Abstract
Nucleotide excision repair (NER) is one of the major DNA repair pathways in eukaryotic cells counteracting genetic changes caused by DNA damage. NER removes a wide set of structurally diverse lesions such as pyrimidine dimers arising upon UV irradiation and bulky chemical adducts arising upon exposure to carcinogens or chemotherapeutic drugs. NER defects lead to severe diseases including some forms of cancer. In view of the broad substrate specificity of NER, it is of interest to understand how a certain set of proteins recognizes various DNA lesions in the context of a large excess of intact DNA. This review focuses on DNA damage recognition and following stages resulting in preincision complex assembly, the key and still most unclear steps of NER. The major models of primary damage recognition and preincision complex assembly are considered. The contribution of affinity labeling techniques in study of this process is discussed.
Similar content being viewed by others
Abbreviations
- a.a.:
-
amino acid residue
- Cen2:
-
protein centrin-2
- NER:
-
nucleotide excision repair
- nt:
-
nucleotide residue
- RPA:
-
replication protein A
- XP:
-
xeroderma pigmentosum
References
Lindahl, T., and Wood, R. D. (1999) Science, 286, 1897–1905.
Hoeijmakers, J. H. (2001) Nature, 411, 366–374.
Scharer, O. D. (2003) Angew. Chem. Int. Ed. Engl., 42, 2946–2974.
Sancar, A., Lindsey-Boltz, L. A., Unsal-Kacmaz, K., and Linn, S. (2004) Annu. Rev. Biochem., 73, 39–85.
Wood, R. D., Mitchell, M., Sgouros, J., and Lindahl, T. (2001) Science, 291, 1284–1289.
Gillet, L. C., and Scharer, O. D. (2006) Chem. Rev., 106, 253–276.
Sweder, K. S., and Hanawalt, P. C. (1993) Science, 262, 439–440.
Aboussekhra, A., Biggerstaff, M., Shivji, M. K., Vilpo, J. A., Moncollin, V., Podust, V. N., Protic, M., Hubscher, U., Egly, J. M., and Wood, R. D. (1995) Cell, 80, 859–681.
Mu, D., Park, C. H., Matsunaga, T. D., Hsu, S. J., Reardon, T., and Sancar, A. (1995) J. Biol. Chem., 270, 2415–2418.
Araujo, S. J., Tirode, F., Coin, F., Pospiech, H., Syvaoja, J. E., Stucki, M., Hubscher, U., Egly, J. M., and Wood, R. D. (2000) Genes Dev., 14, 349–359.
Hoogstraten, D., Nigg, A. L., Heath, H. L., Mullenders, H., van Driel, R., Hoeijmakers, J. H., Vermeulen, W., and Houtsmuller, A. B. (2002) Mol. Cell, 10, 1163–1174.
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.
Hoogstraten, D., Bergink, S., Verbiest, V. H., Luijsterburg, M. S., Geverts, B., Raams, A., Dinant, C., Hoeijmakers, J. H., Vermeulen, W., and Houtsmuller, A. B. (2008) J. Cell. Sci., 121, 2850–2859.
Shimizu, Y., Iwai, S., Hanaoka, F., and Sugasawa, K. (2003) EMBO J., 22, 164–173.
D’Errico, M., Parlanti, E., Teson, M., de Jesus, B. M., Degan, P., Calcagnile, A., Jaruga, P., Bjoras, M., Crescenzi, M., Pedrini, A. M., Egly, J. M., Zambruno, G., Stefanini, M., Dizdaroglu, M., and Dogliotti, E. (2006) EMBO J., 25, 4305–4315.
Hiyama, H., Yokoi, M., Masutani, C., Sugasawa, K., Maekawa, T., Tanaka, K., Hoeijmakers, J. H., and Hanaoka, F. (1999) J. Biol. Chem., 274, 28019–28025.
Schaeffer, L., Roy, R., Humbert, S., Moncollin, V., Vermeulen, W., Hoeijmakers, J. H., Chambon, P., and Egly, J. M. (1993) Science, 260, 58–63.
Matsuno, M., Kose, H., Okabe, M., and Hiromi, Y. (2007) Genes Cells, 12, 1289–1300.
Zhang, N., Liu, X., Li, L., and Legerski, R. (2007) DNA Repair, 6, 1670–1678.
Klungland, A., Hoss, M., Gunz, D., Constantinou, A., Clarkson, S. G., Doetsch, P. W., Bolton, P. H., Wood, R. D., and Lindahl, T. (1999) Mol. Cell, 3, 33–42.
