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Biochemistry (Moscow)

, Volume 79, Issue 6, pp 545–554 | Cite as

Effect of point substitutions within the minimal DNA-binding domain of xeroderma pigmentosum group a protein on interaction with DNA intermediates of nucleotide excision repair

  • E. A. Maltseva
  • Y. S. Krasikova
  • H. Naegeli
  • O. I. Lavrik
  • N. I. RechkunovaEmail author
Article

Abstract

Xeroderma pigmentosum factor A (XPA) is one of the key proteins in the nucleotide excision repair (NER) process. The effects of point substitutions in the DNA-binding domain of XPA (positively charged lysine residues replaced by negatively charged glutamate residues: XPA K204E, K179E, K141E, and tandem mutant K141E/K179E) on the inter-action of the protein with DNA structures modeling intermediates of the damage recognition and pre-incision stages in NER were analyzed. All these mutations decreased the affinity of the protein to DNA, the effect depending on the substitution and the DNA structure. The mutant as well as wild-type proteins bind with highest efficiency partly open damaged DNA duplex, and the affinity of the mutants to this DNA is reduced in the order: K204E > K179E ≫ K141E = K141/179E. For all the mutants, decrease in DNA binding efficiency was more pronounced in the case of full duplex and single-stranded DNA than with bubble-DNA structure, the difference between protein affinities to different DNA structures increasing as DNA binding activity of the mutant decreased. No effect of the studied XPA mutations on the location of the protein on the partially open DNA duplex was observed using photoinduced crosslinking with 5-I-dUMP in different positions of the damaged DNA strand. These results combined with earlier published data suggest no direct correlation between DNA binding and activity in NER for these XPA mutants.

Key words

nucleotide excision repair XPA mutants DNA binding 

Abbreviations

Flu-dUMP

5-{3-[6-(carboxyamido-fluoresceinyl)amidocapromoyl]allyl}-2′-deoxyuridine 5′-monophosphate

