Phosphorylation of histone H3 serine 10 in early mouse embryos: Active phosphorylation at late S phase and differential effects of ZM447439 on first two embryonic mitoses

Cell Cycle

Volumn 9, Issue 23, 2010, Pages 4674-4687

  Teperek Tkacz, Marta ^a,c   Meglicki, Maciej ^a   Pasternak, Michal ^a   Kubiak, Jacek Z ^b   Borsuk, Ewa ^a  

^a UNIVERSITY OF WARSAW   (Poland)

^b UNIVERSITÉ DE RENNES 1   (France)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Aurora kinases; H3S10 phosphorylation; Karyokinesis; Mad2; Spindle assembly checkpoint; ZM447439

Indexed keywords

AURORA A KINASE; AURORA B KINASE; AURORA KINASE INHIBITOR; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; DNA; HISTONE H3; SERINE; UNCLASSIFIED DRUG; ZM 477439;

ANIMAL CELL; ARTICLE; CELL CYCLE; CELL CYCLE S PHASE; CELL DIVISION; CONTROLLED STUDY; DNA REPLICATION; EMBRYO; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; MAMMAL CELL; MITOSIS; MITOSIS SPINDLE; MOUSE; NONHUMAN; OOCYTE; PROTEIN PHOSPHORYLATION; THYMOCYTE; ZYGOTE;

MAMMALIA;

EID: 78650161647     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.9.23.14023     Document Type: Article

References (94)

