The generation of 5′-deoxyadenosyl radicals by adenosylmethionine-dependent radical enzymes

Current Opinion in Chemical Biology

Volumn 7, Issue 2, 2003, Pages 174-182

  Jarrett, Joseph T ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALKYL GROUP; FREE RADICAL; IRON SULFUR PROTEIN; S ADENOSYLMETHIONINE; 5' DEOXYADENOSINE; 5'-DEOXYADENOSINE; DEOXYADENOSINE DERIVATIVE; ENZYME;

BIODIVERSITY; CATALYSIS; CATALYST; CHEMICAL INTERACTION; COVALENT BOND; ELECTRON TRANSPORT; ENZYME MECHANISM; MOLECULAR BIOLOGY; PROTEIN MOTIF; REDUCTION; REGULATORY MECHANISM; REVIEW; STOICHIOMETRY; CHEMISTRY;

DEOXYADENOSINES; ENZYMES; FREE RADICALS; S-ADENOSYLMETHIONINE;

EID: 0037399004     PISSN: 13675931     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1367-5931(03)00022-X     Document Type: Review

References (53)

1. Stubbe J., van der Donk W.A. Protein radicals in enzyme catalysis. Chem. Rev. 98:1998;705-762.
2. Frey P.A. Radical mechanisms of enzymatic catalysis. Annu. Rev. Biochem. 70:2001;121-148 Review that focuses on mechanisms of AdoMet- and adenosylcobalamin-dependent radical enzymes.
3. Stubbe J: Di-iron-tyrosyl radical (Y•) ribonucleotide reductases. Curr Opin Chem Biol 2003, 7: this issue.
4. Licht S., Stubbe J. Mechanistic investigations of ribonucleotide reductases. Comprehen. Nat. Prod. Chem. 5:1999;163-203.
5. Rogers M, Dooley D: Copper-tyrosyl radical enzymes. Curr Opin Chem Biol 2003, 7: this issue.
6. Marsh E.N., Drennan C.L. Adenosylcobalamin-dependent isomerases: new insights into structure and mechanism. Curr. Opin. Chem. Biol. 5:2001;499-505.
7. Frey P.A., Reed G.H. Radical mechanisms in adenosylmethionine- and adenosylcobalamin-dependent enzymatic reactions. Arch. Biochem. Biophys. 382:2000;6-14.
8. Frey P.A., Booker S.J. Radical mechanisms of S-adenosylmethionine-dependent enzymes. Adv. Protein Chem. 58:2001;1-45 Review with emphasis on the radical-mediated catalytic mechanisms of AdoMet radical enzymes, with a particularly good section on lysine 2,3-aminomutase.
9. Fontecave M., Mulliez E., Ollagnier-de-Choudens S. Adenosylmethionine as a source of 5′-deoxyadenosyl radicals. Curr. Opin. Chem. Biol. 5:2001;506-511.
10. Cheek J., Broderick J.B. Adenosylmethionine-dependent iron-sulfur enzymes: versatile clusters in a radical new role. J. Biol. Inorg. Chem. 6:2001;209-226 Review that highlights the properties and spectroscopy of the FeS clusters in AdoMet radical enzymes.
11. Magnusson O.T., Reed G.H., Frey P.A. Spectroscopic evidence for the participation of an allylic analogue of the 5′-deoxyadenosyl radical in the reaction of lysine 2,3-aminomutase. J. Am. Chem. Soc. 121:1999;9764-9765.
12. Magnusson O.T., Reed G.H., Frey P.A. Characterization of an allylic analogue of the 5′-deoxyadenosyl radical: an intermediate in the reaction of lysine 2,3-aminomutase. Biochemistry. 40:2001;7773-7782 EPR characterization of the 3′,4′-anhydro-5′-deoxyadenosyl radical with isotopically labeled anhydroAdoMet analogs.
13. Moss M., Frey P.A. The role of S-adenosylmethionine in the lysine 2,3-aminomutase reaction. J. Biol. Chem. 262:1987;14859-14862.
14. Cheek J., Broderick J.B. Direct H atom abstraction from spore photoproduct C-6 initiates DNA repair in the reaction catalyzed by spore photoproduct lyase: evidence for a reversibly generated adenosyl radical intermediate. J. Am. Chem. Soc. 124:2002;2860-2861 Tritium transfer into AdoMet demonstrates that photoproduct repair is initiated by H atom abstraction from the UV-crosslinked nucleotides.
