S-Adenosylmethionine-dependent radical-based modification of biological macromolecules

Current Opinion in Structural Biology

Volumn 20, Issue 6, 2010, Pages 684-692

  Atta, Mohamed ^a   Mulliez, Etienne ^a   Arragain, Simon ^a   Forouhar, Farhad ^b   Hunt, John F ^b   Fontecave, Marc ^a,c  

^a CEA GRENOBLE   (France)

^b Columbia University ^*  (United States)

^c Centre de Recherche Interdisciplinaire en Biologie   (France)

Author keywords

[No Author keywords available]

Indexed keywords

FREE RADICAL; GLYCINE; RNA; S ADENOSYLMETHIONINE;

CATALYSIS; CHEMICAL REACTION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME MECHANISM; ENZYME STRUCTURE; MACROMOLECULE; METHYLATION; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTEIN SYNTHESIS; REVIEW;

AMINO ACID SEQUENCE; ENZYMES; FREE RADICALS; HUMANS; PROTEINS; RNA; S-ADENOSYLMETHIONINE;

EID: 78649637486     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.sbi.2010.09.009     Document Type: Review

References (46)

1. Posttranslational Modification of Proteins: Expanding Nature's Inventory 2006, Roberts, B and Company Publishers, Colorado. C.T. Walsh (Ed.).
2. DNA and RNA Modification Enzymes: Structure, Mechanism, Function and Evolution 2009, Landes Bioscience, Texas. H. Grosjean (Ed.).
3. Dunin-Horkawicz S., Czerwoniec A., Gajda M.J., Feder M., Grosjean H., Bujnicki J.M. MODOMICS: a database of RNA modification pathways. Nucleic Acids Res 2006, 34:D145-D149.
4. Atta M., Fontecave M., Mulliez E. RNA-modifying metalloenzymes. DNA and RNA Modification Enzymes: Structure Mechanism, Function and Evolution 2009, 347-357. Landes Bioscience. H. Grosjean (Ed.).
5. Marsh E.N.G., Patterson D.P., Li L. Adenosyl radical: reagent and catalyst in enzyme reactions. Chembiochem 2010, 11:604-621.
6. Arragain S., Garcia-Serres R., Blondin G., Douki T., Clemancey M., Latour J.M., Forouhar F., Neely H., Montelione G.T., Hunt J.F., et al. Post-translational modification of ribosomal proteins structural and functional characterization of RimO from thermotoga maritima, a radical s-adenosylmethionine methylthiotransferase. J Biol Chem 2010, 285:5792-5801.
7. Lee K.H., Saleh L., Anton B.P., Madinger C.L., Benner J.S., Iwig D.F., Roberts R.J., Krebs C., Booker S.J. Characterization of RimO, a new member of the methylthiotransferase subclass of the radical SAM superfamily. Biochemistry 2009, 48:10162-10174.
8. Frey P.A., Hegeman A.D., Ruzicka F.J. The radical SAM superfamily. Crit Rev Biochem Mol Biol 2008, 43:63-88.
9. Layer G., Moser J., Heinz D.W., Jahn D., Schubert W.D. Crystal structure of coproporphyrinogen III oxidase reveals cofactor geometry of Radical SAM enzymes. EMBO J 2003, 22:6214-6224.
10. Berkovitch F., Nicolet Y., Wan J.T., Jarrett J.T., Drennan C.L. Crystal structure of biotin synthase, an S-adenosylmethionine-dependent radical enzyme. Science 2004, 303:76-79.
11. Hanzelmann P., Schindelin H. Crystal structure of the S-adenosylmethionine-dependent enzyme MoaA and its implications for molybdenum cofactor deficiency in humans. Proc Natl Acad Sci U S A 2004, 101:12870-12875.
12. Lepore B.W., Ruzicka F.J., Frey P.A., Ringe D. The X-ray crystal structure of lysine-2,3-aminomutase from Clostridium subterminale. Proc Natl Acad Sci U S A 2005, 102:13819-13824.
13. Suzuki Y., Noma A., Suzuki T., Senda M., Senda T., Ishitani R., Nureki O. Crystal structure of the radical SAM enzyme catalyzing tricyclic modified base formation in tRNA. J Mol Biol 2007, 372:1204-1214.
