Histone H3 lysine 14 acetylation is required for activation of a DNA damage checkpoint in fission yeast

Journal of Biological Chemistry

Volumn 287, Issue 6, 2012, Pages 4386-4393

  Wang, Yu ^a   Kallgren, Scott P ^a   Reddy, Bharat D ^a   Kuntz, Karen ^b   López Maury, Luis ^c   Thompson, James ^d   Watt, Stephen ^c   Chun, Ma ^e   Hou, Haitong ^a   Shi, Yang ^e,f,g   Yates III, John R ^d   Bähler, Jürg ^c   O'Connell, Matthew J ^b   Jia, Songtao ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

^e FUDAN UNIVERSITY   (China)

^f HARVARD MEDICAL SCHOOL   (United States)

^g BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL TRANSFERASE; CELLULAR FUNCTION; CHECKPOINT ACTIVATION; CHROMATIN REMODELING; DNA DAMAGES; FISSION YEAST; GENOME ORGANIZATION; GLOBAL LEVELS; HISTONE ACETYLTRANSFERASES; HISTONE DEACETYLASES; HISTONE H3; KEY REGULATORS; PROTEIN COMPLEXES; SCHIZOSACCHAROMYCES POMBE;

ACETYLATION; CHROMOSOMES;

AMINO ACIDS;

FUNGAL DNA; FUNGAL PROTEIN; HISTONE ACETYLTRANSFERASE; HISTONE ACETYLTRANSFERASE GCN5; HISTONE H3; LYSINE; PROTEIN MST2 COMPLEX; PROTEIN RSC; UNCLASSIFIED DRUG;

ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; DNA DAMAGE CHECKPOINT; ENZYME ACTIVITY; ENZYME INACTIVATION; GENE EXPRESSION PROFILING; GENE MUTATION; GENETIC REGULATION; HISTONE ACETYLATION; METABOLIC ACTIVATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEPLETION; PROTEIN PROTEIN INTERACTION; SCHIZOSACCHAROMYCES POMBE;

ACETYLATION; ACETYLTRANSFERASES; CHROMATIN; DNA DAMAGE; DNA, FUNGAL; HISTONES; MUTATION; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS;

SCHIZOSACCHAROMYCES POMBE; SCHIZOSACCHAROMYCETACEAE;

EID: 84863017224     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.329417     Document Type: Article

References (47)

