into the Nup84 complex. J. Biol. Chem. 280, 18442–18451.10.1074/jbc.M412787200Suche in Google Scholar

Maimon, T., Elad, N., Dahan, I., and Medalia, O. (2012). The human nuclear pore complex as revealed by cryo-electron tomography. Structure 20, 998–1006.10.1016/j.str.2012.03.025Suche in Google Scholar

Makhnevych, T., Lusk, C.P., Anderson, A.M., Aitchison, J.D., and Wozniak, R.W. (2003). Cell cycle regulated transport controlled by alterations in the nuclear pore complex. Cell 115, 813–823.10.1016/S0092-8674(03)00986-3Suche in Google Scholar

Makio, T., Stanton, L.H., Lin, C.C., Goldfarb, D.S., Weis, K., and Wozniak, R.W. (2009). The nucleoporins Nup170p and Nup157p are essential for nuclear pore complex assembly. J. Cell Biol. 185, 459–473.10.1083/jcb.200810029Suche in Google Scholar PubMed PubMed Central

Mans, B.J., Anantharaman, V., Aravind, L., and Koonin, E.V. (2004). Comparative genomics, evolution and origins of the nuclear envelope and nuclear pore complex. Cell Cycle 3, 1612–1637.10.4161/cc.3.12.1316Suche in Google Scholar PubMed

Mansfeld, J., Guttinger, S., Hawryluk-Gara, L.A., Pante, N., Mall, M., Galy, V., Haselmann, U., Muhlhausser, P., Wozniak, R.W., Mattaj, I.W., et al. (2006). The conserved transmembrane nucleoporin NDC1 is required for nuclear pore complex assembly in vertebrate cells. Mol. Cell 22, 93–103.10.1016/j.molcel.2006.02.015Suche in Google Scholar PubMed

Marelli, M., Aitchison, J.D., and Wozniak, R.W. (1998). Specific binding of the karyopherin Kap121p to a subunit of the nuclear pore complex containing Nup53p, Nup59p, and Nup170p. J. Cell. Biol. 143, 1813–1830..10.1083/jcb.143.7.1813Suche in Google Scholar PubMed PubMed Central

Marelli, M., Lusk, C.P., Chan, H., Aitchison, J.D., and Wozniak, R.W. (2001). A link between the synthesis of nucleoporins and the biogenesis of the nuclear envelope. J. Cell Biol. 153, 709–724.10.1083/jcb.153.4.709Suche in Google Scholar PubMed PubMed Central

Meinema, A.C., Laba, J.K., Hapsari, R.A., Otten, R., Mulder, F.A., Kralt, A., van den Bogaart, G., Lusk, C.P., Poolman, B., and Veenhoff, L.M. (2011). Long unfolded linkers facilitate membrane protein import through the nuclear pore complex. Science 333, 90–93.10.1126/science.1205741Suche in Google Scholar PubMed

Mendjan, S., Taipale, M., Kind, J., Holz, H., Gebhardt, P., Schelder, M., Vermeulen, M., Buscaino, A., Duncan, K., Mueller, J., et al. (2006). Nuclear pore components are involved in the transcriptional regulation of dosage compensation in Drosophila. Mol. Cell 21, 811–823.10.1016/j.molcel.2006.02.007Suche in Google Scholar PubMed

Miller, B.R., Powers, M., Park, M., Fischer, W., and Forbes, D.J. (2000). Identification of a new vertebrate nucleoporin, Nup188, with the use of a novel organelle trap assay. Mol. Biol. Cell 11, 3381–3396.10.1091/mbc.11.10.3381Suche in Google Scholar PubMed PubMed Central

Mitchell, J.M., Mansfeld, J., Capitanio, J., Kutay, U., and Wozniak, R.W. (2010). Pom121 links two essential subcomplexes of the nuclear pore complex core to the membrane. J. Cell Biol. 191, 505–521.10.1083/jcb.201007098Suche in Google Scholar PubMed PubMed Central

Mohr, D., Frey, S., Fischer, T., Guttler, T., and Gorlich, D. (2009). Characterisation of the passive permeability barrier of nuclear pore complexes. EMBO J. 28, 2541–2553.10.1038/emboj.2009.200Suche in Google Scholar PubMed PubMed Central

Nehrbass, U., Rout, M.P., Maguire, S., Blobel, G., and Wozniak, R.W. (1996). The yeast nucleoporin Nup188p interacts genetically and physically with the core structures of the nuclear pore complex. J. Cell Biol. 133, 1153–1162.10.1083/jcb.133.6.1153Suche in Google Scholar PubMed PubMed Central

Neumann, N., Lundin, D., and Poole, A.M. (2010). Comparative genomic evidence for a complete nuclear pore complex in the last eukaryotic common ancestor. PLoS One 5, e13241.10.1371/journal.pone.0013241Suche in Google Scholar PubMed PubMed Central

