γH2A-binding protein Brc1 affects centromere function in fission yeast

Molecular and Cellular Biology

Volumn 33, Issue 7, 2013, Pages 1410-1416

  Lee, Si Young ^a   Rozenzhak, Sophie ^a,b   Russell, Paul ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b Life Technologies Corporation   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; HISTONE H2A; HISTONE H3; LYSINE; PROTEIN BRC 1; TIABENDAZOLE; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE S PHASE; CENTROMERE; CHROMOSOME SEGREGATION; CONTROLLED STUDY; DNA DAMAGE CHECKPOINT; GENE SILENCING; HETEROCHROMATIN; HISTONE METHYLATION; M PHASE CELL CYCLE CHECKPOINT; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN LOCALIZATION; YEAST;

CARRIER PROTEINS; CELL CYCLE PROTEINS; CENTROMERE; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOME SEGREGATION; CHROMOSOMES, FUNGAL; DNA METHYLATION; DNA REPLICATION; GENE SILENCING; HETEROCHROMATIN; HISTONES; LYSINE; METHYLTRANSFERASES; MICROTUBULES; S PHASE; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS;

EID: 84875234378     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01654-12     Document Type: Article

References (50)

1. Harper JW, Elledge SJ. 2007. The DNA damage response: ten years after. Mol. Cell 28:739 -745.
2. Musacchio A, Salmon ED. 2007. The spindle-assembly checkpoint in space and time. Nat. Rev. Mol. Cell Biol. 8:379 -393.
3. Jackson SP, Bartek J. 2009. The DNA-damage response in human biology and disease. Nature 461:1071-1078.
4. Cam HP, Sugiyama T, Chen ES, Chen X, FitzGerald PC, Grewal SI. 2005. Comprehensive analysis of heterochromatin- and RNAi-mediated epigenetic control of the fission yeast genome. Nat. Genet. 37:809-819.
5. Almeida R, Allshire RC. 2005. RNA silencing and genome regulation. Trends Cell Biol. 15:251-258.
6. Pidoux AL, Allshire RC. 2004. Kinetochore and heterochromatin domains of the fission yeast centromere. Chromosome Res. 12:521-534.
7. Bernard P, Hardwick K, Javerzat JP. 1998. Fission yeast bub1 is a mitotic centromere protein essential for the spindle checkpoint and the preservation of correct ploidy through mitosis. J. Cell Biol. 143:1775-1787.
8. Kawashima SA, Yamagishi Y, Honda T, Ishiguro K, Watanabe Y. 2010. Phosphorylation of H2A by Bub1 prevents chromosomal instability through localizing shugoshin. Science 327:172-177.
9. Cimprich KA, Cortez D. 2008. ATR: an essential regulator of genome integrity. Nat. Rev. Mol. Cell Biol. 9:616-627.
10. Branzei D, Foiani M. 2010. Maintaining genome stability at the replication fork. Nat. Rev. Mol. Cell Biol. 11:208 -219.
11. Dickey JS, Redon CE, Nakamura AJ, Baird BJ, Sedelnikova OA, Bonner WM. 2009. H2AX: functional roles and potential applications. Chromosoma 118:683- 692.
12. Stucki M, Jackson SP. 2006. gammaH2AX and MDC1: anchoring the DNA-damage-response machinery to broken chromosomes.DNARepair 5:534 -543.
13. Nakamura TM, Du LL, Redon C, Russell P. 2004. Histone H2A phosphorylation controls Crb2 recruitment at DNA breaks, maintains checkpoint arrest, and influences DNA repair in fission yeast. Mol. Cell. Biol. 24:6215- 6230.
14. Kilkenny ML, Dore AS, Roe SM, Nestoras K, Ho JC, Watts FZ, Pearl LH. 2008. Structural and functional analysis of the Crb2-BRCT2 domain reveals distinct roles in checkpoint signaling and DNA damage repair. Genes Dev. 22:2034 -2047.
15. Sofueva S, Du LL, Limbo O, Williams JS, Russell P. 2010. BRCT domain interactions with phospho-histone H2A target Crb2 to chromatin at double- strand breaks and maintain the DNA damage checkpoint. Mol. Cell. Biol. 30:4732- 4743.
