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DNA Dynamics and Chromosome Structure

Multiple Genetic Pathways Involving the Caenorhabditis elegans Bloom's Syndrome Genes him-6, rad-51, and top-3 Are Needed To Maintain Genome Stability in the Germ Line

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Pages 5016-5027 | Received 15 Dec 2003, Accepted 08 Mar 2004, Published online: 27 Mar 2023

REFERENCES

  • Ababou, M., Dumaire V., Lécluse Y., and Amor-Guéret M.. 2002. Bloom's syndrome protein response to ultraviolet-C radiation and hydroxyurea-mediated DNA synthesis inhibition. Oncogene 21:2079–2088.
  • Adams, M. D., McVey M., and Sekelsky J. J.. 2003. Drosophila BLM in double-strand break repair by synthesis-dependent strand annealing. Science 299:265–267.
  • Ahmed, S., Alpi A., Hengartner M. O., and Gartner A.. 2001. Caenorhabditis elegans RAD-5/CLK-2 defines a new DNA damage checkpoint protein. Curr. Biol. 11:1934–1944.
  • Alpi, A., Pawel P., Gartner A., and Loidl J.. 2003. Genetic and cytological characterization of the recombination protein RAD-51 in Caenorhabditis elegans. Chromosoma 112:6–16.
  • Bishop, D. K., Park D., Xu L., and Kleckner N.. 1992. DMC1: a meiosis-specific yeast homolog of Escherichia coli recA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell 69:439–456.
  • Bjergbaek, L., Cobb J. A., and Gasser S. M.. 2002. RecQ helicases and genome stability: lessons from model organisms and human disease. Swiss Med. Wkly. 132:433–442.
  • Blumenthal, T. 1995. Trans-splicing and polycistronic transcription in Caenorhabditis elegans. Trends Genet. 11:132–136.
  • Boulton, S. J., Gartner A., Reboul J., Vaglio P., Dyson N., Hill D. E., and Vidal M.. 2002. Combined functional genomic maps of the Caenorhabditis elegans DNA damage response. Science 295:127–131.
  • Brenner, S. 1974. The genetics of Caenorhabditis elegans. Genetics 77:71–94.
  • Clark, D. V., and Baillie D. L.. 1992. Genetic analysis and complementation by germ-line transformation of lethal mutations in the unc-22 IV region of Caenorhabditis elegans. Mol. Gen. Genet. 232:97–105.
  • Crow, E. L., and Gardner R. S.. 1959. Confidence intervals for the expectation of a Poisson variable. Biometrika 46:441–453.
  • Dasika, G. K., Lin S. C., Zhao S., Sung P., Tomkinson A., and Lee E. Y.. 1999. DNA damage-induced cell cycle checkpoints and DNA strand break repair in development and tumorigenesis. Oncogene 18:7883–7899.
  • Ellis, N. A., Groden J., Ye T. Z., Straughen J., Lennon D. J., Ciocci S., Proytcheva M., and German J.. 1995. The Bloom's syndrome gene product is homologous to RecQ helicases. Cell 83:655–666.
  • Fire, A., Xu S., Montgomery M. K., Kostas S. A., Driver S. E., and Mello C. C.. 1998. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806–811.
  • Frei, C., and Gasser S. M.. 2000. The yeast Sgs1p helicase acts upstream of Rad53p in the DNA replication checkpoint and colocalizes with Rad53p in S-phase-specific foci. Genes Dev. 14:81–96.
  • Gangloff, S., de Massy B., Arthur L., Rothstein R., and Fabre F.. 1999. The essential role of yeast topoisomerase III in meiosis depends on recombination. EMBO J. 18:1701–1711.
  • Gangloff, S., McDonald J. P., Bendixen C., Arthur L., and Rothstein R.. 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.
  • Gangloff, S., Soustelle C., and Fabre F.. 2000. Homologous recombination is responsible for cell death in the absence of the Sgs1 and Srs2 helicases. Nature Genetics 25:192–194.
