Polo-like kinase-1 triggers Histone phosphorylation by Haspin in mitosis

EMBO Reports

Volumn 15, Issue 3, 2014, Pages 273-281

  Zhou, Linli ^a   Tian, Xiaoying ^a   Zhu, Cailei ^b   Wang, Fangwei ^a   Higgins, Jonathan Mg ^b,c  

^a ZHEJIANG UNIVERSITY   (China)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

cyclin dependent kinase; haspin; histone modification; mitosis; polo like kinase 1

Indexed keywords

AMINO ACID; HASPIN; HISTONE H3; POLO LIKE KINASE 1; PROTEIN KINASE; THREONINE 3; UNCLASSIFIED DRUG;

ARTICLE; CELL CULTURE; CELL CYCLE; CELL MIGRATION; CELL SYNCHRONIZATION; CONTROLLED STUDY; FEMALE; HELA CELL; HISTONE MODIFICATION; HISTONE PHOSPHORYLATION; HUMAN; HUMAN CELL; MITOSIS; MOLECULAR WEIGHT; PRIORITY JOURNAL; PROMETAPHASE; PROPHASE;

AMINO ACID SEQUENCE; CELL CYCLE PROTEINS; HELA CELLS; HISTONES; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MITOSIS; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS;

EID: 84898626760     PISSN: 1469221X     EISSN: 14693178     Source Type: Journal    
DOI: 10.1002/embr.201338080     Document Type: Article

References (46)

