Biochemistry (Moscow)

, Volume 76, Issue 1, pp 4–15 | Cite as

Role of nucleotide excision repair proteins in oxidative DNA damage repair: an updating

  • B. Pascucci
  • M. D’Errico
  • E. Parlanti
  • S. Giovannini
  • E. DogliottiEmail author


DNA repair is a crucial factor in maintaining a low steady-state level of oxidative DNA damage. Base excision repair (BER) has an important role in preventing the deleterious effects of oxidative DNA damage, but recent evidence points to the involvement of several repair pathways in this process. Oxidative damage may arise from endogenous and exogenous sources and may target nuclear and mitochondrial DNA as well as RNA and proteins. The importance of preventing mutations associated with oxidative damage is shown by a direct association between defects in BER (i.e. MYH DNA glycosylase) and colorectal cancer, but it is becoming increasingly evident that damage by highly reactive oxygen species plays also central roles in aging and neurodegeneration. Mutations in genes of the nucleotide excision repair (NER) pathway are associated with diseases, such as xeroderma pigmentosum and Cockayne syndrome, that involve increased skin cancer risk and/or developmental and neurological symptoms. In this review we will provide an updating of the current evidence on the involvement of NER factors in the control of oxidative DNA damage and will attempt to address the issue of whether this unexpected role may unlock the difficult puzzle of the pathogenesis of these syndromes.

Key words

oxidative damage DNA repair oxidative metabolism xeroderma pigmentosum Cockayne syndrome 





