Domain topology of nucleoporin Nup98 within the nuclear pore complex

Journal of Structural Biology

Volumn 177, Issue 1, 2012, Pages 81-89

  Chatel, Guillaume ^a   Desai, Sachin H ^b   Mattheyses, Alexa L ^b   Powers, Maureen A ^b   Fahrenkrog, Birthe ^a,c  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Electron microscopy; FG repeats; Nuclear pore complex; Nucleoporin; Nup98; Permeability barrier; SIM

Indexed keywords

EPITOPE; NUCLEOPORIN; NUCLEOPORIN 98;

ACTIN FILAMENT; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL NUCLEUS; CELL TRANSPORT; CYTOPLASM; EUKARYOTIC CELL; FLUORESCENCE MICROSCOPY; IMMUNOELECTRON MICROSCOPY; NONHUMAN; NUCLEAR PORE COMPLEX; OOCYTE; PERMEABILITY BARRIER; PHENYLALANINE GLYCINE REPEAT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; XENOPUS;

ANIMALS; ANTIBODIES; BIOLOGICAL TRANSPORT; BLOTTING, WESTERN; CELL NUCLEUS; MICROSCOPY, IMMUNOELECTRON; NUCLEAR PORE; NUCLEAR PORE COMPLEX PROTEINS; OOCYTES; PROTEIN STRUCTURE, TERTIARY; XENOPUS;

EUKARYOTA; VERTEBRATA;

EID: 84855824315     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2011.11.004     Document Type: Article

References (63)