14. Goto-Ito S., Ishii R., Ito T., Shibata R., Fusatomi E., Sekine S., Bessho Y., Yokoyama S. Structure of an archaeal TYW1, the enzyme catalyzing the second step of wye-base biosynthesis. Acta Crystallogr D Biol Crystallogr 2007, 63:1059-1068.
15. Nicolet Y., Rubach J.K., Posewitz M.C., Amara P., Mathevon C., Atta M., Fontecave M., Fontecilla-Camps J.C. X-ray structure of the [FeFe]-hydrogenase maturase HydE from Thermotoga maritima. J Biol Chem 2008, 283:18861-18872.
16. Chatterjee A., Li Y., Zhang Y., Grove T.L., Lee M., Krebs C., Booker S.J., Begley T.P., Ealick S.E. Reconstitution of ThiC in thiamine pyrimidine biosynthesis expands the radical SAM superfamily. Nat Chem Biol 2008, 4:758-765.
17. Vey J.L., Yang J., Li M., Broderick W.E., Broderick J.B., Drennan C.L. Structural basis for glycyl radical formation by pyruvate formate-lyase activating enzyme. Proc Natl Acad Sci U S A 2008, 105:16137-16141.
18. Wagner A.F.V., Frey M., Neugebauer F.A., Schafer W., Knappe J. The free-radical in pyruvate formate-lyase is located on glycine-734. Proc Natl Acad Sci U S A 1992, 89:996-1000.
19. Sun X.Y., Ollagnier S., Schmidt P.P., Atta M., Mulliez E., Lepape L., Eliasson R., Graslund A., Fontecave M., Reichard P., et al. The free radical of the anaerobic ribonucleotide reductase from Escherichia coli is at glycine 681. J Biol Chem 1996, 271:6827-6831.
20. Krieger C.J., Roseboom W., Albracht S.P.J., Spormann A.M. A stable organic free radical in anaerobic benzylsuccinate synthase of Azoarcus sp. strain T. J Biol Chem 2001, 276:12924-12927.
21. Kowalak J.A., Walsh K.A. Beta-methylthio-aspartic acid: identification of a novel posttranslational modification in ribosomal protein S12 from Escherichia coli. Protein Sci 1996, 5:1625-1632.
22. Anton B.P., Saleh L., Benner J.S., Raleigh E.A., Kasif S., Roberts R.J. RimO, a MiaB-like enzyme, methylthiolates the universally conserved Asp88 residue of ribosomal protein S12 in Escherichia coli. Proc Natl Acad Sci U S A 2008, 105:1826-1831.
23. Hanson S.R., Best M.D., Wong C.H. Sulfatases: structure, mechanism, biological activity, inhibition, and synthetic utility. Angew Chem Int Ed 2004, 43:5736-5763.
24. Fang Q.H., Peng J.H., Dierks T. Post-translational formylglycine modification of bacterial sulfatases by the radical S-adenosylmethionine protein AtsB. J Biol Chem 2004, 279:14570-14578.
25. Grove T.L., Lee K.H., St Clair J., Krebs C., Booker S.J. In vitro characterization of AtsB, a radical SAM formylglycine-generating enzyme that contains three [4Fe-4S] clusters. Biochemistry 2008, 47:7523-7538.
26. Benjdia A., Leprince J., Sandstrom C., Vaudry H., Berteau O. Mechanistic investigations of anaerobic sulfatase-maturating enzyme: direct C-beta H-atom abstraction catalyzed by a radical AdoMet enzyme. J Am Chem Soc 2009, 131. 8348-+.
27. Benjdia A., Subramanian S., Leprince J., Vaudry H., Johnson M.K., Berteau O. Anaerobic sulfatase-maturating enzyme-a mechanistic link with glycyl radical-activating enzymes?. FEBS J 2010, 277:1906-1920.
28. Liu S.H., Milne G.T., Kuremsky J.G., Fink G.R., Leppla S.H. Identification of the proteins required for biosynthesis of diphthamide, the target of bacterial ADP-ribosylating toxins on translation elongation factor 2. Mol Cell Biol 2004, 24:9487-9497.
29. Zhang Y., Zhu X.L., Torelli A.T., Lee M., Dzikovski B., Koralewski R.M., Wang E., Freed J., Krebs C., Ealick S.E., et al. Diphthamide biosynthesis requires an organic radical generated by an iron-sulphur enzyme. Nature 2010, 465:U891-U894.
