Three-step model for condensin activation during mitotic chromosome condensation

Cell Cycle

Volumn 9, Issue 16, 2010, Pages 3263-3275

  Bazile, Franck ^a   St Pierre, Julie ^b   D'Amours, Damien ^a  

^a INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

Chromosome condensation; Condensin; Cyclin dependent kinase; Genome integrity; Mitosis; Polo kinase

Indexed keywords

AURORA B KINASE; CASEIN KINASE II; CONDENSIN; CYCLIN DEPENDENT KINASE 1; DNA; PROTEOME;

ANAPHASE; CELL CYCLE; CHROMOSOME CONDENSATION; DNA BINDING; DNA SUPERCOILING; ENZYME ACTIVITY; GENE ACTIVATION; GENETIC MODEL; HUMAN; MASS SPECTROMETRY; MITOSIS; PROPHASE; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; RECEPTOR SENSITIVITY; REVIEW;

EID: 77955734595     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.9.16.12620     Document Type: Review

References (67)

1. Hirano T. At the heart of the chromosome: SMC proteins in action. Nat Rev Mol Cell Biol 2006; 7:311-22.
2. Hudson DF, Marshall KM, Earnshaw WC. Condensin: Architect of mitotic chromosomes. Chromosome Res 2009; 17:131-44.
3. Saka Y, Sutani T, Yamashita Y, Saitoh S, Takeuchi M, Nakaseko Y, et al. Fission yeast cut3 and cut14, members of a ubiquitous protein family, are required for chromosome condensation and segregation in mitosis. EMBO Journal 1994; 13:4938-52. (Pubitemid 24319377)
4. Strunnikov AV, Hogan E, Koshland D. SMC2, a Saccharomyces cerevisiae gene essential for chromosome segregation and condensation, defines a subgroup within the SMC family. Genes and Development 1995; 9:587-99.
5. Hudson DF, Vagnarelli P, Gassmann R, Earnshaw WC. Condensin is required for nonhistone protein assembly and structural integrity of vertebrate mitotic chromosomes. Dev Cell 2003; 5:323-36. (Pubitemid 37006475)
6. Ono T, Losada A, Hirano M, Myers MP, Neuwald AF, Hirano T. Differential contributions of condensin I and condensin II to mitotic chromosome architecture in vertebrate cells. Cell 2003; 115:109-21. (Pubitemid 37255322)
7. Gerlich D, Hirota T, Koch B, Peters JM, Ellenberg J. Condensin I stabilizes chromosomes mechanically through a dynamic interaction in live cells. Curr Biol 2006; 16:333-44. (Pubitemid 43259343)
8. Vagnarelli P, Hudson DF, Ribeiro SA, Trinkle-Mulcahy L, Spence JM, Lai F, et al. Condensin and Repo-Man-PP1 co-operate in the regulation of chromosome architecture during mitosis. Nat Cell Biol 2006; 8:1133-42. (Pubitemid 44473609)
9. Mora-Bermudez F, Gerlich D, Ellenberg J. Maximal chromosome compaction occurs by axial shortening in anaphase and depends on Aurora kinase. Nat Cell Biol 2007; 9:822-31. (Pubitemid 47019469)
10. Gurdon JB. Changes in somatic cell nuclei inserted into growing and maturing amphibian oocytes. J Embryol Exp Morphol 1968; 20:401-14.
11. McCleland ML, O'Farrell PH. RNAi of mitotic cyclins in Drosophila uncouples the nuclear and centrosome cycle. Curr Biol 2008; 18:245-54.
12. McCleland ML, Farrell JA, O'Farrell PH. Influence of cyclin type and dose on mitotic entry and progression in the early Drosophila embryo. J Cell Biol 2009; 184:639-46.
13. Kimura K, Hirano M, Kobayashi R, Hirano T. Phosphorylation and activation of 13S condensin by Cdc2 in vitro. Science 1998; 282:487-90. (Pubitemid 28483678)
14. Freeman L, Aragon-Alcaide L, Strunnikov A. The condensin complex governs chromosome condensation and mitotic transmission of rDNA. Journal of Cell Biology 2000; 149:811-24.