Abelson murine leukemia kinase


ataxia oculomotor apraxia type 1


apurinic/apyrimidinic endonuclease 1


ataxia telangiectasia and Rad 3 related


base excision repair


benzo(a)pyrene diol epoxide


Cockayne syndrome


COP9 signalosome


8,5′-cyclopurine 2′-deoxynucleosides


DNA damage-binding protein


damage repair capacity


double-strand DNA breaks


embryonic stem


formamide pyrimidine adenine


formamide pyrimidine guanine


formamidopyrimidine DNA glycosylase


global genome repair


host cell reactivation


high-mobility group nucleosome binding domain 1


4-hydroxy-2-nonenal-modified protein


mouse embryo fibroblasts


mitochondrial single stranded DNA binding protein


nei endonuclease VIII-like 1


nucleotide excision repair


8-oxoguanine DNA glycosylase






poly(ADP-ribose) polymerase 1


proliferating cell nuclear antigen


PiggyBac transposable element-derived protein 3


RNA polymerase II


reactive oxygen species


replication protein A


spinocerebellar ataxia with axonal neuropathy


sirtuin 1


single-strand-specific monofunctional uracil-DNA glycosylases


single nucleotide polymorphisms


superoxide dismutase


single-strand DNA breaks


transcription-coupled repair


thymine DNA glycosylase


transcription factor H-II


transcription factor S-II


thymine glycol


transglutaminase-homology domain


UV sensitive syndrome


XPA binding protein 2


xeroderma pigmentosum


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Scharer, O. D. (2008) Adv. Exp. Med. Biol., 637, 83–92.PubMedGoogle Scholar
  2. 2.
    Masutani, C., Sugasawa, K., Yanagisawa, J., Sonoyama, T., Ui, M., Enomoto, T., Takio, K., Tanaka, K., van der Spek, P. J., Bootsma, D., et al. (1994) EMBO J., 13, 1831–1843.PubMedGoogle Scholar
  3. 3.
    Camenisch, U., Trautlein, D., Clement, F. C., Fei, J., Leitenstorfer, A., Ferrando-May, E., and Naegeli, H. (2009) EMBO J., 28, 2387–2399.PubMedGoogle Scholar
  4. 4.
    Min, J. H., and Pavletich, N. P. (2007) Nature, 449, 570–575.PubMedGoogle Scholar
  5. 5.
    Yokoi, T., Ohmichi, M., Tasaka, K., Kimura, A., Kanda, Y., Hayakawa, J., Tahara, M., Hisamoto, K., Kurachi, H., and Murata, Y. (2000) J. Biol. Chem., 275, 21639–21647.PubMedGoogle Scholar
  6. 6.
    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.PubMedGoogle Scholar
  7. 7.
    Araki, M., Masutani, C., Takemura, M., Uchida, A., Sugasawa, K., Kondoh, J., Ohkuma, Y., and Hanaoka, F. (2001) J. Biol. Chem., 276, 18665–18672.PubMedGoogle Scholar
  8. 8.
    Charbonnier, J. B., Renaud, E., Miron, S., Le Du, M. H., Blouquit, Y., Duchambon, P., Christova, P., Shosheva, A., Rose, T., Angulo, J. F., and Craescu, C. T. (2007) J. Mol. Biol., 373, 1032–1046.PubMedGoogle Scholar
  9. 9.
    Popescu, A., Miron, S., Blouquit, Y., Duchambon, P., Christova, P., and Craescu, C. T. (2003) J. Biol. Chem., 278, 40252–40261.PubMedGoogle Scholar
  10. 10.
    Miao, F., Bouziane, M., Dammann, R., Masutani, C., Hanaoka, F., Pfeifer, G., and O’Connor, T. R. (2000) J. Biol. Chem., 275, 28433–28438.PubMedGoogle Scholar
  11. 11.
    Shimizu, Y., Iwai, S., Hanaoka, F., and Sugasawa, K. (2003) EMBO J., 22, 164–173.PubMedGoogle Scholar
  12. 12.