Bomgarden, R. D., Lupardus, P. J., Soni, D. V., Yee, M. C., Ford, J. M., and Cimprich, K. A. (2006) EMBO J., 25, 2605–2614.
Wu, X., Shell, S. M., Yan, Z., and Zou, Y. (2006) Cancer Res., 66, 2997–3005.
Wu, X., Shell, S. M., Liu, Y., and Zou, Y. (2007) Oncogene, 26, 757–764.
Wold, M. S. (1997) Annu. Rev. Biochem., 66, 61–92.
Fanning, E., Klimovich, V., and Nager, A. R. (2006) Nucleic Acids Res., 34, 4126–4137.
Pestryakov, P. E., and Lavrik, O. I. (2008) Biochemistry (Moscow), 73, 1388–1404.
Fitch, M. E., Nakajima, S., Yasui, A., and Ford, J. M. (2003) J. Biol. Chem., 278, 46906–46910.
Wang, Q. E., Zhu, Q., Wani, G., Chen, J., and Wani, A. A. (2004) Carcinogenesis, 25, 1033–1043.
Moser, J., Volker, M., Kool, H., Alekseev, S., Vrieling, H., Yasui, A., van Zeeland, A. A., and Mullenders, L. H. (2005) DNA Repair, 4, 571–582.
Nishi, R., Alekseev, S., Dinant, C., Hoogstraten, D., Houtsmuller, A. B., Hoeijmakers, J. H., Vermeulen, W., Hanaoka, F., and Sugasawa, K. (2009) DNA Repair, 8, 767–776.
Hey, T., Lipps, G., Sugasawa, K., Iwai, S., Hanaoka, F., and Krauss, G. (2002) Biochemistry, 41, 6583–6587.
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.
Batty, D., Rapic-Otrin, V. A., Levine, S., and Wood, R. D. (2000) J. Mol. Biol., 300, 275–290.
Sugasawa, K., Shimizu, Y., Iwai, S., and Hanaoka, F. (2002) DNA Repair, 1, 95–107.
Riedl, T., Hanaoka, F., and Egly, J. M. (2003) EMBO J., 22, 5293–5303.
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.
Reardon, J. T., and Sancar, A. (2003) Genes Dev., 17, 2539–2551.
Maltzeva, E. A., Rechkunova, N. I., Petruseva, I. O., Sil’nikov, V. N., Vermeulen, V., and Lavrik, O. I. (2006) Biochemistry (Moscow), 71, 270–278.
Kesseler, K. J., Kaufmann, W. K., Reardon, J. T., Elston, T. C., and Sancar, A. (2007) J. Theor. Biol., 249, 361–375.
Krasikova, U. S., Rechkunova, N. I., Maltzeva, E. A., Petruseva, I. O., Sil’nikov, V. N., Zatsepin, T. S., Oretskaya, T. S., Sherer, O. D., and Lavrik, O. I. (2008) Biochemistry (Moscow), 73, 886–896.
Van der Spek, P. J., Eker, A., Rademakers, S., Visser, C., Sugasawa, K., Masutani, C., Hanaoka, F., Bootsma, D., and Hoeijmakers, J. H. (1996) Nucleic Acids Res., 24, 2551–2559.
Araki, M., Masutani, C., Takemura, M., Uchida, A., Sugasawa, K., Kondoh, J., Ohkuma, Y., and Hanaoka, F. (2001) J. Biol. Chem., 276, 18665–18672.
Ng, J. M., Vermeulen, W., van der Horst, G. T., Bergink, S., Sugasawa, K., Vrieling, H., and Hoeijmakers, J. H. (2003) Genes Dev., 17, 1630–1645.
Sugasawa, K., Masutani, C., Uchida, A., Maekawa, T., van der Spek, P. J., Bootsma, D., Hoeijmakers, J. H., and Hanaoka, F. (1996) Mol. Cell. Biol., 16, 4852–4861.
Masutani, C., Araki, M., Sugasawa, K., van der Spek, P. J., Yamada, A., Uchida, A., Maekawa, T., Bootsma, D., Hoeijmakers, J. H., and Hanaoka, F. (1997) Mol. Cell. Biol., 17, 6915–6923.
Sugasawa, K., Ng, J. M., Masutani, C., Maekawa, T., Uchida, A., van der Spek, P. J., Eker, A. P., Rademakers, S., Visser, C., Aboussekhra, A., Wood, R. D., Hanaoka, F., Bootsma, D., and Hoeijmakers, J. H. (1997) Mol. Cell. Biol., 17, 6924–6931.
