X-ray analysis of butirosin biosynthetic enzyme BtrN redefines structural motifs for AdoMet radical chemistry

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 40, 2013, Pages 15949-15954

  Goldman, Peter J ^a   Groèe, Tyler L ^b   Booker, Squire J ^b,c   Drennan, Catherine L ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b Department of Chemistry ^*  (United States)

^c PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Iron sulfur cluster fold; Radical SAM enzyme; Twitch domain

Indexed keywords

BACTERIAL ENZYME; BUTIROSIN; MOLYBDENUM; OXIDOREDUCTASE; S ADENOSYLMETHIONINE;

ARTICLE; BACILLUS CIRCULANS; BIOSYNTHESIS; ENZYME CHEMISTRY; ENZYME METABOLISM; ENZYME STRUCTURE; ENZYME SUBSTRATE; NONHUMAN; PRIORITY JOURNAL; STRUCTURAL HOMOLOGY; X RAY ANALYSIS;

IRON-SULFUR CLUSTER FOLD; RADICAL SAM ENZYME; TWITCH DOMAIN;

BACILLUS; BIOSYNTHETIC PATHWAYS; BUTIROSIN SULFATE; CARBOHYDRATE DEHYDROGENASES; CRYSTALLIZATION; DNA PRIMERS; IRON COMPOUNDS; MODELS, MOLECULAR; MOLECULAR STRUCTURE; PROTEIN BINDING; PROTEIN CONFORMATION; S-ADENOSYLMETHIONINE; SULFUR COMPOUNDS;

EID: 84885045053     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1312228110     Document Type: Article

References (44)