    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.PubMedGoogle Scholar
  13. 13.
    Hill, J. W., Hazra, T. K., Izumi, T., and Mitra, S. (2001) Nucleic Acids Res., 29, 430–438.PubMedGoogle Scholar
  14. 14.
    Shimizu, Y., Uchimura, Y., Dohmae, N., Saitoh, H., Hanaoka, F., and Sugasawa, K. (2010) J. Nucleic Acids, ID805698.Google Scholar
  15. 15.
    Brown, K. L., Roginskaya, M., Zou, Y., Altamirano, A., Basu, A. K., and Stone, M. P. (2010) Nucleic Acids Res., 38, 428–440.PubMedGoogle Scholar
  16. 16.
    Yasuda, G., Nishi, R., Watanabe, E., Mori, T., Iwai, S., Orioli, D., Stefanini, M., Hanaoka, F., and Sugasawa, K. (2007) Mol. Cell Biol., 27, 6606–6614.PubMedGoogle Scholar
  17. 17.
    Bernardes de Jesus, B. M., Bjoras, M., Coin, F., and Egly, J.M. (2008) Mol. Cell Biol., 28, 7225–7235.PubMedGoogle Scholar
  18. 18.
    Melis, J. P., Wijnhoven, S. W., Beems, R. B., Roodbergen, M., van den Berg, J., Moon, H., Friedberg, E., van der Horst, G. T., Hoeijmakers, J. H., Vijg, J., and van Steeg, H. (2008) Cancer Res., 68, 1347–1353.PubMedGoogle Scholar
  19. 19.
    Kassam, S. N., and Rainbow, A. J. (2007) Biochem. Biophys. Res. Commun., 359, 1004–1009.PubMedGoogle Scholar
  20. 20.
    Quilliet, X., Chevallier-Lagente, O., Zeng, L., Calvayrac, R., Mezzina, M., Sarasin, A., and Vuillaume, M. (1997) Mutat. Res., 385, 235–242.PubMedGoogle Scholar
  21. 21.
    Liu, S. Y., Wen, C. Y., Lee, Y. J., and Lee, T. C. (2010) Toxicol. Sci., 116, 183–193.PubMedGoogle Scholar
  22. 22.
    Sands, A. T., Abuin, A., Sanchez, A., Conti, C. J., and Bradley, A. (1995) Nature, 377, 162–165.PubMedGoogle Scholar
  23. 23.
    Hoogervorst, E. M., van Oostrom, C. T., Beems, R. B., van Benthem, J., van den Berg, J., van Kreijl, C. F., Vos, J. G., de Vries, A., and van Steeg, H. (2005) DNA Repair (Amst.), 4, 3–9.Google Scholar
  24. 24.
    Wijnhoven, S. W., Kool, H. J., Mullenders, L. H., van Zeeland, A. A., Friedberg, E. C., van der Horst, G. T., van Steeg, H., and Vrieling, H. (2000) Oncogene, 19, 5034–5037.PubMedGoogle Scholar
  25. 25.
    Friedberg, E. C. (2004) DNA Repair (Amst.), 3, 183–195.Google Scholar
  26. 26.
    Brooks, P. J. (2008) DNA Repair (Amst.), 7, 1168–1179.Google Scholar
  27. 27.
    Giglia, G., Dumaz, N., Drougard, C., Avril, M.-F., Daya-Grosjean, L., and Sarasin, A. (1998) Cancer Res., 58, 4402–4409.PubMedGoogle Scholar
  28. 28.
    Agar, N. S., Halliday, G. M., Barnetson, R. S., Ananthaswamy, H. N., Wheeler, M., and Jones, A. M. (2004) Proc. Natl. Acad. Sci. USA, 101, 4954–4959.PubMedGoogle Scholar
  29. 29.
    Shen, H., Sturgis, E. M., Khan, S. G., Qiao, Y., Shahlavi, T., Eicher, S. A., Xu, Y., Wang, X., Strom, S. S., Spitz, M. R., Kraemer, K. H., and Wei, Q. (2001) Cancer Res., 61, 3321–3325.PubMedGoogle Scholar
  30. 30.
    Marin, M. S., Lopez-Cima, M. F., Garcia-Castro, L., Pascual, T., Marron, M. G., and Tardon, A. (2004) Cancer Epidemiol. Biomarkers Prev., 13, 1788–1793.PubMedGoogle Scholar
  31. 31.
    Shen, M. R., Hsu, Y. M., Hsu, K. F., Chen, Y. F., Tang, M. J., and Chou, C. Y. (2006) Carcinogenesis, 27, 962–971.PubMedGoogle Scholar
  32. 32.
