Recql5 and Blm RecQ DNA helicases have nonredundant roles in suppressing crossovers

Molecular and Cellular Biology

Volumn 25, Issue 9, 2005, Pages 3431-3442

  Hu, Yiduo ^a,b   Lu, Xincheng ^a,b   Barnes, Ellen ^a,b   Yan, Min ^a   Lou, Hua ^a,b   Luo, Guangbin ^a,b  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HELICASE; RECQ HELICASE;

ANIMAL CELL; ARTICLE; BLOOM SYNDROME HOMOLOGUE GENE; CONTROLLED STUDY; CROSSING OVER; DATA ANALYSIS; EMBRYONIC STEM CELL; FIBROBLAST; GENE; GENE DELETION; GENE FUNCTION; GENE MUTATION; GENE REPRESSION; KNOCKOUT MOUSE; MITOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; SISTER CHROMATID EXCHANGE; WILD TYPE;

ADENOSINE TRIPHOSPHATASES; ANIMALS; BLOOM SYNDROME; CROSSING OVER, GENETIC; DNA HELICASES; FIBROBLASTS; GAMMA RAYS; GENE DELETION; GENE SILENCING; GENE TARGETING; MICE; MICE, KNOCKOUT; MITOSIS; RECQ HELICASES; SISTER CHROMATID EXCHANGE; STEM CELLS;

EUKARYOTA; MAMMALIA; SACCHAROMYCES CEREVISIAE;

EID: 17644410077     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.9.3431-3442.2005     Document Type: Article

References (64)

1. 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.
2. 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.
3. 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.
4. 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.
5. 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.
6. 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.
7. Cox, M. M. 2002. The nonmutagenic repair of broken replication forks via recombination. Mutat. Res. 510:107-120.
8. 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.
9. 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.
10. 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.
11. 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.
12. 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.
13. 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.
14. 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.
15. German, J. 1993. Bloom syndrome: a mendelian prototype of somatic mutational disease. Medicine (Baltimore) 72:393-406.
16. German, J. 1995. Bloom's syndrome. Dermatol. Clin. 13:7-18.
17. 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.
18. 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.
19. 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.
20. 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.
21. Haber, J. E. 1999. DNA recombination: the replication connection. Trends Biochem. Sci. 24:271-275.
22. 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.
23. Hassold, T., S. Sherman, and P. Hunt. 2000. Counting cross-overs: characterizing meiotic recombination in mammals. Hum. Mol. Genet. 9:2409-2419.
24. Hickson, I. D. 2003. RecQ helicases: caretakers of the genome. Nat. Rev. Cancer 3:169-178.
25. 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.
26. 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.
27. 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.
28. 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.
29. 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.
30. 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.
31. Knudson, A. G., Jr. 1971. Mutation and cancer: statistical study of retinoblastoma. Proc. Natl. Acad. Sci. USA 68:820-823.
32. Knudson, A. G., Jr. 1978. Retinoblastoma: a prototypic hereditary neoplasm. Semin. Oncol. 5:57-60.
33. 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.
34. Kuzminov, A. 2001. DNA replication meets genetic exchange: chromosomal damage and its repair by homologous recombination. Proc. Natl. Acad. Sci. USA 98:8461-8468.
35. 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.
36. 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.
37. 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.
38. 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.
39. 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.
40. 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.
41. 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.
42. 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.
43. 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.
44. 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.
45. 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.
46. 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.
47. 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.
48. 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.
49. 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.
50. 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.
51. 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.
52. 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.
53. 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.
54. 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.
55. 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.
56. 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.
57. 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.
58. 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.
59. 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.
60. 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.
61. 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.
62. Wu, L., and I. D. Hickson. 2003. The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 426:870-874.
63. 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.
64. 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.