Defective break-induced replication leads to half-crossovers in Saccharomyces cerevisiae

Genetics

Volumn 179, Issue 4, 2008, Pages 1845-1860

  Deem, Angela ^a   Barker, Krista ^a   VanHulle, Kelly ^a   Downing, Brandon ^a   Vayl, Alexandra ^a   Malkova, Anna ^a,b  

^a Biology SL332   (United States)

^b INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BREAK INDUCED REPLICATION; CONTROLLED STUDY; CROSSING OVER; DNA REPAIR; DNA REPLICATION; DNA STRAND BREAKAGE; FUNGAL GENE; FUNGAL STRAIN; GENE DELETION; GENE MUTATION; GENETIC REGULATION; NONHUMAN; POL32 GENE; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; BIOLOGICAL MODEL; DOUBLE STRANDED DNA BREAK; ENZYMOLOGY; GENETICS; METABOLISM; MUTATION;

EUKARYOTA; MAMMALIA; SACCHAROMYCES CEREVISIAE;

DNA DIRECTED DNA POLYMERASE; POL32 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN;

DNA BREAKS, DOUBLE-STRANDED; DNA REPLICATION; DNA-DIRECTED DNA POLYMERASE; MODELS, GENETIC; MUTATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 53349168503     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.108.087940     Document Type: Article

References (62)

