Histone H4 lysine 12 acetylation regulates telomeric heterochromatin plasticity in saccharomyces cerevisiae

PLoS Genetics

Volumn 7, Issue 1, 2011, Pages

  Zhou, Bo O ^a   Wang, Shan Shan ^a   Zhang, Yang ^a   Fu, Xiao Hong ^a   Dang, Wei ^a   Lenzmeier, Brian A ^b   Zhou, Jin Qiu ^a  

^a INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^b BUENA VISTA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE ACETYLTRANSFERASE; HISTONE ACETYLTRANSFERASE COMPLEX NUA4; HISTONE H4; HISTONE H4 LYSINE 12; SILENT INFORMATION REGULATOR PROTEIN; TELOMERASE; UNCLASSIFIED DRUG; ESA1 PROTEIN, S CEREVISIAE; HISTONE; LYSINE; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CHROMOSOME REPLICATION; CONTROLLED STUDY; DNA METABOLISM; GENETIC RECOMBINATION; GENETIC TRANSCRIPTION; HETEROCHROMATIN; HISTONE ACETYLATION; NONHUMAN; PLASTICITY; SACCHAROMYCES CEREVISIAE; TELOMERE; YEAST CELL; ACETYLATION; DNA REPLICATION; GENETICS; METABOLISM;

SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES;

ACETYLATION; DNA REPLICATION; HETEROCHROMATIN; HISTONE ACETYLTRANSFERASES; HISTONES; LYSINE; RECOMBINATION, GENETIC; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TELOMERASE; TELOMERE; TRANSCRIPTION, GENETIC;

EID: 79851496150     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1001272     Document Type: Article

References (62)