5-I-dUMP

5-iodo-2′-deoxyuridine 5′-monophosphate

MDB-domain

minimal DNA binding domain

NER

nucleotide excision repair

RPA

replication protein A

XPA

xeroderma pigmentosum factor A

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References

  1. 1.
    Bootsma, D., Kraemer, K. H., Cleaver, J. E., and Hoeijmakers, J. H. J. (1998) in The Genetic Basis of Human Cancer (Vogelstein, B., and Kinzler, K. W., eds.) McGraw-Hill Book Co., N. Y., pp. 245–274.Google Scholar
  2. 2.
    Cleaver, J. E., and Kraemer, K. H. (1989) in The Metabolic Basis of Inherited Disease (Scriver, C. R., Beaudet, A. L., Sly, W. S., and Valle, D., eds.) McGraw-Hill Book Co., N. Y., pp. 2949–2971.Google Scholar
  3. 3.
    Reardon, J. T., and Sancar, A. (2003) Genes Dev., 17, 2539–2551.PubMedCentralPubMedCrossRefGoogle Scholar
  4. 4.
    Kesseler, K. J., Kaufmann, W. K., Reardon, J. T., Elston, T. C., and Sancar, A. (2007) J. Theor. Biol., 249, 361–375.PubMedCentralPubMedCrossRefGoogle Scholar
  5. 5.
    Park, C. J., and Choi, B. S. (2006) FEBS J., 273, 1600–1608.PubMedCrossRefGoogle Scholar
  6. 6.
    Krasikova, Y. S., Rechkunova, N. I., Maltseva, E. A., Petruseva, I. O., and Lavrik, O. I. (2010) Nucleic Acids Res., 38, 8083–8094.PubMedCentralPubMedCrossRefGoogle Scholar
  7. 7.
    Li, L., Lu, X., Peterson, C. A., and Legerski, R. J. (1995) Mol. Cell Biol., 15, 5396–5402.PubMedCentralPubMedGoogle Scholar
  8. 8.
    Li, L., Elledge, S. J., Peterson, C. A., Bales, E. S., and Legerski, R. J. (1994) Proc. Natl. Acad. Sci. USA, 91, 5012–5016.PubMedCentralPubMedCrossRefGoogle Scholar
  9. 9.
    Li, L., Peterson, C. A., Lu, X., and Legerski, R. J. (1995) Mol. Cell Biol., 15, 1993–1998.PubMedCentralPubMedGoogle Scholar
  10. 10.
    Park, C. H., Mu, D., Reardon, J. T., and Sancar, A. (1995) J. Biol. Chem., 270, 4896–4902.PubMedCrossRefGoogle Scholar
  11. 11.
    Miyamoto, I., Miura, N., Niwa, H., Miyazaki, J., and Tanaka, K. (1992) J. Biol. Chem., 267, 12182–121877.PubMedGoogle Scholar
  12. 12.
    Yang, Z. G., Liu, Y., Mao, L. Y., Zhang, J. T., and Zou, Y. (2002) Biochemistry, 41, 13012–13020.PubMedCentralPubMedCrossRefGoogle Scholar
  13. 13.
    Kuraoka, I., Morita, E. H., Saijo, M., Matsuda, T., Morikawa, K., Shirakawa, M., and Tanaka, K. (1996) Mutat. Res., 362, 87–95.PubMedCrossRefGoogle Scholar
  14. 14.
    Buchko, G. W., Ni, S., Thrall, B. D., and Kennedy, M. A. (1998) Nucleic Acids Res., 26, 2779–2788.PubMedCentralPubMedCrossRefGoogle Scholar
  15. 15.
    Ikegami, T., Kuraoka, I., Saijo, M., Kodo, N., Kyogoku, Y., Morikawa, K., Tanaka, K., and Shirakawa, M. (1998) Nat. Struct. Biol., 5, 701–706.PubMedCrossRefGoogle Scholar
  16. 16.
    Buchko, G. W., Isern, N. G., Spicer, L. D., and Kennedy, M. A. (2001) Mutat. Res., 486, 1–10.PubMedCrossRefGoogle Scholar
  17. 17.
    Camenisch, U., Dip, R., Schumacher, S. B., Schuler, B., and Naegeli, H. (2006) Nat. Struct. Mol. Biol., 13, 278–284.PubMedCrossRefGoogle Scholar
  18. 18.
    Cleaver, J. E., and States, J. C. (1997) Biochem. J., 328, 1–12.PubMedCentralPubMedGoogle Scholar
  19. 19.
    Laemmli, U. K. (1970) Nature, 227, 680–685.PubMedCrossRefGoogle Scholar
  20. 20.
    Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd Edn.Google Scholar
  21. 21.
    Riedl, T., Hanaoka, F., and Egly, J. M. (2003) EMBO J., 22, 5293–5303.PubMedCentralPubMedCrossRefGoogle Scholar
  22. 22.
    Rademakers, S., Volker, M., Hoogstraten, D., Nigg, A. L., Mone, M. J., van Zeeland, A. A., Hoeijmakers, J. H., Houtsmuller, A. B., and Vermeulen, W. (2003) Mol. Cell Biol., 23, 5755–5767.PubMedCentralPubMedCrossRefGoogle Scholar
