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Activity of error-prone DNA polymerase iota in different periods of house mouse Mus musculus ontogeny

  • Biochemistry of Development
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Abstract

Analysis of incorrect activity of error-prone DNA polymerase iota in M. musculus ontogeny demonstrated considerable changes in its activity, which peaks in most organs during prenatal development and decreases in the adult body. We propose that the capacity of error-prone DNA polymerases to synthesize on damaged DNA regions is critical for the realization of rapidly changing genetic program in mammalian embryogenesis, which relieves the replication block and prevents cell death.

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References

  • Albertella, M.R., Lau, A., and O’Connor, M.J., The Overexpression of Specialized DNA Polymerases in Cancer, DNA Repair, 2005, vol. 4, pp. 583–593.

    Article  PubMed  CAS  Google Scholar 

  • Aoufouchi, S., Flatter, E., Dahan, A., et al., Two Novel Human and Mouse DNA Polymerase of the PolX Family, Nucl. Acids Res., 2000, vol. 28, pp. 3684–3693.

    Article  PubMed  CAS  Google Scholar 

  • Bebenek, K., Tissier, A.K., Frank, E.G., et al., 5′-Deoxyribose Phosphate Lyase Activity of Human DNA Polymerase Iota in Vitro, Science, 2001, vol. 291, pp. 2156–2159.

    Article  PubMed  CAS  Google Scholar 

  • Bergoglio, V., Pillaire, M.J., Lacroix-Triki, M., et al., Deregulated DNA Polymerase beta Induced Chromosome Instability and Tumorigenesis, Cancer Res., 2002, vol. 62, pp. 3511–3514.

    PubMed  CAS  Google Scholar 

  • Budd, M.E. and Campbell, J.L., Purification and Enzymatic and Functional Characterization of DNA Polymerase betalike Enzyme, POL4, Expressed during Yeast Meiosis, Methods Enzymol., 1995, vol. 262, pp. 108–130.

    Article  PubMed  CAS  Google Scholar 

  • Canitrot, Y., Cazaux, C., Frechet, M., et al., Overexpression of DNA Polymerase beta in Cells Results in a Mutator Phenotype and a Decreased Sensitivity to Anticancer Drugs, Proc. Natl. Acad. Sci. USA, 1998, vol. 95, pp. 12586–12590.

    Article  PubMed  CAS  Google Scholar 

  • Dianov, G.L., Prasad, R., Wilson, S.H., et al., Role of DNA Polymerase beta in the Excision Step of Long Patch Mammalian Base Excision Repair, J. Biol. Chem., 1999, vol. 274, pp. 13741–13743.

    Article  PubMed  CAS  Google Scholar 

  • Esposito, G., Godindagger, I., Klein, Y., et al., Disraption of the Rev-31-Encoded Catalytic Subunit of Polymerases Zeta in Mice Results in Early Embryonic Lethality, Curr. Biol., 2000, vol. 10, pp. 1221–1224.

    Article  PubMed  CAS  Google Scholar 

  • Federico, L., Kunkel, T., and Shaw, B., A Sensitive Genetic Assay for the Detection of Cytosine Deamination: Determination of Rate Constants and the Activation Energy, Biochemistry, 1990, vol. 29, pp. 2532–2537.

    Article  Google Scholar 

  • Gan, G.N., Wittschieben, J.P., Wittschieben, B., et al., DNA Polymerase Zeta (Pol zeta) in Higher Eukaryotes, Cell Res., 2008, vol. 18, pp. 174–183.

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Diaz, M., Dominguez, O., Lopez-Fernandez, L.A., et al., DNA Polymerase lambda (pol lambda), A Novel Eukaryotic DNA Polymerase with a Potential Role in Meiosis, J. Mol. Biol., 2000, vol. 301, pp. 851–867.

    Article  PubMed  CAS  Google Scholar 

  • Gening, L.V., Makarova, A.V., Malashenko, A.M., et al., A false note of DNA polymerase iota in the choir of genome caretakers in mammals, Genetika, 2006a, vol. 70, pp. 201–207.

    Google Scholar 

  • Gening, L.V., Grishina, E.E., Petrochenkov, A.N., et al., Association between High Activity of DNA Polymerase iota and the Development of Human Uveal Melanoma, Genetika, 2006b, vol. 42, pp. 98–103.

