Inhibiting Crm1 causes the formation of excess acentriolar spindle poles containing NuMA and B23, but does not affect centrosome numbers

Biology of the Cell

Volumn 101, Issue 12, 2009, Pages 679-693

  Rousselet, Annie ^a,b  

^a INSTITUT CURIE   (France)

^b ESPCI   (France)

Author keywords

B23; Centrosome duplication; Crm1; Quiescent; Spindle

Indexed keywords

EXPORTIN 1; GAMMA TUBULIN; NUCLEOPHOSMIN;

ANIMAL CELL; ARTICLE; CELL COUNT; CELL GROWTH; CENTROMERE; CENTROSOME; CHROMOSOME DUPLICATION; CONTROLLED STUDY; CYTOKINESIS; ENZYME INHIBITION; HUMAN; HUMAN CELL; METAPHASE; MICROTUBULE; MITOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMETAPHASE; PROTEIN LOCALIZATION; PROTEIN POLYMERIZATION; PROTEIN STRUCTURE; PROTEIN TRANSPORT;

ANIMALS; ANTIGENS, NUCLEAR; CELL LINE; CENTROSOME; DOWN-REGULATION; HUMANS; KARYOPHERINS; METAPHASE; MICE; MITOTIC SPINDLE APPARATUS; NUCLEAR MATRIX-ASSOCIATED PROTEINS; NUCLEAR PROTEINS; PROTEIN TRANSPORT; RECEPTORS, CYTOPLASMIC AND NUCLEAR;

EID: 70350124039     PISSN: 02484900     EISSN: 1768322X     Source Type: Journal    
DOI: 10.1042/BC20080218     Document Type: Article

References (46)