1. Rusche LN, Kirchmaier AL, Rine J (2003) The establishment, inheritance, and function of silenced chromatin in Saccharomyces cerevisiae. Annu Rev Biochem 72: 481-516.
2. Luo K, Vega-Palas MA, Grunstein M (2002) Rap1-Sir4 binding independent of other Sir, yKu, or histone interactions initiates the assembly of telomeric heterochromatin in yeast. Genes Dev 16: 1528-1539.
3. Imai S, Armstrong CM, Kaeberlein M, Guarente L (2000) Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature 403: 795-800.
4. Hecht A, Laroche T, Strahl-Bolsinger S, Gasser SM, Grunstein M (1995) Histone H3 and H4 N-termini interact with SIR3 and SIR4 proteins: a molecular model for the formation of heterochromatin in yeast. Cell 80: 583-592.
5. Carmen AA, Milne L, Grunstein M (2002) Acetylation of the yeast histone H4 N terminus regulates its binding to heterochromatin protein SIR3. J Biol Chem 277: 4778-4781.
6. Kimura A, Umehara T, Horikoshi M (2002) Chromosomal gradient of histone acetylation established by Sas2p and Sir2p functions as a shield against gene silencing. Nat Genet 32: 370-377.
7. Suka N, Luo K, Grunstein M (2002) Sir2p and Sas2p opposingly regulate acetylation of yeast histone H4 lysine16 and spreading of heterochromatin. Nat Genet 32: 378-383.
8. Katan-Khaykovich Y, Struhl K (2005) Heterochromatin formation involves changes in histone modifications over multiple cell generations. Embo J 24: 2138-2149.
9. Bi X, Broach JR (2001) Chromosomal boundaries in S. cerevisiae. Curr Opin Genet Dev 11: 199-204.
10. Smith ER, Eisen A, Gu W, Sattah M, Pannuti A, et al. (1998) ESA1 is a histone acetyltransferase that is essential for growth in yeast. Proc Natl Acad Sci U S A 95: 3561-3565.
11. Cheng TH, Gartenberg MR (2000) Yeast heterochromatin is a dynamic structure that requires silencers continuously. Genes Dev 14: 452-463.
12. Sekinger EA, Gross DS (2001) Silenced chromatin is permissive to activator binding and PIC recruitment. Cell 105: 403-414.
13. Chen L, Widom J (2005) Mechanism of transcriptional silencing in yeast. Cell 120: 37-48.
14. Andrau JC, van de Pasch L, Lijnzaad P, Bijma T, Koerkamp MG, et al. (2006) Genome-wide location of the coactivator mediator: Binding without activation and transient Cdk8 interaction on DNA. Mol Cell 22: 179-192.
15. Teytelman L, Eisen MB, Rine J (2008) Silent but not static: accelerated base-pair substitution in silenced chromatin of budding yeasts. PLoS Genet 4: e1000247 doi:10.1371/journal.pgen.1000247.
16. Diede SJ, Gottschling DE (1999) Telomerase-mediated telomere addition in vivo requires DNA primase and DNA polymerases alpha and delta. Cell 99: 723-733.
17. Tamburini BA, Tyler JK (2005) Localized histone acetylation and deacetylation triggered by the homologous recombination pathway of double-strand DNA repair. Mol Cell Biol 25: 4903-4913.
18. Meneghini MD, Wu M, Madhani HD (2003) Conserved histone variant H2A.Z protects euchromatin from the ectopic spread of silent heterochromatin. Cell 112: 725-736.
19. Zhou BO, Wang SS, Xu LX, Meng FL, Xuan YJ, et al. (2010) SWR1 complex poises heterochromatin boundaries for antisilencing activity propagation. Mol Cell Biol 30: 2391-2400.
20. Suka N, Suka Y, Carmen AA, Wu J, Grunstein M (2001) Highly specific antibodies determine histone acetylation site usage in yeast heterochromatin and euchromatin. Mol Cell 8: 473-479.
21. Negrini S, Ribaud V, Bianchi A, Shore D (2007) DNA breaks are masked by multiple Rap1 binding in yeast: implications for telomere capping and telomerase regulation. Genes Dev 21: 292-302.
22. Zhu X, Gustafsson CM (2009) Distinct differences in chromatin structure at subtelomeric X and Y' elements in budding yeast. PLoS ONE 4: e6363 doi:10.1371/journal.pone.0006363.
23. Boudreault AA, Cronier D, Selleck W, Lacoste N, Utley RT, et al. (2003) Yeast enhancer of polycomb defines global Esa1-dependent acetylation of chromatin. Genes Dev 17: 1415-1428.
24. Kleff S, Andrulis ED, Anderson CW, Sternglanz R (1995) Identification of a gene encoding a yeast histone H4 acetyltransferase. J Biol Chem 270: 24674-24677.
25. Ruiz-Garcia AB, Sendra R, Galiana M, Pamblanco M, Perez-Ortin JE, et al. (1998) HAT1 and HAT2 proteins are components of a yeast nuclear histone acetyltransferase enzyme specific for free histone H4. J Biol Chem 273: 12599-12605.
26. Shahbazian MD, Grunstein M (2007) Functions of site-specific histone acetylation and deacetylation. Annu Rev Biochem 76: 75-100.
27. Vega-Palas MA, Venditti S, Di Mauro E (1998) Heterochromatin organization of a natural yeast telomere. Changes of nucleosome distribution driven by the absence of Sir3p. J Biol Chem 273: 9388-9392.
28. Palladino F, Laroche T, Gilson E, Axelrod A, Pillus L, et al. (1993) SIR3 and SIR4 proteins are required for the positioning and integrity of yeast telomeres. Cell 75: 543-555.
29. Wright JH, Gottschling DE, Zakian VA (1992) Saccharomyces telomeres assume a non-nucleosomal chromatin structure. Genes Dev 6: 197-210.
30. Schober H, Ferreira H, Kalck V, Gehlen LR, Gasser SM (2009) Yeast telomerase and the SUN domain protein Mps3 anchor telomeres and repress subtelomeric recombination. Genes Dev 23: 928-938.
31. de Bruin D, Kantrow SM, Liberatore RA, Zakian VA (2000) Telomere folding is required for the stable maintenance of telomere position effects in yeast. Mol Cell Biol 20: 7991-8000.
32. Strahl-Bolsinger S, Hecht A, Luo K, Grunstein M (1997) SIR2 and SIR4 interactions differ in core and extended telomeric heterochromatin in yeast. Genes Dev 11: 83-93.