    Qiao, Y., Spitz, M. R., Shen, H., Guo, Z., Shete, S., Hedayati, M., Grossman, L., Mohrenweiser, H., and Wei, Q. (2002) Carcinogenesis, 23, 295–299.PubMedGoogle Scholar
  33. 33.
    Sanyal, S., Festa, F., Sakano, S., Zhang, Z., Steineck, G., Norming, U., Wijkstrom, H., Larsson, P., Kumar, R., and Hemminki, K. (2004) Carcinogenesis, 25, 729–734.PubMedGoogle Scholar
  34. 34.
    Palli, D., Polidoro, S., D’Errico, M., Saieva, C., Guarrera, S., Calcagnile, A. S., Sera, F., Allione, A., Gemma, S., Zanna, I., Filomena, A., Testai, E., Caini, S., Moretti, R., Gomez-Miguel, M. J., Nesi, G., Luzzi, I., Ottini, L., Masala, G., Matullo, G., and Dogliotti, E. (2010) Mutagenesis, Epub ahead of print.Google Scholar
  35. 35.
    Kuraoka, I., Morita, E. H., Saijo, M., Matsuda, T., Morikawa, K., Shirakawa, M., and Tanaka, K. (1996) Mutat. Res., 362, 87–95.PubMedGoogle Scholar
  36. 36.
    Missura, M., Buterin, T., Hindges, R., Hubscher, U., Kasparkova, J., Brabec, V., and Naegeli, H. (2001) EMBO J., 20, 3554–3564.PubMedGoogle Scholar
  37. 37.
    Ikegami, T., Kuraoka, I., Saijo, M., Kodo, N., Kyogoku, Y., Morikawa, K., Tanaka, K., and Shirakawa, M. (1998) Nat. Struct. Biol., 5, 701–706.PubMedGoogle Scholar
  38. 38.
    Buchko, G. W., Daughdrill, G. W., de Lorimier, R., Rao, B. K., Isern, N. G., Lingbeck, J. M., Taylor, J. S., Wold, M. S., Gochin, M., Spicer, L. D., Lowry, D. F., and Kennedy, M. A. (1999) Biochemistry, 38, 15116–15128.PubMedGoogle Scholar
  39. 39.
    Yang, Z. G., Liu, Y., Mao, L. Y., Zhang, J. T., and Zou, Y. (2002) Biochemistry, 41, 13012–13020.PubMedGoogle Scholar
  40. 40.
    Gillet, L. C., and Scharer, O. D. (2006) Chem. Rev., 106, 253–276.PubMedGoogle Scholar
  41. 41.
    Wu, X., Shell, S. M., Yang, Z., and Zou, Y. (2006) Cancer Res., 66, 2997–3005.PubMedGoogle Scholar
  42. 42.
    Wu, X., Shell, S. M., Liu, Y., and Zou, Y. (2007) Oncogene, 26, 757–764.PubMedGoogle Scholar
  43. 43.
    Shell, S. M., Li, Z., Shkriabai, N., Kvaratskhelia, M., Brosey, C., Serrano, M. A., Chazin, W. J., Musich, P. R., and Zou, Y. (2009) J. Biol. Chem., 284, 24213–24222.PubMedGoogle Scholar
  44. 44.
    Fan, W., and Luo, J. (2010) Mol. Cell, 39, 247–258.PubMedGoogle Scholar
  45. 45.
    He, W., Wang, Y., Zhang, M. Z., You, L., Davis, L. S., Fan, H., Yang, H. C., Fogo, A. B., Zent, R., Harris, R. C., Breyer, M. D., and Hao, C. M. (2010) J. Clin. Invest., 120, 1056–1068.PubMedGoogle Scholar
  46. 46.
    States, J. C., McDuffie, E. R., Myrand, S. P., McDowell, M., and Cleaver, J. E. (1998) Hum. Mutat., 12, 103–113.PubMedGoogle Scholar
  47. 47.
    De Waard, H., de Wit, J., Gorgels, T. G., van den Aardweg, G., Andressoo, J. O., Vermeij, M., van Steeg, H., Hoeijmakers, J. H., and van der Horst, G. T. (2003) DNA Repair (Amst.), 2, 13–25.Google Scholar
  48. 48.
    De Waard, H., Sonneveld, E., de Wit, J., Esveldt-van Lange, R., Hoeijmakers, J. H., Vrieling, H., and van der Horst, G. T. (2008) DNA Repair (Amst.), 7, 1659–1669.Google Scholar
  49. 49.
    Wang, H. T., Choi, B., and Tang, M. S. (2010) Proc. Natl. Acad. Sci. USA, 107, 12180–12185.PubMedGoogle Scholar
  50. 50.
    De Vries, A., van Oostrom, C. T., Hofhuis, F. M., Dortant, P. M., Berg, R. J., de Gruijl, F. R., Wester, P. W., van Kreijl, C. F., Capel, P. J., van Steeg, H., et al. (1995) Nature, 377, 169–173.PubMedGoogle Scholar
