5-Hydroxy-5-methylhydantoin DNA lesion, a molecular trap for DNA glycosylases

Nucleic Acids Research

Volumn 39, Issue 14, 2011, Pages 6277-6290

  Le Bihan, Yann Vaï ^a   Izquierdo, Maria Angeles ^b,d,e   Coste, Franck ^a   Aller, Pierre ^c   Culard, Franoise ^a   Gehrke, Tim H ^b   Essalhi, Kadija ^a   Carell, Thomas ^b   Castaing, Bertrand ^a  

^a CENTRE DE BIOPHYSIQUE MOLÉCULAIRE   (France)

^b UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

^d UNIVERSITAT JAUME I   (Spain)

^e NONE   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

5 HYDROXY 5 METHYLHYDANTOIN; DNA; DNA FORMAMIDOPYRIMIDINE GLYCOSYLASE; DNA GLYCOSYLTRANSFERASE; DNA HYDANTOIN CARBANUCLEOSIDE; PROLINE; THYMINE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BIOCHEMISTRY; CATALYSIS; CRYSTAL STRUCTURE; DNA DAMAGE; ENZYME STRUCTURE; LACTOCOCCUS LACTIS; NONHUMAN; NUCLEOPHILICITY; PRIORITY JOURNAL; PROTEIN DNA BINDING; SITE DIRECTED MUTAGENESIS;

LACTOCOCCUS LACTIS;

EID: 79960738714     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr215     Document Type: Article

References (64)

