Nup153 Recruits the Nup107-160 Complex to the Inner Nuclear Membrane for Interphasic Nuclear Pore Complex Assembly

Developmental Cell

Volumn 33, Issue 6, 2015, Pages 717-728

  Vollmer, Benjamin ^a,d   Lorenz, Michael ^a   Moreno Andrés, Daniel ^a   Bodenhöfer, Mona ^a   De Magistris, Paola ^a   Astrinidis, Susanne Adina ^a   Schooley, Allana ^a   Flötenmeyer, Matthias ^b   Leptihn, Sebastian ^c   Antonin, Wolfram ^a  

^a FRIEDRICH MIESCHER LABORATORY OF THE MAX PLANCK SOCIETY   (Germany)

^b MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

^c UNIVERSITY OF HOHENHEIM   (Germany)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

KARYOPHERIN ALPHA; KARYOPHERIN BETA; LAMIN; NUCLEOPORIN; NUCLEOPORIN 107-160; NUCLEOPORIN 153; RAN PROTEIN; UNCLASSIFIED DRUG; KARYOPHERINS; NUCLEAR PORE COMPLEX PROTEINS; NUCLEAR PROTEINS; NUP107 PROTEIN, HUMAN; NUP153 PROTEIN, HUMAN; NUP153 PROTEIN, XENOPUS; NUP160 PROTEIN, HUMAN; NUP160 PROTEIN, XENOPUS; RAN GTP-BINDING PROTEIN; RECOMBINANT PROTEINS; XENOPUS PROTEINS;

ANIMAL CELL; ARTICLE; ARTIFICIAL MEMBRANE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL NUCLEUS MEMBRANE; CHROMATIN; COMPLEX FORMATION; CONTROLLED STUDY; EMBRYO; ENZYME REGULATION; FLOTATION; GENE MUTATION; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IN VITRO STUDY; INTERPHASE; LIPID COMPOSITION; MEMBRANE BINDING; MITOSIS; NONHUMAN; NUCLEAR IMPORT; NUCLEAR PORE COMPLEX; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN SECRETION; PROTEIN STABILITY; SEQUENCE ANALYSIS; SURFACE PROPERTY; XENOPUS LAEVIS; ACTIVE TRANSPORT, CELL NUCLEUS; AMINO ACID SEQUENCE; ANIMALS; CHEMISTRY; GENETICS; HELA CELLS; HUMANS; METABOLISM; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; NUCLEAR ENVELOPE; NUCLEAR PORE; PROTEIN INTERACTION DOMAINS AND MOTIFS; SEQUENCE HOMOLOGY, AMINO ACID;

METAZOA;

ACTIVE TRANSPORT, CELL NUCLEUS; AMINO ACID SEQUENCE; ANIMALS; HELA CELLS; HUMANS; INTERPHASE; KARYOPHERINS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; NUCLEAR ENVELOPE; NUCLEAR PORE; NUCLEAR PORE COMPLEX PROTEINS; NUCLEAR PROTEINS; PROTEIN INTERACTION DOMAINS AND MOTIFS; RAN GTP-BINDING PROTEIN; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; XENOPUS LAEVIS; XENOPUS PROTEINS;

EID: 84937565658     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2015.04.027     Document Type: Article

References (52)

