Cell cycle-dependent expression of the mouseRad51 gene in proliferating cells (original) (raw)

Abstract

The mouse_Rad51_ gene is a mammalian homologue of the_Escherichia coli recA_ and yeast_RAD51_ genes, both of which are involved in homologous recombination and DNA repair in mitosis and meiosis. The expression of mouse_Rad51_ mRNA was examined in synchronized mouse m5S cells. The_Rad51_ transcript was observed from late G1 phase through to M phase. During the period of late G1-S-G2, the RAD51 proteins were observed exclusively in nuclei. Activation by mitogens of T cell and B cell proliferation in spleen induced the expression of_Rad51_ mRNA. By immunohistochemical analyses, the mouse RAD51 protein was detected in proliferating cells: spermatogonia in testis, immature T cells in thymus, germinal center cells of the secondary lymphatic nodules of spleen and intestine, follicle cells in ovary and epithelial cells in uterus and intestine. It was also expressed in spermatocytes during early and mid-prophase of meiosis and in resting oocytes before maturation. Thus, mouse_Rad51_ expression is closely related to the state of cell proliferation and is presumably involved in DNA repair coupled with DNA replication, as well as in meiotic DNA recombination in spermatocytes.

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References

• Aboussekhara A, Chanet R, Adjiri A, Fabre F (1992) Semidominant suppressors of Srs2 helicase mutations of_Saccharomyces cerevisiae_ map in the_RAD51_ Gene, whose sequence predicts a protein with similarities to procaryotic RecA proteins. Mol Cell Biol 12:3224–3234
  PubMed Google Scholar
• Adzuma K, Ogawa T, Ogawa T (1984) Primary structure of the_RAD52_ gene in_Saccharomyces cerevisiae_. Mol Cell Biol 4:2735–2744
  PubMed Google Scholar
• Alani E, Padmore R, Kleckner N (1990) Analysis of wild-type and_rad50_ mutants of yeast suggests an intimate relationship between meiotic chromosome synapsis and recombination. Cell 61:419–436
  PubMed Google Scholar
• Basile G, Aker M, Mortimer RK (1992) Nucleotide sequence and transcriptional regulation of the yeast recombinational repair gene_RAD51_. Mol Cell Biol 12:3235–3246
  PubMed Google Scholar
• Benson FE, Stasiak A, West SC (1994) Purification and characterization of the human Rad51 protein, an analogue of_E. coli_ RecA. EMBO J 13:5764–5771
  PubMed Google Scholar
• Bezzubova O, Shinohara A, Mueller RG, Ogawa H, Buerstedde JM (1993) A chicken RAD51 homologue is expressed at high levels in lymphoid and reproductive organs. Nucleic Acids Res 21:1577–1580
  PubMed Google Scholar
• Bishop DK (1994) RecA homologs Dmc1 and Rad51 interact to form multiple nuclear complexes prior to meiotic chromosome synapsis. Cell 79:1081–1092
  PubMed Google Scholar
• Bishop DK, Paark D, Xu L, Kleckner N (1992)DMC1: A meiosis-specific yeast homolog of_E. coli recA_ required for recombination, synaptonemal complex formation, and cell cycle progression. Cell 69:439–456
  PubMed Google Scholar
• Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156–159
  PubMed Google Scholar
• Emery HS, Schild D, Kellogg DE, Mortimer RK (1991) Sequence of_RAD54_, a_Sacchromyces cerevisiae_ gene involved in recombination and repair. Gene 104:103–106
  PubMed Google Scholar
• Habu T, Taki T, West A, Nishimune Y, Morita T (1996) The mouse and human homologs of_DMC1_, the yeast meiosis-specific homologous recombination gene, have a common unique form of exon-skipped transcript in meiosis. Nucleic Acids Res, in press
• Hendrickson EA, Qin XQ, Bump EA, Schatz DG, Oettinger M, Weaver DT (1991) A link between double-strand break-related repair and V(D)J recombination: the_scid_ mutation. Proc Natl Acad Sci USA 88:4061–4065
  PubMed Google Scholar
• Johnson DG, Ohtani K, Nevins JR (1994) Autoregulatory control of_E2F1_ expression in response to positive and negative regulators of cell cycle progression. Genes Dev 8:1514–1525
  PubMed Google Scholar
• Kans JA, Mortimer RK (1991) Nucleotide sequence of the_RAD57_ gene of_Saccharomyces cerevisiae_. Gene 105:139–140
  PubMed Google Scholar
• Kastan MB, Onyekwere O, Sidransky DBV, Craig RW (1991) Participation of p53 protein in the cellular response to DNA damage. Cancer Res 51:6304–6311
  PubMed Google Scholar
• Kastan MB, Zhan Q, El-Deiry W, Carrier GJT, Walsh WV, Plunkett BS, Vogelstein B, Fornace JAJ (1992) A mammalian cell cycle checkpoint pathway utilizing p53 and GADD45 is defective in ataxia telangiectasia. Cell 71:587–597
  PubMed Google Scholar
• Kato H (1974) Possible role of DNA synthesis in formation of sister chromatid exchanges. Nature 252:739–741
  PubMed Google Scholar
• Kowalczykowski SC (1991) Biochemistry of genetic recombination: energetics and mechanism of DNA strand exchange. Annu Rev Biophys Biophys Chem 20:539–575
  PubMed Google Scholar
• Kowalczykowski SC, Eggleston K (1994) Homologous pairing and DNA strand-exchange proteins. Annu Rev Biochem 63:991–1043
