Domain organization in Candida glabrata THI6, a bifunctional enzyme required for thiamin biosynthesis in Eukaryotes

Biochemistry

Volumn 49, Issue 45, 2010, Pages 9922-9934

  Paul, Debamita ^a   Chatterjee, Abhishek ^b   Begley, Tadhg P ^b   Ealick, Steven E ^a  

^a Department of Obstetrics Gynecology   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; ATP-BINDING SITE; BACTERIAL ENZYMES; BIFUNCTIONAL ENZYMES; BIOCHEMICAL STUDIES; BIOSYNTHETIC PATHWAY; C-TERMINAL DOMAINS; CAGE-LIKE STRUCTURES; CANDIDA GLABRATA; GENE PRODUCTS; KINASE DOMAINS; LOOP REGIONS; MONOFUNCTIONAL; N-TERMINAL DOMAINS; PROTEIN-LIGAND COMPLEXES; PROTOMERS; SALVAGE PATHWAY; STRUCTURAL STUDIES; SYNTHASES; TWO DOMAINS;

BACTERIOLOGY; BINDING ENERGY; BIOCHEMISTRY; BIOSYNTHESIS; CARBOXYLIC ACIDS; CATALYSIS; COMPLEXATION; CRYSTAL STRUCTURE; ENZYMES; METHANOL; PHOSPHORYLATION; YEAST;

BINDING SITES;

4 METHYL 5 HYDROXYETHYLTHIAZOLE KINASE; ADENOSINE TRIPHOSPHATE; BACTERIAL ENZYME; FUNGAL ENZYME; PHOSPHATE; PHOSPHOTRANSFERASE; PYROPHOSPHORIC ACID DERIVATIVE; SYNTHETASE; THI6 PROTEIN; THIAMIN PHOSPHATE SYNTHASE; THIAMINE; THIAZOLE; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; BIOCHEMISTRY; BIOSYNTHESIS; CANDIDA GLABRATA; CHEMICAL REACTION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN STRUCTURE;

CANDIDA GLABRATA; CLONING, MOLECULAR; ESCHERICHIA COLI; EUKARYOTIC CELLS; FUNGAL PROTEINS; HYDROLASES; KINETICS; LIGANDS; MODELS, MOLECULAR; RECOMBINANT PROTEINS; THIAMINE; TRANSFERASES;

BACTERIA (MICROORGANISMS); CANDIDA GLABRATA; EUKARYOTA; PROKARYOTA;

EID: 78149459858     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi101008u     Document Type: Article

References (47)