1. Ball J.R., Ullman K.S. Versatility at the nuclear pore complex: lessons learned from the nucleoporin Nup153. Chromosoma 2005, 114:319-330.
2. Bastos R., Lin A., Enarson M., Burke B. Targeting and function in mRNA export of nuclear pore complex protein Nup153. J. Cell Biol. 1996, 134:1141-1156.
3. Baur T., Ramadan K., Schlundt A., Kartenbeck J., Meyer H.H. NSF- and SNARE-mediated membrane fusion is required for nuclear envelope formation and completion of nuclear pore complex assembly in Xenopus laevis egg extracts. J. Cell Sci. 2007, 120:2895-2903.
4. Brohawn S.G., Leksa N.C., Spear E.D., Rajashankar K.R., Schwartz T.U. Structural evidence for common ancestry of the nuclear pore complex and vesicle coats. Science 2008, 322:1369-1373.
5. Bui K.H., von Appen A., DiGuilio A.L., Ori A., Sparks L., Mackmull M.T., Bock T., Hagen W., Andrés-Pons A., Glavy J.S., Beck M. Integrated structural analysis of the human nuclear pore complex scaffold. Cell 2013, 155:1233-1243.
6. Cordes V.C., Reidenbach S., Rackwitz H.R., Franke W.W. Identification of protein p270/Tpr as a constitutive component of the nuclear pore complex-attached intranuclear filaments. J. Cell Biol. 1997, 136:515-529.
7. 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. 2002, 158:915-927.
8. D'Angelo M.A., Anderson D.J., Richard E., Hetzer M.W. Nuclear pores form de novo from both sides of the nuclear envelope. Science 2006, 312:440-443.
9. Daigle N., Beaudouin J., Hartnell L., Imreh G., Hallberg E., Lippincott-Schwartz J., Ellenberg J. Nuclear pore complexes form immobile networks and have a very low turnover in live mammalian cells. J. Cell Biol. 2001, 154:71-84.
10. Dawson T.R., Lazarus M.D., Hetzer M.W., Wente S.R. ER membrane-bending proteins are necessary for de novo nuclear pore formation. J. Cell Biol. 2009, 184:659-675.
11. Doucet C.M., Talamas J.A., Hetzer M.W. Cell cycle-dependent differences in nuclear pore complex assembly in metazoa. Cell 2010, 141:1030-1041.
12. Drin G., Casella J.F., Gautier R., Boehmer T., Schwartz T.U., Antonny B. A general amphipathic α-helical motif for sensing membrane curvature. Nat. Struct. Mol. Biol. 2007, 14:138-146.
13. Dultz E., Ellenberg J. Live imaging of single nuclear pores reveals unique assembly kinetics and mechanism in interphase. J. Cell Biol. 2010, 191:15-22.
14. Eisenhardt N., Schooley A., Antonin W. Xenopus in vitro assays to analyze the function of transmembrane nucleoporins and targeting of inner nuclear membrane proteins. Methods Cell Biol. 2014, 122:193-218.
15. Enarson P., Enarson M., Bastos R., Burke B. Amino-terminal sequences that direct nucleoporin nup153 to the inner surface of the nuclear envelope. Chromosoma 1998, 107:228-236.
16. Floch A.G., Tareste D., Fuchs P.F., Chadrin A., Naciri I., Léger T., Schlenstedt G., Palancade B., Doye V. Nuclear pore targeting of the yeast Pom33 nucleoporin depends on karyopherin and lipid binding. J. Cell Sci. 2015, 128:305-316.
17. Franz C., Walczak R., Yavuz S., Santarella R., Gentzel M., Askjaer P., Galy V., Hetzer M., Mattaj I.W., Antonin W. MEL-28/ELYS is required for the recruitment of nucleoporins to chromatin and postmitotic nuclear pore complex assembly. EMBO Rep. 2007, 8:165-172.
18. Galy V., Mattaj I.W., Askjaer P. Caenorhabditis elegans nucleoporins Nup93 and Nup205 determine the limit of nuclear pore complex size exclusion in vivo. Mol. Biol. Cell 2003, 14:5104-5115.
19. Gant T.M., Wilson K.L. Nuclear assembly. Annu. Rev. Cell Dev. Biol. 1997, 13:669-695.
20. Gautier R., Douguet D., Antonny B., Drin G. HELIQUEST: a web server to screen sequences with specific α-helical properties. Bioinformatics 2008, 24:2101-2102.
21. Gillespie P.J., Khoudoli G.A., Stewart G., Swedlow J.R., Blow J.J. ELYS/MEL-28 chromatin association coordinates nuclear pore complex assembly and replication licensing. Curr. Biol. 2007, 17:1657-1662.
22. Guan T., Kehlenbach R.H., Schirmer E.C., Kehlenbach A., Fan F., Clurman B.E., Arnheim N., Gerace L. Nup50, a nucleoplasmically oriented nucleoporin with a role in nuclear protein export. Mol. Cell. Biol. 2000, 20:5619-5630.
23. Harborth J., Elbashir S.M., Bechert K., Tuschl T., Weber K. Identification of essential genes in cultured mammalian cells using small interfering RNAs. J. Cell Sci. 2001, 114:4557-4565.
24. 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.
25. Hase M.E., Cordes V.C. Direct interaction with nup153 mediates binding of Tpr to the periphery of the nuclear pore complex. Mol. Biol. Cell 2003, 14:1923-1940.
26. Kim S.J., Fernandez-Martinez J., Sampathkumar P., Martel A., Matsui T., Tsuruta H., Weiss T.M., Shi Y., Markina-Inarrairaegui A., Bonanno J.B., et al. Integrative structure-function mapping of the nucleoporin Nup133 suggests a conserved mechanism for membrane anchoring of the nuclear pore complex. Mol. Cell. Proteomics 2014, 13:2911-2926.
