Characterization of quinolinate synthases from Escherichia coli, Mycobacterium tuberculosis, and Pyrococcus horikoshii indicates that [4Fe-4S] clusters are common cofactors throughout this class of enzymes

Biochemistry

Volumn 47, Issue 41, 2008, Pages 10999-11012

  Saunders, Allison H ^a   Griffiths, Amy E ^a   Lee, Kyung Hoon ^a   Cicchillo, Robert M ^a,b   Tu, Loretta ^a   Stromberg, Jeffrey A ^a   Krebs, Carsten ^a   Booker, Squire J ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACIDS; AMIDES; BIOCHEMICAL ENGINEERING; BIOCHEMISTRY; BIOSYNTHESIS; ELECTRON SPIN RESONANCE SPECTROSCOPY; ENZYMES; ESCHERICHIA COLI; MOLYBDENUM; OXYGEN; PARAMAGNETIC RESONANCE; PARAMAGNETISM; PROTEINS; PYRIDINE; RATE CONSTANTS; SULFUR;

ACID PRODUCTION; ANALYTICAL METHODS; ASPARTATE; COFACTORS; DIHYDROXYACETONE PHOSPHATES; ELECTRON PARAMAGNETIC RESONANCE; HYPERBARIC OXYGEN; IRON-SULFUR CLUSTERS; MYCOBACTERIUM TUBERCULOSIS; NICOTINAMIDE ADENINE DINUCLEOTIDE; PRIMARY STRUCTURES; PYROCOCCUS HORIKOSHII; QUINOLINATE; QUINOLINATE SYNTHASE; SYNTHASES; X-RAY STRUCTURES;

CONDENSATION REACTIONS;

QUINOLINATE SYNTHASE; SYNTHETASE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BIOINFORMATICS; ENZYME ANALYSIS; ENZYME STRUCTURE; ESCHERICHIA COLI; MOLECULAR CLONING; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN MOTIF; PYROCOCCUS HORIKOSHII;

CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CLONING, MOLECULAR; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, ENZYMOLOGIC; MULTIENZYME COMPLEXES; MYCOBACTERIUM TUBERCULOSIS; PYROCOCCUS HORIKOSHII; SPECTROPHOTOMETRY, ULTRAVIOLET;

ESCHERICHIA COLI; MYCOBACTERIUM TUBERCULOSIS; PROKARYOTA; PYROCOCCUS HORIKOSHII;

EID: 53849132731     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi801268f     Document Type: Article

References (43)

