Skip to main content

Advertisement

SpringerLink
Log in

Diversity of mechanisms and functions of enzyme systems of DNA repair in Drosophila melanogaster

  • Theoretical Papers and Reviews
  • Published:
Russian Journal of Genetics Aims and scope Submit manuscript

Abstract

The review presents a description and comparative analysis of the known enzymatic systems of DNA repair in Drosophila melanogaster. Data on protein products, mechanisms of action, and the involvement of the repair system elements in other cellular processes are summarized.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Kelner, A., Effect of Visible Light on the Recovery of Streptomyces griseus Conidia from Ultraviolet Irradiation Injury, Proc. Natl. Acad. Sci. USA, 1949, vol. 35, pp. 73–79.

    PubMed  Google Scholar 

  2. Dulbecco, R., Reactivation of Ultraviolet-Inactivated Bacteriophage by Visible Light, Nature, 1949, vol. 163, pp. 949–950.

    Google Scholar 

  3. Sandler, L., Lindsley, D.L., Nicoletti, B., and Trippa, G., Mutants Affecting Meiosis in Natural Populations of Drosophila melanogaster, Genetics, 1968, vol. 60, no. 3, pp. 525–558.

    PubMed  CAS  Google Scholar 

  4. Baker, B.S. and Carpenter, A.T.C., Genetic Analysis of Sex Chromosomal Meiotic Mutants in Drosophila melanogaster, Genetics, 1972, vol. 71, pp. 255–286.

    PubMed  CAS  Google Scholar 

  5. Smith, P.D., Mutagen Sensitivity of Drosophila melanogaster: III. X-Linked Loci Governing Sensitivity to Methyl Methanesulfonate, Mol. Gen. Genet., 1976, vol. 149, no. 1, pp. 73–85.

    Article  PubMed  CAS  Google Scholar 

  6. Boyd, J.B., Golino, M.D., Shaw, K.E., et al., Third-Chromosome Mutagen-Sensitive Mutants of Drosophila melanogaster, Genetics, 1981, vol. 97, nos. 3–4, pp. 607–623.

    PubMed  CAS  Google Scholar 

  7. Henderson, D.S., Bailey, D.A., Sinclair, D.A., and Grigliatti, T.A., Isolation and Characterization of Second Chromosome Mutagen-Sensitive Mutations in Drosophila melanogaster, Mutat. Res., 1987, vol. 177, no. 1, pp. 83–93.

    PubMed  CAS  Google Scholar 

  8. Baker, B.S., Boyd, J.B., Carpenter, A.T.C., et al., Genetic Controls of Meiotic Recombination and Somatic DNA Metabolism in Drosophila melanogaster, Proc. Natl. Acad. Sci. USA, 1976, vol. 73, no. 11, pp. 4140–4144.

    PubMed  CAS  Google Scholar 

  9. Baker, B.S., Carpenter, A.T.C., and Ripoll, P., The Utilization during Mitotic Cell Division of Loci Controlling Meiotic Recombination in Drosophila melanogaster, Genetics, 1978, vol. 90, pp. 531–578.

    Google Scholar 

  10. Gatti, M., Pimpinelli, S., and Baker, B.S., Relationships among Chromatid Interchanges, Sister Chromatid Exchanges, and Meiotic Recombination in Drosophila melanogaster, Proc. Natl. Acad. Sci. USA, 1980, vol. 77, no. 3, pp. 1575–1579.

    PubMed  CAS  Google Scholar 

  11. Omel’yanchuk, L.V., Genetic Strategies of Studying the Cell Cycle in Drosophila melanogaster, Doctoral (Biol.) Dissertation, Novosibirsk: Inst. Cytol. Genet., 1999.

    Google Scholar 

  12. Sekelsky, J.J., Burtis, K.C., and Hawley, R.S., Damage Control: The Pleiotropy of DNA Repair Genes in Drosophila melanogaster, Genetics, 1998, vol. 148, no. 4, pp. 1587–1598.

    PubMed  CAS  Google Scholar 

  13. Brodsky, M.H., Sekelsky, J.J., Tsang, G., et al., mus304 Encodes a Novel DNA Damage Checkpoint Protein Required during Drosophila Development, Genes Dev., 2000, vol. 14, no. 6, pp. 666–678.

    PubMed  CAS  Google Scholar 

  14. Yildiz, O., Majumder, S., Kramer, B., and Sekelsky, J.J., Drosophila MUS312 Interacts with the Nucleotide Excision Repair Endonuclease MEI-9 to Generate Meiotic Crossovers, Mol. Cell, 2002, vol. 10, no. 6, pp. 1503–1509.

    Article  PubMed  CAS  Google Scholar 

  15. Heyer, W.D., Ehmsen, K.T., and Solinger, J.A., Holliday Junction in the Eukaryotic Nucleus: Resolution in Sight, Trends Biochem. Sci., 2003, vol. 28, no. 10, pp. 548–557.

    Article  PubMed  CAS  Google Scholar 

  16. Fujikawa, K. and Kondo, S., DNA Repair Dependence of Somatic Mutagenesis of Transposon-Caused white Alleles in Drosophila melanogaster after Treatment with Alkylating Agents, Genetics, 1986, vol. 112, no. 3, pp. 505–522.

    PubMed  CAS  Google Scholar 

  17. Margulies, L., A High Level of Hybrid Dysgenesis in Drosophila: High Thermosensitivity, Dependence on DNA Repair, and Incomplete Cytotype Regulation, Mol. Gen. Genet., 1990, vol. 220, no. 3, pp. 448–455.

    Article  PubMed  CAS  Google Scholar 

  18. Banga, S.S., Velazquez, A., and Boyd, J.B., P Transposition in Drosophila Provides a New Tool for Analyzing Postreplication Repair and Double-Strand Break Repair, Mutat. Res., 1991, vol. 255, no. 1, pp. 79–88.