27. Kupke T., Di Cecco L., Müller H.M., Neuner A., Adolf F., Wieland F., Nickel W., Schiebel E. Targeting of Nbp1 to the inner nuclear membrane is essential for spindle pole body duplication. EMBO J. 2011, 30:3337-3352.
28. Lorenz M., Vollmer B., Unsay J.D., Klupp B.G., García-Sáez A.J., Mettenleiter T.C., Antonin W. A single herpesvirus protein can mediate vesicle formation in the nuclear envelope. J. Biol. Chem. 2015, 290:6962-6974.
29. Lutzmann M., Kunze R., Buerer A., Aebi U., Hurt E. Modular self-assembly of a Y-shaped multiprotein complex from seven nucleoporins. EMBO J. 2002, 21:387-397.
30. Mitchell J.M., Mansfeld J., Capitanio J., Kutay U., Wozniak R.W. Pom121 links two essential subcomplexes of the nuclear pore complex core to the membrane. J. Cell Biol. 2010, 191:505-521.
31. Moroianu J., Blobel G., Radu A. RanGTP-mediated nuclear export of karyopherin alpha involves its interaction with the nucleoporin Nup153. Proc. Natl. Acad. Sci. USA 1997, 94:9699-9704.
32. Nakielny S., Shaikh S., Burke B., Dreyfuss G. Nup153 is an M9-containing mobile nucleoporin with a novel Ran-binding domain. EMBO J. 1999, 18:1982-1995.
33. Ogawa Y., Miyamoto Y., Oka M., Yoneda Y. The interaction between importin-α and Nup153 promotes importin-α/β-mediated nuclear import. Traffic 2012, 13:934-946.
34. Ralle T., Grund C., Franke W.W., Stick R. Intranuclear membrane structure formations by CaaX-containing nuclear proteins. J. Cell Sci. 2004, 117:6095-6104.
35. Rasala B.A., Orjalo A.V., Shen Z., Briggs S., Forbes D.J. ELYS is a dual nucleoporin/kinetochore protein required for nuclear pore assembly and proper cell division. Proc. Natl. Acad. Sci. USA 2006, 103:17801-17806.
36. Rasala B.A., Ramos C., Harel A., Forbes D.J. Capture of AT-rich chromatin by ELYS recruits POM121 and NDC1 to initiate nuclear pore assembly. Mol. Biol. Cell 2008, 19:3982-3996.
37. Rotem A., Gruber R., Shorer H., Shaulov L., Klein E., Harel A. Importin beta regulates the seeding of chromatin with initiation sites for nuclear pore assembly. Mol. Biol. Cell 2009, 20:4031-4042.
38. Schooley A., Vollmer B., Antonin W. Building a nuclear envelope at the end of mitosis: coordinating membrane reorganization, nuclear pore complex assembly, and chromatin de-condensation. Chromosoma 2012, 121:539-554.
39. Shah S., Forbes D.J. Separate nuclear import pathways converge on the nucleoporin Nup153 and can be dissected with dominant-negative inhibitors. Curr. Biol. 1998, 8:1376-1386.
40. Shah S., Tugendreich S., Forbes D. Major binding sites for the nuclear import receptor are the internal nucleoporin Nup153 and the adjacent nuclear filament protein Tpr. J. Cell Biol. 1998, 141:31-49.
41. Sukegawa J., Blobel G. A nuclear pore complex protein that contains zinc finger motifs, binds DNA, and faces the nucleoplasm. Cell 1993, 72:29-38.
42. Theerthagiri G., Eisenhardt N., Schwarz H., Antonin W. The nucleoporin Nup188 controls passage of membrane proteins across the nuclear pore complex. J. Cell Biol. 2010, 189:1129-1142.
43. Ullman K.S., Shah S., Powers M.A., Forbes D.J. The nucleoporin nup153 plays a critical role in multiple types of nuclear export. Mol. Biol. Cell 1999, 10:649-664.
44. Varadarajan P., Mahalingam S., Liu P., Ng S.B., Gandotra S., Dorairajoo D.S., Balasundaram D. The functionally conserved nucleoporins Nup124p from fission yeast and the human Nup153 mediate nuclear import and activity of the Tf1 retrotransposon and HIV-1 Vpr. Mol. Biol. Cell 2005, 16:1823-1838.
45. 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.
46. Vollmer B., Antonin W. The diverse roles of the Nup93/Nic96 complex proteins - structural scaffolds of the nuclear pore complex with additional cellular functions. Biol. Chem. 2014, 395:515-528.
47. Vollmer B., Schooley A., Sachdev R., Eisenhardt N., Schneider A.M., Sieverding C., Madlung J., Gerken U., Macek B., Antonin W. Dimerization and direct membrane interaction of Nup53 contribute to nuclear pore complex assembly. EMBO J. 2012, 31:4072-4084.
48. Walther T.C., Fornerod M., Pickersgill H., Goldberg M., Allen T.D., Mattaj I.W. The nucleoporin Nup153 is required for nuclear pore basket formation, nuclear pore complex anchoring and import of a subset of nuclear proteins. EMBO J. 2001, 20:5703-5714.
49. Walther T.C., Alves A., Pickersgill H., Loïodice I., Hetzer M., Galy V., Hülsmann B.B., Köcher T., Wilm M., Allen T., et al. The conserved Nup107-160 complex is critical for nuclear pore complex assembly. Cell 2003, 113:195-206.
50. Walther T.C., Askjaer P., Gentzel M., Habermann A., Griffiths G., Wilm M., Mattaj I.W., Hetzer M. RanGTP mediates nuclear pore complex assembly. Nature 2003, 424:689-694.
51. Wente S.R., Rout M.P. The nuclear pore complex and nuclear transport. Cold Spring Harb. Perspect. Biol. 2010, 2:a000562.
52. Yavuz S., Santarella-Mellwig R., Koch B., Jaedicke A., Mattaj I.W., Antonin W. NLS-mediated NPC functions of the nucleoporin Pom121. FEBS Lett. 2010, 584:3292-3298.