1. Frey, P. A., and Hegeman, A. D. (2007) Enzymatic Reaction Mechanisms, Oxford University Press, Oxford.
2. + metabolism in health and disease. Trends Biochem. Sci. 32, 12-19.
3. Pollak, N., Dölle, C., and Ziegler, M. (2007) The power to reduce: pyridine nucleotides-small molecules with a multitude of functions. Biochem. J. 402, 205-218.
4. Kessler, D., Rétey, J., and Schulz, G. E. (2004) Structure and action of urocanase. J. Mol. Biol. 342, 183-194.
5. Begley, T. P., Chatterjee, A., Hanes, J. W., Hazra, A., and Ealick, S. E. (2008) Cofactor biosynthesis - still yielding fascinating new biological chemistry. Curr. Opin. Chem. Biol. 12, 118-125.
6. Foster, J. W., and Moat, A. G. (1980) Nicotinamide adenine dinucleotide biosynthesis and pyridine nucleotide cycle metabolism in microbial systems. Microbiol. Rev. 44, 83-105.
7. Chandler, J. L., and Gholson, R. K. (1972) Studies on the de novo biosynthesis of NAD in Escherichia coli. Anal. Biochem. 48, 529-535.
8. Mortarino, M., Negri, A., Tedeschi, G., Simonie, T., Duga, S., Gassen, H. G., and Ronchi, S. (1996) L-Aspartate oxidase from Escherichia coli. I. Characterization of coenzyme binding and product inhibition. Eur. J. Biochem. 239, 418-426.
9. 4 dicarboxylic acids and identification of a novel L-aspartate:fumarate oxidoreductase activity. Eur. J. Biochem. 239, 427-433.
10. Nasu, S., Wicks, F. D., and Gholson, R. K. (1982) L-Aspartate oxidase, a newly discovered enzyme of Escherichia coli, is the B protein of quinolinate synthetase. J. Biol. Chem. 257, 626-632.
11. Nasu, S., and Gholson, R. K. (1981) Replacement of the B protein requirement of the E. coli quinolinate synthetase system by chemically-generated iminoaspartate. Biochem. Biophys. Res. Commun. 101, 533-539.
12. Yasunobu, K. T. , and Tanaka, M. (1973) The types, distribution in nature, structure-function, and evolutionary data of the iron-sulfur proteins, in Iron-Sulfur Proteins Vol. II (Lovenberg, W., Ed.) Academic Press, New York.
13. + biosynthesis. Arch. Biochem. Biophys. 284, 106-111.
14. Cicchillo, R. M., Tu, L., Stromberg, J. A., Hoffart, L. M., Krebs, C., and Booker, S. J. (2005) Escherichia coli quinolinate synthetase does indeed harbor a [4Fe 194 4S] cluster. J. Am. Chem. Soc. 127, 7310-7311.
15. Ollagnier-de Choudens, S., Loiseau, L., Sanakis, Y., Banas, F., and Fontecave, M. (2005) Quinolinate synthetase, an iron-sulfur enzyme in NAD biosynthesis. FEBS Lett. 579, 3737-3743.
16. Flint, D. H., and Allen, R. M. (1996) Iron-sulfur proteins with nonredox functions. Chem. Rev. 96, 2315-2334.
17. Beinert, H., Kennedy, M. C., and Stout, C. D. (1996) Aconitase as iron-sulfur protein, enzyme, and iron-regulatory protein. Chem. Rev. 96, 2335-2373.
18. Emptage, M. H., Kent, T. A., Kennedy, M. C., Beinert, H., and Mtinck, E. (1983) Mössbauer and EPR studies of activated aconitase: Development of a localized valence state at a subsite of the [4Fe-4S] cluster on binding of citrate. Proc. Natl. Acad. Sci. U.S.A. 80, 4674-4678.
19. 13C electron-nuclear double resonance spectroscopy. Proc. Natl. Acad. Sci. U.S.A. 84, 8854-8858.
20. Kent, T. A., Emptage, M. H., Merkle, H., Kennedy, M. C., Beinert, H., and Münck, E. (1985) Mössbauer studies of aconitase. Substrate and inhibitor binding, reaction intermediates, and hyperfine interactions of reduced 3Fe and 4Fe clusters. J. Biol. Chem. 260, 6871-6881.
21. Lauble, H., Kennedy, M. C., Beinert, H., and Stout, C. D. (1992) Crystal structures of aconitase with isocitrate and nitroisocitrate bound. Biochemistry 31, 2735-2748.
22. Sakuraba, H., Tsuge, H., Yoneda, K., Katunuma, N., and Ohshima, T. (2005) Crystal structure of the NAD biosynthetic enzyme quinolinate synthase. J. Biol. Chem. 280, 26645-26648.
23. Beinert, H. (1978) Micro methods for the quantitative determination of iron and copper in biological material. Methods Enzymol. 54, 435-445.
24. Beinert, H. (1983) Semi-micro methods for analysis of labile sulfide and of labile sulfide plus sulfane sulfur in unusually stable iron-sulfur proteins. Anal. Biochem. 131, 373-378.
