Phosphorylation of Nup98 by multiple kinases is crucial for NPC disassembly during mitotic entry

Cell

Volumn 144, Issue 4, 2011, Pages 539-550

  Laurell, Eva ^a   Beck, Katja ^a   Krupina, Ksenia ^a   Theerthagiri, Gandhi ^b   Bodenmiller, Bernd ^a   Horvath, Peter ^a   Aebersold, Ruedi ^a,c   Antonin, Wolfram ^b   Kutay, Ulrike ^a  

^a ETH ZURICH   (Switzerland)

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

^c UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE 1; MUTANT PROTEIN; NUCLEOPORIN 98;

ARTICLE; CELL NUCLEUS MEMBRANE; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MITOSIS SPINDLE; NONHUMAN; NUCLEAR PORE COMPLEX; PRIORITY JOURNAL; PROPHASE; PROTEIN FAMILY; PROTEIN PHOSPHORYLATION;

EID: 79951683953     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2011.01.012     Document Type: Article

References (48)

1. Belham, C., Roig, J., Caldwell, J.A., Aoyama, Y., Kemp, B.E., Comb, M., and Avruch, J. (2003). A mitotic cascade of NIMA family kinases. Nercc1/Nek9 activates the Nek6 and Nek7 kinases. J. Biol. Chem. 278, 34897-34909.
2. Blethrow, J.D., Glavy, J.S., Morgan, D.O., and Shokat, K.M. (2008). Covalent capture of kinase-specific phosphopeptides reveals Cdk1-cyclin B substrates. Proc. Natl. Acad. Sci. USA 105, 1442-1447.
3. Blower, M.D., Nachury, M., Heald, R., and Weis, K. (2005). A Rae1-containing ribonucleoprotein complex is required for mitotic spindle assembly. Cell 121, 223-234. (Pubitemid 40546390)
4. Brohawn, S.G., Partridge, J.R., Whittle, J.R., and Schwartz, T.U. (2009). The nuclear pore complex has entered the atomic age. Structure 17, 1156-1168.
5. Chase, D., Serafinas, C., Ashcroft, N., Kosinski, M., Longo, D., Ferris, D.K., and Golden, A. (2000). The polo-like kinase PLK-1 is required for nuclear envelope breakdown and the completion of meiosis in Caenorhabditis elegans. Genesis 26, 26-41. (Pubitemid 30123463)
6. Cronshaw, J.M., Krutchinsky, A.N., Zhang, W., Chait, B.T., and Matunis, M.J. (2002). Proteomic analysis of the mammalian nuclear pore complex. J. Cell Biol. 158, 915-927. (Pubitemid 35001082)
7. Daub, H., Olsen, J.V., Bairlein, M., Gnad, F., Oppermann, F.S., Korner, R., Greff, Z., Keri, G., Stemmann, O., and Mann, M. (2008). Kinase-selective enrichment enables quantitative phosphoproteomics of the kinome across the cell cycle. Mol. Cell 31, 438-448.
8. De Souza, C.P., Osmani, A.H., Hashmi, S.B., and Osmani, S.A. (2004). Partial nuclear pore complex disassembly during closed mitosis in Aspergillus nidulans. Curr. Biol. 14, 1973-1984.
9. 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. 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. (Pubitemid 351398413)
11. Favreau, C., Worman, H.J., Wozniak, R.W., Frappier, T., and Courvalin, J.C. (1996). Cell cycle-dependent phosphorylation of nucleoporins and nuclear pore membrane protein Gp210. Biochemistry (Mosc.) 35, 8035-8044. (Pubitemid 26202546)
12. Frey, S., and Gorlich, D. (2009). FG/FxFG as well as GLFG repeats form a selective permeability barrier with self-healing properties. EMBO J. 28, 2554-2567.
13. Fry, A.M. (2002). The Nek2 protein kinase: a novel regulator of centrosome structure. Oncogene 21, 6184-6194.
14. Fry, A.M., Meraldi, P., and Nigg, E.A. (1998). A centrosomal function for the human Nek2 protein kinase, a member of the NIMA family of cell cycle regulators. EMBO J. 17, 470-481. (Pubitemid 28045488)