    PubMed  CAS  Google Scholar 

  19. Koromyslov, Yu.A., Chmuzh, E.V., Shestakova, L.A., et al., Mutability of Unstable Sex-Linked Alleles of Drosophila melanogaster and Their Interaction with Mutations of the Genes of the Repair System, Dros. Inf. Serv., 2004, no. 86, p. 35.

  20. Yasui, A., Eker, A.P.M., Yasuhira, S., et al., A New Class of DNA Photolyases Present in Various Organisms Including Aplacental Mammals, EMBO J., 1994, vol. 13, no. 24, pp. 6143–6151.

    PubMed  CAS  Google Scholar 

  21. Sancar, A., No “End of History” for Photolyases, Science, 1996, vol. 272, no. 5258, pp. 48–49.

    PubMed  CAS  Google Scholar 

  22. Todo, T., Functional Diversity of the DNA Photolyase/Blue Light Receptor Family, Mutat. Res., 1999, vol. 434, no. 2, pp. 89–97.

    PubMed  CAS  Google Scholar 

  23. Thoma, F., Light and Dark in Chromatin Repair: Repair of UV-Induced DNA Lesions by Photolyase and Nucleotide Excision Repair, EMBO J., 1999, vol. 18, no. 23, pp. 6585–6598.

    Article  PubMed  CAS  Google Scholar 

  24. Pegg, A.E., Dolan, M.E., and Moschel, R.C., Structure, Function, and Inhibition of O6-Alkylguanine-DNA-Alkyltransferase, Prog. Nucleic Acid Res. Mol. Biol., 1995, vol. 51, pp. 167–223.

    PubMed  CAS  Google Scholar 

  25. Soifer, V.N., Repair of Genetic Lesions, Soros. Obrazovat. Zh., 1997, no. 8, pp. 4–13.

  26. Potter, P.M., Wilkinson, M.C., Fitton, J., et al., Characterization and Nucleotide Sequence of ogt, the O6-Alkylguanine-DNA-Alkyltransferase Gene of E. coli, Nucleic Acids Res., 1987, vol. 15, no. 22, pp. 9177–9193.

    PubMed  CAS  Google Scholar 

  27. Xiao, W., Derfler, B., Chen, J., and Samson, L., Primary Sequence and Biological Functions of a Saccharomyces cerevisiae O6-Methylguanine/O4-Methylthymine DNA Repair Methyltransferase Gene, EMBO J., 1991, vol. 10, no. 8, pp. 2179–2186.

    PubMed  CAS  Google Scholar 

  28. Potter, P.M., Rafferty, J.A., Cawkwell, L., et al., Isolation and cDNA Cloning of a Rat O6-Alkylguanine-DNA-Alkyltransferase Gene, Molecular Analysis of Expression in Rat Liver, Carcinogenesis, 1991, vol. 12, no. 4, pp. 727–733.

    PubMed  CAS  Google Scholar 

  29. Kooistra, R., Zonneveld, J.B., Watson, A.J., et al., Identification and Characterization of the Drosophila melanogaster O6-Alkylguanine-DNA-Alkyltransferase cDNA, Nucleic Acids Res., 1999, vol. 27, no. 8, pp. 1795–1801.

    Article  PubMed  CAS  Google Scholar 

  30. Lindahl, T., Sedgwick, B., Sekiguchi, M., and Nakabeppu, Y., Regulation and Expression of the Adaptive Response to Alkylating Agents, Annu. Rev. Biochem., 1988, vol. 57, pp. 133–157.

    Article  PubMed  CAS  Google Scholar 

  31. Graves, R.J., Li, B.F., and Swann, P.F., Repair of O6-Methylguanine, O6-Ethylguanine, O6-Isopropylguanine, and O4-Methylthymine in Synthetic Oligodeoxynucleotides by Escherichia coli ada Gene O6-Alkylguanine DNA-Alkyltransferase, Carcinogenesis, 1989 vol. 10, no. 4, pp. 661–666.

    PubMed  CAS  Google Scholar 

  32. Green, D.A. and Deutsch, W.A., Repair of Alkylated DNA: Drosophila Have DNA Methyltransferases but Not DNA Glycosylases, Mol. Gen. Genet., 1983, vol. 192, no. 3, pp. 322–325.

    Article  PubMed  CAS  Google Scholar 

  33. Guzder, S.N., Kelley, M.R., and Deutsch, W.A., Drosophila Methyltransferase Activity and the Repair of Alkylated DNA, Mutat. Res., 1991, vol. 255, no. 2, pp. 143–153.

    PubMed  CAS  Google Scholar 

  34. Deutsch, W.A. and Spiering, A.L., Characterization of a Depurinated-DNA Purine-Base-Insertion Activity from Drosophila, Biochem. J., 1985, vol. 232, no. 1, pp. 285–288.

    PubMed  CAS  Google Scholar 

  35. Mitzel-Landbeck, L., Schutz, G., and Hagen, U., In Vitro Repair of Radiation-Induced Strand Breaks in DNA, Biochem. Biophys. Acta, 1976, vol. 432, no. 2, pp. 145–153.

    PubMed  CAS  Google Scholar 

  36. Lindahl, T. and Wood, R.D., Quality Control by DNA Repair, Science, 1999, vol. 286, no. 5446, pp. 1897–1905.

    Article  PubMed  CAS  Google Scholar 

  37. Deutsch, W.A., Yacoub, A., Jaruga, P., et al., Characterization and Mechanism of Action of Drosophila Ribosomal Protein S3 DNA Glycosylase Activity for the Removal of Oxidatively Damaged DNA Bases, J. Biol. Chem., 1997, vol. 272, no. 52, pp. 32 857–32 860.

    Article  CAS  Google Scholar 

  38. Dherin, C., Dizdaroglu, M., Doerflinger, H., et al., Repair of Oxidative DNA Damage in Drosophila melanogaster: Identification and Characterization of dOgg1, a Second DNA Glycosylase Activity for 8-Hydroxyguanine and Formamidopyrimidines, Nucleic Acids Res., 2000, vol. 28, no. 23, pp. 4583–4592.