1. Arnaoutov A., Azuma Y., Ribbeck K., Joseph J., Boyarchuk Y., Karpova T., McNally J., Dasso M. Crm1 is a mitotic effector of Ran-GTP in somatic cells. Nat. Cell Biol. 2005, 7:626-632.
2. Bayliss R., Littlewood T., Stewart M. Structural basis for the interaction between FxFG nucleoporin repeats and importin-beta in nuclear trafficking. Cell 2000, 102:99-108.
3. Beck M., Lucic V., Forster F., Baumeister W., Medalia O. Snapshots of nuclear pore complexes in action captured by cryo-electron tomography. Nature 2007, 449:611-615.
4. Blevins M.B., Smith A.M., Phillips E.M., Powers M.A. Complex formation among the RNA export proteins Nup98, Rae1/Gle2, and TAP. J. Biol. Chem. 2003, 278:20979-20988.
5. Bodoor K., Shaikh S., Salina D., Raharjo W.H., Bastos R., Lohka M., Burke B. Sequential recruitment of NPC proteins to the nuclear periphery at the end of mitosis. J. Cell Sci. 1999, 112:2253-2264.
6. Capelson M., Liang Y., Schulte R., Mair W., Wagner U., Hetzer M.W. Chromatin-bound nuclear pore components regulate gene expression in higher eukaryotes. Cell 2010, 140:372-383.
7. Cross M.K., Powers M.A. Nup98 regulates bipolar spindle assembly through association with microtubules and opposition of MCAK. Mol. Biol. Cell 2011, 22:661-672.
8. D'Angelo M.A., Hetzer M.W. Structure, dynamics and function of nuclear pore complexes. Trends Cell Biol. 2008, 18:456-466.
9. Denning D.P., Patel S.S., Uversky V., Fink A.L., Rexach M. Disorder in the nuclear pore complex: the FG repeat regions of nucleoporins are natively unfolded. Proc. Natl. Acad. Sci. USA 2003, 100:2450-2455.
10. Dultz E., Zanin E., Wurzenberger C., Braun M., Rabut G., Sironi L., Ellenberg J. Systematic kinetic analysis of mitotic dis- and reassembly of the nuclear pore in living cells. J. Cell Biol. 2008, 180:857-865.
11. Fahrenkrog B., Aebi U. The nuclear pore complex: nucleocytoplasmic transport and beyond. Nat. Rev. Mol. Cell Biol. 2003, 4:757-766.
12. Fahrenkrog B., Maco B., Fager A.M., Koser J., Sauder U., Ullman K.S., Aebi U. Domain-specific antibodies reveal multiple-site topology of Nup153 within the nuclear pore complex. J. Struct. Biol. 2002, 140:254-267.
13. Feldherr C.M., Akin D. The location of the transport gate in the nuclear pore complex. J. Cell Sci. 1997, 110(Pt 24):3065-3070.
14. Fiserova J., Kiseleva E., Goldberg M.W. Nuclear envelope and nuclear pore complex structure and organization in tobacco BY-2 cells. Plant J. 2009, 59:243-255.
15. Fiserova J., Richards S.A., Wente S.R., Goldberg M.W. Facilitated transport and diffusion take distinct spatial routes through the nuclear pore complex. J. Cell Sci. 2010, 123:2773-2780.
16. Fontoura B.M., Blobel G., Matunis M.J. A conserved biogenesis pathway for nucleoporins: proteolytic processing of a 186-kilodalton precursor generates Nup98 and the novel nucleoporin, Nup96. J. Cell Biol. 1999, 144:1097-1112.
17. Fontoura B.M., Blobel G., Yaseen N.R. The nucleoporin Nup98 is a site for GDP/GTP exchange on ran and termination of karyopherin beta 2-mediated nuclear import. J. Biol. Chem. 2000, 275:31289-31296.
18. Frenkiel-Krispin D., Maco B., Aebi U., Medalia O. Structural analysis of a metazoan nuclear pore complex reveals a fused concentric ring architecture. J. Mol. Biol. 2009, 395:578-586.
19. Fried H., Kutay U. Nucleocytoplasmic transport: taking an inventory. Cell Mol. Life Sci. 2003, 60:1659-1688.
20. Frosst P., Guan T., Subauste C., Hahn K., Gerace L. Tpr is localized within the nuclear basket of the pore complex and has a role in nuclear protein export. J. Cell Biol. 2002, 156:617-630.
21. Fukuhara T., Ozaki T., Shikata K., Katahira J., Yoneda Y., Ogino K., Tachibana T. Specific monoclonal antibody against the nuclear pore complex protein, nup98. Hybridoma (Larchmt) 2005, 24:244-247.
22. Griffis E.R., Xu S., Powers M.A. Nup98 localizes to both nuclear and cytoplasmic sides of the nuclear pore and binds to two distinct nucleoporin subcomplexes. Mol. Biol. Cell 2003, 14:600-610.
23. Griffis E.R., Altan N., Lippincott-Schwartz J., Powers M.A. Nup98 is a mobile nucleoporin with transcription-dependent dynamics. Mol. Biol. Cell 2002, 13:1282-1297.
24. Griffis E.R., Craige B., Dimaano C., Ullman K.S., Powers M.A. Distinct functional domains within nucleoporins Nup153 and Nup98 mediate transcription-dependent mobility. Mol. Biol. Cell 2004, 15:1991-2002.
25. Gustafsson M.G., Agard D.A., Sedat J.W. Doubling the lateral resolution of wide-field fluorescence microscopy using structured illumination. Proc. SPIE 2000, 3919:141-150.
26. Gustafsson M.G., Shao L., Carlton P.M., Wang C.J., Golubovskaya I.N., et al. Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination. Biophys. J. 2008, 94:4957-4970.
27. Harel A., Orjalo A.V., Vincent T., Lachish-Zalait A., Vasu S., Shah S., Zimmerman E., Elbaum M., Forbes D.J. Removal of a single pore subcomplex results in vertebrate nuclei devoid of nuclear pores. Mol. Cell 2003, 11:853-864.
28. Heintzmann R., Cremer C. Laterally modulated excitation microscopy: improvement of resolution by using a diffraction grating. Proc. SPIE 1998, 3568:185-195.
29. Hodel A.E., Hodel M.R., Griffis E.R., Hennig K.A., Ratner G.A., Xu S., Powers M.A. The three-dimensional structure of the autoproteolytic, nuclear pore-targeting domain of the human nucleoporin Nup98. Mol. Cell 2002, 10:347-358.
30. Jeganathan K.B., Malureanu L., van Deursen J.M. The Rae1-Nup98 complex prevents aneuploidy by inhibiting securin degradation. Nature 2005, 438:1036-1039.
31. Joseph J., Liu S.T., Jablonski S.A., Yen T.J., Dasso M. The RanGAP1-RanBP2 complex is essential for microtubule-kinetochore interactions in vivo. Curr. Biol. 2004, 14:611-617.