16. Williams JS, Williams RS, Dovey CL, Guenther G, Tainer JA, Russell P. 2010. gammaH2A binds Brc1 to maintain genome integrity during Sphase. EMBO J. 29:1136 -1148.
17. Lee KM, Nizza S, Hayes T, Bass KL, Irmisch A, Murray JM, O'Connell MJ. 2007. Brc1-mediated rescue of Smc5/6 deficiency: requirement for multiple nucleases and a novel Rad18 function. Genetics 175:1585-1595.
18. Li X, Liu K, Li F, Wang J, Huang H, Wu J, Shi Y. 2012. Structure of C-terminal tandem BRCT repeats of Rtt107 protein reveals critical role in interaction with phosphorylated histoneH2AduringDNAdamage repair. J. Biol. Chem. 287:9137-9146.
19. Yan W, Shao Z, Li F, Niu L, Shi Y, Teng M, Li X. 2011. Structural basis of gammaH2AX recognition by human PTIP BRCT5-BRCT6 domains in the DNA damage response pathway. FEBS Lett. 585:3874 -3879.
20. Szilard RK, Jacques PE, Laramee L, Cheng B, Galicia S, Bataille AR, Yeung M, Mendez M, Bergeron M, Robert F, Durocher D. 2010. Systematic identification of fragile sites via genome-wide location analysis of gamma-H2AX. Nat. Struct. Mol. Biol. 17:299 -305.
21. Rozenzhak S, Mejia-Ramirez E, Williams JS, Schaffer L, Hammond JA, Head SR, Russell P. 2010. Rad3 decorates critical chromosomal domains with gammaH2A to protect genome integrity during S-phase in fission yeast. PLoS Genet. 6:e1001032. doi:10.1371/journal.pgen.1001032.
22. Zaratiegui M, Castel SE, Irvine DV, Kloc A, Ren J, Li F, de Castro E, Marin L, Chang AY, Goto D, Cande WZ, Antequera F, Arcangioli B, Martienssen RA. 2011. RNAi promotes heterochromatic silencing through replication-coupled release of RNA Pol II. Nature 479:135-138.
23. Li F, Martienssen R, Cande WZ. 2011. Coordination of DNA replication and histone modification by the Rik1-Dos2 complex. Nature 475:244- 248.
24. Forsburg SL, Rhind N. 2006. Basic methods for fission yeast. Yeast 23: 173-183.
25. Nakagawa H, Lee JK, Hurwitz J, Allshire RC, Nakayama J, Grewal SI, Tanaka K, Murakami Y. 2002. Fission yeast CENP-B homologs nucleate centromeric heterochromatin by promoting heterochromatin-specific histone tail modifications. Genes Dev. 16:1766 -1778.
26. Halic M, Moazed D. 2010. Dicer-independent primal RNAs trigger RNAi and heterochromatin formation. Cell 140:504 -516.
27. Li F, Goto DB, Zaratiegui M, Tang X, Martienssen R, Cande WZ. 2005. Two novel proteins, dos1 and dos2, interact with rik1 to regulate heterochromatic RNA interference and histone modification. Curr. Biol. 15: 1448-1457.
28. Yamane K, Mizuguchi T, Cui B, Zofall M, Noma K, Grewal SI. 2011. Asf1/HIRA facilitate global histone deacetylation and associate with HP1 to promote nucleosome occupancy at heterochromatic loci. Mol. Cell 41:56-66.
29. Rougemaille M, Shankar S, Braun S, Rowley M, Madhani HD. 2008. Ers1, a rapidly diverging protein essential for RNA interferencedependent heterochromatic silencing in Schizosaccharomyces pombe. J. Biol. Chem. 283:25770 -25773.
30. Rodriguez-Gabriel MA, Watt S, Bahler J, Russell P. 2006. Upf1, an RNA helicase required for nonsense-mediated mRNA decay, modulates the transcriptional response to oxidative stress in fission yeast. Mol. Cell. Biol. 26:6347- 6356.
31. Pebernard S, Wohlschlegel J, McDonald WH, Yates JR, III, Boddy MN. 2006. The Nse5-Nse6 dimer mediates DNA repair roles of the Smc5-Smc6 complex. Mol. Cell. Biol. 26:1617-1630.
32. Partridge JF, Borgstrom B, Allshire RC. 2000. Distinct protein interaction domains and protein spreading in a complex centromere. Genes Dev. 14:783-791.
