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Influence of poly(ADP-ribose) polymerase-1 and its apoptotic 24-kD fragment on repair of DNA duplexes in bovine testis nuclear extract

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Abstract

Effects of exogenous proteins poly(ADP-ribose) polymerase-1 (PARP1) and its 24-kD proteolytic fragment (p24) on the repair of DNA duplexes containing a one nucleotide gap with furan phosphate or phosphate group at the 5′-end of the downstream primer were studied in bovine testis nuclear extract. These damaged DNAs are repaired by the long-patch or short-patch subpathways of base excision repair (BER), respectively. Exogenous PARP1 and p24 decreased the efficiency of gap filling DNA synthesis for both duplexes, but did not influence the ligation stage in the repair of DNA duplex by the short-patch subpathway. Under the same conditions, these proteins inhibited strand-displacement DNA synthesis and decreased the efficiency of the flap endonuclease 1 (FEN1)-catalyzed endonuclease reaction in the nuclear extract, blocking repair of DNA duplex by the long-patch subpathway. Addition of exogenous PARP1 and p24 also reduced the efficiency of UV light crosslinking of extract BER proteins to the photoreactive BER intermediates carrying a nick. Thus, PARP1 and p24 interact with DNA intermediates of BER and compete with nuclear extract proteins for binding to DNA. The interaction of PARP1 and p24 with DNA intermediates of the long-patch subpathway of BER resulted in inhibition of subsequent stages of the repair mediated by this mechanism. However, on recovery of the intact structure of DNA duplex by the short-patch subpathway, PARP1 and p24 suppressed the repair of the one nucleotide gap less efficiently and failed to influence the final stage of the repair, ligation.

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Abbreviations

APE1:

apurinic/apyrimidinic endonuclease

BER:

base excision repair

dRP:

2′-deoxyribose 5′-phosphate

FEN1:

flap endonuclease 1

nt:

nucleotides

PARP1:

poly(ADP-ribose) polymerase-1

p24:

24-kD apoptotic fragment of PARP1

pF-N1 :

3-hydroxy-2-hydroxymethyl tetrahydrofuran 5′-phosphate mononucleotide

pol β:

DNA polymerase β

References

  1. Lindahl, T. (1993) Nature, 362, 709–715.

    Article  PubMed  CAS  Google Scholar 

  2. Lindahl, T. (2000) Mutat. Res., 462, 129–135.

    Article  PubMed  CAS  Google Scholar 

  3. Frosina, G., Fortini, P., Rossit, O., Raspaglion, G., Cox, L. S., Lane, D. P., Abbondanolo, A., and Dogliotti, E. (1996) J. Biol. Chem., 271, 9573–9578.

    Article  PubMed  CAS  Google Scholar 

  4. Klungland, A., and Lindahl, T. (1997) EMBO J., 16, 3341–3348.

    Article  PubMed  CAS  Google Scholar 

  5. Fan, J., and Wilson III, D. M. (2005) Free Rad. Biol. Med., 38, 1121–1138.

    Article  PubMed  CAS  Google Scholar 

  6. Shall, S., and de Murcia, G. (2000) Mutat. Res., 460, 1–15.

    PubMed  CAS  Google Scholar 

  7. Lindahl, T., Satoh, M. S., Poirier, G. G., and Klungland, A. (1995) Trends Biochem. Sci., 20, 405–411.

    Article  PubMed  CAS  Google Scholar 

  8. D’Amours, D., Desnoyers, S., D’silva, I., and Poirier, G. G. (1999) Biochem. J., 342, 249–268.

    Article  PubMed  CAS  Google Scholar 

  9. Ha, H. C., and Snyder, S. H. (2000) Neurobiol. Dis., 7, 225–239.

    Article  PubMed  CAS  Google Scholar 

  10. Bernstein, C., Bernstein, H., Payne, C. M., and Gareval, H. (2002) Mutat. Res., 511, 145–178.

    Article  PubMed  CAS  Google Scholar 

  11. Kaufmann, S. H., Desnoyers, S., Ottaviano, Y., Davidson, N. E., and Poirier, G. G. (1993) Cancer Res., 53, 3976–3985.

    PubMed  CAS  Google Scholar 

  12. Simonin, F., Menissier-de Murcia, J:, Poch, O., Muller, S., Gradwohl, G., Molinete, M., Penning, C., Keith, G., and de Murcia, G. (1990) J. Biol. Chem., 265, 19249–19256.

