Generation and management of excess histones during the cell cycle

Frontiers in Bioscience

Volumn 14, Issue 8, 2009, Pages 3145-3158

  Singh, Rakesh Kumar ^a   Paik, Johanna ^a   Gunjan, Akash ^a  

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

Author keywords

DNA damage; Genomic stability; Histones; Rad53; Ubiquitylation

Indexed keywords

EUKARYOTA; SACCHAROMYCETALES;

HISTONE;

BIOSYNTHESIS; CELL CYCLE; HUMAN; REVIEW;

CELL CYCLE; HISTONES; HUMANS;

EID: 63849151495     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2735/3441     Document Type: Article

References (111)

1. van Holde, K. E.: Chromatin. Springer-Verlag, New York (1988).
2. Wolffe, A. P.: Chromatin: Structure and Function. Academic Press, San Diego (1995).
3. Richmond, T. J. and C. A. Davey: The structure of DNA in the nucleosome core. Nature, 423(6936), 145-50 (2003). (Pubitemid 36569532)
4. Brown, D. T.: Histone H1 and the dynamic regulation of chromatin function. Biochem Cell Biol, 81(3), 221-7 (2003). (Pubitemid 37076244)
5. Verreault, A.: De novo nucleosome assembly: new pieces in an old puzzle. Genes Dev, 14(12), 1430-8 (2000). (Pubitemid 30421836)
6. Gunjan, A., J. Paik and A. Verreault: Regulation of histone synthesis and nucleosome assembly. Biochimie, 87(7), 625-35 (2005). (Pubitemid 40884625)
7. Han, M., 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(4), 589-97 (1987).
8. Ye, X., 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(2), 341-51 (2003). (Pubitemid 36293829)
9. Nelson, D. M., 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(21), 7459-72 (2002).
10. Prado, F. and A. Aguilera: Partial depletion of histone H4 increases homologous recombination-mediated genetic instability. Mol Cell Biol, 25(4), 1526-36 (2005). (Pubitemid 40204927)
11. Lengauer, C., K. W. Kinzler and B. Vogelstein: Genetic instabilities in human cancers. Nature, 396(6712), 643-9 (1998). (Pubitemid 29003936)
12. Hoeijmakers, J. H.: Genome maintenance mechanisms for preventing cancer. Nature, 411(6835), 366-74 (2001). (Pubitemid 32467046)
13. Steger, D. J. and J. L. Workman: Transcriptional analysis of purified histone acetyltransferase complexes. Methods, 19(3), 410-6 (1999). (Pubitemid 30028600)
14. Meeks-Wagner, D. and L. H. Hartwell: Normal stoichiometry of histone dimer sets is necessary for high fidelity of mitotic chromosome transmission. Cell, 44(1), 43-52 (1986). (Pubitemid 16036712)
15. Sullivan, E., 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 mature histone mRNA with cell cycle progression. Genes Dev, 15(2), 173-87 (2001). (Pubitemid 32107663)
16. Berloco, M., 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 U S A, 98(21), 12126-31 (2001). (Pubitemid 32959838)
17. Gunjan, A. and A. Verreault: A Rad53 kinasedependent surveillance mechanism that regulates histone protein levels in S. cerevisiae. Cell, 115(5), 537-49 (2003). (Pubitemid 37506043)
18. Bonner, W. M., 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(17), 6542-50 (1988).
19. Reis, C. C. and J. L. Campbell: Contribution of Trf4/5 and the nuclear exosome to genome stability through regulation of histone mRNA levels in Saccharomyces cerevisiae. Genetics, 175(3), 993-1010 (2007). (Pubitemid 46798207)
20. Pan, X., P. Ye, D. S. Yuan, X. Wang, J. S. Bader and J. D. Boeke: A DNA integrity network in the yeast Saccharomyces cerevisiae. Cell, 124(5), 1069-81 (2006). (Pubitemid 43344244)