  • Gartner, A., Milstein S., Ahmed S., Hodgkin J., and Hengartner M. O.. 2000. A conserved checkpoint pathway mediates DNA damaged-induced apoptosis and cell cycle arrest in Caenorhabditis elegans. Mol. Cell 5:435–443.
  • German, J. 1993. Bloom syndrome: a Mendelian prototype of somatic mutational disease. Medicine 72:393–406.
  • Harmon, F. G., and Kowalczykowski S. C.. 1998. RecQ helicase, in concert with recA and SSB proteins, initiates and disrupts DNA recombination. Genes Dev. 12:1134–1144.
  • Hirao, A., Kong Y.-Y., Matsuoka S., Wakeham A., Ruland J., Yoshida H., Liu D., Elledge S. J., and Mak T. W.. 2000. DNA damage-induced activation of p53 by the checkpoint kinase Chk2. Science 287:1824–1827.
  • Hodgkin, J., Horvitz R., and Brenner S.. 1979. Nondisjunction mutants of the nematode Caenorhabditis elegans. Genetics 91:67–94.
  • Hofmann, E. R., Milstein S., Boulton S. J., Mianjia Y., Hofmann J. J., Stergiou L., Gartner A., Vidal M., and Hengartner M. O.. 2002. Caenorhabditis elegans HUS-1 is a DNA damage checkpoint protein required for genome stability and EGL-1-mediated apoptosis. Curr. Biol. 12:1908–1918.
  • Ira, G., Malkova A., Liberi G., Foiani M., and Haber J. E.. 2003. Srs2 and Sgs1-Top3 suppress crossovers during double-strand break repair in yeast. Cell 115:401–411.
  • Johnson, F. B., Lombard D. B., Neff N. F., Mastrangelo M.-A., Dewolf W., Ellis N. A., Marciniak R. A., Yin Y., Jaenisch R., and Guarente L.. 2000. Association of the Bloom syndrome protein with topoisomerase IIIα in somatic cells and meiotic cells. Cancer Res. 60:1162–1167.
  • Kaneko, H., Orii K. O., Matsui E., Shimozawa N., Fukao T., Matsumoto T., Shimamoto A., Furuichi Y., Hayakawa S., Kasahara K., and Kondo N.. 1997. BLM (the causative gene of Bloom syndrome) protein translocation into the nucleus by a nuclear localization signal. Biochem. Biophys. Res. Commun. 240:348–353.
  • Kelly, K. O., Dernburg A., F., Stanfield G. M., and Villeneuve A., M. 2000. Caenorhabditis elegans msh-5 is required for both normal and radiation-induced meiotic crossing over but not for completion of meiosis. Genetics 156:617–630.
  • Kim, Y. C., Lee J., and Koo H. S.. 2000. Functional characterization of. Caenorhabditis elegans DNA topoisomerase IIIα. Nucleic Acids Res. 28:2012–2017.
  • Kim, Y. C., Lee M. H., Ryu S. S., Kim J. H., and Koo H. S.. 2002. Coaction of DNA topoisomerase IIIα and a RecQ homologue during the germ-line mitosis in Caenorhabditis elegans. Genes Cells 1:19–27.
  • Kitao, S., Shimamoto A., Goto M., Miller R. W., Smithson W. A., Lindor N. M., and Furuichi Y.. 1999. Mutations in RECQL4 cause a subset of cases of Rothmund-Thomson syndrome. Nat. Genet. 22:82–84.
  • Kohara, Y. 1996. Large scale analysis of Caenorhabditis elegans cDNA. Tanpakushitsu Kakusan Koso 41:715–720.
  • Krejci, L., Van Komen S., Li Y., Villemain J., Reddy M. S., Klein H., Ellenberger T., and Sung P.. 2003. DNA helicase Srs2 disrupts the Rad51 presynaptic filament. Nature 423:305–309.
  • Laursen, L. V., Ampatzidou E., Andersen A. H., and Murray J. M.. 2003. Role for the fission yeast RecQ helicase in DNA repair in G2. Mol. Cell. Biol. 10:3692–3705.
  • Lim, D.-S., and Hasty P.. 1996. A mutation in mouse rad51 results in an early embryonic lethal that is suppressed by a mutation in p53. Mol. Cell. Biol. 16:7133–7143.