  51. 51.
    De Vries, A., Dolle, M. E., Broekhof, J. L., Muller, J. J., Kroese, E. D., van Kreijl, C. F., Capel, P. J., Vijg, J., and van Steeg, H. (1997) Carcinogenesis, 18, 2327–2332.PubMedGoogle Scholar
  52. 52.
    Takahashi, Y., Nakatsuru, Y., Zhang, S., Shimizu, Y., Kume, H., Tanaka, K., Ide, F., and Ishikawa, T. (2002) Carcinogenesis, 23, 627–633.PubMedGoogle Scholar
  53. 53.
    Wijnhoven, S. W., Hoogervorst, E. M., de Waard, H., van der Horst, G. T., and van Steeg, H. (2007) Mutat. Res., 614, 77–94.PubMedGoogle Scholar
  54. 54.
    Murai, M., Enokido, Y., Inamura, N., Yoshino, M., Nakatsu, Y., van der Horst, G. T., Hoeijmakers, J. H., Tanaka, K., and Hatanaka, H. (2001) Proc. Natl. Acad. Sci. USA, 98, 13379–13384.PubMedGoogle Scholar
  55. 55.
    Andrews, A. D., Barrett, S. F., and Robbins, J. H. (1978) Proc. Natl. Acad. Sci. USA, 75, 1984–1988.PubMedGoogle Scholar
  56. 56.
    Kraemer, K. H., Lee, M. M., and Scotto, J. (1987) Arch. Dermatol., 123, 241–249.PubMedGoogle Scholar
  57. 57.
    Anttinen, A., Koulu, L., Nikoskelainen, E., Portin, R., Kurki, T., Erkinjuntti, M., Jaspers, N. G., Raams, A., Green, M. H., Lehmann, A. R., Wing, J. F., Arlett, C. F., and Marttila, R. J. (2008) Brain, 131, 1979–1989.PubMedGoogle Scholar
  58. 58.
    Hayashi, M., Araki, S., Kohyama, J., Shioda, K., and Fukatsu, R. (2005) Brain Dev., 27, 34–38.PubMedGoogle Scholar
  59. 59.
    Brooks, P. J. (2007) Neuroscience, 145, 1407–1417.PubMedGoogle Scholar
  60. 60.
    Dusinska, M., Dzupinkova, Z., Wsolova, L., Harrington, V., and Collins, A. R. (2006) Mutagenesis, 21, 205–211.PubMedGoogle Scholar
  61. 61.
    Pavanello, S., Pulliero, A., Siwinska, E., Mielzynska, D., and Clonfero, E. (2005) Carcinogenesis, 26, 169–175.PubMedGoogle Scholar
  62. 62.
    Lin, J., Swan, G. E., Shields, P. G., Benowitz, N. L., Gu, J., Amos, C. I., de Andrade, M., Spitz, M. R., and Wu, X. (2007) Cancer Epidemiol. Biomarkers Prev., 16, 2065–2071.PubMedGoogle Scholar
  63. 63.
    Park, J. Y., Park, S. H., Choi, J. E., Lee, S. Y., Jeon, H. S., Cha, S. I., Kim, C. H., Park, J. H., Kam, S., Park, R. W., Kim, I. S., and Jung, T. H. (2002) Cancer Epidemiol. Biomarkers Prev., 11, 993–997.PubMedGoogle Scholar
  64. 64.
    Wu, X., Zhao, H., Wei, Q., Amos, C. I., Zhang, K., Guo, Z., Qiao, Y., Hong, W. K., and Spitz, M. R. (2003) Carcinogenesis, 24, 505–509.PubMedGoogle Scholar
  65. 65.
    Butkiewicz, D., Popanda, O., Risch, A., Edler, L., Dienemann, H., Schulz, V., Kayser, K., Drings, P., Bartsch, H., and Schmezer, P. (2004) Cancer Epidemiol. Biomarkers Prev., 13, 2242–2246.PubMedGoogle Scholar
  66. 66.
    Neer, E. J., Schmidt, C. J., Nambudripad, R., and Smith, T. F. (1994) Nature, 371, 297–300.PubMedGoogle Scholar
  67. 67.
    Christiansen, M., Stevnsner, T., Modin, C., Martensen, P. M., Brosh, R. M., Jr., and Bohr, V. A. (2003) Nucleic Acids Res., 31, 963–973.PubMedGoogle Scholar
  68. 68.
    Selby, C. P., and Sancar, A. (1997) Proc. Natl. Acad. Sci. USA, 94, 11205–11209.PubMedGoogle Scholar
  69. 69.
    Tantin, D., Kansal, A., and Carey, M. (1997) Mol. Cell Biol., 17, 6803–6814.PubMedGoogle Scholar