21. Lee, C. K., Y. Shibata, B. Rao, B. D. Strahl and J. D. Lieb: Evidence for nucleosome depletion at active regulatory regions genome-wide. Nat Genet, 36(8), 900-5 (2004). (Pubitemid 39014111)
22. Schermer, U. J., P. Korber and W. Horz: Histones are incorporated in trans during reassembly of the yeast PHO5 promoter. Mol Cell, 19(2), 279-85 (2005). (Pubitemid 41019674)
23. Morillo-Huesca, M., M.-C. Muñoz-Centeno, R. K. Singh, G. U. Reddy, V. Oreal, D. Liang, D. Maya, A. Gunjan, V. Géli and S. Chávez: Accumulation of transcription-evicted histones induces a CLN3-dependent cell cycle delay in G1. Submitted (2008).
24. Stein G. S., J. L. Stein and W. F. Marzluff: Histonegenes: Structure Organization and Regulation. John Wiley & Sons, New York. (1984).
25. Marzluff, W. F., P. Gongidi, K. R. Woods, J. Jin and L. J. Maltais: The human and mouse replicationdependent histone genes. Genomics, 80(5), 487-98 (2002). (Pubitemid 35333791)
26. Sogo, J. M., H. Stahl, T. Koller and R. Knippers: Structure of replicating simian virus 40 minichromosomes. The replication fork, core histone segregation and terminal structures. J Mol Biol, 189(1), 189-204 (1986). (Pubitemid 16063831)
27. Osley, M. A.: The regulation of histone synthesis in the cell cycle. Annu Rev Biochem, 60, 827-61 (1991).
28. Takami, Y., 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(4), 394-408 (1997). (Pubitemid 27110676)
29. Ghaemmaghami, S., 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(6959), 737-41 (2003). (Pubitemid 37314318)
30. Jamai, A., R. M. Imoberdorf and M. Strubin: Continuous histone H2B and transcription-dependent histone H3 exchange in yeast cells outside of replication. Mol Cell, 25(3), 345-55 (2007). (Pubitemid 46199292)
31. Dammann, R., R. Lucchini, T. Koller and J. M. Sogo: Chromatin structures and transcription of rDNA in yeast Saccharomyces cerevisiae. Nucleic Acids Res, 21(10), 2331-8 (1993). (Pubitemid 23180807)
32. Belotserkovskaya, R. and D. Reinberg: Facts about FACT and transcript elongation through chromatin. Curr Opin Genet Dev, 14(2), 139-46 (2004). (Pubitemid 38520141)
33. Williams, S. K. and J. K. Tyler: Transcriptional regulation by chromatin disassembly and reassembly. Curr Opin Genet Dev, 17(2), 88-93 (2007). (Pubitemid 46551714)
34. Loyola, A. and G. Almouzni: Histone chaperones, a supporting role in the limelight. Biochim Biophys Acta, 1677(1-3), 3-11 (2004). (Pubitemid 38327083)
35. Paulovich, A. G. and L. H. Hartwell: A checkpoint regulates the rate of progression through S phase in S. cerevisiae in response to DNA damage. Cell, 82(5), 841-7 (1995).
36. Tercero, J. A. and J. F. Diffley: Regulation of DNA replication fork progression through damaged DNA by the Mec1/Rad53 checkpoint. Nature, 412(6846), 553-7 (2001). (Pubitemid 32743835)
37. Groth, A., 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(2), 301-11 (2005). (Pubitemid 40138623)
38. Downs, J. A., M. C. Nussenzweig and A. Nussenzweig: Chromatin dynamics and the preservation of genetic information. Nature, 447(7147), 951-8 (2007). (Pubitemid 46975762)
39. Tsukuda, T., A. B. Fleming, J. A. Nickoloff and M. A. Osley: Chromatin remodelling at a DNA double-strand break site in Saccharomyces cerevisiae. Nature, 438(7066), 379-83 (2005). (Pubitemid 41643956)
40. Kastan, M. B. and J. Bartek: Cell-cycle checkpoints and cancer. Nature, 432(7015), 316-23 (2004). (Pubitemid 39551659)
