Histone H3 Lysine 56 Methylation Regulates DNA Replication through Its Interaction with PCNA

Molecular Cell

Volumn 46, Issue 1, 2012, Pages 7-17

  Yu, Yongxin ^a   Song, Chunying ^a   Zhang, Qiongyi ^a   DiMaggio, Peter A ^b   Garcia, Benjamin A ^b   York, Autumn ^a   Carey, Michael F ^a   Grunstein, Michael ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLINE; DNA; HISTONE H3; HISTONE H3 LYSINE 56; LYSINE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ACETYLATION; ANIMAL CELL; ARTICLE; CELL CYCLE; CHROMATIN; CONTROLLED STUDY; DNA REPAIR; DNA REPLICATION; DNA SUPERCOILING; FEMALE; HETEROCHROMATIN; HISTONE METHYLATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MAMMAL CELL; MOUSE; NONHUMAN;

DNA REPLICATION; G1 PHASE; HEK293 CELLS; HELA CELLS; HISTONES; HUMANS; LYSINE; METHYLATION; NUCLEOSOMES; PROLIFERATING CELL NUCLEAR ANTIGEN; PROTEIN PROCESSING, POST-TRANSLATIONAL;

MAMMALIA;

EID: 84862777220     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2012.01.019     Document Type: Article

References (42)