25. Kennedy, M. C., Kent, T. A., Emptage, M., Merkle, H., Beinert, H., and Münck, E. (1984) Evidence for the formation of a linear [3Fe-4S] cluster in partially unfolded aconitase. J. Biol. Chem. 259, 14463-14471.
26. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd ed., Vol. 3, Cold Spring Harbor Laboratory Press, Plainview, NY.
27. Cicchillo, R. M., Lee, K.-H., Baleanu-Gogonea, C., Nesbitt, N. M., Krebs, C., and Booker, S. J. (2004) Escherichia coli lipoyl synthase binds two distinct [4Fe 194 4S] clusters per polypeptide. Biochemistry 43, 11770-11781.
28. Ramamurthy, V., Swann, S. L., Paulson, J. L., Spedaliere, C. J., and Mueller, E. G. (1999) Critical aspartic acid residues in pseudouridine synthases. J. Biol. Chem. 274, 22225-22230.
29. Cicchillo, R. M., Iwig, D. F., Jones, A. D., Nesbitt, N. M., Baleanu-Gogonea, C., Souder, M. G., Tu, L., and Booker, S. J. (2004) Lipoyl synthase requires two equivalents of S-adenosyl-L-methionine to synthesize one equivalent of lipoic acid. Biochemistry 43, 6378-6386.
30. Parkin, S. E., Chen, S., Ley, B. A., Mangravite, L., Edmondson, D. E., Huynh, B. H., and Bollinger, J. M., Jr. (1998) Electron injection through a specific pathway determines the outcome of oxygen activation at the diiron cluster in the F208Y mutant of Escherichia coli ribonucleotide reductase Protein R2. Biochemistry 37, 1124-1130.
31. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
32. 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] of pyruvate formate-lyase activating enzyme: a Mössbauer spectroscopic study. J. Am. Chem. Soc. 124, 912-913.
33. Gerdes, S. Y., Scholle, M. D., D'Souza, M., Bernal, A., Baev, M. V., Fanell, M., Kurnasov, O. V., Daugherty, M. D., Mseeh, F., Polanuyer, B. M., Campbell, J. W., Anantha, S., Shatalin, K. Y., Chowdhury, S. A., Fonstein, M. Y., and Osterman, A. L. (2002) From genetic footprinting to antimicrobial drug targets: examples in cofactor biosynthetic pathways. J. Bacteriol. 184, 4555-4572.
34. Sassetti, C. M., Boyd, D. H., and Rubin, E. J. (2003) Genes required for mycobacterial growth defined by high density mutagenesis. Mol. Microbiol. 48, 77-84.
35. Lauhon, C. T., and Kambampati, R. (2000) The iscS gene in Escherichia coli is required for the biosynthesis of 4-thiouridine, thiamin, and NAD. J. Biol. Chem. 275, 20096-20103.
36. Zheng, L., White, R. H., Cash, V. L., and Dean, D. R. (1994) Mechanism for the desulfurization of L-cysteine catalyzed by the nifS gene product. Biochemistry 33, 4714-4720.
37. Mueller, E. G. (2006) Trafficking in persulfides: delivering sulfur in biosynthetic pathways. Nat. Chem. Biol. 2, 185-194.
38. Ceciliani, F., Camori, T., Ronchi, S., Tedeschi, G., Mortarino, M., and Galizzi, A. (2000) Cloning, overexpression, and purification of Escherichia coli quinolinate synthetase. Protein Expression Purif. 18, 64-70.
39. The_UniProt_Consortium. (2007) The Universal Protein Resource (UniProt). Nucleic Acids Res. 35, D193-D197.
40. Murthy U. M., N., Ollagnier-de-Choudens, S., Sanakis, Y., Abdel-Ghany, S. E., Rousset, C., Ye, H., Fontecave, M., Pilon-Smits, E. A. H., and Pilon, M. (2007) Characterization of Arabidopsis thaliana SufE2 and SufE3 Functions in chloroplast iron-sulfur cluster assembly and NAD synthesis. J. Biol. Chem. 282, 18254-18264.
41. Tamarit, J., Gerez, G., Meier, C., Mulliez, E., Trautwein, A. X., and Fontecave, M. (2000) The activating component of the anaerobic ribonucleotide reductase from Escherichia coli: An iron-sulfur center with only three cysteines. J. Biol. Chem. 275, 15669-15675.
42. Saunders, A. H., and Booker, S. J. (2008) Regulation of the activity of Escherichia coli quinolinate synthase by reversible disulfide-bond formation. Biochemistry 47, 8467-8469.
43. Boshoff, H. I. M., Xu, X., Tahlan, K., Dowd, C. S., Pefhe, K., Camacho, L. R., Park, T.-H., Yun, C.-S., Schnappinger, D., Ehrt, S., Williams, K. J., and Barry III, C. E. (2008) Biosynthesis and recylcing of nicotinamide cofactorsin Mycobacterium tuberculosis: an essential role for NAD in nonreplicating bacilli. J. Biol. Chem. 283, 19329-19341.