15. Sofia H.J., Chen G., Hetzler B.G., Reyes-Spindola J.F., Miller N.E. Radical SAM, a novel protein superfamily linking unresolved steps in familiar biosynthetic pathways with radical mechanisms: functional characterization using new analysis and information visualization methods. Nucleic Acids Res. 29:2001;1097-1106 Genome sequence analysis that suggests AdoMet radical enzymes are present in many organisms, and identifies numerous genes that were not previously known to be radical enzymes. Some predictions may prove to be false leads, but this is not unexpected given the very low sequence homology among AdoMet radical enzymes.
16. Layer G., Verfurth K., Mahlitz E., Jahn D. Oxygen-independent coproporphyrinogen-III oxidase HemN from Escherichia coli. J. Biol. Chem. 277:2002;34136-34142 Demonstration that the enzyme activity requires AdoMet and NADPH, and is abolished by mutations in residues conserved within the AdoMet radical superfamily. The precise reaction catalyzed by this enzyme was unknown until it was identified as an AdoMet radical enzyme solely on the basis of sequence homology.
17. Pierrel F., Bjork G.R., Fontecave M., Atta M. Enzymatic modification of tRNAs: MiaB is an iron-sulfur protein. J. Biol. Chem. 277:2002;13367-13370.
18. Marquet A. Enzymology of carbon-sulfur bond formation. Curr. Opin. Chem. Biol. 5:2001;541-549.
19. Allen R.M., Chatterjee R., Ludden P.W., Shah V.K. Incorporation of iron and sulfur from NifB cofactor into the iron-molybdenum cofactor of dinitrogenase. J. Biol. Chem. 270:1995;26890-26896.
20. Broderick J.B., Duderstadt R.E., Fernandez D.C., Wojtuszewski K., Henshaw T.F., Johnson M.K. Pyruvate formate-lyase activating enzyme is an iron-sulfur protein. J. Am. Chem. Soc. 119:1997;7396-7397.
21. + cluster. Biochem. Biophys. Res. Commun. 269:2000;451-456.
22. Krebs C., Henshaw T.F., Cheek J., Huynh B.H., Broderick J.B. Conversion of 3Fe-4S to 4Fe-4S clusters in native pyruvate formate-lyase activating enzyme: Mössbauer characterization and implications for mechanism. J. Am. Chem. Soc. 122:2000;12497-12506.
23. Ollagnier S., Mulliez E., Gaillard J., Eliasson R., Fontecave M., Reichard P. The anaerobic Escherichia coli ribonucleotide reductase. Subunit structure and iron sulfur center. J. Biol. Chem. 271:1996;9410-9416.
24. Ollagnier S., Meier C., Mulliez E., Gaillard J., Schuenemann V., Trautwein A., Mattioli T., Lutz M., Fontecave M. Assembly of 2Fe-2S and 4Fe-4S clusters in the anaerobic ribonucleotide reductase from Escherichia coli. J. Am. Chem. Soc. 121:1999;6344-6350.
25. 2+ center. J. Biol. Chem. 274:1999;31291-31296.
26. + clusters with endogenous iron and sulfide in anaerobic ribonucleotide reductase activase in vitro. J. Biol. Chem. 275:2000;12367-12373.
27. Busby R.W., Schelvis J.P.M., Yu D.S., Babcock G.T., Marletta M.A. Lipoic acid biosynthesis: LipA is an iron-sulfur protein. J. Am. Chem. Soc. 121:1999;4706-4707.
28. Miller J.R., Busby R.W., Jordan S.W., Cheek J., Henshaw T.F., Ashley G.W., Broderick J.B., Cronan J.E. Jr., Marletta M.A. Escherichia coli LipA is a lipoyl synthase: in vitro biosynthesis of lipoylated pyruvate dehydrogenase complex from octanoyl-acyl carrier protein. Biochemistry. 39:2000;15166-15178.
29. Duin E.C., Lafferty M.E., Crouse B.R., Allen R.M., Sanyal I., Flint D.H., Johnson M.K. [2Fe-2S] to [4Fe-4S] cluster conversion in Escherichia coli biotin synthase. Biochemistry. 36:1997;11811-11820.
30. 2+ clusters. FEBS Lett. 459:1999;411-414.
31. Ugulava N.B., Gibney B.R., Jarrett J.T. Iron-sulfur cluster interconversions in biotin synthase: dissociation and reassociation of iron during conversion of [2Fe-2S] to [4Fe-4S] clusters. Biochemistry. 39:2000;5206-5214.
32. Ollagnier-De Choudens S., Sanakis Y., Hewitson K.S., Roach P., Baldwin J.E., Munck E., Fontecave M. Iron-sulfur center of biotin synthase and lipoate synthase. Biochemistry. 39:2000;4165-4173.