1. Kouzarides, T. (2007) Chromatin modifications and their function. Cell 128, 693-705
2. Lee, K. K., and Workman, J. L. (2007) Histone acetyltransferase complexes. One size doesn't fit all. Nat. Rev. Mol. Cell Biol. 8, 284-295 (Pubitemid 46474661)
3. Shahbazian, M. D., and Grunstein, M. (2007) Functions of site-specific histone acetylation and deacetylation. Annu. Rev. Biochem. 76, 75-100
4. Sanchez, R., and Zhou, M. M. (2009) The role of human bromodomains in chromatin biology and gene transcription. Curr. Opin. Drug Discov. Devel. 12, 659-665
5. Shogren-Knaak, M., Ishii, H., Sun, J. M., Pazin, M. J., Davie, J. R., and Peterson, C. L. (2006) Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 311, 844-847 (Pubitemid 43228847)
6. Megee, P. C., Morgan, B. A., Mittman, B. A., and Smith, M. M. (1990) Genetic analysis of histone H4. Essential role of lysines subject to reversible acetylation. Science 247, 841-845
7. Park, E. C., and Szostak, J. W. (1990) Point mutations in the yeast histone H4 gene prevent silencing of the silent mating type locus HML. Mol. Cell Biol. 10, 4932-4934
8. Durrin, L. K., Mann, R. K., Kayne, P. S., and Grunstein, M. (1991) Yeast histone H4 N-terminal sequence is required for promoter activation in vivo. Cell 65, 1023-1031 (Pubitemid 121001690)
9. Megee, P. C., Morgan, B. A., and Smith, M. M. (1995) Histone H4 and the maintenance of genome integrity. Genes Dev. 9, 1716-1727
10. Dion, M. F., Altschuler, S. J., Wu, L. F., and Rando, O. J. (2005) Genomic characterization reveals a simple histone H4 acetylation code. Proc. Natl. Acad. Sci. U.S.A. 102, 5501-5506 (Pubitemid 40530287)
11. Schneider, J., Bajwa, P., Johnson, F. C., Bhaumik, S. R., and Shilatifard, A. (2006) Rtt109 is required for proper H3K56 acetylation. A chromatin mark associated with the elongating RNA polymerase II. J. Biol. Chem. 281, 37270-37274 (Pubitemid 46042030)
12. Collins, S. R., Miller, K. M., Maas, N. L., Roguev, A., Fillingham, J., Chu, C. S., Schuldiner, M., Gebbia, M., Recht, J., Shales, M., Ding, H., Xu, H., Han, J., Ingvarsdottir, K., Cheng, B., Andrews, B., Boone, C., Berger, S. L., Hieter, P., Zhang, Z., Brown, G. W., Ingles, C. J., Emili, A., Allis, C. D., Toczyski, D. P., Weissman, J. S., Greenblatt, J. F., and Krogan, N. J. (2007) Functional dissection of protein complexes involved in yeast chromosome biology using a genetic interaction map. Nature 446, 806-810 (Pubitemid 46582025)
13. Driscoll, R., Hudson, A., and Jackson, S. P. (2007) Yeast Rtt109 promotes genome stability by acetylating histone H3 on lysine 56. Science 315, 649-652 (Pubitemid 46214709)
14. Han, J., Zhou, H., Horazdovsky, B., Zhang, K., Xu, R. M., and Zhang, Z. (2007) Rtt109 acetylates histone H3 lysine 56 and functions in DNA replication. Science 315, 653-655 (Pubitemid 46214710)
15. Bähler, J., Wu, J. Q., Longtine, M. S., Shah, N. G., McKenzie, A., 3rd, Steever, A. B., Wach, A., Philippsen, P., and Pringle, J. R. (1998) Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 14, 943-951 (Pubitemid 28328000)
16. Wang, Y., Reddy, B., Thompson, J., Wang, H., Noma, K., Yates, J. R., 3rd, and Jia, S. (2009) Regulation of Set9-mediated H4K20 methylation by a PWWP domain protein. Mol. Cell 33, 428-437
17. Eberharter, A., John, S., Grant, P. A., Utley, R. T., and Workman, J. L. (1998) Identification and analysis of yeast nucleosomal histone acetyltransferase complexes. Methods 15, 315-321
18. Lopez-Girona, A., Tanaka, K., Chen, X. B., Baber, B. A., McGowan, C. H., and Russell, P. (2001) Serine-345 is required for Rad3-dependent phosphorylation and function of checkpoint kinase Chk1 in fission yeast. Proc. Natl. Acad. Sci. U.S.A. 98, 11289-11294 (Pubitemid 32928721)
