The emergence of regulated histone proteolysis

Current Opinion in Genetics and Development

Volumn 16, Issue 2, 2006, Pages 112-118

  Gunjan, Akash ^a   Paik, Johanna ^a   Verreault, Alain ^b  

^a FLORIDA STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

CHECKPOINT KINASE 2; DNA; HISTONE; HISTONE H3;

CELL PROLIFERATION; CHROMOSOMAL LOCALIZATION; DNA METABOLISM; DNA SYNTHESIS; HUMAN; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVIEW;

ANIMALS; DNA; GENE EXPRESSION REGULATION; HISTONES; HUMANS; HYDROLYSIS; MODELS, BIOLOGICAL; VARIATION (GENETICS);

EID: 33644858609     PISSN: 0959437X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.gde.2006.02.010     Document Type: Review

References (79)

1. A. Gunjan, J. Paik, and A. Verreault Regulation of histone synthesis and nucleosome assembly Biochimie 87 2005 625 635
2. S.E. Polo, and Almouzni G Chromatin assembly: a basic recipe with various flavours Curr Opin Genet Dev 16 2006 104 111
3. M. Han, M. Chang, U.-J. Kim, and M. Grunstein Histone H2B repression causes cell cycle-specific arrest in yeast: effects on chromosomal segregation, replication and transcription Cell 48 1987 589 597
4. D.M. Nelson, X. Ye, C. Hall, H. Santos, T. Ma, G.D. Kao, T.J. Yen, J.W. Harper, and P.D. Adams Coupling of DNA synthesis and histone synthesis in S phase independent of cyclin/cdk2 activity Mol Cell Biol 22 2002 7459 7472
5. X. Ye, A.A. Franco, H. Santos, D.M. Nelson, P.D. Kaufman, and P.D. Adams Defective S phase chromatin assembly causes DNA damage, activation of the S phase checkpoint and S phase arrest Mol Cell 11 2003 341 351
6. X. Zhao, S. McKillop-Smith, and B. Müller The human histone gene expression regulator HBP/SLBP is required for histone and DNA synthesis, cell cycle progression and cell proliferation in mitotic cells J Cell Sci 117 2004 6043 6051
7. E.J. Wagner, A. Berkow, and W.F. Marzluff Expression of an RNAi-resistant SLBP restores proper S-phase progression Biochem Soc Trans 33 2005 471 473
8. K. Myung, V. Pennaneach, E.S. Kats, and R.D. Kolodner Saccharomyces cerevisiae chromatin assembly factors that act during DNA replication function in the maintenance of genome stability Proc Natl Acad Sci USA 100 2003 6640 6645
9. •].
10. •] demonstrate that S. cerevisiae cells lacking the nucleosome assembly factor Asf1 exhibit a high incidence of spontaneous DNA breaks and chromosome rearrangements.
11. C. Lengauer, K.W. Kinzler, and B. Vogelstein Genetic instabilities in human cancers Nature 396 1998 643 649
12. W.M. Bonner, R.S. Wu, H.T. Panusz, and C. Muneses Kinetics of accumulation and depletion of soluble newly synthesized histone in the reciprocal regulation of histone and DNA synthesis Biochemistry 27 1988 6542 6550
13. A. Gunjan, and A. Verreault A Rad53 kinase-dependent surveillance mechanism that regulates histone protein levels in S. cerevisiae Cell 115 2003 537 549 The authors describe the existence of a post-translational surveillance mechanism that monitors the accumulation of excess histones and triggers their degradation in a manner that depends upon the kinase activity of Rad53, a key effector protein kinase in the DNA damage response.
14. A. Groth, D. Ray-Gallet, J.-P. Quivy, J. Lukas, J. Bartek, and G. Almouzni Human ASF1 regulates the flow of S phase histones during replicational stress Mol Cell 17 2005 301 311
15. D.J. Steger, and J.L. Workman Transcription analysis of purified histone acetyltransferase complexes Methods 19 1999 410 416