    Article  PubMed  CAS  Google Scholar 

  39. Hardeland, U., Bentele, M., Jiricny, J., and Schar, P., The Versatile Thymine DNA-Glycosylase: A Comparative Characterization of the Human, Drosophila and Fission Yeast Orthologs, Nucleic Acids Res., 2003, vol. 31, no. 9, pp. 2261–2271.

    Article  PubMed  CAS  Google Scholar 

  40. Yacoub, A., Kelley, M.R., and Deutsch, W.A., Drosophila Ribosomal Protein PO Contains Apurinic/Apyrimidinic Endonuclease Activity, Nucleic Acids Res., 1996, vol. 24, no. 21, pp. 4298–4303.

    Article  PubMed  CAS  Google Scholar 

  41. Krokan, H.E., Standal, R., and Slupphaug, G., DNA Glycosylases in the Base Excision Repair of DNA, Biochem. J., 1997, vol. 325, no. 1, pp. 1–16.

    PubMed  CAS  Google Scholar 

  42. Mol, C.D., Parikh, S.S., Putnam, C.D., et al., DNA Repair Mechanisms for the Recognition and Removal of Damaged DNA Bases, Annu. Rev. Biophys. Biomol. Struct., 1999, vol. 28, pp. 101–128.

    Article  PubMed  CAS  Google Scholar 

  43. Krokan, H.E., Nilsen, H., Skorpen, F., et al., Base Excision Repair of DNA in Mammalian Cells, FEBS Lett., 2000, vol. 476, nos. 1–2, pp. 73–77.

    PubMed  CAS  Google Scholar 

  44. Sekelsky, J.J., Brodsky, M.H., and Burtis, K.C., DNA Repair in Drosophila: Insights from the Drosophila Genome Sequence, J. Cell Biol., 2000, vol. 150, no. 2, pp. F31–F36.

    Article  PubMed  CAS  Google Scholar 

  45. Sandigursky, M., Yacoub, A., Kelley, M.R., et al., The Drosophila Ribosomal Protein S3 Contains a DNA Deoxyribophosphodiesterase (dRpase) Activity, J. Biol. Chem., 1997, vol. 272, no. 28, pp. 17 480–17 484.

    Article  CAS  Google Scholar 

  46. Sobol, R.W., Horton, J.K., Kuhn, R., et al., Requirement of Mammalian DNA Polymerase-Beta in Base-Excision Repair, Nature, 1996, vol. 379, no. 6561, pp. 183–186.

    Article  PubMed  CAS  Google Scholar 

  47. Dianov, G.L., Prasad, R., Wilson, S.H., and Bohr, V.A., Role of DNA Polymerase β in the Excision Step of Long Patch Mammalian Base Excision Repair, J. Biol. Chem., 1999, vol. 274, no. 20, pp. 13 741–13 743.

    Article  CAS  Google Scholar 

  48. Miura, M., Watanabe, H., Okochi, K., et al., Biological Response to Ionizing Radiation in Mouse Embryo Fibroblasts with a Targeted Disruption of the DNA Polymerase β Gene, Radiat. Res., 2000, vol. 153, no. 6, pp. 773–780.

    PubMed  CAS  Google Scholar 

  49. Eisen, J.A. and Hanawalt, P.C., A Phylogenomic Study of DNA Repair Genes, Proteins, and Processes, Mutat. Res., 1999, vol. 435, no. 3, pp. 171–213.

    PubMed  CAS  Google Scholar 

  50. Aboussekhra, A., Biggerstaff, M., Shivji, M.K., et al., Mammalian DNA Nucleotide Excision Repair Reconstituted with Purified Protein Components, Cell (Cambridge, Mass.), 1995, vol. 80, no. 6, pp. 859–868.

    CAS  Google Scholar 

  51. Mu, D., Hsu, D.S., and Sancar, A., Reaction Mechanism of Human DNA Repair Excision Nuclease, J. Biol. Chem., 1996, vol. 271, no. 14, pp. 8285–8294.

    PubMed  CAS  Google Scholar 

  52. Mu, D., Park, C.H., Matsunaga, T., et al., Reconstitution of Human DNA Repair Excision Nuclease in a Highly Defined System, J. Biol. Chem., 1995, vol. 270, no. 6, pp. 2415–2418.

    PubMed  CAS  Google Scholar 

  53. Asahina, H., Kuraoka, I., Shirakawa, M., et al., The XPA Protein Is a Zinc Metalloprotein with an Ability to Recognize Various Kinds of DNA Damage, Mutat. Res., 1994, vol. 315, no. 3, pp. 229–237.

    PubMed  CAS  Google Scholar 

  54. He, Z., Henricksen, L.A., Wold, M.S., and Ingles, C.J., RPA Involvement in the Damage-Recognition and Incision Steps of Nucleotide Excision Repair, Nature, 1995, vol. 374, no. 6522, pp. 566–569.

    Article  PubMed  CAS  Google Scholar 

  55. Burns, J.L., Guzder, S.N., Sung, P., et al., An Affinity of Human Replication Protein A for Ultraviolet-Damaged DNA, J. Biol. Chem., 1996, vol. 271, no. 20, pp. 11 607–11 610.

    CAS  Google Scholar 

  56. Drapkin, R. and Reinberg, D., The Multifunctional TFIIH Complex and Transcriptional Control, Trends Biochem. Sci., 1994, vol. 19, no. 11, pp. 504–508.

    Article  PubMed  CAS  Google Scholar 

  57. Drapkin, R., Reardon, J.T., Ansari, A., et al., Dual Role of TFIIH in DNA Excision Repair and in Transcription by RNA Polymerase II, Nature, 1994, vol. 368, no. 6473, pp. 769–772.

