A high-sensitivity phospho-switch triggered by Cdk1 governs chromosome morphogenesis during cell division

Genes and Development

Volumn 29, Issue 4, 2015, Pages 426-439

  Robellet, Xavier ^a,b   Thattikota, Yogitha ^a,b   Wang, Fang ^a,b   Wee, Tse Luen ^c   Pascariu, Mirela ^a,b   Shankar, Sahana ^a,b   Bonneil, EÉric ^a   Brown, Claire M ^c   D’amours, Damien ^a,b  

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

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

Cdk1; Chromosome; Morphogenesis; Multisite phosphorylation ; Smc4

Indexed keywords

CHROMOSOME PROTEIN; CONDENSIN; CYCLIN DEPENDENT KINASE 1; PROTEIN SMC4; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATASE; CYCLIN DEPENDENT KINASE; DNA BINDING PROTEIN; MULTIPROTEIN COMPLEX; NONHISTONE PROTEIN; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE PROTEIN; SMC4 PROTEIN, S CEREVISIAE;

ARTICLE; CELL DIVISION; CELL PROLIFERATION; CHROMOSOME CONDENSATION; CHROMOSOME SEGREGATION; CHROMOSOME STRUCTURE; DOWN REGULATION; ENZYME ACTIVATION; ENZYME ACTIVITY; MITOSIS; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; SACCHAROMYCES CEREVISIAE; CHEMISTRY; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOME; CYTOLOGY; GENETICS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; REGULATOR GENE;

EUKARYOTA;

ADENOSINE TRIPHOSPHATASES; CELL DIVISION; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOMES, FUNGAL; CYCLIN-DEPENDENT KINASES; DNA-BINDING PROTEINS; GENES, SWITCH; MITOSIS; MULTIPROTEIN COMPLEXES; PHOSPHORYLATION; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84923017548     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.253294.114     Document Type: Article

References (56)

