Aurora B kinase maintains chromatin organization during the MI to MII transition in surf clam oocytes

Cell Cycle

Volumn 5, Issue 22, 2006, Pages 2648-2656

  George, Olivia ^b   Johnston, Mantissa A ^b   Shuster, Charles B ^a  

^a NEW MEXICO STATE UNIVERSITY   (United States)

^b NONE

Author keywords

Aurora B; Chromatin condensation; Histone; Meiosis; Oocyte maturation; Spisula; Surf clam

Indexed keywords

AURORA B KINASE; HISTONE H3;

ARTICLE; CELL CYCLE; CELL NUCLEUS MEMBRANE; CHROMATIN; CLAM; CYTOKINESIS; MEIOSIS; MITOSIS; NONHUMAN; OOCYTE MATURATION; PROTEIN SYNTHESIS; SISTER CHROMATID; SPISULA SOLIDISSIMA;

PSEUDOCARDIUM SACHALINENSIS; SPISULA; SPISULA SOLIDISSIMA;

EID: 33751212443     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.5.22.3444     Document Type: Article

References (93)

1. Arion D, Meijer L, Brizuela L, Beach D. cdc2 is a component of the M phase-specific histone H1 kinase: Evidence for identity with MPF. Cell 1988; 55:371-8.
2. Gautier J, Norbury C, Lohka M, Nurse P, Maller J. Purified maturation-promoting factor contains the product of a Xenopus homolog of the fission yeast cell cycle control gene cdc2+. Cell 1988; 54:433-9.
3. Vinot S, Le T, Maro B, Louvet-Vallee S. Two PAR6 proteins become asymmetrically localized during establishment of polarity in mouse oocytes. Curr Biol 2004; 14:520-5.
4. Duncan FE, Moss SB, Schultz RM, Williams CJ. PAR-3 defines a central subdomain of the cortical actin cap in mouse eggs. Dev Biol 2005; 280:38-47.
5. Kishimoto T. Cell-cycle control during meiotic maturation. Curr Opin Cell Biol 2003; 15:654-63.
6. Sagata N. Introduction: Meiotic maturation and arrest in animal oocytes. Semin Cell Dev Biol 1998; 9:535-7.
7. Draetta G, Luca F, Westendorf J, Brizuela L, Ruderman J, Beach D. Cdc2 protein kinase is complexed with both cyclin A and B: Evidence for proteolytic inactivation of MPF. Cell 1989; 56:829-38.
8. Murray AW, Solomon MJ, Kirschner MW. The role of cyclin synthesis and degradation in the control of maturation promoting factor activity. Nature 1989; 339:280-6.
9. Gautier J, Minshull J, Lohka M, Glotzer M, Hunt T, Maller JL. Cyclin is a component of maturation-promoting factor from Xenopus. Cell 1990; 60:487-94.
10. 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.
11. Murray AW, Kirschner MW. Cyclin synthesis drives the early embryonic cell cycle. Nature 1989; 339:275-80.
12. Homer HA, McDougall A, Levasseur M, Murdoch AP, Herbert M. Mad2 is required for inhibiting securin and cyclin B degradation following spindle depolymerisation in meiosis I mouse oocytes. Reproduction 2005; 130:829-43.
13. Homer HA. Mad2 and spindle assembly checkpoint function during meiosis I in mammalian oocytes. Histol Histopathol 2006; 21:873-86.
14. Zhang D, Li M, Ma W, Hou Y, Li YH, Li SW, Sun QY, Wang WH. Localization of mitotic arrest deficient 1 (MAD1) in mouse oocytes during the first meiosis and its functions as a spindle checkpoint protein. Biol Reprod 2005; 72:58-68.
15. Poss KD, Nechiporuk A, Stringer KF, Lee C, Keating MT. Germ cell aneuploidy in zebrafish with mutations in the mitotic checkpoint gene mps1. Genes Dev 2004; 18:1527-32.
16. Tsurumi C, Hoffmann S, Geley S, Graeser R, Polanski Z. The spindle assembly checkpoint is not essential for CSF arrest of mouse oocytes. J Cell Biol 2004; 167:1037-50.
17. Wassmann K, Niault T, Maro B. Metaphase I arrest upon activation of the Mad2-dependent spindle checkpoint in mouse oocytes. Curr Biol 2003; 13:1596-608.
18. Tunquist BJ, Schwab MS, Chen LG, Maller JL. The spindle checkpoint kinase bub1 and cyclin e/cdk2 both contribute to the establishment of meiotic metaphase arrest by cytostatic factor. Curr Biol 2002; 12:1027-33.
19. Fulka Jr J, Bradshaw J, Moor R. Meiotic cycle checkpoints in mammalian oocytes. Zygote 1994; 2:351-4.
20. Maller JL, Gross SD, Schwab MS, Finkielstein CV, Taieb FE, Qian YW. Cell cycle transitions in early Xenopus development. Novartis Found Symp 2001; 237:58-73, (discussion-8).