1. Lindahl, T. (1993) Instability and decay of the primary structure of DNA. Nature, 362, 709-715. (Pubitemid 23125973)
2. Cadet, J., Douki, T., Gasparutto, D. and Ravanat, J.L. (2003) Oxidative damage to DNA: formation, measurement and biochemical features. Mutat. Res., 531, 5-23. (Pubitemid 37456721)
3. Cadet, J., Berger, M., Douki, T. and Ravanat, J.L. (1997) Oxidative damage to DNA: formation, measurement, and biological significance. Rev. Physiol. Biochem. Pharmacol., 131, 1-87.
4. Maynard, S., Schurman, S.H., Harboe, C., de Souza-Pinto, N.C. and Bohr, V.A. (2009) Base excision repair of oxidative DNA damage and association with cancer and aging. Carcinogenesis, 30, 2-10.
5. Dizdaroglu, M. (2005) Base-excision repair of oxidative DNA damage by DNA glycosylases. Mutat. Res., 591, 45-59. (Pubitemid 41654839)
6. Xu, G., Herzig, M., Rotrekl, V. and Walter, C.A. (2008) Base excision repair, aging and health span. Mech. Ageing Dev., 129, 366-382.
7. Hazra, T.K., Das, A., Das, S., Choudhury, S., Kow, Y.W. and Roy, R. (2007) Oxidative DNA damage repair in mammalian cells: a new perspective. DNA Repair, 6, 470-480. (Pubitemid 46357682)
8. Dalhus, B., Laerdahl, J.K., Backe, P.H. and Bjoras, M. (2009) DNA base repair-recognition and initiation of catalysis. FEMS Microbiol. Rev., 33, 1044-1078.
9. van der Kemp, P.A., Thomas, D., Barbey, R., de Oliveira, R. and Boiteux, S. (1996) Cloning and expression in Escherichia coli of the OGG1 gene of Saccharomyces cerevisiae, which codes for a DNA glycosylase that excises 7, 8-dihydro-8-oxoguanine and 2, 6-diamino-4-hydroxy-5-N-methylformamidopyrimidine. Proc. Natl Acad. Sci. USA, 93, 5197-5202.
10. Scharer, O.D. (2003) Chemistry and biology of DNA repair. Angew. Chem. Int. Ed. Engl., 42, 2946-2974. (Pubitemid 36903177)
11. Coste, F., Ober, M., Carell, T., Boiteux, S., Zelwer, C. and Castaing, B. (2004) Structural basis for the recognition of the FapydG lesion (2, 6-diamino-4-hydroxy-5-formamidopyrimidine) by formamidopyrimidine-DNA glycosylase. J. Biol. Chem., 279, 44074-44083. (Pubitemid 39390717)
12. Coste, F., Ober, M., Le Bihan, Y.V., Izquierdo, M.A., Hervouet, N., Mueller, H., Carell, T. and Castaing, B. (2008) Bacterial base excision repair enzyme Fpg recognizes bulky N7-substituted-FapydG lesion via unproductive binding mode. Chem. Biol., 15, 706-717. (Pubitemid 351965501)
13. Fromme, J.C. and Verdine, G.L. (2003) DNA lesion recognition by the bacterial repair enzyme MutM. J. Biol. Chem., 278, 51543-51548. (Pubitemid 38020397)
14. Pereira de Jesus, K., Serre, L., Zelwer, C. and Castaing, B. (2005) Structural insights into abasic site for Fpg specific binding and catalysis: comparative high-resolution crystallographic studies of Fpg bound to various models of abasic site analogues-containing DNA. Nucleic Acids Res., 33, 5936-5944. (Pubitemid 41742613)
15. Serre, L., Pereira de Jesus, K., Boiteux, S., Zelwer, C. and Castaing, B. (2002) Crystal structure of the Lactococcus lactis formamidopyrimidine-DNA glycosylase bound to an abasic site analogue-containing DNA. EMBO J., 21, 2854-2865. (Pubitemid 34670370)
16. Gilboa, R., Zharkov, D.O., Golan, G., Fernandes, A.S., Gerchman, S.E., Matz, E., Kycia, J.H., Grollman, A.P. and Shoham, G. (2002) Structure of formamidopyrimidine-DNA glycosylase covalently complexed to DNA. J. Biol. Chem., 277, 19811-19816. (Pubitemid 34967498)
17. Castaing, B., Geiger, A., Seliger, H., Nehls, P., Laval, J., Zelwer, C. and Boiteux, S. (1993) Cleavage and binding of a DNA fragment containing a single 8-oxoguanine by wild type and mutant FPG proteins. Nucleic Acids Res., 21, 2899-2905. (Pubitemid 23220442)
