An iron-sulfur cluster loop motif in the archaeoglobus fulgidus uracil-DNA glycosylase mediates efficient uracil recognition and removal

Biochemistry

Volumn 51, Issue 25, 2012, Pages 5187-5197

  Engstrom, Lisa M ^a   Partington, Olga A ^b   David, Sheila S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF UTAH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARCHAEOGLOBUS FULGIDUS; BASE EXCISION REPAIRS; CYS RESIDUES; DAMAGED SITES; DNA BINDING; DNA DAMAGES; DOUBLE STRANDED DNA; DUPLEX DNA; ENDONUCLEASES; HYPERTHERMOPHILIC ORGANISMS; IRON-SULFUR CLUSTERS; LOOP CONFORMATION; LOOP MOTIFS; POSITIVELY CHARGED; THIOLATES; URACIL-DNA GLYCOSYLASE;

AMINO ACIDS; DNA; SULFUR;

AROMATIC COMPOUNDS;

ALANINE; ARGININE; CYSTEINE; DNA GLYCOSYLASE MUTY; DOUBLE STRANDED DNA; ENDONUCLEASE; IRON SULFUR PROTEIN; LYSINE; SINGLE STRANDED DNA; THIOL; URACIL; URACIL DNA GLYCOSIDASE;

ALPHA HELIX; ARCHAEOGLOBUS FULGIDUS; ARTICLE; CATALYSIS; DNA BINDING; DNA DAMAGE; ENZYME STABILITY; EXCISION REPAIR; HYPERTHERMOPHILIC ARCHAEON; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN MOTIF;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ARCHAEAL PROTEINS; ARCHAEOGLOBUS FULGIDUS; CATALYSIS; DNA REPAIR; IRON-SULFUR PROTEINS; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; NUCLEIC ACID HETERODUPLEXES; PROTEIN BINDING; URACIL; URACIL-DNA GLYCOSIDASE;

ARCHAEOGLOBUS FULGIDUS;

EID: 84862881944     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi3000462     Document Type: Article

References (43)