    PubMed  CAS  Google Scholar 

  • Gening, L.V., Petrochenkov, A.N., Reshetnyak, A.B., et al., Aktivnost’, kharakternaya dlya DNK-polimerazy iota, v ekstraktakh kletok iz raznykh organov myshi, Biokhimiya, 2004, vol. 69, pp. 537–543.

    Google Scholar 

  • Gening, L.V. and Tarantul, V.Z., Involvement of DNA-Polymerase iota in Hypermutagenesis and Tumorigenesis: An Improper Model Can Lead to Inaccurate Results, Immunol. Lett., 2006, vol. 106, pp. 198–199.

    Article  PubMed  CAS  Google Scholar 

  • Holbeek, S.L. and Strathern, J., A Role for REV3 in Mutagenesis during Doublestrand Break Repair in Saccharomyces cerevisiae, Genetics, 1997, vol. 147, pp. 1017–1024.

    Google Scholar 

  • Johnson, R.E., Washington, M.T., Haracska, L., et al., Eukaryotic Polymerases iota and zeta Act Sequentially to Bypass DNA Lesions, Nature, 2000a, vol. 406, pp. 1015–1019.

    Article  PubMed  CAS  Google Scholar 

  • Johnson, R.E, Washington, M.T., Prakash, S., et al., Fidelity of Human DNA Polymerase eta, Mol. Biol., 2000b, vol. 275, pp. 7447–7450.

    CAS  Google Scholar 

  • Kunkel, T.A., Frameshift Mutagenesis by Eucaryotic DNA Polymerases in Vitro, J. Biol. Chem., 1986, vol. 261, pp. 13581–13587.

    PubMed  CAS  Google Scholar 

  • Lang, T., Dalal, S., Chikova, A., et al., The E295K DNA Polymerase Beta Gastric Cancer-Associated Variant Interferes with Base Excision Repair and Induces Cellular Transformation, Mol. Cell. Biol., 2007, vol. 27, pp. 5587–5596.

    Article  PubMed  CAS  Google Scholar 

  • Magni, G. and von Borstel, R., Different Rates of Spontaneous Mutation during Mitosis and Meiosis in Yeast, Genetics, 1962, vol. 47, pp. 1097–1108.

    PubMed  CAS  Google Scholar 

  • Makarova, A.V., Tarantul, V.Z., and Gening, L.V., Evolution of DNA Polymerase iota Structure and Function in Eukaryotes, Biokhimiya, 2008, vol. 73, pp. 426–433.

    Google Scholar 

  • Masutani, C., Kusumoto, R., Yamada, A., et al., The XPV (Xeroderma Pigmentosum Variant) Gene Encodes Human DNA Polymerase eta, Nature, 1999, vol. 399, pp. 700–704.

    Article  PubMed  CAS  Google Scholar 

  • Matsuda, T., Bebenek, K., Masutani, C., et al., Low Fidelity DNA Synthesis by Human DNA Polymerase-eta, Nature, 2000, vol. 404, pp. 1011–1013.

    Article  PubMed  CAS  Google Scholar 

  • McDonald, J.P., Rapic-Otrin, V., Epstein, J.A., et al., Novel Human and Mouse Homologs of Saccharomyces cerevisiae DNA Polymerase eta, Genomics, 1999, vol. 60, pp. 20–30.

    Article  PubMed  CAS  Google Scholar 

  • McDonald, J.P., Tissier, A., Frank, E.G., et al., DNA Polymerase iota and Related Rad30-like Enzymes, Philos. Trans. Roy. Soc. (Lond. B. Biol. Sci.)., 2001, vol. 356, pp. 53–60.

    Article  CAS  Google Scholar 

  • McDonald, J.P., Frank, E.G., Plosky, B.S., et al., 129-Derived Strains of Mice Are Deficient in DNA Polymerase and Have Normal Immunoglobulin Hypermutation, J. Exp. Med., 2003, vol., 198, pp. 635–643.

    Article  PubMed  CAS  Google Scholar 

  • McLean, D.J., Friel, P.J., Johnston, D.S., et al., Characterization of Spermatogonial Stem Cell Maturation and Differentiation in Neonatal Mice, Biol. Reprod., 2003, vol. 69, pp. 2085–2091.