1. Wang F, Higgins JMG, (2013) Histone modifications and mitosis: countermarks, landmarks, and bookmarks. Trends Cell Biol 23: 175-184
2. Dai J, Sultan S, Taylor SS, Higgins JMG, (2005) The kinase haspin is required for mitotic histone H3 Thr 3 phosphorylation and normal metaphase chromosome alignment. Genes Dev 19: 472-488 (Pubitemid 40256279)
3. Wang F, Dai J, Daum JR, Niedzialkowska E, Banerjee B, Stukenberg PT, Gorbsky GJ, Higgins JMG, (2010) Histone H3 Thr-3 phosphorylation by Haspin positions Aurora B at centromeres in mitosis. Science 330: 231-235
4. Wang F, Ulyanova NP, Daum JR, Patnaik D, Kateneva AV, Gorbsky GJ, Higgins JMG, (2012) Haspin inhibitors reveal centromeric functions of Aurora B in chromosome segregation. J Cell Biol 199: 251-268
5. Niedzialkowska E, Wang F, Porebski PJ, Minor W, Higgins JMG, Stukenberg PT, (2012) Molecular basis for phosphospecific recognition of histone H3 tails by Survivin paralogs at inner centromeres. Mol Biol Cell 23: 1457-1466
6. Kelly AE, Ghenoiu C, Xue JZ, Zierhut C, Kimura H, Funabiki H, (2010) Survivin reads phosphorylated histone H3 threonine 3 to activate the mitotic kinase Aurora B. Science 330: 235-239
7. De Antoni A, Maffini S, Knapp S, Musacchio A, Santaguida S, (2012) A small molecule inhibitor of Haspin alters the kinetochore functions of Aurora B. J Cell Biol 199: 269-284
8. Yamagishi Y, Honda T, Tanno Y, Watanabe Y, (2010) Two histone marks establish the inner centromere and chromosome bi-orientation. Science 330: 239-243
9. Varier RA, Outchkourov NS, de Graaf P, van Schaik FM, Ensing HJ, Wang F, Higgins JM, Kops GJ, Timmers HT, (2010) A phospho/methyl switch at histone H3 regulates TFIID association with mitotic chromosomes. EMBO J 29: 3967-3978
10. Fischle W, Tseng BS, Dormann HL, Ueberheide BM, Garcia BA, Shabanowitz J, Hunt DF, Funabiki H, Allis CD, (2005) Regulation of HP1-chromatin binding by histone H3 methylation and phosphorylation. Nature 438: 1116-1122 (Pubitemid 41831675)
11. Hirota T, Lipp JJ, Toh BH, Peters JM, (2005) Histone H3 serine 10 phosphorylation by Aurora B causes HP1 dissociation from heterochromatin. Nature 438: 1176-1180 (Pubitemid 41831689)
12. Kawashima SA, Yamagishi Y, Honda T, Ishiguro K, Watanabe Y, (2010) Phosphorylation of H2A by Bub1 prevents chromosomal instability through localizing shugoshin. Science 327: 172-177
13. Wang F, Ulyanova NP, van der Waal MS, Patnaik D, Lens SMA, Higgins JMG, (2011) A positive feedback loop involving Haspin and Aurora B promotes CPC accumulation at centromeres in mitosis. Curr Biol 21: 1061-1069
14. Qian J, Beullens M, Lesage B, Bollen M, (2013) Aurora B Defines Its Own Chromosomal Targeting by Opposing the Recruitment of the Phosphatase Scaffold Repo-Man. Curr Biol 23: 1136-1143
15. Qian J, Lesage B, Beullens M, Van Eynde A, Bollen M, (2011) PP1/Repo-man dephosphorylates mitotic histone H3 at T3 and regulates chromosomal aurora B targeting. Curr Biol 21: 766-773
16. Vagnarelli P, Ribeiro S, Sennels L, Sanchez-Pulido L, de Lima Alves F, Verheyen T, Kelly DA, Ponting CP, Rappsilber J, Earnshaw WC, (2011) Repo-Man coordinates chromosomal reorganization with nuclear envelope reassembly during mitotic exit. Dev Cell 21: 328-342
17. Polioudaki H, Markaki Y, Kourmouli N, Dialynas G, Theodoropoulos PA, Singh PB, Georgatos SD, (2004) Mitotic phosphorylation of histone H3 at threonine 3. FEBS Lett 560: 39-44 (Pubitemid 38264290)
18. Dai J, Sullivan BA, Higgins JMG, (2006) Regulation of mitotic chromosome cohesion by Haspin and Aurora B. Dev Cell 11: 741-750 (Pubitemid 44644965)
19. 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
20. Degenhardt Y, Greshock J, Laquerre S, Gilmartin AG, Jing J, Richter M, Zhang X, Bleam M, Halsey W, Hughes A, Moy C, Liu-Sullivan N, Powers S, Bachman K, Jackson J, Weber B, Wooster R, (2010) Sensitivity of cancer cells to Plk1 inhibitor GSK461364A is associated with loss of p53 function and chromosome instability. Mol Cancer Ther 9: 2079-2089
21. 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 (Pubitemid 36529846)
22. 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 (Pubitemid 36529847)
23. Colnaghi R, Wheatley SP, (2010) Liaisons between survivin and Plk1 during cell division and cell death. J Biol Chem 285: 22592-22604
24. Chu Y, Yao PY, Wang W, Wang D, Wang Z, Zhang L, Huang Y, Ke Y, Ding X, Yao X, (2011) Aurora B kinase activation requires survivin priming phosphorylation by PLK1. J Mol Cell Biol 3: 260-267