1. David, S. S. and Williams, S. D. (1998) Chemistry of Glycosylases and Endonucleases Involved in Base-Excision Repair Chem. Rev. 98, 1221-1262
2. Lindahl, T. (1993) Instability and decay of the primary structure of DNA Nature 362, 709-715 (Pubitemid 23125973)
3. Tye, B. K., Nyman, P. O., Lehman, I. R., Hochhauser, S., and Weiss, B. (1977) Transient accumulation of Okazaki fragments as a result of uracil incorporation into nascent DNA Proc. Natl. Acad. Sci. U. S. A. 74, 154-157 (Pubitemid 8025890)
4. Pearl, L. H. (2000) Structure and function in the uracil-DNA glycosylase superfamily Mutat. Res. 460, 165-181 (Pubitemid 30628589)
5. Lee, H. W., Dominy, B. N., and Cao, W. A new family of deamination repair enzymes in the uracil DNA glycosylase superfamily. J. Biol. Chem. 2012, in press.
6. Savva, R., McAuley-Hecht, K., Brown, T., and Pearl, L. (1995) The structural basis of specific base-excision repair by uracil-DNA glycosylase Nature 373, 487-493
7. Mol, C. D., Arvai, A. S., Slupphaug, G., Kavli, B., Alseth, I., Krokan, H. E., and Tainer, J. A. (1995) Crystal structure and mutational analysis of human uracil-DNA glycosylase: structural basis for specificity and catalysis Cell 80, 869-878
8. Slupphaug, G., Mol, C. D., Kavli, B., Arvai, A. S., Krokan, H. E., and Tainer, J. A. (1996) A nucleotide-flipping mechanism from the structure of human uracil-DNA glycosylase bound to DNA Nature 384, 87-92 (Pubitemid 26374594)
9. Werner, R. M. and Stivers, J. T. (2000) Kinetic isotope effect studies of the reaction catalyzed by uracil DNA glycosylase: evidence for an oxocarbenium ion-uracil anion intermediate Biochemistry 39, 14054-14064
10. Stivers, J. T., Pankiewicz, K. W., and Watanabe, K. A. (1999) Kinetic mechanism of damage site recognition and uracil flipping by Escherichia coli uracil DNA glycosylase Biochemistry 38, 952-963
11. Lindahl, T. and Nyberg, B. (1974) Heat-induced deamination of cytosine residues in deoxyribonucleic acid Biochemistry 13, 3405-3410
12. Sandigursky, M. and Franklin, W. A. (1999) Thermostable uracil-DNA glycosylase from Thermotoga maritima a member of a novel class of DNA repair enzymes Curr. Biol. 9, 531-534 (Pubitemid 29257108)
13. Starkuviene, V. and Fritz, H. J. (2002) A novel type of uracil-DNA glycosylase mediating repair of hydrolytic DNA damage in the extremely thermophilic eubacterium Thermus thermophilus Nucleic Acids Res. 30, 2097-2102 (Pubitemid 34567930)
14. Sandigursky, M. and Franklin, W. A. (2000) Uracil-DNA glycosylase in the extreme thermophile Archaeoglobus fulgidus J. Biol. Chem. 275, 19146-19149 (Pubitemid 30422884)
15. Boal, A. K., Yavin, E., Lukianova, O. A., O′Shea, V. L., David, S. S., and Barton, J. K. (2005) DNA-bound redox activity of DNA repair glycosylases containing [4Fe-4S] clusters Biochemistry 44, 8397-8407 (Pubitemid 40799920)
16. Hinks, J. A., Evans, M. C., De Miguel, Y., Sartori, A. A., Jiricny, J., and Pearl, L. H. (2002) An iron-sulfur cluster in the family 4 uracil-DNA glycosylases J. Biol. Chem. 277, 16936-16940 (Pubitemid 34967721)
17. Kosaka, H., Hoseki, J., Nakagawa, N., Kuramitsu, S., and Masui, R. (2007) Crystal structure of family 5 uracil-DNA glycosylase bound to DNA J. Mol. Biol. 373, 839-850 (Pubitemid 47498437)
18. Hoseki, J., Okamoto, A., Masui, R., Shibata, T., Inoue, Y., Yokoyama, S., and Kuramitsu, S. (2003) Crystal structure of a family 4 uracil-DNA glycosylase from Thermus thermophilus HB8 J. Mol. Biol. 333, 515-526 (Pubitemid 37229078)
19. Porello, S. L., Cannon, M. J., and David, S. S. (1998) A substrate recognition role for the [4Fe-4S]2+ cluster of the DNA repair glycosylase MutY Biochemistry 37, 6465-6475 (Pubitemid 28213667)
20. Cunningham, R. P., Asahara, H., Bank, J. F., Scholes, C. P., Salerno, J. C., Surerus, K., Munck, E., McCracken, J., Peisach, J., and Emptage, M. H. (1989) Endonuclease III is an iron-sulfur protein Biochemistry 28, 4450-4455 (Pubitemid 19141656)
21. Chepanoske, C. L., Golinelli, M. P., Williams, S. D., and David, S. S. (2000) Positively charged residues within the iron-sulfur cluster loop of E. coli MutY participate in damage recognition and removal Arch. Biochem. Biophys. 380, 11-19 (Pubitemid 30616765)