Sugasawa, K., Okuda, Y., Saijo, M., Nishi, R., Matsuda, N., Chu, G., Mori, T., Iwai, S., Tanaka, K., and Hanaoka, F. (2005) Cell, 121, 387–400.
Nishi, R., Okuda, Y., Watanabe, E., Mori, T., Iwai, S., Masutani, C., Sugasawa, K., and Hanaoka, F. (2005) Mol. Cell. Biol., 25, 5664–5674.
Kusumoto, R., Masutani, C., Sugasawa, K., Iwai, S., Araki, M., Uchida, A., Mizukoshi, T., and Hanaoka, F. (2001) Mutat. Res., 485, 219–227.
Sugasawa, K., Okamoto, T., Shimizu, Y., Masutani, C., Iwai, S., and Hanaoka, F. (2001) Genes Dev., 15, 507–521.
Buterin, T., Meyer, C., Giese, B., and Naegeli, H. (2005) Chem. Biol., 12, 913–922.
Maillard, O., Solyom, S., and Naegeli, H. (2007) PLoS Biol., 5, e79.
Min, J.-H., and Pavletich, N. P. (2007) Nature, 449, 570–575.
Maillard, O., Camenisch, U., Blagoev, K. B., and Naegeli, H. (2008) Mutat. Res., 658, 271–286.
Camenisch, U., Trautlein, D., Clement, F. C., Fei, J., Leitenstorfer, A., Ferrando-May, E., and Naegeli, H. (2009) EMBO J., 28, 2387–2399.
Sugasawa, K., Akagi, J., Nishi, R., Iwai, S., and Hanaoka, F. (2009) Mol. Cell., 36, 642–653.
Blagoev, K. B., Alexandrov, B. S., Goodwin, E. H., and Bishop, A. R. (2006) DNA Repair, 5, 863–867.
Maillard, O., Camenisch, U., Clement, F. C., Blagoev, K. B., and Naegeli, H. (2007) Trends Biochem. Sci., 32, 494–499.
Janicijevic, A., Sugasawa, K., Shimizu, Y., Hanaoka, F., Wijgers, N., Djurica, M., Hoeijmakers, J. H., and Wyman, C. (2003) DNA Repair, 2, 325–336.
Yokoi, M., Masutani, C., Maekawa, T., Sugasawa, K., Ohkuma, Y., and Hanaoka, F. (2000) J. Biol. Chem., 275, 9870–9875.
Yang, Z. G., Liu, Y., Mao, L. Y., Zhang, J. T., and Zou, Y. (2002) Biochemistry, 41, 13012–13020.
Li, L., Lu, X., Peterson, C. A., and Legerski, R. J. (1995) Mol. Cell. Biol., 15, 5396–5402.
Li, L., Elledge, S. J., Peterson, C. A., Bales, E. S., and Legerski, R. J. (1994) Proc. Natl. Acad. Sci. USA, 91, 5012–5016.
Park, C. H., Mu, D., Reardon, J. T., and Sancar, A. (1995) J. Biol. Chem., 270, 4896–4902.
Missura, M., Buterin, T., Hindges, R., Hubscher, U., Kasparkova, J., Brabec, V., and Naegeli, H. (2001) EMBO J., 20, 3554–3564.
Schweizer, U., Hey, T., Lipps, G., and Krauss, G. (1999) Nucleic Acids Res., 27, 3183–3189.
Wang, M., Mahrenholz, A., and Lee, S. (2000) Biochemistry, 39, 6433–6439.
Hey, T., Lipps, G., and Krauss, G. (2001) Biochemistry, 40, 2901–2910.
Camenisch, U., Dip, R., Schumacher, S. B., Schuler, B., and Naegeli, H. (2006) Nat. Struct. Mol. Biol., 13, 278–284.
Yang, Z., Roginskaya, M., Colis, L. C., Basu, A. K., Shell, S. M., Liu, Y., Musich, P. R., Harris, C. M., Harris, T. M., and Zou, Y. (2006) Biochemistry, 45, 15921–15930.
Saijo, M., Kuraoka, I., Masutani, C., Hanaoka, F., and Tanaka, K. (1996) Nucleic Acids Res., 24, 4719–4724.
Orelli, B., McClendon, T. B., Tsodikov, O. V., Ellenberger, T., Niedernhofer, L. J., and Scharer, O. D. (2010) J. Biol. Chem., 285, 3705–3712.