16. D. Meeks-Wagner, and L.H. Hartwell Normal stoichiometry of histone dimer sets is necessary for high fidelity of mitotic chromosome transmission Cell 44 1986 43 52
17. M. Berloco, L. Fanti, A. Breiling, V. Orlando, and S. Pimpinelli The maternal effect gene, abnormal oocyte (abo), of Drosophila melanogaster encodes a specific negative regulator of histones Proc Natl Acad Sci USA 98 2001 12126 12131
18. E. Sullivan, C. Santiago, E.D. Parker, Z. Dominski, X. Yang, D.J. Lanzotti, T.C. Ingledue, W.F. Marzluff, and R.J. Duronio Drosophila stem loop binding protein coordinates accumulation of histone mRNA with cell cycle progression Genes Dev 15 2001 173 187
19. Y. Doyon, and J. Côté The highly conserved and multifunctional NuA4 HAT complex Curr Opin Genet Dev 14 2004 147 154
20. S. Henikoff, and Y. Dalal Centromeric chromatin: what makes it unique? Curr Opin Genet Dev 15 2005 177 184
21. S. Henikoff, and K. Ahmad Assembly of variant histones into chromatin Annu Rev Cell Dev Biol 21 2005 133 153
22. H. Tagami, D. Ray-Gallet, G. Almouzni, and Y. Nakatani Histone H3.1 and H3. 3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis Cell 116 2004 51 61 This study provides compelling evidence that, in human cells, CAF-1 is dedicated to replication-dependent nucleosome assembly, whereas HIRA (a homologue of two yeast Hir proteins) is involved exclusively in replication-independent nucleosome assembly.
23. P.G. Giresi, M. Gupta, and J.D. Lieb Regulation of nucleosome assembly as a mediator of chromatin function Curr Opin Genet Dev 16 2006 171 176
24. H.R. Woodland Histone synthesis during the development of Xenopus FEBS Lett 121 1980 1 7
25. J.A. Kleinschmidt, C. Dingwall, G. Maier, and W.W. Franke Molecular characterization of a karyophilic histone binding protein: cDNA cloning, amino acid sequence and expression of nuclear protein N1/N2 of Xenopus laevis EMBO J 5 1986 3547 3552
26. S.M. Dilworth, S.J. Black, and R.A. Laskey Two complexes that contain histones are required for nucleosome assembly in vitro: Role of nucleoplasmin and N1 in Xenopus egg extracts Cell 51 1987 1009 1018
27. S. Dutta, I.V. Akey, C. Dingwall, K.L. Hartman, T. Laue, R.T. Nolte, J.F. Head, and C.W. Akey The crystal structure of nucleoplasmin core: implications for histone binding and nucleosome assembly Mol Cell 8 2001 841 853
28. K. Shintomi, M. Iwabuchi, H. Saeki, K. Ura, T. Kishimoto, and K. Ohsumi Nucleosome assembly protein-1 is a linker histone chaperone in Xenopus eggs Proc Natl Acad Sci USA 102 2005 8210 8215 The physiologically relevant assembly factors for linker histones are not known. The authors purified a complex of NAP-1 and the embryonic linker histone B4 from Xenopus eggs and showed that NAP-1 can act as a chaperone to promote the incorporation of B4 into nucleosomes in vitro. This is a novel function for NAP-1, which had previously been shown to associate with H2A-H2B in vivo.
29. D. Oliver, D. Granner, and R. Chalkley Identification of a distinction between cytoplasmic histone synthesis and subsequent histone deposition within the nucleus Biochemistry 13 1974 746 749
30. Z. Dominski, X. Yang, H. Kaygun, M. Dadlez, and W.F. Marzluff A 3′ exonuclease that specifically interacts with the 3′ end of histone mRNA Mol Cell 12 2003 295 305
