In-cell architecture of the nuclear pore and snapshots of its turnover.
Journal
Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462
Informations de publication
Date de publication:
10 2020
10 2020
Historique:
received:
07
08
2019
accepted:
01
06
2020
pubmed:
4
9
2020
medline:
3
2
2021
entrez:
4
9
2020
Statut:
ppublish
Résumé
Nuclear pore complexes (NPCs) fuse the inner and outer membranes of the nuclear envelope. They comprise hundreds of nucleoporins (Nups) that assemble into multiple subcomplexes and form large central channels for nucleocytoplasmic exchange
Identifiants
pubmed: 32879490
doi: 10.1038/s41586-020-2670-5
pii: 10.1038/s41586-020-2670-5
doi:
Substances chimiques
NUP116 protein, S cerevisiae
0
NUP159 protein, S cerevisiae
0
Nuclear Pore Complex Proteins
0
Saccharomyces cerevisiae Proteins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
796-800Subventions
Organisme : European Research Council
Pays : International
Références
Lin, D. H. & Hoelz, A. The structure of the nuclear pore complex (an update). Annu. Rev. Biochem. 88, 725–783 (2019).
pubmed: 30883195
pmcid: 6588426
doi: 10.1146/annurev-biochem-062917-011901
Beck, M. & Hurt, E. The nuclear pore complex: understanding its function through structural insight. Nat. Rev. Mol. Cell Biol. 18, 73–89 (2017).
pubmed: 27999437
doi: 10.1038/nrm.2016.147
Wente, S. R. & Blobel, G. A temperature-sensitive NUPll6 null mutant forms a nuclear envelope seal over the yeast nuclear pore complex thereby blocking nucleocytoplasmic traffic. J. Cell Biol. 123, 275–284 (1993).
pubmed: 7691829
doi: 10.1083/jcb.123.2.275
Fernandez-Martinez, J. et al. Structure and function of the nuclear pore complex cytoplasmic mRNA export platform. Cell 167, 1215–1228 (2016).
pubmed: 27839866
pmcid: 5130164
doi: 10.1016/j.cell.2016.10.028
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).
pubmed: 25646085
pmcid: 4315244
doi: 10.1083/jcb.201411003
Murphy, R., Watkins, J. L. & Wente, S. R. GLE2, a Saccharomyces cerevisiae homologue of the Schizosaccharomyces pombe export factor RAE1, is required for nuclear pore complex structure and function. Mol. Biol. Cell 7, 1921–1937 (1996).
pubmed: 8970155
pmcid: 276040
doi: 10.1091/mbc.7.12.1921
Scarcelli, J. J., Hodge, C. A. & Cole, C. N. The yeast integral membrane protein Apq12 potentially links membrane dynamics to assembly of nuclear pore complexes. J. Cell Biol. 178, 799–812 (2007).
pubmed: 17724120
pmcid: 2064545
doi: 10.1083/jcb.200702120
Pappas, S. S., Liang, C. C., Kim, S., Rivera, C. O. & Dauer, W. T. TorsinA dysfunction causes persistent neuronal nuclear pore defects. Hum. Mol. Genet. 27, 407–420 (2018).
pubmed: 29186574
doi: 10.1093/hmg/ddx405
Laudermilch, E. et al. Dissecting Torsin/cofactor function at the nuclear envelope: a genetic study. Mol. Biol. Cell 27, 3964–3971 (2016).
pubmed: 27798237
pmcid: 5156537
doi: 10.1091/mbc.E16-07-0511
Thaller, D. J. & Patrick Lusk, C. Fantastic nuclear envelope herniations and where to find them. Biochem. Soc. Trans. 46, 877–889 (2018).
pubmed: 30026368
pmcid: 6195200
doi: 10.1042/BST20170442
Lee, C.-W. et al. Selective autophagy degrades nuclear pore complexes. Nat. Cell Biol. 22, 159–166 (2020).
pubmed: 32029894
doi: 10.1038/s41556-019-0459-2
Hoelz, A., Glavy, J. S. & Beck, M. Toward the atomic structure of the nuclear pore complex: when top down meets bottom up. Nat. Struct. Mol. Biol. 23, 624–630 (2016).
pubmed: 27273515
pmcid: 5156573
doi: 10.1038/nsmb.3244
Mosalaganti, S. et al. In situ architecture of the algal nuclear pore complex. Nat. Commun. 9, 2361 (2018).
