Characterization of the Cofactor Composition of Escherichia coli Biotin Synthase

Biochemistry

Volumn 43, Issue 7, 2004, Pages 2007-2021

  Cosper, Michele Mader ^a   Jameson, Guy N L ^b   Hernández, Heather L ^a   Krebs, Carsten ^b,c   Huynh, Boi Hanh ^b   Johnson, Michael K ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b EMORY UNIVERSITY   (United States)

^c PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABSORPTION SPECTROSCOPY; BIOASSAY; BIODEGRADATION; BIOSYNTHESIS; CATALYSIS; CELLS; ENZYME KINETICS; ENZYMES; ESCHERICHIA COLI; RAMAN SPECTROSCOPY; ULTRAVIOLET RADIATION;

AEROBIC GROWTH; CLUSTER TRANSFORMATIONS;

BIOCHEMISTRY;

BIOTIN; BIOTIN SYNTHASE; CYSTATHIONINE GAMMA LYASE; IRON; OXYGEN; PYRIDOXAL 5 PHOSPHATE; S ADENOSYLMETHIONINE; SULFUR;

ANAEROBIC METABOLISM; ARTICLE; BIOSYNTHESIS; CELL GROWTH; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME ASSAY; ENZYME BINDING; ESCHERICHIA COLI; IN VITRO STUDY; IN VIVO STUDY; MOSSBAUER SPECTROSCOPY; NONHUMAN; PRIORITY JOURNAL; RAMAN SPECTROMETRY; SCIENTIFIC LITERATURE; ULTRAVIOLET SPECTROSCOPY;

ANAEROBIOSIS; BINDING SITES; BIOTIN; CARBON-SULFUR LYASES; COENZYMES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; IRON-SULFUR PROTEINS; LYASES; PYRIDOXAL PHOSPHATE; RECOMBINANT PROTEINS; S-ADENOSYLMETHIONINE; SPECTROPHOTOMETRY, ULTRAVIOLET; SPECTROSCOPY, MOSSBAUER; SPECTRUM ANALYSIS, RAMAN; SULFURTRANSFERASES;

ESCHERICHIA COLI; NEGIBACTERIA;

EID: 1242285458     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0356653     Document Type: Article

References (53)

