A role for iron-sulfur clusters in DNA repair

Current Opinion in Chemical Biology

Volumn 9, Issue 2, 2005, Pages 145-151

  Lukianova, Olga A ^a   David, Sheila S ^a  

^a UNIVERSITY OF UTAH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; DNA GLYCOSYLTRANSFERASE; IRON COMPLEX; SULFUR DERIVATIVE;

COMPLEX FORMATION; DNA BINDING; DNA DAMAGE; DNA REPAIR; DNA SEQUENCE; DNA STRUCTURE; EXCISION REPAIR; MOLECULAR CLONING; OXIDATION; OXIDATION REDUCTION REACTION; PROTEIN DNA INTERACTION; REVIEW;

EID: 16344377473     PISSN: 13675931     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbpa.2005.02.006     Document Type: Review

References (34)

1. S. Bian, and J.A. Cowan Protein-bound iron-sulfur centers. Form, function, and assembly Coord Chem Rev 190-192 1999 1049 1066
2. R.H. Holm, P. Kennepohl, and E.I. Solomon Structural and functional aspects of metal sites in biology Chem Rev 96 1996 2239 2314
3. J.A. Cowan, and S.M. Lui Structure-function correlations in high-potential iron proteins Adv Inorg Chem 45 1998 313 351
4. C.W. Carter X-ray analysis of high-potential iron-sulfur proteins and ferredoxins W. Lovenberg Iron-Sulfur Proteins vol. 3 1977 Academic Press 157 204
5. D.H. Flint, and R.M. Allen Iron-sulfur proteins with nonredox functions Chem Rev 96 1996 2315 2334
6. P.J. Kiley, and H. Beinert The role of Fe-S cluster proteins in sensing and regulation in bacteria Curr Opin Microbiol 6 2003 181 186
7. P.J. Kiley, and H. Beinert Oxygen Sensing by the global regulator, FNR: the role of the iron-sulfur cluster FEMS Microbiol Rev 22 1998 341 352
8. R.P. Cunningham, H. Asahara, J.F. Bank, C.P. Scholes, J.C. Salerno, K. Surerus, E. Münck, J. McCracken, J. Peisach, and M.H. Emptage Endonuclease III is an iron-sulfur protein Biochemistry 28 1989 4450 4455
9. S.S. David, and S.D. Williams Chemistry of glycosylases and endonucleases involved in base-excision repair Chem Rev 98 1998 1221 1261
10. J.A. Hinks, M.C.W. Evans, Y. de Miguel, A.A. Sartori, J. Jiricny, and L.H. Pearl An iron-sulfur cluster in the Family 4 uracil-DNA glycosylase J Biol Chem 277 2002 16936 16940
11. M. Sandigursky, and W.A. Franklin Thermostable uracil-DNA glycosylase from Thermotoga maritima, a member of a novel class of DNA repair enzymes Curr Biol 9 1999 531 534
12. J. Hoseki, A. Okamoto, R. Masui, T. Shibata, Y. Inoue, S. Yokoyama, and S. Kuramitsu Crystal structure of a Family 4 uracil-DNA glycosylase from Thermus thermophilus HB8 J Mol Biol 333 2003 515 526
13. L.H. Pearl Structure and function in the uracil-DNA glycosylase superfamily Mutat Res 460 2000 165 181
14. J. Frazzon, J.R. Flick, and D.R. Dean Biosynthesis of iron-sulfur clusters is a complex and highly conserved process Biochem Soc Trans 30 2002 680 685
15. S.S. Mansy, and J.A. Cowan Iron-sulfur cluster biosynthesis: toward an understanding of cellular machinery and molecular mechanism Acc Chem Res 37 2004 719 725
16. W. Fu, S. O'Handley, R.P. Cunningham, and M.K. Johnson The role of the iron-sulfur cluster in Escherichia coli endonuclease III J Biol Chem 267 1992 16135 16137
17. M.M. Thayer, H. Ahern, D. Xing, R.P. Cunningham, and J.A. Tainer Novel DNA binding motifs in the DNA repair enzyme endonuclease III crystal structure EMBO J 14 1995 4108 4120
18. Y. Guan, R.C. Manuel, A.S. Arvai, S.S. Parikh, C.D. Mol, J.H. Miller, R.S. Lloyd, and J.A. Tainer MutY catalytic core, mutant and bound adenine structures define specificity for DNA repair enzyme superfamily Nat Struct Biol 5 1998 1058 1064
19. S.L. Porello, A.E. Leyes, and S.S. David Single-turnover and pre-steady-state kinetics of the reaction of the adenine glycosylase MutY with mismatch-containing DNA substrates Biochemistry 37 1998 14756 14764
20. J.P. Radicella, E.A. Clark, and M.S. Fox Some mismatch repair activities in Escherichia coli Proc Natl Acad Sci USA 85 1988 9674 9678
21. J.-J. Tsai-Wu, H.-F. Liu, and A.-L. Lu Escherichia coli MutY protein has both N-glycosylase and apurinic/apyrimidinic endonuclease activities on A-C and A-G Mispairs Proc Natl Acad Sci USA 89 1992 8779 8783
22. S.L. Porello, M.J. Cannon, and S.S. David Assembly of the iron-sulfur cluster in the adenine glycosylase, MutY: evidence for a critical role of the [4Fe-4S] cluster in substrate recognition Biochemistry 37 1998 6465 6475