1. Davies J, Davies D (2010) Origins and evolution of antibiotic resistance. Microbiol Mol Biol Rev 74(3):417-433.
2. Vakulenko SB, Mobashery S (2003) Versatility of aminoglycosides and prospects for their future. Clin Microbiol Rev 16(3):430-450.
3. Wehmeier UF, Piepersberg W (2009) Enzymology of aminoglycoside biosynthesisdeduction from gene clusters. Methods Enzymol 459:459-491.
4. Kudo F, Yamamoto Y, Yokoyama K, Eguchi T, Kakinuma K (2005) Biosynthesis of 2-deoxystreptamine by three crucial enzymes in Streptomyces fradiae NBRC 12773. J Antibiot (Tokyo) 58(12):766-774.
5. Yokoyama K, Numakura M, Kudo F, Ohmori D, Eguchi T (2007) Characterization and mechanistic study of a radical SAM dehydrogenase in the biosynthesis of butirosin. J Am Chem Soc 129(49):15147-15155.
6. Kudo F, Eguchi T (2009) Biosynthetic genes for aminoglycoside antibiotics. J Antibiot (Tokyo) 62(9):471-481.
7. Frey PA, Hegeman AD, Ruzicka FJ (2008) The Radical SAM Superfamily. Crit Rev Biochem Mol Biol 43(1):63-88.
8. Benjdia A, et al. (2008) Anaerobic sulfatase-maturating enzymes, first dual substrate radical S-adenosylmethionine enzymes. J Biol Chem 283(26):17815-17826.
9. Grove TL, Lee KH, St Clair J, Krebs C, Booker SJ (2008) In vitro characterization of AtsB, a radical SAM formylglycine-generating enzyme that contains three [4Fe-4S] clusters. Biochemistry 47(28):7523-7538.
10. Lanz ND, Booker SJ (2012) Identification and function of auxiliary iron-sulfur clusters in radical SAM enzymes. Biochim Biophys Acta 1824(11):1196-1212.
11. Szu PH, Ruszczycky MW, Choi SH, Yan F, Liu HW (2009) Characterization and mechanistic studies of DesII: A radical S-adenosyl-L-methionine enzyme involved in the biosynthesis of TDP-D-desosamine. J Am Chem Soc 131(39):14030-14042.
12. Sofia HJ, Chen G, Hetzler BG, Reyes-Spindola JF, Miller NE (2001) 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(5):1097-1106.
13. Hiscox MJ, Driesener RC, Roach PL (2012) Enzyme catalyzed formation of radicals from S-adenosylmethionine and inhibition of enzyme activity by the cleavage products. Biochim Biophys Acta 1824(11):1165-1177.
14. Walsby CJ, Ortillo D, Broderick WE, Broderick JB, Hoffman BM (2002) An anchoring role for FeS clusters: Chelation of the amino acid moiety of S-adenosylmethionine to the unique iron site of the [4Fe-4S] cluster of pyruvate formate-lyase activating enzyme. J Am Chem Soc 124(38):11270-11271.
15. Vey JL, Drennan CL (2011) Structural insights into radical generation by the radical SAM superfamily. Chem Rev 111(4):2487-2506.
16. Dowling DP, Vey JL, Croft AK, Drennan CL (2012) Structural diversity in the AdoMet radical enzyme superfamily. Biochim Biophys Acta 1824(11):1178-1195.
17. Yokoyama K, Ohmori D, Kudo F, Eguchi T (2008) Mechanistic study on the reaction of a radical SAM dehydrogenase BtrN by electron paramagnetic resonance spectroscopy. Biochemistry 47(34):8950-8960.
18. Grove TL, Ahlum JH, Sharma P, Krebs C, Booker SJ (2010) A consensus mechanism for Radical SAM-dependent dehydrogenation? BtrN contains two [4Fe-4S] clusters. Biochemistry 49(18):3783-3785.
19. Benjdia A, et al. (2010) Anaerobic sulfatase-maturating enzyme-a mechanistic link with glycyl radical-activating enzymes? FEBS J 277(8):1906-1920.
20. Goldman PJ, et al. (2013) X-ray structure of an AdoMet radical activase reveals an anaerobic solution for formylglycine posttranslational modification. Proc Natl Acad Sci USA 110(21):8519-8524.
21. Haft DH, Basu MK (2011) Biological systems discovery in silico: Radical Sadenosylmethionine protein families and their target peptides for posttranslational modification. J Bacteriol 193(11):2745-2755.
22. Flühe L, et al. (2012) The radical SAM enzyme AlbA catalyzes thioether bond formation in subtilosin A. Nat Chem Biol 8(4):350-357.
23. Wecksler SR, et al. (2009) Pyrroloquinoline quinone biogenesis: Demonstration that PqqE from Klebsiella pneumoniae is a radical S-adenosyl-L-methionine enzyme. Biochemistry 48(42):10151-10161.
24. Haft DH (2011) Bioinformatic evidence for a widely distributed, ribosomally produced electron carrier precursor, its maturation proteins, and its nicotinoprotein redox partners. BMC Genomics 12:21.
25. Hänzelmann P, Schindelin H (2004) Crystal structure of the S-adenosylmethioninedependent enzyme MoaA and its implications for molybdenum cofactor deficiency in humans. Proc Natl Acad Sci USA 101(35):12870-12875.
26. Hover BM, Loksztejn A, Ribeiro AA, Yokoyama K (2013) Identification of a cyclic nucleotide as a cryptic intermediate in molybdenum cofactor biosynthesis. J Am Chem Soc 135(18):7019-7032.
27. Hänzelmann P, Schindelin H (2006) 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 USA 103(18):6829-6834.
28. Lees NS, et al. (2009) ENDOR spectroscopy shows that guanine N1 binds to [4Fe-4S] cluster II of the S-adenosylmethionine-dependent enzyme MoaA: Mechanistic implications. J Am Chem Soc 131(26):9184-9185.
29. Layer G, Moser J, Heinz DW, Jahn D, Schubert WD (2003) Crystal structure of coproporphyrinogen III oxidase reveals cofactor geometry of Radical SAM enzymes. EMBO J 22(23):6214-6224.
30. Nicolet Y, Amara P, Mouesca JM, Fontecilla-Camps JC (2009) Unexpected electron transfer mechanism upon AdoMet cleavage in radical SAM proteins. Proc Natl Acad Sci USA 106(35):14867-14871.
31. Quitterer F, List A, Eisenreich W, Bacher A, Groll M (2012) Crystal structure of methylornithine synthase (PylB): Insights into the pyrrolysine biosynthesis. Angew Chem Int Ed Engl 51(6):1339-1342.
32. Hayon E, Simic M (1974) Acid-base properties of free-radicals in solution. Acc Chem Res 7(4):114-121.
33. Guillén Schlippe YV, Hedstrom L (2005) A twisted base? The role of arginine in enzyme-catalyzed proton abstractions. Arch Biochem Biophys 433(1):266-278.
34. Ruszczycky MW, Choi SH, Liu HW (2013) EPR-kinetic isotope effect study of the mechanism of radical-mediated dehydrogenation of an alcohol by the radical SAM enzyme DesII. Proc Natl Acad Sci USA 110(6):2088-2093.
35. Moser CC, Anderson JL, Dutton PL (2010) Guidelines for tunneling in enzymes. Biochim Biophys Acta 1797(9):1573-1586.
36. Ruszczycky MW, Choi SH, Liu HW (2010) Stoichiometry of the redox neutral deamination and oxidative dehydrogenation reactions catalyzed by the radical SAM enzyme DesII. J Am Chem Soc 132(7):2359-2369.
37. Ruszczycky MW, Choi SH, Mansoorabadi SO, Liu HW (2011) Mechanistic studies of the radical S-adenosyl-L-methionine enzyme DesII: EPR characterization of a radical intermediate generated during its catalyzed dehydrogenation of TDP-D-quinovose. J Am Chem Soc 133(19):7292-7295.
38. Szu PH, He X, Zhao L, Liu HW (2005) Biosynthesis of TDP-D-desosamine: Identification of a strategy for C4 deoxygenation. Angew Chem Int Ed Engl 44(41):6742-6746.
39. Ruszczycky MW, Ogasawara Y, Liu HW (2012) Radical SAM enzymes in the biosynthesis of sugar-containing natural products. Biochim Biophys Acta 1824(11): 1231-1244.
40. Pegg SC, et al. (2006) Leveraging enzyme structure-function relationships for functional inference and experimental design: The structure-function linkage database. Biochemistry 45(8):2545-2555.
41. Flühe L, et al. (2013) Two [4Fe-4S] clusters containing radical SAM enzyme SkfB catalyze thioether bond formation during the maturation of the sporulation killing factor. J Am Chem Soc 135(3):959-962.
42. Grove TL, et al. (2013) Further characterization of Cys-type and Ser-type anaerobic sulfatase maturating enzymes suggests a commonality in the mechanism of catalysis. Biochemistry 52(17):2874-2887.
43. Long F, et al. (2010) Crystal structures of the CusA efflux pump suggest methioninemediated metal transport. Nature 467(7314):484-488.
44. Smoot ME, Ono K, Ruscheinski J, Wang PL, Ideker T (2011) Cytoscape 2.8: New features for data integration and network visualization. Bioinformatics 27(3):431-432.