    Article  PubMed  CAS  Google Scholar 

  58. Schaeffer, L., Moncollin, V., Roy, R., et al., The ERCC2/DNA Repair Protein Is Associated with the Class II BTF2/TFIIH Transcription Factor, EMBO J., 1994, vol. 13, no. 10, pp. 2388–2392.

    PubMed  CAS  Google Scholar 

  59. Schaeffer, L., Roy, R., Humbert, S., et al., DNA Repair Helicase: A Component of BTF2 (TFIIH) Basic Transcription Factor, Science, 1993, vol. 260, no. 5104, pp. 58–63.

    PubMed  CAS  Google Scholar 

  60. O’Donovan, A., Davies, A.A., Moggs, J.G., et al., XPG Endonuclease Makes the 3′ Incision in Human DNA Nucleotide Excision Repair, Nature, 1994, vol. 371, no. 6496, pp. 432–435.

    PubMed  CAS  Google Scholar 

  61. Matsunaga, T., Mu, D., Park, C.H., et al., Human DNA Repair Excision Nuclease: Analysis of the Roles of the Subunits Involved in Dual Incisions by Using Anti-XPG and Anti-ERCC1 Antibodies, J. Biol. Chem., 1995, vol. 270, no. 35, pp. 20 862–20 869.

    CAS  Google Scholar 

  62. Matsunaga, T., Park, C.H., Bessho, T., et al., Replication Protein A Confers Structure-Specific Endonuclease Activities to the XPF-ERCC1 and XPG Subunits of Human DNA Repair Excision Nuclease, J. Biol. Chem., 1996, vol. 271, no. 19, pp. 11 047–11 050.

    CAS  Google Scholar 

  63. Shivji, M.K., Podust, V.N., Hubscher, U., and Wood, R.D., Nucleotide Excision Repair DNA Synthesis by DNA Polymerase ε in the Presence of PCNA, RFC, and RPA, Biochemistry, 1995, vol. 34, no. 15, pp. 5011–5017.

    Article  PubMed  CAS  Google Scholar 

  64. Shimamoto, T., Tanimura, T., Yoneda, Y., et al., Expression and Functional Analyses of the Dxpa Gene, the Drosophila Homolog of the Human Excision Repair Gene XPA, J. Biol. Chem., 1995, vol. 270, no. 38, pp. 22 452–22 459.

    CAS  Google Scholar 

  65. Mounkes, L.C., Jones, R.S., Liang, B.C., et al., A Drosophila Model for Xeroderma Pigmentosum and Cockayne’s Syndrome: haywire Encodes the Fly Homolog of ERCC3, a Human Excision Repair Gene, Cell (Cambridge, Mass.), 1992, vol. 71, no. 6, pp. 925–937.

    CAS  Google Scholar 

  66. Reynaud, E., Lomeli, H., Vazquez, M., and Zurita, M., The Drosophila melanogaster Homolog of the Xeroderma Pigmentosum D Gene Product Is Located in Euchromatic Regions and Has a Dynamic Response to UV Light-Induced Lesions in Polytene Chromosomes, Mol. Biol. Cell, 1999, vol. 10, no. 4, pp. 1191–1203.

    PubMed  CAS  Google Scholar 

  67. Sekelsky, J.J., McKim, K.S., Chin, G.M., and Hawley, R.S., The Drosophila Meiotic Recombination Gene mei-9 Encodes a Homolog of the Yeast Excision Repair Protein Rad1, Genetics, 1995, vol. 141, no. 2, pp. 619–627.

    PubMed  CAS  Google Scholar 

  68. Brookman, K.W., Lamerdin, J.E., Thelen, M.P., et al., ERCC4 (XPF) Encodes a Human Nucleotide Excision Repair Protein with Eukaryotic Recombination Homologs, Mol. Cell. Biol., 1996, vol. 16, no. 11, pp. 6553–6562.

    PubMed  CAS  Google Scholar 

  69. Sekelsky, J.J., Hollis, K.J., Eimerl, A.I., et al., Nucleotide Excision Repair Endonuclease Genes in Drosophila melanogaster, Mutat. Res., 2000, vol. 459, no. 3, pp. 219–228.

    PubMed  CAS  Google Scholar 

  70. Lahue, R.S., Au, K.G., and Modrich, P., DNA Mismatch Correction in a Defined System, Science, 1989, vol. 245, no. 4914, pp. 160–164.

    PubMed  CAS  Google Scholar 

  71. Modrich, P., Mechanisms and Biological Effects of Mismatch Repair, Annu. Rev. Genet., 1991, vol. 25, pp. 229–253.

    Article  PubMed  CAS  Google Scholar 

  72. Modrich, P. and Lahue, R., Mismatch Repair in Replication Fidelity, Genetic Recombination, and Cancer Biology, Annu. Rev. Biochem., 1996, vol. 65, pp. 101–133.

    Article  PubMed  CAS  Google Scholar 

  73. Wagner, R., Jr. and Meselson, M., Repair Tracts in Mismatched DNA Heteroduplexes, Proc. Natl. Acad. Sci. USA, 1976, vol. 73, no. 11, pp. 4135–4139.

    PubMed  CAS  Google Scholar 

  74. Jiricny, J., Replication Errors: Challenging the Genome, EMBO J., 1998, vol. 17, no. 22, pp. 6427–6436.

    Article  PubMed  CAS  Google Scholar 

  75. Dao, V. and Modrich, P., Mismatch-, MutS-, MutL-, and Helicase II-Dependent Unwinding from the Single-Strand Break of an Incised Heteroduplex, J. Biol. Chem., 1998, vol. 273, no. 15, pp. 9202–9207.

    Article  PubMed  CAS  Google Scholar 

  76. Yamaguchi, M., Dao, V., and Modrich, P., MutS and MutL Activate DNA Helicase II in a Mismatch-Dependent Manner, J. Biol. Chem., 1998, vol. 273, no. 15, pp. 9197–9201.