pubmed: 29915221
pmcid: 6006428
doi: 10.1038/s41467-018-04739-y
Ungricht, R. & Kutay, U. Mechanisms and functions of nuclear envelope remodelling. Nat. Rev. Mol. Cell Biol. 18, 229–245 (2017).
doi: 10.1038/nrm.2016.153
pubmed: 28120913
Kim, S. J. et al. Integrative structure and functional anatomy of a nuclear pore complex. Nature 555, 475–482 (2018).
pubmed: 29539637
pmcid: 6022767
doi: 10.1038/nature26003
Mahamid, J. et al. Visualizing the molecular sociology at the HeLa cell nuclear periphery. Science 351, 969–972 (2016).
pubmed: 26917770
doi: 10.1126/science.aad8857
von Appen, A. et al. In situ structural analysis of the human nuclear pore complex. Nature 526, 140–143 (2015).
doi: 10.1038/nature15381
Rajoo, S., Vallotton, P., Onischenko, E. & Weis, K. Stoichiometry and compositional plasticity of the yeast nuclear pore complex revealed by quantitative fluorescence microscopy. Proc. Natl Acad. Sci. USA 115, E3969–E3977 (2018).
pubmed: 29632211
doi: 10.1073/pnas.1719398115
pmcid: 5924907
Stuwe, T. et al. Nuclear pores. Architecture of the nuclear pore complex coat. Science 347, 1148–1152 (2015).
pubmed: 25745173
pmcid: 5180592
doi: 10.1126/science.aaa4136
Stelter, P. et al. Molecular basis for the functional interaction of dynein light chain with the nuclear-pore complex. Nat. Cell Biol. 9, 788–796 (2007).
pubmed: 17546040
doi: 10.1038/ncb1604
Strawn, L. A., Shen, T. & Wente, S. R. The GLFG regions of Nup116p and Nup100p serve as binding sites for both Kap95p and Mex67p at the nuclear pore complex. J. Biol. Chem. 276, 6445–6452 (2001).
pubmed: 11104765
doi: 10.1074/jbc.M008311200
Schmidt, H. B. & Görlich, D. Nup98 FG domains from diverse species spontaneously phase-separate into particles with nuclear pore-like permselectivity. eLife 4, e04251 (2015).
pmcid: 4283134
doi: 10.7554/eLife.04251
Adams, R. L., Terry, L. J. & Wente, S. R. Nucleoporin FG domains facilitate mRNP remodeling at the cytoplasmic face of the nuclear pore complex. Genetics 197, 1213–1224 (2014).
pubmed: 24931410
pmcid: 4125395
doi: 10.1534/genetics.114.164012
Stage-Zimmermann, T., Schmidt, U. & Silver, P. A. Factors affecting nuclear export of the 60S ribosomal subunit in vivo. Mol. Biol. Cell 11, 3777–3789 (2000).
pubmed: 11071906
pmcid: 15036
doi: 10.1091/mbc.11.11.3777
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).
pubmed: 26344569
doi: 10.1038/nsmb.3084
Onischenko, E. et al. Natively unfolded FG repeats stabilize the structure of the nuclear pore complex. Cell 171, 904–917.e19 (2017).
pubmed: 29033133
pmcid: 5992322
doi: 10.1016/j.cell.2017.09.033
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. USA 108, 16571–16576 (2011).
pubmed: 21930948
doi: 10.1073/pnas.1112846108
pmcid: 3189060
Andersen, K. R. et al. Scaffold nucleoporins Nup188 and Nup192 share structural and functional properties with nuclear transport receptors. eLife 2, e00745 (2013).
pubmed: 23795296
pmcid: 3679522
doi: 10.7554/eLife.00745
Rout, M. P. et al. The yeast nuclear pore complex: composition, architecture, and transport mechanism. J. Cell Biol. 148, 635–652 (2000).
pubmed: 10684247
pmcid: 2169373
doi: 10.1083/jcb.148.4.635
Terry, L. J. & Wente, S. R. Nuclear mRNA export requires specific FG nucleoporins for translocation through the nuclear pore complex. J. Cell Biol. 178, 1121–1132 (2007).
