Chaperoning Histones during DNA Replication and Repair

Cell

Volumn 140, Issue 2, 2010, Pages 183-195

  Ransom, Monica ^a   Dennehey, Briana K ^a   Tyler, Jessica K ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ANTISILENCING FUNCTION 1 PROTEIN; CARRIER PROTEIN; CENTROMERE PROTEIN A; CHAPERONE; CHROMATIN ASSEMBLY FACTOR 1; CHZ1 PROTEIN; FACILITATE CHROMATIN TRANSCRIPTION PROTEIN; HISTONE; HISTONE H2A; HISTONE H3; LYSINE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NUCLEAR AUTOANTIGENIC SPERM PROTEIN; NUCLEOPHOSMIN; NUCLEOSOME ASSEMBLY PROTEIN 1; PROTEIN HJURP; RTT106 PROTEIN; SUPPRESSOR OF CHROMOSOME MISEGREGATION 3 PROTEIN; UNCLASSIFIED DRUG;

BINDING KINETICS; CENTROMERE; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA REPAIR; DNA REPLICATION; DNA STRAND BREAKAGE; HISTONE CODE; HUMAN; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS REGULATION; PROTEIN VARIANT; REVIEW;

EID: 74549138158     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2010.01.004     Document Type: Review

References (101)

1. Belotserkovskaya R., Oh S., Bondarenko V.A., Orphanides G., Studitsky V.M., and Reinberg D. FACT facilitates transcription-dependent nucleosome alteration. Science 301 (2003) 1090-1093
2. Black B.E., and Bassett E.A. The histone variant CENP-A and centromere specification. Curr. Opin. Cell Biol. 20 (2008) 91-100
3. Black B.E., Brock M.A., Bédard S., Woods Jr. V.L., and Cleveland D.W. An epigenetic mark generated by the incorporation of CENP-A into centromeric nucleosomes. Proc. Natl. Acad. Sci. USA 104 (2007) 5008-5013
4. Chen C.C., Carson J.J., Feser J., Tamburini B., Zabaronick S., Linger J., and Tyler J.K. Acetylated lysine 56 on histone H3 drives chromatin assembly after repair and signals for the completion of repair. Cell 134 (2008) 231-243
5. Corpet A., and Almouzni G. Making copies of chromatin: the challenge of nucleosomal organization and epigenetic information. Trends Cell Biol. 19 (2009) 29-41
6. Dinant C., Houtsmuller A.B., and Vermeulen W. Chromatin structure and DNA damage repair. Epigenetics Chromatin 1 (2008) 9
7. Dubrana K., van Attikum H., Hediger F., and Gasser S.M. The processing of double-strand breaks and binding of single-strand-binding proteins RPA and Rad51 modulate the formation of ATR-kinase foci in yeast. J. Cell Sci. 120 (2007) 4209-4220
8. Dunleavy E.M., Roche D., Tagami H., Lacoste N., Ray-Gallet D., Nakamura Y., Daigo Y., Nakatani Y., and Almouzni-Pettinotti G. HJURP is a cell-cycle-dependent maintenance and deposition factor of CENP-A at centromeres. Cell 137 (2009) 485-497
9. Dutta S., Akey I.V., Dingwall C., Hartman K.L., Laue T., Nolte R.T., Head J.F., and Akey C.W. The crystal structure of nucleoplasmin-core: implications for histone binding and nucleosome assembly. Mol. Cell 8 (2001) 841-853
10. English C.M., Adkins M.W., Carson J.J., Churchill M.E., and Tyler J.K. Structural basis for the histone chaperone activity of Asf1. Cell 127 (2006) 495-508
11. Escargueil A.E., Soares D.G., Salvador M., Larsen A.K., and Henriques J.A. What histone code for DNA repair?. Mutat. Res. 658 (2008) 259-270
12. Finn R.M., Browne K., Hodgson K.C., and Ausió J. sNASP, a histone H1-specific eukaryotic chaperone dimer that facilitates chromatin assembly. Biophys. J. 95 (2008) 1314-1325
13. Foltz D.R., Jansen L.E., Bailey A.O., Yates III J.R., Bassett E.A., Wood S., Black B.E., and Cleveland D.W. Centromere-specific assembly of CENP-a nucleosomes is mediated by HJURP. Cell 137 (2009) 472-484