1. Jordan, F. (2003) Current mechanistic understanding of thiamin diphosphate-dependent enzymatic reactions Nat. Prod. Rep. 20, 184-201
2. Monsen, E. R. (1989) The 10th edition of the Recommended Dietary Allowances: what's new in the 1989 RDAs? J. Am. Diet. Assoc. 89, 1748-1752
3. Butterworth, R. F. (2003) Thiamin deficiency and brain disorders Nutr. Res. Rev. 16, 277-284
4. Martin, P. R., Singleton, C. K., and Hiller-Sturmhofel, S. (2003) The role of thiamine deficiency in alcoholic brain disease Alcohol Res. Health 27, 134-142
5. Begley, T. P. and Ealick, S. E. (2010) Thiamin biosynthesis, in Comprehensive Natural Products II (Lew, M. and Hung-Wen, L., Eds.) pp 547 - 559, Elsevier, Oxford.
6. Jurgenson, C. T., Begley, T. P., and Ealick, S. E. (2009) The structural and biochemical foundations of thiamin biosynthesis Annu. Rev. Biochem. 78, 569-603
7. Jurgenson, C. T., Ealick, S. E., and Begley, T. P. (2009) Chapter 3.6.3.7, Biosynthesis of thiamine pyrophosphate, in EcolSal? - ?Escherichia coli and Salmonella: Cellular and Molecular Biology (Böck, A., Curtiss, R., III, Kaper, J. B., Neidhardt, F. C., Nyström, T., Rudd, K. E., and Squires, C. L., Eds.) ASM Press, Washington, DC.
8. Dorrestein, P. C., Zhai, H., McLafferty, F. W., and Begley, T. P. (2004) The biosynthesis of the thiazole phosphate moiety of thiamin: the sulfur transfer mediated by the sulfur carrier protein ThiS Chem. Biol. 11, 1373-1381
9. Kriek, M., Martins, F., Leonardi, R., Fairhurst, S. A., Lowe, D. J., and Roach, P. L. (2007) Thiazole synthase from Escherichia coli: an investigation of the substrates and purified proteins required for activity in vitro J. Biol. Chem. 282, 17413-17423
10. Chatterjee, A., Li, Y., Zhang, Y., Grove, T. L., Lee, M., Krebs, C., Booker, S. J., Begley, T. P., and Ealick, S. E. (2008) Reconstitution of ThiC in thiamine pyrimidine biosynthesis expands the radical SAM superfamily Nat. Chem. Biol. 4, 758-765
11. Martinez-Gomez, N. C. and Downs, D. M. (2008) ThiC is an [Fe-S] cluster protein that requires AdoMet to generate the 4-amino-5-hydroxymethyl-2- methylpyrimidine moiety in thiamin synthesis Biochemistry 47, 9054-9056
12. Cheng, G., Bennett, E. M., Begley, T. P., and Ealick, S. E. (2002) Crystal structure of 4-amino-5-hydroxymethyl-2-methylpyrimidine phosphate kinase from Salmonella typhimurium at 2.3 Å resolution Structure 10, 225-235
13. Chiu, H. J., Reddick, J. J., Begley, T. P., and Ealick, S. E. (1999) Crystal structure of thiamin phosphate synthase from Bacillus subtilis at 1.25 Å resolution Biochemistry 38, 6460-6470
14. Hanes, J. W., Ealick, S. E., and Begley, T. P. (2007) Thiamin phosphate synthase: the rate of pyrimidine carbocation formation J. Am. Chem. Soc. 129, 4860-4861
15. Reddick, J. J., Nicewonger, R., and Begley, T. P. (2001) Mechanistic studies on thiamin phosphate synthase: evidence for a dissociative mechanism Biochemistry 40, 10095-10102
16. McCulloch, K. M., Kinsland, C., Begley, T. P., and Ealick, S. E. (2008) Structural studies of thiamin monophosphate kinase in complex with substrates and products Biochemistry 47, 3810-3821
17. Webb, E. and Downs, D. (1997) Characterization of thiL, encoding thiamin-monophosphate kinase, in Salmonella typhimurium J. Biol. Chem. 272, 15702-15707
18. Campobasso, N., Mathews, I. I., Begley, T. P., and Ealick, S. E. (2000) Crystal structure of 4-methyl-5-β-hydroxyethylthiazole kinase from Bacillus subtilis at 1.5 Å resolution Biochemistry 39, 7868-7877
19. Jurgenson, C. T., Chatterjee, A., Begley, T. P., and Ealick, S. E. (2006) Structural insights into the function of the thiamin biosynthetic enzyme Thi4 from Saccharomyces cerevisiae Biochemistry 45, 11061-11070
20. Chatterjee, A., Jurgenson, C. T., Schroeder, F. C., Ealick, S. E., and Begley, T. P. (2006) Thiamin biosynthesis in eukaryotes: characterization of the enzyme-bound product of thiazole synthase from Saccharomyces cerevisiae and its implications in thiazole biosynthesis J. Am. Chem. Soc. 128, 7158-7159
21. Zeidler, J., Sayer, B. G., and Spenser, I. D. (2003) Biosynthesis of vitamin B1 in yeast. Derivation of the pyrimidine unit from pyridoxine and histidine. Intermediacy of urocanic acid J. Am. Chem. Soc. 125, 13094-13105
22. Haas, A. L., Laun, N. P., and Begley, T. P. (2005) Thi20, a remarkable enzyme from Saccharomyces cerevisiae with dual thiamin biosynthetic and degradation activities Bioorg. Chem. 33, 338-344