15. Takemoto A, Kimura K, Yokoyama S, Hanaoka F. Cell cycle-dependent phosphorylation, nuclear localization and activation of human condensin. J Biol Chem 2004; 279:4551-9.
16. Hirota T, Gerlich D, Koch B, Ellenberg J, Peters JM. Distinct functions of condensin I and II in mitotic chromosome assembly. J Cell Sci 2004; 117:6435-45.
17. Ono T, Fang Y, Spector DL, Hirano T. Spatial and temporal regulation of Condensins I and II in mitotic chromosome assembly in human cells. Mol Biol Cell 2004; 15:3296-308.
18. Takemoto A, Kimura K, Yanagisawa J, Yokoyama S, Hanaoka F. Negative regulation of condensin I by CK2-mediated phosphorylation. EMBO J 2006; 25:5339-48.
19. Lipp JJ, Hirota T, Poser I, Peters JM. Aurora B controls the association of condensin I but not condensin II with mitotic chromosomes. J Cell Sci 2007; 120:1245-55.
20. St-Pierre J, Douziech M, Bazile F, Pascariu M, Bonneil E, Sauve V, et al. Polo kinase regulates mitotic chromosome condensation by hyperactivation of condensin DNA supercoiling activity. Mol Cell 2009; 34:416-26.
21. Giet R, Glover DM. Drosophila aurora B kinase is required for histone H3 phosphorylation and condensin recruitment during chromosome condensation and to organize the central spindle during cytokinesis. J Cell Biol 2001; 152:669-82.
22. Hagstrom KA, Holmes VF, Cozzarelli NR, Meyer BJ. C. elegans condensin promotes mitotic chromosome architecture, centromere organization and sister chromatid segregation during mitosis and meiosis. Genes & Development 2002; 16:729-42.
23. Kaitna S, Pasierbek P, Jantsch M, Loidl J, Glotzer M. The aurora B kinase AIR-2 regulates kinetochores during mitosis and is required for separation of homologous Chromosomes during meiosis. Curr Biol 2002; 12:798-812.
24. Petersen J, Hagan IM. S. pombe aurora kinase/survivin is required for chromosome condensation and the spindle checkpoint attachment response. Current Biology 2003; 13:590-7.
25. Lavoie BD, Hogan E, Koshland D. In vivo requirements for rDNA chromosome condensation reveal two cell cycle-regulated pathways for mitotic chromosome folding. [erratum appears in Genes Dev 2004; 18:355]. Genes and Development 2004; 18:76-87.
26. Takemoto A, Murayama A, Katano M, Urano T, Furukawa K, Yokoyama S, et al. Analysis of the role of Aurora B on the chromosomal targeting of condensin I. Nucleic Acids Res 2007; 35:2403-12.
27. 2-M transition. EMBO J 1990; 9:2563-72.
28. Pines J, Hunter T. Human cyclins A and B1 are differentially located in the cell and undergo cell cycle-dependent nuclear transport. J Cell Biol 1991; 115:1-17.
29. Yeong FM, Lim HH, Padmashree CG, Surana U. Exit from mitosis in budding yeast: biphasic inactivation of the Cdc28-Clb2 mitotic kinase and the role of Cdc20. Mol Cell 2000; 5:501-11.
30. Guacci V, Hogan E, Koshland D. Chromosome condensation and sister chromatid pairing in budding yeast. Journal of Cell Biology 1994; 125:517-30.
31. Beausoleil SA, Jedrychowski M, Schwartz D, Elias JE, Villen J, Li J, et al. Large-scale characterization of HeLa cell nuclear phosphoproteins. Proc Natl Acad Sci USA 2004; 101:12130-5.
32. Hornbeck PV, Chabra I, Kornhauser JM, Skrzypek E, Zhang B. PhosphoSite: A bioinformatics resource dedicated to physiological protein phosphorylation. Proteomics 2004; 4:1551-61.
33. Nousiainen M, Sillje HH, Sauer G, Nigg EA, Korner R. Phosphoproteome analysis of the human mitotic spindle. Proc Natl Acad Sci USA 2006; 103:5391-6.