15. Gavet, O., and Pines, J. (2010). Progressive activation of CyclinB1-Cdk1 coordinates entry to mitosis. Dev. Cell 18, 533-543.
16. Glavy, J.S., Krutchinsky, A.N., Cristea, I.M., Berke, I.C., Boehmer, T., Blobel, G., and Chait, B.T. (2007). Cell-cycle-dependent phosphorylation of the nuclear pore Nup107-160 subcomplex. Proc. Natl. Acad. Sci. USA 104, 3811-3816.
17. Griffis, E.R., Xu, S., and Powers, M.A. (2003). Nup98 localizes to both nuclear and cytoplasmic sides of the nuclear pore and binds to two distinct nucleoporin subcomplexes. Mol. Biol. Cell 14, 600-610.
18. Griffis, E.R., Craige, B., Dimaano, C., Ullman, K.S., and Powers, M.A. (2004). Distinct functional domains within nucleoporins Nup153 and Nup98 mediate transcription-dependent mobility. Mol. Biol. Cell 15, 1991-2002.
19. Guttinger, S., Laurell, E., and Kutay, U. (2009). Orchestrating nuclear envelope disassembly and reassembly during mitosis. Nat. Rev. Mol. Cell Biol. 10, 178-191.
20. Hase, M.E., and Cordes, V.C. (2003). Direct interaction with nup153 mediates binding of Tpr to the periphery of the nuclear pore complex. Mol. Biol. Cell 14, 1923-1940.
21. Iovine, M.K., Watkins, J.L., and Wente, S.R. (1995). The GLFG repetitive region of the nucleoporin Nup116p interacts with Kap95p, an essential yeast nuclear import factor. J. Cell Biol. 131, 1699-1713. (Pubitemid 26007968)
22. Jeganathan, K.B., Malureanu, L., and van Deursen, J.M. (2005). The Rae1-Nup98 complex prevents aneuploidy by inhibiting securin degradation. Nature 438, 1036-1039. (Pubitemid 43093978)
23. Kiseleva, E., Rutherford, S., Cotter, L.M., Allen, T.D., and Goldberg, M.W. (2001). Steps of nuclear pore complex disassembly and reassembly during mitosis in early Drosophila embryos. J. Cell Sci. 114, 3607-3618. (Pubitemid 33041043)
24. Lenart, P., Rabut, G., Daigle, N., Hand, A.R., Terasaki, M., and Ellenberg, J. (2003). Nuclear envelope breakdown in starfish oocytes proceeds by partial NPC disassembly followed by a rapidly spreading fenestration of nuclear membranes. J. Cell Biol. 160, 1055-1068. (Pubitemid 36443874)
25. Lenart, P., Petronczki, M., Steegmaier, M., Di Fiore, B., Lipp, J.J., Hoffmann, M., Rettig, W.J., Kraut, N., and Peters, J.M. (2007). The small-molecule inhibitor BI 2536 reveals novel insights into mitotic roles of polo-like kinase 1. Curr. Biol. 17, 304-315.
26. Li, H., Liu, X.S., Yang, X., Song, B., Wang, Y., and Liu, X. (2010). Polo-like kinase 1 phosphorylation of p150Glued facilitates nuclear envelope breakdown during prophase. Proc. Natl. Acad. Sci. USA 107, 14633-14638.
27. Lu, K.P., Osmani, S.A., and Means, A.R. (1993). Properties and regulation of the cell cycle-specific NIMA protein kinase of Aspergillus nidulans. J. Biol. Chem. 268, 8769-8776.
28. Lu, K.P., and Means, A.R. (1994). Expression of the noncatalytic domain of the NIMA kinase causes a G2 arrest in Aspergillus nidulans. EMBO J. 13, 2103-2113. (Pubitemid 24139723)
29. Macaulay, C., Meier, E., and Forbes, D.J. (1995). Differential mitotic phosphorylation of proteins of the nuclear pore complex. J. Biol. Chem. 270, 254-262.
30. 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.
31. Muhlhausser, P., and Kutay, U. (2007). An in vitro nuclear disassembly system reveals a role for the RanGTPase system and microtubule-dependent steps in nuclear envelope breakdown. J. Cell Biol. 178, 595-610. (Pubitemid 47267272)
