Abstract
Histone H3 is specifically phosphorylated during both mitosis and meiosis in patterns that are specifically coordinated in both space and time. Histone H3 phosphorylation may initiate at different phases of the cell division in different organisms, but metaphase chromosomes are always found to be heavily phosphorylated. Upon exit of mitosis/meiosis a global dephosphorylation of H3 takes place. Potential candidates for H3 kinases are described and their hypothetical mechanism of action on highly condensed chromatin templates is discussed. In addition, a novel hypothesis for the role of histone H3 phosphorylation during cell division is proposed. This hypothesis, termed the ‘ready production label’ model, explains the results in the literature and suggests that phosphorylation of histone H3 is a part of a complex signaling mechanism.
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References
Adams RR, Wheatley SP, Gouldsworthy AM, Kandels-Lewis SE, Carmena M, Smythe C, Gerloff DL, Earnshaw WC . 2000 Curr. Biol. 10: 1075–1078
Allis CD, Gorovsky MA . 1981 Biochemistry 20: 3828–3833
Arents G, Burlingame RW, Wang BC, Love WE, Moudrianakis EN . 1991 Proc. Natl. Acad. Sci. USA 88: 10148–10152
Biggins S, Severin FF, Bhalla N, Sassoon I, Hyman AA, Murray AW . 1999 Genes Dev. 13: 532–544
Bischoff JR, Plowman GD . 1999 Trends Cell Biol. 9: 454–459
Bradbury EM . 1992 Bioessays 14: 9–16
Bradbury EM, Inglis RJ, Matthews HR, Sarner N . 1973 Eur. J. Biochem. 33: 131–139
Cairns BR, Lorch Y, Zhang M, Lacomis L, Erdjument-Bromage H, Tempst P, Du J, Laurent B, Kornberg RD . 1996 Cell 87: 1249–1260
Chan CS, Botstein D . 1993 Genetics 135: 677–691
Cheung P, Allis CD, Sassone-Corsi P . 2000a Cell 103: 263–271
Cheung P, Tanner KG, Cheung WL, Sassone-Corsi P, Denu JM, Allis CD . 2000b Mol. Cell 5: 905–915
Clayton AL, Rose S, Barratt MJ, Mahadevan LC . 2000 EMBO J. 19: 3714–3726
Crosio C, Cermakian N, Allis CD, Sassone-Corsi P . 2000 Nat. Neurosci. 3: 1241–1247
Dasso M, Dimitrov S, Wolffe AP . 1994 Proc. Natl. Acad. Sci. USA 91: 12477–12481
de la Barre AE, Gerson V, Gout S, Creaven M, Allis CD, Dimitrov S . 2000 EMBO J. 19: 379–391
De Souza CP, Osmani AH, Wu LP, Spotts JL, Osmani SA . 2000 Cell 102: 293–302
Dimitrov S, Dasso MC, Wolffe AP . 1994 J. Cell Biol. 126: 591–601
Dimitrov S, Makarov V, Apostolova T, Pashev I . 1986 FEBS Lett. 197: 217–220
Earnshaw WC, Bernat RL . 1991 Chromosoma 100: 139–146
Garcia-Ramirez M, Dong F, Ausio J . 1992 J. Biol. Chem. 267: 19587–19595
Garcia-Ramirez M, Rocchini C, Ausio J . 1995 J. Biol. Chem. 270: 17923–17928
Giet R, Prigent C . 1999 J. Cell Sci. 112: 3591–3601
Giet R, Uzbekov R, Kireev I, Prigent C . 1999 Biol. Cell. 91: 461–470
Goto H, Tomono Y, Ajiro K, Kosako H, Fujita M, Sakurai M, Okawa K, Iwamatsu A, Okigaki T, Takahashi T, Inagaki M . 1999 J. Biol. Chem. 274: 25543–25549
Gurley LR, D'Anna JA, Barham SS, Deaven LL, Tobey RA . 1978 Eur. J. Biochem. 84: 1–15
Helps NR, Luo X, Barker HM, Cohen PT . 2000 Biochem. J. 349: 509–518
Hendzel MJ, Wei Y, Mancini MA, Van Hooser A, Ranalli T, Brinkley BR, Bazett-Jones DP, Allis CD . 1997 Chromosoma 106: 348–360
Herrera JE, West KL, Schiltz RL, Nakatani Y, Bustin M . 2000 Mol. Cell. Biol. 20: 523–529
Hirano T, Mitchison TJ . 1993 J. Cell Biol. 120: 601–612
Houchmandzadeh B, Dimitrov S . 1999 J. Cell Biol. 145: 215–223