34. Rikova K, Guo A, Zeng Q, Possemato A, Yu J, Haack H, et al. Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer. Cell 2007; 131:1190-203.
35. Smolka MB, Albuquerque CP, Chen SH, Zhou H. Proteome-wide identification of in vivo targets of DNA damage checkpoint kinases. Proc Natl Acad Sci USA 2007; 104:10364-9.
36. Villen J, Beausoleil SA, Gerber SA, Gygi SP. Large-scale phosphorylation analysis of mouse liver. Proc Natl Acad Sci USA 2007; 104:1488-93.
37. Yu LR, Zhu Z, Chan KC, Issaq HJ, Dimitrov DS, Veenstra TD. Improved titanium dioxide enrichment of phosphopeptides from HeLa cells and high confident phosphopeptide identification by cross-validation of MS/MS and MS/MS/MS spectra. J Proteome Res 2007; 6:4150-62. (Pubitemid 350158493)
38. Albuquerque CP, Smolka MB, Payne SH, Bafna V, Eng J, Zhou H. A multidimensional chromatography technology for in-depth phosphoproteome analysis. Mol Cell Proteomics 2008; 7:1389-96. (Pubitemid 352038280)
39. Bodenmiller B, Campbell D, Gerrits B, Lam H, Jovanovic M, Picotti P, et al. PhosphoPep - a database of protein phosphorylation sites in model organisms. Nat Biotechnol 2008; 26:1339-40.
40. Daub H, Olsen JV, Bairlein M, Gnad F, Oppermann FS, Korner R, et al. Kinase-selective enrichment enables quantitative phosphoproteomics of the kinome across the cell cycle. Mol Cell 2008; 31:438-48.
41. Dephoure N, Zhou C, Villen J, Beausoleil SA, Bakalarski CE, Elledge SJ, et al. A quantitative atlas of mitotic phosphorylation. Proc Natl Acad Sci USA 2008; 105:10762-7.
42. Sui S, Wang J, Yang B, Song L, Zhang J, Chen M, et al. Phosphoproteome analysis of the human Chang liver cells using SCX and a complementary mass spectrometric strategy. Proteomics 2008; 8:2024-34.
43. Holt LJ, Tuch BB, Villen J, Johnson AD, Gygi SP, Morgan DO. Global analysis of Cdk1 substrate phosphorylation sites provides insights into evolution. Science 2009; 325:1682-6.
44. Oppermann FS, Gnad F, Olsen JV, Hornberger R, Greff Z, Keri G, et al. Large-scale proteomics analysis of the human kinome. Mol Cell Proteomics 2009; 8:1751-64.
45. Murphy LA, Sarge KD. Phosphorylation of CAP-G is required for its chromosomal DNA localization during mitosis. Biochem Biophys Res Commun 2008; 377:1007-11.
46. Kraft C, Herzog F, Gieffers C, Mechtler K, Hagting A, Pines J, et al. Mitotic regulation of the human anaphase-promoting complex by phosphorylation. EMBO J 2003; 22:6598-609. (Pubitemid 38009606)
47. Songyang Z, Blechner S, Hoagland N, Hoekstra MF, Piwnica-Worms H, Cantley LC. Use of an oriented peptide library to determine the optimal substrates of protein kinases. Curr Biol 1994; 4:973-82. (Pubitemid 124001033)
48. Nakajima H, Toyoshima-Morimoto F, Taniguchi E, Nishida E. Identification of a consensus motif for Plk (Polo-like kinase) phosphorylation reveals Myt1 as a Plk1 substrate. J Biol Chem 2003; 278:25277-80. (Pubitemid 36835273)
49. Kimura K, Cuvier O, Hirano T. Chromosome condensation by a human condensin complex in Xenopus egg extracts. J Biol Chem 2001; 276:5417-20. (Pubitemid 37385681)
50. Clark DJ, Leblanc B. Analysis of DNA super-coiling induced by DNA-protein interactions. Methods Mol Biol 2009; 543:523-35.
51. Stern B, Nurse P. A quantitative model for the cdc2 control of S phase and mitosis in fission yeast. Trends Genet 1996; 12:345-50. (Pubitemid 26294693)
