Recql5 and Blm RecQ DNA Helicases Have Nonredundant Roles in Suppressing Crossovers

REFERENCES

• Aladjem, M. I., B. T. Spike, L. W. Rodewald, T. J. Hope, M. Klemm, R. Jaenisch, and G. M. Wahl. 1998. ES cells do not activate p53-dependent stress responses and undergo p53-independent apoptosis in response to DNA damage. Curr. Biol. 8:145–155.
   PubMed Web of Science ®Google Scholar
• Beumer, K. J., S. Pimpinelli, and K. G. Golic. 1998. Induced chromosomal exchange directs the segregation of recombinant chromatids in mitosis of Drosophila. Genetics 150:173–188.
   PubMedGoogle Scholar
• Braybrooke, J. P., J. L. Li, L. Wu, F. Caple, F. E. Benson, and I. D. Hickson. 2003. Functional interaction between the Bloom's syndrome helicase and the RAD51 paralog, RAD51L3 (RAD51D). J. Biol. Chem. 278:48357–48366.
   PubMedGoogle Scholar
• Chaganti, R. S., S. Schonberg, and J. German. 1974. A manyfold increase in sister chromatid exchanges in Bloom's syndrome lymphocytes. Proc. Natl. Acad. Sci. USA 71:4508–4512.
   PubMed Web of Science ®Google Scholar
• Chester, N., F. Kuo, C. Kozak, C. D. O'Hara, and P. Leder. 1998. Stage-specific apoptosis, developmental delay, and embryonic lethality in mice homozygous for a targeted disruption in the murine Bloom's syndrome gene. Genes Dev. 12:3382–3393.
   PubMedGoogle Scholar
• Constantinou, A., M. Tarsounas, J. K. Karow, R. M. Brosh, V. A. Bohr, I. D. Hickson, and S. C. West. 2000. Werner's syndrome protein (WRN) migrates Holliday junctions and co-localizes with RPA upon replication arrest. EMBO Rep. 1:80–84.
   PubMed Web of Science ®Google Scholar
• Cox, M. M. 2002. The nonmutagenic repair of broken replication forks via recombination. Mutat. Res. 510:107–120.
   PubMedGoogle Scholar
• de Vries, W. N., L. T. Binns, K. S. Fancher, J. Dean, R. Moore, R. Kemler, and B. B. Knowles. 2000. Expression of Cre recombinase in mouse oocytes: a means to study maternal effect genes. Genesis 26:110–112.
   PubMedGoogle Scholar
• Ellis, N. A., J. Groden, T. Z. Ye, J. Straughen, D. J. Lennon, S. Ciocci, M. Proytcheva, and J. German. 1995. The Bloom's syndrome gene product is homologous to RecQ helicases. Cell 83:655–666.
   PubMed Web of Science ®Google Scholar
• Essers, J., R. W. Hendriks, S. M. Swagemakers, C. Troelstra, J. de Wit, D. Bootsma, J. H. Hoeijmakers, and R. Kanaar. 1997. Disruption of mouse RAD54 reduces ionizing radiation resistance and homologous recombination. Cell 89:195–204.
   PubMed Web of Science ®Google Scholar
• Essers, J., H. van Steeg, J. de Wit, S. M. Swagemakers, M. Vermeij, J. H. Hoeijmakers, and R. Kanaar. 2000. Homologous and non-homologous recombination differentially affect DNA damage repair in mice. EMBO J. 19:1703–1710.
   PubMed Web of Science ®Google Scholar
• Fukuchi, K., G. M. Martin, and R. J. Monnat, Jr. 1989. Mutator phenotype of Werner syndrome is characterized by extensive deletions. Proc. Natl. Acad. Sci. USA 86:5893–5897.
   PubMedGoogle Scholar
• Gangloff, S., J. P. McDonald, C. Bendixen, L. Arthur, and R. Rothstein. 1994. The yeast type I topoisomerase Top3 interacts with Sgs1, a DNA helicase homolog: a potential eukaryotic reverse gyrase. Mol. Cell. Biol. 14:8391–8398.
   PubMed Web of Science ®Google Scholar
• Garcia, P. L., Y. Liu, J. Jiricny, S. C. West, and P. Janscak. 2004. Hum. RECQ5β, a protein with DNA helicase and strand-annealing activities in a single polypeptide. EMBO J. 23:2882–2891.
   PubMed Web of Science ®Google Scholar
• German, J. 1993. Bloom syndrome: a mendelian prototype of somatic mutational disease. Medicine (Baltimore) 72:393–406.
   PubMed Web of Science ®Google Scholar
• German, J. 1995. Bloom's syndrome. Dermatol. Clin. 13:7–18.