Ohba, T., Schirmer, E.C., Nishimoto, T., and Gerace, L. (2004). Energy- and temperature-dependent transport of integral proteins to the inner nuclear membrane via the nuclear pore. J. Cell Biol. 167, 1051–1062.10.1083/jcb.200409149Suche in Google Scholar PubMed PubMed Central

Onischenko, E., Stanton, L.H., Madrid, A.S., Kieselbach, T., and Weis, K. (2009). Role of the Ndc1 interaction network in yeast nuclear pore complex assembly and maintenance. J. Cell Biol. 185, 475–491.10.1083/jcb.200810030Suche in Google Scholar PubMed PubMed Central

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. (2013). Cell type-specific nuclear pores: a case in point for context-dependent stoichiometry of molecular machines. Mol. Syst. Biol. 9, 648.10.1038/msb.2013.4Suche in Google Scholar PubMed PubMed Central

Osmani, A.H., Davies, J., Liu, H.L., Nile, A., and Osmani, S.A. (2006). Systematic deletion and mitotic localization of the nuclear pore complex proteins of Aspergillus nidulans. Mol. Biol. Cell 17, 4946–4961.10.1091/mbc.e06-07-0657Suche in Google Scholar PubMed PubMed Central

Patel, S.S. and Rexach, M.F. (2008). Discovering novel interactions at the nuclear pore complex using bead halo: a rapid method for detecting molecular interactions of high and low affinity at equilibrium. Mol. Cell Proteomics 7, 121–131.10.1074/mcp.M700407-MCP200Suche in Google Scholar PubMed

Powell, L. and Burke, B. (1990). Internuclear exchange of an inner nuclear membrane protein (p55). in heterokaryons: in vivo evidence for the interaction of p55 with the nuclear lamina. J. Cell. Biol. 111, 2225–2234.10.1083/jcb.111.6.2225Suche in Google Scholar PubMed PubMed Central

Rabut, G., Doye, V., and Ellenberg, J. (2004). Mapping the dynamic organization of the nuclear pore complex inside single living cells. Nat. Cell Biol. 6, 1114–1121.10.1038/ncb1184Suche in Google Scholar PubMed

Reichelt, R., Holzenburg, A., Buhle, E.L., Jr., Jarnik, M., Engel, A., and Aebi, U. (1990). Correlation between structure and mass distribution of the nuclear pore complex and of distinct pore complex components. J. Cell Biol. 110, 883–894.10.1083/jcb.110.4.883Suche in Google Scholar PubMed PubMed Central

Ribbeck, K. and Gorlich, D. (2002). The permeability barrier of nuclear pore complexes appears to operate via hydrophobic exclusion. EMBO J. 21, 2664–2671.10.1093/emboj/21.11.2664Suche in Google Scholar PubMed PubMed Central

Rodenas, E., Klerkx, E.P., Ayuso, C., Audhya, A., and Askjaer, P. (2009). Early embryonic requirement for nucleoporin Nup35/NPP-19 in nuclear assembly. Dev. Biol. 327, 399–409.10.1016/j.ydbio.2008.12.024Suche in Google Scholar PubMed

Rothballer, A. and Kutay, U. (2013). Poring over pores: nuclear pore complex insertion into the nuclear envelope. Trends Biochem. Sci. 38, 292–301.10.1016/j.tibs.2013.04.001Suche in Google Scholar PubMed

Rout, M.P., Aitchison, J.D., Suprapto, A., Hjertaas, K., Zhao, Y., and Chait, B.T. (2000). The yeast nuclear pore complex: composition, architecture, and transport mechanism. J. Cell Biol. 148, 635–651.10.1083/jcb.148.4.635Suche in Google Scholar PubMed PubMed Central

Sachdev, R., Sieverding, C., Flotenmeyer, M., and Antonin, W. (2012). The C-terminal domain of Nup93 is essential for assembly of the structural backbone of nuclear pore complexes. Mol. Biol. Cell 23, 740–749.10.1091/mbc.e11-09-0761Suche in Google Scholar PubMed PubMed Central

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. (2013). Structure, dynamics, evolution, and function of a major scaffold component in the nuclear pore complex. Structure 21, 560–571.10.1016/j.str.2013.02.005Suche in Google Scholar PubMed PubMed Central

Savas, J.N., Toyama, B.H., Xu, T., Yates, J.R., and Hetzer, M.W. (2012). Extremely long-lived nuclear pore proteins in the rat brain. Science 335, 942.10.1126/science.1217421Suche in Google Scholar PubMed PubMed Central