pubmed: 17875746
pmcid: 2064648
doi: 10.1083/jcb.200704174
Weirich, C. S., Erzberger, J. P., Berger, J. M. & Weis, K. The N-terminal domain of Nup159 forms a β-propeller that functions in mRNA export by tethering the helicase Dbp5 to the nuclear pore. Mol. Cell 16, 749–760 (2004).
pubmed: 15574330
doi: 10.1016/j.molcel.2004.10.032
Vallotton, P. et al. Mapping the native organization of the yeast nuclear pore complex using nuclear radial intensity measurements. Proc. Natl Acad. Sci. USA 116, 14606–14613 (2019).
pubmed: 31262825
doi: 10.1073/pnas.1903764116
pmcid: 6642398
Otsuka, S. et al. Nuclear pore assembly proceeds by an inside-out extrusion of the nuclear envelope. eLife 5, e19071 (2016).
pubmed: 27630123
pmcid: 5065316
doi: 10.7554/eLife.19071
Zhang, W. et al. Brr6 and Brl1 locate to nuclear pore complex assembly sites to promote their biogenesis. J. Cell Biol. 217, 877–894 (2018).
pubmed: 29439116
pmcid: 5839787
doi: 10.1083/jcb.201706024
Beck, M., Mosalaganti, S. & Kosinski, J. From the resolution revolution to evolution: structural insights into the evolutionary relationships between vesicle coats and the nuclear pore. Curr. Opin. Struct. Biol. 52, 32–40 (2018).
pubmed: 30103204
doi: 10.1016/j.sbi.2018.07.012
Cantwell, H. & Nurse, P. Unravelling nuclear size control. Curr. Genet. 65, 1281–1285 (2019).
pubmed: 31147736
pmcid: 6820586
doi: 10.1007/s00294-019-00999-3
Kukulski, W. et al. Correlated fluorescence and 3D electron microscopy with high sensitivity and spatial precision. J. Cell Biol. 192, 111–119 (2011).
pubmed: 21200030
pmcid: 3019550
doi: 10.1083/jcb.201009037
Arnold, J. et al. Site-specific cryo-focused ion beam sample preparation guided by 3D correlative microscopy. Biophys. J. 110, 860–869 (2016).
pubmed: 26769364
pmcid: 4775854
doi: 10.1016/j.bpj.2015.10.053
Aitchison, J. D., Blobel, G. & Rout, M. P. Nup120p: a yeast nucleoporin required for NPC distribution and mRNA transport. J. Cell Biol. 131, 1659–1675 (1995).
pubmed: 8557736
doi: 10.1083/jcb.131.6.1659
Shvets, E., Abada, A., Weidberg, H. & Elazar, Z. Dissecting the involvement of LC3B and GATE-16 in p62 recruitment into autophagosomes. Autophagy 7, 683–688 (2011).
pubmed: 21460636
doi: 10.4161/auto.7.7.15279
Sawa-Makarska, J. et al. Cargo binding to Atg19 unmasks additional Atg8 binding sites to mediate membrane-cargo apposition during selective autophagy. Nat. Cell Biol. 16, 425–433 (2014).
pubmed: 24705553
pmcid: 4009068
doi: 10.1038/ncb2935
Osawa, T. et al. Atg2 mediates direct lipid transfer between membranes for autophagosome formation. Nat. Struct. Mol. Biol. 26, 281–288 (2019).
pubmed: 30911189
doi: 10.1038/s41594-019-0203-4
Schütter, M., Giavalisco, P., Brodesser, S. & Graef, M. Local fatty acid channeling into phospholipid synthesis drives phagophore expansion during autophagy. Cell 180, 135–149 (2020).
pubmed: 31883797
doi: 10.1016/j.cell.2019.12.005
Valverde, D. P. et al. ATG2 transports lipids to promote autophagosome biogenesis. J. Cell Biol. 218, 1787–1798 (2019).
pubmed: 30952800
pmcid: 6548141
doi: 10.1083/jcb.201811139
Thaller, D. J. et al. An ESCRT–LEM protein surveillance system is poised to directly monitor the nuclear envelope and nuclear transport system. eLife 8, e45284 (2019).
pubmed: 30942170
pmcid: 6461442
doi: 10.7554/eLife.45284
Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).
pubmed: 22743772
Hampoelz, B. et al. Pre-assembled nuclear pores insert into the nuclear envelope during early development. Cell 166, 664–678 (2016).
