Rtt109 Prevents Hyper-Amplification of Ribosomal RNA Genes through Histone Modification in Budding Yeast

PLoS Genetics

Volumn 9, Issue 4, 2013, Pages

  Ide, Satoru ^a   Saka, Kimiko ^a   Kobayashi, Takehiko ^a,b  

^a NATIONAL INSTITUTE OF GENETICS   (Japan)

^b GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLTRANSFERASE; COHESIN; RIBOSOME DNA; RIBOSOME RNA;

ACETYLATION; ARTICLE; CELL DIVISION; CONTROLLED STUDY; DNA RECOMBINATION; GENE AMPLIFICATION; GENE DOSAGE; GENOME ANALYSIS; HISTONE ACETYLATION; HISTONE MODIFICATION; LYSINE ACETYLATION; NONHUMAN; NUCLEOSOME; PHENOTYPE; REGULATORY MECHANISM; RNA REPLICATION; RTT 109 GENE; SISTER CHROMATID; YEAST;

CELL CYCLE PROTEINS; CHROMATIDS; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA REPLICATION; DNA-BINDING PROTEINS; GENOME, FUNGAL; HISTONE ACETYLTRANSFERASES; HISTONES; RECOMBINATION, GENETIC; RNA, RIBOSOMAL; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EUKARYOTA; SACCHAROMYCETALES;

EID: 84876820158     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003410     Document Type: Article

References (46)