52. Ball AR Jr, Schmiesing JA, Zhou C, Gregson HC, Okada Y, Doi T, et al. Identification of a chromosome-targeting domain in the human condensin subunit CNAP1/hCAP-D2/Eg7. Mol Cell Biol 2002; 22:5769-81. (Pubitemid 34815826)
53. Sutani T, Yuasa T, Tomonaga T, Dohmae N, Takio K, Yanagida M. Fission yeast condensin complex: essential roles of non-SMC subunits for condensation and Cdc2 phosphorylation of Cut3/SMC4. Genes & Development 1999; 13:2271-83. (Pubitemid 29426731)
54. Ubersax JA, Woodbury EL, Quang PN, Paraz M, Blethrow JD, Shah K, et al. Targets of the cyclin-dependent kinase Cdk1. Nature 2003; 425:859-64.
55. Hagting A, Jackman M, Simpson K, Pines J. Translocation of cyclin B1 to the nucleus at prophase requires a phosphorylation-dependent nuclear import signal. Curr Biol 1999; 9:680-9. (Pubitemid 29332349)
56. Morishita J, Matsusaka T, Goshima G, Nakamura T, Tatebe H, Yanagida M. Bir1/Cut17 moving from chromosome to spindle upon the loss of cohesion is required for condensation, spindle elongation and repair. Genes to Cells 2001; 6:743-63. (Pubitemid 32894069)
57. Nakazawa N, Nakamura T, Kokubu A, Ebe M, Nagao K, Yanagida M. Dissection of the essential steps for condensin accumulation at kinetochores and rDNAs during fission yeast mitosis. J Cell Biol 2008; 180:1115-31. (Pubitemid 351468469)
58. Maddox PS, Portier N, Desai A, Oegema K. Molecular analysis of mitotic chromosome condensation using a quantitative time-resolved fluorescence microscopy assay. Proc Natl Acad Sci USA 2006; 103:15097-102. (Pubitemid 44583170)
59. Losada A, Hirano M, Hirano T. Cohesin release is required for sister chromatid resolution, but not for condensin-mediated compaction, at the onset of mitosis. Genes Dev 2002; 16:3004-16. (Pubitemid 35424189)
60. MacCallum DE, Losada A, Kobayashi R, Hirano T. ISWI remodeling complexes in Xenopus egg extracts: identification as major chromosomal components that are regulated by INCENP-aurora B. Mol Biol Cell 2002; 13:25-39. (Pubitemid 34106056)
61. Hauf S, Cole RW, LaTerra S, Zimmer C, Schnapp G, Walter R, et al. The small molecule Hesperadin reveals a role for Aurora B in correcting kinetochore-microtubule attachment and in maintaining the spindle assembly checkpoint. J Cell Biol 2003; 161:281-94.
62. Rajagopalan S, Balasubramanian MK. Schizosaccharomyces pombe Bir1p, a nuclear protein that localizes to kinetochores and the spindle midzone, is essential for chromosome condensation and spindle elongation during mitosis. Genetics 2002; 160:445-56.
63. Vas AC, Andrews CA, Kirkland Matesky K, Clarke DJ. In vivo analysis of chromosome condensation in Saccharomyces cerevisiae. Mol Biol Cell 2007; 18:557-68.
64. Varela E, Shimada K, Laroche T, Leroy D, Gasser SM. Lte1, Cdc14 and MEN-controlled Cdk inactivation in yeast coordinate rDNA decompaction with late telophase progression. EMBO J 2009; 28:1562-75.
65. Choudhary C, Kumar C, Gnad F, Nielsen ML, Rehman M, Walther TC, et al. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 2009; 325:834-40.
66. D'Amours D, Stegmeier F, Amon A. Cdc14 and condensin control the dissolution of cohesin-independent chromosome linkages at repeated DNA. Cell 2004; 117:455-69. (Pubitemid 38610231)
67. Dosztanyi Z, Csizmok V, Tompa P, Simon I. IUPred: web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content. Bioinformatics 2005; 21:3433-4. (Pubitemid 41222453)