1. Marquet, A. (2001) Enzymology of carbon-sulfur bond formation, Curr. Opin. Chem. Biol. 5, 541-549.
2. Fontecave, M., Ollagnier-de-Choudens, S., and Mulliez, E. (2003) Biological radical sulfur insertion reactions, Chem. Rev. 103, 2149-2166.
3. Frey, P. A., and Magnusson, O. Th. (2003) S-Adenosylmethionine: A wolf in sheep's clothing, or a rich man's adenosylcobalamin? Chem. Rev. 103, 2129-2148.
4. Jarrett, J. T. (2003) The generation of 5′-deoxyadenosyl radicals by adenosylmethioine-dependent radical enzymes, Curr. Opin. Chem. Biol. 7, 174-182.
5. 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.
6. Ollagnier-de-Choudens, S., Sanakis, Y., Hewitson, K. S., Roach, P. L., Münck, E., and Fontecave, M. (2002) Reductive cleavage of S-adenosylmethionine by biotin synthase from Escherichia coli, J. Biol. Chem. 277, 13449-13454.
7. 2+ cluster in reconstituted biotin synthase binds S-adenosylmethionine, J. Am. Chem. Soc. 124, 14006-14007.
8. 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.
9. Escalettes, 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.
10. 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.
11. Ollagnier-de-Choudens, S., Mulliez, E., and Fontecave, M. (2002) The PLP-dependent biotin synthase from Escherichia coli: mechanistic studies, FEBS Lett. 532, 465-468.
12. 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.
13. 2+ cluster of Escherichia coli biotin synthase during reaction: a Mössbauer characterization, Biochemistry 42, 8791-8798.
14. Ollagnier-de-Choudens, S., Mulliez, E., Hewitson, K. S., and Fontecave, M. (2002) Biotin synthase is a pyridoxal phosphate-dependent cysteine desulfurase, Biochemistry 41, 9145-9152.
15. 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.
16. Picciocchi, A., Douce, R., and Alban, C. (2001) Biochemical characterization of the Arabidopsis biotin synthase reaction. The importance of mitochondria in biotin synthesis. Plant Physiol. 127, 1224-1233.
17. 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.
18. Ollagnier-de-Choudens, S., Sanakis, Y., Hewitson, K. S., Roach, P., Baldwin, J. E., Münck, E., and Fontecave, M. (2000) Iron-sulfur center of biotin synthase and lipoate synthase, Biochemistry 39, 4165-4173.
19. 2+ clusters, FEBS Lett. 459, 411-414.
20. Hewitson, K. S., Baldwin, J. E., Shaw, N. M., and Roach, P. L. (2000) Mutagenesis of the proposed iron-sulfur cluster binding ligands in Escherichia coli biotin synthase, FEBS Lett. 466, 372-376.
21. Hewitson, K. S., Ollagnier-de-Choudens, S., Sanakis, Y., Shaw, N. M., Baldwin, J. E., Münck, E., Roach, P. L., and Fontecave, M. (2002) The iron-sulfur center of biotin synthase: site-directed mutants, J. Biol. Inorg. Chem. 7, 83-93.
22. Zheng, L., White, R. H., Cash, V. L., Jack, R. F., and Dean, D. R. (1993) Cysteine desulfurase activity indicates a role for NIFS in metallocluster biosynthesis, Proc. Natl. Acad. Sci. U.S.A. 90, 2754-2758.
23. Mihara, H., and Esaki, N. (2002) Bacterial cysteine desulfurases: their function and mechanisms, Appl. Microbiol. Biotechnol. 60, 12-23.
24. 2+ protein in whole cells, FEBS Lett. 529, 332-336.
25. Benda, R., Tse Sum Bui, B., Schünemann, V., Florentin, D., Marquet, A., and Trautwein, A. X. (2002) Iron-sulfur clusters of biotin synthase in vivo: a Mössbauer study, Biochemistry 41, 15000-15006.
26. Tabor, S. (1990) Expression using the T7 RNA polymerase/promotor system, in Current Protocols in Molecular Biology (Ausubel, F. A., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A., and Sthuhl, K., Eds.) pp 16.2.1-16.2.11. Greene Publishing and Wiley-Interscience, New York.
27. Harwood, C. R., and Cutting, S. M. (1990) Modern Microbiological Methods: Molecular Biology Methods for Bacillus, Wiley and Sons, Chichester, U.K.
28. Yoshida, A., and Freese, E. (1970) L-Alanine dehydrogenase (Bacillus subtilis), Methods Enzymol. 17a, 176-181.
29. Siegel, L. M. (1965) A direct microdetermination for sulfide, Anal. Biochem. 11, 126-132.
30. Fish, W. W. (1988) Rapid colorimetric micromethod for the quantitation of complexed iron in biological samples, Methods Enzymol. 158, 357-364.
31. Bates, C. J., Pentieva, K. D., Matthews, N., and Macdonald, A. (1999) A simple, sensitive and reproducible assay for pyridoxal 5′-phosphate and 4-pyridoxic acid in human plasma, Clin. Chim. Acta 280, 101-111.
32. Drozdzewski, P. M., and Johnson, M. K. (1988) A simple anaerobic cell for low-temperature Raman spectroscopy, Appl. Spectrosc. 42, 1575-1577.