14. Franco A.A., Lam W.M., Burgers P.M., and Kaufman P.D. Histone deposition protein Asf1 maintains DNA replisome integrity and interacts with replication factor C. Genes Dev. 19 (2005) 1365-1375
15. Fujita Y., Hayashi T., Kiyomitsu T., Toyoda Y., Kokubu A., Obuse C., and Yanagida M. Priming of centromere for CENP-A recruitment by human hMis18alpha, hMis18beta, and M18BP1. Dev. Cell 12 (2007) 17-30
16. Furuyama T., and Henikoff S. Centromeric nucleosomes induce positive DNA supercoils. Cell 138 (2009) 104-113
17. Gaillard P.H., Martini E.M., Kaufman P.D., Stillman B., Moustacchi E., and Almouzni G. Chromatin assembly coupled to DNA repair: a new role for chromatin assembly factor I. Cell 86 (1996) 887-896
18. Galvani A., Courbeyrette R., Agez M., Ochsenbein F., Mann C., and Thuret J.Y. In vivo study of the nucleosome assembly functions of ASF1 histone chaperones in human cells. Mol. Cell. Biol. 28 (2008) 3672-3685
19. Gambus A., Jones R.C., Sanchez-Diaz A., Kanemaki M., van Deursen F., Edmondson R.D., and Labib K. GINS maintains association of Cdc45 with MCM in replisome progression complexes at eukaryotic DNA replication forks. Nat. Cell Biol. 8 (2006) 358-366
20. Gasser R., Koller T., and Sogo J.M. The stability of nucleosomes at the replication fork. J. Mol. Biol. 258 (1996) 224-239
21. Gravel S., Chapman J.R., Magill C., and Jackson S.P. DNA helicases Sgs1 and BLM promote DNA double-strand break resection. Genes Dev. 22 (2008) 2767-2772
22. Green C.M., and Almouzni G. Local action of the chromatin assembly factor CAF-1 at sites of nucleotide excision repair in vivo. EMBO J. 22 (2003) 5163-5174
23. Groth A., Ray-Gallet D., Quivy J.P., Lukas J., Bartek J., and Almouzni G. Human Asf1 regulates the flow of S phase histones during replicational stress. Mol. Cell 17 (2005) 301-311
24. Groth A., Corpet A., Cook A.J., Roche D., Bartek J., Lukas J., and Almouzni G. Regulation of replication fork progression through histone supply and demand. Science 318 (2007) 1928-1931
25. Han J., Zhou H., Horazdovsky B., Zhang K., Xu R.M., and Zhang Z. Rtt109 acetylates histone H3 lysine 56 and functions in DNA replication. Science 315 (2007) 653-655
26. Haushalter K.A., and Kadonaga J.T. Chromatin assembly by DNA-translocating motors. Nat. Rev. Mol. Cell Biol. 4 (2003) 613-620
27. Heo K., Kim H., Choi S.H., Choi J., Kim K., Gu J., Lieber M.R., Yang A.S., and An W. FACT-mediated exchange of histone variant H2AX regulated by phosphorylation of H2AX and ADP-ribosylation of Spt16. Mol. Cell 30 (2008) 86-97
28. Hertel L., De Andrea M., Bellomo G., Santoro P., Landolfo S., and Gariglio M. The HMG protein T160 colocalizes with DNA replication foci and is down-regulated during cell differentiation. Exp. Cell Res. 250 (1999) 313-328
29. Hoek M., and Stillman B. Chromatin assembly factor 1 is essential and couples chromatin assembly to DNA replication in vivo. Proc. Natl. Acad. Sci. USA 100 (2003) 12183-12188
30. Huang S., Zhou H., Katzmann D., Hochstrasser M., Atanasova E., and Zhang Z. Rtt106p is a histone chaperone involved in heterochromatin-mediated silencing. Proc. Natl. Acad. Sci. USA 102 (2005) 13410-13415
31. Huang S., Zhou H., Tarara J., and Zhang Z. A novel role for histone chaperones CAF-1 and Rtt106p in heterochromatin silencing. EMBO J. 26 (2007) 2274-2283