    Article  PubMed  CAS  Google Scholar 

  77. Jones, M., Wagner, R., and Radman, M., Repair of a Mismatch Is Influenced by the Base Composition of the Surrounding Nucleotide Sequence, Genetics, 1987, vol. 115, no. 4, pp. 605–610.

    PubMed  CAS  Google Scholar 

  78. Kolodner, R., Biochemistry and Genetics of Eukaryotic Mismatch Repair, Genes Dev., 1996, vol. 10, no. 12, pp. 1433–1442.

    PubMed  CAS  Google Scholar 

  79. Buermeyer, A.B., Deschenes, S.M., Baker, S.M., and Liskay, R.M., Mammalian DNA Mismatch Repair, Annu. Rev. Genet., 1999, vol. 33, pp. 533–564.

    Article  PubMed  CAS  Google Scholar 

  80. Flores, C. and Engels, W., Microsatellite Instability in Drosophila spellchecker1 (MutS Homolog) Mutants, Proc. Natl. Acad. Sci. USA, 1999, vol. 96, no. 6, pp. 2964–2969.

    Article  PubMed  CAS  Google Scholar 

  81. Marsischky, G.T., Filosi, N., Kane, M.F., and Kolodner, R., Redundancy of Saccharomyces cerevisiae MSH3 and MSH6 in MSH2-Dependent Mismatch Repair, Genes Dev., 1996, vol. 10, no. 4, pp. 407–420.

    PubMed  CAS  Google Scholar 

  82. Li, G.M. and Modrich, P., Restoration of Mismatch Repair to Nuclear Extracts of H6 Colorectal Tumor Cells by a Heterodimer of Human MutL Homologs, Proc. Natl. Acad. Sci. U.S.A., 1995, vol. 92, no. 6, pp. 1950–1954.

    PubMed  CAS  Google Scholar 

  83. Carpenter, A.T., Mismatch Repair, Gene Conversion, and Crossing-Over in Two Recombination-Defective Mutants of Drosophila melanogaster, Proc. Natl. Acad. Sci. USA, 1982, vol. 79, no. 19, pp. 5961–5965.

    PubMed  CAS  Google Scholar 

  84. Bhui-Kaur, A., Goodman, M.F., and Tower, J., DNA Mismatch Repair by Extracts of Mitotic, Postmitotic, and Senescent Drosophila Tissues and Involvement of mei-9 Gene Function for Full Activity, Mol. Cell. Biol., 1998, vol. 18, no. 3, pp. 1436–1443.

    PubMed  CAS  Google Scholar 

  85. Holmes, J., Jr., Clark, S., and Modrich, P., Strand-Specific Mismatch Correction in Nuclear Extracts of Human and Drosophila melanogaster Cell Lines, Proc. Natl. Acad. Sci. USA, 1990, vol. 87, no. 15, pp. 5837–5841.

    PubMed  CAS  Google Scholar 

  86. Thomas, D.C., Roberts, J.D., and Kunkel, T.A., Heteroduplex Repair in Extracts of Human HeLa Cells, J. Biol. Chem., 1991, vol. 266, no. 6, pp. 3744–3751.

    PubMed  CAS  Google Scholar 

  87. Au, K.G., Welsh, K., and Modrich, P., Initiation of Methyl-Directed Mismatch Repair, J. Biol. Chem., 1992, vol. 267, no. 17, pp. 12 142–12 148.

    CAS  Google Scholar 

  88. Balganesh, T.S. and Lacks, S.A., Heteroduplex DNA Mismatch Repair System of Streptococcus pneumoniae: Cloning and Expression of the hexA Gene, J. Bacteriol., 1985, vol. 162, no. 3, pp. 979–984.

    PubMed  CAS  Google Scholar 

  89. Umar, A., Buermeyer, A.B., Simon, J.A., et al., Requirement for PCNA in DNA Mismatch Repair at a Step Preceding DNA Resynthesis, Cell (Cambridge, Mass.), 1996, vol. 87, no. 1, pp. 65–73.

    CAS  Google Scholar 

  90. Gu, L., Hong, Y., McCulloch, S., et al., ATP-Dependent Interaction of Human Mismatch Repair Proteins and Dual Role of PCNA in Mismatch Repair, Nucleic Acids Res., 1998, vol. 26, no. 5, pp. 1173–1178.

    Article  PubMed  CAS  Google Scholar 

  91. Longley, M.J., Pierce, A.J., and Modrich, P., DNA Polymerase δ Is Required for Human Mismatch Repair in Vitro, J. Biol. Chem., 1997, vol. 272, no. 16, pp. 10 917–10 921.

    CAS  Google Scholar 

  92. Tishkoff, D.X., Boerger, A.L., Bertrand, P., et al., Identification and Characterization of Saccharomyces cerevisiae EXO1, a Gene Encoding an Exonuclease that Interacts with MSH2, Proc. Natl. Acad. Sci. USA, 1997, vol. 94, no. 14, pp. 7487–7492.

    Article  PubMed  CAS  Google Scholar 

  93. Lin, Y.L., Shivji, M.K., Chen, C., et al., The Evolutionarily Conserved Zinc Finger Motif in the Largest Subunit of Human Replication Protein A Is Required for DNA Replication and Mismatch Repair but Not for Nucleotide Excision Repair, J. Biol. Chem., 1998, vol. 273, no. 3, pp. 1453–1461.

    Article  PubMed  CAS  Google Scholar 

  94. Umezu, K., Sugawara, N., Chen, C., et al., Genetic Analysis of Yeast RPA1 Reveals Its Multiple Functions in DNA Metabolism, Genetics, 1998, vol. 148, no. 3, pp. 989–1005.

    PubMed  CAS  Google Scholar 

  95. Lankenau, D.H. and Gloor, G.B., In Vivo Gap Repair in Drosophila: A One-Way Street with Many Destinations, BioEssays, 1998, vol. 20, no. 4, pp. 317–327.