1. Warner JR, (1999) The economics of ribosome biosynthesis in yeast. Trends Biochem Sci 24: 437-40.
2. Ide S, Miyazaki T, Maki H, Kobayashi T, (2010) Abundance of ribosomal RNA gene copies maintains genome integrity. Science 327: 693-6.
3. Kobayashi T, Heck DJ, Nomura M, Horiuchi T, (1998) Expansion and contraction of ribosomal DNA repeats in Saccharomyces cerevisiae: requirement of replication fork blocking (Fob1) protein and the role of RNA polymerase I. Genes Dev 12: 3821-30.
4. Kobayashi T, (2006) Strategies to maintain the stability of the ribosomal RNA gene repeats-collaboration of recombination, cohesion, and condensation. Genes Genet Syst 81: 155-61.
5. Kobayashi T, (2003) The replication fork barrier site forms a unique structure with Fob1p and inhibits the replication fork. Mol Cell Biol 23: 9178-88.
6. Kobayashi T, Horiuchi T, Tongaonkar P, Vu L, Nomura M, (2004) SIR2 regulates recombination between different rDNA repeats, but not recombination within individual rRNA genes in yeast. Cell 117: 441-53.
7. Kobayashi T, Ganley AR, (2005) Recombination regulation by transcription-induced cohesin dissociation in rDNA repeats. Science 309: 1581-4.
8. Driscoll R, Hudson A, Jackson SP, (2007) Yeast Rtt109 promotes genome stability by acetylating histone H3 on lysine 56. Science 315: 649-52.
9. Tsubota T, Berndsen CE, Erkmann JA, Smith CL, Yang L, Freitas MA, Denu JM, Kaufman PD, (2007) Histone H3-K56 acetylation is catalyzed by histone chaperone-dependent complexes. Mol Cell 25: 703-12.
10. Han J, Zhou H, Horazdovsky B, Zhang K, Xu RM, Zhang Z, (2007) Rtt109 acetylates histone H3 lysine 56 and functions in DNA replication. Science 315: 653-5.
11. Han J, Zhou H, Li Z, Xu RM, Zhang Z, (2007) Acetylation of lysine 56 of histone H3 catalyzed by RTT109 and regulated by ASF1 is required for replisome integrity. J Biol Chem 282: 28587-96.
12. Li Q, Zhou H, Wurtele H, Davies B, Horazdovsky B, Verreault A, Zhang Z, (2008) Acetylation of histone H3 lysine 56 regulates replication-coupled nucleosome assembly. Cell 134: 244-55.
13. Masumoto H, Hawke D, Kobayashi R, Verreault A, (2005) A role for cell-cycle-regulated histone H3 lysine 56 acetylation in the DNA damage response. Nature 436: 294-8.
14. Prado F, Cortes-Ledesma F, Aguilera A, (2004) The absence of the yeast chromatin assembly factor Asf1 increases genomic instability and sister chromatid exchange. EMBO Rep 5: 497-502.
15. Duro E, Vaisica JA, Brown GW, Rouse J, (2008) Budding yeast Mms22 and Mms1 regulate homologous recombination induced by replisome blockage. DNA Repair (Amst) 7: 811-8.
16. Endo H, Kawashima S, Sato L, Lai MS, Enomoto T, Seki M, Horikoshi M, (2010) Chromatin dynamics mediated by histone modifiers and histone chaperones in postreplicative recombination. Genes Cells 15: 945-58.
17. Houseley J, Tollervey D, (2011) Repeat expansion in the budding yeast ribosomal DNA can occur independently of the canonical homologous recombination machinery. Nucleic Acids Res 39: 8778-91.
18. Celic I, Verreault A, Boeke JD, (2008) Histone H3 K56 hyperacetylation perturbs replisomes and causes DNA damage. Genetics 179: 1769-84.
19. Recht J, Tsubota T, Tanny JC, Diaz RL, Berger JM, Zhang X, Garcia BA, Shabanowitz J, Burlingame AL, Hunt DF, Kaufman PD, Allis CD, (2006) Histone chaperone Asf1 is required for histone H3 lysine 56 acetylation, a modification associated with S phase in mitosis and meiosis. Proc Nat Acad Sci USA 103: 6988-93.
20. Schneider J, Bajwa P, Johnson FC, Bhaumik SR, Shilatifard A, (2006) Rtt109 is required for proper H3K56 acetylation: a chromatin mark associated with the elongating RNA polymerase II. J Biol Chem 281: 37270-4.
21. Berndsen CE, Tsubota T, Lindner SE, Lee S, Holton JM, Kaufman PD, Keck JL, Denu JM, (2008) Molecular functions of the histone acetyltransferase chaperone complex Rtt109-Vps75. Nat Struct Mol Biol 15: 948-56.
22. Park YJ, Sudhoff KB, Andrews AJ, Stargell LA, Luger K, (2008) Histone chaperone specificity in Rtt109 activation. Nat Struct Mol Biol 15: 957-64.
