The methylated N-terminal tail of RCC1 is required for stabilisation of its interaction with chromatin by Ran in live cells

BMC Cell Biology

Volumn 11, Issue , 2010, Pages

  Hitakomate, Ekarat ^a   Hood, Fiona E ^a,b   Sanderson, Helen S ^a   Clarke, Paul R ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTIC ACID; GREEN FLUORESCENT PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; ISOPROTEIN; LYSINE; NUCLEOTIDE; RAN PROTEIN; REGULATOR OF CHROMOSOME CONDENSATION 1 ALPHA PROTEIN; REGULATOR OF CHROMOSOME CONDENSATION 1 PROTEIN; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; NUCLEAR PROTEIN; RCC1 PROTEIN, HUMAN;

AMINO TERMINAL SEQUENCE; ARTICLE; CHROMATIN; CHROMOSOMAL INSTABILITY; CONTROLLED STUDY; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; HUMAN; HUMAN CELL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN METHYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN TRANSPORT; ACTIVE TRANSPORT; ALLOSTERISM; CELL NUCLEUS; GENETICS; HELA CELL; METABOLISM; METHYLATION; MOLECULAR CLONING; MUTATION; PROTEIN TERTIARY STRUCTURE;

ACTIVE TRANSPORT, CELL NUCLEUS; ALLOSTERIC REGULATION; CELL CYCLE PROTEINS; CELL NUCLEUS; CHROMATIN; CLONING, MOLECULAR; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HELA CELLS; HUMANS; METHYLATION; MUTATION; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; RAN GTP-BINDING PROTEIN;

EID: 77953680892     PISSN: None     EISSN: 14712121     Source Type: Journal    
DOI: 10.1186/1471-2121-11-43     Document Type: Article

References (28)

