Reconstitution of ThiC in thiamine pyrimidine biosynthesis expands the radical SAM superfamily

Nature Chemical Biology

Volumn 4, Issue 12, 2008, Pages 758-765

  Chatterjee, Abhishek ^a   Li, Yue ^a   Zhang, Yang ^a   Grove, Tyler L ^b   Lee, Michael ^b   Krebs, Carsten ^b   Booker, Squire J ^b   Begley, Tadhg P ^a   Ealick, Steven E ^a  

^a Department of Obstetrics Gynecology   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINO 5 HYDROXYMETHYL 2 METHYLPYRIMIDINE PHOSPHATE; 4 AMINO 5 HYDROXYMETHYL 2 METHYLPYRIMIDINE PHOSPHATE SYNTHASE; PYRIMIDINE; S ADENOSYLMETHIONINE; SYNTHETASE; THIAMINE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BIOSYNTHESIS; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME STRUCTURE; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN MOTIF; SEQUENCE HOMOLOGY;

EID: 56249110190     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.121     Document Type: Article

References (47)

1. Begley, T.P. et al. Thiamin biosynthesis in prokaryotes. Arch. Microbiol. 171, 293-300 (1999).
2. Settembre, E., Begley, T.P. & Ealick, S.E. Structural biology of enzymes of the thiamin biosynthesis pathway. Curr. Opin. Struct. Biol. 13, 739-747 (2003).
3. Chatterjee, A., Jurgenson, C.T., Schroeder, F.C., Ealick, S.E. & Begley, T.P. 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 (2006).
4. Chatterjee, A., Jurgenson, C.T., Schroeder, F.C., Ealick, S.E. & Begley, T.P. Biosynthesis of thiamin thiazole in eukaryotes: conversion of NAD to an advanced intermediate. J. Am. Chem. Soc. 129, 2914-2922 (2007).
5. Jurgenson, C.T., Chatterjee, A., Begley, T.P. & Ealick, S.E. Structural insights into the function of the thiamin biosynthetic enzyme Thi4 from Saccharomyces cerevisiae. Biochemistry 45, 11061-11070 (2006).
6. Kriek, M. et al. Thiazole synthase from Escherichia coli: an investigation of the substates and purified proteins required for activity in vitro. J. Biol. Chem. 282, 17413-17423 (2007).
7. Lawhorn, B.G., Mehl, R.A. & Begley, T.P. Biosynthesis of the thiamin pyrimidine: the reconstitution of a remarkable rearrangement reaction. Org. Biomol. Chem. 2, 2538-2546 (2004).
8. Newell, P.C. & Tucker, R.G. Biosynthesis of the pyrimidine moiety of thiamine. A new route of pyrimidine biosynthesis involving purine intermediates. Biochem. J. 106, 279-287 (1968).
9. Zeidler, J., Sayer, B.G. & Spenser, I.D. 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 (2003).
10. Frey, P.A. & Booker, S.J. Radical mechanisms of S- adenosylmethionine-dependent enzymes. Adv. Protein Chem. 58, 1-45 (2001).
11. Wang, S.C. & Frey, P.A. S-adenosylmethionine as an oxidant: the radical SAM superfamily. Trends Biochem. Sci. 32, 101-110 (2007).
12. Sofia, H.J., Chen, G., Hetzler, B.G., Reyes-Spindola, J.F. & Miller, N.E. 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 (2001).
13. Dougherty, M.J. & Downs, D.M. A connection between iron-sulfur cluster metabolism and the biosynthesis of 4-amino-5-hydroxymethyl-2- methylpyrimidine pyrophosphate in Salmonella enterica. Microbiology 152, 2345-2353 (2006).
14. Raschke, M. et al. Vitamin B1 biosynthesis in plants requires the essential iron sulfur cluster protein, THIC. Proc. Natl. Acad. Sci. USA 104, 19637-19642 (2007).
15. Reddick, J.J., Nicewonger, R. & Begley, T.P. Mechanistic studies on thiamin phosphate synthase: evidence for a dissociative mechanism. Biochemistry 40, 10095-10102 (2001).
16. Park, J.-H., Burns, K., Kinsland, C. & Begley, T.P. Characterization of two kinases involved in thiamine pyrophosphate and pyridoxal phosphate biosynthesis in Bacillus subtilis: 4-amino-5-hydroxymethyl-2- methylpyrimidine kinase and pyridoxal kinase. J. Bacteriol. 186, 1571-1573 (2004).
17. Cicchillo, R.M. et al. Escherichia coli lipoyl synthase binds two distinct [4Fe-4S] clusters per polypeptide. Biochemistry 43, 11770-11781 (2004).
18. Münck, E. in Physical Methods in Bioinorganic Chemistry (ed. Que, L. Jr.) 287-319 (University Science Books, Sausalito, California, USA, 2000).