   PubMed Web of Science ®Google Scholar
• German, J., and B. Alhadeff. 1994. Sister chromatic exchange (SCE) analysis, p. 8.6.1–8.6.10. In N. C. Dracopoli, J. L. Haines, B. R. Korf, D. T. Moir, C. C. Morton, C. E. Seidman, J. A. Seidman and D. R. Smith (ed.), Current protocols in human genetics. John Wiley & Sons, New York, N.Y.
   Google Scholar
• Goss, K. H., M. A. Risinger, J. J. Kordich, M. M. Sanz, J. E. Straughen, L. E. Slovek, A. J. Capobianco, J. German, G. P. Boivin, and J. Groden. 2002. Enhanced tumor formation in mice heterozygous for Blm mutation. Science 297:2051–2053.
   PubMedGoogle Scholar
• Guo, G., W. Wang, and A. Bradley. 2004. Mismatch repair genes identified using genetic screens in Blm-deficient embryonic stem cells. Nature 429:891–895.
   PubMed Web of Science ®Google Scholar
• Gupta, P. K., A. Sahota, S. A. Boyadjiev, S. Bye, C. Shao, J. P. O'Neill, T. C. Hunter, R. J. Albertini, P. J. Stambrook, and J. A. Tischfield. 1997. High frequency in vivo loss of heterozygosity is primarily a consequence of mitotic recombination. Cancer Res. 57:1188–1193.
   PubMedGoogle Scholar
• Haber, J. E. 1999. DNA recombination: the replication connection. Trends Biochem. Sci. 24:271–275.
   PubMed Web of Science ®Google Scholar
• Haigis, K. M., and W. F. Dove. 2003. A Robertsonian translocation suppresses a somatic recombination pathway to loss of heterozygosity. Nat. Genet. 33:33–39.
   PubMedGoogle Scholar
• Hassold, T., S. Sherman, and P. Hunt. 2000. Counting cross-overs: characterizing meiotic recombination in mammals. Hum. Mol. Genet. 9:2409–2419.
   PubMedGoogle Scholar
• Hickson, I. D. 2003. RecQ helicases: caretakers of the genome. Nat. Rev. Cancer 3:169–178.
   PubMed Web of Science ®Google Scholar
• Hu, P., S. F. Beresten, A. J. van Brabant, T. Z. Ye, P. P. Pandolfi, F. B. Johnson, L. Guarente, and N. A. Ellis. 2001. Evidence for BLM and topoisomerase IIIα interaction in genomic stability. Hum. Mol. Genet. 10:1287–1298.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Johnson, R. D., and M. Jasin. 2000. Sister chromatid gene conversion is a prominent double-strand break repair pathway in mammalian cells. EMBO J. 19:3398–3407.
   PubMed Web of Science ®Google Scholar
• Karow, J. K., A. Constantinou, J. L. Li, S. C. West, and I. D. Hickson. 2000. The Bloom's syndrome gene product promotes branch migration of holliday junctions. Proc. Natl. Acad. Sci. USA 97:6504–6508.
   PubMed Web of Science ®Google Scholar
• Kitao, S., I. Ohsugi, K. Ichikawa, M. Goto, Y. Furuichi, and A. Shimamoto. 1998. Cloning of two new human helicase genes of the RecQ family: biological significance of multiple species in higher eukaryotes. Genomics 54:443–452.
   PubMed Web of Science ®Google Scholar
• Kitao, S., A. Shimamoto, M. Goto, R. W. Miller, W. A. Smithson, N. M. Lindor, and Y. Furuichi. 1999. Mutations in RECQL4 cause a subset of cases of Rothmund-Thomson syndrome. Nat. Genet. 22:82–84.
   PubMed Web of Science ®Google Scholar
• Knudson, A. G., Jr. 1971. Mutation and cancer: statistical study of retinoblastoma. Proc. Natl. Acad. Sci. USA 68:820–823.
   PubMed Web of Science ®Google Scholar
• Knudson, A. G., Jr. 1978. Retinoblastoma: a prototypic hereditary neoplasm. Semin. Oncol. 5:57–60.
   PubMed Web of Science ®Google Scholar
• Krejci, L., S. Van Komen, Y. Li, J. Villemain, M. S. Reddy, H. Klein, T. Ellenberger, and P. Sung. 2003. DNA helicase Srs2 disrupts the Rad51 presynaptic filament. Nature 423:305–309.
   PubMed Web of Science ®Google Scholar
• Kuzminov, A. 2001. DNA replication meets genetic exchange: chromosomal damage and its repair by homologous recombination. Proc. Natl. Acad. Sci. USA 98:8461–8468.
   PubMedGoogle Scholar
• Lee, E. C., D. Yu, J. Martinez de Velasco, L. Tessarollo, D. A. Swing, D. L. Court, N. A. Jenkins, and N. G. Copeland. 2001. A highly efficient Escherichia coli-based chromosome engineering system adapted for recombinogenic targeting and subcloning of BAC DNA. Genomics 73:56–65.