32. Ito T., Bulger M., Kobayashi R., and Kadonaga J.T. Drosophila NAP-1 is a core histone chaperone that functions in ATP-facilitated assembly of regularly spaced nucleosomal arrays. Mol. Cell. Biol. 16 (1996) 3112-3124
33. Jackson V. Deposition of newly synthesized histones: hybrid nucleosomes are not tandemly arranged on daughter DNA strands. Biochemistry 27 (1988) 2109-2120
34. Jansen L.E., Black B.E., Foltz D.R., and Cleveland D.W. Propagation of centromeric chromatin requires exit from mitosis. J. Cell Biol. 176 (2007) 795-805
35. Jiao R., Bachrati C.Z., Pedrazzi G., Kuster P., Petkovic M., Li J.L., Egli D., Hickson I.D., and Stagljar I. Physical and functional interaction between the Bloom's syndrome gene product and the largest subunit of chromatin assembly factor 1. Mol. Cell. Biol. 24 (2004) 4710-4719
36. Jiao R., Harrigan J.A., Shevelev I., Dietschy T., Selak N., Indig F.E., Piotrowski J., Janscak P., Bohr V.A., and Stagljar I. The Werner syndrome protein is required for recruitment of chromatin assembly factor 1 following DNA damage. Oncogene 26 (2007) 3811-3822
37. Kalocsay M., Hiller N.J., and Jentsch S. Chromosome-wide Rad51 spreading and SUMO-H2A.Z-dependent chromosome fixation in response to a persistent DNA double-strand break. Mol. Cell 33 (2009) 335-343
38. Kim J.A., and Haber J.E. Chromatin assembly factors Asf1 and CAF-1 have overlapping roles in deactivating the DNA damage checkpoint when DNA repair is complete. Proc. Natl. Acad. Sci. USA 106 (2009) 1151-1156
39. Krude T. Chromatin assembly factor 1 (CAF-1) colocalizes with replication foci in HeLa cell nuclei. Exp. Cell Res. 220 (1995) 304-311
40. Kusch T., Florens L., Macdonald W.H., Swanson S.K., Glaser R.L., Yates III J.R., Abmayr S.M., Washburn M.P., and Workman J.L. Acetylation by Tip60 is required for selective histone variant exchange at DNA lesions. Science 306 (2004) 2084-2087
41. Laskey R.A., Honda B.M., Mills A.D., and Finch J.T. Nucleosomes are assembled by an acidic protein which binds histones and transfers them to DNA. Nature 275 (1978) 416-420
42. Li Q., Zhou H., Wurtele H., Davies B., Horazdovsky B., Verreault A., and Zhang Z. Acetylation of histone H3 lysine 56 regulates replication-coupled nucleosome assembly. Cell 134 (2008) 244-255
43. Ling X., Harkness T.A., Schultz M.C., Fisher-Adams G., and Grunstein M. Yeast histone H3 and H4 amino termini are important for nucleosome assembly in vivo and in vitro: redundant and position-independent functions in assembly but not in gene regulation. Genes Dev. 10 (1996) 686-699
44. Linger J., and Tyler J.K. The yeast histone chaperone chromatin assembly factor 1 protects against double-strand DNA-damaging agents. Genetics 171 (2005) 1513-1522
45. Lorch Y., Maier-Davis B., and Kornberg R.D. Chromatin remodeling by nucleosome disassembly in vitro. Proc. Natl. Acad. Sci. USA 103 (2006) 3090-3093
46. Luger K., Mäder A.W., Richmond R.K., Sargent D.F., and Richmond T.J. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389 (1997) 251-260
47. Luk E., Vu N.D., Patteson K., Mizuguchi G., Wu W.H., Ranjan A., Backus J., Sen S., Lewis M., Bai Y., and Wu C. Chz1, a nuclear chaperone for histone H2AZ. Mol. Cell 25 (2007) 357-368
48. Masumoto H., Hawke D., Kobayashi R., and Verreault A. A role for cell-cycle-regulated histone H3 lysine 56 acetylation in the DNA damage response. Nature 436 (2005) 294-298
49. Mello J.A., Silljé H.H., Roche D.M., Kirschner D.B., Nigg E.A., and Almouzni G. Human Asf1 and CAF-1 interact and synergize in a repair-coupled nucleosome assembly pathway. EMBO Rep. 3 (2002) 329-334