21. Tunquist BJ, Eyers PA, Chen LG, Lewellyn AL, Maller JL. Spindle checkpoint proteins Madl and Mad2 are required for cytostatic factor-mediated metaphase arrest. J Cell Biol 2003; 163:1231-42.
22. Holloway SL, Glotzer M, King RW, Murray AW. Anaphase is initiated by proteolysis rather than by the inactivation of maturation-promoting factor. Cell 1993; 73:1393-402.
23. Stemmann O, Zou H, Gerber SA, Gygi SP, Kirschner MW. Dual inhibition of sister chromatid separation at metaphase. Cell 2001; 107:715-26.
24. Hunt T, Luca FC, Ruderman JV. The requirements for protein synthesis and degradation, and the control of destruction of cyclins A and B in the meiotic and mitotic cell cycles of the clam embryo. J Cell Biol 1992; 116:707-24.
25. Hochegger H, Klotzbucher A, Kirk J, Howell M, le Guellec K, Fletcher K, Duncan T, Sohail M, Hunt T. New B-type cyclin synthesis is required between meiosis I and II during Xenopus oocyte maturation. Development 2001; 128:3795-807.
26. Minshull J, Murray A, Colman A, Hunt T. Xenopus oocyte maturation does not require new cyclin synthesis. J Cell Biol 1991; 114:767-72.
27. Gerhart J, Wu M, Kirschner M. Cell cycle dynamics of an M-phase-specific cytoplasmic factor in Xenopus laevis oocytes and eggs. J Cell Biol 1984; 98:1247-55.
28. Longo FJ, Cook S, Mathews L, Wright SJ. Nascent protein requirement for completion of meiotic maturation and pronuclear development: Examination of fertilized and A-23187-activated surf clam (Spisula solidissima) eggs. Dev Biol 1991; 148:75-86.
29. Okano-Uchida T, Sekiai T, Lee K, Okumura E, Tachibana K, Kishimoto T. In vivo regulation of cyclin A/Cdc2 and cyclin B/Cdc2 through meiotic and early cleavage cycles in starfish. Dev Biol 1998; 197:39-53.
30. Kubiak JZ, Weber M, Geraud G, Maro B. Cell cycle modification during the transitions between meiotic M-phases in mouse oocytes. J Cell Sci 1992; 102:457-67.
31. Doree M, Peaucellier G, Picard A. Activity of the maturation-promoting factor and the extent of protein phosphorylation oscillate simultaneously during meiotic maturation of starfish oocytes. Dev Biol 1983; 99:489-501.
32. Donahue RP. Maturation of the mouse oocyte in vitro I: Sequence and timing of nuclear progression. J Exp Zool 1968; 169:237-50.
33. Longo FJ, Anderson E. An ultrastructural analysis of fertilization in the surf clam, Spisula solidissima. I. Polar body formation and development of the female pronucleus. J Ultrastruct Res 1970; 33:495-514.
34. Murray AW, Solomon MJ, Kirschner MW. The role of cyclin synthesis and degradation in the contol of maturation promoting factor activity. Nature 1989; 339:280-6.
35. Wheatley SP, Hinchcliffe EH, Glotzer M, Hyman AA, Sluder G, Wang YL. CDK1 Inactivation regulated anaphase spindle dynamics and cytokinesis in vivo. J Cell Biol 1997; 138:385-93.
36. Parry DH, O'Farrell PH. The schedule of destruction of three mitotic cyclins can dictate the timing of events during exit from mitosis. Curr Biol 2001; 11:671-83.
37. Surana U, Robitsch H, Price C, Schuster T, Fitch I, Futcher AB, Nasmyth K. The role of CDC28 and cyclins during mitosis in the budding yeast S. cerevisiae. Cell 1991; 65:145-61.
38. Shuster CB, Burgess DR. Transitions regulating the timing of cytokinesis in embryonic cells. Curr Biol 2002; 12:854-8.
39. Shuster CB, Burgess DR. Parameters that specify the timing of cytokinesis. J Cell Biol 1999; 146:981-92.
40. Izawa D, Goto M, Yamashita A, Yamano H, Yamamoto M. Fission yeast Meslp ensures the onset of meiosis II by blocking degradation of cyclin Cdc13p. Nature 2005; 434:529-33.
41. Tung JJ, Jackson PK. Emi1 class of proteins regulate entry into meiosis and the meiosis I to meiosis II transition in Xenopus oocytes. Cell Cycle 2005; 4:478-82.
42. Iwabuchi M, Ohsumi K, Yamamoto TM, Sawada W, Kishimoto T. Residual Cdc2 activity remaining at meiosis I exit is essential for meiotic M-M transition in Xenopus oocyte extracts. Embo J 2000; 19:4513-23.
