Table of Contents Author Guidelines Submit a Manuscript
Journal of Nucleic Acids
Volume 2010, Article ID 174252, 9 pages
http://dx.doi.org/10.4061/2010/174252
Review Article

Base Sequence Context Effects on Nucleotide Excision Repair

1Department of Biology, New York University, New York, NY 10003, USA
2Structural Biology Program, Memorial Sloan-Kettering Cancer Center, New York, NY 10021, USA
3Department of Chemistry, New York University, New York, NY 10003, USA

Received 16 May 2010; Accepted 16 June 2010

Academic Editor: Ashis Basu

Copyright © 2010 Yuqin Cai et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. E. C. Friedberg, G. C. Walker et al., DNA Repair and Mutagenesis, ASM Press, Wahsington, DC, USA, 2006.
  2. L. C. J. Gillet and O. D. Schärer, “Molecular mechanisms of mammalian global genome nucleotide excision repair,” Chemical Reviews, vol. 106, no. 2, pp. 253–276, 2006. View at Publisher · View at Google Scholar · View at Scopus
  3. K. H. Kraemer, N. J. Patronas, R. Schiffmann, B. P. Brooks, D. Tamura, and J. J. DiGiovanna, “Xeroderma pigmentosum, trichothiodystrophy and Cockayne syndrome: a complex genotype-phenotype relationship,” Neuroscience, vol. 145, no. 4, pp. 1388–1396, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. J. E. Cleaver, “Cancer in xeroderma pigmentosum and related disorders of DNA repair,” Nature Reviews Cancer, vol. 5, no. 7, pp. 564–573, 2005. View at Publisher · View at Google Scholar · View at Scopus
  5. L. P. Martin, T. C. Hamilton, and R. J. Schilder, “Platinum resistance: the role of DNA repair pathways,” Clinical Cancer Research, vol. 14, no. 5, pp. 1291–1295, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. C. Li, L. E. Wang, and Q. Wie, “DNA repair phenotype and cancer susceptibility—a mini review,” International Journal of Cancer, vol. 124, no. 5, pp. 999–1007, 2009. View at Publisher · View at Google Scholar · View at Scopus
  7. F. Wang, Y. He, H. Guo et al., “Genetic variants of nucleotide excision repair genes are associated with DNA damage in coke oven workers,” Cancer Epidemiology Biomarkers and Prevention, vol. 19, no. 1, pp. 211–218, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. P. A. Bradbury, M. H. Kulke, R. S. Heist et al., “Cisplatin pharmacogenetics, DNA repair polymorphisms, and esophageal cancer outcomes,” Pharmacogenetics and Genomics, vol. 19, no. 8, pp. 613–625, 2009. View at Publisher · View at Google Scholar · View at Scopus
  9. T. Nouspikel, “Nucleotide excision repair: variations on versatility,” Cellular and Molecular Life Sciences, vol. 66, no. 6, pp. 994–1009, 2009. View at Publisher · View at Google Scholar · View at Scopus
  10. K. Sugasawa, “Regulation of damage recognition in mammalian global genomic nucleotide excision repair,” Mutation Research, vol. 685, no. 1-2, pp. 29–37, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. D. A. Scicchitano, “Transcription past DNA adducts derived from polycyclic aromatic hydrocarbons,” Mutation Research, vol. 577, no. 1-2, pp. 146–154, 2005. View at Publisher · View at Google Scholar · View at Scopus
  12. P. C. Hanawalt and G. Spivak, “Transcription-coupled DNA repair: two decades of progress and surprises,” Nature Reviews Molecular Cell Biology, vol. 9, no. 12, pp. 958–970, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. S. Tornaletti, “DNA repair in mammalian cells: transcription-coupled DNA repair: directing your effort where it's most needed,” Cellular and Molecular Life Sciences, vol. 66, no. 6, pp. 1010–1020, 2009. View at Google Scholar
  14. K. Dreij, J. A. Burns et al., “DNA damage and transcription elongation: consequences and RNA Integrity,” in The Chemical Biology of DNA Damage, N. E. Geacintov and S. Broyde, Eds., WILEY-VCH, Weinheim, Germany, 2010. View at Google Scholar
  15. K. Sugasawa, J. M. Y. Ng, C. Masutani et al., “Xeroderma pigmentosum group C protein complex is the initiator of global genome nucleotide excision repair,” Molecular Cell, vol. 2, no. 2, pp. 223–232, 1998. View at Google Scholar · View at Scopus