32. Nigg, E.A. (2001). Mitotic kinases as regulators of cell division and its checkpoints. Nat. Rev. Mol. Cell Biol. 2, 21-32.
33. Nousiainen, M., Sillje, H.H., Sauer, G., Nigg, E.A., and Korner, R. (2006). Phosphoproteome analysis of the human mitotic spindle. Proc. Natl. Acad. Sci. USA 103, 5391-5396.
34. O'Connell, M.J., Krien, M.J., and Hunter, T. (2003). Never say never. The NIMA-related protein kinases in mitotic control. Trends Cell Biol. 13, 221-228.
35. O'Regan, L., and Fry, A.M. (2009). The Nek6 and Nek7 protein kinases are required for robust mitotic spindle formation and cytokinesis. Mol. Cell. Biol. 29, 3975-3990.
36. O'Regan, L., Blot, J., and Fry, A.M. (2007). Mitotic regulation by NIMA-related kinases. Cell Div. 2, 25.
37. Onischenko, E.A., Gubanova, N.V., Kiseleva, E.V., and Hallberg, E. (2005). Cdk1 and okadaic acid-sensitive phosphatases control assembly of nuclear pore complexes in Drosophila embryos. Mol. Biol. Cell 16, 5152-5162.
38. Osmani, A.H., McGuire, S.L., and Osmani, S.A. (1991). Parallel activation of the NIMA and p34cdc2 cell cycle-regulated protein kinases is required to initiate mitosis in A. nidulans. Cell 67, 283-291. (Pubitemid 121001444)
39. Patel, S.S., Belmont, B.J., Sante, J.M., and Rexach, M.F. (2007). Natively unfolded nucleoporins gate protein diffusion across the nuclear pore complex. Cell 129, 83-96. (Pubitemid 46507580)
40. Powers, M.A., Forbes, D.J., Dahlberg, J.E., and Lund, E. (1997). The vertebrate GLFG nucleoporin, Nup98, is an essential component of multiple RNA export pathways. J. Cell Biol. 136, 241-250.
41. Rapley, J., Nicolas, M., Groen, A., Regue, L., Bertran, M.T., Caelles, C., Avruch, J., and Roig, J. (2008). The NIMA-family kinase Nek6 phosphorylates the kinesin Eg5 at a novel site necessary for mitotic spindle formation. J. Cell Sci. 121, 3912-3921.
42. Schultz, C., Link, A., Leost, M., Zaharevitz, D.W., Gussio, R., Sausville, E.A., Meijer, L., and Kunick, C. (1999). Paullones, a series of cyclin-dependent kinase inhibitors: synthesis, evaluation of CDK1/cyclin B inhibition, and in vitro antitumor activity. J. Med. Chem. 42, 2909-2919.
43. Santamaria, A., Wang, B., Elowe, S., Malik, R., Zhang, F., Bauer, M., Schmidt, A., Sillje, H.H., Koerner, R., and Nigg, E.A. (2010). The Plk1-dependent phosphoproteome of the early mitotic spindle. Mol. Cell. Proteomics 10, M110.004457.
44. Strawn, L.A., Shen, T., Shulga, N., Goldfarb, D.S., and Wente, S.R. (2004). Minimal nuclear pore complexes define FG repeat domains essential for transport. Nat. Cell Biol. 6, 197-206.
45. Terasaki, M., Campagnola, P., Rolls, M.M., Stein, P.A., Ellenberg, J., Hinkle, B., and Slepchenko, B. (2001). A new model for nuclear envelope breakdown. Mol. Biol. Cell 12, 503-510.
46. Terry, L.J., and Wente, S.R. (2009). Flexible gates: dynamic topologies and functions for FG nucleoporins in nucleocytoplasmic transport. Eukaryot. Cell 8, 1814-1827.
47. Wu, W., Baxter, J.E., Wattam, S.L., Hayward, D.G., Fardilha, M., Knebel, A., Ford, E.M., da Cruz e Silva, E.F., and Fry, A.M. (2007). Alternative splicing controls nuclear translocation of the cell cycle-regulated Nek2 kinase. J. Biol. Chem. 282, 26431-26440.
48. Wu, X., Kasper, L.H., Mantcheva, R.T., Mantchev, G.T., Springett, M.J., and van Deursen, J.M. (2001). Disruption of the FG nucleoporin NUP98 causes selective changes in nuclear pore complex stoichiometry and function. Proc. Natl. Acad. Sci. USA 98, 3191-3196.