43. Palazzo RE, Vogel JM. Isolation of centrosomes from Spisula solidissima oocytes. Methods Cell Biol 1999; 61:35-56.
44. Strickland L, von Dassow G, Ellenberg J, Foe V, Lenart P, Burgess D. Light microscopy of echinoderm embryos. Methods Cell Biol 2004; 74:371-409.
45. Allen RD. Fertilization and artificial activation in the egg of the surf clam Spisula solidissima. Biol Bull 1953; 105:213-9.
46. Davis FM, Tsao TY, Fowler SK, Rao PN. Monoclonal antibodies to mitotic cells. Proc Natl Acad Sci USA 1983; 80:2926-30.
47. Logarinho E, Sunkel CE. The Drosophila POLO kinase localises to multiple compartments of the mitotic apparatus and is required for the phosphorylation of MPM2 reactive epitopes. J Cell Sci 1998; 111(Pt 19):2897-909.
48. Ohsumi K, Sawada W, Kishimoto T. Meiosis-specific cell cycle regulation in maturing Xenopus oocytes. J Cell Sci 1994; 107(Pt 11):3005-13.
49. Portillo-Lopez A, Gould MC, Stephano JL. MAPK is involved in metaphase I arrest in oyster and mussel oocytes. Biol Cell 2003; 95:275-82.
50. Andrews PD, Knatko E, Moore WJ, Swedlow JR. Mitotic mechanics: The auroras come into view. Curr Opin Cell Biol 2003; 15:672-83.
51. Scrittori L, Hans F, Angelov D, Charra M, Prigent C, Dimitrov S. pEg2 aurora-A kinase, histone H3 phosphorylation, and chromosome assembly in Xenopus egg extract. J Biol Chem 2001; 276:30002-10.
52. Crosio C, Fimia GM, Loury R, Kimura M, Okano Y, Zhou H, Sen S, Allis CD, Sassone-Corsi P. Mitotic phosphorylation of histone H3: Spatio-temporal regulation by mammalian Aurora kinases. Mol Cell Biol 2002; 22:874-85.
53. Ota T, Suto S, Katayama H, Han ZB, Suzuki F, Maeda M, Tanino M, Terada Y, Tatsuka M. Increased mitotic phosphorylation of histone H3 attributable to AIM-1/Aurora-B overexpression contributes to chromosome number instability. Cancer Res 2002; 62:5168-77.
54. Petersen J, Hagan IM. S. pombe aurora kinase/survivin is required for chromosome condensation and the spindle checkpoint attachment response. Curr Biol 2003; 13:590-7.
55. Goto H, Yasui Y, Nigg EA, Inagaki M. Aurora-B phosphorylates Histone H3 at serine28 with regard to the mitotic chromosome condensation. Genes Cells 2002; 7:11-7.
56. 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.
57. Pascreau G, Arlot-Bonnemains Y, Prigent C. Phosphorylation of histone and histone-like proteins by aurora kinases during mitosis. Prog Cell Cycle Res 2003; 5:369-74.
58. 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.
59. Hauf S, Cole RW, LaTerra S, Zimmer C, Schnapp G, Walter R, Heckel A, van Meel J, Rieder CL, Peters JM. 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.
60. Terada Y. Role of chromosomal passenger complex in chromosome segregation and cytokinesis. Cell Struct Funct 2001; 26:653-7.
61. Ducat D, Zheng Y. Aurora kinases in spindle assembly and chromosome segregation. Exp Cell Res 2004; 301:60-7.
62. Sessa F, Mapelli M, Ciferri C, Tarricone C, Areces LB, Schneider TR, Stukenberg PT, Musacchio A. Mechanism of Aurora B activation by INCENP and inhibition by Hesperadin. Mol Cell 2005; 18:379-91.
63. 2/M-phase transition in Xenopus oocytes. J Cell Sci 2001; 114:3397-406.
64. Su TT, Campbell SD, O'Farrell PH. Drosophila grapes/CHK1 mutants are defective in cyclin proteolysis and coordination of mitotic events. Curr Biol 1999; 9:919-22.
65. Huang X, Tran T, Zhang L, Hatcher R, Zhang P. DNA damage-induced mitotic catastrophe is mediated by the Chk1-dependent mitotic exit DNA damage checkpoint. Proc Natl Acad Sci USA 2005; 102:1065-70.
66. Nakajo N, Oe T, Uto K, Sagata N. Involvement of Chk1 kinase in prophase I arrest of Xenopus oocytes. Dev Biol 1999; 207:432-44.
67. Tsai MY, Wiese C, Cao K, Martin O, Donovan P, Ruderman J, Prigent C, Zheng Y. A Ran signalling pathway mediated by the mitotic kinase Aurora A in spindle assembly. Nat Cell Biol 2003; 5:242-8.
68. Eyers PA, Erikson E, Chen LG, Maller JL. A novel mechanism for activation of the protein kinase aurora a. Curr Biol 2003; 13:691-7.
