The Saccharomyces cerevisiae Mre11-Rad50-Xrs2 complex promotes trinucleotide repeat expansions independently of homologous recombination

DNA Repair

Volumn 43, Issue , 2016, Pages 1-8

  Ye, Yanfang ^a,b   Kirkham McCarthy, Lucy ^a   Lahue, Robert S ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^b FUJIAN AGRICULTURE AND FORESTRY UNIVERSITY   (China)

Author keywords

Expansion; Homologous recombination; Mre11 Rad50 Xrs2 complex; Neurological disease; Trinucleotide repeat

Indexed keywords

ARGININE; MRE11 PROTEIN; NUCLEIC ACID BINDING PROTEIN; RAD50 PROTEIN; UNCLASSIFIED DRUG; XRS2 PROTEIN; DEOXYRIBONUCLEASE; DNA BINDING PROTEIN; DNA HELICASE; EXODEOXYRIBONUCLEASE; FUNGAL DNA; HISTONE DEACETYLASE; MRE11 PROTEIN, S CEREVISIAE; RAD5 PROTEIN, S CEREVISIAE; RAD50 PROTEIN, S CEREVISIAE; REPRESSOR PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; SIN3 PROTEIN, S CEREVISIAE; XRS2 PROTEIN, S CEREVISIAE;

ARTICLE; BACTERIAL STRAIN; DNA REPAIR; GENE DELETION; GENE MUTATION; GENETIC DISORDER; HOMOLOGOUS RECOMBINATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ACETYLATION; SACCHAROMYCES CEREVISIAE; TRINUCLEOTIDE REPEAT; ACETYLATION; DNA REPLICATION; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; MUTATION;

ACETYLATION; DNA HELICASES; DNA REPAIR; DNA REPLICATION; DNA, FUNGAL; DNA-BINDING PROTEINS; ENDODEOXYRIBONUCLEASES; EXODEOXYRIBONUCLEASES; GENE EXPRESSION REGULATION, FUNGAL; HISTONE DEACETYLASES; HOMOLOGOUS RECOMBINATION; HUMANS; MUTATION; REPRESSOR PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRINUCLEOTIDE REPEAT EXPANSION; TRINUCLEOTIDE REPEATS;

EID: 84965018008     PISSN: 15687864     EISSN: 15687856     Source Type: Journal    
DOI: 10.1016/j.dnarep.2016.04.012     Document Type: Article

References (44)

