Histone H3 lysine 56 acetylation by Rtt109 is crucial for chromosome positioning

Journal of Cell Biology

Volumn 183, Issue 4, 2008, Pages 641-651

  Hiraga, Shin Ichiro ^a   Botsios, Sotirios ^a   Donaldson, Anne D ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; HISTONE; HISTONE ACETYLTRANSFERASE; HISTONE ACETYLTRANSFERASE RTT109; HISTONE CHAPERONE ASF1; HISTONE H3; HISTONE H3 K56; LYSINE DERIVATIVE; UNCLASSIFIED DRUG; ASF1 PROTEIN, S CEREVISIAE; CELL CYCLE PROTEIN; CHAPERONE; RTT109 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN;

ACETYLATION; ARTICLE; CELL CYCLE S PHASE; CHROMATIN; CHROMOSOME POSITIONING; DEACETYLATION; DNA REPLICATION; EPIGENETICS; FUNGUS MUTANT; INHERITANCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; SACCHAROMYCES CEREVISIAE; TELOMERE; CELL NUCLEUS; CHROMOSOME; FUNGAL GENOME; GENETICS; METABOLISM; PHYSIOLOGY;

SACCHAROMYCES CEREVISIAE;

ACETYLATION; CELL CYCLE PROTEINS; CELL NUCLEUS; CHROMOSOME POSITIONING; CHROMOSOMES, FUNGAL; GENOME, FUNGAL; HISTONE ACETYLTRANSFERASES; HISTONES; MOLECULAR CHAPERONES; S PHASE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TELOMERE;

EID: 58149183980     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200806065     Document Type: Article

References (67)