1. Bischoff JR, Plowman GD. The Aurora/Ipl1p kinase family: Regulators of chromosome segregation and cytokinesis. Trends Cell Biol 1999; 9:454-9. (Pubitemid 29469430)
2. Giet R, Prigent C. Aurora/Ipl1p-related kinases, a new oncogenic family of mitotic serine-threonine kinases. J Cell Sci 1999; 112:3591-601. (Pubitemid 129783931)
3. Vader G, Maia AF, Lens SM. The chromosomal passenger complex and the spindle assembly checkpoint: Kinetochore-microtubule error correction and beyond. Cell Div 2008; 3:10.
4. Hsu JY, Sun ZW, Li X, Reuben M, Tatchell K, Bishop DK, et al. Mitotic phosphorylation of histone H3 is governed by Ipl1/aurora kinase and Glc7/PP1 phosphatase in budding yeast and nematodes. Cell 2000; 102:279-91.
5. Petersen J, Paris J, Willer M, Philippe M, Hagan IM. The S. pombe aurora-related kinase Ark1 associates with mitotic structures in a stage dependent manner and is required for chromosome segregation. J Cell Sci 2001; 114:4371-84. (Pubitemid 34082858)
6. Schumacher JM, Ashcroft N, Donovan PJ, Golden A. A highly conserved centrosomal kinase, AIR-1, is required for accurate cell cycle progression and segregation of developmental factors in Caenorhabditis elegans embryos. Development 1998; 125:4391-402. (Pubitemid 28564284)
7. Schumacher JM, Golden A, Donovan PJ. AIR-2: An Aurora/Ipl1-related protein kinase associated with chromosomes and midbody microtubules is required for polar body extrusion and cytokinesis in Caenorhabditis elegans embryos. J Cell Biol 1998; 143:1635-46. (Pubitemid 29006508)
8. Glover DM, Leibowitz MH, McLean DA, Parry H. Mutations in aurora prevent centrosome separation leading to the formation of monopolar spindles. Cell 1995; 81:95-105.
9. Reich A, Yanai A, Mesilaty-Gross S, Chen-Moses A, Wides R, Motro B. Cloning, mapping, and expression of ial, a novel Drosophila member of the Ipl1/aurora mitotic control kinase family. DNA Cell Biol 1999; 18:593-603. (Pubitemid 29357772)
10. Barr AR, Gergely F. Aurora-A: The maker and breaker of spindle poles. J Cell Sci 2007; 120:2987-96. (Pubitemid 47517082)
11. Hannak E, Kirkham M, Hyman AA, Oegema K. Aurora-A kinase is required for centrosome maturation in Caenorhabditis elegans. J Cell Biol 2001; 155:1109-16.
12. Terada Y, Uetake Y, Kuriyama R. Interaction of Aurora-A and centrosomin at the microtubule-nucleating site in Drosophila and mammalian cells. J Cell Biol 2003; 162:757-63. (Pubitemid 37087715)
13. DeLuca JG, Gall WE, Ciferri C, Cimini D, Musacchio A, Salmon ED. Kinetochore microtubule dynamics and attachment stability are regulated by Hec1. Cell 2006; 127:969-82.
14. Giet O, Van Bockstaele DR, Di Stefano I, Huygen S, Greimers R, Beguin Y, et al. Increased binding and defective migration across fibronectin of cycling hematopoietic progenitor cells. Blood 2002; 99:2023-31. (Pubitemid 34525484)
15. Nishimura Y, Endo T, Kano K, Naito K. Porcine Aurora A accelerates Cyclin B and Mos synthesis and promotes meiotic resumption of porcine oocytes. Anim Reprod Sci 2009; 113:114-24.
16. Qin L, Tong T, Song Y, Xue L, Fan F, Zhan Q. Aurora-A interacts with Cyclin B1 and enhances its stability. Cancer Lett 2009; 275:77-85.
17. Slattery SD, Moore RV, Brinkley BR, Hall RM. Aurora-C and Aurora-B share phosphorylation and regulation of CENP-A and Borealin during mitosis. Cell Cycle 2008; 7:787-95. (Pubitemid 351520043)
18. Slattery SD, Mancini MA, Brinkley BR, Hall RM. Aurora-C kinase supports mitotic progression in the absence of Aurora-B. Cell Cycle 2009; 8:2984-94.
19. Vader G, Cruijsen CW, van Harn T, Vromans MJ, Medema RH, Lens SM. The chromosomal passenger complex controls spindle checkpoint function independent from its role in correcting microtubule kinetochore interactions. Mol Biol Cell 2007; 18:4553-64. (Pubitemid 350060181)
20. Kelly AE, Funabiki H. Correcting aberrant kinetochore microtubule attachments: an Aurora B-centric view. Curr Opin Cell Biol 2009; 21:51-8.
21. Adams RR, Carmena M, Earnshaw WC. Chromosomal passengers and the (aurora) ABCs of mitosis. Trends Cell Biol 2001; 11:49-54. (Pubitemid 32144751)
22. Liu D, Vader G, Vromans MJ, Lampson MA, Lens SM. Sensing chromosome bi-orientation by spatial separation of aurora B kinase from kinetochore substrates. Science 2009; 323:1350-3.
23. Chesnel F, Bazile F, Pascal A, Kubiak JZ. Cyclin B dissociation from CDK1 precedes its degradation upon MPF inactivation in mitotic extracts of Xenopus laevis embryos. Cell Cycle 2006; 5:1687-98. (Pubitemid 44285257)