1. Orr H.T., Zoghbi H.Y. Trinucleotide repeat disorders. Annu. Rev. Neurosci. 2007, 30:575-621.
2. Mirkin S.M. Expandable DNA repeats and human disease. Nature 2007, 447:932-940.
3. Kovtun I.V., McMurray C.T. Features of trinucleotide repeat instability in vivo. Cell Res. 2008, 18:198-213.
4. Lopez Castel A., Cleary J.D., Pearson C.E. Repeat instability as the basis for human diseases and as a potential target for therapy. Nat. Rev. Mol. Cell. Biol. 2010, 11:165-170.
5. Paulson H.L., Fischbeck K.H. Trinucleotide repeats in neurogenetic disorders. Annu. Rev. Neurosci. 1996, 19:79-107.
6. Lee D.-Y., McMurray C.T. Trinucleotide expansion in disease: why is there a length threshold?. Curr. Opin. Genet. Dev. 2014, 26:131-140.
7. Leeflang E.P., Zhang L., Tavare S., Hubert R., Srinidhi J., MacDonald M.E., Myers R.H., de Young M., Wexler N.S., Gusella J.F., Arnheim N. Single sperm analysis of the trinucleotide repeats in the Huntington's disease gene: quantification of the mutation frequency spectrum. Hum. Mol. Genet. 1995, 4:1519-1526.
8. Lahue R.S., Slater D.L. DNA repair and trinucleotide repeat instability. Front. Biosci. 2003, 8:s553-s565.
9. Bak S.T., Sakellariou D., Pena-Diaz J. The dual nature of mismatch repair as anitmutator and mutator: for better or worse. Front. Genet. 2014, 5. 10.3389/fgene.2014.00287.
10. Usdin K., House N.C., Freudenreich C.H. Repeat instability during DNA repair: insights from model systems. Crit. Rev. Biochem. Mol. Biol. 2015, 142-167.
11. Zhao X.-N., Usdin K. The repeat expansion diseases: the dark side of DNA repair. DNA Repair 2015, 32:96-105.
12. Iyer R.R., Pluciennik A., Napierala M., Wells R.D. DNA triplet repeat expansion and mismatch repair. Annu. Rev. Biochem. 2015, 84:199-226.
13. Manley K., Shirley T.L., Flaherty L., Messer A. Msh2 deficiency prevents in vivo somatic instability of the CAG repeat in Huntington disease transgenic mice. Nat. Genet. 1999, 23:471-473.
14. Kovtun I.V., McMurray C.T. Trinucleotide expansion in haploid germ cells by gap repair. Nat. Genet. 2001, 27:407-411.
15. van den Broek W.J., Nelen M.R., Wansink D.G., Coerwinkel M.M., te Riele H., Groenen P.J., Wieringa B. Somatic expansion behaviour of the (CTG)n repeat in myotonic dystrophy knock-in mice is differentially affected by Msh3 and Msh6 mismatch-repair proteins. Hum. Mol. Genet. 2002, 11:191-198.
16. Savouret C., Brisson E., Essers J., Kanaar R., Pastink A., te Riele H., Junien C., Gourdon G. CTG repeat instability and size variation timing in DNA repair-deficient mice. EMBO J. 2003, 22:2264-2273.
17. Wheeler V.C., Lebel L.-A., Vrbanac V., Teed A., te Riele H., MacDonald M.E. Mismatch repair gene Msh2 modifies the timing of early disease in HdhQ111 striatum. Hum. Mol. Genet. 2003, 12:273-281.
18. Owen B.A., Yang Z., Lai M., Gajek M., Badger J.D., Hayes J.J., Edelman W., Kucherlapati R., Wilson T.M., McMurray C.T. (CAG)n-hairpin DNA binds to Msh2-Msh3 and changes properties of mismatch recognition. Nat. Struct. Mol. Biol. 2005, 12:663-670.
19. Lokanga R.A., Zhao X.N., Usdin K. The mismatch repair protein MSH2 is rate limiting for repeat expansion in a fragile X premutation mouse model. Hum. Mutat. 2014, 35:129-136.
20. Zhao X.-N., Kumari D., Gupta S., Wu D., Evanitsky M., Yang W., Usdin K. MutSβ generates both expansions and contractions in a mouse model of the Fragile X-associated disorders. Hum. Mol. Genet. 2015, 24:7087-7096.
21. Gannon A.-M., Frizzell A., Healy E., Lahue R.S. MutSβ and histone deacetylase complexes promote expansions of trinucleotide repeats in human cells. Nucleic Acids Res. 2012, 40:10324-10333.
22. Du J., Campau E., Soragni E., Jespersen C., Gottesfeld J.M. Length-dependent CTG·CAG triplet-repeat expansion in myotonic dystrophy patient-derived induced pluripotent stem cells. Hum. Mol. Genet. 2013, 22:5276-5287.
23. Richard G.-F., Goellner G.M., McMurray C.T., Haber J.E. Recombination-induced CAG trinucleotide repeat expansions in yeast involve the MRE11-RAD50-XRS2 complex. EMBO J. 2000, 19:2381-2390.