41. Weinert, T. A., G. L. Kiser and L. H. Hartwell: Mitotic checkpoint genes in budding yeast and the dependence of mitosis on DNA replication and repair. Genes Dev, 8(6), 652-65 (1994). (Pubitemid 24116760)
42. Lowndes, N. F. and J. R. Murguia: Sensing and responding to DNA damage. Curr Opin Genet Dev, 10(1), 17-25 (2000). (Pubitemid 30113701)
43. Rouse, J. and S. P. Jackson: Interfaces between the detection, signaling, and repair of DNA damage. Science, 297(5581), 547-51 (2002). (Pubitemid 34815330)
44. Sanchez, Y., B. A. Desany, W. J. Jones, Q. Liu, B. Wang and S. J. Elledge: Regulation of RAD53 by the ATM-like kinases MEC1 and TEL1 in yeast cell cycle checkpoint pathways. Science, 271(5247), 357-60 (1996).
45. Santocanale, C. and J. F. Diffley: A Mec1- and Rad53- dependent checkpoint controls late-firing origins of DNA replication. Nature, 395(6702), 615-8 (1998). (Pubitemid 28475717)
46. Desany, B. A., A. A. Alcasabas, J. B. Bachant and S. J. Elledge: Recovery from DNA replicational stress is the essential function of the S-phase checkpoint pathway. Genes Dev, 12(18), 2956-70 (1998). (Pubitemid 28440153)
47. Zhao, X., 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(13), 3544-53 (2001). (Pubitemid 32634361)
48. Borun, T. W., M. D. Scharff and E. Robbins: Rapidly labeled, polyribosome-associated RNA having the properties of histone messenger. Proc Natl Acad Sci U S A, 58(5), 1977-83 (1967).
49. Gallwitz, D. and G. C. Mueller: Histone synthesis in vitro on HeLa cell microsomes. The nature of the coupling to deoxyribonucleic acid synthesis. J Biol Chem, 244(21), 5947-52 (1969).
50. Borun, T. W., F. Gabrielli, K. Ajiro, A. Zweidler and C. Baglioni: Further evidence of transcriptional and translational control of histone messenger RNA during the HeLa S3 cycle. Cell, 4(1), 59-67 (1975).
51. Gallwitz, D.: Kinetics of inactivation of histone mRNA in the cytoplasm after inhibition of DNA replication in synchronised HeLa cells. Nature, 257(5523), 247-8 (1975).
52. Sittman, D. B., R. A. Graves and W. F. Marzluff: Histone mRNA concentrations are regulated at the level of transcription and mRNA degradation. Proc Natl Acad Sci U S A, 80(7), 1849-53 (1983). (Pubitemid 13079193)
53. Lycan, D. E., M. A. Osley and L. M. Hereford: Role of transcriptional and posttranscriptional regulation in expression of histone genes in Saccharomyces cerevisiae. Mol Cell Biol, 7(2), 614-21 (1987). (Pubitemid 17004524)
54. Paik, J., G. U. Reddy, M. M. Kabbaj, A. Verreault and A. Gunjan: Checkpoint kinases repress histone gene transcription in response to genotoxic agents that impede replication. Submitted (2008).
55. Su, C., G. Gao, S. Schneider, C. Helt, C. Weiss, M. A. O'Reilly, D. Bohmann and J. Zhao: DNA damage induces downregulation of histone gene expression through the G1 checkpoint pathway. EMBO J, 23(5), 1133-43 (2004). (Pubitemid 38436877)
56. Kaygun, H. and W. F. Marzluff: Regulated degradation of replication-dependent histone mRNAs requires both ATR and Upf1. Nat Struct Mol Biol, 12(9), 794-800 (2005). (Pubitemid 43086254)
57. Muller, B., J. Blackburn, C. Feijoo, X. Zhao and C. Smythe: DNA-activated protein kinase functions in a newly observed S phase checkpoint that links histone mRNA abundance with DNA replication. J Cell Biol, 179(7), 1385-98 (2007).
58. Marzluff, W. F. and R. J. Duronio: Histone mRNA expression: multiple levels of cell cycle regulation and important developmental consequences. Curr Opin Cell Biol, 14(6), 692-9 (2002). (Pubitemid 35449381)