23. C.L. Chepanoske, M.P. Golinelli, S.D. Williams, and S.S. David Positively charged residues within the iron-sulfur cluster loop of E. coli MutY participate in damage recognition and removal Arch Biochem Biophys 380 2000 11 19
24. 2+ cluster-containing glycosylase bound to substrate DNA and provides suggestive evidence consistent with the role of the FCL in recognition of damaged DNA.
25. J.C. Fromme, A. Banerjee, S.J. Huang, and G.L. Verdine Structural basis for removal of adenine mispaired with 8-oxoguanine by MutY adenine DNA glycosylase Nature 427 2004 652 656
26. J.-M. Moulis, V. Devasse, M.-P. Golinelli, J. Meyer, and I. Quinkal The coordination sphere of iron-sulfur clusters: lessons from site-directed mutagenesis experiments J Bioinorg Chem 1 1996 2 14
27. M.-P. Golinelli, N.H. Chmiel, and S.S. David Site-directed mutagenesis of the cysteine ligands to the [4Fe-4S] cluster of Escherichia coli MutY Biochemistry 38 1999 6997 7007
28. 1+ cluster supports the glycosylase activity of MutY. This feature of the enzyme may be a way to preserve the adenine-excision chemistry under conditions of oxidative stress.
29. E.M. Boon, A.L. Livingston, N.H. Chmiel, S.S. David, and J.K. Barton DNA-mediated charge transport for DNA repair Proc Natl Acad Sci USA 100 2003 12543 12547 This paper was the first report showing that the redox properties of the iron-sulfur cluster in MutY may be accessed using DNA-mediated electrochemistry. This provides an important basis for determining how such DNA-mediated electron-transfer may be used in the functional properties of MutY.
30. C.-F. Kuo, D.E. McRee, C.L. Fisher, S.F. O'Handley, R.P. Cunningham, and J.A. Tainer Atomic structure of the DNA repair [4Fe-4S] enzyme endonuclease III Science 258 1992 434 440
31. C.L. Chepanoske, O.L. Lukianova, M. Lombard, M.-P. Golinelli-Cohen, and S.S. David A residue in MutY important for catalysis indentified by photocrosslinking and mass spectrometry Biochemistry 43 2004 651 662 This paper shows that Arg143, which H-bonds to Cys192 of the FCL, may be photochemically cross-linked to 4-thio-T-containing DNA. In addition, mutagenesis of this residue showed its functional importance. Arg143 and Arg147 are strictly conserved among the cluster-containing BER superfamily, and similar residues are also conserved in 4UDGs. This work elaborates the intimate relationship between the region around the cluster and the DNA substrate, further supporting the importance of the cluster in damage recognition and repair.
32. 3+ cluster as monitored by EPR and transient absorption. This oxidation is mediated by the DNA duplex with guanine radicals as an intermediate oxidant that facilitates oxidation of MutY. This suggests that DNA radicals may be directly repaired by oxidation of the cluster and also suggests that DNA damage may provide the signal to stimulate DNA repair.
33. H. Bai, S. Jones, X. Guan, T.M. Wilson, J.R. Sampson, J.P. Cheadle, and A.-L. Lu Functional characterization of two human MutY homolog (hMYH) missense mutations (R227W and V232F) that lie within the putative hMSH6 binding domain and are associated with hMYH polyposis Nucleic Acids Res 33 2005 597 604 This paper shows that R227W hMYH has a reduced ability to bind to an OG:A mismatch-containing duplex. Qualitative glycosylase assays also show minimal adenine glycosylase activity with an OG:A substrate. These results are consistent with those reported for R143A MutY; the magnitude to the decreased activity is less in this case consistent with what is typically seen with the E. coli enzyme, and also the differences in the type of amino acid substitution.
34. C. Fleischman, J. Peto, J. Cheadle, B. Shah, J. Sampson, and R.S. Houlston Comprehensive analysis of the contribution of germline MYH variation to early-onset colorectal cancer Int J Cancer 109 2004 554 558 Biallelic mutations in the gene encoding hMYH have been shown to be associated with predisposition to colorectal adenomas and carcinomas, and this predisposition mechanism is referred to as MYH-associated polyposis (MAP). In this paper, the R227W hMYH variant was identified to be associated with MAP and this underscores the importance of the region supported by the 4Fe-4S cluster.