23. Fillingham J, Recht J, Silva AC, Suter B, Emili A, Stagljar I, Krogan NJ, Allis CD, Keogh MC, Greenblatt JF, (2008) Chaperone control of the activity and specificity of the histone H3 acetyltransferase Rtt109. Mol Cell Biol 28: 4342-53.
24. Defossez PA, Prusty R, Kaeberlein M, Lin SJ, Ferrigno P, Silver PA, Keil RL, Guarente L, (1999) Elimination of replication block protein Fob1 extends the life span of yeast mother cells. Mol Cell 3: 447-55.
25. Takeuchi Y, Horiuchi T, Kobayashi T, (2003) Transcription-dependent recombination and the role of fork collision in yeast rDNA. Genes Dev 17: 1497-506.
26. Oakes M, Siddiqi I, Vu L, Aris J, Nomura M, (1999) Transcription factor UAF, expansion and contraction of ribosomal DNA (rDNA) repeats, and RNA polymerase switch in transcription of yeast rDNA. Mol Cell Biol 19: 8559-69.
27. Bernstein KA, Reid RJ, Sunjevaric I, Demuth K, Burgess RC, Rothstein R, (2011) The Shu complex, which contains Rad51 paralogues, promotes DNA repair through inhibition of the Srs2 anti-recombinase. Mol Biol Cell 22: 1599-607.
28. Dammann R, Lucchini R, Koller T, Sogo JM, (1993) Chromatin structures and transcription of rDNA in yeast Saccharomyces cerevisiae. Nucleic Acids Res 21: 2331-38.
29. Gottlieb S, Esposito RE, (1989) A new role for a yeast transcriptional silencer gene, SIR2, in regulation of recombination in ribosomal DNA. Cell 56: 771-6.
30. Fritze CE, Verschueren K, Strich R, Easton Esposito R, (1997) Direct evidence for SIR2 modulation of chromatin structure in yeast rDNA. EMBO J 16: 6495-509.
31. Imai S, Johnson FB, Marciniak RA, McVey M, Park PU, Guarente L, (2000) Sir2: an NAD-dependent histone deacetylase that connects chromatin silencing, metabolism, and aging. Cold Spring Harb Symp Quant Biol 65: 297-302.
32. Michel AH, Kornmann B, Dubrana K, Shore D, (2005) Spontaneous rDNA copy number variation modulates Sir2 levels and epigenetic gene silencing. Genes Dev 19: 1199-210.
33. Zaidi IW, Rabut G, Poveda A, Scheel H, Malmstrom J, Ulrich H, Hofmann K, Pasero P, Peter M, Luke B, (2008) Rtt101 and Mms1 in budding yeast form a CUL4(DDB1)-like ubiquitin ligase that promotes replication through damaged DNA. EMBO Rep 9: 1034-40.
34. Duro E, Lundin C, Ask K, Sanchez-Pulido L, MacArtney TJ, Toth R, Ponting CP, Groth A, Helleday T, Rouse J, (2010) Identification of the MMS22L-TONSL complex that promotes homologous recombination. Mol Cell 40: 632-44.
35. Kraus E, Leung W-Y, Haber JE, (2001) Break-induced replication: a review and an example in budding yeast. Pro Natl Acad Sci 98: 8255-62.
36. Wurtele H, et al. (2012) Histone H3 lysine 56 acetylation and the response to DNA replication fork damage. Mol Cell Biol 32: 154-72.
37. Hourcade D, Dressler D, Wolfson J, (1973) The amplification of ribosomal RNA genes involves a rolling circle intermediate. Proc Natl Acad Sci U S A 70: 2926-30.
38. Brown DD, Dawid I, (1968) Specific gene amplification in oocytes. Oocyte nuclei contain extrachromosomal replicas of the genes for ribosomal RNA. Science 160: 272-80.
39. Gall JG, (1968) Differential synthesis of the genes for ribosomal RNA during amphibian oögenesis. Proc Nat Acad Sci USA 60: 553-60.
40. Andersson DI, Hughes D, (2009) Gene Amplification and Adaptive Evolution in Bacteria. Ann Rev Genet 43: 167-95.
41. Albertson DG, (2006) Gene amplifiction and cancer. Trend Genet 22: 447-55.
42. Archer SY, Hodin RA, (1999) Histon acetylation and cancer. Cur Opin Genet & Dev 9: 171-74.
43. Ide S, Kobayashi T, (2010) Analysis of DNA replication in Saccharomyces cerevisiae by two-dimensional and pulsed-field gel electrophoresis. Curr Protoc Cell Biol Chapter 22: Unit 22 14.
44. Miller A, Yang B, Foster T, Kirchmaier AL, (2008) Proliferating cell nuclear antigen and ASF1 modulate silent chromatin in Saccharomyces cerevisiae via lysine 56 on histone H3. Genetics 179: 793-809.
45. Nettikadan S, Tokumasu F, Takeyasu K, (1996) Quantitative analysis of the transcription factor AP2 binding to DNA by atomic force microscopy. Biochem Biophys Res Commun 1226: 645-9.
46. Cherry JM, Hong EL, Amundsen C, Balakrishnan R, Binkley G, et al. (2012) Saccharomyces Genome Database: the genomics resource of budding yeast. Nucleic Acids Res 40 (Database issue):: D700-5.