69. 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.
70. Zheng Y. G protein control of microtubule assembly. Annu Rev Cell Dev Biol 2004; 20:867-94.
71. 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.
72. Nowak SJ, Corces VG. Phosphorylation of histone H3: A balancing act between chromosome condensation and transcriptional activation. Trends Genet 2004; 20:214-20.
73. Hans F, Dimitrov S. Histone H3 phosphorylation and cell division. Oncogene 2001; 20:3021-7.
74. Wei Y, Yu L, Bowen J, Gorovsky MA, Allis CD. Phosphorylation of histone H3 is required for proper chromosome condensation and segregation. Cell 1999; 97:99-109.
75. Wei Y, Mizzen CA, Cook RG, Gorovsky MA, Allis CD. Phosphorylation of histone H3 at serine 10 is correlated with chromosome condensation during mitosis and meiosis in Tetrahymena. Proc Natl Acad Sci USA 1998; 95:7480-4.
76. 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(Pt 23):3497-506.
77. 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.
78. Kaszas E, Cande WZ. Phosphorylation of histone H3 is correlated with changes in the maintenance of sister chromatid cohesion during meiosis in maize, rather than the condensation of the chromatin. J Cell Sci 2000; 113(Pt 18):3217-26.
79. Bui HT, Yamaoka E, Miyano T. Involvement of histone H3 (Ser10) phosphorylation in chromosome condensation without Cdc2 kinase and mitogen-activated protein kinase activation in pig oocytes. Biol Reprod 2004; 70:1843-51.
80. Hsu JY, Sun ZW, Li X, Reuben M, Tatchell K, Bishop DK, Grushcow JM, Brame CJ, Caldwell JA, Hunt DF, Lin R, Smith MM, Allis CD. 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.
81. Ke YW, Dou Z, Zhang J, Yao XB. Function and regulation of Aurora/Ipllp kinase family in cell division. Cell Res 2003; 13:69-81.
82. Wang G, Wang CM, Ai JS, Xiong B, Yin S, Hou Y, Chen DY, Schatten H, Sun QY. Histone phosphorylation and pericentromeric histone modifications in oocyte meiosis. Cell Cycle 2006; 5:1974-82.
83. Picard A, Galas S, Peaucellier G, Doree M. Newly assembled cyclin B-cdc2 kinase is required to suppress DNA replication between meiosis I and meiosis II in starfish oocytes. Embo J 1996; 15:3590-8.
84. Furuno N, Nishizawa M, Okazaki K, Tanaka H, Iwashita J, Nakajo N, Ogawa Y, Sagata N. Suppression of DNA replication via Mos function during meiotic divisions in Xenopus oocytes. Embo J 1994; 13:2399-410.
85. Nakajo N, Yoshitome S, Iwashita J, Iida M, Uto K, Ueno S, Okamoto K, Sagata N. Absence of Wee1 ensures the meiotic cell cycle in Xenopus oocytes. Genes Dev 2000; 14:328-38.
86. Surana U, Amon A, Dowzer C, McGrew J, Byers B, Nasmyth K. Destruction of the CDC28/CLB mitotic kinase is not required for the metaphase to anaphase transition in budding yeast. Embo J 1993; 12:1969-78.
87. Gallant P, Nigg EA. Cyclin B2 undergoes cell cycle-dependent nuclear translocation and, when expressed as a nondestructible mutant, causes mitotic arrest in HeLa cells. J Cell Biol 1992; 117:213-24.
88. Sigrist S, Jacobs H, Stratmann R, Lehner CF. Exit from mitosis is regulated by Drosophila fizzy and the sequential destruction of cyclins A, B and B3. Embo J 1995; 14:4827-38.
89. Maller JL, Schwab MS, Gross SD, Taieb FE, Roberts BT, Tunquist BJ. The mechanism of CSF arrest in vertebrate oocytes. Mol Cell Endocrinol 2002; 187:173-8.
90. 2 arrest: Useful starfish oocyte system for investigating skillful MAP kinase. Biol Cell 2004; 96:241-4.
91. Oita E, Harada K, Chiba K. Degradation of polyubiquitinated cyclin B is blocked by the MAPK pathway at the metaphase I arrest in starfish oocytes. J Biol Chem 2004; 279:18633-40.
92. Abrieu A, Doree M, Fisher D. The interplay between cyclin-B-Cdc2 kinase (MPF) and MAP kinase during maturation of oocytes. J Cell Sci 2001; 114:257-67.
93. Shibuya EK, Boulton TG, Cobb MH, Ruderman JV. Activation of p42 MAP kinase and the release of oocytes from cell cycle arrest. Embo J 1992; 11:3963-75.