25. Elia AE, Cantley LC, Yaffe MB, (2003) Proteomic screen finds pSer/pThr-binding domain localizing Plk1 to mitotic substrates. Science 299: 1228-1231 (Pubitemid 36237463)
26. Lowery DW, Mohammad DH, Elia AE, Yaffe MB, (2004) The Polo-box domain: a molecular integrator of mitotic kinase cascades and Polo-like kinase function. Cell Cycle 3: 128-131 (Pubitemid 40268680)
27. Higgins JMG, (2001) Haspin-like proteins: A new family of evolutionarily conserved putative eukaryotic protein kinases. Prot Sci 10: 1677-1684 (Pubitemid 32667061)
28. Hornbeck PV, Kornhauser JM, Tkachev S, Zhang B, Skrzypek E, Murray B, Latham V, Sullivan M, (2012) PhosphoSitePlus: a comprehensive resource for investigating the structure and function of experimentally determined post-translational modifications in man and mouse. Nucleic Acids Res 40: D261-D270
29. Nakajima H, Toyoshima-Morimoto F, Taniguchi E, Nishida E, (2003) Identification of a consensus motif for Plk (Polo-like kinase) phosphorylation reveals Myt1 as a Plk1 substrate. J Biol Chem 278: 25277-25280 (Pubitemid 36835273)
30. Kettenbach AN, Wang T, Faherty BK, Madden DR, Knapp S, Bailey-Kellogg C, Gerber SA, (2012) Rapid determination of multiple linear kinase substrate motifs by mass spectrometry. Chem Biol 19: 608-618
31. Alexander J, Lim D, Joughin BA, Hegemann B, Hutchins JR, Ehrenberger T, Ivins F, Sessa F, Hudecz O, Nigg EA, Fry AM, Musacchio A, Stukenberg PT, Mechtler K, Peters JM, Smerdon SJ, Yaffe MB, (2011) Spatial exclusivity combined with positive and negative selection of phosphorylation motifs is the basis for context-dependent mitotic signaling. Sci Signal 4: ra42
32. Losada A, Hirano M, Hirano T, (2002) Cohesin release is required for sister chromatid resolution, but not for condensin-mediated compaction, at the onset of mitosis. Genes Dev 16: 3004-3016 (Pubitemid 35424189)
33. Sumara I, Vorlaufer E, Stukenberg PT, Kelm O, Redemann N, Nigg EA, Peters JM, (2002) The dissociation of cohesin from chromosomes in prophase is regulated by Polo-like kinase. Mol Cell 9: 515-525 (Pubitemid 34273783)
34. 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
35. Lindqvist A, van Zon W, Karlsson Rosenthal C, Wolthuis RM, (2007) Cyclin B1-Cdk1 activation continues after centrosome separation to control mitotic progression. PLoS Biol 5: e123
36. Gavet O, Pines J, (2010) Progressive activation of CyclinB1-Cdk1 coordinates entry to mitosis. Dev Cell 18: 533-543
37. Xu Z, Vagnarelli P, Ogawa H, Samejima K, Earnshaw WC, (2010) Gradient of increasing Aurora B kinase activity is required for cells to execute mitosis. J Biol Chem 285: 40163-40170
38. Liokatis S, Stützer A, Elsässer SJ, Theillet FX, Klingberg R, van Rossum B, Schwarzer D, Allis CD, Fischle W, Selenko P, (2012) Phosphorylation of histone H3 Ser10 establishes a hierarchy for subsequent intramolecular modification events. Nat Struct Mol Biol 19: 819-823
39. Carmena M, Pinson X, Platani M, Salloum Z, Xu Z, Clark A, Macisaac F, Ogawa H, Eggert U, Glover DM, Archambault V, Earnshaw WC, (2012) The chromosomal passenger complex activates Polo kinase at centromeres. PLoS Biol 10: e1001250
40. Salimian KJ, Ballister ER, Smoak EM, Wood S, Panchenko T, Lampson MA, Black BE, (2011) Feedback control in sensing chromosome biorientation by the Aurora B kinase. Curr Biol 21: 1158-1165
41. Moutinho-Santos T, Conde C, Sunkel CE, (2012) POLO ensures chromosome bi-orientation by preventing and correcting erroneous chromosome-spindle attachments. J Cell Sci 125: 576-583
42. Elowe S, Hummer S, Uldschmid A, Li X, Nigg EA, (2007) Tension-sensitive Plk1 phosphorylation on BubR1 regulates the stability of kinetochore microtubule interactions. Genes Dev 21: 2205-2219 (Pubitemid 47360842)
43. Suijkerbuijk SJ, Vleugel M, Teixeira A, Kops GJ, (2012) Integration of kinase and phosphatase activities by BUBR1 ensures formation of stable kinetochore-microtubule attachments. Dev Cell 23: 745-755
44. Kruse T, Zhang G, Larsen MS, Lischetti T, Streicher W, Kragh Nielsen T, Bjorn SP, Nilsson J, (2013) Direct binding between BubR1 and B56-PP2A phosphatase complexes regulate mitotic progression. J Cell Sci 126: 1086-1092
45. Liu D, Davydenko O, Lampson MA, (2012) Polo-like kinase-1 regulates kinetochore-microtubule dynamics and spindle checkpoint silencing. J Cell Biol 198: 491-499
46. Ghenoiu C, Wheelock MS, Funabiki H, (2013) Autoinhibition and Polo-Dependent Multisite Phosphorylation Restrict Activity of the Histone H3 Kinase Haspin to Mitosis. Mol Cell 52: 734-745.