1. Annunziato, A.T. 2005. Split decision: what happens to nucleosomes during DNA replication? J. Biol. Chem. 280:12065-12068.
2. Annunziato, A.T., and R.L. Seale . 1983 . Histone deacetylation is required for the maturation of newly replicated chromatin. J. Biol. Chem. 258:12675-12684.
3. Askree, S.H., T. Yehuda, S. Smolikov, R. Gurevich, J. Hawk, C. Coker, A. Krauskopf, M. Kupiec, and M.J. McEachern. 2004. A genome-wide screen for Saccharomyces cerevisiae deletion mutants that affect telomere length. Proc. Natl. Acad. Sci. USA. 101:8658-8663.
4. Belgareh , N. , and V. Doye . 1997 . Dynamics of nuclear pore distribution in nucleoporin mutant yeast cells. J. Cell Biol. 136:747-759.
5. Brickner , J.H., and P. Walter . 2004. Gene recruitment of the activated INO1 locus to the nuclear membrane. PLoS Biol. 2:e342.
6. Bupp, J.M., A.E. Martin, E.S. Stensrud, and S.L. Jaspersen. 2007. Telomere anchoring at the nuclear periphery requires the budding yeast Sad1-UNC-84 domain protein Mps3. J. Cell Biol. 179:845-854.
7. Bystricky, K., T. Laroche, G. van Houwe, M. Blaszczyk, and S.M. Gasser. 2005. Chromosome looping in yeast: telomere pairing and coordinated movement ref ect anchoring eff ciency and territorial organization. J. Cell Biol. 168:375-387.
8. Casolari, J.M., C.R. Brown, S. Komili, J. West, H. Hieronymus, and P.A. Silver. 2004 . Genome-wide localization of the nuclear transport machinery couples transcriptional status and nuclear organization. Cell. 117:427-439.
9. Celic, I., H. Masumoto, W. Griffth, P. Meluh, R. Cotter, J. Boeke, and A. Verreault. 2006 . The sirtuins hst3 and Hst4p preserve genome integrity by controlling histone h3 lysine 56 deacetylation. Curr. Biol. 16:1280-1289.
10. Chambeyron, S., and W.A. Bickmore. 2004. Chromatin decondensation and nuclear reorganization of the HoxB locus upon induction of transcription. Genes Dev. 18:1119-1130.
11. Connolly, B., C.I. White, and J.E. Haber. 1988. Physical monitoring of mating type switching in Saccharomyces cerevisiae. Mol. Cell. Biol. 8:2342-2349.
12. Cosgrove, A.J., C.A. Nieduszynski, and A.D. Donaldson. 2002. Ku complex controls the replication time of DNA in telomere regions. Genes Dev. 16:2485-2490.
13. Driscoll , R. , A. Hudson , and S.P. Jackson. 2007. Yeast Rtt109 promotes genome stability by acetylating histone H3 on lysine 56. Science. 315:649-652.
14. Ebrahimi, H., and A.D. Donaldson. 2008. Release of yeast telomeres from the nuclear periphery is triggered by replication and maintained by suppression of Ku-mediated anchoring. Genes Dev. In press.
15. Franco, A.A., W.M. Lam, P.M. Burgers, and P.D. Kaufman. 2005. Histone deposition protein Asf1 maintains DNA replisome integrity and interacts with replication factor C. Genes Dev. 19:1365-1375.
16. Gartenberg, M.R., F.R. Neumann, T. Laroche, M. Blaszczyk, and S.M. Gasser. 2004 . Sir-mediated repression can occur independently of chromosomal and subnuclear contexts. Cell. 119:955-967.
17. Gasser, S.M. 2002. Visualizing chromatin dynamics in interphase nuclei. Science. 296:1412-1416.
18. Gatbonton, T., M. Imbesi, M. Nelson, J.M. Akey, D.M. Ruderfer, L. Kruglyak, J.A. Simon, and A. Bedalov. 2006. Telomere length as a quantitative trait: genome-wide survey and genetic mapping of telomere length-control genes in yeast. PLoS Genet. 2:e35.
19. Giaever, G., A.M. Chu, L. Ni, C. Connelly, L. Riles, S. Veronneau, S. Dow , A. Lucau-Danila, K.Anderson, B.Andre, et al. 2002. Functional prof ling of the Saccharomyces cerevisiae genome. Nature. 418:387-391.
20. Gietz, R.D., and A. Sugino. 1988. New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene. 74:527-534.
21. Goldstein, A.L., and J.H. McCusker. 1999. Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast. 15:1541-1553.
22. Gotta, M., T. Laroche, A. Formenton, L. Maillet, H. Scherthan, and S.M. Gasser. 1996 . The clustering of telomeres and colocalization with Rap1, Sir3, and Sir4 proteins in wild-type Saccharomyces cerevisiae. J. Cell Biol. 134:1349-1363.
23. Gottschling, D.E. 1992. Telomere-proximal DNA in Saccharomyces cerevisiae is refractory to methyltransferase activity in vivo . Proc. Natl. Acad. Sci. USA. 89:4062-4065.
24. Gottschling, D.E., O.M. Aparicio, B.L. Billington, and V.A. Zakian. 1990. Position effect at S. cerevisiae telomeres: reversible repression of Pol II transcription. Cell. 63:751-762.