  70. 70.
    Van Gool, A. J., Citterio, E., Rademakers, S., van Os, R., Vermeulen, W., Constantinou, A., Egly, J. M., Bootsma, D., and Hoeijmakers, J. H. (1997) Embo J., 16, 5955–5965.PubMedGoogle Scholar
  71. 71.
    Bradsher, J., Auriol, J., Proietti de Santis, L., Iben, S., Vonesch, J. L., Grummt, I., and Egly, J. M. (2002) Mol. Cell, 10, 819–829.PubMedGoogle Scholar
  72. 72.
    Yuan, X., Feng, W., Imhof, A., Grummt, I., and Zhou, Y. (2007) Mol. Cell, 27, 585–595.PubMedGoogle Scholar
  73. 73.
    Balajee, A. S., May, A., Dianov, G. L., Friedberg, E. C., and Bohr, V. A. (1997) Proc. Natl. Acad. Sci. USA, 94, 4306–4311.PubMedGoogle Scholar
  74. 74.
    Proietti-De-Santis, L., Drane, P., and Egly, J. M. (2006) EMBO J., 25, 1915–1923.PubMedGoogle Scholar
  75. 75.
    Filippi, S., Latini, P., Frontini, M., Palitti, F., Egly, J. M., and Proietti-De-Santis, L. (2008) EMBO J., 27, 2545–2556.PubMedGoogle Scholar
  76. 76.
    Stevnsner, T., Muftuoglu, M., Aamann, M. D., and Bohr, V. A. (2008) Mech. Ageing Dev., 129, 441–448.PubMedGoogle Scholar
  77. 77.
    Groisman, R., Polanowska, J., Kuraoka, I., Sawada, J., Saijo, M., Drapkin, R., Kisselev, A. F., Tanaka, K., and Nakatani, Y. (2003) Cell, 113, 357–367.PubMedGoogle Scholar
  78. 78.
    Fousteri, M., Vermeulen, W., van Zeeland, A. A., and Mullenders, L. H. (2006) Mol. Cell, 23, 471–482.PubMedGoogle Scholar
  79. 79.
    Anindya, R., Mari, P. O., Kristensen, U., Kool, H., Giglia-Mari, G., Mullenders, L. H., Fousteri, M., Vermeulen, W., Egly, J. M., and Svejstrup, J. Q. (1010) Mol. Cell, 38, 637–648.Google Scholar
  80. 80.
    Tuo, J., Muftuoglu, M., Chen, C., Jaruga, P., Selzer, R. R., Brosh, R. M., Jr., Rodriguez, H., Dizdaroglu, M., and Bohr, V. A. (2001) J. Biol. Chem., 276, 45772–45779.PubMedGoogle Scholar
  81. 81.
    Tuo, J., Jaruga, P., Rodriguez, H., Dizdaroglu, M., and Bohr, V. A. (2002) J. Biol. Chem., 277, 30832–30837.PubMedGoogle Scholar
  82. 82.
    Muftuoglu, M., de Souza-Pinto, N. C., Dogan, A., Aamann, M., Stevnsner, T., Rybanska, I., Kirkali, G., Dizdaroglu, M., and Bohr, V. A. (2009) J. Biol. Chem., 284, 9270–9279.PubMedGoogle Scholar
  83. 83.
    Thorslund, T., von Kobbe, C., Harrigan, J. A., Indig, F. E., Christiansen, M., Stevnsner, T., and Bohr, V. A. (2005) Mol. Cell Biol., 25, 7625–7636.PubMedGoogle Scholar
  84. 84.
    Wong, H. K., Muftuoglu, M., Beck, G., Imam, S. Z., Bohr, V. A., and Wilson, D. M., 3rd. (2007) Nucleic Acids Res., 35, 4103–4113.PubMedGoogle Scholar
  85. 85.
    Kamenisch, Y., Fousteri, M., Knoch, J., von Thaler, A. K., Fehrenbacher, B., Kato, H., Becker, T., Dolle, M. E., Kuiper, R., Majora, M., Schaller, M., van der Horst, G. T., van Steeg, H., Rocken, M., Rapaport, D., Krutmann, J., Mullenders, L. H., and Berneburg, M. (2010) J. Exp. Med., 207, 379–390.PubMedGoogle Scholar
  86. 86.
    Imam, S. Z., Indig, F. E., Cheng, W. H., Saxena, S. P., Stevnsner, T., Kufe, D., and Bohr, V. A. (2007) Nucleic Acids Res., 35, 4941–4951.PubMedGoogle Scholar
  87. 87.
    Licht, C. L., Stevnsner, T., and Bohr, V. A. (2003) Am. J. Hum. Genet., 73, 1217–1239.PubMedGoogle Scholar
  88. 88.