50. Mizuguchi G., Shen X., Landry J., Wu W.H., Sen S., and Wu C. ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science 303 (2004) 343-348
51. Mizuguchi G., Xiao H., Wisniewski J., Smith M.M., and Wu C. Nonhistone Scm3 and histones CenH3-H4 assemble the core of centromere-specific nucleosomes. Cell 129 (2007) 1153-1164
52. Moggs J.G., Grandi P., Quivy J.P., Jónsson Z.O., Hübscher U., Becker P.B., and Almouzni G. A CAF-1-PCNA-mediated chromatin assembly pathway triggered by sensing DNA damage. Mol. Cell. Biol. 20 (2000) 1206-1218
53. Murzina N.V., Pei X.Y., Zhang W., Sparkes M., Vicente-Garcia J., Pratap J.V., McLaughlin S.H., Ben-Shahar T.R., Verreault A., Luisi B.F., and Laue E.D. Structural basis for the recognition of histone H4 by the histone-chaperone RbAp46. Structure 16 (2008) 1077-1085
54. Nabatiyan A., and Krude T. Silencing of chromatin assembly factor 1 in human cells leads to cell death and loss of chromatin assembly during DNA synthesis. Mol. Cell. Biol. 24 (2004) 2853-2862
55. Nabatiyan A., Szüts D., and Krude T. Induction of CAF-1 expression in response to DNA strand breaks in quiescent human cells. Mol. Cell. Biol. 26 (2006) 1839-1849
56. Natsume R., Eitoku M., Akai Y., Sano N., Horikoshi M., and Senda T. Structure and function of the histone chaperone CIA/ASF1 complexed with histones H3 and H4. Nature 446 (2007) 338-341
57. Neumann H., Hancock S.M., Buning R., Routh A., Chapman L., Somers J., Owen-Hughes T., van Noort J., Rhodes D., and Chin J.W. A method for genetically installing site-specific acetylation in recombinant histones defines the effects of H3 K56 acetylation. Mol. Cell 36 (2009) 153-163
58. Okuhara K., Ohta K., Seo H., Shioda M., Yamada T., Tanaka Y., Dohmae N., Seyama Y., Shibata T., and Murofushi H. A DNA unwinding factor involved in DNA replication in cell-free extracts of Xenopus eggs. Curr. Biol. 9 (1999) 341-350
59. Park Y.J., and Luger K. The structure of nucleosome assembly protein 1. Proc. Natl. Acad. Sci. USA 103 (2006) 1248-1253
60. Pidoux A.L., Choi E.S., Abbott J.K., Liu X., Kagansky A., Castillo A.G., Hamilton G.L., Richardson W., Rappsilber J., He X., and Allshire R.C. Fission yeast Scm3: A CENP-A receptor required for integrity of subkinetochore chromatin. Mol. Cell 33 (2009) 299-311
61. Polo S.E., Roche D., and Almouzni G. New histone incorporation marks sites of UV repair in human cells. Cell 127 (2006) 481-493
62. Prior C.P., Cantor C.R., Johnson E.M., and Allfrey V.G. Incorporation of exogenous pyrene-labeled histone into Physarum chromatin: a system for studying changes in nucleosomes assembled in vivo. Cell 20 (1980) 597-608
63. Ramey C.J., Howar S., Adkins M., Linger J., Spicer J., and Tyler J.K. Activation of the DNA damage checkpoint in yeast lacking the histone chaperone anti-silencing function 1. Mol. Cell. Biol. 24 (2004) 10313-10327
64. Ray-Gallet D., Quivy J.P., Silljé H.W., Nigg E.A., and Almouzni G. The histone chaperone Asf1 is dispensable for direct de novo histone deposition in Xenopus egg extracts. Chromosoma 116 (2007) 487-496
65. Raynard S., Niu H., and Sung P. DNA double-strand break processing: the beginning of the end. Genes Dev. 22 (2008) 2903-2907
66. Recht J., Tsubota T., Tanny J.C., Diaz R.L., Berger J.M., Zhang X., Garcia B.A., Shabanowitz J., Burlingame A.L., Hunt D.F., et al. Histone chaperone Asf1 is required for histone H3 lysine 56 acetylation, a modification associated with S phase in mitosis and meiosis. Proc. Natl. Acad. Sci. USA 103 (2006) 6988-6993