  16. M. Volker, M. J. Moné, P. Karmakar et al., “Sequential assembly of the nucleotide excision repair factors in vivo,” Molecular Cell, vol. 8, no. 1, pp. 213–224, 2001. View at Publisher · View at Google Scholar · View at Scopus
  17. T. Riedl, F. Hanaoka, and J.-M. Egly, “The comings and goings of nucleotide excision repair factors on damaged DNA,” EMBO Journal, vol. 22, no. 19, pp. 5293–5303, 2003. View at Publisher · View at Google Scholar · View at Scopus
  18. M. E. Fitch, S. Nakajima, A. Yasui, and J. M. Ford, “In vivo recruitment of XPC to UV-induced cyclobutane pyrimidine dimers by the DDB2 gene product,” Journal of Biological Chemistry, vol. 278, no. 47, pp. 46906–46910, 2003. View at Publisher · View at Google Scholar · View at Scopus
  19. J. Moser, M. Volker, H. Kool et al., “The UV-damaged DNA binding protein mediates efficient targeting of the nucleotide excision repair complex to UV-induced photo lesions,” DNA Repair, vol. 4, no. 5, pp. 571–582, 2005. View at Publisher · View at Google Scholar · View at Scopus
  20. K. Sugasawa, Y. Okuda, M. Saijo et al., “UV-induced ubiquitylation of XPC protein mediated by UV-DDB-ubiquitin ligase complex,” Cell, vol. 121, no. 3, pp. 387–400, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. R. Nishi, S. Alekseev, C. Dinant et al., “UV-DDB-dependent regulation of nucleotide excision repair kinetics in living cells,” DNA Repair, vol. 8, no. 6, pp. 767–776, 2009. View at Publisher · View at Google Scholar · View at Scopus
  22. T. Ogi, S. Limsirichaikul, R. M. Overmeer et al., “Three DNA polymerases, recruited by different mechanisms, carry out NER repair synthesis in human cells,” Molecular Cell, vol. 37, no. 5, pp. 714–727, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. C. Guo, T.-S. Tang, and E. C. Friedberg, “SnapShot: nucleotide excision repair,” Cell, vol. 140, no. 5, pp. 754–754.e1, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. D. Gunz, M. T. Hess, and H. Naegeli, “Recognition of DNA adducts by human nucleotide excision repair. Evidence for a thermodynamic probing mechanism,” Journal of Biological Chemistry, vol. 271, no. 41, pp. 25089–25098, 1996. View at Publisher · View at Google Scholar · View at Scopus
  25. E. Evans, J. G. Moggs, J. R. Hwang, J.-M. Egly, and R. D. Wood, “Mechanism of open complex and dual incision formation by human nucleotide excision repair factors,” EMBO Journal, vol. 16, no. 21, pp. 6559–6573, 1997. View at Publisher · View at Google Scholar · View at Scopus
  26. Y. Fujiwara, C. Masutani, T. Mizukoshi, J. Kondo, F. Hanaoka, and S. Iwai, “Characterization of DNA recognition by the human UV-damaged DNA-binding protein,” Journal of Biological Chemistry, vol. 274, no. 28, pp. 20027–20033, 1999. View at Publisher · View at Google Scholar · View at Scopus
  27. R. D. Wood, “DNA damage recognition during nucleotide excision repair in mammalian cells,” Biochimie, vol. 81, no. 1-2, pp. 39–44, 1999. View at Publisher · View at Google Scholar · View at Scopus
  28. K. Sugasawa, T. Okamoto, Y. Shimizu, C. Masutani, S. Iwai, and F. Hanaoka, “A multistep damage recognition mechanism for global genomic nucleotide excision repair,” Genes and Development, vol. 15, no. 5, pp. 507–521, 2001. View at Publisher · View at Google Scholar · View at Scopus
  29. N. E. Geacintov, S. Broyde, T. Buterin et al., “Thermodynamic and structural factors in the removal of bulky DNA adducts by the nucleotide excision repair machinery,” Biopolymers, vol. 65, no. 3, pp. 202–210, 2002. View at Publisher · View at Google Scholar · View at Scopus
  30. K. Sugasawa, Y. Shimizu, S. Iwai, and F. Hanaoka, “A molecular mechanism for DNA damage recognition by the xeroderma pigmentosum group C protein complex,” DNA Repair, vol. 1, no. 1, pp. 95–107, 2002. View at Publisher · View at Google Scholar · View at Scopus