1. Clarke PR, Zhang C. Spatial and temporal coordination of mitosis by Ran GTPase. Nat Rev Mol Cell Biol 2008, 9:464-477. 10.1038/nrm2410, 18478030.
2. Ohtsubo M, Kai R, Furuno N, Sekiguchi T, Sekiguchi M, Hayashida H, Kuma K, Miyata T, Fukushige S, Murotsu T, et al. Isolation and characterization of the active cDNA of the human cell cycle gene (RCC1) involved in the regulation of onset of chromosome condensation. Genes Dev 1987, 1:585-593. 10.1101/gad.1.6.585, 3678831.
3. Bischoff FR, Ponstingl H. Catalysis of guanine nucleotide exchange on Ran by the mitotic regulator RCC1. Nature 1991, 354:80-82. 10.1038/354080a0, 1944575.
4. Ohtsubo M, Okazaki H, Nishimoto T. The RCC1 protein, a regulator for the onset of chromosome condensation locates in the nucleus and binds to DNA. J Cell Biol 1989, 109:1389-1397. 10.1083/jcb.109.4.1389, 2115805, 2677018.
5. Moore W, Zhang C, Clarke PR. Targeting of RCC1 to chromosomes is required for proper mitotic spindle assembly in human cells. Curr Biol 2002, 12:1442-1447. 10.1016/S0960-9822(02)01076-X, 12194828.
6. Bischoff FR, Klebe C, Kretschmer J, Wittinghofer A, Ponstingl H. RanGAP1 induces GTPase activity of nuclear Ras-related Ran. Proc Natl Acad Sci USA 1994, 91:2587-2591. 10.1073/pnas.91.7.2587, 43414, 8146159.
7. Kalab P, Pralle A, Isacoff EY, Heald R, Weis K. Analysis of a RanGTP-regulated gradient in mitotic somatic cells. Nature 2006, 440:697-701. 10.1038/nature04589, 16572176.
8. Görlich D, Mattaj IW. Nucleocytoplasmic transport. Science 1996, 271:1513-1518. 10.1126/science.271.5255.1513, 8599106.
9. Hetzer M, Gruss OJ, Mattaj IW. The Ran GTPase as a marker of chromosome position in spindle formation and nuclear envelope assembly. Nat Cell Biol 2002, 4:E177-184. 10.1038/ncb0702-e177, 12105431.
10. Renault L, Nassar N, Vetter I, Becker J, Klebe C, Roth M, Wittinghofer A. The 1.7 A crystal structure of the regulator of chromosome condensation (RCC1) reveals a seven-bladed propeller. Nature 1998, 392:97-101. 10.1038/32204, 9510255.
11. Renault L, Kuhlmann J, Henkel A, Wittinghofer A. Structural basis for guanine nucleotide exchange on Ran by the regulator of chromosome condensation (RCC1). Cell 2001, 105:245-255. 10.1016/S0092-8674(01)00315-4, 11336674.
12. Azuma Y, Renault L, Garcia-Ranea JA, Valencia A, Nishimoto T, Wittinghofer A. Model of the Ran-RCC1 interaction using biochemical and docking experiments. J Mol Biol 1999, 289:1119-1130. 10.1006/jmbi.1999.2820, 10369786.
13. Hao Y, Macara IG. Regulation of chromatin binding by a conformational switch in the tail of the Ran exchange factor RCC1. J Cell Biol 2008, 182:827-836. 10.1083/jcb.200803110, 2528582, 18762580.
14. Nemergut ME, Mizzen CA, Stukenberg T, Allis CD, Macara IG. Chromatin docking and exchange activity enhancement of RCC1 by histones H2A and H2B. Science 2001, 292:1540-1543. 10.1126/science.292.5521.1540, 11375490.
15. Nemergut ME, Macara IG. Nuclear import of the Ran exchange factor, RCC1, is mediated by at least two distinct mechanisms. J Cell Biol 2000, 149:835-850. 10.1083/jcb.149.4.835, 2174574, 10811825.
16. Talcott B, Moore MS. The nuclear import of RCC1 requires a specific nuclear localization sequence receptor, karyopherin alpha3/Qip. J Biol Chem 2000, 275:10099-10104. 10.1074/jbc.275.14.10099, 10744690.
17. Seino H, Hisamoto N, Uzawa S, Sekiguchi T, Nishimoto T. DNA-binding domain of RCC1 protein is not essential for coupling mitosis with DNA replication. J Cell Sci 1992, 102:393-400.
18. Chen T, Muratore TL, Schaner-Tooley CE, Shabanowitz J, Hunt DF, Macara IG. N-terminal alpha-methylation of RCC1 is necessary for stable chromatin association and normal mitosis. Nat Cell Biol 2007, 9:596-603. 10.1038/ncb1572, 17435751.
19. Hutchins JR, Moore WJ, Hood FE, Wilson JS, Andrews PD, Swedlow JR, Clarke PR. Phosphorylation regulates the dynamic interaction of RCC1 with chromosomes during mitosis. Curr Biol 2004, 14:1099-1104. 10.1016/j.cub.2004.05.021, 15203004.
20. Li HY, 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. 10.1101/gad.1177304, 374234, 15014043.
21. Hood FE, Clarke PR. RCC1 isoforms differ in their affinity for chromatin, molecular interactions and regulation by phosphorylation. J Cell Sci 2007, 120:3436-3445. 10.1242/jcs.009092, 17855385.
22. Li HY, Wirtz D, Zheng Y. A mechanism of coupling RCC1 mobility to RanGTP production on the chromatin in vivo. J Cell Biol 2003, 160:635-644. 10.1083/jcb.200211004, 2173367, 12604592.
23. Cushman I, Stenoien D, Moore MS. The dynamic association of RCC1 with chromatin is modulated by Ran-dependent nuclear transport. Mol Biol Cell 2004, 15:245-255. 10.1091/mbc.E03-06-0409, 307544, 14565978.
24. Dasso M, Seki T, Azuma Y, Ohba T, Nishimoto T. A mutant form of the Ran/TC4 protein disrupts nuclear function in Xenopus laevis egg extracts by inhibiting the RCC1 protein, a regulator of chromosome condensation. EMBO J 1994, 13:5732-5744. 395539, 7988569.
25. Klebe C, Bischoff FR, Ponstingl H, Wittinghofer A. Interaction of the nuclear GTP-binding protein Ran with its regulatory proteins RCC1 and RanGAP1. Biochemistry 1995, 34:639-647. 10.1021/bi00002a031, 7819259.
26. Hutchins JR, Moore WJ, Clarke PR. Dynamic localisation of Ran GTPase during the cell cycle. BMC Cell Biol 2009, 10:66. 10.1186/1471-2121-10-66, 2755469, 19765287.
27. Bischoff FR, 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. 398135, 7882974.
28. England JR, Huang J, Jennings MJ, Makde RD, Tan S. RCC1 Uses a Conformationally Diverse Loop Region to Interact with the Nucleosome: A Model for the RCC1-Nucleosome Complex. J Mol Biol 2010, 398:518-529. 10.1016/j.jmb.2010.03.037, 20347844.