   PubMed Web of Science ®Google Scholar
• Liu, P., N. A. Jenkins, and N. G. Copeland. 2002. Efficient Cre-loxP-induced mitotic recombination in mouse embryonic stem cells. Nat. Genet. 30:66–72.
   PubMedGoogle Scholar
• Luo, G., I. M. Santoro, L. D. McDaniel, I. Nishijima, M. Mills, H. Youssoufian, H. Vogel, R. A. Schultz, and A. Bradley. 2000. Cancer predisposition caused by elevated mitotic recombination in Bloom mice. Nat. Genet. 26:424–429.
   PubMed Web of Science ®Google Scholar
• Luo, G., M. S. Yao, C. F. Bender, M. Mills, A. R. Bladl, A. Bradley, and J. H. Petrini. 1999. Disruption of mRad50 causes embryonic stem cell lethality, abnormal embryonic development, and sensitivity to ionizing radiation. Proc. Natl. Acad. Sci. USA 96:7376–7381.
   PubMed Web of Science ®Google Scholar
• Mann, M. B., C. A. Hodges, E. Barnes, H. Vogel, T. J. Hassold, and G. Luo. 2005. Defective sister-chromatid cohesion, aneuploidy and cancer predisposition in a mouse model of type II Rothmund-Thomson syndrome. Hum. Mol. Genet. 14:813–825.
   PubMedGoogle Scholar
• McCullough, A. J., and S. M. Berget. 1997. G triplets located throughout a class of small vertebrate introns enforce intron borders and regulate splice site selection. Mol. Cell. Biol. 17:4562–4571.
   PubMedGoogle Scholar
• McDaniel, L. D., N. Chester, M. Watson, A. D. Borowsky, P. Leder, and R. A. Schultz. 2003. Chromosome instability and tumor predisposition inversely correlate with BLM protein levels. DNA Repair (Amsterdam) 2:1387–1404.
   PubMed Web of Science ®Google Scholar
• Moynahan, M. E., and M. Jasin. 1997. Loss of heterozygosity induced by a chromosomal double-strand break. Proc. Natl. Acad. Sci. USA 94:8988–8993.
   PubMed Web of Science ®Google Scholar
• Murray, J. M., H. D. Lindsay, C. A. Munday, and A. M. Carr. 1997. Role of Schizosaccharomyces pombe RecQ homolog, recombination, and checkpoint genes in UV damage tolerance. Mol. Cell. Biol. 17:6868–6875.
   PubMed Web of Science ®Google Scholar
• Nakayama, H., K. Nakayama, R. Nakayama, N. Irino, Y. Nakayama, and P. C. Hanawalt. 1984. Isolation and genetic characterization of a thymineless death-resistant mutant of Escherichia coli K12: identification of a new mutation (recQ1) that blocks the RecF recombination pathway. Mol. Gen. Genet. 195:474–480.
   PubMedGoogle Scholar
• Ohhata, T., R. Araki, R. Fukumura, A. Kuroiwa, Y. Matsuda, and M. Abe. 2001. Cloning, genomic structure and chromosomal localization of the gene encoding mouse DNA helicase RECQL5β. Gene 280:59–66.
   PubMedGoogle Scholar
• Onclercq-Delic, R., P. Calsou, C. Delteil, B. Salles, D. Papadopoulo, and M. Amor-Gueret. 2003. Possible anti-recombinogenic role of Bloom's syndrome helicase in double-strand break processing. Nucleic Acids Res. 31:6272–6282.
   PubMedGoogle Scholar
• Puranam, K. L., and P. J. Blackshear. 1994. Cloning and characterization of RECQL, a potential human homologue of the Escherichia coli DNA helicase RecQ. J. Biol. Chem. 269:29838–29845.
   PubMed Web of Science ®Google Scholar
• Richardson, C., M. E. Moynahan, and M. Jasin. 1998. Double-strand break repair by interchromosomal recombination: suppression of chromosomal translocations. Genes Dev. 12:3831–3842.
   PubMed Web of Science ®Google Scholar
• Sekelsky, J. J., M. H. Brodsky, G. M. Rubin, and R. S. Hawley. 1999. Drosophila and human RecQ5 exist in different isoforms generated by alternative splicing. Nucleic Acids Res. 27:3762–3769.
   PubMed Web of Science ®Google Scholar
• Seki, M., H. Miyazawa, S. Tada, J. Yanagisawa, T. Yamaoka, S. Hoshino, K. Ozawa, T. Eki, M. Nogami, K. Okumura, et al. 1994. Molecular cloning of cDNA encoding human DNA helicase Q1 which has homology to Escherichia coli Rec Q helicase and localization of the gene at chromosome 12p12. Nucleic Acids Res. 22:4566–4573.