33. de Bruin D, Zaman Z, Liberatore RA, Ptashne M (2001) Telomere looping permits gene activation by a downstream UAS in yeast. Nature 409: 109-113.
34. Dion MF, Altschuler SJ, Wu LF, Rando OJ (2005) Genomic characterization reveals a simple histone H4 acetylation code. Proc Natl Acad Sci U S A 102: 5501-5506.
35. Grandin N, Charbonneau M (2007) Control of the yeast telomeric senescence survival pathways of recombination by the Mec1 and Mec3 DNA damage sensors and RPA. Nucleic Acids Res 35: 822-838.
36. Smith CM, Haimberger ZW, Johnson CO, Wolf AJ, Gafken PR, et al. (2002) Heritable chromatin structure: mapping "memory" in histones H3 and H4. Proc Natl Acad Sci U S A 99 (Suppl 4): 16454-16461.
37. Gottschling DE, Aparicio OM, Billington BL, Zakian VA (1990) Position effect at S. cerevisiae telomeres: reversible repression of Pol II transcription. Cell 63: 751-762.
38. Meijsing SH, Ehrenhofer-Murray AE (2001) The silencing complex SAS-I links histone acetylation to the assembly of repressed chromatin by CAF-I and Asf1 in Saccharomyces cerevisiae. Genes Dev 15: 3169-3182.
39. Li YC, Cheng TH, Gartenberg MR (2001) Establishment of transcriptional silencing in the absence of DNA replication. Science 291: 650-653.
40. Kirchmaier AL, Rine J (2001) DNA replication-independent silencing in S. cerevisiae. Science 291: 646-650.
41. Hoppe GJ, Tanny JC, Rudner AD, Gerber SA, Danaie S, et al. (2002) Steps in assembly of silent chromatin in yeast: Sir3-independent binding of a Sir2/Sir4 complex to silencers and role for Sir2-dependent deacetylation. Mol Cell Biol 22: 4167-4180.
42. Braunstein M, Sobel RE, Allis CD, Turner BM, Broach JR (1996) Efficient transcriptional silencing in Saccharomyces cerevisiae requires a heterochromatin histone acetylation pattern. Mol Cell Biol 16: 4349-4356.
43. Ogiwara H, Ui A, Kawashima S, Kugou K, Onoda F, et al. (2007) Actin-related protein Arp4 functions in kinetochore assembly. Nucleic Acids Res 35: 3109-3117.
44. Bird AW, Yu DY, Pray-Grant MG, Qiu Q, Harmon KE, et al. (2002) Acetylation of histone H4 by Esa1 is required for DNA double-strand break repair. Nature 419: 411-415.
45. Reid JL, Iyer VR, Brown PO, Struhl K (2000) Coordinate regulation of yeast ribosomal protein genes is associated with targeted recruitment of Esa1 histone acetylase. Mol Cell 6: 1297-1307.
46. Chang CS, Pillus L (2009) Collaboration between the essential Esa1 acetyltransferase and the Rpd3 deacetylase is mediated by H4K12 histone acetylation in Saccharomyces cerevisiae. Genetics 183: 149-160.
47. Rundlett SE, Carmen AA, Kobayashi R, Bavykin S, Turner BM, et al. (1996) HDA1 and RPD3 are members of distinct yeast histone deacetylase complexes that regulate silencing and transcription. Proc Natl Acad Sci U S A 93: 14503-14508.
48. Zhou J, Zhou BO, Lenzmeier BA, Zhou JQ (2009) Histone deacetylase Rpd3 antagonizes Sir2-dependent silent chromatin propagation. Nucleic Acids Res 37: 3699-3713.
49. Smith CM, Gafken PR, Zhang Z, Gottschling DE, Smith JB, et al. (2003) Mass spectrometric quantification of acetylation at specific lysines within the amino-terminal tail of histone H4. Anal Biochem 316: 23-33.
50. Babiarz JE, Halley JE, Rine J (2006) Telomeric heterochromatin boundaries require NuA4-dependent acetylation of histone variant H2A.Z in Saccharomyces cerevisiae. Genes Dev 20: 700-710.
51. Chiu YH, Yu Q, Sandmeier JJ, Bi X (2003) A targeted histone acetyltransferase can create a sizable region of hyperacetylated chromatin and counteract the propagation of transcriptionally silent chromatin. Genetics 165: 115-125.
52. Altaf M, Auger A, Monnet-Saksouk J, Brodeur J, Piquet S, et al. (2010) NuA4-dependent acetylation of nucleosomal histones H4 and H2A directly stimulates incorporation of H2A.Z by the SWR1 complex. J Biol Chem 285: 15966-15977.
53. Clarke AS, Samal E, Pillus L (2006) Distinct roles for the essential MYST family HAT Esa1p in transcriptional silencing. Mol Biol Cell 17: 1744-1757.
54. Auger A, Galarneau L, Altaf M, Nourani A, Doyon Y, et al. (2008) Eaf1 is the platform for NuA4 molecular assembly that evolutionarily links chromatin acetylation to ATP-dependent exchange of histone H2A variants. Mol Cell Biol 28: 2257-2270.
55. Blasco MA (2007) The epigenetic regulation of mammalian telomeres. Nat Rev Genet 8: 299-309.
56. Yu EY, Steinberg-Neifach O, Dandjinou AT, Kang F, Morrison AJ, et al. (2007) Regulation of telomere structure and functions by subunits of the INO80 chromatin remodeling complex. Mol Cell Biol 27: 5639-5649.
57. Kozak ML, Chavez A, Dang W, Berger SL, Ashok A, et al. (2010) Inactivation of the Sas2 histone acetyltransferase delays senescence driven by telomere dysfunction. Embo J 29: 158-170.
58. Turner BM, Birley AJ, Lavender J (1992) Histone H4 isoforms acetylated at specific lysine residues define individual chromosomes and chromatin domains in Drosophila polytene nuclei. Cell 69: 375-384.
59. Xhemalce B, Kouzarides T (2010) A chromodomain switch mediated by histone H3 Lys 4 acetylation regulates heterochromatin assembly. Genes Dev 24: 647-652.
60. Yamagata K, Kitabayashi I (2009) Sirt1 physically interacts with Tip60 and negatively regulates Tip60-mediated acetylation of H2AX. Biochem Biophys Res Commun 390: 1355-1360.
61. Sun Y, Jiang X, Xu Y, Ayrapetov MK, Moreau LA, et al. (2009) Histone H3 methylation links DNA damage detection to activation of the tumour suppressor Tip60. Nat Cell Biol 11: 1376-1382.
62. Meng FL, Hu Y, Shen N, Tong XJ, Wang J, et al. (2009) Sua5p a single-stranded telomeric DNA-binding protein facilitates telomere replication. Embo J 28: 1466-1478.