  23. 23.
    Volker, M., Mone, M. J., Karmakar, P., van Hoffen, A., Schul, W., Vermeulen, W., Hoeijmakers, J. H., van Driel, R., van Zeeland, A. A., and Mullenders, L. H. (2001) Mol. Cell., 8, 213–224.PubMedCrossRefGoogle Scholar
  24. 24.
    Sugasawa, K., Ng, J. M., Masutani, C., Iwai, S., van der Spek, P. J., Eker, A. P., Hanaoka, F., Bootsma, D., and Hoeijmakers, J. H. (1998) Mol. Cell, 2, 223–232.PubMedCrossRefGoogle Scholar
  25. 25.
    Evans, E., Moggs, J. G., Hwang, J. R., Egly, J. M., and Wood, R. D. (1997) EMBO J., 16, 6559–6573.PubMedCentralPubMedCrossRefGoogle Scholar
  26. 26.
    Jones, C. J., and Wood, R. D. (1993) Biochemistry, 32, 12096–12104.PubMedCrossRefGoogle Scholar
  27. 27.
    Buschta-Hedayat, N., Buterin, T., Hess, M. T., Missura, M., and Naegeli, H. (1999) Proc. Natl. Acad. Sci. USA, 96, 6090–6095.PubMedCentralPubMedCrossRefGoogle Scholar
  28. 28.
    Wakasugi, M., and Sancar, A. (1999) J. Biol. Chem., 274, 18759–18768.PubMedCrossRefGoogle Scholar
  29. 29.
    Maltseva, E. A., Rechkunova, N. I., Gillet, L. C., Petruseva, I. O., Scharer, O. D., and Lavrik, O. I. (2007) Biochim. Biophys. Acta, 1770, 781–789.PubMedCrossRefGoogle Scholar
  30. 30.
    Krasikova, Y. S., Rechkunova, N. I., Maltseva, E. A., Petruseva, I. O., Silnikov, V. N., Zatsepin, T. S., Oretskaya, T. S., Scharer, O. D., and Lavrik, O. I. (2008) Biochemistry (Moscow), 73, 886–896.CrossRefGoogle Scholar
  31. 31.
    Krasikova, Y. S., Rechkunova, N. I., Maltseva, E. A., Pestryakov, P. E., Petruseva, I. O., Sugasawa, K., Chen, X., Min, J. H., and Lavrik, O. I. (2013) J. Biol. Chem., 288, 10936–10947.PubMedCentralPubMedCrossRefGoogle Scholar
  32. 32.
    Tapias, A., Auriol, J., Forget, D., Enzlin, J. H., Scharer, O. D., Coin, F., Coulombe, B., and Egly, J. M. (2004) J. Biol. Chem., 279, 19074–19083.PubMedCrossRefGoogle Scholar
  33. 33.
    Nakano, T., Katafuchi, A., Shimizu, R., Terato, H., Suzuki, T., Tauchi, H., Makino, K., Skorvaga, M., van Houten, B., and Ide, H. (2005) Nucleic Acids Res., 33, 2181–2191.PubMedCentralPubMedCrossRefGoogle Scholar
  34. 34.
    Camenisch, U., Dip, R., Vitanescu, M., and Naegeli, H. (2007) DNA Repair, 6, 1819–1828.PubMedCrossRefGoogle Scholar
  35. 35.
    Dip, R., Camenisch, U., and Naegeli, H. (2004) DNA Repair, 3, 1409–1423.PubMedCrossRefGoogle Scholar
  36. 36.
    Hey, T., Lipps, G., and Krauss, G. (2001) Biochemistry, 40, 2901–2910.PubMedCrossRefGoogle Scholar
  37. 37.
    Meisenheimer, K. M., and Koch, T. H. (1997) Crit. Rev. Biochem. Mol. Biol., 32, 101–140.PubMedCrossRefGoogle Scholar
  38. 38.
    Missura, M., Buterin, T., Hindges, R., Hubscher, U., Kasparkova, J., Brabec, V., and Naegeli, H. (2001) EMBO J., 20, 3554–3564.PubMedCentralPubMedCrossRefGoogle Scholar
  39. 39.
    Tsodikov, O. V., Ivanov, D., Orelli, B., Staresincic, L., Shoshani, I., Oberman, R., Scharer, O. D., Wagner, G., and Ellenberger, T. (2007) EMBO J., 26, 4768–4776.PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2014

Authors and Affiliations

  • E. A. Maltseva
    • 1
  • Y. S. Krasikova
    • 1
  • H. Naegeli
    • 2
  • O. I. Lavrik
    • 1
    • 3
    • 4
  • N. I. Rechkunova
    • 1
    • 3
    Email author
  1. 1.Institute of Chemical Biology and Fundamental MedicineSiberian Branch of the Russian Academy of SciencesNovosibirskRussia
  2. 2.Institute of Pharmacology and ToxicologyUniversity of Zurich-VetsuisseZurichSwitzerland
  3. 3.Novosibirsk State UniversityNovosibirskRussia
  4. 4.Altay State UniversityBarnaulRussia

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