  PubMed Google Scholar
• Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (Lond.) 227:680–685
  Google Scholar
• Lalande M (1990) A reversible arrest point in the late G1 phase of the mammalian cell cycle. Exp Cell Res 186:332–339
  PubMed Google Scholar
• Latt SA, Loveday KS (1978) Characterization of sister chromatid exchange induction by 8-methoxypsoralen plus near UV light. Cytogenet Cell Genet 21:184–200
  PubMed Google Scholar
• Lin WC, Desiderio S (1994) Cell cycle regulation of V(D)J recombination-activating protein RAG-2. Proc Natl Acad Sci USA 91:2733–2737
  PubMed Google Scholar
• Lovet ST (1994) Sequence of the_RAD55_ gene of_Saccharomyces cerevisiae_: similarity of RAD55 to prokaryotic RecA and other RecA-like proteins. Gene 142:103–106
  PubMed Google Scholar
• Lu X, Lane DP (1993) Differential induction of transcriptionally active p53 following UV or ionizing radiation: defects in chromosome instability syndromes? Cell 75:765–778
  PubMed Google Scholar
• Miwa M, Sugimura T, Inui N, Takayama S (1973) Poly (adenosine diphosphate ribose) synthesis during the cell cycle of transformed hamster lung cells. Cancer Res 33:1306–1309
  PubMed Google Scholar
• Morita T, Yoshimura Y, Yamamoto A, Murata K, Mori M, Yamamoto H, Matsushiro A (1993) A mouse homolog of the_Escherichia coli recA_ and_Saccharomyces cerevisiae RAD51_ genes. Proc Natl Acad Sci USA 90:6577–6580
  PubMed Google Scholar
• Nishimune Y, Okabe M (1993) Mammalian male gametogenesis: growth, differentiation and maturation of germ cells. Develop Growth Differ 35:479–486
  Google Scholar
• Oettinger MA, Schatz DG, Gorka C, Baltimore D (1990) RAG-1 and RAG-2, adjacent genes that synergistically activate V(D)J Recombination. Science 248:1517–1523
  PubMed Google Scholar
• Ogawa T, Yu X, Shinohara A, Egelman EH (1993) Similarity of the yeast RAD51 filament to the bacterial RecA filament. Science 259:1896–1899
  PubMed Google Scholar
• Papathanasiou M, Fargnoli J, Holbrook NJ (1989) Mammalian genes coordinately regulated by growth arrest signals and DNA-damaging agents. Mol Cell Biol 9:4196–4203
  PubMed Google Scholar
• Radding CM (1991) Helical interactions in homologous pairing and strand exchange driven by RecA protein. J Biol Chem 266:5355–5358
  PubMed Google Scholar
• Sasaki MS, Konama S (1987) Establishment and some mutational characteristics of a 3T3-like, near-diploid mouse cell line. J Cell Physiol 131:114–142
  PubMed Google Scholar
• Shinohara A, Ogawa H, Ogawa T (1992) Rad51 protein involved in repair and recombination in_S. cerevisiae_ is a RecA-like protein. Cell 69:457–470
  PubMed Google Scholar
• Shinohara A, Ogawa H, Matsuda Y, Ushio N, Ikeo K, Ogawa T (1993) Cloning of human, mouse and fission yeast recombination genes homologus to_RAD51_ and_recA_. Nature Genet 4:239–243
  PubMed Google Scholar
• Sittman DB, Graves RA, Marzluff WF (1983) Structure of a cluster of mouse histone genes. Nucleic Acids Res 11:6679–6697
  PubMed Google Scholar
• Story RM, Weber IT, Steitz TA (1992) The structure of the_E. coli recA_ protein monomer and polymer. Nature 355:318–325
  PubMed Google Scholar
• Sung P (1994) Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast RAD51 protein. Science 265:1241–1243
  PubMed Google Scholar
• Taccioli GE, Rathbun G, Oltz E, Stamato T, Jeggo PA, Alt FW (1993) Impairment of V(D)J recombination in double-strand break repair mutants. Science 260:207–210
  PubMed Google Scholar
• Takahashi E, Matsuda Y, Hori T, Yasuda T, Satsuki M, Mori M, Yoshimura Y, Yamamoto A, Morita T, Matsushiro A (1994) Chromosome mapping of the human (RECA) and mouse (Reca) homologs of the yeast_RAD51_ and_Escherichia coli recA_ genes by direct R-banding fluorescence in situ hybridization. Genomics 19:376–378
  PubMed Google Scholar
• Weinert TA, Hartwell LH (1988) The_RAD9_ gene controls the cell cycle response to DNA damage in_Saccharomyces cerevisiae_. Science 241:317–241
  PubMed Google Scholar
• West SC (1992) Enzymes and molecular mechanisms of genetic recombination. Annu Rev Biochem 61:603–640
  PubMed Google Scholar
• West SC (1994) The processing of recombination intermediates: mechanistic insights from studies of bacterial proteins. Cell 76:9–15
  PubMed Google Scholar
• Wong EA, Capecchi MR (1985) Effect of cell cycle position on transformation by microinjection. Somat Cell Mol Genet 11:43–51
  PubMed Google Scholar
• Wong EA, Capecchi MR (1987) Homologous recombination between coinjected DNA sequences peaks in early to mid-S phase. Mol Cell Biol 7:2294–2295
  PubMed Google Scholar
• Yoshimura Y, Morita T, Yamamoto A, Matsushiro A (1993) Cloning and sequence of the human RecA-like gene cDNA. Nucleic Acids Res 21:12
  Google Scholar
• Yu X, Egelman EH (1993) The LexA repressor binds within the deep helical groove of the activated RecA filament. J Mol Biol 231:29–40
  PubMed Google Scholar

