Bloom helicase and DNA topoisomerase IIIα are involved in the dissolution of sister chromatids

Molecular and Cellular Biology

Volumn 26, Issue 16, 2006, Pages 6299-6307

  Seki, Masayuki ^a   Nakagawa, Takayuki ^a   Seki, Takahiko ^a   Kato, Genta ^a   Tada, Shusuke ^a   Takahashi, Yuriko ^a   Yoshimura, Akari ^a   Kobayashi, Takayuki ^a   Aoki, Ayako ^a   Otsuki, Makoto ^a   Habermann, Felix A ^b   Tanabe, Hideyuki ^c   Ishii, Yutaka ^d,e   Enomoto, Takemi ^a  

^a TOHOKU UNIVERSITY   (Japan)

^b UNIVERSITY OF MUNICH   (Germany)

^c GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^d OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^e SHUJITSU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; DNA TOPOISOMERASE; DNA TOPOISOMERASE IIIALPHA; GENE PRODUCT; HELICASE; RECQ HELICASE; UNCLASSIFIED DRUG;

ANAPHASE; ARTICLE; AUTOSOMAL DISORDER; BLM GENE; BLOOM SYNDROME; CELL CYCLE G2 PHASE; CELL NUCLEUS; CHROMOSOME ANALYSIS; CONTROLLED STUDY; DISEASE PREDISPOSITION; GENE; GENE DISRUPTION; GENE INTERACTION; GENE MUTATION; HUMAN; HUMAN CELL; LETHALITY; METAPHASE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SISTER CHROMATID;

2-AMINOPURINE; ADENOSINE TRIPHOSPHATASES; ANAPHASE; ANIMALS; APOPTOSIS; CHICKENS; CHROMATIDS; CHROMOSOME ABERRATIONS; DNA HELICASES; DNA TOPOISOMERASES, TYPE I; G2 PHASE; GENE TARGETING; HUMANS; ISOENZYMES; METAPHASE; MICE; MODELS, GENETIC; MUTATION; PHENOTYPE;

EID: 33746966063     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00702-06     Document Type: Article

References (37)

