Both CAG repeats and inverted DNA repeats stimulate spontaneous unequal sister-chromatid exchange in Saccharomyces cerevisiae

Nucleic Acids Research

Volumn 32, Issue 18, 2004, Pages 5677-5684

  Nag, Dilip K ^a,b   Suri, Manisha ^a   Stenson, Erin K ^a  

^a WADSWORTH CENTER   (United States)

^b STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MRE11 PROTEIN; RAD50 PROTEIN; RAD51 PROTEIN; RAD52 PROTEIN; REPETITIVE DNA; DEOXYRIBONUCLEASE; DNA; DNA BINDING PROTEIN; EXODEOXYRIBONUCLEASE; MRE11 PROTEIN, S CEREVISIAE; RAD50 PROTEIN, S CEREVISIAE; RAD51 PROTEIN, S CEREVISIAE; RAD52 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CONTROLLED STUDY; DNA RECOMBINATION; DNA REPAIR; FUNGAL STRAIN; GENE MUTATION; GENE SEQUENCE; GENETIC CODE; GENETIC STABILITY; GENOTYPE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; SACCHAROMYCES CEREVISIAE; SISTER CHROMATID EXCHANGE; TRINUCLEOTIDE REPEAT; YEAST CELL; CHEMISTRY; GENETICS; METABOLISM; NUCLEOTIDE REPEAT; PHYSIOLOGY;

SACCHAROMYCES CEREVISIAE;

DNA; DNA-BINDING PROTEINS; ENDODEOXYRIBONUCLEASES; EXODEOXYRIBONUCLEASES; RAD51 RECOMBINASE; RAD52 DNA REPAIR AND RECOMBINATION PROTEIN; REPETITIVE SEQUENCES, NUCLEIC ACID; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SISTER CHROMATID EXCHANGE; TRINUCLEOTIDE REPEATS;

EID: 6944230944     PISSN: 03051048     EISSN: None     Source Type: Journal    
DOI: 10.1093/nar/gkh901     Document Type: Article

References (58)