    Nardo, T., Oneda, R., Spivak, G., Vaz, B., Mortier, L., Thomas, P., Orioli, D., Laugel, V., Stary, A., Hanawalt, P. C., Sarasin, A., and Stefanini, M. (2009) Proc. Natl. Acad. Sci. USA, 106, 6209–6214.PubMedGoogle Scholar
  89. 89.
    De Waard, H., de Wit, J., Andressoo, J. O., van Oostrom, C. T., Riis, B., Weimann, A., Poulsen, H. E., van Steeg, H., Hoeijmakers, J. H., and van der Horst, G. T. (2004) Mol. Cell Biol., 24, 7941–7948.PubMedGoogle Scholar
  90. 90.
    Leadon, S. A., and Cooper, P. K. (1993) Proc. Natl. Acad. Sci. USA, 90, 10499–10503.PubMedGoogle Scholar
  91. 91.
    Ropolo, M., Degan, P., Foresta, M., D’Errico, M., Lasiglie, D., Dogliotti, E., Casartelli, G., Zupo, S., Poggi, A., and Frosina, G. (2007) Free Radic. Biol. Med., 42, 1807–1817.PubMedGoogle Scholar
  92. 92.
    D’Errico, M., Parlanti, E., Teson, M., Degan, P., Lemma, T., Calcagnile, A., Iavarone, I., Jaruga, P., Ropolo, M., Pedrini, A. M., Orioli, D., Frosina, G., Zambruno, G., Dizdaroglu, M., Stefanini, M., and Dogliotti, E. (2007) Oncogene, 26, 4336–4343.PubMedGoogle Scholar
  93. 93.
    Spivak, G., and Hanawalt, P. C. (2006) DNA Repair (Amst.), 5, 13–22.Google Scholar
  94. 94.
    Osterod, M., Larsen, E., Le Page, F., Hengstler, J. G., van der Horst, G. T., Boiteux, S., Klungland, A., and Epe, B. (2002) Oncogene, 21, 8232–8239.PubMedGoogle Scholar
  95. 95.
    Citterio, E., van den Boom, V., Schnitzler, G., Kanaar, R., Bonte, E., Kingston, R. E., Hoeijmakers, J. H., and Vermeulen, W. (2000) Mol. Cell Biol., 20, 7643–7653.PubMedGoogle Scholar
  96. 96.
    Newman, J. C., Bailey, A. D., and Weiner, A. M. (2006) Proc. Natl. Acad. Sci. USA, 103, 9613–9618.PubMedGoogle Scholar
  97. 97.
    Mosesso, P., Penna, S., Pepe, G., Lorenti-Garcia, C., and Palitti, F. (2004) Cytogenet. Genome Res., 104, 178–181.PubMedGoogle Scholar
  98. 98.
    Kyng, K. J., May, A., Brosh, R. M., Jr., Cheng, W. H., Chen, C., Becker, K. G., and Bohr, V. A. (2003) Oncogene, 22, 1135–1149.PubMedGoogle Scholar
  99. 99.
    Dianov, G., Bischoff, C., Sunesen, M., and Bohr, V. A. (1999) Nucleic Acids Res., 27, 1365–1368.PubMedGoogle Scholar
  100. 100.
    Van der Horst, G. T., van Steeg, H., Berg, R. J., van Gool, A. J., de Wit, J., Weeda, G., Morreau, H., Beems, R. B., van Kreijl, C. F., de Gruijl, F. R., Bootsma, D., and Hoeijmakers, J. H. (1997) Cell, 89, 425–435.PubMedGoogle Scholar
  101. 101.
    Van der Horst, G. T., Meira, L., Gorgels, T. G., de Wit, J., Velasco-Miguel, S., Richardson, J. A., Kamp, Y., Vreeswijk, M. P., Smit, B., Bootsma, D., Hoeijmakers, J. H., and Friedberg, E. C. (2002) DNA Repair (Amst.), 1, 143–157.Google Scholar
  102. 102.
    Berg, R. J., Rebel, H., van der Horst, G. T., van Kranen, H. J., Mullenders, L. H., van Vloten, W. A., and de Gruijl, F. R. (2000) Cancer Res., 60, 2858–2863.PubMedGoogle Scholar
  103. 103.
    Gorgels, T. G., van der Pluijm, I., Brandt, R. M., Garinis, G. A., van Steeg, H., van den Aardweg, G., Jansen, G. H., Ruijter, J. M., Bergen, A. A., van Norren, D., Hoeijmakers, J. H., and van der Horst, G. T. (2007) Mol. Cell Biol., 27, 1433–1441.PubMedGoogle Scholar
  104. 104.