1. Amin, M.A., Matsunaga, S., Uchiyama, S. and Fukui, K. (2008) Nucleophosmin is required for chromosome congression, proper mitotic spindle formation, and kinetochore-microtubule attachment in HeLa cells. FEBS Lett. 582, 3839-3844
2. Arnaoutov, A., Azuma, Y., Ribbeck, K., Joseph, J., Boyarchuk, Y., Karpova, T., McNally, J. and Dasso, M. (2005) Crm1 is a mitotic effector of Ran-GTP in somatic cells. Nat. Cell Biol. 7, 626-632
3. Balczon, R., Bao, L., Zimmer, W.E., Brown, K., Zinkowski, R.P. and Brinkley, B.R. (1995) Dissociation of centrosome replication events from cycles of DNA synthesis and mitotic division in hydroxyurea-arrested Chinese hamster ovary cells. J. Cell Biol. 130, 105-115
4. Bonetti, P., Davoli, T., Sironi, C., Amati, B., Pelicci, P.G. and Colombo, E. (2008) Nucleophosmin and its AML-associated mutant regulate c-Myc turnover through Fbw7 gamma. J. Cell Biol. 182, 19-26
5. Borer, R.A., Lehner, C.F., Eppenberger, H.M. and Nigg, E.A. (1989) Major nucleolar proteins shuttle between nucleus and cytoplasm. Cell 56, 379-390
6. Bornens, M. and Moudjou, M. (1999) Studying the composition and function of centrosomes in vertebrates. Methods Cell Biol. 61, 13-34
7. Chan, P.K. and Chan, F.Y. (1995) Nucleophosmin/B23 (NPM) oligomer is a major and stable entity in HeLa cells. Biochim. Biophys. Acta 1262, 37-42
8. Chen, W., Rassidakis, G.Z. and Medeiros, L.J. (2006) Nucleophosmin gene mutations in acute myeloid leukemia. Arch. Pathol. Lab. Med. 130, 1687-1692
9. Ciciarello, M., Mangiacasale, R. and Lavia, P. (2007) Spatial control of mitosis by the GTPase Ran. Cell. Mol. Life Sci. 64, 1891-1914
10. Di Fiore, B., Ciciarello, M., Mangiacasale, R., Palena, A., Tassin, A.M., Cundari, E. and Lavia, P. (2003) Mammalian RanBP1 regulates centrosome cohesion during mitosis. J. Cell Sci. 116, 3399-3411
11. Di Fiore, B., Ciciarello, M. and Lavia, P. (2004) Mitotic functions of the Ran GTPase network: the importance of being in the right place at the right time. Cell Cycle 3, 305-313
12. Dundr, M., Misteli, T. and Olson, M.O. (2000) The dynamics of postmitotic reassembly of the nucleolus. J. Cell Biol. 150, 433-446
13. Eirin-Lopez, J.M., Frehlick, L.J. and Ausio, J. (2006) Long-term evolution and functional diversification in the members of the nucleophosmin/nucleoplasmin family of nuclear chaperones. Genetics 173, 1835-1850
14. Falini, B., Mecucci, C., Tiacci, E., Alcalay, M., Rosati, R., Pasqualucci, L., La Starza, R., Diverio, D., Colombo, E., Santucci, A. et al. (2005) Cytoplasmic nucleophosmin in acute myelogenous leukemia with a normal karyotype. N. Engl. J. Med. 352, 254-266
15. Frehlick, L.J., Eirin-Lopez, J.M. and Ausio, J. (2007) New insights into the nucleophosmin/nucleoplasmin family of nuclear chaperones. BioEssays 29, 49-59
16. Gaglio, T., Saredi, A. and Compton, D.A. (1995) NuMA is required for the organization of microtubules into aster-like mitotic arrays. J. Cell Biol. 131, 693-708
17. Grisendi, S., Bernardi, R., Rossi, M., Cheng, K., Khandker, L., Manova, K. and Pandolfi, P.P. (2005) Role of nucleophosmin in embryonic development and tumorigenesis. Nature 437, 147-153
18. Grisendi, S., Mecucci, C., Falini, B. and Pandolfi, P.P. (2006) Nucleophosmin and cancer. Nat. Rev. Cancer 6, 493-505
19. Herrera, J.E., Savkur, R. and Olson, M.O. (1995) The ribonuclease activity of nucleolar protein B23. Nucleic Acids Res. 23, 3974-3979
20. Hingorani, K., Szebeni, A. and Olson, M.O. (2000) Mapping the functional domains of nucleolar protein B23. J. Biol. Chem. 275, 24451-24457
21. Jiang, P.S., Chang, J.H. and Yung, B.Y. (2000) Different kinases phosphorylate nucleophosmin/B23 at different sites during G(2) and M phases of the cell cycle. Cancer Lett. 153, 151-160
22. Khodjakov, A., Copenagle, L., Gordon, M.B., Compton, D.A. and Kapoor, T.M. (2003) Minus-end capture of preformed kinetochore fibers contributes to spindle morphogenesis. J. Cell Biol. 160, 671-683
23. Maggi, Jr, L.B., Kuchenruether, M., Dadey, D.Y., Schwope, R.M., Grisendi, S., Townsend, R.R., Pandolfi, P.P. and Weber, J.D. (2008) Nucleophosmin serves as a rate-limiting nuclear export chaperone for the mammalian ribosome. Mol. Cell. Biol. 28, 7050-7065
24. Maiato, H., Rieder, C.L. and Khodjakov, A. (2004) Kinetochore-driven formation of kinetochore fibers contributes to spindle assembly during animal mitosis. J. Cell Biol. 167, 831-840