67. Richardson R.T., Alekseev O.M., Grossman G., Widgren E.E., Thresher R., Wagner E.J., Sullivan K.D., Marzluff W.F., and O'Rand M.G. Nuclear autoantigenic sperm protein (NASP), a linker histone chaperone that is required for cell proliferation. J. Biol. Chem. 281 (2006) 21526-21534
68. Sanematsu F., Takami Y., Barman H.K., Fukagawa T., Ono T., Shibahara K.I., and Nakayama T. Asf1 is required for viability and chromatin assembly during DNA replication in vertebrate cells. J. Biol. Chem. 281 (2006) 13817-13827
69. Schlesinger M.B., and Formosa T. POB3 is required for both transcription and replication in the yeast Saccharomyces cerevisiae. Genetics 155 (2000) 1593-1606
70. Schuh M., Lehner C.F., and Heidmann S. Incorporation of Drosophila CID/CENP-A and CENP-C into centromeres during early embryonic anaphase. Curr. Biol. 17 (2007) 237-243
71. Schulz L.L., and Tyler J.K. The histone chaperone ASF1 localizes to active DNA replication forks to mediate efficient DNA replication. FASEB J. 20 (2006) 488-490
72. Shibahara K., and Stillman B. Replication-dependent marking of DNA by PCNA facilitates CAF-1-coupled inheritance of chromatin. Cell 96 (1999) 575-585
73. Shroff R., Arbel-Eden A., Pilch D., Ira G., Bonner W.M., Petrini J.H., Haber J.E., and Lichten M. Distribution and dynamics of chromatin modification induced by a defined DNA double-strand break. Curr. Biol. 14 (2004) 1703-1711
74. Smerdon M.J. DNA repair and the role of chromatin structure. Curr. Opin. Cell Biol. 3 (1991) 422-428
75. Smerdon M.J., and Lieberman M.W. Nucleosome rearrangement in human chromatin during UV-induced DNA- reapir synthesis. Proc. Natl. Acad. Sci. USA 75 (1978) 4238-4241
76. Smerdon M.J., Lan S.Y., Calza R.E., and Reeves R. Sodium butyrate stimulates DNA repair in UV-irradiated normal and xeroderma pigmentosum human fibroblasts. J. Biol. Chem. 257 (1982) 13441-13447
77. Smith S., and Stillman B. Purification and characterization of CAF-I, a human cell factor required for chromatin assembly during DNA replication in vitro. Cell 58 (1989) 15-25
78. Sogo J.M., Stahl H., Koller T., and Knippers R. Structure of replicating simian virus 40 minichromosomes. The replication fork, core histone segregation and terminal structures. J. Mol. Biol. 189 (1986) 189-204
79. Song J.J., Garlick J.D., and Kingston R.E. Structural basis of histone H4 recognition by p55. Genes Dev. 22 (2008) 1313-1318
80. Stillman B. Chromatin assembly during SV40 DNA replication in vitro. Cell 45 (1986) 555-565
81. Stoler S., Rogers K., Weitze S., Morey L., Fitzgerald-Hayes M., and Baker R.E. Scm3, an essential Saccharomyces cerevisiae centromere protein required for G2/M progression and Cse4 localization. Proc. Natl. Acad. Sci. USA 104 (2007) 10571-10576
82. Stuwe T., Hothorn M., Lejeune E., Rybin V., Bortfeld M., Scheffzek K., and Ladurner A.G. The FACT Spt16 "peptidase" domain is a histone H3-H4 binding module. Proc. Natl. Acad. Sci. USA 105 (2008) 8884-8889
83. Tagami H., Ray-Gallet D., Almouzni G., and Nakatani Y. Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 116 (2004) 51-61
84. Tamburini B.A., and Tyler J.K. Localized histone acetylation and deacetylation triggered by the homologous recombination pathway of double-strand DNA repair. Mol. Cell. Biol. 25 (2005) 4903-4913