    Wong, A. W., McCallum, G. P., Jeng, W., and Wells, P. G. (2008) J. Neurosci., 28, 9047–9054.PubMedGoogle Scholar
  105. 105.
    McCallum, G. P., Wong, A. W., and Wells, P. G. (2010) Antioxid. Redox Signal., Epub ahead of print.Google Scholar
  106. 106.
    Trapp, C., Schwarz, M., and Epe, B. (2007) Cancer Res., 67, 5156–5161.PubMedGoogle Scholar
  107. 107.
    Osenbroch, P. O., Auk-Emblem, P., Halsne, R., Strand, J., Forstrom, R. J., van der Pluijm, I., and Eide, L. (2009) FEBS J., 276, 2811–2821.PubMedGoogle Scholar
  108. 108.
    Aamann, M. D., Sorensen, M. M., Hvitby, C., Berquist, B. R., Muftuoglu, M., Tian, J., de Souza-Pinto, N. C., Scheibye-Knudsen, M., Wilson, D. M., 3rd, Stevnsner, T., and Bohr, V. A. (2010) FASEB J., 24, 2334–2346.PubMedGoogle Scholar
  109. 109.
    Itoh, T., Ono, T., and Yamaizumi, M. (1994) Mutat. Res., 314, 233–248.PubMedGoogle Scholar
  110. 110.
    Hayashi, M., Itoh, M., Araki, S., Kumada, S., Shioda, K., Tamagawa, K., Mizutani, T., Morimatsu, Y., Minagawa, M., and Oda, M. (2001) J. Neuropathol. Exp. Neurol., 60, 350–356.PubMedGoogle Scholar
  111. 111.
    Stevnsner, T., Nyaga, S., de Souza-Pinto, N. C., van der Horst, G. T., Gorgels, T. G., Hogue, B. A., Thorslund, T., and Bohr, V. A. (2002) Oncogene, 21, 8675–8682.PubMedGoogle Scholar
  112. 112.
    Laugel, V., Dalloz, C., Durand, M., Sauvanaud, F., Kristensen, U., Vincent, M. C., Pasquier, L., Odent, S., Cormier-Daire, V., Gener, B., Tobias, E. S., Tolmie, J. L., Martin-Coignard, D., Drouin-Garraud, V., Heron, D., Journel, H., Raffo, E., Vigneron, J., Lyonnet, S., Murday, V., Gubser-Mercati, D., Funalot, B., Brueton, L., Sanchez Del Pozo, J., Munoz, E., Gennery, A. R., Salih, M., Noruzinia, M., Prescott, K., Ramos, L., Stark, Z., Fieggen, K., Chabrol, B., Sarda, P., Edery, P., Bloch-Zupan, A., Fawcett, H., Pham, D., Egly, J. M., Lehmann, A. R., Sarasin, A., and Dollfus, H. (2010) Hum. Mutat., 31, 113–126.PubMedGoogle Scholar
  113. 113.
    Ma, H., Hu, Z., Wang, H., Jin, G., Wang, Y., Sun, W., Chen, D., Tian, T., Jin, L., Wei, Q., Lu, D., Huang, W., and Shen, H. (2009) Cancer Lett., 273, 172–176.PubMedGoogle Scholar
  114. 114.
    Cleaver, J. E., Hefner, E., Laposa, R. R., Karentz, D., and Marti, T. (2007) Neuroscience, 145, 1300–1308.PubMedGoogle Scholar
  115. 115.
    Van der Pluijm, I., Garinis, G. A., Brandt, R. M., Gorgels, T. G., Wijnhoven, S. W., Diderich, K. E., de Wit, J., Mitchell, J. R., van Oostrom, C., Beems, R., Niedernhofer, L. J., Velasco, S., Friedberg, E. C., Tanaka, K., van Steeg, H., Hoeijmakers, J. H., and van der Horst, G. T. (2007) PLoS Biol., 6, e304.Google Scholar
  116. 116.
    Le May, N., Mota-Fernandes, D., Velez-Cruz, R., Iltis, I., Biard, D., and Egly, J. M. (2010) Mol. Cell, 38, 54–66.PubMedGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2011

Authors and Affiliations

  • B. Pascucci
    • 1
    • 2
  • M. D’Errico
    • 2
  • E. Parlanti
    • 2
  • S. Giovannini
    • 2
  • E. Dogliotti
    • 2
    Email author
  1. 1.Istituto di CristallografiaConsiglio Nazionale delle RicercheMonterotondo Stazione, RomeItaly
  2. 2.Department of Environment and Primary PreventionIstituto Superiore di SanitàRomeItaly

Personalised recommendations