25. Han, J., H. Zhou, B. Horazdovsky, K. Zhang, R.M. Xu, and Z. Zhang. 2007a. Rtt109 acetylates histone H3 lysine 56 and functions in DNA replication. Science. 315:653-655.
26. Han, J., H. Zhou, Z. Li, R.M. Xu, and Z. Zhang. 2007b. The Rtt109-Vps75 histone acetyltransferase complex acetylates non-nucleosomal histone H3. J. Biol. Chem. 282:14158-14164.
27. Hayashi, A., H. Ogawa, K. Kohno, S.M. Gasser, and Y. Hiraoka. 1998. Meiotic behaviours of chromosomes and microtubules in budding yeast: relocalization of centromeres and telomeres during meiotic prophase. Genes Cells. 3:587-601.
28. Hector, R.E., R.L. Shtofman, A. Ray, B.R. Chen, T. Nyun, K.L. Berkner, and K.W. Runge . 2007 . Tel1p preferentially associates with short telomeres to stimulate their elongation. Mol. Cell. 27:851-858.
29. Hediger, F., F.R. Neumann, G. Van Houwe, K. Dubrana, and S.M. Gasser. 2002. Live imaging of telomeres: yKu and Sir proteins def ne redundant telomere-anchoring pathways in yeast. Curr. Biol. 12:2076-2089.
30. Heun, P., T. Laroche, M.K. Raghuraman, and S.M. Gasser. 2001. The positioning and dynamics of origins of replication in the budding yeast nucleus. J. Cell Biol. 152:385-400.
31. Hiraga, S., E.D. Robertson, and A.D. Donaldson. 2006. The Ctf18 RFC-like complex positions yeast telomeres but does not specify their replication time. EMBO J. 25:1505-1514.
32. Hyland, E.M., M.S. Cosgrove, H. Molina, D. Wang, A. Pandey, R.J. Cottee, and J.D. Boeke. 2005 . Insights into the role of histone H3 and histone H4 core modif able residues in Saccharomyces cerevisiae. Mol. Cell. Biol. 25:10060-10070.
33. Ivessa, A.S., B.A. Lenzmeier, J.B. Bessler, L.K. Goudsouzian, S.L. Schnakenberg, and V.A. Zakian. 2003. The Saccharomyces cerevisiae helicase Rrm3p facilitates replication past nonhistone protein-DNA complexes. Mol. Cell. 12:1525-1536.
34. Kanoh, J., and F. Ishikawa. 2003. Composition and conservation of the telomeric complex. Cell. Mol. Life Sci. 60:2295-2302.
35. Lengronne, A., and E. Schwob. 2002. The yeast CDK inhibitor Sic1 prevents genomic instability by promoting replication origin licensing in late G(1). Mol. Cell. 9:1067-1078.
36. Li, Q., H. Zhou, H. Wurtele, B. Davies, B. Horazdovsky , A. Verreault, and Z. Zhang . 2008 . Acetylation of histone H3 lysine 56 regulates replicationcoupled nucleosome assembly. Cell. 134:244-255.
37. Maas, N.L., K.M. Miller, L.G. DeFazio, and D.P. Toczyski. 2006. Cell cycle and checkpoint regulation of histone H3 K56 acetylation by Hst3 and Hst4. Mol. Cell. 23:109-119.
38. Maillet, L., F. Gaden, V. Brevet, G. Fourel, S.G. Martin, K. Dubrana, S.M. Gasser, and E. Gilson. 2001. Ku-def cient yeast strains exhibit alternative states of silencing competence. EMBO Rep. 2:203-210.
39. Makovets, S., I. Herskowitz, and E.H. Blackburn . 2004. Anatomy and dynamics of DNA replication fork movement in yeast telomeric regions. Mol. Cell. Biol. 24:4019-4031.
40. Masumoto, H., D. Hawke, R. Kobayashi, and A. Verreault. 2005. A role for cellcycle-regulated histone H3 lysine 56 acetylation in the DNA damage response. Nature. 436:294-298.
41. Moqtaderi, Z., and K. Struhl. 2004. Genome-wide occupancy prof le of the RNA polymerase III machinery in Saccharomyces cerevisiae reveals loci with incomplete transcription complexes. Mol. Cell. Biol. 24:4118-4127.
42. Mousson, F., F. Ochsenbein, and C. Mann. 2007. The histone chaperone Asf1 at the crossroads of chromatin and DNA checkpoint pathways. Chromosoma. 116:79-93.
43. Myers, L.C., C.M. Gustafsson, D.A. Bushnell, M. Lui, H. Erdjument-Bromage, P. Tempst, and R.D. Kornberg. 1998. The Med proteins of yeast and their function through the RNA polymerase II carboxy-terminal domain. Genes Dev. 12:45-54.
44. Noma, K., H.P. Cam, R.J. Maraia, and S.I. Grewal. 2006. A role for TFIIIC transcription factor complex in genome organization. Cell. 125:859-872.
45. Ozdemir, A., S. Spicuglia, E. Lasonder, M. Vermeulen, C. Campsteijn, H.G. Stunnenberg, and C. Logie . 2005 . Characterization of lysine 56 of histone H3 as an acetylation site in Saccharomyces cerevisiae. J. Biol. Chem. 280:25949-25952.
46. Ozdemir, A., H. Masumoto, P. Fitzjohn, A. Verreault, and C. Logie. 2006. Histone H3 lysine 56 acetylation: a new twist in the chromosome cycle. Cell Cycle. 5:2602-2608.