33. 2+ clusters.
34. Hewitson K.S., Baldwin J.E., Shaw N.M., Roach P.L. Mutagenesis of the proposed iron-sulfur cluster binding ligands in Escherichia coli biotin synthase. FEBS Lett. 466:2000;372-376.
35. Beinert H., Holm R.H., Munck E. Iron-sulfur clusters: nature's modular, multipurpose structures. Science. 277:1997;653-659.
36. Flint D.H., Tuminello J.F., Emptage M.H. The inactivation of Fe-S cluster containing hydro-lyases by superoxide. J. Biol. Chem. 268:1993;22369-22376.
37. Brown N.M., Kennedy M.C., Antholine W.E., Eisenstein R.S., Walden W.E. Detection of a [3Fe-4S] cluster intermediate of cytosolic aconitase in yeast expressing iron regulatory protein 1. Insights into the mechanism of Fe-S cluster cycling. J. Biol. Chem. 277:2002;7246-7254.
38. 2: [4Fe-4S] to [2Fe-2S] conversion with loss of biological activity. Proc. Natl. Acad. Sci. U.S.A. 94:1997;6087-6092.
39. Wu W., Booker S., Lieder K.W., Bandarian V., Reed G.H., Frey P.A. Lysine 2,3-aminomutase and trans-4,5-dehydrolysine: characterization of an allylic analogue of a substrate-based radical in the catalytic mechanism. Biochemistry. 39:2000;9561-9570.
40. 1+ cluster of pyruvate formate-lyase activating enzyme generates the glycyl radical on pyruvate formate-lyase: EPR-detected single turnover. J. Am. Chem. Soc. 122:2000;8331-8332.
41. 2 subunit.
42. Ollagnier-de Choudens S., Sanakis Y., Hewitson K.S., Roach P., Munck E., Fontecave M. Reductive cleavage of S-adenosylmethionine by biotin synthase from Escherichia coli. J. Biol. Chem. 277:2002;13449-13454.
43. Saeva F.D., Morgan B.P. Mechanism of one-electron electrochemical reductive cleavage reactions of sulfonium salts. J. Am. Chem. Soc. 106:1984;4121-4125.
44. Beak P., Sullivan T.A. One-electron chemical reduction of phenylalkylsulfonium salts. J. Am. Chem. Soc. 104:1982;4450-4457.
45. 2-,3- clusters with sulfonium cations: analogue reaction systems for the initial step in biotin synthase catalysis. Inorg. Chem. 40:2001;2785-2793 Potential model reactions for 5′-deoxyadenosyl radical generation. Suggests that facile sulfonium reduction may be an inherent property of [4Fe-4S] clusters.
46. 2+ cluster allows sensitive observation of changes in the Mössbauer spectrum that are caused by changes in the Fe coordination environment following AdoMet binding.
47. 2+ cluster in reconstituted biotin synthase binds S-adenosyl-L-methionine. J. Am. Chem. Soc. 124:2002;14006-14007 Changes in the resonance Raman, Mössbauer and EPR spectra accompany AdoMet binding to BS, suggesting direct coordination to the [4Fe-4S] cluster.
48. 13C -methyl AdoMet bound to PFL activase suggest close proximity of the AdoMet sulfonium to the [4Fe-4S] cluster.
49. Ugulava NB, Frederick KK, Jarrett JT: Control of adenosylmethionine-dependent radical generation in biotin synthase: a kinetic and thermodynamic analysis of substrate binding to active and inactive forms of BioB. Biochemistry in press.
50. Cosper N.J., Booker S.J., Ruzicka F., Frey P.A., Scott R.A. Direct FeS cluster involvement in generation of a radical in lysine 2,3-aminomutase. Biochemistry. 39:2000;15668-15673.
51. Adams R.D., Chodosh D.F. Positively charged ligands. The coordination behavior of sulfonium cations. J. Am. Chem. Soc. 100:1978;812-817.
52. 15N -methionyl AdoMet bound to PFL activase suggest covalent coordination of the carboxylate and amine groups to the [4Fe-4S] cluster.
53. Hermuth K., Leuthner B., Heider J. Operon structure and expression of the genes for benzylsuccinate synthase in Thauera aromatica strain K172. Arch. Microbiol. 177:2002;132-138.