RanBP1 governs spindle assembly by defining mitotic Ran-GTP production

Developmental Cell

Volumn 31, Issue 4, 2014, Pages 393-404

  Zhang, MichaelShaofei ^a   Arnaoutov, Alexei ^a   Dasso, Mary ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATE; RAN PROTEIN; RANBP1 PROTEIN; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; CHROMATIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; NUCLEAR PROTEIN; RAN-BINDING PROTEIN 1; XENOPUS PROTEIN;

ANAPHASE; ARTICLE; CELL CYCLE; CELL CYCLE M PHASE; CELL NUCLEUS MEMBRANE; CHROMATIN; CHROMOSOME CONDENSATION; ENZYME ACTIVITY; METAPHASE; MITOSIS SPINDLE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; REGULATORY MECHANISM; SOMATIC CELL; WESTERN BLOTTING; XENOPUS; XENOPUS LAEVIS; ANIMAL; BIOSYNTHESIS; GENETICS; METABOLISM; MITOSIS; PHYSIOLOGY; SPINDLE APPARATUS;

ANIMALS; CELL CYCLE PROTEINS; CHROMATIN; GUANINE NUCLEOTIDE EXCHANGE FACTORS; GUANOSINE TRIPHOSPHATE; MITOSIS; NUCLEAR PROTEINS; RAN GTP-BINDING PROTEIN; SPINDLE APPARATUS; XENOPUS; XENOPUS PROTEINS;

EID: 84921274078     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2014.10.014     Document Type: Article

References (40)