Schetter, A., Askjaer, P., Piano, F., Mattaj, I., and Kemphues, K. (2006). Nucleoporins NPP-1, NPP-3, NPP-4, NPP-11 and NPP-13 are required for proper spindle orientation in C. elegans. Dev. Biol. 289, 360–371.10.1016/j.ydbio.2005.10.038Suche in Google Scholar PubMed PubMed Central

Schlaich, N.L., Haner, M., Lustig, A., Aebi, U., and Hurt, E.C. (1997). In vitro reconstitution of a heterotrimeric nucleoporin complex consisting of recombinant Nsp1p, Nup49p, and Nup57p. Mol. Biol. Cell 8, 33–46.10.1091/mbc.8.1.33Suche in Google Scholar PubMed PubMed Central

Schooley, A., Vollmer, B., and Antonin, W. (2012). Building a nuclear envelope at the end of mitosis: coordinating membrane reorganization, nuclear pore complex assembly, and chromatin de-condensation. Chromosoma 121, 539–554.10.1007/s00412-012-0388-3Suche in Google Scholar PubMed PubMed Central

Schrader, N., Stelter, P., Flemming, D., Kunze, R., Hurt, E., and Vetter, I.R. (2008). Structural basis of the nic96 subcomplex organization in the nuclear pore channel. Mol. Cell 29, 46–55.10.1016/j.molcel.2007.10.022Suche in Google Scholar PubMed

Scott, R.J., Lusk, C.P., Dilworth, D.J., Aitchison, J.D., and Wozniak, R.W. (2005). Interactions between Mad1p and the nuclear transport machinery in the yeast Saccharomyces cerevisiae. Mol. Biol. Cell 16, 4362–4374.10.1091/mbc.e05-01-0011Suche in Google Scholar PubMed PubMed Central

Seo, H.S., Blus, B.J., Jankovic, N.Z., and Blobel, G. (2013). Structure and nucleic acid binding activity of the nucleoporin Nup157. Proc. Natl. Acad. Sci. USA 110, 16450–16455.10.1073/pnas.1316607110Suche in Google Scholar PubMed PubMed Central

Shulga, N. and Goldfarb, D.S. (2003). Binding dynamics of structural nucleoporins govern nuclear pore complex permeability and may mediate channel gating. Mol. Cell Biol. 23, 534–542.10.1128/MCB.23.2.534-542.2003Suche in Google Scholar PubMed PubMed Central

Shulga, N., Mosammaparast, N., Wozniak, R., and Goldfarb, D.S. (2000). Yeast nucleoporins involved in passive nuclear envelope permeability. J. Cell. Biol. 149, 1027–1038.10.1083/jcb.149.5.1027Suche in Google Scholar PubMed PubMed Central

Soullam, B. and Worman, H.J. (1993). The amino-terminal domain of the lamin B receptor is a nuclear envelope targeting signal. J. Cell Biol. 120, 1093–1100.10.1083/jcb.120.5.1093Suche in Google Scholar PubMed PubMed Central

Strawn, L.A., Shen, T., Shulga, N., Goldfarb, D.S., and Wente, S.R. (2004). Minimal nuclear pore complexes define F.G. repeat domains essential for transport. Nat. Cell. Biol. 6, 197–206.10.1038/ncb1097Suche in Google Scholar PubMed

Tamura, K., Fukao, Y., Iwamoto, M., Haraguchi, T., and Hara-Nishimura, I. (2010). Identification and characterization of nuclear pore complex components in Arabidopsis thaliana. Plant Cell 22, 4084–4097.10.1105/tpc.110.079947Suche in Google Scholar PubMed PubMed Central

Theerthagiri, G., Eisenhardt, N., Schwarz, H., and Antonin, W. (2010). The nucleoporin Nup188 controls passage of membrane proteins across the nuclear pore complex. J. Cell Biol. 189, 1129–1142.10.1083/jcb.200912045Suche in Google Scholar PubMed PubMed Central

Thierbach, K., von Appen, A., Thoms, M., Beck, M., Flemming, D., and Hurt, E. (2013). Protein interfaces of the conserved Nup84 complex from Chaetomium thermophilum shown by crosslinking mass spectrometry and electron microscopy. Structure 21, 1672–1682.10.1016/j.str.2013.07.004Suche in Google Scholar PubMed

Toyama, B.H., Savas, J.N., Park, S.K., Harris, M.S., Ingolia, N.T., Yates, J.R., 3rd, and Hetzer, M.W. (2013). Identification of long-lived proteins reveals exceptional stability of essential cellular structures. Cell 154, 971–982.10.1016/j.cell.2013.07.037Suche in Google Scholar PubMed PubMed Central

Tran, E.J. and Wente, S.R. (2006). Dynamic nuclear pore complexes: life on the edge. Cell 125, 1041–1053.10.1016/j.cell.2006.05.027Suche in Google Scholar PubMed