32. Kalverda B., Pickersgill H., Shloma V.V., Fornerod M. Nucleoporins directly stimulate expression of developmental and cell-cycle genes inside the nucleoplasm. Cell 2010, 140:360-371.
33. Keminer O., Siebrasse J.P., Zerf K., Peters R. Optical recording of signal-mediated protein transport through single nuclear pore complexes. Proc. Natl. Acad. Sci. USA 1999, 96:11842-11847.
34. Kowalczyk S.W., Kapinos L., Blosser T.R., Magalhaes T., van Nies P., Lim R.Y., Dekker C. Single-molecule transport across an individual biomimetic nuclear pore complex. Nat. Nanotechnol. 2011, 6:433-438.
35. Laurell E., Beck K., Krupina K., Theerthagiri G., Bodenmiller B., Horvath P., Aebersold R., Antonin W., Kutay U. Phosphorylation of Nup98 by multiple kinases is crucial for NPC disassembly during mitotic entry. Cell 2011, 144:539-550.
36. Lim R.Y., Fahrenkrog B. The nuclear pore complex up close. Curr. Opin. Cell Biol. 2006, 18:342-347.
37. Lim R.Y., Aebi U., Fahrenkrog B. Towards reconciling structure and function in the nuclear pore complex. Histochem. Cell Biol. 2008, 129:105-116.
38. Lussi Y.C., Hugi I., Laurell E., Kutay U., Fahrenkrog B. The nucleoporin Nup88 is interacting with nuclear lamin A. Mol. Biol. Cell 2011, 22:1080-1090.
39. Mackay D.R., Elgort S.W., Ullman K.S. The nucleoporin Nup153 has separable roles in both early mitotic progression and the resolution of mitosis. Mol. Biol. Cell 2009, 20:1652-1660.
40. Mohr D., Frey S., Fischer T., Guttler T., Gorlich D. Characterisation of the passive permeability barrier of nuclear pore complexes. Embo. J. 2009, 28:2541-2553.
41. Naim B., Brumfeld V., Kapon R., Kiss V., Nevo R., Reich Z. Passive and facilitated transport in nuclear pore complexes is largely uncoupled. J. Biol. Chem. 2007, 282:3881-3888.
42. Oka M., Asally M., Yasuda Y., Ogawa Y., Tachibana T., Yoneda Y. The mobile FG nucleoporin Nup98 is a cofactor for Crm1-dependent protein export. Mol. Biol. Cell 2010, 21:1885-1896.
43. 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. 1994, 126:603-617.
44. Park N., Katikaneni P., Skern T., Gustin K.E. Differential targeting of nuclear pore complex proteins in poliovirus-infected cells. J. Virol. 2008, 82:1647-1655.
45. Patel S.S., Belmont B.J., Sante J.M., Rexach M.F. Natively unfolded nucleoporins gate protein diffusion across the nuclear pore complex. Cell 2007, 129:83-96.
46. Paulillo S.M., Powers M.A., Ullman K.S., Fahrenkrog B. Changes in nucleoporin domain topology in response to chemical effectors. J. Mol. Biol. 2006, 363:39-50.
47. Paulillo S.M., Phillips E.M., Koser J., Sauder U., Ullman K.S., Powers M.A., Fahrenkrog B. Nucleoporin domain topology is linked to the transport status of the nuclear pore complex. J. Mol. Biol. 2005, 351:784-798.
48. Powers M.A., Macaulay C., Masiarz F.R., Forbes D.J. Reconstituted nuclei depleted of a vertebrate GLFG nuclear pore protein, p97, import but are defective in nuclear growth and replication. J. Cell Biol. 1995, 128:721-736.
49. 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. 1997, 136:241-250.
50. Pritchard C.E., Fornerod M., Kasper L.H., van Deursen J.M. RAE1 is a shuttling mRNA export factor that binds to a GLEBS-like NUP98 motif at the nuclear pore complex through multiple domains. J. Cell Biol. 1999, 145:237-254.
51. Radu A., Moore M.S., Blobel G. The peptide repeat domain of nucleoporin Nup98 functions as a docking site in transport across the nuclear pore complex. Cell 1995, 81:215-222.
52. Rosenblum J.S., Blobel G. Autoproteolysis in nucleoporin biogenesis. Proc. Natl. Acad. Sci. USA 1999, 96:11370-11375.
53. Schwartz T.U. Modularity within the architecture of the nuclear pore complex. Curr. Opin. Struct. Biol. 2005, 15:221-226.
54. Schwarz-Herion K., Maco B., Sauder U., Fahrenkrog B. Domain Topology of the p62 Complex Within the 3-D Architecture of the Nuclear Pore Complex. J. Mol. Biol. 2007, 370:796-806.
55. Slot J.W., Geuze H.J. A new method of preparing gold probes for multiple-labeling cytochemistry. Eur. J. Cell Biol. 1985, 38:87-93.
56. Terry L.J., Wente S.R. Nuclear mRNA export requires specific FG nucleoporins for translocation through the nuclear pore complex. J. Cell Biol. 2007, 178:1121-1132.
57. Vasu S., Shah S., Orjalo A., Park M., Fischer W.H., Forbes D.J. Novel vertebrate nucleoporins Nup133 and Nup160 play a role in mRNA export. J. Cell Biol. 2001, 155:339-354.
58. Walde S., Kehlenbach R.H. The Part and the Whole: functions of nucleoporins in nucleocytoplasmic transport. Trends Cell Biol. 2011, 20:461-469.
59. Walde, S., Thakar, K., Hutten, S., Spillner, C., Nath, A., Rothbauer, U., Wiemann, S., Kehlenbach, R.H., 2011. The nucleoporin Nup358/RanBP2 promotes nuclear import in a cargo- and transport receptor-specific manner. Traffic.
60. Walther T.C., Alves A., Pickersgill H., Loiodice I., Hetzer M., Galy V., Hulsmann B.B., Kocher T., Wilm M., Allen T., Mattaj I.W., Doye V. The conserved Nup107-160 complex is critical for nuclear pore complex assembly. Cell 2003, 113:195-206.
61. Yamada J., Phillips J.L., Patel S., Goldfien G., Calestagne-Morelli A., Huang H., Reza R., Acheson J., Krishnan V.V., Newsam S., Gopinathan A., Lau E.Y., Colvin M.E., Uversky V.N., Rexach M.F. A bimodal distribution of two distinct categories of intrinsically disordered structures with separate functions in FG nucleoporins. Mol. Cell Proteomics 2010, 9:2205-2224.
62. 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 2011, 108:16571-16576.
63. Zolotukhin A.S., Felber B.K. Nucleoporins nup98 and nup214 participate in nuclear export of human immunodeficiency virus type 1 Rev. J. Virol. 1999, 73:120-127.