1. Modrich,P. and Lahue,R. (1996) Mismatch repair in replication fidelity, genetic recombination, and cancer biology. Annu. Rev. Biochem., 65, 101-133.
2. Wells,R.D. and Warren,S.T. (1998) Genetic Instabilities and Hereditary Neurological Diseases. Academic Press, San Diego.
3. Cummings,C.J. and Zoghbi,H.Y. (2000) Fourteen and counting: unraveling trinucleotide repeat diseases. Hum. Mol. Genet., 9, 909-916.
4. Yoon,S.-R., Dubeau,L., de Young,M., Wexler,N.S. and Arnheim,N. (2003) Huntington disease expansion mutations in humans can occur before meiosis is completed. Proc. Natl Acad. Sci. USA, 100, 8834-8838.
5. Savouret,C., Garcia-Cordier,C., Megret,J., te Riele,H., Junien,C. and Gourdon,G. (2004) MSH2-dependent germinal CTG repeat expansions are produced continuously in spermatogonia from DM1 transgenic mice. Mol. Cell. Biol., 24, 629-637.
6. Kovtun,I.V. and McMurray,C.T. (2001) Trinucleotide expansion in haploid germ cells by gap repair. Nature Genet., 27, 407-411.
7. Nag,D.K. (2003) Trinucleotide repeat expansions: timing is everything. Trends Mol. Med., 9, 455-457.
8. Sia,E.A., Jinks-Robertson,S. and Petes,T.D. (1997) Genetic control of microsatellite stability. Mutat. Res., 383, 61-70.
9. Freudenreich,C.H., Stavenhagen,J.B. and Zakian,V.A. (1997) Stability of CTG/CAG trinucleotide repeat in yeast is dependent on its orientation in the genome. Mol. Cell. Biol., 17, 2090-2098.
10. Maurer,D.J., O'Callaghan,B.L. and Livingston,D.M. (1996) Orientation dependence of trinucleotide CAG repeat instability in yeast. Mol. Cell. Biol., 16, 6617-6622.
11. Miret,J.J., Pessoa-Brandao,L. and Lahue,R.S. (1998) Orientation-dependent and sequence-specific expansions of CTG/CAG trinucleotide repeats in Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA, 95, 12438-12443.
12. Kang,S., Jaworski,A., Ohshima,K. and Wells,R.D. (1995) Expansion and deletion of CTG repeats from human disease genes are determined by the direction of replication in E. coli. Nature Genet. 10, 213-218.
13. Cleary,J.D., Nichol,K., Wang,Y.H. and Pearson,C.E. (2002) Evidence of cis-acting factors in replication-mediated trinucleotide instability in primate cells. Nature Genet., 31, 37-46.
14. Fortune,M.T., Vassilopoulos,C., Coolbaugh,M.I., Siciliano,M.J. and Monckton,D.G. (2000) Dramatic, expansion-biased, age-dependent, tissue-specific somatic mosaicism in a transgenic mouse model of triplet repeat instability. Hum. Mol. Genet., 9, 439-445.
15. Kennedy,L. and Shelbourne,P. (2000) Dramatic mutation ability in HD mouse stratium: does polyglutamine load contribute to cell specific vulnerability in Huntington's disease? Hum. Mol. Genet., 9, 2539-2544.
16. Lia,A.-S., Seznec,H., Hofmann-Radvanyi,H., Radvanyi,F., Duros,C., Saquet,C., Blanche,M., Junien,C. and Gourdon,G. (1998) Somatic instability of the CTG repeat in mice transgenic for the myotonic dystrophy region is age dependent but not correlated to the relative intertissue transcription levels and proliferative capacities. Hum. Mol. Genet., 8, 1285-1291.
17. Manley,K., Shirley,T.L., Flaherty,L. and Messer,A. (1999) Msh2 deficiency prevents in vivo somatic instability of the CAG repeat in Huntington disease transgenic mice. Nature Genet., 23, 471-473.
18. n repeat in myotonic dystrophy knock-in mice is differentially affected by Msh3 and Msh6 mismatch-repair proteins. Hum. Mol. Genet., 2, 191-198.
19. Jakupciak,J.P. and Wells,R.D. (1999) Genetic instabilities in (CTG.CAG) repeats occur by recombination. J. Biol. Chem., 274, 23468-23479.
20. Sarkar,P.S., Chang,H.C., Boudi,F.B. and Reddy,S. (1998) CTG repeats show bimodal amplification in E. coli. Cell, 95, 531-540.
21. Richard,G.-F., Goellner,G.M., McMurray,C.T. and Haber,J.E. (2000) Recombination-induced CAG trinucleotide repeat expansions in yeast involve the MRE11-RAD50-XRS2 complex. EMBO J., 19, 2381-2390.
22. Jankowski,C., Nasar,F. and Nag,D.K. (2000) Meiotic instability of CAG repeat tracts occurs by double-strand break repair in yeast. Proc. Natl Acad. Sci. USA, 97, 2134-2139.
23. Cohen,H., Sears,D.D., Zenvirth,D., Heiter,P. and Simchen,G. (1999) Increased instability of human CTG repeat tracts on yeast artificial chromosomes during gametogenesis. Mol. Cell. Biol., 19, 4153-4158.
24. Schweitzer,J.K., Reinke,S. and Livingston,D.M. (2001) Meiotic alterations in CAG repeat tracts. Genetics, 159, 1861-1865.
25. Sinden,R.R., Potaman,V.D., Oussatcheva,E.A., Pearson,C.E., Lyubchenko,Y.L. and Shlyakhtenko,L.S. (2002) Triplet repeat DNA structures and human genetic disease: dynamic mutations from dynamic DNA. J. Biosci., 27, 53-65.
26. McMurray,C.T. (1995) Mechanisms of DNA expansion. Chromosoma, 104, 2-13.
27. Sakamoto,N., Chastain P.D., Parniewski,P., Ohshima,K., Pandolfo,M., Griffith,J.D. and Wells,R.D. (1999) Sticky DNA: self-association properties of long GAA.TTC repeats in R.R.Y triplex structures from Friedreich's ataxia. Mol. Cell, 3, 465-475.
28. Heidenfelder,B.L., Makhov,A.M. and Topal,M.D. (2003) Hairpin formation in Friedreich's ataxia triplet repeat expansion. J. Biol. Chem., 278, 2425-2431.
29. Moore,H., Greenwell,P.W., Liu,C.P., Arnheim,N. and Petes,T.D. (1999) Triplet repeats form secondary structures that escape DNA repair in yeast. Proc. Natl Acad. Sci. USA, 96, 1504-1509.