19. Du, L. L., Nakamura, T. M., and Russell, P. (2006) Histone modificationdependent and -independent pathways for recruitment of checkpoint protein Crb2 to double-strand breaks. Genes Dev. 20, 1583-1596 (Pubitemid 43901098)
20. Pidoux, A., Mellone, B., and Allshire, R. (2004) Analysis of chromatin in fission yeast. Methods 33, 252-259 (Pubitemid 38648847)
21. Reddy, B. D., Wang, Y., Niu, L., Higuchi, E. C., Marguerat, S. B., Bähler, J., Smith, G. R., and Jia, S. (2011) Elimination of a specific histone H3K14 acetyltransferase complex bypasses the RNAi pathway to regulate pericentric heterochromatin functions. Genes Dev. 25, 214-219
22. Helmlinger, D., Marguerat, S., Villén, J., Gygi, S. P., Bähler, J., and Winston, F. (2008) The S. pombe SAGA complex controls the switch from proliferation to sexual differentiation through the opposing roles of its subunits Gcn5 and Spt8. Genes Dev. 22, 3184-3195
23. Gómez, E. B., Espinosa, J. M., and Forsburg, S. L. (2005) Schizosaccharomyces pombe mst2+ encodes a MYST family histone acetyltransferase that negatively regulates telomere silencing. Mol. Cell Biol. 25, 8887-8903 (Pubitemid 41429080)
24. Taverna, S. D., Ilin, S., Rogers, R. S., Tanny, J. C., Lavender, H., Li, H., Baker, L., Boyle, J., Blair, L. P., Chait, B. T., Patel, D. J., Aitchison, J. D., Tackett, A. J., and Allis, C. D. (2006) Yng1 PHD finger binding to H3 trimethylated at K4 promotes NuA3 HAT activity at K14 of H3 and transcription at a subset of targeted ORFs. Mol. Cell 24, 785-796 (Pubitemid 44839214)
25. Kuo, M. H., Brownell, J. E., Sobel, R. E., Ranalli, T. A., Cook, R. G., Edmondson, D. G., Roth, S. Y., and Allis, C. D. (1996) Transcription-linked acetylation by Gcn5p of histones H3 and H4 at specific lysines. Nature 383, 269-272 (Pubitemid 26317678)
26. Howe, L., Auston, D., Grant, P., John, S., Cook, R. G., Workman, J. L., and Pillus, L. (2001) Histone H3 specific acetyltransferases are essential for cell cycle progression. Genes Dev. 15, 3144-3154 (Pubitemid 33115678)
27. Nugent, R. L., Johnsson, A., Fleharty, B., Gogol, M., Xue-Franzén, Y., Seidel, C., Wright, A. P., and Forsburg, S. L. (2010) Expression profiling of S. pombe acetyltransferase mutants identifies redundant pathways of gene regulation. BMC Genomics 11, 59
28. Wirén, M., Silverstein, R. A., Sinha, I., Walfridsson, J., Lee, H. M., Laurenson, P., Pillus, L., Robyr, D., Grunstein, M., and Ekwall, K. (2005) Genomewide analysis of nucleosome density histone acetylation and HDAC function in fission yeast. EMBO J. 24, 2906-2918 (Pubitemid 43079894)
29. Mellone, B. G., Ball, L., Suka, N., Grunstein, M. R., Partridge, J. F., and Allshire, R. C. (2003) Centromere silencing and function in fission yeast is governed by the amino terminus of histone H3. Curr. Biol. 13, 1748-1757 (Pubitemid 37269116)
30. Jackson, S. P., and Bartek, J. (2009) The DNA-damage response in human biology and disease. Nature 461, 1071-1078
31. Kuntz, K., and O'Connell, M. J. (2009) The G(2)DNAdamage checkpoint. Could this ancient regulator be the Achilles heel of cancer? Cancer Biol. Ther. 8, 1433-1439
32. Tsutsui, Y., Khasanov, F. K., Shinagawa, H., Iwasaki, H., and Bashkirov, V. I. (2001) Multiple interactions among the components of the recombinational DNA repair system in Schizosaccharomyces pombe. Genetics 159, 91-105 (Pubitemid 32917362)
33. Kim, Y. C., Gerlitz, G., Furusawa, T., Catez, F., Nussenzweig, A., Oh, K. S., Kraemer, K. H., Shiloh, Y., and Bustin, M. (2009) Activation of ATM depends on chromatin interactions occurring before induction of DNA damage. Nat. Cell Biol. 11, 92-96
34. Kasten, M., Szerlong, H., Erdjument-Bromage, H., Tempst, P., Werner, M., and Cairns, B. R. (2004) Tandem bromodomains in the chromatin remodeler RSC recognize acetylated histone H3 Lys14. EMBO J. 23, 1348-1359 (Pubitemid 38525006)