1. Abe S, Nagasaka K, Hirayama Y, Kozuka-Hata H, Oyama M, Aoyagi Y, Obuse C, Hirota T. 2011. The initial phase of chromosome condensation requires Cdk1-mediated phosphorylation of the CAP-D3 subunit of condensin II. Genes Dev 25: 863–874.
2. Amon A, Tyers M, Futcher B, Nasmyth K. 1993. Mechanisms that help the yeast cell cycle clock tick: G2 cyclins transcriptionally activate G2 cyclins and repress G1 cyclins. Cell 74: 993–1007.
3. Baxter J, Aragon L. 2012. A model for chromosome condensation based on the interplay between condensin and topoisomerase II. Trends Genet 28: 110–117.
4. Bazile F, St-Pierre J, D’Amours D. 2010. Three-step model for condensin activation during mitotic chromosome condensation. Cell Cycle 9: 3243–3255.
5. Bishop AC, Ubersax JA, Petsch DT, Matheos DP, Gray NS, Blethrow J, Shimizu E, Tsien JZ, Schultz PG, Rose MD, et al. 2000. A chemical switch for inhibitor-sensitive alleles of any protein kinase. Nature 407: 395–401.
6. Cimini D, Mattiuzzo M, Torosantucci L, Degrassi F. 2003. Histone hyperacetylation in mitosis prevents sister chromatid separation and produces chromosome segregation defects. Mol Biol Cell 14: 3821–3833.
7. Coudreuse D, Nurse P. 2010. Driving the cell cycle with a minimal CDK control network. Nature 468: 1074–1079.
8. De Wulf P, Montani F, Visintin R. 2009. Protein phosphatasestake the mitotic stage. Curr Opin Cell Biol 21: 806–815.
9. Ditchfield C, Johnson VL, Tighe A, Ellston R, Haworth C, Johnson T, Mortlock A, Keen N, Taylor SS. 2003. Aurora B couples chromosome alignment with anaphase by targeting BubR1, Mad2, and Cenp-E to kinetochores. J Cell Biol 161: 267–280.
10. Ferrell JE Jr. 1996. Tripping the switch fantastic: How a protein kinase cascade can convert graded inputs into switch-like outputs. Trends Biochem Sci 21: 460–466.
11. Flemming W. 1882. Zellsubstanz, Kern und Zelltheilung. F.C.W. Vogel, Leipzig, Germany.
12. Freeman L, Aragon-Alcaide L, Strunnikov A. 2000. The condensing complex governs chromosome condensation and mitotic transmission of rDNA. J Cell Biol 149: 811–824.
13. Gavet O, Pines J. 2010. Progressive activation of CyclinB1–Cdk1 coordinates entry to mitosis. Dev Cell 18: 533–543.
14. Gerlich D, Hirota T, Koch B, Peters JM, Ellenberg J. 2006. Condensin I stabilizes chromosomes mechanically through a dynamic interaction in live cells. Curr Biol 16: 333–344.
15. Gong D, Ferrell JE Jr. 2010. The roles of cyclin A2, B1, and B2 in early and late mitotic events. Mol Biol Cell 21: 3149–3161.
16. Guacci V, Hogan E, Koshland D. 1994. Chromosome condensation and sister chromatid pairing in budding yeast. J Cell Biol 125: 517–530.
17. Guthrie C, Fink GR., Ed. 1991. Guide to yeast genetics and molecular biology. Academic Press, San Diego.
18. Harvey SL, Charlet A, Haas W, Gygi SP, Kellogg DR. 2005.Cdk1-dependent regulation of the mitotic inhibitor Wee1. Cell 122: 407–420.
19. Hauf S, Cole RW, LaTerra S, Zimmer C, Schnapp G, Walter R, Heckel A, van Meel J, Rieder CL, Peters JM. 2003. 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 161: 281–294.
20. Hirano T. 2012. Condensins: universal organizers of chromosomes with diverse functions. Genes Dev 26: 1659–1678.
21. Holt LJ, Tuch BB, Villen J, Johnson AD, Gygi SP, Morgan DO. 2009. Global analysis of Cdk1 substrate phosphorylation sites provides insights into evolution. Science 325: 1682–1686.
22. Kao L, Wang YT, Chen YC, Tseng SF, Jhang JC, Chen YJ, Teng SC. 2014. Global analysis of cdc14 dephosphorylation sites reveals essential regulatory role in mitosis and cytokinesis. Mol Cell Proteomics 13: 594–605.
23. Kimura K, Hirano M, Kobayashi R, Hirano T. 1998. Phosphorylation and activation of 13S condensin by Cdc2 in vitro. Science 282: 487–490.
24. Kinoshita E, Kinoshita-Kikuta E, Takiyama K, Koike T. 2006. Phosphate-binding tag, a new tool to visualize phosphorylated proteins. Mol Cell Proteomics 5: 749–757.
25. Koivomagi M, Valk E, Venta R, Iofik A, Lepiku M, Morgan DO, Loog M. 2011. Dynamics of Cdk1 substrate specificity during the cell cycle. Mol Cell 42: 610–623.
26. Lavoie BD, Hogan E, Koshland D. 2004. In vivo requirements for rDNA chromosome condensation reveal two cell-cycle-regulated pathways for mitotic chromosome folding. Genes Dev 18: 76–87.
27. Lenart P, Petronczki M, Steegmaier M, Di Fiore B, Lipp JJ, Hoffmann M, Rettig WJ, Kraut N, Peters JM. 2007. The small-molecule inhibitor BI 2536 reveals novel insights into mitotic roles of polo-like kinase 1. Curr Biol 17: 304–315.
28. Li Y, Cross FR, Chait BT. 2014. Method for identifying phosphorylated substrates of specific cyclin/cyclin-dependent kinase complexes. Proc Natl Acad Sci 111: 11323–11328.
29. Loog M, Morgan DO. 2005. Cyclin specificity in the phosphorylation of cyclin-dependent kinase substrates. Nature 434: 104–108.
