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The kinetic analysis of recognition of the damaged nucleotides by mutant forms of the 8-oxoguanine DNA glycosylase hOGG1

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Abstract

We have investigated the role of Tyr-203, His-270, and Lys-249 amino acid residues from the 8-oxoguanine glycosylase (hOGG1) active site in the process of recognition of 7,8-dihydro-8-oxoguanine (oxoG) damaged nucleotide and in the catalytic stages of enzymatic reaction. The pre-steady state kinetic analysis of conformational transitions of mutant forms of the enzyme and model DNA substrates during the enzymatic process revealed that the studied amino acid residues are involved in the specific binding of DNA substrates. The Tyr-203 is responsible for recognition of the damaged nucleotide; interaction between His-270 and DNA is necessary for the formation of the catalytically active complex with the oxoG-containing DNA. The Lys-249 acts not only as one of the catalytically important amino acids of the active site of the enzyme, but also plays a significant role in the formation of specific enzyme–substrate complex. The present study significantly complements the molecular-kinetic model of the enzymatic reaction and helps to clarify the origin of the high specificity of hOGG1 to oxidized bases in DNA.

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Abbreviations

hOGG1:

human 8-oxoguanine-DNA-glycosylase

BER:

base excision repair

oxoGua:

7,8-dihydro-8-oxoguanine

АР-site:

apurinic/apyrimidinic site

F-site:

(2R, 3S)-2-(hydroxy methyl)-3-hydroxytetrahydrofuran residue

ROS:

reactive oxygen species

FRET:

fluorescence resonance energy transfer

aPu:

2- aminopurine

References

  1. Cadet, J., Berger, M., Douki, T., and Ravanat, J.L., Rev. Physiol. Biochem. Pharmacol., 1991, vol. 131, pp. 1–87.

    Google Scholar 

  2. Dizdaroglu, M., Free Radic. Biol. Med., 1991, vol. 10, pp. 225–242.

    Article  CAS  PubMed  Google Scholar 

  3. Kuznetsova, A.A., Knorre, D.G., and Fedorova, O.S., Russ. Chem. Rev., 2009, vol. 78, pp. 659–678.

    Article  CAS  Google Scholar 

  4. Lu, R., Nash, H.M., and Verdine, G.L., Curr. Biol., 1997, vol. 7, pp. 397–407.

    Article  CAS  PubMed  Google Scholar 

  5. Elahi, A., Zheng, Z., Park, J., Eyring, K., McCaffrey, T., and Lazarus, P., Carcinogenes, 2002, vol. 23, pp. 1229–1234.

    Article  CAS  Google Scholar 

  6. Cooke, M.S., Evans, M.D., Dizdaroglu, M., and Lunec, J., FASEB J., 2003, vol. 17, pp. 1195–1214.

    Article  CAS  PubMed  Google Scholar 

  7. Evans, M.D., Dizdaroglu, M., and Cooke, M.S., Mutat. Res., 2004, vol. 567, pp. 1–61.

    Article  CAS  PubMed  Google Scholar 

  8. Kasai, H. and Nishimura, S., Nucleic Acids Res., 1984, vol. 12, pp. 2137–2145.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Wallace, S.S., Free Radic. Biol. Med., 2002, vol. 33, pp. 1–14.

    Article  CAS  PubMed  Google Scholar 

  10. Shibutani, S., Takeshita, M., and Grollman, A.P., Nature, 1991, vol. 349, pp. 431–434.

    Article  CAS  PubMed  Google Scholar 

  11. Grollman, A.P. and Moriya, M., Trends Genet., 1993, vol. 9, pp. 246–249.

    Article  CAS  PubMed  Google Scholar 

  12. Karahalil, B., Girard, P.M., Boiteux, S., and Dizdaroglu, M., Nucleic Acids Res., 1998, vol. 26, pp. 1228–1232.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Fromme, J.C., Bruner, S.D., Yang, W., Karplus, M., and Verdine, G.L., Nat. Struct. Biol., 2003, vol. 10, pp. 204–211.