35. Ferreira, H., Flaus, A., and Owen-Hughes, T. (2007) Histone modifications influence the action of Snf2 family remodelling enzymes by different mechanisms. J. Mol. Biol. 374, 563-579 (Pubitemid 350018763)
36. Liang, B., Qiu, J., Ratnakumar, K., and Laurent, B. C. (2007) RSC functions as an early double-strand-break sensor in the cell's response toDNAdamage. Curr. Biol. 17, 1432-1437 (Pubitemid 47259384)
37. Shim, E. Y., Hong, S. J., Oum, J. H., Yanez, Y., Zhang, Y., and Lee, S. E. (2007) RSC mobilizes nucleosomes to improve accessibility of repair machinery to the damaged chromatin. Mol. Cell. Biol. 27, 1602-1613
38. Monahan, B. J., Villén, J., Marguerat, S., Bähler, J., Gygi, S. P., and Winston, F. (2008) Fission yeast SWI/SNF and RSC complexes show compositional and functional differences from budding yeast. Nat. Struct. Mol. Biol. 15, 873-880
39. Pokholok, D. K., Harbison, C. T., Levine, S., Cole, M., Hannett, N. M., Lee, T. I., Bell, G. W., Walker, K., Rolfe, P. A., Herbolsheimer, E., Zeitlinger, J., Lewitter, F., Gifford, D. K., and Young, R. A. (2005) Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 122, 517-527 (Pubitemid 41191151)
40. Wang, Z., Zang, C., Rosenfeld, J. A., Schones, D. E., Barski, A., Cuddapah, S., Cui, K., Roh, T. Y., Peng, W., Zhang, M. Q., and Zhao, K. (2008) Combinatorial patterns of histone acetylations and methylations in the human genome. Nat. Genet. 40, 897-903 (Pubitemid 351913645)
41. John, S., Howe, L., Tafrov, S. T., Grant, P. A., Sternglanz, R., and Workman, J. L. (2000) The something about silencing protein, Sas3, is the catalytic subunit of NuA3, a yTAF(II)30-containing HAT complex that interacts with the Spt16 subunit of the yeast CP (Cdc68/Pob3)-FACT complex. Genes Dev. 14, 1196-1208 (Pubitemid 30327501)
42. Howe, L., Kusch, T., Muster, N., Chaterji, R., Yates, J. R., 3rd, and Workman, J. L. (2002) Yng1p modulates the activity of Sas3p as a component of the yeast NuA3 histone acetyltransferase complex. Mol. Cell Biol. 22, 5047-5053 (Pubitemid 34700696)
43. Krogan, N. J., Cagney, G., Yu, H., Zhong, G., Guo, X., Ignatchenko, A., Li, J., Pu, S., Datta, N., Tikuisis, A. P., Punna, T., Peregrín-Alvarez, J. M., Shales, M., Zhang, X., Davey, M., Robinson, M. D., Paccanaro, A., Bray, J. E., Sheung, A., Beattie, B., Richards, D. P., Canadien, V., Lalev, A., Mena, F., Wong, P., Starostine, A., Canete, M. M., Vlasblom, J., Wu, S., Orsi, C., Collins, S. R., Chandran, S., Haw, R., Rilstone, J. J., Gandi, K., Thompson, N. J., Musso, G., St. Onge, P., Ghanny, S., Lam, M. H., Butland, G., Altaf-Ul, A. M., Kanaya, S., Shilatifard, A., O'Shea, E., Weissman, J. S., Ingles, C. J., Hughes, T. R., Parkinson, J., Gerstein, M., Wodak, S. J., Emili, A., and Greenblatt, J. F. (2006) Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 440, 637-643
44. Martin, D. G., Baetz, K., Shi, X., Walter, K. L., MacDonald, V. E., Wlodarski, M. J., Gozani, O., Hieter, P., and Howe, L. (2006) The Yng1p plant homeodomain finger is a methyl-histone binding module that recognizes lysine 4-methylated histone H3. Mol. Cell Biol. 26, 7871-7879 (Pubitemid 44630988)
45. Nakanishi, S., Sanderson, B. W., Delventhal, K. M., Bradford, W. D., Staehling-Hampton, K., and Shilatifard, A. (2008) A comprehensive library of histone mutants identifies nucleosomal residues required for H3K4 methylation. Nat. Struct. Mol. Biol. 15, 881-888
46. Vermeulen, M., Eberl, H. C., Matarese, F., Marks, H., Denissov, S., Butter, F., Lee, K. K., Olsen, J. V., Hyman, A. A., Stunnenberg, H. G., and Mann, M. (2010) Quantitative interaction proteomics and genome-wide profiling of epigenetic histone marks and their readers. Cell 142, 967-980
47. Dai, J., Hyland, E. M., Yuan, D. S., Huang, H., Bader, J. S., and Boeke, J. D. (2008) Probing nucleosome function. A highly versatile library of synthetic histone H3 and H4 mutants. Cell 134, 1066-1078