Chromosome aberrations resulting from double-strand DNA breaks at a naturally occurring yeast fragile site composed of inverted Ty elements are independent of Mre11p and Sae2p

Genetics

Volumn 183, Issue 2, 2009, Pages 423-439

  Casper, Anne M ^a   Greenwell, Patricia W ^a   Tang, Wei ^a   Petes, Thomas D ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA POLYMERASE; ENDONUCLEASE; EXO1P PROTEIN; MRE11 PROTEIN; MUS81P PROTEIN; PROTEIN RAD1; PSO2P PROTEIN; RAD27P PROTEIN; SAE2P PROTEIN; SLX4P PROTEIN; UNCLASSIFIED DRUG; YEN1P PROTEIN;

ARTICLE; CELL DIVISION; CHROMOSOME ABERRATION; CHROMOSOME BREAKAGE; CHROMOSOME REARRANGEMENT; DOUBLE STRANDED DNA BREAK; GENE DELETION; HOMOLOGOUS RECOMBINATION; INVERTED REPEAT; MATING; MUTANT; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; TELOMERE; YEAST;

CHROMOSOME ABERRATIONS; CHROMOSOME FRAGILE SITES; CHROMOSOMES, FUNGAL; DEOXYRIBONUCLEASES; DNA BREAKS, DOUBLE-STRANDED; DNA POLYMERASE I; DNA REPLICATION; DNA TRANSPOSABLE ELEMENTS; DNA, FUNGAL; ENDODEOXYRIBONUCLEASES; ENDONUCLEASES; EXODEOXYRIBONUCLEASES; INVERTED REPEAT SEQUENCES; MODELS, GENETIC; MUTATION; NUCLEIC ACID CONFORMATION; RECOMBINATION, GENETIC; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TELOMERE;

SACCHAROMYCES CEREVISIAE;

EID: 70649111379     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.109.106385     Document Type: Article

References (62)