33. Ravi, N., Bollinger, J. M., Huynh, B. H., Edmondson, D. E., and Stubbe, J. (1994) Mechanism of assembly of the tyrosyl radical-diiron(III) cofactor of E. coli ribonucleotide reductase. I. Mössbauer characterization of the diferric radical precusor. J. Am. Chem. Soc. 116, 8007-8014.
34. Tanaka, M., Izumi, Y., and Yamada, H. (1987) Biotin assay using lyophilized and glycerol-suspended cultures, J. Microbiol. Methods 6, 237-246.
35. Tse Sum Bui, B., and Marquet, A. (1997) Biotin synthase of Bacillus sphaericus, Methods Enzymol. 279, 357-362.
36. Tse Sum Bui, B., Florentin, D., Fournier, F., Ploux, O., Méjean, A., and Marquet, A. (1998) Biotin synthase mechanism: on the origin of sulphur, FEBS Lett. 440, 226-230.
37. Spiro, T. G., Hare, J., Yachandra, V., Gewirth, A., Johnson, M. K., and Remsen, E. (1982) Resonance Raman spectra of iron-sulfur proteins and analogues, in Iron-sulfur proteins (Spiro, T. G., Ed.) pp 407-423, Wiley-Interscience, New York.
38. Spiro, T. G., Czernuszewicz, R. S., and Han, S. (1988) Iron-sulfur proteins and analogue complexes, in Resonance Raman spectra of heme and metalloproteins (Spiro, T. G., Ed.) pp 523-554, John Wiley & Sons, New York.
39. Fu, W., Morgan, T. V., Mortenson, L. E., and Johnson, M. K. (1991) Resonance Raman studies of the [4Fe-4S] to [2Fe-2S] cluster conversion in the iron protein of nitrogenase, FEBS Lett. 284, 165-168.
40. Fu, W., Drozdzewski, P. M., Adams, M. W. W., Morgan, T. V., Mortenson, L. E., LeGall, J., Peck, H. D., Jr., DerVartanian, D. V., and Johnson, M. K. (1993) Resonance Raman studies of iron-hydrogenases, Biochemistry 32, 4813-4819.
41. Tong, W.-H., Jameson, G. N. L., Huynh, B. H., and Rouault, T. A. (2003) Subcellular compartmentalization of human Nfu, an iron-sulfur cluster scaffold protein and its ability to assemble a [4Fe-4S] cluster, Proc. Natl. Acad. Sci. U.S.A. 100, 9762-9767.
42. Trautwein, A. X., Bominaar, E. L., and Winkler, H. (1991) Iron-containing proteins and related analogues. Complementary Mössbauer, EPR and magnetic susceptibility studies. Struct. Bonding 78, 1-95.
43. Krebs, C., Agar, J. N., Smith, A. D., Frazzon, J., Dean, D. R., Huynh, B. H., and Johnson, M. K. (2001) IscA, an alternative scaffold for Fe-S cluster biosynthesis, Biochemistry 40, 14069-14080.
44. Johnson, M. K., Staples, C. R., Duin, E. C., Lafferty, M. E., and Duderstadt, R. E. (1998) Novel roles for Fe-S cluster in stabilizing or generating radical intermediates, Pure Appl. Chem. 70, 939-946.
45. Ollagnier, S., Meier, C., Mulliez, E., Gaillard, J., Schuenemann, V., Trautwein, A. X., Mattioli, T., Lutz, M., and Fontecave, M. (1999) Assembly of 2Fe-2S and 4Fe-4S clusters in the anaerobic ribonucleotide reductase from Escherichia coli, J. Am. Chem. Soc. 121, 6344-6350.
46. Broderick, J. B., Duderstadt, R. E., Fernandez, D. C., Wojtuszewski, K., Henshaw, T. F., and Johnson, M. K. (1997) Pyruvate formate-lyase activating enzyme is an iron-sulfur protein, J. Am. Chem. Soc. 119, 7396-7397.
47. Pierrel, F., Hernandez, H., Johnson, M. K., Fontecave, M., and Atta, M. (2003) MiaB protein from Thermotoga maritime: characterization of an extremely thermophilic tRNA-methylthiotransferase, J. Biol. Chem. 278, 29515-29524.
48. 2+ cluster binding sites in biotin synthase from Escherichia coli, J. Am. Chem. Soc. 124, 9050-9051.
49. Flint, D. H. (1996) Escherichia coli contains a protein that is homologous in function and N-terminal sequence to the protein encoded by the NIFS gene of Azotobacter vinelandii and that can participate in the synthesis of the Fe-S cluster of dihyroxy-acid dehydratase, J. Biol. Chem. 271, 16068-16074.
50. Krebs, C., Broderick, W. E., Henshaw, T. F., Broderick, J. B., and Huynh, B. H. (2002) Coordination of adenosylmethionine to a unique iron site of the [4Fe-4S] cluster of pyruvate formate-lyase activating enzyme: a Mössbauer spectroscopic study, J. Am. Chem. Soc. 124, 912-913.
51. + cluster in pyruvate formate-lyase activating enzyme, J. Am. Chem. Soc. 124, 3143-3151.
52. Walsby, C. J., Ortillo, D., Broderick, W. E., Broderick, J. B., and Hoffman, B. M. (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, 11270-11271.
53. Gibson, K. J., Pelletier, D. A., and Turner, I. M., Sr. (1999) Transfer of sulfur to biotin from biotin synthase (bioB protein), Biochem. Biophys. Res. Commun. 254, 632-635.