E. coli SbcCD and RecA Control Chromosomal Rearrangement Induced by an Interrupted Palindrome

Molecular Cell

Volumn 39, Issue 1, 2010, Pages 59-70

  Darmon, Elise ^a   Eykelenboom, John K ^a   Lincker, Frédéric ^a   Jones, Lucy H ^a   White, Martin ^a   Okely, Ewa ^a   Blackwood, John K ^a   Leach, David R ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

DNA; Microbio

Indexed keywords

DNA FRAGMENT; ESCHERICHIA COLI PROTEIN; PALINDROMIC DNA; PROTEIN SBCCD; RECA PROTEIN; SINGLE STRANDED DNA; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CHROMOSOME; CHROMOSOME DUPLICATION; CHROMOSOME REARRANGEMENT; CONTROLLED STUDY; DNA DEGRADATION; DNA HAIRPIN; DNA REPLICATION; DOUBLE STRANDED DNA BREAK; ESCHERICHIA COLI; FLUORESCENCE MICROSCOPY; INVERTED REPEAT; NONHUMAN; SOUTHERN BLOTTING;

BASE PAIRING; CHROMOSOMES, BACTERIAL; DEOXYRIBONUCLEASES; DNA BREAKS, DOUBLE-STRANDED; DNA REPLICATION; DNA, BACTERIAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; EXONUCLEASES; GENE REARRANGEMENT; INVERTED REPEAT SEQUENCES; MICROSCOPY; MODELS, BIOLOGICAL; REC A RECOMBINASES; RECOMBINATION, GENETIC;

ESCHERICHIA COLI;

EID: 77954251862     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2010.06.011     Document Type: Article

References (44)