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Authors and Affiliations

1. Department of Molecular Embryology, Research Institute for Microbial Diseases, Osaka University, 3-1 Yamadaoka, Suita, 565, Osaka, Japan
   A. Yamamoto, H. Yagi, T. Habu, Y. Yoshimura, A. Matsushiro, Y. Nishimune & T. Morita
2. Department of Neurosurgery, Osaka University Medical School, 2-2 Yamadaoka, Suita, 565, Osaka, Japan
   T. Taki
3. Osaka Women's University, 2-1, Daisen-cho, Sakai, 590, Osaka, Japan
   Kayo Yoshida & Kazuhiko Yamamoto
4. Department of Biotechnology, Faculty of Biological Science, Kinki University, 930 Nishimitani, Uchidacho, Nakagun, 649-64, Wakayama, Japan
   A. Matsushiro

Authors

1. A. Yamamoto
2. H. Yagi
3. T. Habu
4. Y. Yoshimura
5. A. Matsushiro
6. Y. Nishimune
7. T. Morita
8. T. Taki
9. Kayo Yoshida
10. Kazuhiko Yamamoto
11. A. Matsushiro

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Communicated by M. Sekiguchi

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Yamamoto, A., Yagi, H., Habu, T. et al. Cell cycle-dependent expression of the mouse_Rad51_ gene in proliferating cells.Molec. Gen. Genet. 251, 1–12 (1996). https://doi.org/10.1007/BF02174338

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• Received: 23 August 1995
• Accepted: 02 October 1995
• Issue date: April 1996
• DOI: https://doi.org/10.1007/BF02174338

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