1. Amato R., Scumaci D., D'Antona L., Iuliano R., Menniti M., Di Sanzo M., Faniello M.C., Colao E., Malatesta P., Zingone A., et al. Sgk1 enhances RANBP1 transcript levels and decreases taxol sensitivity in RKO colon carcinoma cells. Oncogene 2013, 32:4572-4578.
2. Arnaoutov A., Dasso M. The Ran GTPase regulates kinetochore function. Dev. Cell 2003, 5:99-111.
3. Beddow A.L., Richards S.A., Orem N.R., Macara I.G. The Ran/TC4 GTPase-binding domain: identification by expression cloning and characterization of a conserved sequence motif. Proc. Natl. Acad. Sci. USA 1995, 92:3328-3332.
4. Bischoff F.R., Görlich D. RanBP1 is crucial for the release of RanGTP from importin beta-related nuclear transport factors. FEBS Lett. 1997, 419:249-254.
5. Bischoff F.R., Krebber H., Smirnova E., Dong W., Ponstingl H. Co-activation of RanGTPase and inhibition of GTP dissociation by Ran-GTP binding protein RanBP1. EMBO J. 1995, 14:705-715.
6. Carazo-Salas R.E., Guarguaglini G., Gruss O.J., Segref A., Karsenti E., Mattaj I.W. Generation of GTP-bound Ran by RCC1 is required for chromatin-induced mitotic spindle formation. Nature 1999, 400:178-181.
7. Chen T., Muratore T.L., Schaner-Tooley C.E., Shabanowitz J., Hunt D.F., Macara I.G. N-terminal alpha-methylation of RCC1 is necessary for stable chromatin association and normal mitosis. Nat. Cell Biol. 2007, 9:596-603.
8. Ciciarello M., Roscioli E., Di Fiore B., Di Francesco L., Sobrero F., Bernard D., Mangiacasale R., Harel A., Schininà M.E., Lavia P. Nuclear reformation after mitosis requires downregulation of the Ran GTPase effector RanBP1 in mammalian cells. Chromosoma 2010, 119:651-668.
9. Clarke P.R., Zhang C. Spatial and temporal coordination of mitosis by Ran GTPase. Nat. Rev. Mol. Cell Biol. 2008, 9:464-477.
10. Dasso M. The Ran GTPase: theme and variations. Curr. Biol. 2002, 12:R502-508.
11. Dasso M., Nishitani H., Kornbluth S., Nishimoto T., Newport J.W. RCC1, a regulator of mitosis, is essential for DNA replication. Mol. Cell. Biol. 1992, 12:3337-3345.
12. Frasch M. The maternally expressed Drosophila gene encoding the chromatin-binding protein BJ1 is a homolog of the vertebrate gene Regulator of Chromatin Condensation, RCC1. EMBO J. 1991, 10:1225-1236.
13. Halpin D., Kalab P., Wang J., Weis K., Heald R. Mitotic spindle assembly around RCC1-coated beads in Xenopus egg extracts. PLoS Biol. 2011, 9:e1001225.
14. Hasegawa K., Ryu S.J., Kaláb P. Chromosomal gain promotes formation of a steep RanGTP gradient that drives mitosis in aneuploid cells. J.Cell Biol. 2013, 200:151-161.
15. Hatch E.M., Fischer A.H., Deerinck T.J., Hetzer M.W. Catastrophic nuclear envelope collapse in cancer cell micronuclei. Cell 2013, 154:47-60.
16. Hitakomate E., Hood F.E., Sanderson H.S., Clarke P.R. The methylated N-terminal tail of RCC1 is required for stabilisation of its interaction with chromatin by Ran in live cells. BMC Cell Biol. 2010, 11:43.
17. Hutchins J.R., Moore W.J., Hood F.E., Wilson J.S., Andrews P.D., Swedlow J.R., Clarke P.R. Phosphorylation regulates the dynamic interaction of RCC1 with chromosomes during mitosis. Curr. Biol. 2004, 14:1099-1104.
18. Hwang H.I., Ji J.H., Jang Y.J. Phosphorylation of Ran-binding protein-1 by Polo-like kinase-1 is required for interaction with Ran and early mitotic progression. J.Biol. Chem. 2011, 286:33012-33020.
19. Kalab P., Heald R. The RanGTP gradient - a GPS for the mitotic spindle. J.Cell Sci. 2008, 121:1577-1586.
20. Kalab P., Pu R.T., Dasso M. The Ran GTPase regulates mitotic spindle assembly. Curr. Biol. 1999, 9:481-484.
21. Kalab P., Weis K., Heald R. Visualization of a Ran-GTP gradient in interphase and mitotic Xenopus egg extracts. Science 2002, 295:2452-2456.
22. Kaláb P., Pralle A., Isacoff E.Y., Heald R., Weis K. Analysis of a RanGTP-regulated gradient in mitotic somatic cells. Nature 2006, 440:697-701.
23. Li H.Y., Zheng Y. Phosphorylation of RCC1 in mitosis is essential for producing a high RanGTP concentration on chromosomes and for spindle assembly in mammalian cells. Genes Dev. 2004, 18:512-527.
24. Li H.Y., Ng W.P., Wong C.H., Iglesias P.A., Zheng Y. Coordination of chromosome alignment and mitotic progression by the chromosome-based Ran signal. Cell Cycle 2007, 6:1886-1895.
25. Lounsbury K.M., Macara I.G. Ran-binding protein 1 (RanBP1) forms a ternary complex with Ran and karyopherin beta and reduces Ran GTPase-activating protein (RanGAP) inhibition by karyopherin beta. J.Biol. Chem. 1997, 272:551-555.
26. Ly D.H., Lockhart D.J., Lerner R.A., Schultz P.G. Mitotic misregulation and human aging. Science 2000, 287:2486-2492.
27. Murray A.W. Cell cycle extracts. Methods Cell Biol. 1991, 36:581-605.
28. Murray A.W., Kirschner M.W. Cyclin synthesis drives the early embryonic cell cycle. Nature 1989, 339:275-280.
29. Nemergut M.E., Mizzen C.A., Stukenberg T., Allis C.D., Macara I.G. Chromatin docking and exchange activity enhancement of RCC1 by histones H2A and H2B. Science 2001, 292:1540-1543.
30. Newport J., Kirschner M. A major developmental transition in early Xenopus embryos: I. characterization and timing of cellular changes at the midblastula stage. Cell 1982, 30:675-686.
31. Ohba T., Nakamura M., Nishitani H., Nishimoto T. Self-organization of microtubule asters induced in Xenopus egg extracts by GTP-bound Ran. Science 1999, 284:1356-1358.
32. Ouspenski I.I. A RanBP1 mutation which does not visibly affect nuclear import may reveal additional functions of the ran GTPase system. Exp. Cell Res. 1998, 244:171-183.
33. Pu R.T., Dasso M. The balance of RanBP1 and RCC1 is critical for nuclear assembly and nuclear transport. Mol. Biol. Cell 1997, 8:1955-1970.
34. Pujol G., Söderqvist H., Radu A. Age-associated reduction of nuclear protein import in human fibroblasts. Biochem. Biophys. Res. Commun. 2002, 294:354-358.
35. Rensen W.M., Mangiacasale R., Ciciarello M., Lavia P. The GTPase Ran: regulation of cell life and potential roles in cell transformation. Front. Biosci. 2008, 13:4097-4121.
36. Richards S.A., Lounsbury K.M., Macara I.G. The C terminus of the nuclear RAN/TC4 GTPase stabilizes the GDP-bound state and mediates interactions with RCC1, RAN-GAP, and HTF9A/RANBP1. J.Biol. Chem. 1995, 270:14405-14411.
37. Richards S.A., Lounsbury K.M., Carey K.L., Macara I.G. A nuclear export signal is essential for the cytosolic localization of the Ran binding protein, RanBP1. J.Cell Biol. 1996, 134:1157-1168.
38. Tedeschi A., Ciciarello M., Mangiacasale R., Roscioli E., Rensen W.M., Lavia P. RANBP1 localizes a subset of mitotic regulatory factors on spindle microtubules and regulates chromosome segregation in human cells. J.Cell Sci. 2007, 120:3748-3761.
39. Vetter I.R., Nowak C., Nishimoto T., Kuhlmann J., Wittinghofer A. Structure of a Ran-binding domain complexed with Ran bound to a GTP analogue: implications for nuclear transport. Nature 1999, 398:39-46.
40. Zhang C., Hughes M., Clarke P.R. Ran-GTP stabilises microtubule asters and inhibits nuclear assembly in Xenopus egg extracts. J.Cell Sci. 1999, 112:2453-2461.