30. Lyons NA, Morgan DO. 2011. Cdk1-dependent destruction of Eco1 prevents cohesion establishment after S phase. Mol Cell 42: 378–389.
31. Maeshima K, Eltsov M. 2008. Packaging the genome: The structure of mitotic chromosomes. J Biochem 143: 145–153.
32. Marko JF. 2008. Micromechanical studies of mitotic chromosomes. Chromosome Res 16: 469–497.
33. Morgan DO. 2007. The cell cycle: Principles of control. New Science Press, London.
34. Morishita J, Matsusaka T, Goshima G, Nakamura T, Tatebe H, Yanagida M. 2001. Bir1/Cut17 moving from chromosome to spindle upon the loss of cohesion is required for condensation, spindle elongation and repair. Genes Cells 6: 743–763.
35. Mortensen EM, Haas W, Gygi M, Gygi SP, Kellogg DR. 2005. Cdc28-dependent regulation of the Cdc5/Polo kinase. Curr Biol 15: 2033–2037.
36. Naumova N, Imakaev M, Fudenberg G, Zhan Y, Lajoie BR, Mirny LA, Dekker J. 2013. Organization of the mitotic chromosome. Science 342: 948–953.
37. Neurohr G, Naegeli A, Titos I, Theler D, Greber B, Diez J, Gabaldon T, Mendoza M, Barral Y. 2011. A midzone-based ruler adjusts chromosome compaction to anaphase spindle length. Science 332: 465–468.
38. Ono T, Fang Y, Spector DL, Hirano T. 2004. Spatial and temporal regulation of condensins I and II in mitotic chromosome assembly in human cells. Mol Biol Cell 15: 3296–3308.
39. Paulson JR. 2007. Inactivation of Cdk1/Cyclin B in metaphasearrested mouse FT210 cells induces exit from mitosis without chromosome segregation or cytokinesis and allows passage through another cell cycle. Chromosoma 116: 215–225.
40. Pearlman SM, Serber Z, Ferrell JE Jr. 2011. A mechanism for the evolution of phosphorylation sites. Cell 147: 934–946.
41. Peplowska K, Wallek AU, Storchova Z. 2014. Sgo1 regulates both condensin and Ipl1/Aurora B to promote chromosome biorientation. PLoS Genet 10: 1004411.
42. Robbins JA, Cross FR. 2010. Requirements and reasons for effective inhibition of the anaphase promoting complex activator CDH1. Mol Biol Cell 21: 914–925.
43. Sanchez-Diaz A, Nkosi PJ, Murray S, Labib K. 2012. The mitotic exit network and Cdc14 phosphatase initiate cytokinesis by counteracting CDK phosphorylations and blocking polarized growth. EMBO J 31: 3620–3634.
44. Schott EJ, Hoyt MA. 1998. Dominant alleles of Saccharomyces cerevisiae CDC20 reveal its role in promoting anaphase. Genetics 148: 599–610.
45. Slaughter BD, Schwartz JW, Li R. 2007. Mapping dynamic protein interactions in MAP kinase signaling using live-cell fluorescence fluctuation spectroscopy and imaging. Proc Natl Acad Sci 104: 20320–20325.
46. Stern B, Nurse P. 1996. A quantitative model for the cdc2 control of S phase and mitosis in fission yeast. Trends Genet 12: 345–350.
47. St-Pierre J, Douziech M, Bazile F, Pascariu M, Bonneil E, Sauve V, Ratsima H, D’Amours D. 2009. Polo kinase regulates mitotic chromosome condensation by hyperactivation of condensin DNA supercoiling activity. Mol Cell 34: 416–426.
48. Strickfaden SC, Winters MJ, Ben-Ari G, Lamson RE, Tyers M, Pryciak PM. 2007. A mechanism for cell-cycle regulation of MAP kinase signaling in a yeast differentiation pathway. Cell 128: 519–531.
49. Sutani T, Yuasa T, Tomonaga T, Dohmae N, Takio K, Yanagida M. 1999. Fission yeast condensin complex: Essential roles of non-SMC subunits for condensation and Cdc2 phosphorylation of Cut3/SMC4. Genes Dev 13: 2271–2283.
50. Tada K, Susumu H, Sakuno T, Watanabe Y. 2011. Condensin association with histone H2A shapes mitotic chromosomes. Nature 474: 477–483.
51. Takemoto A, Maeshima K, Ikehara T, Yamaguchi K, Murayama A, Imamura S, Imamoto N, Yokoyama S, Hirano T, Watanabe Y, et al. 2009. The chromosomal association of condensin II is regulated by a noncatalytic function of PP2A. Nat Struct Mol Biol 16: 1302–1308.
52. van Heemst D, James F, Poggeler S, Berteaux-Lecellier V, Zickler D. 1999. Spo76p is a conserved chromosome morphogenesis protein that links the mitotic and meiotic programs. Cell 98: 261–271.
53. Vassilev LT, Tovar C, Chen S, Knezevic D, Zhao X, Sun H, Heimbrook DC, Chen L. 2006. Selective small-molecule inhibitor reveals critical mitotic functions of human CDK1. Proc Natl Acad Sci 103: 10660–10665.
54. Wilkins BJ, Rall NA, Ostwal Y, Kruitwagen T, Hiragami-Hamada K, Winkler M, Barral Y, Fischle W, Neumann H. 2014. A cascade of histone modifications induces chromatin condensation in mitosis. Science 343: 77–80.
55. Yeong FM, Hombauer H, Wendt KS, Hirota T, Mudrak I, Mechtler K, Loregger T, Marchler-Bauer A, Tanaka K, Peters JM, et al. 2003. Identification of a subunit of a novel Kleisin-b/SMC complex as a potential substrate of protein phosphatase 2A. Curr Biol 13: 2058–2064.
56. Yu HG, Koshland D. 2005. Chromosome morphogenesis: Condensin-dependent cohesin removal during meiosis. Cell 123: 397–407.