1. ASAI, T., S. SOMMER, A. BAILONE and T. KOGOMA, 1993 Homologous recombination-dependent initiation of DNA replication from DNA damage-inducible origins in Escherichia coli. EMBO J. 12: 3287-3295.
2. BLEUIT, J. S., H. XU, Y. MA, T. WANG, J. LIU et al., 2001 Mediator proteins orchestrate enzyme-ssDNA assembly during T4 recombination-dependent DNA replication and repair. Proc. Natl. Acad. Sci. USA 98: 8298-8305.
3. BOSCO, G., and J. E. HABER, 1998 Chromosome break-induced DNA replication leads to nonreciprocal translocations and telomere capture. Genetics 150: 1037-1047.
4. DAVIS, A. P., and L. S. SYMINGTON, 2004 RAD51-dependent break-induced replication in yeast. Mol. Cell. Biol. 24: 2344-2351.
5. DIFILIPPANTONIO, M. J., S. PETERSEN, H. T. CHEN, R. JOHNSON, M. JASIN et al., 2002 Evidence for replicative repair of DNA double-strand breaks leading to oncogenic translocation and gene amplification. J. Exp. Med. 196: 469-480.
6. FORMOSA, T., and B. M. ALBERTS, 1986a DNA synthesis dependent on genetic recombination: characterization of a reaction catalyzed by purified bacteriophage T4 proteins. Cell 47: 793-806.
7. FORMOSA, T., and B. M. ALBERTS, 1986b Purification and characterization of the T4 bacteriophage uvsX protein. J. Biol. Chem. 261: 6107-6118.
8. GEORGE, J. W., B. A. STOHR, D. J. TOMSO and K. N. KREUZER, 2001 The tight linkage between DNA replication and double-strand break repair in bacteriophage T4. Proc. Natl. Acad. Sci. USA 98: 8290-8297.
9. GOLDSTEIN, A. L., and J. H. MCCUSKER, 1999 Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15: 1541-1553.
10. GOLLIN, S. M., 2001 Chromosomal alterations in squamous cell carcinomas of the head and neck: window to the biology of disease. Head Neck 23: 238-253.
11. GUTHRIE, C., and G. R. FINK, 1991 Guide to Yeast Genetics and Molecular Biology. Academic Press, San Diego.
12. HABER, J. E., and M. HEARN, 1985 Rad52-independent mitotic gene conversion in Saccharomyces cerevisiae frequently results in chromosomal loss. Genetics 111: 7-22.
13. HARACSKA, L., I. UNK, R. E. JOHNSON, E. JOHANSSON, P. M. BURGERS et al., 2001 Roles of yeast DNA polymerases delta and zeta and of Rev1 in the bypass of abasic sites. Genes Dev. 15: 945-954.
14. HUANG, M. E., A. G. RIO, M. D. GALIBERT and F. GALIBERT, 2002 Pol32, a subunit of Saccharomyces cerevisiae DNA polymerase delta, suppresses genomic deletions and is involved in the mutagenic bypass pathway. Genetics 160: 1409-1422.
15. INGVARSSON, S., 1999 Molecular genetics of breast cancer progression. Semin. Cancer Biol. 9: 277-288.
16. IRA, G., A. MALKOVA, G. LIBERI, M. FOIANI and J. E. HABER, 2003 Srs2 and Sgs1-Top3 suppress crossovers during double-strand break repair in yeast. Cell 115: 401-411.
17. JOHANSSON, E., J. MAJKA and P. M. BURGERS, 2001 Structure of DNA polymerase delta from Saccharomyces cerevisiae. J. Biol. Chem. 276: 43824-43828.
18. JOHANSSON, E., P. GARG and P. M. BURGERS, 2004 The Pol32 subunit of DNA polymerase delta contains separable domains for processive replication and proliferating cell nuclear antigen (PCNA) binding. J. Biol. Chem. 279: 1907-1915.
19. KOGOMA, T., 1976 Two types of temperature sensitivity in DNA replication of an Escherichia coli dnaB mutant. J. Mol. Biol. 103: 191-197.
20. KOGOMA, T., 1997 Stable DNA replication: interplay between DNA replication, homologous recombination, and transcription. Microbiol. Mol. Biol. Rev. 61: 212-238.
21. KOGOMA, T., and K. G. LARK, 1975 Characterization of the replication of Escherichia coli DNA in the absence of protein synthesis: stable DNA replication. J. Mol. Biol. 94: 243-256.
22. KREUZER, K. N., 2000 Recombination-dependent DNA replication in phage T4. Trends Biochem. Sci. 25: 165-173.
23. KUZMINOV, A., 1999 Recombinational repair of DNA damage in Escherichia coli and bacteriophage lambda. Microbiol. Mol. Biol. Rev. 63: 751-813.
24. LARK, C. A., J. RIAZI and K. G. LARK, 1978 dnaT, dominant conditional-lethal mutation affecting DNA replication in Escherichia coli. J. Bacteriol. 136: 1008-1017.
25. LAO, J. P., S. D. OH, M. SHINOHARA, A. SHINOHARA and N. HUNTER, 2008 Rad52 promotes post-invasion steps of meiotic double-strand-break repair. Mol. Cell 29: 517-524.
26. LAWRENCE, C., 2002 Cellular roles of DNA polymerase zeta and Rev1 protein. DNA Repair 1: 425-435.
27. LE, S., J. K. MOORE, J. E. HABER and C. W. GREIDER, 1999 RAD50 and RAD51 define two pathways that collaborate to maintain telomeres in the absence of telomerase. Genetics 152: 143-152.
28. 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.
29. LEUNG, W., A. MALKOVA and J. E. HABER, 1997 Gene targeting by linear duplex DNA frequently occurs by assimilation of a single strand that is subject to preferential mismatch correction. Proc. Natl. Acad. Sci. USA 94: 6851-6856.
30. LIANG, X., S. J. MEECH, L. F. ODOM, M. A. BITTER, J. W. RYDER et al., 2004 Assessment of t(2;5)(p23;q35) translocation and variants in pediatric ALK+ anaplastic large cell lymphoma. Am. J. Clin. Pathol. 121: 496-506.
31. LUKE, B., G. VERSINI, M. JAQUENOUD, I. W. ZAIDI, T. KURZ et al., 2006 The cullin Rtt101p promotes replication fork progression through damaged DNA and natural pause sites. Curr. Biol. 16: 786-792.