Tran, E.J., Bolger, T.A., and Wente, S.R. (2007). SnapShot: nuclear transport. Cell 131, 420.10.1016/j.cell.2007.10.015Suche in Google Scholar PubMed

Turgay, Y., Ungricht, R., Rothballer, A., Kiss, A., Csucs, G., Horvath, P., and Kutay, U. (2010). A classical NLS and the SUN domain contribute to the targeting of SUN2 to the inner nuclear membrane. EMBO J. 29, 2262–2275.10.1038/emboj.2010.119Suche in Google Scholar PubMed PubMed Central

Uetz, P., Giot, L., Cagney, G., Mansfield, T.A., Judson, R.S., Knight, J.R., Lockshon, D., Narayan, V., Srinivasan, M., Pochart, P., et al. (2000). A comprehensive analysis of protein-protein interactions in Saccharomyces cerevisiae. Nature 403, 623–627.10.1038/35001009Suche in Google Scholar PubMed

Van de Vosse, D.W., Wan, Y., Wozniak, R.W., and Aitchison, J.D. (2011). Role of the nuclear envelope in genome organization and gene expression. Wiley Interdiscip. Rev. Syst. Biol. Med. 3, 147–166.Suche in Google Scholar

Van de Vosse, D.W., Wan, Y., Lapetina, D.L., Chen, W.M., Chiang, J.H., Aitchison, J.D., and Wozniak, R.W. (2013). A role for the nucleoporin Nup170p in chromatin structure and gene silencing. Cell 152, 969–983.10.1016/j.cell.2013.01.049Suche in Google Scholar PubMed PubMed Central

Vollmer, B., Schooley, A., Sachdev, R., Eisenhardt, N., Schneider, A.M., Sieverding, C., Madlung, J., Gerken, U., Macek, B., and Antonin, W. (2012). Dimerization and direct membrane interaction of Nup53 contribute to nuclear pore complex assembly. EMBO J. 31, 4072–4084.10.1038/emboj.2012.256Suche in Google Scholar PubMed PubMed Central

Wente, S.R. and Rout, M.P. (2010). The nuclear pore complex and nuclear transport. Cold Spring Harb. Perspect. Biol. 2, a000562.10.1101/cshperspect.a000562Suche in Google Scholar

Whalen, W.A., Yoon, J.H., Shen, R., and Dhar, R. (1999). Regulation of mRNA export by nutritional status in fission yeast. Genetics 152, 827–838.10.1093/genetics/152.3.827Suche in Google Scholar

Whittle, J.R. and Schwartz, T.U. (2009). Architectural nucleoporins Nup157/170 and Nup133 are structurally related and descend from a second ancestral element. J. Biol. Chem. 284, 28442–28452.10.1074/jbc.M109.023580Suche in Google Scholar

Wozniak, R., Burke, B., and Doye, V. (2010). Nuclear transport and the mitotic apparatus: an evolving relationship. Cell. Mol. Life Sci. 67, 2215–2230.10.1007/s00018-010-0325-7Suche in Google Scholar

Yang, Q., Rout, M.P., and Akey, C.W. (1998). Three-dimensional architecture of the isolated yeast nuclear pore complex: functional and evolutionary implications. Mol. Cell 1, 223–234.10.1016/S1097-2765(00)80023-4Suche in Google Scholar

Yavuz, S., Santarella-Mellwig, R., Koch, B., Jaedicke, A., Mattaj, I.W., and Antonin, W. (2010). NLS-mediated NPC functions of the nucleoporin Pom121. FEBS Lett. 584, 3292–3298.10.1016/j.febslet.2010.07.008Suche in Google Scholar PubMed

Zabel, U., Doye, V., Tekotte, H., Wepf, R., Grandi, P., and Hurt, E.C. (1996). Nic96p is required for nuclear pore formation and functionally interacts with a novel nucleoporin, Nup188p. J. Cell Biol. 133, 1141–1152.10.1083/jcb.133.6.1141Suche in Google Scholar PubMed PubMed Central

Zhang, X., Chen, S., Yoo, S., Chakrabarti, S., Zhang, T., Ke, T., Oberti, C., Yong, S.L., Fang, F., Li, L., et al. (2008). Mutation in nuclear pore component NUP155 leads to atrial fibrillation and early sudden cardiac death. Cell 135, 1017–1027.10.1016/j.cell.2008.10.022Suche in Google Scholar PubMed

Zuleger, N., Kelly, D.A., Richardson, A.C., Kerr, A.R., Goldberg, M.W., Goryachev, A.B., and Schirmer, E.C. (2011). System analysis shows distinct mechanisms and common principles of nuclear envelope protein dynamics. J. Cell Biol. 193, 109–123.10.1083/jcb.201009068Suche in Google Scholar PubMed PubMed Central