31. C. Blackwell, K.A. Martin, A. Greenall, A. Pidoux, R.C. Allshire, and S.K. Whitehall The Schizosaccharomyces pombe HIRA-like protein, Hip1 is required for the periodic expression of histone genes and contributes to the function of complex centromeres Mol Cell Biol 24 2004 4309 4320 The authors demonstrate that the function of Hir proteins in transcriptional repression is conserved. The S. pombe Hir proteins have evolved a unique function in the maintenance of pericentric chromatin structure that is important for faithful mitotic chromosome segregation.
32. •]
33. •], the authors demonstrate that the degradation of histone mRNAs triggered by replication arrest is dependent upon the protein kinase ATR and occurs during termination of translation.
34. •]
35. •], this study shows that the four Hir proteins exist as part of a complex that promotes replication-independent nucleosome assembly, thereby providing a biochemical rationale for earlier genetic evidence describing the in vivo functions of Hir proteins.
36. S.L. Commerford, A.L. Carsten, and E.P. Cronkite Histone turnover within nonproliferating cells Proc Natl Acad Sci USA 79 1982 1163 1165
37. S. Tsvetkov, E. Ivanova, and L. Djondjurov Metabolic behaviors of the core histones in proliferating Friend cells Exp Cell Res 180 1989 94 105
38. A.M. Wunsch, and J. Lough Histones synthesized at different stages of myogenesis are differentially degraded in myotube cells J Cell Physiol 141 1989 97 102
39. F.D. Sweeney, F. Yang, A. Chi, J. Shabanowitz, D.F. Hunt, and D. Durocher Saccharomyces cerevisiae Rad9 acts as a Mec1 adaptor to allow Rad53 activation Curr Biol 15 2005 1364 1375 This study demonstrates that an important role of Rad9 - a protein related to human 53BP1 - in the DNA damage response is to enable the upstream kinase Mec1 (related to human ATM and ATR) to phosphorylate and activate the effector protein kinase Rad53 (homologous to human CHK1 and CHK2). The authors also demonstrate by mass spectrometry that Mec1 can phosphorylate target sites that do not conform to the generally accepted consensus SQ/TQ dipeptide. These findings greatly enhance the spectrum of phosphorylation sites in targets of Mec1-related protein kinases, which play numerous roles in the DNA damage response.
40. Y. Takami, S. Takeda, and T. Nakayama An approximately half set of histone genes is enough for cell proliferation and a lack of several histone variants causes protein pattern changes in the DT40 chicken B cell line J Mol Biol 265 1997 394 408
41. S.G. Holmes, and M.M. Smith Replication of minichromosomes in Saccharomyces cerevisiae is sensitive to histone gene copy number and strain ploidy Yeast 18 2001 291 300
42. Y. Fan, T. Nikitina, E.M. Morin-Kensicki, J. Zhao, T.R. Magnuson, C.L. Woodcock, and A.I. Skoultchi H1 linker histones are essential for mouse development and affect nucleosome spacing in vivo Mol Cell Biol 23 2003 4559 4572
43. B.G. Mellone, L. Ball, N. Suka, M.R. Grunstein, J.F. Partridge, and R.C. Allshire Centromere silencing and function in fission yeast is governed by the amino terminus of histone H3 Curr Biol 13 2003 1748 1757
44. X. Zhao, A. Chabes, V. Domkin, L. Thelander, and R. Rothstein The ribonucleotide reductase inhibitor Sml1 is a new target of the Mec1/Rad53 kinase cascade during growth and in response to DNA damage EMBO J 20 2001 3544 3553
45. J.A. Tercero, and J.F.X. Diffley Regulation of DNA replication fork progression through damaged DNA by the Mec1/Rad53 checkpoint Nature 412 2001 553 557
46. J.M. Sogo, M. Lopes, and M. Foiani Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects Science 297 2002 599 602