23. Kawasaki, Y. (1993) Copurification of hydroxyethylthiazole kinase and thiamine-phosphate pyrophosphorylase of Saccharomyces cerevisiae: characterization of hydroxyethylthiazole kinase as a bifunctional enzyme in the thiamine biosynthetic pathway J. Bacteriol. 175, 5153-5158
24. Nosaka, K., Nishimura, H., Kawasaki, Y., Tsujihara, T., and Iwashima, A. (1994) Isolation and characterization of the THI6 gene encoding a bifunctional thiamin-phosphate pyrophosphorylase/hydroxyethylthiazole kinase from Saccharomyces cerevisiae J. Biol. Chem. 269, 30510-30516
25. Lawhorn, B. G., Mehl, R. A., and Begley, T. P. (2004) Biosynthesis of the thiamin pyrimidine: the reconstitution of a remarkable rearrangement reaction Org. Biomol. Chem. 2, 2538-2546
26. Hazra, A., Chatterjee, A., and Begley, T. P. (2009) Biosynthesis of the thiamin thiazole in Bacillus subtilis: identification of the product of the thiazole synthase-catalyzed reaction J. Am. Chem. Soc. 131, 3225-3229
27. 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
28. Otwinowski, Z. and Minor, W. (1997) Processing of x-ray diffraction data collected in oscillation mode Methods Enzymol. 276, 307-326
29. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. (1990) Basic local alignment search tool J. Mol. Biol. 215, 403-410
30. Matthews, B. W. (1968) Solvent content of protein crystals J. Mol. Biol. 33, 491-497
31. Thompson, J. D., Higgins, D. G., and Gibson, T. J. (1994) Improved sensitivity of profile searches through the use of sequence weights and gap excision Comput. Appl. Biosci. 10, 19-29
32. Brunger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination Acta Crystallogr. D 54, 905-921
33. Collaborative Computational Project Number 4 (1994) The CCP-4 suite: programs for protein crystallography Acta Crystallogr. D 50, 760-763
34. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics Acta Crystallogr., Sect. D: Biol. Crystallogr. 60, 2126-2132
35. Kleywegt, G. J. and Jones, T. A. (1996) xdlMAPMAN and xdlDATAMAN? - ?programs for reformatting, analysis, and manipulation of biomacromolecular electron-density maps and reflection datasets Acta Crystallogr. D 52, 826-828
36. Adams, P. D., Grosse-Kunstleve, R. W., Hung, L. W., Ioerger, T. R., McCoy, A. J., Moriarty, N. W., Read, R. J., Sacchettini, J. C., Sauter, N. K., and Terwilliger, T. C. (2002) PHENIX: building new software for automated crystallographic structure determination Acta Crystallogr. D 58, 1948-1954
37. van Aalten, D. M., Bywater, R., Findlay, J. B., Hendlich, M., Hooft, R. W., and Vriend, G. (1996) PRODRG, a program for generating molecular topologies and unique molecular descriptors from coordinates of small molecules J. Comput.-Aided Mol. Des. 10, 255-262
38. Gouet, P., Courcelle, E., Stuart, D. I., and Metoz, F. (1999) ESPript: analysis of multiple sequence alignments in PostScript Bioinformatics 15, 305-308
39. DeLano, W. L. (2002) The PyMOL Molecular Graphics System, DeLano Scientific, San Carlos, CA.
40. Krissinel, E. and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state J. Mol. Biol. 372, 774-797
41. Peapus, D. H., Chiu, H. J., Campobasso, N., Reddick, J. J., Begley, T. P., and Ealick, S. E. (2001) Structural characterization of the enzyme-substrate, enzyme-intermediate, and enzyme-product complexes of thiamin phosphate synthase Biochemistry 40, 10103-10114
42. Holm, L. and Sander, C. (1993) Protein structure comparison by alignment of distance matrices J. Mol. Biol. 233, 123-138
43. Toms, A. V., Haas, A. L., Park, J. H., Begley, T. P., and Ealick, S. E. (2005) Structural characterization of the regulatory proteins TenA and TenI from Bacillus subtilis and identification of TenA as a thiaminase II Biochemistry 44, 2319-2329
44. Rodionov, D. A., Vitreschak, A. G., Mironov, A. A., and Gelfand, M. S. (2002) Comparative genomics of thiamin biosynthesis in procaryotes. New genes and regulatory mechanisms J. Biol. Chem. 277, 48949-48959
45. Huang, X., Holden, H. M., and Raushel, F. M. (2001) Channeling of substrates and intermediates in enzyme-catalyzed reactions Annu. Rev. Biochem. 70, 149-180
46. Mathews, I. I., Erion, M. D., and Ealick, S. E. (1998) Structure of human adenosine kinase at 1.5 Å resolution Biochemistry 37, 15607-15620
47. Sigrell, J. A., Cameron, A. D., Jones, T. A., and Mowbray, S. L. (1998) Structure of Escherichia coli ribokinase in complex with ribose and dinucleotide determined to 1.8 Å resolution: insights into a new family of kinase structures Structure 6, 183-193