Protein residues that control the reaction trajectory in s-adenosylmethionine radical enzymes: Mutagenesis of asparagine 153 and aspartate 155 in escherichia coli biotin synthase

Biochemistry

Volumn 48, Issue 11, 2009, Pages 2448-2458

  Farrar, Christine E ^a   Jarrett, Joseph T ^a  

^a UNIVERSITY OF HAWAII   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

9-MERCAPTODETHIOBIOTIN; ACTIVE SITES; ASPARTATE; BIOTIN SYNTHASE; CATALYTIC CYCLES; DEOXYADENOSINE; DETHIOBIOTIN; HYDROGEN ATOMS; HYDROXYL GROUPS; IN-VITRO ASSAYS; MUTANT ENZYMES; OXIDATIVE ADDITIONS; PROTEIN RESIDUES; RADICAL ENZYMES; REDUCTIVE CLEAVAGES; S ADENOSYL L METHIONINES; S-ADENOSYLMETHIONINE; SEQUENCE MOTIFS; SITE-DIRECTED MUTATIONS; SULFUR ATOMS;

BINDING SITES; CATALYSTS; COENZYMES; ENZYMES; ESCHERICHIA COLI; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYDROGEN; MASS SPECTROMETRY; PLANTS (BOTANY); SULFUR;

HYDROGEN BONDS;

ASPARAGINE; ASPARTIC ACID; BIOTIN; BIOTIN SYNTHASE; S ADENOSYLMETHIONINE;

ARTICLE; CONTROLLED STUDY; ENZYME BINDING; ENZYME MECHANISM; ENZYME SUBSTRATE; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS;

AMINO ACID MOTIFS; ASPARAGINE; ASPARTIC ACID; BIOTIN; CATALYSIS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PROTEIN BINDING; S-ADENOSYLMETHIONINE; SULFURTRANSFERASES;

ESCHERICHIA COLI;

EID: 64849087619     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi8022569     Document Type: Article

References (33)