    Article  PubMed  CAS  Google Scholar 

  • Niimi, N., Sugo, N., Aratani, Y., et al., Decreased Mutant Frequency in Embryonic Brain of DNA Polymerase beta Null Mice, Mutagenesis, 2006, vol. 21, pp. 55–59.

    Article  PubMed  CAS  Google Scholar 

  • O-Wang, J., Kajivara, K., Kawamura, K., et al., An Essential Role of REV3 in Mammalian Cell Survival: Absence of REV3 Induced p53-Independent Embryonic Death, Biochem. Biophys. Res. Comm., 2002, vol. 293, pp. 1132–1137.

    Article  PubMed  CAS  Google Scholar 

  • O-Wang, J., Kawamura, M., Tada, Y., DNA Polymerase kappa, Implicated in Spontaneous and DNA Damage-Induced Mutagenesis, Is Overexpressed in Lung Cancer, Cancer Res., 2001, vol. 61, pp. 5366–5369.

    PubMed  CAS  Google Scholar 

  • Ogi, T., Kato, T. Jr., Kato, T., et al., Mutation Enhancement by DINB1, A Mammalian Gomologue of the Escherichia coli Mutagenesis Protein dinB, Genes Cells, 1999, vol. 4, pp. 607–618.

    Article  PubMed  CAS  Google Scholar 

  • Ohashi, E., Bebenek, K., Matsurda, T., Fidelity and Processivity of DNA Synthesis by DNA Polymerase kappa, The Product of the Human DINB1 Gene, Biol. Chemistry, 2000, vol. 275, pp. 39678–39684.

    Article  CAS  Google Scholar 

  • Ohkumo, T., Kondo, Y., Yokoi, M., et al., UV-B Radiation Induces Epithelial Tumors in Mice Lacking DNA Polymerase eta and Mesenchymal Tumors in Mice Deficient for DNA Polymerase iota, Mol. Cell. Biol., 2006, vol. 26, pp. 7696–7706.

    Article  PubMed  CAS  Google Scholar 

  • Podlutsky, A.J., Dianova, I.I., Podust, V.N., et. al. Human DNA Polymerase β Initiates DNA Synthesis during Long-Patch Repair of Reduced AP Sites in DNA, EMBO J., 2001, vol. 20, pp. 1477–1482.

    Article  PubMed  CAS  Google Scholar 

  • Raji, N.S., Krishna, T.H., Rao, K.S., DNA-Polymerase alpha, beta, delta and epsilon Activities in Isolated Neuronal and Astroglial Cell Fractions from Developing and Aging Rat Cerebral Cortex, Int. J. Devel. Neurosci., 2002, vol. 20, pp. 491–496.

    Article  CAS  Google Scholar 

  • Rao, K.S., Annapurna, V.V., and Raji, N.S., DNA Polymerase-beta May Be the Main Player for Defective DNA Repair in Aging Rat Neurons, Ann. New York Acad. Sci., 2001, vol. 928, pp. 113–120.

    Article  CAS  Google Scholar 

  • Romanenko, E.B., Demidenko, Z.N., and Vanyushin, B.F., RNA-Polymerase, DNA-Polymerase, DNA-Methyltransferase and Sphingomyelinase Activities in Liver Nuclei of Rats of Different Age, Biokhimiya, 1998, vol. 63, pp. 159–163.

    CAS  Google Scholar 

  • Schenten, D., Gerlach, V.L., Guo, C., et al., DNA Polymerase kappa Deficiency Does not Affect Somatic Hypermutation in Mice, Eur. J. Immunol., 2002, vol. 32, pp. 3152–3160.

    Article  PubMed  CAS  Google Scholar 

  • Sobol, R.W., Prasad, R., Evenski, A., et al., The Lyase Activity of the DNA Repair Protein beta-Polymerase Protects from DNA-Damage Induced Cytotoxicity, Nature, 2000, vol. 405, pp. 807–810.

    Article  PubMed  CAS  Google Scholar 

  • Srivastava, D.K., Husain, I., Artcaga, C.L., et al., DNA Polymerase beta Expression Differences in Selected Human Tumors and Cell Lines, Carcinogenesis, 1999, vol. 20, pp. 1049–1054.