1. Branzei D., Foiani M. Maintaining genome stability at the replication fork. Nat. Rev. Mol. Cell Biol. 2010, 11:208-219.
2. Das C., Lucia M.S., Hansen K.C., Tyler J.K. CBP/p300-mediated acetylation of histone H3 on lysine 56. Nature 2009, 459:113-117.
3. Eickbush T.H., Moudrianakis E.N. The histone core complex: an octamer assembled by two sets of protein-protein interactions. Biochemistry 1978, 17:4955-4964.
4. Estève P.O., Chin H.G., Smallwood A., Feehery G.R., Gangisetty O., Karpf A.R., Carey M.F., Pradhan S. Direct interaction between DNMT1 and G9a coordinates DNA and histone methylation during replication. Genes Dev. 2006, 20:3089-3103.
5. Feser J., Truong D., Das C., Carson J.J., Kieft J., Harkness T., Tyler J.K. Elevated histone expression promotes life span extension. Mol. Cell 2010, 39:724-735.
6. Garcia B.A., Hake S.B., Diaz R.L., Kauer M., Morris S.A., Recht J., Shabanowitz J., Mishra N., Strahl B.D., Allis C.D., Hunt D.F. Organismal differences in post-translational modifications in histones H3 and H4. J. Biol. Chem. 2007, 282:7641-7655.
7. Greenberg J.I., Shields D.J., Barillas S.G., Acevedo L.M., Murphy E., Huang J., Scheppke L., Stockmann C., Johnson R.S., Angle N., Cheresh D.A. A role for VEGF as a negative regulator of pericyte function and vessel maturation. Nature 2008, 456:809-813.
8. Groth A., Corpet A., Cook A.J., Roche D., Bartek J., Lukas J., Almouzni G. Regulation of replication fork progression through histone supply and demand. Science 2007, 318:1928-1931.
9. Han J., Zhou H., Horazdovsky B., Zhang K., Xu R.M., Zhang Z. Rtt109 acetylates histone H3 lysine 56 and functions in DNA replication. Science 2007, 315:653-655.
10. Hartwell L.H. Cell division from a genetic perspective. J. Cell Biol. 1978, 77:627-637.
11. Huang J., Berger S.L. The emerging field of dynamic lysine methylation of non-histone proteins. Curr. Opin. Genet. Dev. 2008, 18:152-158.
12. Kouzarides T. Chromatin modifications and their function. Cell 2007, 128:693-705.
13. Kurki P., Vanderlaan M., Dolbeare F., Gray J., Tan E.M. Expression of proliferating cell nuclear antigen (PCNA)/cyclin during the cell cycle. Exp. Cell Res. 1986, 166:209-219.
14. Lee M.G., Wynder C., Cooch N., Shiekhattar R. An essential role for CoREST in nucleosomal histone 3 lysine 4 demethylation. Nature 2005, 437:432-435.
15. Li Q., Zhou H., Wurtele H., Davies B., Horazdovsky B., Verreault A., Zhang Z. Acetylation of histone H3 lysine 56 regulates replication-coupled nucleosome assembly. Cell 2008, 134:244-255.
16. Luger K., Mäder A.W., Richmond R.K., Sargent D.F., Richmond T.J. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 1997, 389:251-260.
17. Masumoto H., Hawke D., Kobayashi R., Verreault A. A role for cell-cycle-regulated histone H3 lysine 56 acetylation in the DNA damage response. Nature 2005, 436:294-298.
18. Moldovan G.L., Pfander B., Jentsch S. PCNA, the maestro of the replication fork. Cell 2007, 129:665-679.
19. Mukherjee P., Cao T.V., Winter S.L., Alexandrow M.G. Mammalian MCM loading in late-G(1) coincides with Rb hyperphosphorylation and the transition to post-transcriptional control of progression into S-phase. PLoS ONE 2009, 4:e5462.
20. Peters A.H., Kubicek S., Mechtler K., O'Sullivan R.J., Derijck A.A., Perez-Burgos L., Kohlmaier A., Opravil S., Tachibana M., Shinkai Y., et al. Partitioning and plasticity of repressive histone methylation states in mammalian chromatin. Mol. Cell 2003, 12:1577-1589.
21. Plazas-Mayorca M.D., Zee B.M., Young N.L., Fingerman I.M., LeRoy G., Briggs S.D., Garcia B.A. One-pot shotgun quantitative mass spectrometry characterization of histones. J. Proteome Res. 2009, 8:5367-5374.
22. Pringle J.R. The use of conditional lethal cell cycle mutants for temporal and functional sequence mapping of cell cycle events. J. Cell. Physiol. 1978, 95:393-405.
23. Rathert P., Dhayalan A., Murakami M., Zhang X., Tamas R., Jurkowska R., Komatsu Y., Shinkai Y., Cheng X., Jeltsch A. Protein lysine methyltransferase G9a acts on non-histone targets. Nat. Chem. Biol. 2008, 4:344-346.
24. Rice J.C., Briggs S.D., Ueberheide B., Barber C.M., Shabanowitz J., Hunt D.F., Shinkai Y., Allis C.D. Histone methyltransferases direct different degrees of methylation to define distinct chromatin domains. Mol. Cell 2003, 12:1591-1598.
25. Sclafani R.A., Holzen T.M. Cell cycle regulation of DNA replication. Annu. Rev. Genet. 2007, 41:237-280.
26. Shi Y.J., Matson C., Lan F., Iwase S., Baba T., Shi Y. Regulation of LSD1 histone demethylase activity by its associated factors. Mol. Cell 2005, 19:857-864.
27. Smits V.A., Warmerdam D.O., Martin Y., Freire R. Mechanisms of ATR-mediated checkpoint signalling. Front. Biosci. 2010, 15:840-853.
28. Söderberg O., Gullberg M., Jarvius M., Ridderstråle K., Leuchowius K.J., Jarvius J., Wester K., Hydbring P., Bahram F., Larsson L.G., Landegren U. Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat. Methods 2006, 3:995-1000.
29. Tachibana M., Sugimoto K., Fukushima T., Shinkai Y. Set domain-containing protein, G9a, is a novel lysine-preferring mammalian histone methyltransferase with hyperactivity and specific selectivity to lysines 9 and 27 of histone H3. J. Biol. Chem. 2001, 276:25309-25317.
30. Tachibana M., Sugimoto K., Nozaki M., Ueda J., Ohta T., Ohki M., Fukuda M., Takeda N., Niida H., Kato H., Shinkai Y. G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis. Genes Dev. 2002, 16:1779-1791.
31. Tachibana M., Ueda J., Fukuda M., Takeda N., Ohta T., Iwanari H., Sakihama T., Kodama T., Hamakubo T., Shinkai Y. Histone methyltransferases G9a and GLP form heteromeric complexes and are both crucial for methylation of euchromatin at H3-K9. Genes Dev. 2005, 19:815-826.
32. 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, 116:51-61.
33. Tjeertes J.V., Miller K.M., Jackson S.P. Screen for DNA-damage-responsive histone modifications identifies H3K9Ac and H3K56Ac in human cells. EMBO J. 2009, 28:1878-1889.
34. Trojer P., Zhang J., Yonezawa M., Schmidt A., Zheng H., Jenuwein T., Reinberg D. Dynamic Histone H1 Isotype 4 Methylation and Demethylation by Histone Lysine Methyltransferase G9a/KMT1C and the Jumonji Domain-containing JMJD2/KDM4 Proteins. J. Biol. Chem. 2009, 284:8395-8405.
35. Waga S., Stillman B. The DNA replication fork in eukaryotic cells. Annu. Rev. Biochem. 1998, 67:721-751.
36. Weiss T., Hergeth S., Zeissler U., Izzo A., Tropberger P., Zee B.M., Dundr M., Garcia B.A., Daujat S., Schneider R. Histone H1 variant-specific lysine methylation by G9a/KMT1C and Glp1/KMT1D. Epigenetics Chromatin 2010, 3:7.
37. Williams S.K., Truong D., 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 2008, 105:9000-9005.
38. Xie W., Song C., Young N.L., Sperling A.S., Xu F., Sridharan R., Conway A.E., Garcia B.A., Plath K., Clark A.T., Grunstein M. Histone h3 lysine 56 acetylation is linked to the core transcriptional network in human embryonic stem cells. Mol. Cell 2009, 33:417-427.
39. Xu F., Zhang K., Grunstein M. Acetylation in histone H3 globular domain regulates gene expression in yeast. Cell 2005, 121:375-385.
40. Xu F., Zhang Q., Zhang K., Xie W., Grunstein M. Sir2 deacetylates histone H3 lysine 56 to regulate telomeric heterochromatin structure in yeast. Mol. Cell 2007, 27:890-900.
41. Yuan J., Pu M., Zhang Z., Lou Z. Histone H3-K56 acetylation is important for genomic stability in mammals. Cell Cycle 2009, 8:1747-1753.
42. Zhu P., Tan M.J., Huang R.L., Tan C.K., Chong H.C., Pal M., Lam C.R., Boukamp P., Pan J.Y., Tan S.H., et al. Angiopoietin-like 4 protein elevates the prosurvival intracellular O2(-):H2O2 ratio and confers anoikis resistance to tumors. Cancer Cell 2011, 19:401-415.