  31. M. T. Hess, D. Gunz, N. Luneva, N. E. Geacintov, and H. Naegeli, “Base pair conformation-dependent excision of benzo[a]pyrene diol epoxide-guanine adducts by human nucleotide excision repair enzymes,” Molecular and Cellular Biology, vol. 17, no. 12, pp. 7069–7076, 1997. View at Google Scholar · View at Scopus
  32. M. Missura, T. Buterin, R. Hindges et al., “Double-check probing of DNA bending and unwinding by XPA-RPA: an architectural function in DNA repair,” EMBO Journal, vol. 20, no. 13, pp. 3554–3564, 2001. View at Publisher · View at Google Scholar · View at Scopus
  33. N. E. Geacintov, H. Naegeli et al., “Structural aspects of polycyclic aromatic carcinogen-damged DNA and its recognition by NER proteins,” in DNA Damage and Recognition, W. Siede, Y. W. Kow, and P. W. Doetsch, Eds., Taylor & Francis, London, UK, 2006. View at Google Scholar
  34. W. Yang, “Poor base stacking at DNA lesions may initiate recognition by many repair proteins,” DNA Repair, vol. 5, no. 6, pp. 654–666, 2006. View at Publisher · View at Google Scholar · View at Scopus
  35. W. Yang, “Structure and mechanism for DNA lesion recognition,” Cell Research, vol. 18, no. 1, pp. 184–197, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. R. J. Isaacs and H. P. Spielmann, “A model for initial DNA lesion recognition by NER and MMR based on local conformational flexibility,” DNA Repair, vol. 3, no. 5, pp. 455–464, 2004. View at Publisher · View at Google Scholar · View at Scopus
  37. T. Buterin, C. Meyer, B. Giese, and H. Naegeli, “DNA quality control by conformational readout on the undamaged strand of the double helix,” Chemistry and Biology, vol. 12, no. 8, pp. 913–922, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. E. Malta, G. F. Moolenaar, and N. Goosen, “Base flipping in nucleotide excision repair,” Journal of Biological Chemistry, vol. 281, no. 4, pp. 2184–2194, 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. J. J. Truglio, E. Karakas, B. Rhau et al., “Structural basis for DNA recognition and processing by UvrB,” Nature Structural and Molecular Biology, vol. 13, no. 4, pp. 360–364, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. F. C. Clement, U. Camenisch, J. Fei, N. Kaczmarek, N. Mathieu, and H. Naegeli, “Dynamic two-stage mechanism of versatile DNA damage recognition by xeroderma pigmentosum group C protein,” Mutation Research, vol. 685, no. 1-2, pp. 21–28, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. J.-H. Min and N. P. Pavletich, “Recognition of DNA damage by the Rad4 nucleotide excision repair protein,” Nature, vol. 449, no. 7162, pp. 570–575, 2007. View at Publisher · View at Google Scholar · View at Scopus
  42. A. Luch, “Nature and nurture—lessons from chemical carcinogenesis,” Nature Reviews Cancer, vol. 5, no. 2, pp. 113–125, 2005. View at Publisher · View at Google Scholar · View at Scopus
  43. M. K. Buening, P. G. Wislocki, and H. Levin, “Tumorigenicity of the optical enantiomers of the diastereomeric benzo[a]pyrene 7,8-diol-9,10-epoxides in newborn mice: exceptional activity of (+)-7β,8α-dihydroxy-9α,10α-epoxy-7,8,9,10-tetrahydrobenzo[a]pyrene,” Proceedings of the National Academy of Sciences of the United States of America, vol. 75, no. 11, pp. 5358–5361, 1978. View at Google Scholar · View at Scopus
  44. I. B. Weinstein, A. M. Jeffrey, and K. W. Jennette, “Benzo[a]pyrene diol epoxides as intermediates in nucleic acid binding in vitro and in vivo,” Science, vol. 193, no. 4253, pp. 592–594, 1976. View at Google Scholar · View at Scopus
  45. M. Koreeda, P. D. Moore, and P. Wislocki, “Binding of benzo[a]pyrene 7,8-diol-9,10-epoxides to DNA,RNA, and protein of mouse skin occurs with high stereoselectivity,” Science, vol. 199, no. 4330, pp. 778–781, 1978. View at Google Scholar · View at Scopus
  46. I. B. Weinstein, A. M. Jeffrey, and K. W. Jennette, “Benzo[a]pyrene diol epoxides as intermediates in nucleic acid binding in vitro and in vivo,” Science, vol. 193, no. 4253, pp. 592–594, 1976. View at Google Scholar · View at Scopus