  • Luo, G., Santoro I. M., McDaniel L. D., Nishijima I., Mills M., Youssoufian H., Vogel H., Schultz R. A., and Bradley A.. 2000. Cancer predisposition caused by elevated mitotic recombination in Bloom mice. Nat. Genet. 26:424–429.
  • MacQueen, A. J., and Villeneuve A. M.. 2001. Nuclear reorganization and homologous chromosome pairing during meiotic prophase require C. elegans chk-2. Genes Dev. 15:1674–1687.
  • Moens, P. B., Freire R., Tarsounas M., Spyropoulos B., and Jackson S. P.. 2000. Expression and nuclear localization of BLM, a chromosome stability protein mutated in Bloom's syndrome, suggest a role in recombination during meiotic prophase. J. Cell Sci. 113:663–672.
  • Morozov, V., Mushegian A. R., Koonin E. V., and Bork P.. 1997. A putative nucleic acid-binding domain in Bloom's and Werner's syndrome helicases. Trends Biochem. Sci. 22:417–418.
  • Myung, K., and Kolodner R. D.. 2002. Suppression of genome instability by redundant S-phase checkpoint pathways in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 99:4500–4507.
  • Nakayama, H., Nakayama K., Nakayama R., Irino N., Nakayama Y., and Hanawalt P. C.. 1984. Isolation and genetic characterization of a thymineless death-resistant mutant of Escherichia coli K-12: identification of a new mutation (recQ1) that blocks the RecF recombination pathway. Mol. Gen. Genet. 195:474–480.
  • Nakayama, K., Irino N., and Nakayama H.. 1985. The recQ gene of Escherichia coli K-12: molecular cloning and isolation of insertion mutants. Mol. Gen. Genet. 200:266–271.
  • Reinke, V., Smith H. E., Nance J., Wang J., Van Doren C., Begley R., Jones S. J., Davis E. B., Scherer S., Ward S., and Kim S. K.. 2000. A global profile of germline gene expression in Caenorhabditis elegans. Mol. Cell 6:605–616.
  • Rinaldo, C., Bazzicalupo P., Ederle S., Hilliard M., and La Volpe A.. 2002. Roles for Caenorhabditis elegans rad-51 in meiosis and in resistance to ionizing radiation during development. Genetics 160:471–479.
  • Rockmill, B., Fung J. C., Branda S. S., and Roeder G. S.. 2003. The Sgs1 helicase regulates chromosome synapsis and meiotic crossing over. Curr. Biol. 13:1954–1962.
  • Roeder, G. S. 1997. Meiotic chromosomes: it takes two to tango. Genes Dev. 11:2600–2621.
  • Rose, A. M., and Baillie D. L.. 1979. Effect of temperature and parental age on recombination and nondisjunction in Caenorhabditis elegans. Genetics 92:409–418.
  • Sambrook, J., Fritsch E. F., and Maniatis T.. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Press, New York, N.Y.
  • Schumacher, B., Hofmann K., Boulton S. J., and Gartner A.. 2001. The Caenorhabditis elegans homolog of the p53 tumor suppressor is required for DNA damage-induced apoptosis. Curr. Biol. 11:1722–1727.
  • Shen, J.-L., and Loeb L. A.. 2000. The Werner syndrome gene. Trends Genet. 16:213–220.
  • Sinclair, D. A., and Guarente L.. 1997. Extrachromosomal rDNA circles: a cause of aging in yeast. Cell 91:1033–1042.
  • Smith, G. R. 1991. Conjugational recombination in Escherichia coli: myths and mechanisms. Cell 64:19–27.
  • Stewart, E., Chapman C. R., Al-Khodairy F., Carr A. M., and Enoch T.. 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.
  • Takanami, T., Sato S., Ishihara T., Katsura I., Takahashi H., and Higashitani A.. 1998. Characterization of a Caenorhabditis elegans recA-like gene, Ce-rdh-1, involved in meiotic recombination. DNA Res. 5:373–377.