1. AKGUN, E., J. ZAHN, S. BAUMES, G. BROWN, F. LIANG et al., 1997 Palindrome resolution and recombination in the mammalian germ line. Mol. Cell. Biol. 17: 5559-5570.
2. ALLERS, T., and D. R. LEACH, 1995 DNA palindromes adopt a methylation- resistant conformation that is consistent with DNA cruciform or hairpin formation in vivo. J. Mol. Biol. 252: 70-85.
3. ARGUESO, J. L., J. WESTMORELAND, P. A. MIECZKOWSKI, M. GAWEL, T. D. PETES et al., 2008 Double-strand breaks associated with repetitive DNA can reshape the genome. Proc. Natl. Acad. Sci. USA 105: 11845-11850.
4. BRESSAN, D. A., H. A. OLIVARES, B. E. NELMS and J. H. PETRINI, 1998 Alteration of N-terminal phosphoesterase signature motifs inactivates Saccharomyces cerevisiae Mre11. Genetics 150: 591-600.
5. COLLICK, A., J. DREW, J. PENBERTH, P. BOIS, J. LUCKETT et al., 1996 Instability of long inverted repeats within mouse transgenes. EMBO J. 15: 1163-1171.
6. COLLINS, J., G. VOLCKAERT and P. NEVERS, 1982 Precise and nearly-precise excision of the symmetrical inverted repeats of Tn5; common features of recA-independent deletion events in Escherichia coli. Gene 19: 139-146.
7. COTE, A. G., and S. M. LEWIS, 2008 Mus81-dependent double-strand DNA breaks at in vivo-generated cruciform structures in S. cerevisiae. Mol. Cell 31: 800-812.
8. COUREY, A. J., and J. C. WANG, 1988 Influence of DNA sequence and supercoiling on the process of cruciform formation. J. Mol. Biol. 202: 35-43.
9. D'AMOURS, D., and S. P. JACKSON, 2002 The Mre11 complex: at the crossroads of DNA repair and checkpoint signalling. Nat. Rev. Mol. Cell. Biol. 3: 317-327.
10. DASGUPTA, U., K. WESTON-HAFER and D. E. BERG, 1987 Local DNA sequence control of deletion formation in Escherichia coli plasmid pBR322. Genetics 115: 41-49.
11. DAVIS, A. P., and L. S. SYMINGTON, 2004 RAD51-dependent break-induced replication in yeast. Mol. Cell. Biol. 24: 2344-2351.
12. DEPAMPHILIS, M. L., 2002 Eukaryotic DNA replication forks. Chemtracts. Biochem. Mol. Biol. 15: 313-325.
13. DEPAMPHILIS, M. L., and P. M. WASSARMAN, 1980 Replication of eukaryotic chromosomes: a close-up of the replication fork. Annu. Rev. Biochem. 49: 627-666.
14. EDGAR, R., M. DOMRACHEV and A. E. LASH, 2002 Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30: 207-210. (Pubitemid 34679544)
15. EYKELENBOOM, J. K., J. K. BLACKWOOD, E. OKELY and D. R. LEACH, 2008 SbcCD causes a double-strand break at a DNA palindrome in the Escherichia coli chromosome. Mol. Cell 29: 644-651.
16. FARAH, J. A., E. HARTSUIKER, K. MIZUNO, K. OHTA and G. R. SMITH, 2002 A 160-bp palindrome is a Rad50.Rad32-dependent mitotic recombination hotspot in Schizosaccharomyces pombe. Genetics 161: 461-468.
17. FARAH, J. A., G. CROMIE, W. W. STEINER and G. R. SMITH, 2005 A novel recombination pathway initiated by the Mre11/Rad50/ Nbs1 complex eliminates palindromes during meiosis in Schizosaccharomyces pombe. Genetics 169: 1261-1274.
18. FRIEDBERG, E. C., G. C. WALKER, W. SIEDE, R. D. WOOD, R. A. SCHULTZ et al., 2006 DNA Repair and Mutagenesis. ASM Press, Washington, DC.
19. GORDENIN, D. A., A. L. MALKOVA, A. PETERZEN, V. N. KULIKOV, Y. I. PAVLOV et al., 1992 Transposon Tn5 excision in yeast: influence of DNA polymerases α, δ, and ε and DNA repair genes. Proc. Natl. Acad. Sci. USA 89: 3785-3789.
20. GORDENIN, D. A., K. S. LOBACHEV, N. P. DEGTYAREVA, A. L. MALKOVA, E. PERKINS et al., 1993 Inverted DNA repeats: a source of eukaryotic genomic instability. Mol. Cell. Biol. 13: 5315-5322.
21. GUTHRIE, C., and G. R. FINK, 1991 Guide to Yeast Genetics and Molecular Biology. Academic Press, San Diego.
22. HABER, J. E., and M. HEARN, 1985 RAD52-independent mitotic gene conversion in Saccharomyces cerevisiae frequently results in chromosomal loss. Genetics 111: 7-22.