24. Zou H, McGarry TJ, Bernal T, Kirschner MW. Identification of a vertebrate sister-chromatid separation inhibitor involved in transformation and tumorigenesis. Science 1999; 285:418-22.
25. Varetti G, Musacchio A. The spindle assembly checkpoint. Curr Biol 2008; 18:591-5.
26. Nilsson J, Yekezare M, Minshull J, Pines J. The APC/C maintains the spindle assembly checkpoint by targeting Cdc20 for destruction. Nat Cell Biol 2008; 10:1411-20.
27. Kulukian A, Han JS, Cleveland DW. Unattached kinetochores catalyze production of an anaphase inhibitor that requires a Mad2 template to prime Cdc20 for BubR1 binding. Dev Cell 2009; 16:105-17.
28. Ge S, Skaar JR, Pagano M. APC/C- and Mad2-mediated degradation of Cdc20 during spindle checkpoint activation. Cell Cycle 2009; 8:167-71.
29. Cheeseman IM, Chappie JS, Wilson-Kubalek EM, Desai A. The conserved KMN network constitutes the core microtubule-binding site of the kinetochore. Cell 2006; 127:983-97. (Pubitemid 44792248)
30. Pinsky BA, Kung C, Shokat KM, Biggins S. The Ipl1-Aurora protein kinase activates the spindle checkpoint by creating unattached kinetochores. Nat Cell Biol 2006; 8:78-83. (Pubitemid 43064800)
31. Ditchfield C, Johnson VL, Tighe A, Ellston R, Haworth C, Johnson T, et al. Aurora B couples chromosome alignment with anaphase by targeting BubR1, Mad2 and Cenp-E to kinetochores. J Cell Biol 2003; 161:267-80. (Pubitemid 36529846)
32. 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. (Pubitemid 36529847)
33. Morrow CJ, Tighe A, Johnson VL, Scott MI, Ditchfield C, Taylor SS. Bub1 and aurora B cooperate to maintain BubR1-mediated inhibition of APC/CCdc20. J Cell Sci 2005; 118:3639-52. (Pubitemid 41309411)
34. Yuan K, Li N, Huo Y, Yan F, Yang Y, Ward T, et al. Recruitment of separase to mitotic chromosomes is regulated by Aurora B. Cell Cycle 2009; 8:1433-43.
35. Goto H, Yasui Y, Kawajiri A, Nigg EA, Terada Y, Tatsuka M, et al. Aurora-B regulates the cleavage furrow-specific vimentin phosphorylation in the cytokinetic process. J Biol Chem 2003; 278:8526-30. (Pubitemid 36800605)
36. Minoshima Y, Kawashima T, Hirose K, Tonozuka Y, Kawajiri A, Bao YC, et al. Phosphorylation by aurora B converts MgcRacGAP to a RhoGAP during cytokinesis. Dev Cell 2003; 4:549-60. (Pubitemid 36437561)
37. Guse A, Mishima M, Glotzer M. Phosphorylation of ZEN-4/MKLP1 by aurora B regulates completion of cytokinesis. Curr Biol 2005; 15:778-86. (Pubitemid 40599935)
38. Hirota T, Lipp JJ, Toh BH, Peters JM. Histone H3 serine 10 phosphorylation by Aurora B causes HP1 dissociation from heterochromatin. Nature 2005; 438:1176-80. (Pubitemid 41831689)
39. 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.
40. Adams RR, Maiato H, Earnshaw WC, Carmena M. Essential roles of Drosophila inner centromere protein (INCENP) and aurora B in histone H3 phosphorylation, metaphase chromosome alignment, kinetochore disjunction and chromosome segregation. J Cell Biol 2001; 153:865-80.
41. Crosio C, Fimia GM, Loury R, Kimura M, Okano Y, Zhou H, et al. Mitotic phosphorylation of histone H3: spatio-temporal regulation by mammalian Aurora kinases. Mol Cell Biol 2002; 22:874-85. (Pubitemid 34053065)
42. Jelinkova L, Kubelka M. Neither Aurora B activity nor histone H3 phosphorylation is essential for chromosome condensation during meiotic maturation of porcine oocytes. Biol Reprod 2006; 74:905-12.
43. Sabbattini P, Canzonetta C, Sjoberg M, Nikic S, Georgiou A, Kemball-Cook G, et al. A novel role for the Aurora B kinase in epigenetic marking of silent chromatin in differentiated postmitotic cells. EMBO J 2007; 26:4657-69. (Pubitemid 350126789)
44. Gurley LR, D'Anna JA, Barham SS, Deaven LL, Tobey RA. Histone phosphorylation and chromatin structure during mitosis in Chinese hamster cells. Eur J Biochem 1978; 84:1-15. (Pubitemid 8286682)
45. Paulson JR, Taylor SS. Phosphorylation of histones 1 and 3 and nonhistone high mobility group 14 by an endogenous kinase in HeLa metaphase chromosomes. J Biol Chem 1982; 257:6064-72.
46. Hendzel MJ, Wei Y, Mancini MA, Van Hooser A, Ranalli T, Brinkley BR, et al. Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 1997; 106:348-60. (Pubitemid 27510848)
47. Bolton MA, Lan W, Powers SE, McCleland ML, Kuang J, Stukenberg PT. Aurora B kinase exists in a complex with survivin and INCENP and its kinase activity is stimulated by survivin binding and phosphorylation. Mol Biol Cell 2002; 13:3064-77. (Pubitemid 35034246)