59. Marzluff, W. F.: Metazoan replication-dependent histone mRNAs: a distinct set of RNA polymerase II transcripts. Curr Opin Cell Biol, 17(3), 274-80 (2005). (Pubitemid 40719917)
60. Chang, Y. F., J. S. Imam and M. F. Wilkinson: The nonsense-mediated decay RNA surveillance pathway. Annu Rev Biochem, 76, 51-74 (2007).
61. Dominski, Z., X. C. 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(2), 295-305 (2003). (Pubitemid 37238917)
62. Sutton, A., J. Bucaria, M. A. Osley and R. Sternglanz: Yeast ASF1 protein is required for cell cycle regulation of histone gene transcription. Genetics, 158(2), 587-96 (2001). (Pubitemid 32552299)
63. Ng, H. H., F. Robert, R. A. Young and K. Struhl: Genome-wide location and regulated recruitment of the RSC nucleosome-remodeling complex. Genes Dev, 16(7), 806-19 (2002). (Pubitemid 34280105)
64. Mitchell, P., E. Petfalski, A. Shevchenko, M. Mann and D. Tollervey: The exosome: a conserved eukaryotic RNA processing complex containing multiple 3'->5' exoribonucleases. Cell, 91(4), 457-66 (1997). (Pubitemid 27508235)
65. Sidorova, J. M. and L. L. Breeden: Rad53-dependent phosphorylation of Swi6 and down-regulation of CLN1 and CLN2 transcription occur in response to DNA damage in Saccharomyces cerevisiae. Genes Dev, 11(22), 3032-45 (1997). (Pubitemid 27508513)
66. Sidorova, J. M. and L. L. Breeden: Rad53 checkpoint kinase phosphorylation site preference identified in the Swi6 protein of Saccharomyces cerevisiae. Mol Cell Biol, 23(10), 3405-16 (2003). (Pubitemid 36539174)
67. Commerford, S. L., A. L. Carsten and E. P. Cronkite: Histone turnover within nonproliferating cells. Proc Natl Acad Sci U S A, 79(4), 1163-5 (1982). (Pubitemid 12105567)
68. Tsvetkov, S., E. Ivanova and L. Djondjurov: Metabolic behaviors of the core histones in proliferating Friend cells. Exp Cell Res, 180(1), 94-105 (1989). (Pubitemid 19031010)
69. Henchoz, S., Y. Chi, B. Catarin, I. Herskowitz, R. J. Deshaies and M. Peter: Phosphorylation- and ubiquitindependent degradation of the cyclin-dependent kinase inhibitor Far1p in budding yeast. Genes Dev, 11(22), 3046- 60 (1997). (Pubitemid 27508514)
70. Deshaies, R. J. and J. E. Ferrell Jr.: Multisite phosphorylation and the countdown to S phase. Cell, 107(7), 819-22 (2001). (Pubitemid 34084972)
71. Hershko, A. and A. Ciechanover: The ubiquitin system. Annu Rev Biochem, 67, 425-79 (1998). (Pubitemid 28411135)
72. Haas, A. L., P. M. Bright and V. E. Jackson: Functional diversity among putative E2 isozymes in the mechanism of ubiquitin-histone ligation. J Biol Chem, 263(26), 13268-75 (1988).
73. Pickart, C. M. and A. T. Vella: Ubiquitin carrier protein-catalyzed ubiquitin transfer to histones. Mechanism and specificity. J Biol Chem, 263(29), 15076-82 (1988).
74. Haas, A., 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(35), 21664-9 (1990). (Pubitemid 120014209)
75. Osley, M. A.: H2B ubiquitylation: the end is in sight. Biochim Biophys Acta, 1677(1-3), 74-8 (2004). (Pubitemid 38327091)
76. Jason, L. J., S. C. Moore, J. D. Lewis, G. Lindsey and J. Ausio: Histone ubiquitination: a tagging tail unfolds? Bioessays, 24(2), 166-74 (2002). (Pubitemid 34179295)
77. Singh, R. K., M. M. Kabbaj, J. Paik, and A. Gunjan: Histone levels are regulated by phosphorylation and ubiquitylation dependent proteolysis in S. cerevisiae. Submitted (2008).
78. Collins, K. A., S. Furuyama and S. Biggins: Proteolysis contributes to the exclusive centromere localization of the yeast Cse4/CENP-A histone H3 variant. Curr Biol, 14(21), 1968-72 (2004). (Pubitemid 39464823)