30. Freudenreich,C.H., Kantrow,S.M. and Zakian,V.A. (1998) Expansion and length-dependent fragility of CTG repeats in yeast. Science, 279, 853-856.
31. Usdin,K. and Woodford,K.J. (1995) CGG repeats associated with DNA instability and chromosome fragility from structures that block DNA synthesis in vitro. Nucleic Acids Res., 23, 4202-4209.
32. Kang,S., Ohshima,K., Shimizu,M., Amirhaeri,S. and Wells,R.D. (1995) Pausing of DNA synthesis in vitro at specific loci in CTG and CGG triplet repeats from human hereditary disease genes. J. Biol. Chem., 270, 27014-27021.
33. Pelletier,R., Krasilnikovam M.M., Samadashwily,G.M., Lahue,R. and Mirkin,S.M. (2003) Replication and expansion of trinucleotide repeats in yeast. Mol. Cell. Biol., 23, 1349-1357.
34. n repeats in vivo. Mol. Cell. Biol., 24, 2286-2295.
35. Nag,D.K., White,M.A. and Petes,T.D. (1989) Palindromic sequences in heteroduplex DNA inhibits mismatch repair in yeast. Nature, 340, 318-320.
36. Rose,M.D., Winston,F. and Heiter,P. (1990) Methods in Yeast Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
37. Fasullo,M., Bennet,T. and Koudelik,J. (1998) The Saccharomyces cerevisiae RAD9 checkpoint reduces the DNA-damage-associated stimulation of directed translocations. Mol. Cell. Biol., 18, 1190-1200.
38. Nag,D.K. and Petes,T.D. (1993) Physical detection of heteroduplexes during rneiotic recombination in the yeast Saccharomyces cerevisiae. Mol. Cell. Biol., 13, 2324-2331.
39. Shinohara,A., Ogawa,H. and Ogawa,T. (1992) Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell, 69, 457-470.
40. Nag,D.K. and Kurst,A. (1997) A 140-base-pair long palindromic sequence induces double-strand breaks during meiosis in the yeast Saccharomyces cerevisiae. Genetics, 146, 835-847.
41. Fasullo,M.T. and Davis,R.W. (1987) Recombination substrates designed to study recombination between unique and repetitive sequences in vivo. Proc. Natl Acad. Sci. USA, 84, 6215-6219.
42. Nasar,F., Jankowski,C. and Nag,D.K. (2000) Long palindromic sequences induce double-strand breaks during meiosis in yeast. Mol. Cell. Biol., 20, 3449-3458.
43. Kadyk,L.C. and Hartwell,L.H. (1992) Sister chromatids are preferred over homologs as substrates for recombinational repair in Saccharomyces cerevisiae. Genetics, 132, 387-402.
44. Leach,D.R.F. (1994) Long DNA palindromes, cruciform structures, genetic instability and secondary structure repair. Bioassays, 16, 893-900.
45. Gordenin,D.A., Lobachev,K.S., Degtyareva,N.P., Malkova,A.L., Perkins,E. and Resnick,M.A. (1993) Inverted DNA repeats: a source of eukaryotic genomic instability. Mol. Cell. Biol., 13, 5315-5322.
46. Farah,J.A., Hartsuiker,E., Mizuno,K., Ohta,K. and Smith,G.R., (2002) A 160 bp palindrome is Rad50.Rad32-dependent mitotic recombination hotspot in Schizosaccharomyces pombe. Genetics, 161, 461-468.
47. Rattray,A.J., McGill,C.B., Shafer,B.K. and Strathern,J.N. (2001) Fidelity of mitotic double-strand-break repair in Saccharomyces cerevisiae: a role for SAE2/COM1. Genetics, 158, 109-122.
48. Akgun,E., Zahn,J., Baumes,S., Brown,G., Liang,F., Romanienko,P.J., Lewis,S. and Jasin,M. (1997) Palindrome resolution and recombination in the mammalian germ line. Mol. Cell. Biol., 17, 5559-5570.
49. Connelly,J.C., Kirkham,L.A. and Leach,D.R.F. (1998) The SbcCD nuclease of Escherichia coli is a structural maintenance of chromosomes (SMC) family protein that cleaves hairpin DNA. Proc. Natl Acad. Sci. USA, 95, 7969-7974.
50. Symington,L.S. (2002) Role of RAD52 epistasis group genes in homologous recombination and double-strand break repair. Microbiol. Mol. Biol. Rev., 66, 630-670.
51. Sharples,G.J. and Leach,D.R.F. (1995) Structural and functional similarities between the SbeCD proteins of Escherichia coli and the Rad50 and Mre11 (Rad32) recombination and repair proteins of yeast. Mol. Microbiol., 17, 1215-1220.
52. Trujillo,K.M. and Sung,P. (2001) DNA structure-specific nuclease activities in the Saccharomyces cerevisiae Rad50* Mrc11 complex. J. Biol. Chem., 276, 35458-35464.
53. Lobachev,K.S., Gordenin,D.A. and Resnick,M.A. (2002) The Mre11 complex is required for repair of hairpin-capped double-strand breaks and prevention of chromosome rearrangements. Cell, 108, 183-193.
54. Dong,Z. and Fasullo,M. (2003) Multiple recombination pathways for sister chromatid exchange in Saccharomyces cerevisiae: role of RAD1 and the RAD52 epitasis group genes. Nucleic Acids Res., 31, 2576-2585.
55. Bressan,D.A., Baxter,B.K. and Petrini,J.H. (1999) The Mre11-Rad5O-Xrs2 protein complex facilitates homologous recombination-based double-strand break repair in Saccharomyces cerevisiae. Mol. Cell. Biol., 19, 7681-7687.
56. Davis,A.P. and Symington,L.S. (2004) RAD51-dependent break-induced replication in yeast. Mol. Cell. Biol., 24, 2344-2351.
57. Gonzalez-Barrera,S., Cortes-Ledesma,F., Wellinger,R.E. and Aguilera,A. (2003) Equal sister chromatid exchange is a major mechanism of double-strand break repair in yeast. Mol. Cell, 11, 1661-1671.
58. Callahan,J.L., Andrews,K.J., Zakian,V.A. and Freudenreich,C.H. (2003) Mutations in yeast replication proteins that increase CAG/CTG expansions also increase repeat fragility. Mol. Cell. Biol., 21, 7849-7860.