47. C. Cotta-Ramusino, D. Fachinetti, C. Lucca, Y. Doksani, M. Lopes, J. Sogo, and M. Foiani Exo1 processes stalled replication forks and counteracts fork reversal in checkpoint-defective cells Mol Cell 17 2005 153 159
48. S. Ghaemmaghami, W.-K. Huh, K. Bower, R.W. Howson, A. Belle, N. Dephoure, E.K. O'Shea, and J.S. Weissman Global analysis of protein expression in yeast Nature 425 2003 737 741
49. C.M. Pickart Back to the future with ubiquitin Cell 116 2004 181 190
50. R.L. Welchman, C. Gordon, and R.J. Mayer Ubiquitin and ubiquitin-like proteins as multifunctional signals Nat Rev Mol Cell Biol 6 2005 599 609
51. W.-K. Huh, J.V. Falvo, L.C. Gerke, A.S. Carroll, R.W. Howson, J.S. Weissman, and E.K. O'Shea Global analysis of protein localization in budding yeast Nature 425 2003 686 691
52. A.J. Rivett Intracellular distribution of proteasomes Curr Opin Immunol 10 1998 110 114
53. S.J. Russell, K.A. Steger, and S.A. Johnston Subcellular localization, stoichiometry, and protein levels of 26S proteasome subunits in yeast J Biol Chem 274 1999 21943 21952
54. C. Kahana, G. Asher, and Y. Shaul Mechanisms of protein degradation: an odyssey with ODC Cell Cycle 4 2005 1461 1464
55. A.L. Haas, P.M. Bright, and V.E. Jackson Functional diversity among putative E2 isozymes in the mechanism of ubiquitin-histone ligation J Biol Chem 263 1988 13268 13275
56. C.M. Pickart, and A.T. Vella Ubiquitin carrier protein-catalyzed ubiquitin transfer to histones. Mechanism and specificity J Biol Chem 263 1988 15076 15082
57. A. Haas, P.M. Reback, G. Pratt, and M. Rechsteiner Ubiquitin-mediated degradation of histone H3 does not require the substrate-binding ubiquitin protein ligase, E3, or attachment of polyubiquitin chains J Biol Chem 265 1990 21664 21669
58. 1 DNA damage checkpoint. The p53 and p21 proteins act by preventing NPAT - a known activator or replication-dependent histone genes - from being phosphorylated by cyclin E-CDK2 and recruited to histone gene clusters located in Cajal bodies.
59. R.T. Abraham PI 3-kinase related kinases: 'big' players in stress-induced signaling pathways DNA Repair (Amst) 3 2004 883 887
60. M.D. Blower, and G.H. Karpen The role of Drosophila CID in kinetochore formation, cell-cycle progression and heterochromatin interactions Nat Cell Biol 3 2001 730 739
61. G. Goshima, T. Kiyomitsu, K. Yoda, and M. Yanagida Human centromere chromatin protein hMis12, essential for equal segregation, is independent of CENP-A loading pathway J Cell Biol 160 2003 25 39
62. K.A. Collins, A.R. Castillo, S.Y. Tatsutani, and S. Biggins De novo kinetochore assembly requires the centromeric histone H3 variant Mol Biol Cell 16 2005 5649 5660
63. K.A. Collins, S. Furuyama, and S. Biggins Proteolysis contributes to the exclusive centromere localization of the yeast Cse4/CENP-A histone H3 variant Curr Biol 14 2004 1968 1972 The authors demonstrate that Cse4 molecules mis-incorporated into euchromatin are degraded by proteasomes. In striking contrast, Cse4 properly incorporated at centromeres is protected from degradation even when Cse4 is epitope-tagged with an N-terminal degron in an attempt to force its degradation.
64. A.A. van Hooser, I.I. Ouspenski, H.C. Gregson, D.A. Starr, T.J. Yen, M.L. Goldberg, K. Yokomori, W.C. Earnshaw, K.F. Sullivan, and K.R. Brinkley Specification of kinetochore-forming chromatin by the histone H3 variant CENP-A J Cell Sci 114 2001 3529 3542