1. Andreassen, P. R., F. B. Lacroix, and R. L. Margolis. 1997. Chromosomes with two intact axial cores are induced by G2 checkpoint override: evidence that DNA decatenation is not required to template the chromosome structure. J. Cell Biol. 136:29-43.
2. Duno, M., B. Thomsen, O. Westergaard, L. Krejci, and C. Bendixen. 2000. Genetic analysis of the Saccharomyces cerevisiae Sgs1 helicase defines an essential function for the Sgs1-Top3 complex in the absence of SRS2 or TOP1. Mol. Gen. Genet. 264:89-97.
3. 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.
4. Enomoto, T. 2001. Functions of RecQ family helicases: possible involvement of Bloom's and Werner's syndrome gene products in guarding genome integrity during DNA replication. J. Biochem. 129:501-507.
5. 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.
6. German, J. 1993. Bloom syndrome: a Mendelian prototype of somatic mutational disease. Medicine 72:393-406.
7. Habermann, F. A., M. Cremer, J. Walter, G. Kreth, J. von Hase, K. Bauer, J. Wienberg, C. Cremer, T. Cremer, and I. Solovei. 2001. Arrangements of macro- and microchromosomes in chicken cells. Chromosome Res. 9:569-584.
8. Hanai, R., P. R. Caron, and J. C. Wang. 1996. Human TOP3: a single-copy gene encoding DNA topoisomerase III. Proc. Natl. Acad. Sci. USA 93:3653-3657.
9. Hiasa, H., R. J. DiGate, and K. J. Marians. 1994. Decatenating activity of Escherichia coli DNA gyrase and topoisomerases I and III during oriC and pBR322 DNA replication in vitro. J. Biol. Chem. 269:2093-2099.
10. Holm, C., T. Stearns, and D. Botstein. 1989. DNA topoisomerase II must act at mitosis to prevent nondisjunction and chromosome breakage. Mol. Cell. Biol. 9:159-168.
11. Hu, Y., X. Lu, E. Barnes, M. Yan, H. Lou, and G. Luo. 2005. Recq15 and Blm RecQ DNA helicases have nonredundant roles in suppressing crossovers. Mol. Cell. Biol. 25:3431-3442.
12. Imamura, O., K. Fujita, C. Itoh, S. Takeda, Y. Furuichi, and T. Matsumoto. 2002. Werner and Bloom helicases are involved in DNA repair in a complementary fashion. Oncogene 21:954-963.
13. 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.
14. Johnson, F. B., D. B. Lombard, N. F. Neff, M. A. Mastrangelo, W. Dewolf, N. A. Ellis, R. A. Marciniak, Y. Yin, R. Jaenisch, and L. Guarente. 2000. Association of the Bloom syndrome protein with topoisomerase IIIα in somatic and meiotic cells. Cancer Res. 60:1162-1167.
15. Kwan, K. Y., and J. C. Wang. 2001. Mice lacking DNA topoisomerase IIIβ develop to maturity but show a reduced mean lifespan. Proc. Natl. Acad. Sci. USA 98:5717-5721.
16. LeRoy, G., R. Carroll, S. Kyin, M. Seki, and M. D. Cole. 2005. Identification of RecQL1 as a Holliday junction processing enzyme in human cell lines. Nucleic Acids Res. 33:251-6257.
17. Li, W., and J. C. Wang. 1998. Mammalian DNA topoisomerase IIIα is essential in early embryogenesis. Proc. Natl. Acad. Sci. USA 95:010-1013.
18. Liberi, G., G. Maffioletti, C. Lucca, I. Chiolo, A. Baryshnikova, C. Cotta-Ramusino, M. Lopes, A. Pellicioli, J. E. Haber, and M. Foiani. 2005. Rad51-dependent DNA structures accumulate at damaged replication forks in sgs1 mutants defective in the yeast ortholog of BLM RecQ helicase. Genes Dev. 19:39-350.
19. Mullen, J. R., V. Kaliraman, S. S. Ibrahim, and S. J. Brill. 2001. Requirement for three novel protein complexes in the absence of the Sgs1 DNA helicase in Saccharomyces cerevisiae. Genetics 157:03-118.
20. Onodera, R., M. Seki, A. Ui, Y. Satoh, A. Miyajima, F. Onoda, and T. Enomoto. 2002. Functional and physical interaction between Sgs1 and Top3 and Sgs1-independent function of Top3 in DNA recombination repair. Genes Genet. Syst. 77:1-21.
21. Sakaguchi, A., and A. Kikuchi. 2004. Functional compatibility between isoform α and β of type II DNA topoisomerase. J. Cell Sci. 117:047-1054.
22. Seki, T., M. Seki, T. Katada, and T. Enomoto. 1998. Isolation of a cDNA encoding mouse DNA topoisomerase III which is highly expressed at the mRNA level in the testis. Biochim. Biophys. Acta 1396:27-131.
23. Seki, T., M. Seki, R. Onodera, T. Katada, and T. Enomoto. 1998. Cloning of cDNA encoding a novel mouse DNA topoisomerase III (Topo IIIβ) possessing negatively supercoiled DNA relaxing activity, whose message is highly expressed in the testis. J. Biol. Chem. 273:28553-28556.
24. Shimamoto, A., K. Nishikawa, S. Kitao, and Y. Furuichi. 2000. RecQ5β, a large isomer of RecQ5 DNA helicase, localizes in the nucleoplasm and interacts with lopoisomerases 3α and 3β. Nucleic Acids Res. 28:1647-1655.
25. Sonoda, E., M. S. Sasaki, J. M. Buerstedde, O. Bezzubova, A. Shinohara, H. Ogawa, M. Takata, Y. Yamaguchi-Iwai, and S. Takeda. 1998. Rad51-deficient vertebrate cells accumulate chromosomal breaks prior to cell death. EMBO J. 17:598-608.
26. Uemura, T., H. Ohkura, Y. Adachi, K. Morino, K. Shiozaki, and M. Yanagida. 1987. DNA topoisomerase II is required for condensation and separation of mitotic chromosomes in S. pombe. Cell 50:917-925.
27. Ui, A., Y. Satoh, F. Onoda, A. Miyajima, M. Seki, and T. Enomoto. 2001. The N-terminal region of Sgs1, which interacts with Top3, is required for complementation of MMS sensitivity and suppression of hyper-recombination in sgs1 disruptants. Mol. Genet. Genomics 265:837-850.
28. Wallis, J. W., G. Chrebet, G. Brodsky, M. Rolfe, and R. Rothstein. 1989. A hyper-recombination mutation in S. cerevisiae identifies a novel eukaryotic topoisomerase. Cell 58:409-419.
29. Wang, W., M. Seki, Y. Narita, E. Sonoda, S. Takeda, K. Yamada, T. Musuko, T. Katada, and T. Enomoto. 2000. Possible association of BLM in decreasing DNA double strand breaks during DNA replication. EMBO J. 19:3428-3435.
30. 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.
31. Win, T. Z., A. Goodwin, I. D. Hickson, C. J. Norbury, and S. W. Wang. 2004. Requirement for Schizosaccharomyces pombe Top3 in the maintenance of chromosome integrity. J. Cell Sci. 117:4769-4778.
32. Win, T. Z., H. W. Mankouri, I. D. Hickson, and S. W. Wang. 2005. A role for the fission yeast Rqh1 helicase in chromosome segregation. J. Cell Sci. 118:5777-5784.
33. Winding, P., and M. W. Berchtold. 2001. The chicken B cell line DT40: a novel tool for gene disruption experiments. J. Immunol. Methods 249:1-16.
34. Wu, L., and I. D. Hickson. 2003. The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 426:870-874.
35. Wu, L., S. L. Davies, P. S. North, H. Goulaouic, J. F. Riou, H. Turley, K. C. Gatter, and I. D. Hickson. 2000. The Bloom's syndrome gene product interacts with topoisomerase III. J. Biol. Chem. 275:9636-9644.
36. Yamaguchi-Iwai, Y., E. Sonoda, M. S. Sasaki, C. Morrison, T. Haraguchi, Y. Hiraoka, Y. M. Yamashita, T. Yagi, M. Takata, C. Price, N. Kakazu, and S. Takeda. 1999. Mrel1 is essential for the maintenance of chromosomal DNA in vertebrate cells. EMBO J. 18:6619-6629.
37. Yu, C. E., J. Oshima, Y. H. Fu, E. M. Wijsman, F. Hisama, R. Alisch, S. Matthews, J. Nakura, T. Miki, S. Ouais, and G. M. Martin. 1996. Positional cloning of Ihe Werner's syndrome gene. Science 272:258-262.