    Article  PubMed  CAS  Google Scholar 

  • Strathern, J., Shafer, B., and McGill, C., DNA Synthesis Errors Associated with Double-Strand-Break Repair, Genetics, 1995, vol. 140, pp. 965–972.

    PubMed  CAS  Google Scholar 

  • Sugo, N., Aratani, Y., Nagashima, Y., et al., Neonatal Lethality with Abnormal Neurogenesis in Mice Deficient in DNA Polymerase beta, EMBO J., 2000, vol. 19, pp. 1397–1404.

    Article  PubMed  CAS  Google Scholar 

  • Tissier, A., McDonald, J.P., Frank, E.G., et al., Pol iota, A Remarkably Error-Prone Human DNA Polymerase, Genes Devel., 2000, vol. 14, pp. 1642–1650.

    PubMed  CAS  Google Scholar 

  • Vaisman, A. and Woodgate, R., Unique Misinsertion Specificity of Poliota May Decrease the Mutagenic Potential of Deaminated Cytosines, EMBO J., 2001, vol. 20, pp. 6520–6529.

    Article  PubMed  CAS  Google Scholar 

  • Vaisman, A., Takasawa, K., Iwai, S., et al., DNA Polymerase iota-Dependent Translesion Replication of Uracil Containing Cyclobutane Pyrimidine Dimmers, DNA Repair (Amst.)., 2006, vol. 5, pp. 210–218.

    Article  CAS  Google Scholar 

  • Van Sloun, P.P., Romeijn, R.J., and Ecken, J.C., Molecular Cloning, Expression and Chromosomal Localization of the Mouse Rev31 Gene, Encoding the Catalytic Subunit of Polymerase zeta, Mutat. Rev., 1999, vol. 433, pp. 109–116.

    Article  Google Scholar 

  • Washington, M.T., Johnson, R.E., Prakash, L., et al., Efficient and Error-Free Replication Past a Minor-Groove DNA Adduct by the Sequential Action of Human DNA Polymerases iota and kappa, Mol. Cell. Biol., 2004, vol. 24, pp. 5687–5693.

    Article  PubMed  CAS  Google Scholar 

  • Wilson, S.H., Mammalian Base Excision Repair and DNA Polymerase beta, Mutat. Res., 1998, vol. 407, pp. 203–215.

    PubMed  CAS  Google Scholar 

  • Wittschieben, J., Shivji, M.K., Lalani, E., et al., Disruption of the Developmentally Regulated Rev31 Gene Causes Embryonic Lethality, Curr. Biol., 2000, vol. 10, pp. 1217–1220.

    Article  PubMed  CAS  Google Scholar 

  • Yamada, A., Masutani, C., and Iwai, S., Complementation of Defective Translation Synthesis and UV Light Sensitivity in Xeroderma Pigmentosum Variant Cells by Human and Mouse DNA Polymerase eta, Nucl. Asids Res., 2000, vol. 28, pp. 2473–2480.

    Article  CAS  Google Scholar 

  • Yang, J., Zhiwen, C.H., and Liu, Y., Altered DNA Polymerase ı Expression in Breast Cancer Cells Leads to a Reduction in DNA Replication Fidelity and a Higher Rate of Mutagenesis, Cancer Res., 2004, vol. 64, pp. 5597–5607.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, Y., Yuan, F., Wu, X., et al., Preferential Incorporation of G Opposite Template T by the Low-Fidelity Human DNA Polymerase iota, Mol. Cell. Biol., 2000, vol. 20, pp. 7099–7108.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Institute of Molecular Genetics, Russian Academy of Sciences, Moscow, 123182, Russia

    A. V. Makarova, L. V. Gening, I. V. Makarova & V. Z. Tarantul

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  1. A. V. Makarova
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  2. L. V. Gening
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  3. I. V. Makarova
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  4. V. Z. Tarantul
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Correspondence to A. V. Makarova.

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Original Russian Text © A.V. Makarova, L.V. Gening, I.V. Makarova, V.Z. Tarantul, 2008, published in Ontogenez, 2008, Vol. 38, No. 5, pp. 367–373.

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Makarova, A.V., Gening, L.V., Makarova, I.V. et al. Activity of error-prone DNA polymerase iota in different periods of house mouse Mus musculus ontogeny. Russ J Dev Biol 39, 297–302 (2008). https://doi.org/10.1134/S1062360408050068

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