30. Hernandez H.L., Pierrel F., Elleingand E., Garcia-Serres R., Huynh B.H., Johnson M.K., Fontecave M., Atta M. MiaB, a bifunctional radical-S-adenosylmethionine enzyme involved in the thiolation and methylation of tRNA, contains two essential [4Fe-4S] clusters. Biochemistry 2007, 46:5140-5147.
31. Yan F., LaMarre J.M., Rohrich R., Wiesner J., Jomaa H., Mankin A.S., Fujimori D.G. RImN and Cfr are radical SAM enzymes involved in methylation of ribosomal RNA. J Am Chem Soc 2010, 132:3953-3964.
32. phe. DNA and RNA Modification Enzymes: Structure, Mechanism, Function and Evolution. 2009, 423-435. Lands Bioscience. H. Grosjean (Ed.).
33. Frey M., Rothe M., Wagner A.F.V., Knappe J. Adenosylmethionine-dependent synthesis of the glycyl radical in pyruvate formate-lyase by abstraction of the glycine C-2 Pro-S hydrogen-atom-studies of [H-2]glycine-substituted enzyme and peptides homologous to the glycine-734 site. J Biol Chem 1994, 269:12432-12437.
34. Gambarelli S., Luttringer F., Padovani D., Mulliez E., Fontecave M. Activation of the anaerobic ribonucleotide reductase by S-adenosylmethionine. Chembiochem 2005, 6:1960-1962.
35. Becker A., Fritz-Wolf K., Kabsch W., Knappe J., Schultz S., Wagner A.F.V. Structure and mechanism of the glycyl radical enzyme pyruvate formate-lyase. Nat Struct Biol 1999, 6:969-975.
36. Logan D.T., Andersson J., Sjoberg B.M., Nordlund P. A glycyl radical site in the crystal structure of a class III ribonucleotide reductase. Science 1999, 283:1499-1504.
37. Anton BP, Russell SP, Vertrees J, Kasif S, Raleigh EA, Limbach PA, Roberts RJ: Functional characterization of the YmcB and YqeV tRNA methylthiotransferases of Bacillus subtilis. Nucleic Acids Res.
38. Arragain S., Handelman S.K., Forouhar F., Wei F.Y., Tomizawa K., Hunt J.F., Douki T., Fontecave M., Mulliez E., Atta M. Identification of eukaryotic and prokaryotic methylthiotransferase for biosynthesis of 2-methylthio-N6-threonylcarbamoyladenosine in tRNA. J Biol Chem 2010, 285:28425-28433.
39. Steinthorsdottir V., Thorleifsson G., Reynisdottir I., Benediktsson R., Jonsdottir T., Walters G.B., Styrkarsdottir U., Gretarsdottir S., Emilsson V., Ghosh S., et al. A variant in CDKAL1 influences insulin response and risk of type 2 diabetes. Nat Genet 2007, 39:770-775.
40. Pierrel F., Douki T., Fontecave M., Atta M. MiaB protein is a bifunctional radical-S-adenosylmethionine enzyme involved in thiolation and methylation of tRNA. J Biol Chem 2004, 279:47555-47563.
41. Fontecave M., Ollagnier-de-Choudens S., Mulliez E. Biological radical sulfur insertion reactions. Chem Rev 2003, 103:2149-2166.
42. Booker S.J., Cicchillo R.M., Grove T.L. Self-sacrifice in radical S-adenosylmethionine proteins. Curr Opin Chem Biol 2007, 11:543-552.
43. Hou Y.M., Perona J.J. Stereochemical mechanisms of tRNA methyltransferases. FEBS Lett 2010, 584:278-286.
44. Grove T.L., Ahlum J.H., Sharma P., Krebs C., Booker S.J. A consensus mechanism for radical SAM-dependent dehydrogenation? BtrN contains two [4Fe-4S] clusters. Biochemistry 2010, 49:3783-3785.
45. Umitsu M., Nishimasu H., Noma A., Suzuki T., Ishitani R., Nureki O. Structural basis of AdoMet-dependent aminocarboxypropyl transfer reaction catalyzed by tRNA-wybutosine synthesizing enzyme, TYW2. Proc Natl Acad Sci U S A 2009, 106:15616-15621.
46. Hanzelmann P., Schindelin H. Binding of 5′-GTP to the C-terminal FeS cluster of the radical S-adenosylmethionine enzyme MoaA provides insights into its mechanism. Proc Natl Acad Sci U S A 2006, 103:6829-6834.