79. Varshavsky, A.: The N-end rule pathway of protein degradation. Genes Cells, 2(1), 13-28 (1997). (Pubitemid 127688555)
80. Labib, K., J. A. Tercero and J. F. Diffley: Uninterrupted MCM2-7 function required for DNA replication fork progression. Science, 288(5471), 1643-7 (2000). (Pubitemid 30387430)
81. English, C. M., M. W. Adkins, J. J. Carson, M. E. Churchill and J. K. Tyler: Structural basis for the histone chaperone activity of Asf1. Cell, 127(3), 495-508 (2006). (Pubitemid 44647420)
82. Tagami, H., 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(1), 51-61 (2004). (Pubitemid 38156183)
83. Bloom, J., V. Amador, F. Bartolini, G. DeMartino and M. Pagano: Proteasome-mediated degradation of p21 via N-terminal ubiquitinylation. Cell, 115(1), 71-82 (2003). (Pubitemid 37255319)
84. Coulombe, P., G. Rodier, E. Bonneil, P. Thibault and S. Meloche: N-Terminal ubiquitination of extracellular signalregulated kinase 3 and p21 directs their degradation by the proteasome. Mol Cell Biol, 24(14), 6140-50 (2004). (Pubitemid 38891117)
85. Chen, X., Y. Chi, A. Bloecher, R. Aebersold, B. E. Clurman and J. M. Roberts: N-acetylation and ubiquitinindependent proteasomal degradation of p21(Cip1). Mol Cell, 16(5), 839-47 (2004). (Pubitemid 39586541)
86. Touitou, R., J. Richardson, S. Bose, M. Nakanishi, J. Rivett and M. J. Allday: A degradation signal located in the C-terminus of p21WAF1/CIP1 is a binding site for the C8 alpha-subunit of the 20S proteasome. EMBO J, 20(10), 2367-75 (2001). (Pubitemid 32452854)
87. Shringarpure, R., T. Grune, J. Mehlhase and K. J. Davies: Ubiquitin conjugation is not required for the degradation of oxidized proteins by proteasome. J Biol Chem, 278(1), 311-8 (2003). (Pubitemid 36043578)
88. Ullrich, O., N. Sitte, O. Sommerburg, V. Sandig, K. J. Davies and T. Grune: Influence of DNA binding on the degradation of oxidized histones by the 20S proteasome. Arch Biochem Biophys, 362(2), 211-6 (1999). (Pubitemid 29394349)
89. Downs, J. A., S. Allard, O. Jobin-Robitaille, A. Javaheri, A. Auger, N. Bouchard, S. J. Kron, S. P. Jackson and J. Cote: Binding of chromatin-modifying activities to phosphorylated histone H2A at DNA damage sites. Mol Cell, 16(6), 979-90 (2004). (Pubitemid 40018407)
90. Unal, E., A. Arbel-Eden, U. Sattler, R. Shroff, M. Lichten, J. E. Haber and D. Koshland: DNA damage response pathway uses histone modification to assemble a double-strand break-specific cohesin domain. Mol Cell, 16(6), 991-1002 (2004). (Pubitemid 40018408)
91. Osley, M. A., T. Tsukuda and J. A. Nickoloff: ATPdependent chromatin remodeling factors and DNA damage repair. Mutat Res, 618(1-2), 65-80 (2007). (Pubitemid 46574743)
92. Krogan, N. J., M. H. Lam, J. Fillingham, M. C. Keogh, M. Gebbia, J. Li, N. Datta, G. Cagney, S. Buratowski, A. Emili and J. F. Greenblatt: Proteasome involvement in the repair of DNA double-strand breaks. Mol Cell, 16(6), 1027- 34 (2004). (Pubitemid 40018411)
93. Muratani, M. and W. P. Tansey: How the ubiquitinproteasome system controls transcription. Nat Rev Mol Cell Biol, 4(3), 192-201 (2003). (Pubitemid 36288041)
94. Collins, G. A. and W. P. Tansey: The proteasome: a utility tool for transcription? Curr Opin Genet Dev, 16(2), 197-202 (2006). (Pubitemid 43376068)
95. Ferdous, A., F. Gonzalez, L. Sun, T. Kodadek and S. A. Johnston: The 19S regulatory particle of the proteasome is required for efficient transcription elongation by RNA polymerase II. Mol Cell, 7(5), 981-91 (2001). (Pubitemid 32525745)