48. Murata-Hori M, Tatsuka M, Wang YL. Probing the dynamics and functions of aurora B kinase in living cells during mitosis and cytokinesis. Mol Biol Cell 2002; 13:1099-108. (Pubitemid 34309608)
49. Sauve DM, Anderson HJ, Ray JM, James WM, Roberge M. Phosphorylation- induced rearrangement of the histone H3 NH2-terminal domain during mitotic chromosome condensation. J Cell Biol 1999; 145:225-35. (Pubitemid 29198297)
50. Van Hooser A, Goodrich DW, Allis CD, Brinkley BR, Mancini MA. Histone H3 phosphorylation is required for the initiation, but not maintenance, of mammalian chromosome condensation. J Cell Sci 1998; 111:3497-506. (Pubitemid 29015387)
51. de la Barre AE, Gerson V, Gout S, Creaven M, Allis CD, Dimitrov S. Core histone N-termini play an essential role in mitotic chromosome condensation. EMBO J 2000; 19:379-91. (Pubitemid 30072608)
52. Perez-Cadahia B, Drobic B, Davie JR. H3 phosphorylation: dual role in mitosis and interphase. Biochem Cell Biol 2009; 87:695-709.
53. Zippo A, Serafini R, Rocchigiani M, Pennacchini S, Krepelova A, Oliviero S. Histone crosstalk between H3S10ph and H4K16ac generates a histone code that mediates transcription elongation. Cell 2009; 138:1122-36.
54. Wang Q, Wang CM, Ai JS, Xiong B, Yin S, Hou Y, et al. Histone phosphorylation and pericentromeric histone modifications in oocyte meiosis. Cell Cycle 2006; 5:1974-82. (Pubitemid 44435304)
55. Swain JE, Ding J, Brautigan DL, Villa-Moruzzi E, Smith GD. Proper chromatin condensation and maintenance of histone H3 phosphorylation during mouse oocyte meiosis requires protein phosphatase activity. Biol Reprod 2007; 76:628-38. (Pubitemid 46466520)
56. Bouniol C, Nguyen E, Debey P. Endogenous transcription occurs at the 1-cell stage in the mouse embryo. Exp Cell Res 1995; 218:57-62.
57. Bouniol-Baly C, Nguyen E, Besombes D, Debey P. Dynamic organization of DNA replication in one-cell mouse embryos: relationship to transcriptional activation. Exp Cell Res 1997; 236:201-11. (Pubitemid 27452364)
58. Ciemerych MA, Czolowska R. Differential chromatin condensation of female and male pronuclei in mouse zygotes. Mol Reprod Dev 1993; 34:73-80. (Pubitemid 23014506)
59. Ciemerych MA, Maro B, Kubiak JZ. Control of duration of the first two mitoses in a mouse embryo. Zygote 1999; 7:293-300. (Pubitemid 129639241)
60. Schultz RM. The molecular foundations of the maternal to zygotic transition in the preimplantation embryo. Hum Reprod Update 2002; 8:323-31. (Pubitemid 34919247)
61. Kubiak JZ, Ciemerych MA. Cell cycle regulation in early mouse embryos. Novartis Found Symp 2001; 237:79-89.
62. Brunet S, Maro B. Cytoskeleton and cell cycle control during meiotic maturation of the mouse oocyte: integrating time and space. Reproduction 2005; 130:801-11. (Pubitemid 41830090)
63. Madgwick S, Jones KT. How eggs arrest at metaphase II: MPF stabilisation plus APC/C inhibition equals Cytostatic Factor. Cell Div 2007; 2:4.
64. Verlhac MH, Kubiak JZ, Clarke HJ, Maro B. Microtubule and chromatin behavior follow MAP kinase activity but not MPF activity during meiosis in mouse oocytes. Development 1994; 120:1017-25. (Pubitemid 24111564)
65. Sikora-Polaczek M, Hupalowska A, Polanski Z, Kubiak JZ, Ciemerych MA. The first mitosis of the mouse embryo is prolonged by transitional metaphase arrest. Biol Reprod 2006; 74:734-43.
66. Huang JC, Lei ZL, Shi LH, Miao YL, Yang JW, Ouyang YC, et al. Comparison of histone modifications in in vivo and in vitro fertilization mouse embryos. Biochem Biophys Res Commun 2007; 354:77-83. (Pubitemid 46123203)
67. Wang Y, Toppari J, Parvinen M, Kallio MJ. Inhibition of Aurora kinases perturbs chromosome alignment and spindle checkpoint signaling in rat spermatocytes. Exp Cell Res 2006; 312:3459-70. (Pubitemid 44470769)
68. Swain JE, Ding J, Wu J, Smith GD. Regulation of spindle and chromatin dynamics during early and late stages of oocyte maturation by aurora kinases. Mol Hum Reprod 2008; 14:291-9. (Pubitemid 351804030)
69. Fulton BP, Whittingham DG. Activation of mammalian oocytes by intracellular injection of calcium. Nature 1978; 273:149-51. (Pubitemid 8322613)
70. Cuthbertson KS. Parthenogenetic activation of mouse oocytes in vitro with ethanol and benzyl alcohol. J Exp Zool 1983; 226:311-4.