65. B. Black, D.R. Foltz, S. Chakravarty, K. Luger, V.L. Woods Jr., and D.W. Cleveland Structural determinants for generating centromeric chromatin Nature 430 2004 578 582 On the basis of hydrodynamic and deuterium exchange measurements, the authors conclude that CENP-A-H4 tetramers are more compact and conformationally rigid than canonical H3-H4 tetramers. They also identified a highly rigid region of CENP-A comprising residues in the L1 loop and the α2 helix of the CENP-A histone-fold. A histone H3 hybrid protein containing the L1 loop and the α2 helix of CENP-A was specifically targeted to centromeres rather than being deposited throughout the genome.
66. M.K. Raghuraman, E.A. Winzeler, D. Collingwood, S. Hunt, L. Wodicka, A. Conway, D.J. Lockhart, R.W. Davis, B.J. Brewer, and W.L. Fangman Replication dynamics of the yeast genome Science 294 2001 115 121
67. C.G. Pearson, E. Yeh, M. Gardner, D. Odde, E.D. Salmon, and K. Bloom Stable kinetochore-microtubule attachment constrains centromere positioning in metaphase Curr Biol 14 2004 1962 1967 Fluorescence recovery after photobleaching of Cse4-GFP was used to demonstrate that, during most of the cell cycle, Cse4-GFP was stably bound to centromeres. However, at the time of bud emergence during early S phase, pre-existing Cse4 molecules were displaced from centromeres and replaced by newly synthesized molecules.
68. R.T. Kamakaka, and S. Biggins Histone variants: deviants? Genes Dev 19 2005 295 310
69. A. Ciechanover, and R. Ben-Saadon N-terminal ubiquitination: more protein substrates join in Trends Cell Biol 14 2004 103 106
70. N. Mosammaparast, Y. Guo, J. Shabanowitz, D.F. Hunt, and L.F. Pemberton Pathways mediating the nuclear import of histones H3 and H4 in yeast J Biol Chem 277 2002 862 868
71. N. Mosammaparast, C.S. Ewart, and L.F. Pemberton A role for nucleosome assembly protein 1 in the nuclear import of histones H2A and H2B EMBO J 21 2002 6527 6538
72. ••].
73. •] discovered a novel nucleosome assembly factor termed Hif1 (Hat1-interacting factor), which formed a complex with the Hat1-Hat2 B-type histone acetyltransferase (HAT) and newly synthesized histones. The existence of this stable complex suggests that newly synthesized histones are not immediately released as free histones following their acetylation by B-type HATs.
74. O. Ullrich, T. Reinheckel, N. Sitte, R. Hass, T. Grune, and K.J.A. Davies Poly (ADP-ribose) polymerase activates nuclear proteasome to degrade oxidatively damaged histones Proc Natl Acad Sci USA 96 1999 6223 6228
75. R. Shringarpure, T. Grune, J. Mehlhase, and K.J.A. Davies Ubiquitin conjugation is not required for the degradation of oxidized proteins by proteasome J Biol Chem 278 2003 311 318
76. L.K. Mee, and S.J. Adelstein Predominance of core histones in formation of DNA-protein crosslinks in γ-irradiated chromatin Proc Natl Acad Sci USA 78 1981 2194 2198
77. Y. Pommier, C. Redon, V.A. Rao, J.A. Seiler, O. Sordet, H. Takemura, S. Antony, L. Meng, Z. Liao, G. Kohlhagen, H. Zhang, and K.W. Kohn Repair of and checkpoint response to topoisomerase I-mediated DNA damage Mutat Res 532 2003 173 203
78. C. Caron, J. Govin, S. Rousseaux, and S. Khochbin How to pack the genome for a safe trip Prog Mol Subcell Biol 38 2005 65 89
79. A. Greenall, E.S. Williams, K.A. Martin, J.M. Palmer, J. Gray, C. Liu, and S.K. Whitehall Hip3 interacts with the hira proteins Hip1 and Slm9 and is required for transcriptional silencing and accurate chromosome segregation J Biol Chem 2006 DOI:10.1074/jbc.M512170200 See update.