32. LYDEARD, J. R., S. JAIN, M. YAMAGUCHI and J. E. HABER, 2007 Break-induced replication and telomerase-independent telomere maintenance require Pol32. Nature 448: 820-823.
33. MALKOVA, A., E. L. IVANOV and J. E. HABER, 1996 Double-strand break repair in the absence of RAD51 in yeast: a possible role for break-induced DNA replication. Proc. Natl. Acad. Sci. USA 93: 7131-7136.
34. MALKOVA, A., M. L. NAYLOR, M. YAMAGUCHI, G. IRA and J. E. HABER, 2005 RAD51-dependent break-induced replication differs in kinetics and checkpoint responses from RAD51-mediated gene conversion. Mol. Cell. Biol. 25: 933-944.
35. MARIANS, K. J., 2000 PriA-directed replication fork restart in Escherichia coli. Trends Biochem. Sci. 25: 185-189.
36. MCEACHERN, M. J., and J. E. HABER, 2006 Break-induced replication and recombinational telomere elongation in yeast. Annu. Rev. Biochem. 75: 111-135.
37. MICHEL, B., M. J. FLORES, E. VIGUERA, G. GROMPONE, M. SEIGNEUR et al., 2001 Rescue of arrested replication forks by homologous recombination. Proc. Natl. Acad. Sci. USA 98: 8181-8188.
38. MICHEL, J. J., J. F. MCCARVILLE and Y. XIONG, 2003 A role for Saccharomyces cerevisiae Cul8 ubiquitin ligase in proper anaphase progression. J. Biol. Chem. 278: 22828-22837.
39. MORROW, D. M., C. CONNELLY and P. HIETER, 1997 "Break copy" duplication: a model for chromosome fragment formation in Saccharomyces cerevisiae. Genetics 147: 371-382.
40. MYUNG, K., A. DATTA, C. CHEN and R. D. KOLODNER, 2001 SGS1, the Saccharomyces cerevisiae homologue of BLM and WRN, suppresses genome instability and homeologous recombination. Nat. Genet. 27: 113-116.
41. NARAYANAN, V., P. A. MIECZKOWSKI, H. M. KIM, T. D. PETES and K. V. LOBACHEV, 2006 The pattern of gene amplification is determined by the chromosomal location of hairpin-capped breaks. Cell 125: 1283-1296.
42. NEUMANN, A. A., and R. R. REDDEL, 2002 Telomere maintenance and cancer - look, no telomerase. Nat. Rev. Cancer 2: 879-884.
43. OH, S. D., J. P. LAO, P. Y-H. HWANG, A. F. TAYLOR, G. R. SMITH et al., 2007 BLM ortholog, Sgs1, prevents aberrant crossing-over by suppressing formation of multichromatid joint molecules. Cell 130: 259-272.
44. PAN, X., P. YE, D. S. YUAN, X. WANG, J. S. BADER et al., 2006 A DNA integrity network in the yeast Saccharomyces cerevisiae. Cell 124: 1069-1081.
45. 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.
46. PIERCE, A. J., J. M. STARK, F. D. ARAUJO, M. E. MOYNAHAN, M. BERWICK et al., 2001 Double-strand breaks and tumorigenesis. Trends Cell Biol. 11: S52-S59.
47. PUI, C. H., M. V. RELLING and J. R. DOWNING, 2004 Acute lymphoblastic leukemia. N. Engl. J. Med. 350: 1535-1548.
48. REDDEL, R. R., 2003 Alternative lengthening of telomeres, telomerase, and cancer. Cancer Lett. 194: 155-162.
49. ROBERTS, T. M., I. W. ZAIDI, J. A. VAISICA, M. PETER and G. W. BROWN, 2008 Regulation of Rtt107 recruitment to stalled DNA replication forks by the cullin Rtt101 and the Rtt109 acetyltransferase. Mol. Cell. Biol. 19: 171-180.
50. SABATIER, L., M. RICOUL, G. POTTIER and J. P. MURNANE, 2005 The loss of a single telomere can result in instability of multiple chromosomes in a human tumor cell line. Mol. Cancer Res. 3: 139-150.
51. SCHMIDT, K. H., J. WU and R. D. KOLODNER, 2006 Control of translocations between highly diverged genes by Sgs1, the Saccharomyces cerevisiae homolog of the Bloom's syndrome protein. Mol. Cell. Biol. 26: 5406-5420.
52. SCHOLES, D. T., M. BANERJEE, B. BOWEN and M. J. CURICIO, 2001 Multiple regulators of Ty1 transposition in Saccharomyces cerevisiae have conserved roles in genome maintenance. Genetics 159: 1449-1465.
53. SMITH, C. E., B. LLORENTE and L. S. SYMINGTON, 2007 Template switching during break-induced replication. Nature 447: 102-105.
54. SPELL, R. M., and S. JINKS-ROBERTSON, 2004 Examination of the roles of Sgs1 and Srs2 helicases in the enforcement of recombination fidelity in Saccharomyces cerevisiae. Genetics 168: 1855-1865.
55. STARK, J. M., and M. JASIN, 2003 Extensive loss of heterozygosity is suppressed during homologous repair of chromosomal breaks. Mol. Cell. Biol. 23: 733-743.
56. STORICI, F., L. K. LEWIS and M. A. RESNICK, 2001 In vivo site-directed mutagenesis using oligonucleotides. Nat. Biotechnol. 19: 773-776.
57. STRAUCHEN, J. A., 2004 Immunophenotypic and molecular studies in the diagnosis and classification of malignant lymphoma. Cancer Invest. 22: 138-148.
58. TENG, S. C., J. CHANG, B. MCCOWAN and V. A. ZAKIAN, 2000 Telomerase-independent lengthening of yeast telomeres occurs by an abrupt Rad50p-dependent, Rif-inhibited recombinational process. Mol. Cell 6: 947-952.
59. TENG, S. C., and V. A. ZAKIAN, 1999 Telomere-telomere recombination is an efficient bypass pathway for telomere maintenance in Saccharomyces cerevisiae. Mol. Cell. Biol. 19: 8083-8093.
60. 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.
61. VOELKEL-MEIMAN, K., and G. S. ROEDER, 1990 Gene conversion tracts stimulated by HOT1-promoted transcription are long and continuous. Genetics 126: 851-867.
62. WACH, A., A. BRACHAT, R. POHLMANN and P. PHILIPPSEN, 1994 New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10: 1793-1808.