    Article  PubMed  CAS  Google Scholar 

  96. Lambert, S., Saintigny, Y., Delacote, F., et al., Analysis of Intrachromosomal Homologous Recombination in Mammalian Cell, Using Tandem Repeat Sequences, Mutat. Res., 1999, vol. 433, no. 3, pp. 159–168.

    PubMed  CAS  Google Scholar 

  97. Paques, F. and Haber, J.E., Multiple Pathways of Recombination Induced by Double-Strand Breaks in Saccharomyces cerevisiae, Microbiol. Mol. Biol. Rev., 1999, vol. 63, no. 2, pp. 349–404.

    PubMed  CAS  Google Scholar 

  98. Pastink, A., Eeken, J.C., and Lohman, P.H., Genomic Integrity and the Repair of Double-Strand DNA Breaks, Mutat. Res., 2001, vols. 480–481, pp. 37–50.

    PubMed  Google Scholar 

  99. Fishman-Lobell, J., Rudin, N., and Haber, J.E., Two Alternative Pathways of Double-Strand Break Repair That Are Kinetically Separable and Independently Modulated, Mol. Cell. Biol., 1992, vol. 12, no. 3, pp. 1292–1303.

    PubMed  CAS  Google Scholar 

  100. Ivanov, E.L., Sugawara, N., Fishman-Lobell, J., and Haber, J.E., Genetic Requirements for the Single-Strand Annealing Pathway of Double-Strand Break Repair in Saccharomyces cerevisiae, Genetics, 1996, vol. 142, no. 3, pp. 693–704.

    PubMed  CAS  Google Scholar 

  101. Lambert, S. and Lopez, B.S., Characterization of Mammalian RAD51 Double Strand Break Repair Using Non-Lethal Dominant-Negative Forms, EMBO J., 2000, vol. 19, no. 12, pp. 3090–3099.

    Article  PubMed  CAS  Google Scholar 

  102. Fiorenza, M.T., Bevilacqua, A., Bevilacqua, S., and Mangia, F., Growing Dictyate Oocytes, but Not Early Preimplantation Embryos, of the Mouse Display High Levels of DNA Homologous Recombination by Single-Strand Annealing and Lack DNA Nonhomologous End Joining, Dev. Biol., 2001, vol. 233, no. 1, pp. 214–224.

    Article  PubMed  CAS  Google Scholar 

  103. Saintigny, Y., Delacote, F., Vares, G., et al., Characterization of Homologous Recombination Induced by Replication Inhibition in Mammalian Cells, EMBO J., 2001, vol. 20, no. 14, pp. 3861–3870.

    Article  PubMed  CAS  Google Scholar 

  104. Featherstone, C. and Jackson, S.P., Ku, a DNA Repair Protein with Multiple Cellular Functions?, Mutat. Res., 1999, vol. 434, no. 1, pp. 3–15.

    PubMed  CAS  Google Scholar 

  105. Doherty, A.J. and Jackson, S.P., DNA Repair: How Ku Makes Ends Meet, Curr. Biol., 2001, vol. 11, no. 22, pp. R920–R924.

    Article  PubMed  CAS  Google Scholar 

  106. Van Gent, D.C., Hoeijmakers, J.H., and Kanaar, R., Chromosomal Stability and the DNA Double-Stranded Break Connection, Nat. Rev. Genet., 2001, vol. 2, no. 3, pp. 196–206.

    PubMed  Google Scholar 

  107. Critchlow, S.E., Bowater, R.P., and Jackson, S.P., Mammalian DNA Double-Strand Break Repair Protein XRCC4 Interacts with DNA Ligase IV, Curr. Biol., 1997, vol. 7, no. 8, pp. 588–598.

    Article  PubMed  CAS  Google Scholar 

  108. Grawunder, U., Wilm, M., Wu, X., et al., Activity of DNA Ligase IV Stimulated by Complex Formation with XRCC4 Protein in Mammalian Cells, Nature, 1997, vol. 388, no. 6641, pp. 492–495.

    PubMed  CAS  Google Scholar 

  109. McElhinny, N.S.A., Snowden, C.M., McCarville, J., and Ramsden, D.A., Ku Recruits the XRCC4-Ligase IV Complex to DNA Ends, Mol. Cell. Biol., 2000, vol. 20, no. 9, pp. 2996–3003.

    Google Scholar 

  110. Moshous, D., Callebaut, I., de Chasseval, R., et al., Artemis, a Novel DNA Double-Strand Break Repair/V(D)J Recombination Protein, Is Mutated in Human Severe Combined Immune Deficiency, Cell (Cambridge, Mass.), 2001, vol. 105, no. 2, pp. 177–186.

    CAS  Google Scholar 

  111. Ma, Y., Pannicke, U., Schwarz, K., and Lieber, M.R., Hairpin Opening and Overhang Processing by an Artemis/DNA-Dependent Protein Kinase Complex in Nonhomologous End Joining and V(D)J Recombination, Cell (Cambridge, Mass.), 2002, vol. 108, no. 6, pp. 781–794.

    CAS  Google Scholar 

  112. Boulton, S.J. and Jackson, S.P., Components of the Ku-Dependent Non-Homologous End-Joining Pathway Are Involved in Telomeric Length Maintenance and Telomeric Silencing, EMBO J., 1998, vol. 17, no. 6, pp. 1819–1828.

    Article  PubMed  CAS  Google Scholar 

  113. Ma, J.L., Kim, E.M., Haber, J.E., and Lee, S.E., Yeast Mre11 and Rad1 Proteins Define a Ku-Independent Mechanism to Repair Double-Strand Breaks Lacking Overlapping End Sequences, Mol. Cell. Biol., 2003, vol. 23, no. 23, pp. 8820–8828.

    Article  PubMed  CAS  Google Scholar 

  114. Gorski, M.M., Eeken, J.C., de Jong, A.W., et al., The Drosophila melanogaster DNA Ligase IV Gene Plays a Crucial Role in the Repair of Radiation-Induced DNA Double-Strand Breaks and Acts Synergistically with Rad54, Genetics, 2003, vol. 165, no. 4, pp. 1929–1941.