18. Tchou, J., Bodepudi, V., Shibutani, S., Antoshechkin, I., Miller, J., Grollman, A.P. and Johnson, F. (1994) Substrate specificity of Fpg protein. Recognition and cleavage of oxidatively damaged DNA. J. Biol. Chem., 269, 15318-15324.
19. Chetsanga, C.J. and Lindahl, T. (1979) Release of 7-methylguanine residues whose imidazole rings have been opened from damaged DNA by a DNA glycosylase from Escherichia coli. Nucleic Acids Res., 6, 3673-3684. (Pubitemid 9237430)
20. Dizdaroglu, M., Kirkali, G. and Jaruga, P. (2008) Formamidopyrimidines in DNA: mechanisms of formation, repair, and biological effects. Free Radic. Biol. Med., 45, 1610-1621.
21. Gasparutto, D., Ait-Abbas, M., Jaquinod, M., Boiteux, S. and Cadet, J. (2000) Repair and coding properties of 5-hydroxy-5-methylhydantoin nucleosides inserted into DNA oligomers. Chem. Res. Toxicol., 13, 575-584. (Pubitemid 30491118)
22. Gasparutto, D., Muller, E., Boiteux, S. and Cadet, J. (2009) Excision of the oxidatively formed 5-hydroxyhydantoin and 5-hydroxy-5-methylhydantoin pyrimidine lesions by Escherichia coli and Saccharomyces cerevisiae DNA N-glycosylases. Biochim. Biophys. Acta, 1790, 16-24.
23. Zharkov, D.O., Shoham, G. and Grollman, A.P. (2003) Structural characterization of the Fpg family of DNA glycosylases. DNA Repair, 2, 839-862. (Pubitemid 37303943)
24. Bandaru, V., Sunkara, S., Wallace, S.S. and Bond, J.P. (2002) A novel human DNA glycosylase that removes oxidative DNA damage and is homologous to Escherichia coli endonuclease VIII. DNA Repair, 1, 517-529. (Pubitemid 34655710)
25. Jiang, D., Hatahet, Z., Blaisdell, J.O., Melamede, R.J. and Wallace, S.S. (1997) Escherichia coli endonuclease VIII: cloning, sequencing, and overexpression of the nei structural gene and characterization of nei and nei nth mutants. J. Bacteriol., 179, 3773-3782. (Pubitemid 27233022)
26. Girard, P.M. and Boiteux, S. (1997) Repair of oxidized DNA bases in the yeast Saccharomyces cerevisiae. Biochimie, 79, 559-566. (Pubitemid 28021563)
27. Kabsch, W. (1993) Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallogr., 26, 795-800.
28. Evans, P.R. (1997) Jnt CCP4/ESFEACBM Newsl. Protein Crystallogr, 33, 22-24.
29. McCoy, A.J. (2007) Solving structures of protein complexes by molecular replacement with Phaser. Acta Crystallogr. D Biol. Crystallogr., 63, 32-41.
30. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr., 60, 2126-2132. (Pubitemid 41742764)
31. Adams, P.D., Grosse-Kunstleve, R.W., Hung, L.W., Ioerger, T.R., McCoy, A.J., Moriarty, N.W., Read, R.J., Sacchettini, J.C., Sauter, N.K. and Terwilliger, T.C. (2002) PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D Biol. Crystallogr., 58, 1948-1954. (Pubitemid 35337293)
32. Davis, I.W., Murray, L.W., Richardson, J.S. and Richardson, D.C. (2004) MOLPROBITY: structure validation and all-atom contact analysis for nucleic acids and their complexes. Nucleic Acids Res., 32, W615-619. (Pubitemid 38997409)
33. Teule, R. and Cadet, J. (1978) Radiation-induced degradation of the base component in DNA and related substances. In Hüttermann, J., Kohnlein, W., Teule, R. and Bertinchamps, A.J. (eds), Effects of ionizing radiation on DNA. Spring, Berlin, pp. 171-203.
34. von Sonntag, C. and Schuchmann, H.P. (1986) The radiolysis of pyrimidines in aqueous solutions: an updating review. Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med., 49, 1-34. (Pubitemid 16174925)