1. Jarrett, J. T. (2005) The novel structure and chemistry of ironsulfur clusters in the adenosylmethionine-dependent radical enzyme biotin synthase. Arch. Biochem. Biophys. 433, 312-321.
2. Marquet, A., Tse Sum Bui, B., and Florentin, D. (2001) Biosynthesis of biotin and lipoic acid. Vitam. Horm. 61, 51-101.
3. Escalletes, F., Florentin, D., Tse Sum Bui, B., Lesage, D., and Marquet, A. (1999) Biotin synthase mechanism: evidence for hydrogen transfer from the substrate into deoxyadenosine. J. Am. Chem. Soc. 121, 3571-3578.
4. Ugulava, N. B., Sacanell, C. J., and Jarrett, J. T. (2001) Spectroscopic changes during a single turnover of biotin synthase: destruction of a [2Fe-2S] cluster accompanies sulfur insertion. Biochemistry 40, 8352-8358.
5. Taylor, A. M., Farrar, C. E., and Jarrett, J. T. (2008) 9-Mercaptodethiobiotin is formed as a competent catalytic intermediate by Escherichia coli biotin synthase. Biochemistry 47, 9309-9317.
6. Farrar, C. E., and Jarrett, J. T. (2007) Radical S-Adenosylmethionine (SAM) Superfamily, in Encyclopedia of Life Sciences, John Wiley & Sons, Chichester(http://www.els.net/[doi:10.1002/ 9780470015902.a0020547]).
7. Sofia, H. J., Chen, G., Hetzler, B. G., Reyes-Spindola, J. F., and Miller, N. E. (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, 1097-1106.
8. Nicolet, Y., and Drennan, C. L. (2004)AdoMetradical proteinssfrom structure to evolutionsalignment of divergent protein sequences reveals strong secondary structure element conservation. Nucleic Acids Res. 32, 4015-4025.
9. Layer, G., Moser, J., Heinz, D. W., Jahn, D., and Schubert, W. D. (2003) Crystal structure of coproporphyrinogen III oxidase reveals cofactor geometry of Radical SAM enzymes. EMBO J. 22, 6214- 6224.
10. Hanzelmann, P., and Schindelin, H. (2004) 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. 101, 12870-12875.
11. Lepore, B. W., Ruzicka, F. J., Frey, P. A., and Ringe, D. (2005) The x-ray crystal structure of lysine-2,3-aminomutase from Clostridium subterminale. Proc. Natl. Acad. Sci. U.S.A. 102, 13819-13824.
12. Lotierzo, M., Raux, E., Tse Sum Bui, B., Goasdoue, N., Libot, F., Florentin, D., Warren, M. J., and Marquet, A. (2006) Biotin synthase mechanism: mutagenesis of the YNHNLD conserved motif. Biochemistry 45, 12274-12281.
13. Marquet, A., Frappier, F., Guillerm, G., Azoulay, M., Florentin, D., and Tabet, J.-C. (1993) Biotin biosynthesis: synthesis and biological evaluation of the putative intermediate thiols. J. Am. Chem. Soc. 115, 2139-2145.
14. Ugulava, N. B., Gibney, B. R., and Jarrett, J. T. (2000) Iron-sulfur cluster interconversions in biotin synthase: dissociation and reassociation of iron during conversion of [2Fe-2S] to [4Fe-4S] clusters. Biochemistry 39, 5206-5214.
15. Ugulava, N. B., Gibney, B. R., and Jarrett, J. T. (2001) Biotin synthase contains two distinct iron-sulfur cluster binding sites: chemical and spectroelectrochemical analysis of iron-sulfur cluster interconversions. Biochemistry 40, 8343-8351.
16. Beinert, H. (1978) Micro methods for the quantitative determination of iron and copper in biological material. Methods Enzymol. 54, 435-445.
17. Fish, W. W. (1988) Rapid colorimetric micromethod for the quantitation of complexed iron in biological samples. Methods Enzymol. 158, 357-364.
18. Beinert, H. (1983) Semi-micro methods for analysis of labile sulfide and of labile sulfide plus sulfane sulfur in unusually stable ironsulfur proteins. Anal. Biochem. 131, 373-378.
19. Broderick, J. B., Henshaw, T. F., Cheek, J., Wojtuszewski, K., Smith, S. R., Trojan, M. R., McGhan, R. M., Kopf, A., Kibbey, M., and Broderick, W. E. (2000) Pyruvate formate-lyase-activating enzyme: strictly anaerobic isolation yields active enzyme containing a [3Fe-4S]+ cluster. Biochem. Biophys. Res. Commun. 269, 451- 456.
20. Berkovitch, F., Nicolet, Y., Wan, J. T., Jarrett, J. T., and Drennan, C. L. (2004) Crystal structure of biotin synthase, an S-adenosylmethionine- dependent radical enzyme. Science 303, 76-79.
21. Ugulava, N. B., Surerus, K. K., and Jarrett, J. T. (2002) Evidence from Mossbauer spectroscopy for distinct [2Fe-2S]2+ and [4Fe- 4S]2+ cluster binding sites in biotin synthase from Escherichia coli. J. Am. Chem. Soc. 124, 9050-9051.
22. Ugulava, N. B., Frederick, K. K., and Jarrett, J. T. (2003) 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 42, 2708-2719.
23. Sanyal, I., Cohen, G., and Flint, D. H. (1994) Biotin synthase: purification, characterization as a [2Fe-2S] cluster protein, and in vitro activity of the Escherichia coli bioB gene product. Biochemistry 33, 3625-3631.
24. Duin, E. C., Lafferty, M. E., Crouse, B. R., Allen, R. M., Sanyal, I., Flint, D. H., and Johnson, M. K. (1997) [2Fe-2S] to [4Fe-4S] cluster conversion in Escherichia coli biotin synthase. Biochemistry 36, 11811-11820.
25. Sanyal, I., Gibson, K. J., and Flint, D. H. (1996) Escherichia coli biotin synthase: an investigation into the factors required for its activity and its sulfur donor. Arch. Biochem. Biophys. 326, 48-56.
26. Salib, A. G., Frappier, F., Guillerm, G., and Marquet, A. (1979) On the mechanism of conversion of dethiobiotin to biotin in Escherichia coli. III. Isolation of an intermediate in the biosynthesis of biotin from dethiobiotin. Biochem. Biophys. Res. Commun. 88, 312-319.
27. Shaw, N. M., Birch, O. M., Tinschert, A., Venetz, V., Dietrich, R., and Savoy, L. A. (1998) Biotin synthase from Escherichia coli: isolation of an enzyme-generated intermediate and stoichiometry of S-adenosylmethionine use. Biochem. J. 330, 1079-1085.
28. Baldet, P., Gerbling, H., Axiotis, S., and Douce, R. (1993) Biotin biosynthesis in higher plant cells. Identification of intermediates. Eur. J. Biochem. 217, 479-485.
29. Frey, P. A., Hegeman, A. D., and Reed, G. H. (2006) Free radical mechanisms in enzymology. Chem. Rev. 106, 3302-3316.
30. Stubbe, J., and van Der Donk, W. A. (1998) Protein radicals in enzyme catalysis. Chem. Rev. 98, 705-762.
31. Cosper, M. M., Jameson, G. N., Davydov, R., Eidsness, M. K., Hoffman, B. M., Huynh, B. H., and Johnson, M. K. (2002) The [4Fe-4S]2+ cluster in reconstituted biotin synthase binds S-adenosyl- L-methionine. J. Am. Chem. Soc. 124, 14006-14007.
32. Jarrett, J. T. (2003) The generation of 5'-deoxyadenosyl radicals by adenosylmethionine-dependent radical enzymes. Curr. Opin. Chem. Biol. 7, 174-182.
33. Ollagnier-de Choudens, S., Sanakis, Y., Hewiston, K. S., Roach, P., and Munck, E. (2002) Reductive cleavage of S-adenosylmethionine by biotin synthase from Escherichia coli. J. Biol. Chem. 277, 13449-13454.