33. Grewal SI, Elgin SC. 2007. Transcription and RNA interference in the formation of heterochromatin. Nature 447:399-406.
34. Ekwall K, Javerzat JP, Lorentz A, Schmidt H, Cranston G, Allshire R. 1995. The chromodomain protein Swi6: a key component at fission yeast centromeres. Science 269:1429 -1431.
35. Nonaka N, Kitajima T, Yokobayashi S, Xiao G, Yamamoto M, Grewal SI, Watanabe Y. 2002. Recruitment of cohesin to heterochromatic regions by Swi6/HP1 in fission yeast. Nat. Cell Biol. 4:89 -93.
36. Bernard P, Maure JF, Partridge JF, Genier S, Javerzat JP, Allshire RC. 2001. Requirement of heterochromatin for cohesion at centromeres. Science 294:2539 -2542.
37. Verkade HM, Bugg SJ, Lindsay HD, Carr AM, O'Connell MJ. 1999. Rad18 is required for DNA repair and checkpoint responses in fission yeast. Mol. Biol. Cell 10:2905-2918.
38. Hammet A, Magill C, Heierhorst J, Jackson SP. 2007. Rad9 BRCT domain interaction with phosphorylated H2AX regulates the G1 checkpoint in budding yeast. EMBO Rep. 8:851- 857.
39. Du LL, Nakamura TM, Russell P. 2006. Histone modificationdependent and -independent pathways for recruitment of checkpoint protein Crb2 to double-strand breaks. Genes Dev. 20:1583-1596.
40. Braun S, Garcia JF, Rowley M, Rougemaille M, Shankar S, Madhani HD. 2011. The Cul4-Ddb1(Cdt)(2) ubiquitin ligase inhibits invasion of a boundary-associated antisilencing factor into heterochromatin. Cell 144: 41-54.
41. Pebernard S, Schaffer L, Campbell D, Head SR, Boddy MN. 2008. Localization of Smc5/6 to centromeres and telomeres requires heterochromatin and SUMO, respectively. EMBO J. 27:3011-3023.
42. Scholes DT, Banerjee M, Bowen B, Curcio MJ. 2001. Multiple regulators of Ty1 transposition in Saccharomyces cerevisiae have conserved roles in genome maintenance. Genetics 159:1449 -1465.
43. Brady TL, Schmidt CL, Voytas DF. 2008. Targeting integration of the Saccharomyces Ty5 retrotransposon. Methods Mol. Biol. 435:153-163.
44. Qian Z, Huang H, Hong JY, Burck CL, Johnston SD, Berman J, Carol A, Liebman SW. 1998. Yeast Ty1 retrotransposition is stimulated by a synergistic interaction between mutations in chromatin assembly factor I and histone regulatory proteins. Mol. Cell. Biol. 18:4783- 4792.
45. Houben A, Schubert I. 2003. DNA and proteins of plant centromeres. Curr. Opin. Plant Biol. 6:554 -560.
46. Andrulis ED, Zappulla DC, Alexieva-Botcheva K, Evangelista C, Sternglanz R. 2004. One-hybrid screens at the Saccharomyces cerevisiae HMR locus identify novel transcriptional silencing factors. Genetics 166: 631-635.
47. Zappulla DC, Maharaj AS, Connelly JJ, Jockusch RA, Sternglanz R. 2006. Rtt107/Esc4 binds silent chromatin and DNA repair proteins using different BRCT motifs. BMC Mol. Biol. 7:40. doi:10.1186/1471-2199-7-40.
48. Fernandez-Capetillo O, Mahadevaiah SK, Celeste A, Romanienko PJ, Camerini-Otero RD, Bonner WM, Manova K, Burgoyne P, Nussenzweig A. 2003. H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Dev. Cell 4:497-508.
49. Ichijima Y, Ichijima M, Lou Z, Nussenzweig A, Camerini-Otero RD, Chen J, Andreassen PR, Namekawa SH. 2011. MDC1 directs chromosome- wide silencing of the sex chromosomes in male germ cells. Genes Dev. 25:959 -971.
50. Nakamura K, Okamoto A, Katou Y, Yadani C, Shitanda T, Kaweeteerawat C, Takahashi TS, Itoh T, Shirahige K, Masukata H, Nakagawa T. 2008. Rad51 suppresses gross chromosomal rearrangement at centromere in Schizosaccharomyces pombe. EMBO J. 27:3036 -3046.