35. Girault, I., Molko, D. and Cadet, J. (1994) Ozonolysis of thymidine: isolation and identification of the main oxidation products. Free Radic Res., 20, 315-325. (Pubitemid 2094938)
36. Kasprzak, K.S., Jaruga, P., Zastawny, T.H., North, S.L., Riggs, C.W., Olinski, R. and Dizdaroglu, M. (1997) Oxidative DNA base damage and its repair in kidneys and livers of nickel(II)-treated male F344 rats. Carcinogenesis, 18, 271-277. (Pubitemid 28132418)
37. Senturker, S., Karahalil, B., Inal, M., Yilmaz, H., Muslumanoglu, H., Gedikoglu, G. and Dizdaroglu, M. (1997) Oxidative DNA base damage and antioxidant enzyme levels in childhood acute lymphoblastic leukemia. FEBS Lett., 416, 286-290. (Pubitemid 27475383)
38. d'Abbadie, M., Hofreiter, M., Vaisman, A., Loakes, D., Gasparutto, D., Cadet, J., Woodgate, R., Paabo, S. and Holliger, P. (2007) Molecular breeding of polymerases for amplification of ancient DNA. Nat. Biotechnol., 25, 939-943. (Pubitemid 47236914)
39. Jaruga, P., Birincioglu, M., Rosenquist, T.A. and Dizdaroglu, M. (2004) Mouse NEIL1 protein is specific for excision of 2, 6-diamino-4-hydroxy-5- formamidopyrimidine and 4, 6-diamino-5-formamidopyrimidine from oxidatively damaged DNA. Biochemistry, 43, 15909-15914. (Pubitemid 39665090)
40. Senturker, S., Auffret van der Kemp, P., You, H.J., Doetsch, P.W., Dizdaroglu, M. and Boiteux, S. (1998) Substrate specificities of the ntg1 and ntg2 proteins of Saccharomyces cerevisiae for oxidized DNA bases are not identical. Nucleic Acids Res., 26, 5270-5276. (Pubitemid 28542724)
41. Boiteux, S., O'Connor, T.R., Lederer, F., Gouyette, A. and Laval, J. (1990) Homogeneous Escherichia coli FPG protein. A DNA glycosylase which excises imidazole ring-opened purines and nicks DNA at apurinic/apyrimidinic sites. J. Biol. Chem., 265, 3916-3922.
42. Guo, Y., Bandaru, V., Jaruga, P., Zhao, X., Burrows, C.J., Iwai, S., Dizdaroglu, M., Bond, J.P. and Wallace, S.S. The oxidative DNA glycosylases of Mycobacterium tuberculosis exhibit different substrate preferences from their Escherichia coli counterparts. DNA Repair, 9, 177-190.
43. Hazra, T.K., Muller, J.G., Manuel, R.C., Burrows, C.J., Lloyd, R.S. and Mitra, S. (2001) Repair of hydantoins, one electron oxidation product of 8-oxoguanine, by DNA glycosylases of Escherichia coli. Nucleic Acids Res., 29, 1967-1974. (Pubitemid 32433282)
44. Zharkov, D.O., Rieger, R.A., Iden, C.R. and Grollman, A.P. (1997) NH2-terminal proline acts as a nucleophile in the glycosylase/AP-lyase reaction catalyzed by Escherichia coli formamidopyrimidine-DNA glycosylase (Fpg) protein. J. Biol. Chem., 272, 5335-5341. (Pubitemid 27090098)
45. Ober, M., Linne, U., Gierlich, J. and Carell, T. (2003) The two main DNA lesions 8-Oxo-7, 8-dihydroguanine and 2, 6-diamino-5-formamido-4- hydroxypyrimidine exhibit strongly different pairing properties. Angew. Chem. Int. Ed. Engl., 42, 4947-4951. (Pubitemid 37345399)
46. Ober, M., Muller, H., Pieck, C., Gierlich, J. and Carell, T. (2005) Base pairing and replicative processing of the formamidopyrimidine-dG DNA lesion. J. Am. Chem. Soc., 127, 18143-18149. (Pubitemid 43038477)
47. Song, K., Kelso, C., de los Santos, C., Grollman, A.P. and Simmerling, C. (2007) Molecular simulations reveal a common binding mode for glycosylase binding of oxidatively damaged DNA lesions. J. Am. Chem. Soc., 129, 14536-14537. (Pubitemid 350207849)
48. Fromme, J.C. and Verdine, G.L. (2002) Structural insights into lesion recognition and repair by the bacterial 8-oxoguanine DNA glycosylase MutM. Nat. Struct. Biol., 9, 544-552. (Pubitemid 34693811)