    PubMed  CAS  Google Scholar 

  13. Ikejima, M., Noguchi, S., Yamashita, R., Ogura, T., Sugimura, T., Gill, D. M., and Miwa, M. (1999) J. Biol. Chem., 265, 21907–21913.

    Google Scholar 

  14. D’Amours, D., Sallmann, F. R., Dixit, V. M., and Poirier, G. G. (2001) J. Cell Sci., 114, 3771–3778.

    PubMed  CAS  Google Scholar 

  15. Yung, T. M., and Satoh, M. S. (2001) J. Biol. Chem., 276, 11279–11286.

    Article  PubMed  CAS  Google Scholar 

  16. Lavrik, O. I., Prasad, R., Sobol, R. W., Horton, J. K., Ackerman, E. J., and Wilson, S. H. (2001) J. Biol. Chem., 276, 25541–25548.

    Article  PubMed  CAS  Google Scholar 

  17. Lebedeva, N. A., Rechkunova, N. I., Khodyreva, S. N., Favre, A., and Lavrik, O. I. (2002) Biochem. Biophys. Res. Commun., 297, 714–721.

    Article  PubMed  CAS  Google Scholar 

  18. Sukhanova, M. V., Khodyreva, S. N., and Lavrik, O. I. (2004) Biochemistry (Moscow), 69, 558–568.

    Article  CAS  Google Scholar 

  19. Safronov, I. V., Shcherbin, I. V., Khodyreva, S. N., Vlasov, V. A., Dobrikov, M. I., Shishkin, G. V., and Lavrik, O. I. (1997) Bioorg. Khim., 23, 576–585.

    PubMed  CAS  Google Scholar 

  20. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd Edn., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N. Y.

    Google Scholar 

  21. Drachkova, I. A., Petruseva, I. O., Safronov, I. V., Zakharenko, A. L., Shishkin, G. V., Lavrik, O. I., and Khodyreva, S. N. (2001) Bioorg. Khim. 27, 197–204.

    PubMed  CAS  Google Scholar 

  22. Prasad, R., Singhal, R. K., Srivastava, R. K., Molina, J. T., Tomkinson, A. E., and Wilson, S. H. (1996) J. Biol. Chem., 271, 16000–16007.

    Article  PubMed  CAS  Google Scholar 

  23. Bradford, M. M. (1976) Analyt. Biochem., 72, 248–254.

    Article  PubMed  CAS  Google Scholar 

  24. Laemmli, U. K. (1970) Nature, 227, 680–685.

    Article  PubMed  CAS  Google Scholar 

  25. Nash, R., and Lindahl, T. (1996) DNA Ligases: DNA Replication in Eukaryotic Cells, Cold Spring Harbor Laboratory Press, N. Y., pp. 575–580.

    Google Scholar 

  26. Matsumoto, Y., Kim, K., and Bogenhagen, D. F. (1994) Mol. Cell Biol., 14, 6187–6197.

    PubMed  CAS  Google Scholar 

  27. Copeland, W. C., Chen, M. S., and Wang, T. S. (1992) J. Biol. Chem., 267, 21459–21464.

    PubMed  CAS  Google Scholar 

  28. Harrington, J. J., and Lieber, M. R. (1994) EMBO J., 13, 1235–1246.

    PubMed  CAS  Google Scholar 

  29. Prasad, R., Dianov, G. L., Bohr, V. A., and Wilson, S. H. (2000) J. Biol. Chem., 275, 4460–4466.

    Article  PubMed  CAS  Google Scholar 

  30. Liu, Y., Beard, W. A., Shock, D. D., Prasad, R., Hou, E. W., and Wilson, S. H. (2005) J. Biol. Chem., 280, 3665–3674.

    Article  PubMed  CAS  Google Scholar 

  31. Cistulli, C., Lavrik, O. I., Prasad, R., Hou, E., and Wilson, S. H. (2004) DNA Repair, 3, 581–591.

    PubMed  CAS  Google Scholar 

  32. Osterman, L. A. (1981) Approaches to Study Proteins and Nucleic Acids. Electrophoresis and Ultracentrifugation [in Russian], Nauka, Moscow.