    PubMed  CAS  Google Scholar 

  115. McVey, M., Radut, D., and Sekelsky, J.J., End-Joining Repair of Double-Strand Breaks in Drosophila melanogaster Is Largely DNA Ligase IV Independent, Genetics, 2004, vol. 168, no. 4, pp. 2067–2076.

    Article  PubMed  CAS  Google Scholar 

  116. McKee, B.D., Ren, X., and Hong, C., A RecA-Like Gene in Drosophila melanogaster That Is Expressed at High Levels in Female but Not Male Meiotic Tissues, Chromosoma, 1996, vol. 104, no. 7, pp. 479–488.

    PubMed  CAS  Google Scholar 

  117. Ghabrial, A., Ray, R.P., and Schupbach, T., okra and spindle-B Encode Components of the RAD52 DNA Repair Pathway and Affect Meiosis and Patterning in Drosophila Oogenesis, Genes Dev., 1998, vol. 12, no. 17, pp. 2711–2723.

    PubMed  CAS  Google Scholar 

  118. Engels, W.R., Johnson-Schlitz, D.M., Eggleston, W.B., and Sved, J., High-Frequency P-Element Loss in Drosophila Is Homolog-Dependent, Cell (Cambridge, Mass.), 1990, vol. 62, no. 3, pp. 515–525.

    CAS  Google Scholar 

  119. Gloor, G.B., Nassif, N.A., Johnson-Schlitz, D.M., et al., Targeted Gene Replacement in Drosophila Via P Element-Induced Gap Repair, Science, 1991, vol. 253, no. 5024, pp. 1110–1117.

    PubMed  CAS  Google Scholar 

  120. Nassif, N., Penney, J., Pal, S., et al., Efficient Copying of Nonhomologous Sequences from Ectopic Sites Via P Element-Induced Gap Repair, Mol. Cell. Biol., 1994, vol. 14, no. 3, pp. 1613–1625.

    PubMed  CAS  Google Scholar 

  121. Flores, C.C., Repair of DNA Double-Strand Breaks and Mismatches in Drosophila, DNA Damage and Repair, vol. 3: Advances from Phage to Humans, Nickoloff, J.A. and Hoekstra, M.F., Eds., Totowa: Humana, 2001, pp. 173–206.

    Google Scholar 

  122. McIlwraith, M.J., Van Dyck, E., Masson, J.Y., et al., Reconstitution of the Strand Invasion Step of Double-Strand Break Repair Using Human Rad51, Rad52 and RPA Proteins, J. Mol. Biol., 2000, vol. 304, no. 2, pp. 151–164.

    Article  PubMed  CAS  Google Scholar 

  123. Maryon, E. and Carroll, D., Degradation of Linear DNA by a Strand-Specific Exonuclease Activity in Xenopus laevis Oocytes, Mol. Cell. Biol., 1989, vol. 9, no. 11, pp. 4862–4871.

    PubMed  CAS  Google Scholar 

  124. Sugawara, N. and Haber, J.E., Characterization of Double-Strand Break-Induced Recombination: Homology Requirements and Single-Stranded DNA Formation, Mol. Cell. Biol., 1992, vol. 12, no. 2, pp. 563–575.

    PubMed  CAS  Google Scholar 

  125. Staeva-Vieira, E., Yoo, S., and Lehmann, R., An Essential Role of DmRad51/SpnA in DNA Repair and Meiotic Checkpoint Control, EMBO J., 2003, vol. 22, no. 21, pp. 5863–5874.

    Article  PubMed  CAS  Google Scholar 

  126. Paques, F., Leung, W.Y., and Haber, J.E., Expansions and Contractions in a Tandem Repeat Induced by Double-Strand Break Repair, Mol. Cell. Biol., 1998, vol. 18, no. 4, pp. 2045–2054.

    PubMed  CAS  Google Scholar 

  127. McVey, M., Adams, M., Staeva-Vieira, E., and Sekelsky, J.J., Evidence for Multiple Cycles of Strand Invasion during Repair of Double-Strand Gaps in Drosophila, Genetics, 2004, vol. 167, no. 2, pp. 699–705.

    Article  PubMed  CAS  Google Scholar 

  128. Lin, F.L., Sperle, K., and Sternberg, N., Model for Homologous Recombination during Transfer of DNA into Mouse L Cells: Role for DNA Ends in the Recombination Process, Mol. Cell. Biol., 1984, vol. 4, no. 6, pp. 1020–1034.

    PubMed  CAS  Google Scholar 

  129. Preston, C.R., Engels, W., and Flores, C., Efficient Repair of DNA Breaks in Drosophila: Evidence for Single-Strand Annealing and Competition with Other Repair Pathways, Genetics, 2002, vol. 161, no. 2, pp. 711–720.

    PubMed  CAS  Google Scholar 

  130. Fishman-Lobell, J. and Haber, J.E., Removal of Nonhomologous DNA Ends in Double-Strand Break Recombination: The Role of the Yeast Ultraviolet Repair Gene RAD1, Science, 1992, vol. 258, no. 5081, pp. 480–484.

    PubMed  CAS  Google Scholar 

  131. Sugawara, N., Paques, F., Colaiacovo, M., and Haber, J.E., Role of Saccharomyces cerevisiae Msh2 and Msh3 Repair Proteins in Double-Stand Break-Induced Recombination, Proc. Natl. Acad. Sci. USA, 1997, vol. 94, no. 17, pp. 9214–9219.

    Article  PubMed  CAS  Google Scholar 

  132. Colaiacovo, M.P., Paques, F., and Haber, J.E., Removal of One Nonhomologous DNA End during Gene Conversion by a RAD1-and MSH2-Independent Pathway, Genetics, 1999, vol. 151, no. 4, pp. 1409–1423.