49. Juaristi, E. and Cuevas, G. (1992) Recent studies of the Anomeric effect. Tetrahedron, 48, 5019-5087.
50. Qi, Y., Spong, M.C., Nam, K., Karplus, M. and Verdine, G.L. (2009) Entrapment and structure of an extrahelical guanine attempting to enter the active site of a bacterial DNA glycosylase, MutM. J. Biol. Chem., 285, 1468-1478.
51. Lavrukhin, O.V. and Lloyd, R.S. (2000) Involvement of phylogenetically conserved acidic amino acid residues in catalysis by an oxidative DNA damage enzyme formamidopyrimidine glycosylase. Biochemistry, 39, 15266-15271.
52. Sung, J.S. and Demple, B. (2006) Analysis of base excision DNA repair of the oxidative lesion 2-deoxyribonolactone and the formation of DNA-protein cross-links. Methods Enzymol., 408, 48-64.
53. Nakano, T., Terato, H., Asagoshi, K., Masaoka, A., Mukuta, M., Ohyama, Y., Suzuki, T., Makino, K. and Ide, H. (2003) DNA-protein cross-link formation mediated by oxanine. A novel genotoxic mechanism of nitric oxide-induced DNA damage. J. Biol. Chem., 278, 25264-25272. (Pubitemid 37548691)
54. Kroeger, K.M., Hashimoto, M., Kow, Y.W. and Greenberg, M.M. (2003) Cross-linking of 2-deoxyribonolactone and its beta-elimination product by base excision repair enzymes. Biochemistry, 42, 2449-2455. (Pubitemid 36258381)
55. Lebedeva, N., Auffret van der Kemp, P., Bjornsti, M.A., Lavrik, O. and Boiteux, S. (2006) Trapping of DNA topoisomerase I on nick-containing DNA in cell free extracts of Saccharomyces cerevisiae. DNA Repair, 5, 799-809. (Pubitemid 43928883)
56. Barker, S., Weinfeld, M. and Murray, D. (2005) DNA-protein crosslinks: their induction, repair, and biological consequences. Mutat. Res., 589, 111-135. (Pubitemid 40431691)
57. Sung, J.S., DeMott, M.S. and Demple, B. (2005) Long-patch base excision DNA repair of 2-deoxyribonolactone prevents the formation of DNA-protein cross-links with DNA polymerase beta. J. Biol. Chem., 280, 39095-39103. (Pubitemid 41713860)
58. Nakano, T., Katafuchi, A., Matsubara, M., Terato, H., Tsuboi, T., Masuda, T., Tatsumoto, T., Pack, S.P., Makino, K., Croteau, D.L. et al. (2009) Homologous recombination but not nucleotide excision repair plays a pivotal role in tolerance of DNA-protein cross-links in mammalian cells. J. Biol. Chem., 284, 27065-27076.
59. Muller, E., Gasparutto, D., Castaing, B., Favier, A. and Cadet, J. (2003) Recognition of cyclonucleoside lesions by the Lactococcus lactis FPG protein. Nucleos. Nucleot. Nucleic Acids, 22, 1563-1565. (Pubitemid 37139445)
60. Jaruga, P., Xiao, Y., Vartanian, V., Lloyd, R.S. and Dizdaroglu, M. (2010) Evidence for the involvement of DNA repair enzyme NEIL1 in nucleotide excision repair of (50R)-and (50S)-8, 50-cyclo-20-deoxyadenosines. Biochemistry, 49, 1053-1055.
61. Pallis, A.G. and Karamouzis, M.V. (2010) DNA repair pathways and their implication in cancer treatment. Cancer Metastasis Rev., 29, 677-685.
62. Drew, Y. and Plummer, R. (2009) PARP inhibitors in cancer therapy: two modes of attack on the cancer cell widening the clinical applications. Drug. Resist. Updat., 12, 153-156.
63. Quanz, M., Berthault, N., Roulin, C., Roy, M., Herbette, A., Agrario, C., Alberti, C., Josserand, V., Coll, J.L., Sastre-Garau, X. et al. (2009) Small-molecule drugs mimicking DNA damage: a new strategy for sensitizing tumors to radiotherapy. Clin. Cancer Res., 15, 1308-1316.
64. Quanz, M., Chassoux, D., Berthault, N., Agrario, C., Sun, J.S. and Dutreix, M. (2009) Hyperactivation of DNA-PK by double-strand break mimicking molecules disorganizes DNA damage response. PLoS ONE, 4, e6298.