Advertisement

Biochemistry (Moscow)

, Volume 76, Issue 1, pp 147–156 | Cite as

Interaction of poly(ADP-ribose) polymerase 1 with apurinic/apyrimidinic sites within clustered DNA damage

  • M. M. Kutuzov
  • E. S. Ilina
  • M. V. Sukhanova
  • I. A. Pyshnaya
  • D. V. Pyshnyi
  • O. I. Lavrik
  • S. N. KhodyrevaEmail author
Article

Abstract

To study the interaction of poly(ADP-ribose) polymerase 1 (PARP1) with apurinic/apyrimidinic sites (AP sites) within clustered damages, DNA duplexes were created that contained an AP site in one strand and one of its analogs situated opposite the AP site in the complementary strand. Residues of 3-hydroxy-2-hydroxymethyltetrahydrofuran (THF), diethylene glycol (DEG), and decane-1,10-diol (DD) were used. It is shown for the first time that apurinic/apyrimidinic endonuclease 1 (APE1) cleaves the DNA strands at the positions of DEG and DD residues, and this suggests these groups as AP site analogs. Insertion of DEG and DD residues opposite an AP site decreased the rate of AP site hydrolysis by APE1 similarly to the effect of the THF residue, which is a well-known analog of the AP site, and this allowed us to use such AP DNAs to imitate DNA with particular types of clustered damages. PARP1, isolated and in cell extracts, efficiently interacted with AP DNA with analogs of AP sites producing a Schiff base. PARP1 competes with APE1 upon interaction with AP DNAs, decreasing the level of its cross-linking with AP DNA, and inhibits hydrolysis of AP sites within AP DNAs containing DEG and THF residues. Using glutaraldehyde as a linking agent, APE1 is shown to considerably decrease the amount of AP DNA-bound PARP1 dimer, which is the catalytically active form of this enzyme. Autopoly(ADP-ribosyl)ation of PARP1 decreased its inhibitory effect. The possible involvement of PARP1 and its automodification in the regulation of AP site processing within particular clustered damages is discussed.

Key words

affinity modification poly(ADP ribose) polymerase 1 Schiff base apurinic/apyrimidinic sites and their analogs 