Lavrik, O. I., Kolpashchikov, D. M., Weisshart, K., Nasheuer, H. P., Khodyreva, S. N., and Favre, A. (1999) Nucleic Acids Res., 27, 4235–4240.
Bochkareva, E., Korolev, S., Lees-Miller, S. P., and Bochkarev, A. (2002) EMBO J., 21, 1855–1863.
Lavrik, O. I., Nasheuer, H. P., Weisshart, K., Wold, M. S., Prasad, R., Beard, W. A., Wilson, S. H., and Favre, A. (1998) Nucleic Acids Res., 26, 602–607.
De Laat, W. L., Appeldoorn, E., Sugasawa, K., Weterings, E., Jaspers, N. G., and Hoeijmakers, J. H. (1998) Genes Dev., 12, 2598–2609.
Kolpashchikov, D. M., Khodyreva, S. N., Khlimankov, D. Y., Wold, M. S., Favre, A., and Lavrik, O. I. (2001) Nucleic Acids Res., 29, 373–379.
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.
Hermanson-Miller, I. L., and Turchi, J. J. (2002) Biochemistry, 41, 2402–2408.
Lee, J. H., Park, C. J., Arunkumar, A. I., Chazin, W. J., and Choi, B. S. (2003) Nucleic Acids Res., 31, 4747–4754.
Patrick, S. M., and Turchi, J. J. (2002) J. Biol. Chem., 277, 16096–16101.
Gomes, X. V., and Burgers, P. M. (2001) J. Biol. Chem., 276, 34768–34775.
Della Vecchia, M. J., Croteau, D. L., Skorvaga, M., Dezhurov, S. V., Lavrik, O. I., and van Houten, B. (2004) J. Biol. Chem., 279, 45245–45256.
Khodyreva, S. N., and Lavrik, O. I. (2005) Curr. Med. Chem., 12, 641–655.
Rechkunova, N. I., and Lavrik, O. I. (2010) Subcell. Biochem., 50, 251–277.
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.
Heflich, R. H., and Neft, R. E. (1994) Mutat. Res., 318, 73–114.
Gillet, L. C., Alzeer, J., and Scharer, O. D. (2005) Nucleic Acids Res., 33, 1961–1969.
Shivji, M. K., Moggs, J. G., Kuraoka, I., and Wood, R. D. (1999) Meth. Mol. Biol., 113, 373–392.
Gunz, D., Hess, M. T., and Naegeli, H. (1996) J. Biol. Chem., 271, 25089–25098.
Geacintov, N. E., Broyde, S., Buterin, T., Naegeli, H., Wu, M., Yan, S., and Patel, D. J. (2002) Biopolymers, 65, 202–210.
Mocquet, V., Kropachev, K., Kolbanovskiy, M., Kolbanovskiy, A., Tapias, A., Cai, Y., Broyde, S., Geacintov, N. E., and Egly, J. M. (2007) EMBO J., 26, 2923–2932.
Maltseva, E. A., Rechkunova, N. I., Petruseva, I. O., Vermeulen, W., Scharer, O. D., and Lavrik, O. I. (2008) Bioorg. Chem., 36, 77–84.
Petruseva, I. O., Tikhanovich, I. S., Chelobanov, B. P., and Lavrik, O. I. (2008) J. Mol. Recognit., 21, 154–162.
Meisenheimer, K. M., and Koch, T. H. (1997) Crit. Rev. Biochem. Mol. Biol., 32, 101–140.
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.
Wakasugi, M., and Sancar, A. (1999) J. Biol. Chem., 274, 18759–18768.
Krasikova, Y. S., Rechkunova, N. I., Maltseva, E. A., Petruseva, I. O., and Lavrik, O. I. (2010) Nucleic Acids Res., 38, 8083–8094.
Salas, T. R., Petruseva, I., Lavrik, O., Bourdoncle, A., Mergny, J. L., Favre, A., and Saintome, C. (2006) Nucleic Acids Res., 34, 4857–4865.
Author information
Authors and Affiliations
Corresponding author
Additional information
Original Russian Text © N. I. Rechkunova, Yu. S. Krasikova, O. I. Lavrik, 2011, published in Biokhimiya, 2011, Vol. 76, No. 1, pp. 32–45.
Rights and permissions
About this article
Cite this article
Rechkunova, N.I., Krasikova, Y.S. & Lavrik, O.I. Nucleotide excision repair: DNA damage recognition and preincision complex assembly. Biochemistry Moscow 76, 24–35 (2011). https://doi.org/10.1134/S0006297911010056
Received:
Revised:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S0006297911010056