pubmed: 27397507
pmcid: 4967450
doi: 10.1016/j.cell.2016.06.015
Mastronarde, D. N. Automated electron microscope tomography using robust prediction of specimen movements. J. Struct. Biol. 152, 36–51 (2005).
pubmed: 16182563
doi: 10.1016/j.jsb.2005.07.007
Kremer, J. R., Mastronarde, D. N. & McIntosh, J. R. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116, 71–76 (1996).
doi: 10.1006/jsbi.1996.0013
pubmed: 8742726
Paul-Gilloteaux, P. et al. eC-CLEM: flexible multidimensional registration software for correlative microscopies. Nat. Methods 14, 102–103 (2017).
pubmed: 28139674
doi: 10.1038/nmeth.4170
de Chaumont, F. et al. Icy: an open bioimage informatics platform for extended reproducible research. Nat. Methods 9, 690–696 (2012).
pubmed: 22743774
Rigort, A. et al. Focused ion beam micromachining of eukaryotic cells for cryoelectron tomography. Proc. Natl Acad. Sci. USA 109, 4449–4454 (2012).
pubmed: 22392984
doi: 10.1073/pnas.1201333109
pmcid: 3311327
Schaffer, M. et al. Optimized cryo-focused ion beam sample preparation aimed at in situ structural studies of membrane proteins. J. Struct. Biol. 197, 73–82 (2017).
pubmed: 27444390
doi: 10.1016/j.jsb.2016.07.010
Hagen, W. J. H., Wan, W. & Briggs, J. A. G. Implementation of a cryo-electron tomography tilt-scheme optimized for high resolution subtomogram averaging. J. Struct. Biol. 197, 191–198 (2017).
pubmed: 27313000
pmcid: 5287356
doi: 10.1016/j.jsb.2016.06.007
Kosinski, J. et al. Molecular architecture of the inner ring scaffold of the human nuclear pore complex. Science 352, 363–365 (2016).
pubmed: 27081072
doi: 10.1126/science.aaf0643
pmcid: 8926079
Zhang, K. Gctf: Real-time CTF determination and correction. J. Struct. Biol. 193, 1–12 (2016).
pubmed: 26592709
pmcid: 4711343
doi: 10.1016/j.jsb.2015.11.003
Turoňová, B., Schur, F. K. M., Wan, W. & Briggs, J. A. G. Efficient 3D-CTF correction for cryo-electron tomography using NovaCTF improves subtomogram averaging resolution to 3.4Å. J. Struct. Biol. 199, 187–195 (2017).
pubmed: 28743638
pmcid: 5614107
doi: 10.1016/j.jsb.2017.07.007
Beck, M., Lucić, V., Förster, F., Baumeister, W. & Medalia, O. Snapshots of nuclear pore complexes in action captured by cryo-electron tomography. Nature 449, 611–615 (2007).
pubmed: 17851530
doi: 10.1038/nature06170
Kucukelbir, A., Sigworth, F. J. & Tagare, H. D. Quantifying the local resolution of cryo-EM density maps. Nat. Methods 11, 63–65 (2014).
doi: 10.1038/nmeth.2727
pubmed: 24213166
Pettersen, E. F. et al. UCSF Chimera—a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004).
doi: 10.1002/jcc.20084
pubmed: 15264254
Wriggers, W. Conventions and workflows for using Situs. Acta Crystallogr. D 68, 344–351 (2012).
pubmed: 22505255
doi: 10.1107/S0907444911049791
pmcid: 3322594
Strimmer, K. fdrtool: a versatile R package for estimating local and tail area-based false discovery rates. Bioinformatics 24, 1461–1462 (2008).
pubmed: 18441000
doi: 10.1093/bioinformatics/btn209
Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57, 289–300 (1995).
Kosinski, J. et al. Xlink Analyzer: software for analysis and visualization of cross-linking data in the context of three-dimensional structures. J. Struct. Biol. 189, 177–183 (2015).
pubmed: 25661704
pmcid: 4359615
doi: 10.1016/j.jsb.2015.01.014
Webb, B. et al. Integrative structure modeling with the Integrative Modeling Platform. Protein Sci. 27, 245–258 (2018).
pubmed: 28960548
doi: 10.1002/pro.3311
Dauden, M. I. et al. Architecture of the yeast Elongator complex. EMBO Rep. 18, 264–279 (2017).
pubmed: 27974378
doi: 10.15252/embr.201643353