23. HAWTHORNE, D. C., 1963 A deletion in yeast and its bearing on the structure of the mating type locus. Genetics 48: 1727-1729.
24. IP, S. C., U. RASS, M. G. BLANCO, H. R. FLYNN, J. M. SKEHEL et al., 2008 Identification of Holliday junction resolvases from humans and yeast. Nature 456: 357-361.
25. KOGO, H., H. INAGAKI, T. OHYE, T. KATO, B. S. EMANUEL et al., 2007 Cruciform extrusion propensity of human translocation-mediating palindromic AT-rich repeats. Nucleic Acids Res. 35: 1198-1208.
26. KOKOSKA, R. J., L. STEFANOVIC, J. DEMAI and T. D. PETES, 2000 Increased rates of genomic deletions generated by mutations in the yeast gene encoding DNA polymerase delta or by decreases in the cellular levels of DNA polymerase delta. Mol. Cell. Biol. 20: 7490-7504.
27. KRISHNA, S., B. M. WAGENER, H. P. LIU, Y. C. LO, R. STERK et al., 2007 Mre11 and Ku regulation of double-strand break repair by gene conversion and break-induced replication. DNA Repair (Amst.) 6: 797-808.
28. KURAHASHI, H., H. INAGAKI, T. OHYE, H. KOGO, T. KATO et al., 2006 Palindrome-mediated chromosomal translocations in humans. DNA Repair (Amst.) 5: 1136-1145.
29. KURAHASHI, H., H. INAGAKI, E. HOSOBA, T. KATO, T. OHYE et al., 2007 Molecular cloning of a translocation breakpoint hotspot in 22q11. Genome Res. 17: 461-469.
30. LEMOINE, F. J., N. P. DEGTYAREVA, K. LOBACHEV and T. D. PETES, 2005 Chromosomal translocations in yeast induced by low levels of DNA polymerase a model for chromosome fragile sites. Cell 120: 587-598.
31. LEMOINE, F. J., N. P. DEGTYAREVA, R. J. KOKOSKA and T. D. PETES, 2008 Reduced levels of DNA polymerase delta induce chromosome fragile site instability in yeast. Mol. Cell. Biol. 28: 5359-5368.
32. LENGSFELD, B. M., A. J. RATTRAY, V. BHASKARA, R. GHIRLANDO and T. T. PAULL, 2007 Sae2 is an endonuclease that processes hairpin DNA cooperatively with the Mre11/Rad50/Xrs2 complex. Mol. Cell 28: 638-651.
33. LEWIS, S. M., and A. G. COTE, 2006 Palindromes and genomic stress fractures: bracing and repairing the damage. DNA Repair (Amst.) 5: 1146-1160.
34. LLORENTE, B., C. E. SMITH and L. S. SYMINGTON, 2008 Break-induced replication: What is it and what is it for? Cell Cycle 7: 859-864.
35. LOBACHEV, K. S., D. A. GORDENIN and M. A. RESNICK, 2002 The Mre11 complex is required for repair of hairpin-capped doublestrand breaks and prevention of chromosome rearrangements. Cell 108: 183-193.
36. MIMITOU, E. P., and L. S. SYMINGTON, 2009 Nucleases and helicases take center stage in homologous recombination. Trends Biochem. Sci. 34: 264-272.
37. MOREAU, S., J. R. FERGUSON and L. S. SYMINGTON, 1999 The nuclease activity of Mre11 is required for meiosis but not for mating type switching, end joining, or telomere maintenance. Mol. Cell. Biol. 19: 556-566.
38. NARAYANAN, V., P. A. MIECZKOWSKI, H. M. KIM, T. D. PETES and K. S. LOBACHEV, 2006 The pattern of gene amplification is determined by the chromosomal location of hairpin-capped breaks. Cell 125: 1283-1296.
39. OZENBERGER, B. A., and G. S. ROEDER, 1991 A unique pathway of double-strand break repair operates in tandemly repeated genes. Mol. Cell. Biol. 11: 1222-1231.
40. PAQUES, F., and J. E. HABER, 1999 Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 63: 349-404.
41. RATTRAY, A. J., 2004 A method for cloning and sequencing long palindromic DNA junctions. Nucleic Acids Res. 32: e155.
42. RATTRAY, A. J., C. B. MCGILL, B. K. SHAFER and J. N. STRATHERN, 2001 Fidelity of mitotic, double-strand-break repair in Saccharomyces cerevisiae: a role for SAE2/COM1. Genetics 158: 109-122. (Pubitemid 32428634)
43. RATTRAY, A. J., B. K. SHAFER, B. NEELAM and J. N. STRATHERN, 2005 A mechanism of palindromic gene amplification in Saccharomyces cerevisiae. Genes Dev. 19: 1390-1399. (Pubitemid 41003027)