    PubMed  CAS  Google Scholar 

  133. Friedberg, E.C., Walker, G.C., and Siede, W., DNA Repair and Mutagenesis, Washington, DC: Am. Soc. Microbiol., 1995.

    Google Scholar 

  134. Sladek, F.M., Munn, M.M., Rupp, W.D., and Howard-Flanders, P., In Vitro Repair of Psoralen-DNA Cross-Links by RecA, UvrABC, and the 5′-Exonuclease of DNA Polymerase I, J. Biol. Chem., 1989, vol. 264, no. 12, pp. 6755–6765.

    PubMed  CAS  Google Scholar 

  135. Bessho, T., Mu, D., and Sancar, A., Initiation of DNA Interstrand Cross-Link Repair in Humans: The Nucleotide Excision Repair System Makes Dual Incisions 5′ to the Cross-Linked Base and Removes a 22-to 28-Nucleotide-Long Damage-Free Strand, Mol. Cell. Biol., 1997, vol. 17, no. 12, pp. 6822–6830.

    PubMed  CAS  Google Scholar 

  136. Harris, P.V., Mazina, O.M., Leonhardt, E.A., et al., Molecular Cloning of Drosophila mus308, a Gene Involved in DNA Cross-Link Repair with Homology to Prokaryotic DNA Polymerase I Genes, Mol. Cell. Biol., 1996, vol. 16, no. 10, pp. 5764–5771.

    PubMed  CAS  Google Scholar 

  137. Aguirrezabalaga, I., Sierra, L.M., and Comendador, M.A., The Hypermutability Conferred by the mus308 Mutation of Drosophila Is Not Specific for Cross-Linking Agents, Mutat. Res., 1995, vol. 336, no. 3, pp. 243–250.

    PubMed  CAS  Google Scholar 

  138. Kitazono, A. and Matsumoto, T., “Isogaba Maware”: Quality Control of Genome DNA by Checkpoints, BioEssays, 1998, vol. 20, no. 5, pp. 391–399.

    Article  PubMed  CAS  Google Scholar 

  139. Fogarty, P., Campbell, S.D., Abu-Shumays, R., et al., The Drosophila grapes Gene Is Related to Checkpoint Gene chk1/rad27 and Is Required for Late Syncytial Division Fidelity, Curr. Biol., 1997, vol. 7, no. 6, pp. 418–426.

    Article  PubMed  CAS  Google Scholar 

  140. Oishi, I., Sugiyama, S., Otani, H., et al., A Novel Drosophila Nuclear Protein Serine/Threonine Kinase Expressed in the Germline during Its Establishment, Mech. Dev., 1998, vol. 71, nos. 1–2, pp. 49–63.

    PubMed  CAS  Google Scholar 

  141. Chang, H.C. and Rubin, G.M., 14-3-3 ε Positively Regulates Ras-Mediated Signaling in Drosophila, Genes Dev., 1997, vol. 11, no. 9, pp. 1132–1139.

    PubMed  CAS  Google Scholar 

  142. Hari, K.L., Santerre, A., Sekelsky, J.J., et al., The mei-41 Gene of D. melanogaster Is a Structural and Functional Homolog of the Human Ataxia Telangiectasia Gene, Cell (Cambridge, Mass.), 1995, vol. 82, no. 5, pp. 815–821.

    CAS  Google Scholar 

  143. Brodsky, M.H., Sekelsky, J.J., Tsang, G., et al., mus304 Encodes a Novel DNA Damage Checkpoint Protein Required during Drosophila Development, Genes Dev., 2000, vol. 14, no. 6, pp. 666–678.

    PubMed  CAS  Google Scholar 

  144. Prakash, S., Sung, P., and Prakash, L., DNA Repair Genes and Proteins of Saccharomyces cerevisiae, Annu. Rev. Genet., 1993, vol. 27, pp. 33–70.

    Article  PubMed  CAS  Google Scholar 

  145. De Buendia, P.G., Search for DNA Repair Pathways in Drosophila melanogaster, Mutat. Res., 1998, vol. 407, no. 1, pp. 67–84.

    PubMed  Google Scholar 

  146. Eeken, J.C. and Sobels, F.H., The Influence of Deficiencies in DNA-Repair on MR-Mediated Reversion of an Insertion-Sequence Mutation in Drosophila melanogaster, Mutat. Res., 1983, vol. 110, no. 2, pp. 287–295.

    PubMed  CAS  Google Scholar 

  147. Chmuzh, E.V., Shestakova, L.A., Koromyslov, Yu.A., et al., Effects of Mutations of the DNA Repair Genes on the Mutation Rate of Unstable Alleles of the Drosophila melanogaster X Chromosome, Dokl. Akad. Nauk, 2004, vol. 397, no. 1, pp. 128–141.

    Google Scholar 

  148. Huang, W. and Smith, P.D., The mus206 Gene of Drosophila melanogaster Is Required in Excision Repair of Alkylation-Induced DNA Lesions, Mutat. Res., 1997, vol. 384, no. 2, pp. 81–88.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Cytology and Genetics, Novosibirsk State University, Novosibirsk, 630090, Russia

    E. V. Chmuzh, L. A. Shestakova & I. K. Zakharov

  2. Institute of Cytology and Genetics, Russian Academy of Sciences, Novosibirsk, 630090, Russia

    V. S. Volkova & I. K. Zakharov

Authors
  1. E. V. Chmuzh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. L. A. Shestakova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. V. S. Volkova
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. I. K. Zakharov
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Original Russian Text © E.V. Chmuzh, L.A. Shestakova, V.S. Volkova, I.K. Zakharov, 2006, published in Genetika, 2006, Vol. 42, No. 4, pp. 462–476.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chmuzh, E.V., Shestakova, L.A., Volkova, V.S. et al. Diversity of mechanisms and functions of enzyme systems of DNA repair in Drosophila melanogaster . Russ J Genet 42, 363–375 (2006). https://doi.org/10.1134/S1022795406040028

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1022795406040028

Keywords

Search

Navigation