  47. D. Wei, V. M. Maher, and J. J. Mccormick, “Site-specific rates of excision repair of benzo[a]pyrene diol epoxide adducts in the hypoxanthine phosphoribosyltransferase gene of human fibroblasts: correlation with mutation spectra,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 6, pp. 2204–2208, 1995. View at Publisher · View at Google Scholar · View at Scopus
  48. A. Fernandes, T. Liu, S. Amin, N. E. Geacintov, A. P. Grollman, and M. Moriya, “Mutagenic potential of stereoisomeric bay region (+)- and ()-cis-anti-benzo[a]pyrene diol epoxide-N2-2-deoxyguanosine adducts in Escherichia coli and Simian kidney cells,” Biochemistry, vol. 37, no. 28, pp. 10164–10172, 1998. View at Publisher · View at Google Scholar · View at Scopus
  49. K. Y. Seo, A. Nagalingam, M. Tiffany, and E. L. Loechler, “Mutagenesis studies with four stereoisomeric N2-dG benzo[a]pyrene adducts in the identical 5-CGC sequence used in NMR studies: G→T mutations dominate in each case,” Mutagenesis, vol. 20, no. 6, pp. 441–448, 2005. View at Publisher · View at Google Scholar · View at Scopus
  50. M. Cosman, C. de los Santos, R. Fiala et al., “Solution conformation of the major adduct between the carcinogen (+)-anti-benzo[a]pyrene diol epoxide and DNA,” Proceedings of the National Academy of Sciences of the United States of America, vol. 89, no. 5, pp. 1914–1918, 1992. View at Google Scholar · View at Scopus
  51. F. A. Rodríguez, Y. Cai, C. Lin et al., “Exocyclic amino groups of flanking guanines govern sequence-dependent adduct conformations and local structural distortions for minor groove-aligned benzo[a]pyrenyl-guanine lesions in a GG mutation hotspot context,” Nucleic Acids Research, vol. 35, no. 5, pp. 1555–1568, 2007. View at Publisher · View at Google Scholar · View at Scopus
  52. Y. Cai, D. J. Patel, N. E. Geacintov, and S. Broyde, “Differential nucleotide excision repair susceptibility of bulky DNA adducts in different sequence contexts: hierarchies of recognition signals,” Journal of Molecular Biology, vol. 385, no. 1, pp. 30–44, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. K. Kropachev, M. Kolbanovskii, Y. Cai et al., “The sequence dependence of human nucleotide excision repair efficiencies of benzo[a]pyrene-derived DNA lesions: insights into the structural factors that favor dual incisions,” Journal of Molecular Biology, vol. 386, no. 5, pp. 1193–1203, 2009. View at Publisher · View at Google Scholar · View at Scopus
  54. J. Xu, Sequence dependence of carcinogen-induced DNA bending, Ph.D. thesis, New York University, New York, NY, USA, 1999.
  55. A. A. Gorin, V. B. Zhurkin, and W. K. Olson, “B-DNA twisting correlates with base-pair morphology,” Journal of Molecular Biology, vol. 247, no. 1, pp. 34–48, 1995. View at Publisher · View at Google Scholar · View at Scopus
  56. R. E. Dickerson, “DNA bending: the prevalence of kinkiness and the virtues of normality,” Nucleic Acids Research, vol. 26, no. 8, pp. 1906–1926, 1998. View at Publisher · View at Google Scholar · View at Scopus
  57. W. K. Olson, A. A. Gorin, X.-J. Lu, L. M. Hock, and V. B. Zhurkin, “DNA sequence-dependent deformability deduced from protein-DNA crystal complexes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 19, pp. 11163–11168, 1998. View at Publisher · View at Google Scholar · View at Scopus
  58. N. E. Geacintov, M. Cosman, B. E. Hingerty, S. Amin, S. Broyde, and D. J. Patel, “NMR solution structures of stereoisomeric covalent polycyclic aromatic carcinogen-DNA adducts: Principles, patterns, and diversity,” Chemical Research in Toxicology, vol. 10, no. 2, pp. 111–146, 1997. View at Publisher · View at Google Scholar · View at Scopus
  59. R. Xu, B. Mao, S. Amin, and N. E. Geacintov, “Bending and circularization of site-specific and stereoisomeric carcinogen-DNA adducts,” Biochemistry, vol. 37, no. 2, pp. 769–778, 1998. View at Publisher · View at Google Scholar · View at Scopus