44. ROUSE, J., 2009 Control of genome stability by Slx protein complexes. Biochem. Soc. Trans. 37: 495-510.
45. RUSKIN, B., and G. R. FINK, 1993 Mutations in POL1 increase the mitotic instability of tandem inverted repeats in Saccharomyces cerevisiae. Genetics 134: 43-56.
46. SCHMIDT, K. H., V. PENNANEACH, C. P. PUTNAM and R. D. KOLODNER, 2006 Analysis of gross-chromosomal rearrangements in Saccharomyces cerevisiae. Methods Enzymol. 409: 462-476. (Pubitemid 43912303)
47. SINDEN, R. R., S. S. BROYLES and D. E. PETTIJOHN, 1983 Perfect palindromic lac operator DNA sequence exists as a stable cruciform structure in supercoiled DNA in vitro but not in vivo. Proc. Natl. Acad. Sci. USA 80: 1797-1801.
48. SINDEN, R. R., G. X. ZHENG, R. G. BRANKAMP and K. N. ALLEN, 1991 On the deletion of inverted repeated DNA in Escherichia coli: effects of length, thermal stability, and cruciform formation in vivo. Genetics 129: 991-1005.
49. SMITH, C. E., A. F. LAM and L. S. SYMINGTON, 2009 Aberrant doublestrand break repair resulting in half crossovers in mutants defective for Rad51 or the DNA polymerase delta complex. Mol. Cell. Biol. 29: 1432-1441.
50. STRATHERN, J., J. HICKS and I. HERSKOWITZ, 1981 Control of cell type in yeast by the mating type. The alpha1-alpha2 hypothesis. J. Mol. Biol. 147: 239-244.
51. 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.
52. TANAKA, H., D. A. BERGSTROM, M. C. YAO and S. J. TAPSCOTT, 2005 Widespread and nonrandom distribution of DNA palindromes in cancer cells provides a structural platform for subsequent gene amplification. Nat. Genet. 37: 320-327.
53. TANAKA, H., Y. CAO, D. A. BERGSTROM, C. KOOPERBERG, S. J. TAPSCOTT et al., 2007 Intrastrand annealing leads to the formation of a large DNA palindrome and determines the boundaries of genomic amplification in human cancer. Mol. Cell. Biol. 27: 1993-2002.
54. TAVASSOLI, M., M. SHAYEGHI, A. NASIM and F. Z. WATTS, 1995 Cloning and characterisation of the Schizosaccharomyces pombe rad32 gene: a gene required for repair of double strand breaks and recombination. Nucleic Acids Res. 23: 383-388.
55. TRINH, T. Q., and R. R. SINDEN, 1991 Preferential DNA secondary structure mutagenesis in the lagging strand of replication in E. coli. Nature 352: 544-547.
56. TRUJILLO, K. M., and P. SUNG, 2001 DNA structure-specific nuclease activities in the Saccharomyces cerevisiae Rad50*Mre11 complex. J. Biol. Chem. 276: 35458-35464.
57. VANHULLE, K., F. J. LEMOINE, V. NARAYANAN, B. DOWNING, K. HULL et al., 2007 Inverted DNA repeats channel repair of distant double-strand breaks into chromatid fusions and chromosomal rearrangements. Mol. Cell. Biol. 27: 2601-2614.
58. VOINEAGU, I., V. NARAYANAN, K. S. LOBACHEV and S. M. MIRKIN, 2008 Replication stalling at unstable inverted repeats: interplay between DNA hairpins and fork stabilizing proteins. Proc. Natl. Acad. Sci. USA 105: 9936-9941.
59. WARMINGTON, J. R., R. ANWAR, C. S. NEWLON, R. B. WARING, R. W. DAVIES et al., 1986 A 'hot-spot' for Ty transposition on the left arm of yeast chromosome III. Nucleic Acids Res. 14: 3475-3485.
60. ZAMB, T. J., and T. D. PETES, 1981 Unequal sister-strand recombination within the yeast ribosomal DNA does not require the RAD52 gene product. Curr. Genet. 3: 125-132.
61. ZHENG, G. X., and R. R. SINDEN, 1988 Effect of base composition at the center of inverted repeated DNA sequences on cruciform transitions in DNA. J. Biol. Chem. 263: 5356-5361.
62. ZHENG, G. X., T. KOCHEL, R. W. HOEPFNER, S. E. TIMMONS and R. R. SINDEN, 1991 Torsionally tuned cruciform and Z-DNA probes for measuring unrestrained supercoiling at specific sites in DNA of living cells. J. Mol. Biol. 221: 107-122.