47. Porter, S.E., P.W. Greenwell, K.B. Ritchie, and T.D. Petes. 1996. The DNA- binding protein Hdf1p (a putative Ku homologue) is required for maintaining normal telomere length in Saccharomyces cerevisiae. Nucleic Acids Res. 24:582-585.
48. Pryde, F.E., H.C. Gorham, and E.J. Louis. 1997. Chromosome ends: all the same under their caps. Curr. Opin. Genet. Dev. 7:822-828.
49. Raghuraman, M.K., E.A. Winzeler, D. Collingwood, S. Hunt, L. Wodicka, A. Conway, D.J. Lockhart, R.W. Davis, B.J. Brewer, and W.L. Fangman. 2001 . Replication dynamics of the yeast genome. Science. 294:115-121.
50. Recht, J., T. Tsubota, J.C. Tanny, R.L. Diaz, J.M. Berger, X. Zhang, B.A. Garcia, J. Shabanowitz, A.L. Burlingame , D.F. Hunt , et al . 2006 . Histone chaperone Asf1 is required for histone H3 lysine 56 acetylation, a modif cation associated with S phase in mitosis and meiosis. Proc. Natl. Acad. Sci. USA. 103:6988-6993.
51. Sabourin , M. , C.T. Tuzon , and V.A. Zakian . 2007 . Telomerase and Tel1p preferentially associate with short telomeres in S. cerevisiae. Mol. Cell. 27 : 550-561 .
52. Schmid, M., G. Arib, C. Laemmli, J. Nishikawa, T. Durussel, and U.K. Laemmli. 2006 . Nup-PI: the nucleopore-promoter interaction of genes in yeast. Mol. Cell. 21:379-391.
53. Schmidt, K.H., K.L. Derry, and R.D. Kolodner. 2002. Saccharomyces cerevisiae RRM3, a 5' to 3' DNA helicase, physically interacts with proliferating cell nuclear antigen. J. Biol. Chem. 277:45331-45337.
54. Schneider, J., P. Bajwa, F.C. Johnson, S.R. Bhaumik, and A. Shilatifard. 2006. Rtt109 is required for proper H3K56 acetylation: a chromatin mark associated with the elongating RNA polymerase II. J. Biol. Chem. 281:37270-37274.
55. Selth, L., and J.Q. Svejstrup. 2007. Vps75, a new yeast member of the NAP histone chaperone family. J. Biol. Chem. 282:12358-12362.
56. Singer, M.S., A. Kahana, A.J. Wolf, L.L. Meisinger, S.E. Peterson, C. Goggin, M. Mahowald, and D.E. Gottschling. 1998. Identif cation of high-copy disruptors of telomeric silencing in Saccharomyces cerevisiae. Genetics. 150:613-632.
57. Straight, A.F., A.S. Belmont, C.C. Robinett, and A.W. Murray. 1996. GFP tagging of budding yeast chromosomes reveals that protein-protein interactions can mediate sister chromatid cohesion. Curr Biol. 6:1599-1608.
58. Svejstrup, J.Q. 2007. Elongator complex: how many roles does it play? Curr. Opin. Cell Biol. 19:331-336.
59. Taddei, A., F. Hediger , F.R. Neumann, C. Bauer , and S.M. Gasser. 2004. Separation of silencing from perinuclear anchoring functions in yeast Ku80, Sir4 and Esc1 proteins. EMBO J. 23:1301-1312.
60. Tanabe, H., FA. Habermann, I. Solovei, M. Cremer, and T. Cremer. 2002. Nonrandom radial arrangements of interphase chromosome territories: evolutionary considerations and functional implications. Mutat. Res. 504:37-45.
61. Thrower, D.A., and K. Bloom. 2001. Dicentric chromosome stretching during anaphase reveals roles of Sir2/Ku in chromatin compaction in budding yeast. Mol. Biol. Cell. 12:2800-2812.
62. Tsubota, T., C. Berndsen, J. Erkmann, C. Smith, L. Yang, M. Freitas, J. Denu, and P. Kaufman . 2007 . Histone H3-K56 acetylation is catalyzed by histone chaperone-dependent complexes. Mol. Cell. 25:703-712.
63. Williams, R.R.E., V. Azuara, P. Perry, S. Sauer , M. Dvorkina, H. Jorgensen, J. Roix, P. McQueen, T. Misteli, M. Merkenschlager, and A.G. Fisher. 2006. Neural induction promotes large-scale chromatin reorganisation of the Mash1 locus. J. Cell Sci. 119:132-140.
64. Wright, J.H., D.E. Gottschling, and V.A. Zakian. 1992. Saccharomyces telomeres assume a non-nucleosomal chromatin structure. Genes Dev. 6:197-210
65. Xu, F, K. Zhang, and M. Grunstein. 2005. Acetylation in histone H3 globular domain regulates gene expression in yeast. Cell. 121:375-385.
66. Xu, F, Q. Zhang , K. Zhang, W. Xie, and M. Grunstein. 2007. Sir2 deacetylates histone H3 lysine 56 to regulate telomeric heterochromatin structure in yeast. Mol. Cell. 27:890-900.
67. Zink, D., M.D. Amaral, A. Englmann, S. Lang, L.A. Clarke, C. Rudolph, F Alt, K. Luther , C. Braz, N. Sadoni, et al. 2004. Transcription-dependent spatial arrangements of CFTR and adjacent genes in human cell nuclei. J. Cell Biol. 166:815-825.