Dynamic Regulation of Replication Independent Deposition of Histone H3 in Fission Yeast

Overview

Journal Nucleic Acids Res

Publisher Oxford University Press

Specialty Biochemistry

Date 2005 Dec 20

PMID 16361268

Citations 24

Authors

Eun Shik Choi

Jin A Shin

Hyun Soo Kim

Yeun Kyu Jang

Affiliations

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Abstract

Recently, a histone H3 variant in Drosophila and humans, the H3.3 protein, was shown to replace canonical H3 in active chromatin in a replication-independent (RI) manner. In the fission yeast Schizosaccharomyces pombe, there exists a single form of H3, which is equivalent to H3.3 and is thought to participate in both replication-independent (RI) and replication-coupled (RC) nucleosome assembly. In this study, we show that RI deposition of H3 at heterochromatic regions is consistently lower than that at a gene-free euchromatic region, and deletion of the conserved heterochromatin-specific proteins Swi6 or Clr4 markedly increases RI deposition at heterochromatic regions such as the silent mating-type loci or centromeres. These results clearly show that RI deposition of H3 occurs preferentially in euchromatic regions. We also observed that RI deposition of H3 could be increased at the thi3(+) gene when transcription is induced, indicating transcription further facilitates RI deposition of H3. Taken together, these observations demonstrate that selective deposition of histone H3.3 at transcriptionally active chromatin by the RI assembly pathway is conserved in fission yeast and, thus, our data support an essential role of histone H3 replacement in maintaining active chromatin among diverse eukaryotic organisms ranging from fission yeast to humans.

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References

Partridge J, Borgstrom B, Allshire R . Distinct protein interaction domains and protein spreading in a complex centromere. Genes Dev. 2000; 14(7):783-91. PMC: 316498. View

Takahashi K, Chen E, Yanagida M . Requirement of Mis6 centromere connector for localizing a CENP-A-like protein in fission yeast. Science. 2000; 288(5474):2215-9. DOI: 10.1126/science.288.5474.2215. View

Lachner M, OCarroll D, Rea S, Mechtler K, Jenuwein T . Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature. 2001; 410(6824):116-20. DOI: 10.1038/35065132. View

Bannister A, Zegerman P, Partridge J, Miska E, Thomas J, Allshire R . Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature. 2001; 410(6824):120-4. DOI: 10.1038/35065138. View

Mello J, Almouzni G . The ins and outs of nucleosome assembly. Curr Opin Genet Dev. 2001; 11(2):136-41. DOI: 10.1016/s0959-437x(00)00170-2. View

Noma K , Allis C, Grewal S . Transitions in distinct histone H3 methylation patterns at the heterochromatin domain boundaries. Science. 2001; 293(5532):1150-5. DOI: 10.1126/science.1064150. View

Ray-Gallet D, Quivy J, Scamps C, Lipinski M, Almouzni G . HIRA is critical for a nucleosome assembly pathway independent of DNA synthesis. Mol Cell. 2002; 9(5):1091-100. DOI: 10.1016/s1097-2765(02)00526-9. View

Ahmad K, Henikoff S . The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol Cell. 2002; 9(6):1191-200. DOI: 10.1016/s1097-2765(02)00542-7. View

Volpe T, Kidner C, Hall I, Teng G, Grewal S, Martienssen R . Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science. 2002; 297(5588):1833-7. DOI: 10.1126/science.1074973. View

10.

Choi E, Kim H, Jang Y, Hong S, Park S . Two ubiquitin-conjugating enzymes, Rhp6 and UbcX, regulate heterochromatin silencing in Schizosaccharomyces pombe. Mol Cell Biol. 2002; 22(23):8366-74. PMC: 134062. DOI: 10.1128/MCB.22.23.8366-8374.2002. View

11.

Ahmad K, Henikoff S . Histone H3 variants specify modes of chromatin assembly. Proc Natl Acad Sci U S A. 2002; 99 Suppl 4:16477-84. PMC: 139911. DOI: 10.1073/pnas.172403699. View

12.

Boeger H, Griesenbeck J, Strattan J, Kornberg R . Nucleosomes unfold completely at a transcriptionally active promoter. Mol Cell. 2003; 11(6):1587-98. DOI: 10.1016/s1097-2765(03)00231-4. View

13.

Reinke H, Horz W . Histones are first hyperacetylated and then lose contact with the activated PHO5 promoter. Mol Cell. 2003; 11(6):1599-607. DOI: 10.1016/s1097-2765(03)00186-2. View

14.

Krogan N, Keogh M, Datta N, Sawa C, Ryan O, Ding H . A Snf2 family ATPase complex required for recruitment of the histone H2A variant Htz1. Mol Cell. 2003; 12(6):1565-76. DOI: 10.1016/s1097-2765(03)00497-0. View

15.

Tagami H, Ray-Gallet D, Almouzni G, Nakatani Y . Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell. 2004; 116(1):51-61. DOI: 10.1016/s0092-8674(03)01064-x. View

16.

Mizuguchi G, Shen X, Landry J, Wu W, Sen S, Wu C . ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science. 2003; 303(5656):343-8. DOI: 10.1126/science.1090701. View

17.

Janicki S, Tsukamoto T, Salghetti S, Tansey W, Sachidanandam R, Prasanth K . From silencing to gene expression: real-time analysis in single cells. Cell. 2004; 116(5):683-98. PMC: 4942132. DOI: 10.1016/s0092-8674(04)00171-0. View

18.

Kobor M, Venkatasubrahmanyam S, Meneghini M, Gin J, Jennings J, Link A . A protein complex containing the conserved Swi2/Snf2-related ATPase Swr1p deposits histone variant H2A.Z into euchromatin. PLoS Biol. 2004; 2(5):E131. PMC: 374244. DOI: 10.1371/journal.pbio.0020131. View

19.

Lee C, Shibata Y, Rao B, Strahl B, Lieb J . Evidence for nucleosome depletion at active regulatory regions genome-wide. Nat Genet. 2004; 36(8):900-5. DOI: 10.1038/ng1400. View

20.

Kristjuhan A, Svejstrup J . Evidence for distinct mechanisms facilitating transcript elongation through chromatin in vivo. EMBO J. 2004; 23(21):4243-52. PMC: 524397. DOI: 10.1038/sj.emboj.7600433. View