24. Sundararajan R., Gellon L., Zunder R.M., Freudenreich C.H. Double-strand break repair pathways protect against CAG/CTG repeat expansions, contractions and repeat-mediated chromosomal fragility in Saccharomyces cerevisiae. Genetics 2010, 184:65-77.
25. Sundararajan R., Freudenreich C.H. Expanded CAG/CTG repeat DNA induces a checkpoint response that impacts cell proiferation in Saccharomyces cerevisiae. PLoS Genet. 2011, 7:e1001339.
26. Jamieson D.J., Rivers S.L., Stephen D.W. Analysis of Saccharomyces cerevisiae proteins induced by peroxide and superoxide stress. Microbiology 1995, 140:3277-3283.
27. Krogh B.O., Llorente B., Lam A., Symington L.S. Mutations in Mre11 phosphoesterase motif I that impair Saccharomyces cerevisiae Mre11-Rad50-Xrs2 complex stability in addition to nuclease activity. Genetics 2005, 171:1561-1570.
28. Sikorski R.S., Hieter P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 1989, 122:19-27.
29. Debacker K., Frizzell A., Gleeson O., Kirkham-McCarthy L., Mertz T., Lahue R.S. Histone deacetylase complexes promote trinucleotide repeat expansions. PLoS Biol. 2012, 10(12):e1001257. 10.1371/journal.pbio.1001257.
30. Concannon C., Lahue R.S. The 26S proteasome drives trinucleotide repeat expansions. Nucleic Acids Res. 2013, 41:6098-6108.
31. Bhattacharyya S., Lahue R.S. Yeast Srs2 DNA helicase selectively blocks expansions of trinucleotide repeats. Mol. Cell. Biol. 2004, 24:7324-7330.
32. Miret J.J., Pessoa-Brandao L., Lahue R.S. Orientation-dependent and sequence-specific expansions of CTG/CAG trinucleotide repeats in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:12438-12443.
33. Rattray A.J., McGill C.B., Shafer B.K., Strathern J.N. Fidelity of mitotic double-strand-break repair in Saccharomyces cerevisiae: a role for SAE2/COM1. Genetics 2001, 158:109-122.
34. Lobachev K.S., Gordenin D.A., Resnick M.A. The Mre11 complex is required for repair of hairpin-capped double-strand breaks and prevention of chromosome rearrangements. Cell 2002, 108:183-193.
35. Farah J.A., Cromie G., Steiner W.W., Smith G.R. A novel recombination pathway initiated by the Mre11/Rad50/Nbs1 complex eliminates palindromes during meiosis in Schizosaccharomyces pombe. Genetics 2005, 169:1261-1274.
36. Daee D.L., Mertz T., Lahue R.S. Postreplication repair inhibits CAG·CTG repeat expansions in Saccharomyces cerevisiae Mol. Cell. Biol. 2007, 27:102-110.
37. Scholz C., Weinert B.T., Wagner S.A., Beli P., Miyake Y., Qi J., Jensen L.J., Streicher W., McCarthy A.R., Westwood N.J., Lain S., Cox J., Matthias P., Mann M., Bradner J.E., Choudhary C. Acetylation site specificities of lysine deacetylase inhibitors in human cells. Nat. Biotechnol. 2015, 33:415-423.
38. Hopfner K.-P., Craig L., Moncalian G., Zinkel R.A., Usui T., Owen B.A., Karcher A., Henderson B., Bodmer J.-L., McMurray C.T., Carney J.P., Petrini J.H., Tainer J.A. The Rad50 zinc-hook is a structure joining Mre11 complexes in DNA recombination and repair. Nature 2002, 418:562-566.
39. Freudenreich C.H., Kantrow S.M., Zakian V.A. Expansion and length-dependent fragility of CTG repeats in yeast. Science 1998, 279:853-856.
40. Moore H., Greenwell P.W., Liu C.-P., Arnheim N., Petes T.D. Triplet repeats form secondary structures that escape DNA repair in yeast. Proc. Natl. Acad. Sci. USA 1999, 96:1504-1509.
41. Callahan J.L., Andrews K.J., Zakian V.A., Freudenreich C.H. Mutations in yeast replication proteins that increase CAG/CTG expansions also increase repeat fragility. Mol. Cell. Biol. 2003, 23:7849-7860.
42. Minesinger B.K., Jinks-Robertson S. Roles of RAD6 epistasis group members in spontaneous Pol zeta-dependent translesion synthesis in Saccharomyces cerevisiae. Genetics 2005, 169:1939-1955.
43. Makharashvili N., Tubbs A.T., Yang S.-H., Wang H., Barton O., Zhou Y., Deshpande R.A., Lee J.-H., Lobrich M., Sleckman B.P., Wu X., Paull T.T. Catalytic and noncatalytic roles of the CtIP endonuclease in double-strand break end resection. Mol. Cell 2014, 54:1022-1033.
44. Williams G.J., Lees-Miller S.P., Tainer J.A. Mre11-Rad50-Nbs1 conformations and the control of sensing, signaling, and effector responses at DNA double-strand breaks. DNA Repair 2010, 9:1299-1306.