    Google Scholar 

  33. Griesenbeek, J., Oei, L. S., Mayer-Kuckuk, P., Ziegler, M., Bushlow, G., and Schweiger, M. (1997) Biochemistry, 36, 7297–7304.

    Article  Google Scholar 

  34. Satoh, M. S., and Lindahl, T. (1992) Nature, 356, 356–358.

    Article  PubMed  CAS  Google Scholar 

  35. Althaus, F. R., Kleczkowska, H. E., Malanga, M., Muntener, C. R., Pleschke, J. M., Ebner, M., and Auer, B. (1999) Mol. Cell Biochem., 193, 5–11.

    Article  PubMed  CAS  Google Scholar 

  36. Dantzer, F., Schreiber, V., Niedergant, C., Trusso, C., Flatter, E., de la Rubia, G., Oliver, J., Rolli, V., de Murcia, J. M., and de Murcia, G. (1999) Biochimie, 81, 69–75.

    Article  PubMed  CAS  Google Scholar 

  37. Caldecott, K. W., Aoufouchi, S., Johnson, P., and Shall, S. (1996) Nucleic Acids Res., 24, 4387–4394.

    Article  PubMed  CAS  Google Scholar 

  38. Dantzer, F., de la Rubia, G., de Murcia, J. M., Hostomsky, Z., de Murcia, G., and Schreiber, V. (2000) Biochemistry, 39, 7559–7569.

    Article  PubMed  CAS  Google Scholar 

  39. Vodenicharov, M. D., Sallmann, F. R., Satoh, M. S., and Poirier, G. G. (2000) Nucleic Acids Res., 28, 3887–3896.

    Article  PubMed  CAS  Google Scholar 

  40. Sanderson, R. J., and Lindahl, T. (2002) DNA Repair, 1, 547–558.

    Article  PubMed  CAS  Google Scholar 

  41. Allinson, S. L., Dianova, I. I., and Dianov, G. L. (2003) Acta Biochim. Polon., 50, 169–179.

    PubMed  CAS  Google Scholar 

  42. Prasad, R., Lavrik, O. I., Kim, S. J., Kedar, P., Yang, X. P., Berg, B. J. V., and Wilson, S. H. (2001) J. Biol. Chem., 276, 32411–32414.

    Article  PubMed  CAS  Google Scholar 

  43. Sukhanova, M. V., Khodyreva, S. N., Lebedeva, N. A., Prasad, R., Wilson, S. H., and Lavrik, O. I. (2005) Nucleic Acids Res., 33, 1222–1229.

    Article  PubMed  CAS  Google Scholar 

  44. Mackey, Z. B., Niedergang, C., de Murcia, J. M., Leppard, J., Au, K., Chen, J., de Murcia G., and Tomkinson, A. E. (1999) J. Biol. Chem., 274, 21679–21687.

    Article  PubMed  CAS  Google Scholar 

  45. Eki, T., and Hurwitz, J. (1991) J. Biol. Chem., 266, 3087–3100.

    PubMed  CAS  Google Scholar 

  46. Frouin, I., Maga, G., Denegri, M., Riva, F., Savio, M., Spadari, S., Prosperi, E., and Scovassi, A. I. (2003) J. Biol. Chem., 278, 39265–39268.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Institute of Chemical Biology and Fundamental Medicine, Siberian Division of the Russian Academy of Sciences, pr. Lavrentieva 8, 630090, Novosibirsk, Russia

    M. V. Sukhanova, S. N. Khodyreva & O. I. Lavrik

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  1. M. V. Sukhanova
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  2. S. N. Khodyreva
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  3. O. I. Lavrik
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Correspondence to O. I. Lavrik.

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Original Russian Text © M. V. Sukhanova, S. N. Khodyreva, O. I. Lavrik, 2006, published in Biokhimiya, 2006, Vol. 71, No. 7, pp. 909–923.

Originally published in Biochemistry (Moscow) On-Line Papers in Press, as Manuscript BM05-222, March 26, 2006.

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Sukhanova, M.V., Khodyreva, S.N. & Lavrik, O.I. Influence of poly(ADP-ribose) polymerase-1 and its apoptotic 24-kD fragment on repair of DNA duplexes in bovine testis nuclear extract. Biochemistry (Moscow) 71, 736–748 (2006). https://doi.org/10.1134/S0006297906070066

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  • DOI: https://doi.org/10.1134/S0006297906070066

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