96. Laribee, R. N., S. M. Fuchs and B. D. Strahl: H2B ubiquitylation in transcriptional control: a FACT-finding mission. Genes Dev, 21(7), 737-43 (2007). (Pubitemid 46572353)
97. Dion, M. F., T. Kaplan, M. Kim, S. Buratowski, N. Friedman and O. J. Rando: Dynamics of replicationindependent histone turnover in budding yeast. Science, 315(5817), 1405-8 (2007). (Pubitemid 46399548)
98. M. L. Meistrich: Histones and Other Basic Nuclear Proteins. CRC, Orlando, FL (1989).
99. Chen, H. Y., J. M. Sun, Y. Zhang, J. R. Davie and M. L. Meistrich: Ubiquitination of histone H3 in elongating spermatids of rat testes. J Biol Chem, 273(21), 13165-9 (1998). (Pubitemid 28246885)
100. Rajapurohitam, V., C. R. Morales, M. El-Alfy, S. Lefrancois, N. Bedard and S. S. Wing: Activation of a UBC4-dependent pathway of ubiquitin conjugation during postnatal development of the rat testis. Dev Biol, 212(1), 217-28 (1999). (Pubitemid 29368348)
101. Wing, S. S., N. Bedard, C. Morales, P. Hingamp and J. Trasler: A novel rat homolog of the Saccharomyces cerevisiae ubiquitin-conjugating enzymes UBC4 and UBC5 with distinct biochemical features is induced during spermatogenesis. Mol Cell Biol, 16(8), 4064-72 (1996). (Pubitemid 26251205)
102. Liu, Z., R. Oughtred and S. S. Wing: Characterization of E3Histone, a novel testis ubiquitin protein ligase which ubiquitinates histones. Mol Cell Biol, 25(7), 2819-31 (2005). (Pubitemid 40381643)
103. Enenkel, C., A. Lehmann and P. M. Kloetzel: Subcellular distribution of proteasomes implicates a major location of protein degradation in the nuclear envelope-ER network in yeast. EMBO J, 17(21), 6144-54 (1998). (Pubitemid 28497788)
104. Russell, S. J., K. A. Steger and S. A. Johnston: Subcellular localization, stoichiometry, and protein levels of 26 S proteasome subunits in yeast. J Biol Chem, 274(31), 21943-52 (1999).
105. Hassa, P. O., S. S. Haenni, M. Elser and M. O. Hottiger: Nuclear ADP-ribosylation reactions in mammalian cells: where are we today and where are we going? Microbiol Mol Biol Rev, 70(3), 789-829 (2006). (Pubitemid 44484693)
106. Ullrich, O., T. Reinheckel, N. Sitte, R. Hass, T. Grune and K. J. Davies: Poly-ADP ribose polymerase activates nuclear proteasome to degrade oxidatively damaged histones. Proc Natl Acad Sci U S A, 96(11), 6223-8 (1999). (Pubitemid 29256647)
107. Sobel, R. E., R. G. Cook, C. A. Perry, A. T. Annunziato and C. D. Allis: Conservation of depositionrelated acetylation sites in newly synthesized histones H3 and H4. Proc Natl Acad Sci U S A, 92(4), 1237-41 (1995).
108. Ma, X. J., J. Wu, B. A. Altheim, M. C. Schultz and M. Grunstein: Deposition-related sites K5/K12 in histone H4 are not required for nucleosome deposition in yeast. Proc Natl Acad Sci U S A, 95(12), 6693-8 (1998). (Pubitemid 28278042)
109. Groth, A., A. Corpet, A. J. Cook, D. Roche, J. Bartek, J. Lukas and G. Almouzni: Regulation of replication fork progression through histone supply and demand. Science, 318(5858), 1928-31 (2007).
110. Zou, L. and S. J. Elledge: Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science, 300(5625), 1542-8 (2003). (Pubitemid 36682880)
111. Muller, B., J. Blackburn, C. Feijoo, X. Zhao and C. Smythe: Are multiple checkpoint mediators involved in a checkpoint linking histone gene expression with DNA replication? Biochem Soc Trans, 35(Pt 5), 1369-71 (2007). (Pubitemid 350206502)