25. Manning, A.L. and Compton, D.A. (2007) Mechanisms of spindle-pole organization are influenced by kinetochore activity in mammalian cells. Curr. Biol. 17, 260-265
26. Manning, A.L. and Compton, D.A. (2008) Structural and regulatory roles of nonmotor spindle proteins. Curr. Opin. Cell Biol. 20, 101-106
27. Mariano, A.R., Colombo, E., Luzi, L., Martinelli, P., Volorio, S., Bernard, L., Meani, N., Bergomas, R., Alcalay, M. and Pelicci, P.G. (2006) Cytoplasmic localization of NPM in myeloid leukemias is dictated by gain-of-function mutations that create a functional nuclear export signal. Oncogene 25, 4376-4380
28. Moudjou, M., Bordes, N., Paintrand, M. and Bornens, M. (1996) gamma-Tubulin in mammalian cells: the centrosomal and the cytosolic forms. J. Cell Sci. 109, 875-887
29. Nachury, M.V., Maresca, T.J., Salmon, W.C., Waterman-Storer, C.M., Heald, R. and Weis, K. (2001) Importin β is a mitotic target of the small GTPase Ran in spindle assembly. Cell 104, 95-106
30. Neben, K.,Glesecke,C., Schwelzer, S., Ho, A.D. and A, Krämer. (2003) Centrosome aberrations in acute myeloid leukemia are correlated with cytogenic risk profile. Blood 101, 289-291
31. Negi, S.S. and Olson, M.O. (2006) Effects of interphase and mitotic phosphorylation on the mobility and location of nucleolar protein B23. J. Cell Sci. 119, 3676-3685
32. Nishimura, Y., Ohkubo, T., Furuichi, Y. and Umekawa, H. (2002) Tryptophans 286 and 288 in the C-terminal region of protein B23.1 are important for its nucleolar localization. Biosci. Biotechnol. Biochem. 66, 2239-2242
33. O'Connell, C.B. and Khodjakov, A.L. (2007) Cooperative mechanisms of mitotic spindle formation. J. Cell Sci: 120, 1717-1722
34. Okuda, M. (2002) The role of nucleophosmin in centrosome duplication. Oncogene 21, 6170-6174
35. Okuda, M., Horn, H.F., Tarapore, P., Tokuyama, Y., Smulian, A.G., Chan, P.K., Knudsen, E.S., Hofmann, I.A., Snyder, J.D., Bove, K.E. et al. (2000) Nucleophosmin/B23 is a target of CDK2/cyclin E in centrosome duplication. Cell 103, 127-140
36. Piel, M., Meyer, P., Khodjakov, A., Rieder, C.L. and Bornens, M. (2000) The respective contributions of the mother and daughter centrioles to centrosome activity and behavior in vertebrate cells. J. Cell Biol. 149, 317-330
37. Taddei, A., Roche, D., Sibarita, J.B., Turner, B.M. and Almouzni, G. (1999) Duplication and maintenance of heterochromatin domains. J. Cell Biol. 147, 1153-1166
38. Tassin, A.M., Celati, C., Moudjou, M. and Bornens, M. (1998) Characterization of the human homologue of the yeast spc98p and its association with gamma-tubulin. J. Cell Biol. 141, 689-701
39. Tokuyama, Y., Henning, H.F., Kawamura, K., Tarapore, P. and Fukasawa, K. (2001) Specific phosphorylation of nucleophosmin on Thr199 by CDK2/ cyclin E, and its role in centrosome duplication. J. Biol. Chem. 27, 21529-21537
40. Torosantucci, L., De Luca, M., Guarguaglini, G., Lavia, P. and Degrassi, F. (2008) Localized RanGTP accumulation promotes microtubule nucleation at kinetochores in somatic mammalian cells. Mol. Biol. Cell 19, 1873-1882
41. Tournier, F., Komesli, S., Paintrand, M., Job, D. and Bornens, M. (1991) The intercentriolar linkage is critical for the ability of heterologous centrosomes to induce parthenogenesis in Xenopus. J. Cell Biol. 113, 1361-1369
42. Tulu, U.S., Fagerstrom, C., Ferenz, N.P. and Wadsworth, P. (2006) Molecular requirements for kinetochore-associated microtubule formation in mammalian cells. Curr. Biol. 16, 536-541
43. Wang, W., Budhu, A., Forgues, M. and Wang, X.W. (2005) Temporal and spatial control of nucleophosmin by the Ran-Crm1 complex in centrosome duplication. Nat. Cell Biol. 7, 823-830
44. Wolff, A., de Nechaud, B., Chillet, D., Mazarguil, H., Desbruyeres, E., Audebert, S., Edde, B., Gros, F. and Denoulet, P. (1992) Distribution of glutamylated alpha and beta-tubulin in mouse tissues using a specific monoclonal antibody, GT335. Eur. J. Cell Biol. 59, 425-432
45. Yu, Y., Maggi, Jr, L.B., Brady, S.N., Apicelli, A.J., Dai, M.S., Lu, H. and Weber, J.D. (2006) Nucleophosmin is essential for ribosomal protein L5 nuclear export. Mol. Cell. Biol. 26, 3798-3809
46. Zatsepina, O.V., Rousselet, A., Chan, P.K., Olson, M.O., Jordan, E.G. and Bornens, M. (1999) The nucleolar phosphoprotein B23 redistributes in part to the spindle poles during mitosis. J. Cell Sci. 112, 455-466