1. Bi X., Liu L.F. A replicational model for DNA recombination between direct repeats. J. Mol. Biol. 1996, 256:849-858.
2. Bolt E.L., Lloyd R.G. Substrate specificity of RusA resolvase reveals the DNA structures targeted by RuvAB and RecG in vivo. Mol. Cell 2002, 10:187-198.
3. Butler D.K., Yasuda L.E., Yao M.C. Induction of large DNA palindrome formation in yeast: implications for gene amplification and genome stability in eukaryotes. Cell 1996, 87:1115-1122.
4. Butler D.K., Gillespie D., Steele B. Formation of large palindromic DNA by homologous recombination of short inverted repeat sequences in Saccharomyces cerevisiae. Genetics 2002, 161:1065-1075.
5. Coté A.G., Lewis S.M. Mus81-dependent double-strand DNA breaks at in vivo-generated cruciform structures in S. cerevisiae. Mol. Cell 2008, 31:800-812.
6. Cromie G.A., Connelly J.C., Leach D.R. Recombination at double-strand breaks and DNA ends: conserved mechanisms from phage to humans. Mol. Cell 2001, 8:1163-1174.
7. Cunningham L.A., Coté A.G., Cam-Ozdemir C., Lewis S.M. Rapid, stabilizing palindrome rearrangements in somatic cells by the center-break mechanism. Mol. Cell. Biol. 2003, 23:8740-8750.
8. Davison A., Leach D.R. The effects of nucleotide sequence changes on DNA secondary structure formation in Escherichia coli are consistent with cruciform extrusion in vivo. Genetics 1994, 137:361-368.
9. Dillingham M.S., Kowalczykowski S.C. RecBCD enzyme and the repair of double-stranded DNA breaks. Microbiol. Mol. Biol. Rev. 2008, 72:642-671.
10. Downing B., Morgan R., VanHulle K., Deem A., Malkova A. Large inverted repeats in the vicinity of a single double-strand break strongly affect repair in yeast diploids lacking Rad51. Mutat. Res. 2008, 645:9-18.
11. Eykelenboom J.K., Blackwood J.K., Okely E., Leach D.R. SbcCD causes a double-strand break at a DNA palindrome in the Escherichia coli chromosome. Mol. Cell 2008, 29:644-651.
12. Fricke W.M., Bastin-Shanower S.A., Brill S.J. Substrate specificity of the Saccharomyces cerevisiae Mus81-Mms4 endonuclease. DNA Repair (Amst.) 2005, 4:243-251.
13. Friedenson B. The BRCA1/2 pathway prevents hematologic cancers in addition to breast and ovarian cancers. BMC Cancer. 2007, 7:152.
14. Haber J.E., Debatisse M. Gene amplification: yeast takes a turn. Cell 2006, 125:1237-1240.
15. Harada S., Uchida M., Shimizu N. Episomal high copy number maintenance of hairpin-capped DNA bearing a replication initiation region in human cells. J. Biol. Chem. 2009, 284:24320-24327.
16. Kurahashi H., Inagaki H., Ohye T., Kogo H., Kato T., Emanuel B.S. Palindrome-mediated chromosomal translocations in humans. DNA Repair (Amst.) 2006, 5:1136-1145.
17. Lewis S.M., Coté A.G. Palindromes and genomic stress fractures: bracing and repairing the damage. DNA Repair (Amst.) 2006, 5:1146-1160.
18. Lin C.T., Lyu Y.L., Liu L.F. A cruciform-dumbbell model for inverted dimer formation mediated by inverted repeats. Nucleic Acids Res. 1997, 25:3009-3016.
19. Lin C.T., Lin W.H., Lyu Y.L., Whang-Peng J. Inverted repeats as genetic elements for promoting DNA inverted duplication: implications in gene amplification. Nucleic Acids Res. 2001, 29:3529-3538.
20. 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.
21. Lobachev K.S., Rattray A.J., Narayanan V. Hairpin- and cruciform-mediated chromosome breakage: causes and consequences in eukaryotic cells. Front. Biosci. 2007, 12:4208-4220.
22. Lyu Y.L., Lin C.T., Liu L.F. Inversion/dimerization of plasmids mediated by inverted repeats. J. Mol. Biol. 1999, 285:1485-1501.
23. Malagón F., Aguilera A. Genetic stability and DNA rearrangements associated with a 2 x 1.1-Kb perfect palindrome in Escherichia coli. Mol. Gen. Genet. 1998, 259:639-644.
24. Maringele L., Lydall D. Telomerase- and recombination-independent immortalization of budding yeast. Genes Dev. 2004, 18:2663-2675.
25. McClintock B. The stability of broken ends of chromosomes in Zea Mays. Genetics 1941, 26:234-282.
26. Michel B., Ehrlich S.D., Uzest M. DNA double-strand breaks caused by replication arrest. EMBO J. 1997, 16:430-438.
27. Nakamura K., Okamoto A., Katou Y., Yadani C., Shitanda T., Kaweeteerawat C., Takahashi T.S., Itoh T., Shirahige K., Masukata H., Nakagawa T. Rad51 suppresses gross chromosomal rearrangement at centromere in Schizosaccharomyces pombe. EMBO J. 2008, 27:3036-3046.
28. Narayanan V., Mieczkowski P.A., Kim H.M., Petes T.D., Lobachev K.S. The pattern of gene amplification is determined by the chromosomal location of hairpin-capped breaks. Cell 2006, 125:1283-1296.
29. Oh S.D., Jessop J., Lao J.P., Allers T., Lichten M., Hunter N. Stabilization and electrophoretic analysis of meiotic recombination intermediates in Saccharomyces cerevisiae. Methods Mol. Biol. 2009, 557:209-234.
30. Possoz C., Filipe S.R., Grainge I., Sherratt D.J. Tracking of controlled Escherichia coli replication fork stalling and restart at repressor-bound DNA in vivo. EMBO J. 2006, 25:2596-2604.
31. Qin Z., Cohen S.N. Long palindromes formed in Streptomyces by nonrecombinational intra-strand annealing. Genes Dev. 2000, 14:1789-1796.
32. 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.
33. Rattray A.J., Shafer B.K., Neelam B., Strathern J.N. A mechanism of palindromic gene amplification in Saccharomyces cerevisiae. Genes Dev. 2005, 19:1390-1399.
34. Sambrook J., Fritsh E.F., Maniatis T. Molecular Cloning: a Laboratory Manual 1989, Cold Spring Harbor, New York.
35. Savelyeva L., Claas A., Matzner I., Schlag P., Hofmann W., Scherneck S., Weber B., Schwab M. Constitutional genomic instability with inversions, duplications, and amplifications in 9p23-24 in BRCA2 mutation carriers. Cancer Res. 2001, 61:5179-5185.
36. Sharples G.J. The X philes: structure-specific endonucleases that resolve Holliday junctions. Mol. Microbiol. 2001, 39:823-834.
37. Sinden R.R., Zheng G.X., Brankamp R.G., Allen K.N. On the deletion of inverted repeated DNA in Escherichia coli: effects of length, thermal stability, and cruciform formation in vivo. Genetics 1991, 129:991-1005.
38. Tanaka H., Yao M.C. Palindromic gene amplification-an evolutionarily conserved role for DNA inverted repeats in the genome. Nat. Rev. Cancer 2009, 9:216-224.
39. Tanaka H., Tapscott S.J., Trask B.J., Yao M.C. Short inverted repeats initiate gene amplification through the formation of a large DNA palindrome in mammalian cells. Proc. Natl. Acad. Sci. USA 2002, 99:8772-8777.
40. Tanaka H., Bergstrom D.A., Yao M.C., Tapscott S.J. Widespread and nonrandom distribution of DNA palindromes in cancer cells provides a structural platform for subsequent gene amplification. Nat. Genet. 2005, 37:320-327.
41. Tanaka H., Cao Y., Bergstrom D.A., Kooperberg C., Tapscott S.J., Yao M.C. Intrastrand annealing leads to the formation of a large DNA palindrome and determines the boundaries of genomic amplification in human cancer. Mol. Cell. Biol. 2007, 27:1993-2002.
42. VanHulle K., Lemoine F.J., Narayanan V., Downing B., Hull K., McCullough C., Bellinger M., Lobachev K., Petes T.D., Malkova A. Inverted DNA repeats channel repair of distant double-strand breaks into chromatid fusions and chromosomal rearrangements. Mol. Cell. Biol. 2007, 27:2601-2614.
43. White M.A., Eykelenboom J.K., Lopez-Vernaza M.A., Wilson E., Leach D.R. Non-random segregation of sister chromosomes in Escherichia coli. Nature 2008, 455:1248-1250.
44. Yu V.P., Koehler M., Steinlein C., Schmid M., Hanakahi L.A., van Gool A.J., West S.C., Venkitaraman A.R. Gross chromosomal rearrangements and genetic exchange between nonhomologous chromosomes following BRCA2 inactivation. Genes Dev. 2000, 14:1400-1406.