Houchmandzadeh B, Marko JF, Chatenay D, Libchaber A . 1997 J. Cell Biol. 139: 1–12
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 . 2000 Cell 102: 279–291
Hunter T . 2000 Cell 100: 113–127
Kaszas E, Cande WZ . 2000 J. Cell Sci. 113: 3217–3226
Khochbin S, Wolffe AP . 1997 FEBS Lett. 419: 157–160
Kimura K, Hirano T . 2000 Proc. Natl. Acad. Sci. USA 97: 11972–11977
Lee DY, Hayes JJ, Pruss D, Wolffe AP . 1993 Cell 72: 73–84
Lohka MJ, Masui Y . 1983 Science 220: 719–721
Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ . 1997 Nature 389: 251–260
Mahadevan LC, Willis AC, Barratt MJ . 1991 Cell 65: 775–783
Makarov VL, Dimitrov SI, Tsaneva IR, Pashev IG . 1984 Biochem. Biophys. Res. Commun. 122: 1021–1027
McGhee JD, Nickol JM, Felsenfeld J, Rau DC . 1983 Nucleic Acids Res. 11: 4065–4075
Mutskov V, Gerber D, Angelov D, Ausio J, Workman J, Dimitrov S . 1998 Mol. Cell. Biol. 18: 6293–6304
Nowak SJ, Corces V . 2000 Genes Dev. 14: 3003–3013
Ohsumi K, Katagiri C, Kishimoto T . 1993 Science 262: 2033–2035
Osmani AH, McGuire SL, Osmani SA . 1991 Cell 67: 283–291
Osmani SA, May GS, Morris NR . 1987 J. Cell Biol. 104: 1495–1504
Perry M, Chalkley R . 1982 J. Biol. Chem. 257: 7336–7347
Sassone-Corsi P, Mizzen CA, Cheung P, Crosio C, Monaco L, Jacquot S, Hanauer A, Allis CD . 1999 Science 285: 886–891
Sauve DM, Anderson HJ, Ray JM, James WM, Roberge M . 1999 J. Cell Biol. 145: 225–235
Schumacher JM, Golden A, Donovan PJ . 1998 J. Cell Biol. 143: 1635–1646
Shen X, Yu L, Weir JW, Gorovsky MA . 1995 Cell 82: 47–56
Speliotes EK, Uren A, Vaux D, Horvitz HR . 2000 Mol. Cell 6: 211–223
Strahl BD, Allis CD . 2000 Nature 403: 41–45
Thomson S, Clayton AL, Hazzalin CA, Rose S, Barratt MJ, Mahadevan LC . 1999a EMBO J. 18: 4779–4793
Thomson S, Mahadevan LC, Clayton AL . 1999b Semin. Cell. Dev. Biol. 10: 205–214
Tse C, Hansen JC . 1997 Biochemistry 36: 11381–11388
Tse C, Sera T, Wolffe AP, Hansen JC . 1998 Mol. Cell. Biol. 18: 4629–4638
Turner BM . 1999 Semin. Cell. Dev. Biol. 10: 165–167
Turner BM . 2000 Bioessays 22: 836–845
Van Hooser A, Goodrich DW, Allis CD, Brinkley BR, Mancini MA . 1998 J. Cell Sci. 111: 3497–3506
Vettese-Dadey M, Grant PA, Hebbes TR, Crane-Robinson C, Allis CD, Workman JL . 1996 EMBO J. 15: 2508–2518
Wei Y, Mizzen CA, Cook RG, Gorovsky MA, Allis CD . 1998 Proc. Natl. Acad. Sci. USA 95: 7480–7484
Wei Y, Yu L, Bowen J, Gorovsky MA, Allis CD . 1999 Cell 97: 99–109
Wolffe AP, Hayes JJ . 1999 Nucleic Acids Res. 27: 711–720
Wolffe AP, Pruss D . 1996 Cell 84: 817–819
Xue Y, Canman JC, Lee CS, Nie Z, Yang D, Moreno GT, Young MK, Salmon ED, Wang W . 2000 Proc. Natl. Acad. Sci. USA 97: 13015–13020
Ye X, Xu G, Fincher RR, Osmani SA . 1997 Methods Enzymol. 283: 520–532
Acknowledgements
We thank Drs J Hayes, S Nonchev and S Khochbin for providing critical input. We appreciate the support of Dr Jean-Jacques Lawrence throughout the course of this work. This study was supported by INSERM and La Ligue Nationale Contre Le Cancer.
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Hans, F., Dimitrov, S. Histone H3 phosphorylation and cell division. Oncogene 20, 3021–3027 (2001). https://doi.org/10.1038/sj.onc.1204326
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DOI: https://doi.org/10.1038/sj.onc.1204326
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