    Article  CAS  PubMed  Google Scholar 

  14. Girard, P.M., Guibourt, N., and Boiteux, S., Nucleic Acids Res., 1997, vol. 25, pp. 3404–3411.

    Article  Google Scholar 

  15. Zharkov, D.O., Rosenquist, T.A., Gerchman, S.E., and Grollman, A.P., J. Biol. Chem., 2000, vol. 275, pp. 28607–28617.

    Article  CAS  PubMed  Google Scholar 

  16. Norman, D.P., Chung, S.J., and Verdine, G.L., Biochemistry, 2003, vol. 42, pp. 1564–1572.

    Article  CAS  PubMed  Google Scholar 

  17. Dalhus, B., Forsbring, M., Helle, I.H., Vik, E.S., Forstrom, R.J., Backe, P.H., Alseth, I., and Bjoras, M., Structure, 2011, vol. 19, pp. 117–127.

    Article  CAS  PubMed  Google Scholar 

  18. Nash, H.M., Lu, R., Lane, W.S., and Verdine, G.L., Chem. Biol., 1997, vol. 4, pp. 693–702.

    Article  CAS  PubMed  Google Scholar 

  19. Guibourt, N., Castaing, B., Van Der Kemp, P.A., and Boiteux, S., Biochemistry, 2000, vol. 39, pp. 1716–1724.

    Article  CAS  PubMed  Google Scholar 

  20. Bruner, S.D., Norman, D.P., and Verdine, G.L., Nature, 2000, vol. 403, pp. 859–866.

    Article  CAS  PubMed  Google Scholar 

  21. Bjoras, M., Seeberg, E., Luna, L., Pearl, L.H., and Barrett, T.E., J. Mol. Biol., 2002, vol. 317, pp. 171–177.

    Article  CAS  PubMed  Google Scholar 

  22. Banerjee, A., Yang, W., Karplus, M., and Verdine, G.L., Nature, 2005, vol. 434, pp. 612–618.

    Article  CAS  PubMed  Google Scholar 

  23. Radom, C.T., Banerjee, A., and Verdine, G.L., J. Biol. Chem., 2007, vol. 282, pp. 9182–9194.

    Article  CAS  PubMed  Google Scholar 

  24. Crenshaw, C.M., Nam, K., Oo, K., Kutchukian, P.S., Bowman, B.R., Karplus, M., and Verdine, G.L., J. Biol. Chem., 2012, vol. 287, pp. 24916–24928.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Kuznetsov, N.A., Koval, V.V., Zharkov, D.O., Nevinsky, G.A., Douglas, K.T., and Fedorova, O.S., Nucleic Acids Res., 2005, vol. 33, pp. 3919–3931.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Kuznetsov, N.A., Koval, V.V., Nevinsky, G.A., Douglas, K.T., Zharkov, D.O., and Fedorova, O.S., J. Biol. Chem., 2007, vol. 282, pp. 1029–1038.

    Article  CAS  PubMed  Google Scholar 

  27. Kuznetsov, N.A., Koval, V.V., and Fedorova, O.S., Biochemistry (Moscow), 2011, vol. 76, pp. 142–156.

    Article  Google Scholar 

  28. Kuznetsova, A.A., Kuznetsov, N.A., Ishchenko, A.A., Saparbaev, M.K., and Fedorova, O.S., Biochim. Biophys. Acta, 2014, vol. 1840, pp. 387–395.

    Article  CAS  PubMed  Google Scholar 

  29. Lukina, M.V., Popov, A.V., Koval, V.V., Vorobjev, Y.N., Fedorova, O.S., and Zharkov, D.O., J. Biol. Chem., 2013, vol. 288, pp. 28936–28947.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Kuznetsov, N.A., Kuznetsova, A.A., Vorobjev, Y.N., Krasnoperov, L.N., and Fedorova, O.S., PLoS One, 2014, vol. 9, p. e98495.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Rachofsky, E.L., Osman, R., and Ross, J.B.A., Biochemistry, 2001, vol. 40, pp. 946–956.