71. Cuthbertson KS, Whittingham DG, Cobbold PH. Free Ca2+ increases in exponential phases during mouse oocyte activation. Nature 1981; 294:754-7. (Pubitemid 12174446)
72. Czolowska R, Modlinski JA, Tarkowski AK. Behaviour of thymocyte nuclei in non-activated and activated mouse oocytes. J Cell Sci 1984; 69:19-34. (Pubitemid 14015954)
73. Szollosi D, Czolowska R, Soltynska MS, Tarkowski AK. Remodelling of thymocyte nuclei in activated mouse oocytes: an ultrastructural study. Eur J Cell Biol 1986; 42:140-51.
74. Szollosi D, Czolowska R, Szollosi MS, Tarkowski AK. Remodeling of mouse thymocyte nuclei depends on the time of their transfer into activated, homologous oocytes. J Cell Sci 1988; 91:603-13.
75. Borsuk E, Maleszewski M. DNA replication and RNA synthesis in thymocyte nuclei microinjected into the cytoplasm of artificially activated mouse eggs. Zygote 2002; 10:229-38. (Pubitemid 135714176)
76. Borsuk E, Szollosi MS, Besomebes D, Debey P. Fusion with activated mouse oocytes modulates the transcriptional activity of introduced somatic cell nuclei. Exp Cell Res 1996; 225:93-101. (Pubitemid 26158459)
77. Gadea BB, Ruderman JV. Aurora kinase inhibitor ZM447439 blocks chromosome-induced spindle assembly, the completion of chromosome condensation, and the establishment of the spindle integrity checkpoint in Xenopus egg extracts. Mol Biol Cell 2005; 16:1305-18. (Pubitemid 40349566)
78. Nakajima N, Inomata T, Ito J, Kashiwazaki N. Treatment with proteasome inhibitor MG132 during cloning improves survival and pronuclear number of reconstructed rat embryos. Cloning Stem Cells 2008; 10:461-8.
79. Yi YJ, Nagyova E, Manandhar G, Prochazka R, Sutovsky M, Park CS, et al. Proteolytic activity of the 26S proteasome is required for the meiotic resumption, germinal vesicle breakdown and cumulus expansion of porcine cumulus-oocyte complexes matured in vitro. Biol Reprod 2008; 78:115-26.
80. Cimini D, Moree B, Canman JC, Salmon ED. Merotelic kinetochore orientation occurs frequently during early mitosis in mammalian tissue cells and error correction is achieved by two different mechanisms. J Cell Sci 2003; 116:4213-25.
81. Uetake Y, Sluder G. Prolonged prometaphase blocks daughter cell proliferation despite normal completion of mitosis. Curr Biol 2010; 20:1666-71.
82. Prigent C, Dimitrov S. Phosphorylation of serine 10 in histone H3, what for? J Cell Sci 2003; 116:3677-85.
83. Stewart S, Fang G. Destruction box-dependent degradation of aurora B is mediated by the anaphase-promoting complex/cyclosome and Cdh1. Cancer Res 2005; 65:8730-5. (Pubitemid 41377361)
84. Marangos P, Carroll J. Securin regulates entry into M-phase by modulating the stability of cyclin B. Nat Cell Biol 2008; 10:445-51.
85. Shuda K, Schindler K, Ma J, Schultz RM, Donovan PJ. Aurora kinase B modulates chromosome alignment in mouse oocytes. Mol Reprod Dev 2009; 76:1094-105.
86. Yanagimachi R. Mammalian fertilization, in: Knobil E, Neill JD, Eds. The Physiology of Reproduction. New York: Raven Press Ltd 1994; 189-317.
87. Probst AV, Almouzni G. Pericentric heterochromatin: Dynamic organization during early development in mammals. Differentiation 2008; 76:15-23.
88. Probst AV, Santos F, Reik W, Almouzni G, Dean W. Structural differences in centromeric heterochromatin are spatially reconciled on fertilisation in the mouse zygote. Chromosoma 2007; 116:403-15. (Pubitemid 46995578)
89. Taddei A, Maison C, Roche D, Almouzni G. Reversible disruption of pericentric heterochromatin and centromere function by inhibiting deacetylases. Nat Cell Biol 2001; 3:114-20. (Pubitemid 32118363)
90. Robbins AR, Jablonski SA, Yen TJ, Yoda K, Robey R, Bates SE, et al. Inhibitors of histone deacetylases alter kinetochore assembly by disrupting pericentromeric heterochromatin. Cell Cycle 2005; 4:717-26. (Pubitemid 41353858)
91. Kloc A, Zaratiegui M, Nora E, Martienssen R. RNA interference guides histone modification during the S phase of chromosomal replication. Curr Biol 2008; 18:490-5.
92. Adenot PG, Szollosi MS, Geze M, Renard JP, Debey P. Dynamics of paternal chromatin changes in live one-cell mouse embryo after natural fertilization. Mol Reprod Dev 1991; 28:23-34.
93. Santaguida S, Musacchio A. The life and miracles of kinetochores. EMBO J 2009; 28:2511-31.
94. Golbus MS, Calarco PG, Epstein CJ. The effects of inhibitors of RNA synthesis (alpha-amanitin and actinomycin D) on preimplantation mouse embryogenesis. J Exp Zool 1973; 186:207-16.