  60. H. Tsao, B. Mao, P. Zhuang, R. Xu, S. Amin, and N. E. Geacintov, “Sequence dependence and characteristics of bends induced by site-specific polynuclear aromatic carcinogen-deoxyguanosine lesions in oligonucleotides,” Biochemistry, vol. 37, no. 14, pp. 4993–5000, 1998. View at Publisher · View at Google Scholar · View at Scopus
  61. Q. Ruan, T. Liu, A. Kolbanovskiy et al., “Sequence context- and temperature-dependent nucleotide excision repair of a benzo[a]pyrene diol epoxide-guanine DNA adduct catalyzed by thermophilic UvrABC proteins,” Biochemistry, vol. 46, no. 23, pp. 7006–7015, 2007. View at Publisher · View at Google Scholar · View at Scopus
  62. K. J. Breslauer, R. Frank, H. Blocker, and L. A. Marky, “Predicting DNA duplex stability from the base sequence,” Proceedings of the National Academy of Sciences of the United States of America, vol. 83, no. 11, pp. 3746–3750, 1986. View at Google Scholar · View at Scopus
  63. J. SantaLucia Jr., H. T. Allawi, and P. A. Seneviratne, “Improved nearest-neighbor parameters for predicting DNA duplex stability,” Biochemistry, vol. 35, no. 11, pp. 3555–3562, 1996. View at Publisher · View at Google Scholar · View at Scopus
  64. Y. Cai, D. J. Patel, N. E. Geacintov, and S. Broyde, “Dynamics of a benzo[a]pyrene-derived guanine DNA lesion in TGT and CGC sequence contexts: enhanced mobility in TGT explains conformational heterogeneity, flexible bending, and greater susceptibility to nucleotide excision repair,” Journal of Molecular Biology, vol. 374, no. 2, pp. 292–305, 2007. View at Publisher · View at Google Scholar · View at Scopus
  65. E. J. Gardiner, C. A. Hunter, M. J. Packer, D. S. Palmer, and P. Willett, “Sequence-dependent DNA Structure: a database of octamer structural parameters,” Journal of Molecular Biology, vol. 332, no. 5, pp. 1025–1035, 2003. View at Publisher · View at Google Scholar · View at Scopus
  66. Y. Cai, K. Kropachev, R. Xu et al., “Distant neighbor base sequence context effects in human nucleotide excision repair of a benzo[a]pyrene-derived DNA lesion,” Journal of Molecular Biology, vol. 399, no. 3, pp. 397–409, 2010. View at Publisher · View at Google Scholar · View at Scopus
  67. R. C. Johnson, S. Stella et al., “Bending and compaction of DNA by proteins,” in Protein-Nucleic Acid Interactions, P. A. Rice and C. C. Correll, Eds., The Royal Society of Chemistry, Cambridge, UK, 2008. View at Google Scholar
  68. C. R. Calladine, “Mechanics of sequence-dependent stacking of bases in B-DNA,” Journal of Molecular Biology, vol. 161, no. 2, pp. 343–352, 1982. View at Google Scholar · View at Scopus
  69. M. A. el Hassan and C. R. Calladine, “Conformational characteristics of DNA: empirical classifications and a hypothesis for the conformational behaviour of dinucleotide steps,” Philosophical Transactions of the Royal Society A, vol. 355, no. 1722, pp. 43–100, 1997. View at Google Scholar · View at Scopus
  70. M. A. el Hassan and C. R. Calladine, “Two distinct modes of protein-induced bending in DNA,” Journal of Molecular Biology, vol. 282, no. 2, pp. 331–343, 1998. View at Publisher · View at Google Scholar · View at Scopus
  71. M. J. Packer, M. P. Dauncey, and C. A. Hunter, “Sequence-dependent DNA structure: dinucleotide conformational maps,” Journal of Molecular Biology, vol. 295, no. 1, pp. 71–83, 2000. View at Publisher · View at Google Scholar · View at Scopus
  72. T. M. Okonogi, S. C. Alley, A. W. Reese, P. B. Hopkins, and B. H. Robinson, “Sequence-dependent dynamics of duplex DNA: the applicability of a dinucleotide model,” Biophysical Journal, vol. 83, no. 6, pp. 3446–3459, 2002. View at Google Scholar · View at Scopus
  73. O. D. Schärer, “A molecular basis for damage recognition in eukaryotic nucleotide excision repair,” ChemBioChem, vol. 9, no. 1, pp. 21–23, 2008. View at Publisher · View at Google Scholar · View at Scopus
  74. T. Buterin, M. T. Hess, N. Luneva et al., “Unrepaired fjord region polycyclic aromatic hydrocarbon-DNA adducts in ras codon 61 mutational hot spots,” Cancer Research, vol. 60, no. 7, pp. 1849–1856, 2000. View at Google Scholar · View at Scopus