85. Tan B.C., Chien C.T., Hirose S., and Lee S.C. Functional cooperation between FACT and MCM helicase facilitates initiation of chromatin DNA replication. EMBO J. 25 (2006) 3975-3985
86. Tsubota T., Berndsen C.E., Erkmann J.A., Smith C.L., Yang L., Freitas M.A., Denu J.M., and Kaufman P.D. Histone H3-K56 acetylation is catalyzed by histone chaperone-dependent complexes. Mol. Cell 25 (2007) 703-712
87. Tsukuda T., Fleming A.B., Nickoloff J.A., and Osley M.A. Chromatin remodelling at a DNA double-strand break site in Saccharomyces cerevisiae. Nature 438 (2005) 379-383
88. Tyler J.K., Adams C.R., Chen S.R., Kobayashi R., Kamakaka R.T., and Kadonaga J.T. The RCAF complex mediates chromatin assembly during DNA replication and repair. Nature 402 (1999) 555-560
89. Tyler J.K., Collins K.A., Prasad-Sinha J., Amiott E., Bulger M., Harte P.J., Kobayashi R., and Kadonaga J.T. Interaction between the Drosophila CAF-1 and ASF1 chromatin assembly factors. Mol. Biol. Cell 21 (2001) 6574-6584
90. van Attikum H., Fritsch O., and Gasser S.M. Distinct roles for SWR1 and INO80 chromatin remodeling complexes at chromosomal double-strand breaks. EMBO J. 26 (2007) 4113-4125
91. VanDemark A.P., Blanksma M., Ferris E., Heroux A., Hill C.P., and Formosa T. The structure of the yFACT Pob3-M domain, its interaction with the DNA replication factor RPA, and a potential role in nucleosome deposition. Mol. Cell 22 (2006) 363-374
92. VanDemark A.P., Xin H., McCullough L., Rawlins R., Bentley S., Heroux A., Stillman D.J., Hill C.P., and Formosa T. Structural and functional analysis of the Spt16p N-terminal domain reveals overlapping roles of yFACT subunits. J. Biol. Chem. 283 (2008) 5058-5068
93. Verreault A., Kaufman P.D., Kobayashi R., and Stillman B. Nucleosome assembly by a complex of CAF-1 and acetylated histones H3/H4. Cell 87 (1996) 95-104
94. Wieland G., Orthaus S., Ohndorf S., Diekmann S., and Hemmerich P. Functional complementation of human centromere protein A (CENP-A) by Cse4p from Saccharomyces cerevisiae. Mol. Cell. Biol. 24 (2004) 6620-6630
95. Williams S.K., Truong D., and Tyler J.K. Acetylation in the globular core of histone H3 on lysine-56 promotes chromatin disassembly during transcriptional activation. Proc. Natl. Acad. Sci. USA 105 (2008) 9000-9005
96. Williams J.S., Hayashi T., Yanagida M., and Russell P. Fission yeast Scm3 mediates stable assembly of Cnp1/CENP-A into centromeric chromatin. Mol. Cell 33 (2009) 287-298
97. Wittmeyer J., and Formosa T. The Saccharomyces cerevisiae DNA polymerase alpha catalytic subunit interacts with Cdc68/Spt16 and with Pob3, a protein similar to an HMG1-like protein. Mol. Cell. Biol. 17 (1997) 4178-4190
98. Xin H., Takahata S., Blanksma M., McCullough L., Stillman D.J., and Formosa T. yFACT induces global accessibility of nucleosomal DNA without H2A-H2B displacement. Mol. Cell 35 (2009) 365-376
99. Ye X., Franco A.A., Santos H., Nelson D.M., Kaufman P.D., and Adams P.D. Defective S phase chromatin assembly causes DNA damage, activation of the S phase checkpoint, and S phase arrest. Mol. Cell 11 (2003) 341-351
100. Ye J., Ai X., Eugeni E.E., Zhang L., Carpenter L.R., Jelinek M.A., Freitas M.A., and Parthun M.R. Histone H4 lysine 91 acetylation a core domain modification associated with chromatin assembly. Mol. Cell 18 (2005) 123-130
101. Zhou Z., Feng H., Hansen D.F., Kato H., Luk E., Freedberg D.I., Kay L.E., Wu C., and Bai Y. NMR structure of chaperone Chz1 complexed with histones H2A.Z-H2B. Nat. Struct. Mol. Biol. 15 (2008) 868-869