   PubMed Web of Science ®Google Scholar
• Shimamoto, A., K. Nishikawa, S. Kitao, and Y. Furuichi. 2000. Human RecQ5β, a large isomer of RecQ5 DNA helicase, localizes in the nucleoplasm and interacts with topoisomerases 3α and 3β. Nucleic Acids Res. 28:1647–1655.
   PubMedGoogle Scholar
• Sieber, O. M., H. Lamlum, M. D. Crabtree, A. J. Rowan, E. Barclay, L. Lipton, S. Hodgson, H. J. Thomas, K. Neale, R. K. Phillips, S. M. Farrington, M. G. Dunlop, H. J. Mueller, M. L. Bisgaard, S. Bulow, P. Fidalgo, C. Albuquerque, M. I. Scarano, W. Bodmer, I. P. Tomlinson, and K. Heinimann. 2002. Whole-gene APC deletions cause classical familial adenomatous polyposis, but not attenuated polyposis or “multiple” colorectal adenomas. Proc. Natl. Acad. Sci. USA 99:2954–2958.
   PubMedGoogle Scholar
• Stewart, E., C. R. Chapman, F. Al-Khodairy, A. M. Carr, and T. Enoch. 1997. rqh1+, a fission yeast gene related to the Bloom's and Werner's syndrome genes, is required for reversible S phase arrest. EMBO J. 16:2682–2692.
   PubMed Web of Science ®Google Scholar
• Traverso, G., C. Bettegowda, J. Kraus, M. R. Speicher, K. W. Kinzler, B. Vogelstein, and C. Lengauer. 2003. Hyper-recombination and genetic instability in BLM-deficient epithelial cells. Cancer Res. 63:8578–8581.
   PubMed Web of Science ®Google Scholar
• Veaute, X., J. Jeusset, C. Soustelle, S. C. Kowalczykowski, E. Le Cam, and F. Fabre. 2003. The Srs2 helicase prevents recombination by disrupting Rad51 nucleoprotein filaments. Nature 423:309–312.
   PubMed Web of Science ®Google Scholar
• Vilenchik, M. M., and A. G. Knudson. 2003. Endogenous DNA double-strand breaks: production, fidelity of repair, and induction of cancer. Proc. Natl. Acad. Sci. USA 100:12871–12876.
   PubMed Web of Science ®Google Scholar
• Wang, W., M. Seki, Y. Narita, T. Nakagawa, A. Yoshimura, M. Otsuki, Y. Kawabe, S. Tada, H. Yagi, Y. Ishii, and T. Enomoto. 2003. Functional relation among RecQ family helicases RecQL1, RecQL5, and BLM in cell growth and sister chromatid exchange formation. Mol. Cell. Biol. 23:3527–3535.
   PubMedGoogle Scholar
• Wang, Y., D. Cortez, P. Yazdi, N. Neff, S. J. Elledge, and J. Qin. 2000. BASC, a super complex of BRCA1-associated proteins involved in the recognition and repair of aberrant DNA structures. Genes Dev. 14:927–939.
   PubMed Web of Science ®Google Scholar
• Watt, P. M., I. D. Hickson, R. H. Borts, and E. J. Louis. 1996. SGS1, a homologue of the Bloom's and Werner's syndrome genes, is required for maintenance of genome stability in Saccharomyces cerevisiae. Genetics 144:935–945.
   PubMed Web of Science ®Google Scholar
• Watt, P. M., E. J. Louis, R. H. Borts, and I. D. Hickson. 1995. Sgs1: a eukaryotic homolog of E. coli RecQ that interacts with topoisomerase II in vivo and is required for faithful chromosome segregation. Cell 81:253–260.
   PubMed Web of Science ®Google Scholar
• Wu, L., S. L. Davies, N. C. Levitt, and I. D. Hickson. 2001. Potential role for the BLM helicase in recombinational repair via a conserved interaction with RAD51. J. Biol. Chem. 276:19375–19381.
   PubMed Web of Science ®Google Scholar
• Wu, L., and I. D. Hickson. 2003. The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 426:870–874.
   PubMed Web of Science ®Google Scholar
• Yu, C. E., J. Oshima, Y. H. Fu, E. M. Wijsman, F. Hisama, R. Alisch, S. Matthews, J. Nakura, T. Miki, S. Ouais, G. M. Martin, J. Mulligan, and G. D. Schellenberg. 1996. Positional cloning of the Werner's syndrome gene. Science 272:258–262.
   PubMed Web of Science ®Google Scholar
• Yu, D., H. M. Ellis, E. C. Lee, N. A. Jenkins, N. G. Copeland, and D. L. Court. 2000. An efficient recombination system for chromosome engineering in Escherichia coli. Proc. Natl. Acad. Sci. USA 97:5978–5983.
   PubMed Web of Science ®Google Scholar