Abbreviations

A

dAMP

APE1

human apurinic/apyrimidinic (AP) endonuclease 1

AP site

apurinic/apyrimidinic site

BER

base excision repair

DD

decane-1,10-diol residue

DEG

diethylene glycol residue

DTT

dithiothreitol

PARP1

human poly(ADP-ribose) polymerase 1

THF

3-hydroxy-2-hydroxymethyltetrahydrofuran residue

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Lindahl, T. (2000) Mutat. Res., 462, 129–135.CrossRefPubMedGoogle Scholar
  2. 2.
    Boiteux, S., and Guillet, M. (2004) DNA Repair, 3, 1–12.CrossRefPubMedGoogle Scholar
  3. 3.
    Sung, J. S., and Demple, B. (2006) FEBS J., 273, 1620–629.CrossRefPubMedGoogle Scholar
  4. 4.
    Lomax, M. E., and Gulston, M. K. (2002) Radiat. Prot. Dosimetry, 99, 63–68.PubMedGoogle Scholar
  5. 5.
    David-Cordonnier, M. H., Cunniffe, S. M., Hickson, I. D., and O’Neill, P. (2002) Biochemistry, 41, 634–642.CrossRefPubMedGoogle Scholar
  6. 6.
    Gulston, M., de Lara, C., Jenner, T., Davis, E., and O’Neill, P. (2004) Nucleic Acids Res., 32, 1602–1609.CrossRefPubMedGoogle Scholar
  7. 7.
    Shall, S., and de Murcia, G. (2000) Mutat. Res., 460, 1–15.PubMedGoogle Scholar
  8. 8.
    Lindahl, T., Satoh, M. S., Poirier, G. G., and Klungland, A. (1995) Trends Biochem. Sci., 20, 405–411.CrossRefPubMedGoogle Scholar
  9. 9.
    Khodyreva, S. N., Ilina, E. S., Sukhanova, M. V., Kutuzov, M. M., and Lavrik, O. I. (2010) Dokl. Akad. Nauk, 431, 132–135.Google Scholar
  10. 10.
    Wilson, D. M., III, and Barsky, D. (2001) Mutat. Res., 485, 283–307.PubMedGoogle Scholar
  11. 11.
    Ilina, E. S., Lavrik, O. I., and Khodyreva, S. N. (2008) Biochim. Biophys. Acta, 1784, 1777–1785.PubMedGoogle Scholar
  12. 12.
    Zharkov, D. O., and Grollman, A. P. (1998) Biochemistry, 37, 12384–12394.CrossRefPubMedGoogle Scholar
  13. 13.
    Levina, E. S., Bavykin, S. G., Shick, V. V., and Mirzabekov, A. D. (1981) Analyt. Biochem., 110, 93–101.CrossRefPubMedGoogle Scholar
  14. 14.
    Takeshita, M., Chang, C. N., Johnson, F., Will, S., and Grollman, A. P. (1987) J. Biol. Chem., 262, 10171–10179.PubMedGoogle Scholar
  15. 15.
    Erzberger, J., and Wilson, D., III. (1999) J. Mol. Biol., 290, 447–457.CrossRefPubMedGoogle Scholar
  16. 16.
    Lebedeva, N. A., Khodyreva, S. N., Favre, A., and Lavrik, O. I. (2003) Biochem. Biophys. Res. Commun., 300, 182–187.CrossRefPubMedGoogle Scholar
  17. 17.
    Sukhanova, M. V., Khodyreva, S. N., and Lavrik, O. I. (2004) Biochemistry (Moscow), 69, 558–568.CrossRefGoogle Scholar
  18. 18.
    Bradford, M. M. (1976) Analyt. Biochem., 72, 248–254.CrossRefPubMedGoogle Scholar
  19. 19.
    Pyshnaya, I. A., Pyshnyi, D. V., Lomzov, A. A., Zarytova, V. F., and Ivanova, E. M. (2004) Nucleosides, Nucleotides and Nucleic Acids, 23, 1065–1071.CrossRefGoogle Scholar
  20. 20.
    Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd Edn., Cold Spring Harbor, Cold Spring Harbor Laboratory Press, New York.Google Scholar
  21. 21.
    Laemmli, U. K. (1970) Nature, 277, 680–685.CrossRefGoogle Scholar
  22. 22.
    Chaudhry, M. A., and Weinfeld, M. (1997) J. Biol. Chem., 272, 15650–15655.CrossRefPubMedGoogle Scholar
  23. 23.
    McKenzie, J. A., and Strauss, P. R. (2001) Biochemistry, 40, 13254–13261.CrossRefPubMedGoogle Scholar
  24. 24.
    Kun, E., Kirsten, E., Mendeleyev, J., and Ordahl, C. P. (2004) Biochemistry, 43, 210–216.CrossRefPubMedGoogle Scholar
  25. 25.
    Beernink, P. T., Segelke, B. W., Hadi, M. Z., Erzberger, J. P., Wilson, D. M., III, and Rupp, B. (2001) J. Mol. Biol., 307, 1023–1034.CrossRefPubMedGoogle Scholar
  26. 26.
    Barzilay, G., Mol, C. D., Robson, C. N., Walker, L. J., Cunningham, R. P., Tainer, J. A., and Hickson, I. D. (1995) Nature Struct. Biol., 2, 561–568.CrossRefPubMedGoogle Scholar
  27. 27.
    Dyrkheeva, N. S., Khodyreva, S. N., and Lavrik, O. I. (2008) Biochemistry (Moscow), 73, 261–272.Google Scholar
  28. 28.
    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.CrossRefPubMedGoogle Scholar
  29. 29.
    Cistulli, C., Lavrik, O. I., Prasad, R., Hou, E., and Wilson, S. H. (2004) DNA Repair, 3, 581–591.PubMedGoogle Scholar
  30. 30.
    Peddi, S. R., Chattopadhyay, R., Naidu, C. V., and Izumi, T. (2006) Toxicology, 224, 44–55.CrossRefPubMedGoogle Scholar
  31. 31.
    Enguita, F. J., Liras, P., Leitao, A. L., and Martin, J. F. (1996) J. Biol. Chem., 271, 33225–33230.CrossRefPubMedGoogle Scholar
  32. 32.
    Mendoza-Alvarez, H., and Alvarez-Gonzalez, R. (1993) J. Biol. Chem., 268, 22575–22580.PubMedGoogle Scholar
  33. 33.
    Pion, E., Ullmann, G. M., Ame, J. C., Gerard, D., de Murcia, G., and Bombarda, E. (2005) Biochemistry, 44, 14670–14681.CrossRefPubMedGoogle Scholar
  34. 34.
    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.CrossRefPubMedGoogle Scholar
  35. 35.
    Sukhanova, M. V., Khodyreva, S. N., and Lavrik, O. I. (2006) Biochemistry (Moscow), 71, 736–748.CrossRefGoogle Scholar
  36. 36.
    Sukhanova, M., Khodyreva, S., and Lavrik, O. (2010) Mutat. Res., 685, 80–89.PubMedGoogle Scholar
  37. 37.
    Woodhouse, B. C., Dianova, I. I., Parsons, J. L., and Dianov, G. L. (2008) DNA Repair, 7, 932–940.CrossRefPubMedGoogle Scholar
  38. 38.
    Jorgensen, T. J. (2009) Cancer Bio. Ther., 8, 665–670.CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2011

Authors and Affiliations

  • M. M. Kutuzov
    • 1
  • E. S. Ilina
    • 1
  • M. V. Sukhanova
    • 1
  • I. A. Pyshnaya
    • 1
  • D. V. Pyshnyi
    • 1
  • O. I. Lavrik
    • 1
  • S. N. Khodyreva
    • 1
    Email author
  1. 1.Institute of Chemical Biology and Fundamental MedicineSiberian Branch of the Russian Academy of SciencesNovosibirskRussia

Personalised recommendations