22. Thayer, M. M., Ahern, H., Xing, D., Cunningham, R. P., and Tainer, J. A. (1995) Novel DNA binding motifs in the DNA repair enzyme endonuclease III crystal structure EMBO J. 14, 4108-4120
23. Lukianova, O. A. and David, S. S. (2005) A role for iron-sulfur clusters in DNA repair Curr. Opin. Chem. Biol. 9, 145-151 (Pubitemid 40467576)
24. Sambrook, J. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2 nd ed., Cold Spring Harbor Press, Cold Spring Harbor, NY.
25. Shaw, R. W., Feller, J. A., and Bloom, L. B. (2004) Contribution of a conserved phenylalanine residue to the activity of Escherichia coli uracil DNA glycosylase DNA Repair 3, 1273-1283 (Pubitemid 39164591)
26. Maher, R. L. and Bloom, L. B. (2007) Pre-steady-state kinetic characterization of the AP endonuclease activity of human AP endonuclease 1 J. Biol. Chem. 282, 30577-30585 (Pubitemid 350035165)
27. Fersht, A. (1985) Enzyme Structure and Mechanism, W.H. Freeman and Co., New York.
28. Porello, S. L., Leyes, A. E., and David, S. S. (1998) Single-turnover and pre-steady-state kinetics of the reaction of the adenine glycosylase MutY with mismatch-containing DNA substrates Biochemistry 37, 14756-14764 (Pubitemid 28487583)
29. Fersht, A. (1999) Structure and Mechanism in Protein Science: A Guide to Enzyme Catalysis and Protein Folding, W.H. Freeman and Co., New York.
30. Golinelli, M. P., Chmiel, N. H., and David, S. S. (1999) Site-directed mutagenesis of the cysteine ligands to the [4Fe-4S] cluster of Escherichia coli MutY Biochemistry 38, 6997-7007
31. Lindahl, T. (1974) An N-glycosidase from Escherichia coli that releases free uracil from DNA containing deaminated cytosine residues Proc. Natl. Acad. Sci. U. S. A. 71, 3649-3653
32. Parikh, S. S., Putnam, C. D., and Tainer, J. A. (2000) Lessons learned from structural results on uracil-DNA glycosylase Mutat. Res. 460, 183-199 (Pubitemid 30628590)
33. Zharkov, D. O., Mechetin, G. V., and Nevinsky, G. A. (2010) Uracil-DNA glycosylase: Structural, thermodynamic and kinetic aspects of lesion search and recognition Mutat. Res. 685, 11-20
34. Slupphaug, G., Olsen, L. C., Helland, D., Aasland, R., and Krokan, H. E. (1991) Cell cycle regulation and in vitro hybrid arrest analysis of the major human uracil-DNA glycosylase Nucleic Acids Res. 19, 5131-5137 (Pubitemid 21912901)
35. Krokan, H. E., Drablos, F., and Slupphaug, G. (2002) Uracil in DNA - occurrence, consequences and repair Oncogene 21, 8935-8948 (Pubitemid 36110823)
36. Knaevelsrud, I., Ruoff, P., Anensen, H., Klungland, A., Bjelland, S., and Birkeland, N. K. (2001) Excision of uracil from DNA by the hyperthermophilic Afung protein is dependent on the opposite base and stimulated by heat-induced transition to a more open structure Mutat. Res. 487, 173-190 (Pubitemid 34002970)
37. Rothschild, L. J. and Mancinelli, R. L. (2001) Life in extreme environments Nature 409, 1092-1102
38. Parikh, S. S., Mol, C. D., Slupphaug, G., Bharati, S., Krokan, H. E., and Tainer, J. A. (1998) Base excision repair initiation revealed by crystal structures and binding kinetics of human uracil-DNA glycosylase with DNA EMBO J. 17, 5214-5226 (Pubitemid 28408487)
39. Chen, C.-Y., Mosbaugh, D. W., and Bennet, S. E. (2004) Mutational Analysis of Arginine 276 in the Leucine-loop of Human Uracil-DNA Glycosylase J. Biol. Chem. 279, 48177-48188 (Pubitemid 39540973)
40. Chen, C.-Y., Mosbaugh, D. W., and Bennet, S. E. (2005) Mutations at Arginine 276 transform human uracil-DNA glycosylase into a single-stranded DNA-specific uracil-DNA glycosylase DNA Repair 4, 793-805 (Pubitemid 40835851)
41. Hof, F., Craig, S. L., Nuckolls, C., and Rebek, J. (2002) Molecular Encapsulation Angew. Chem., Int. Ed. 41, 1488-1508 (Pubitemid 34534385)
42. White, M. F. and Dillingham, M. S. (2011) Iron-sulphur clusters in nucleic acid processing enzymes Curr. Opin. Struct. Biol 22, 1-7
43. Netz, D. J. A., Stith, C. M., Stumpfig, M., Kopf, G., Vogel, D., Genau, H. M., Stodola, J. L., Lill, R., Burgers, P. M. J., and Pierik, A. J. (2011) Eukaryotic DNA polymerases require an iron-sulfur cluster for the formation of active complexes Nat. Chem. Biol. 8, 125-132