    Article  CAS  PubMed  Google Scholar 

  32. Sowers, L.C., Boulard, Y., and Fazakerley, G.V., Biochemistry, 2000, vol. 39, pp. 7613–7620.

    Article  CAS  PubMed  Google Scholar 

  33. Kuznetsov, N.A., Koval, V.V., Zharkov, D.O., and Fedorova, O.S., DNA Repair (Amst.), 2012, vol. 11, pp. 884–891.

    Article  CAS  Google Scholar 

  34. Koval, V.V., Kuznetsov, N.A., Zharkov, D.O., Ishchenko, A.A., Douglas, K.T., Nevinsky, G.A., and Fedorova, O.S., Nucleic Acids Res., 2004, vol. 32, pp. 926–935.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Miroshnikova, A.D., Kuznetsova, A.A., Vorobjev, Y.N., Kuznetsov, N.A., and Fedorova, O.S., Mol. BioSyst., 2016, vol. 12, pp. 1527–1539.

    Article  CAS  PubMed  Google Scholar 

  36. Kuznetsov, N.A., Kiryutin, A.S., Kuznetsova, A.A., Panov, M.S., Barsukova, M.O., Yurkovskaya, A.V., and Fedorova, O.S., J. Biomol. Struct. Dyn., 2016, pp. 1–18. doi 10.1080/07391102.2016.1171800

    Google Scholar 

  37. Sambrook, J., Fritsch, E.F., and Maniatis, T., Molecular Cloning: A Laboratory Manual, 2nd ed., Cold Spring Harbor, New York: Cold Spring Harbor Laboratory, 1989.

    Google Scholar 

  38. Fasman, G.D., Handbook of Biochemistry and Molecular Biology, 3rd ed., Cleveland: CRC Press, 1975.

    Google Scholar 

  39. Kuznetsov, N.A., Zharkov, D.O., Koval, V.V., Buckle, M., and Fedorova, O.S., Biochemistry, 2009, vol. 48, pp. 11335–11343.

    Article  CAS  PubMed  Google Scholar 

  40. Kuzmic, P., Anal. Biochem., 1996, vol. 237, pp. 260–273.

    Article  CAS  PubMed  Google Scholar 

  41. Kuznetsov, N.A., Vorobjev, Y.N., Krasnoperov, L.N., and Fedorova, O.S., Nucleic Acids Res., 2012, vol. 40, pp. 7384–7392.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Kuznetsov, N.A., Kladova, O.A., Kuznetsova, A.A., Ishchenko, A.A., Saparbaev, M.K., Zharkov, D.O., and Fedorova, O.S., J. Biol. Chem., 2015, vol. 290, pp. 14338–14349.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Institute of Chemical Biology and Fundamental Medicine, Siberian Branch, Russian Academy of Sciences, Novosibirsk, 630090, Russia

    M. V. Lukina, A. A. Kuznetsova, N. A. Kuznetsov & O. S. Fedorova

  2. Novosibirsk State University, Novosibirsk, 630090, Russia

    M. V. Lukina, A. A. Kuznetsova, N. A. Kuznetsov & O. S. Fedorova

Authors
  1. M. V. Lukina
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  2. A. A. Kuznetsova
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  3. N. A. Kuznetsov
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  4. O. S. Fedorova
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Corresponding authors

Correspondence to N. A. Kuznetsov or O. S. Fedorova.

Additional information

Original Russian Text © M.V. Lukina, A.A. Kuznetsova, N.A. Kuznetsov, O.S. Fedorova, 2017, published in Bioorganicheskaya Khimiya, 2017, Vol. 43, No. 1, pp. 4–17.

The paper is based on the materials of the “Chemical Biology 2016” conference; Novosibirsk, Russia, July 24–29, 2016.

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Lukina, M.V., Kuznetsova, A.A., Kuznetsov, N.A. et al. The kinetic analysis of recognition of the damaged nucleotides by mutant forms of the 8-oxoguanine DNA glycosylase hOGG1. Russ J Bioorg Chem 43, 1–12 (2017). https://doi.org/10.1134/S1068162017010058

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  • DOI: https://doi.org/10.1134/S1068162017010058

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