  • Tsuzuki, T., Fujii Y., Sakumi K., Tominaga Y., Nakao K., Sekiguchi M., Matsushiro A., Yoshimura Y., and Morita T.. 1996. Targeted disruption of the Rad51 gene leads to lethality in embryonic mice. Proc. Natl. Acad. Sci. USA 93:6236–6240.
  • Veaute, X., Jeusset J., Soustelle C., Kowalczykowski S. C., Le Cam E., and Fabre F.. 2003. The Srs2 helicase prevents recombination by disrupting Rad51 nucleoprotein filaments. Nature 423:309–312.
  • Vennos, E. M., and James W. D.. 1995. Rothmund-Thomson syndrome. Dermat. Clin. 13:143–150.
  • Wang, J. C. 2002. Cellular roles of DNA topoisomerases: a molecular perspective. Nat. Rev. Mol. Cell. Biol. 3:430–440.
  • Wang, X. W., Tseng A., Ellis N. A., Spillare E. A., Linke S. P., Robles A. I., Seker H., Yang Q., Hu P., Beresten S., Bemmels N. A., Garfield S., and Harris C. C.. 2001. Functional interaction of p53 and BLM DNA helicase in apoptosis. J. Biol. Chem. 276:32948–32955.
  • Watt, P. M., Hickson I. D., Borts R. H., and Louis E. J.. 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.
  • Watt, P. M., Louis E. J., Borts R. H., and Hickson I. D.. 1995. Sgs1: a eukaryotic homolog of Escherichia coli RecQ that interacts with topoisomerase II in vivo and is required for faithful chromosome segregation. Cell 81:253–260.
  • Wilson, R., Ainscough R., Anderson K., Baynes C., Berks M., Bonfield J., Burton J., Connell M., Copsey T., Cooper J., et al. 1994. 2.2 Mb of contiguous nucleotide sequence from chromosome III of Caenorhabditis elegans. Nature 368:32–38.
  • Wu, L., and Hickson I. D.. 2001. RecQ helicases and topoisomerases: components of a conserved complex for the regulation of genetic recombination. Cell. Mol. Life Sci. 58:894–901.
  • Wu, L., Sally L. D., Phillip S. N., Goulaouic H., Riou J.-F., Turley H., Gatter K. C., and Hickson I. D.. 2000. The Bloom's syndrome gene product interacts with topoisomerase III. J. Biol. Chem. 275:9636–9644.
  • Xiao, Y., and Weaver D. T.. 1997. Conditional gene targeted deletion by Cre recombinase demonstrates the requirement for the double-strand break repair Mre11 protein in murine embryonic stem cells. Nucleic Acids Res. 25:2985–2991.
  • Yamagata, K., Kato J., Shimamoto A., Goto M., Furuichi Y., and Ikeda H.. 1998. Bloom's and Werner's syndrome genes suppress hyper-recombination in yeast sgs1 mutant: implication for genomic instability in human diseases. Proc. Natl. Acad. Sci. USA 95:8733–8738.
  • Yamaguchi-Iwai, Y., Sonoda E., Sasaki M. S., Morrison C., Haraguchi T., Hiraoka Y., Yamashita Y. M., Yagi T., Takata M., Price C., Kakasu N., and Takeda S.. 1999. Mre11 is essential for the maintenance of chromosomal DNA in vertebrate cells. EMBO J. 18:6619–6629.
  • Yu, C., Oshima J., Fu Y., Wijsman E. M., Hisama F., Alish R., Matthews S., Nakura J., Miki T., Ouais S., Martin G. M., Mulligan J., and Schellenberg G. D.. 1996. Positional cloning of the Werner's syndrome gene. Science 272:258–262.
  • Zetka, M. C., Kawasaki I., Strome S., and Müller F.. 1999. Synapsis and chiasma formation in Caenorhabditis elegans require HIM-3, a meiotic chromosome core component that functions in chromosome segregation. Genes Dev. 13:2258–2270.
  • Zetka, M. C., and Rose A. M.. 1995. Mutant rec-1 eliminates the meiotic pattern of crossing over in Caenorhabditis elegans. Genetics 141:1339–1349.

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