19. Vallazza, M. et al. First look at RNA in L-configuration. Acta Crystallogr. D Biol. Crystallogr. 60, 1-7 (2004).
20. Layer, G., Moser, J., Heinz, D.W., Jahn, D. & Schubert, W.D. Crystal structure of coproporphyrinogen III oxidase reveals cofactor geometry of radical SAM enzymes. EMBO J. 22, 6214-6224 (2003).
21. Hanzelmann, P. & Schindelin, H. Crystal structure of the S-adenosylmethionine-dependent enzyme MoaA and its implications for molybdenum cofactor deficiency in humans. Proc. Natl. Acad. Sci. USA 101, 12870-12875 (2004).
22. Lepore, B.W., Ruzicka, F.J., Frey, P.A. & Ringe, D. The x-ray crystal structure of lysine-2,3-aminomutase from Clostridium subterminale. Proc. Natl. Acad. Sci. USA 102, 13819-13824 (2005).
23. Reitzer, R. et al. Glutamate mutase from Clostridium cochlearium: the structure of a coenzyme B12-dependent enzyme provides new mechanistic insights. Structure 7, 891-902 (1999).
24. Berkovitch, F. et al. A locking mechanism preventing radical damage in the absence of substrate, as revealed by the x-ray structure of lysine 5,6-aminomutase. Proc. Natl. Acad. Sci. USA 101, 15870-15875 (2004).
25. Evans, J.C. et al. Structures of the N-terminal modules imply large domain motions during catalysis by methionine synthase. Proc. Natl. Acad. Sci. USA 101, 3729-3736 (2004).
26. Mancia, F. et al. How coenzyme B12 radicals are generated: the crystal structure of methylmalonyl-coenzyme A mutase at 2 Å resolution. Structure 4, 339-350 (1996).
27. Svetlitchnaia, T., Svetlitchnyi, V., Meyer, O. & Dobbek, H. Structural insights into methyltransfer reactions of a corrinoid iron-sulfur protein involved in acetyl-CoA synthesis. Proc. Natl. Acad. Sci. USA 103, 14331-14336 (2006).
28. Frey, P.A. Radical mechanisms of enzymatic catalysis. Annu. Rev. Biochem. 70, 121-148 (2001).
29. Berkovitch, F., Nicolet, Y., Wan, J.T., Jarrett, J.T. & Drennan, C.L. Crystal structure of biotin synthase, an S-adenosylmethionine-dependent radical enzyme. Science 303, 76-79 (2004).
30. Matthews, B.W. Solvent content of protein crystals. J. Mol. Biol. 33, 491-497 (1968).
31. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997).
32. Schneider, T.R. & Sheldrick, G.M. Substructure solution with SHELXD. Acta Crystallogr. D Biol. Crystallogr. 58, 1772-1779 (2002).
33. Uson, I. & Sheldrick, G.M. Advances in direct methods for protein crystallography. Curr. Opin. Struct. Biol. 9, 643-648 (1999).
34. Otwinowski, Z. in CCP4 Proceedings (eds. Wolf, W., Evans, P.R. & Leslie, A.G.W.) 80-88 (SERC Daresbury Laboratory, Warrington, UK, 1991).
35. Terwilliger, T.C. Maximum-likelihood density modification. Acta Crystallogr. D Biol. Crystallogr. 56, 965-972 (2000).
36. Jones, T.A., Zou, J.-Y., Cowan, S.W. & Kjeldgaard, M. Improved methods for the building of protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47, 110-119 (1991).
37. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004).
38. Brünger, A.T. et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54, 905-921 (1998).
39. Laskowski, R.A., Moss, D.S. & Thornton, J.M. Main-chain bond lengths and bond angles in protein structures. J. Mol. Biol. 231, 1049-1067 (1993).
40. Krissinel, E. & Henrick, K. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr. D Biol. Crystallogr. 60, 2256-2268 (2004).
41. Kabsch, W., Kabsch, H. & Eisenberg, D. Packing in a new crystalline form of glutamine synthetase from Escherichia coli. J. Mol. Biol. 100, 283-291 (1976).
42. Gouet, P., Courcelle, E., Stuart, D.I. & Metoz, F. ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15, 305-308 (1999).
43. Jones, S. & Thornton, J.M. Protein-protein interactions: a review of protein dimer structures. Prog. Biophys. Mol. Biol. 63, 31-65 (1995).
44. Jones, S. & Thornton, J.M. Principles of protein-protein interactions. Proc. Natl. Acad. Sci. USA 93, 13-20 (1996).
45. DeLano, W.L. The PyMOL Molecular Graphics System (DeLano Scientific, San Carlos, California, USA, 2002).
46. Potterton, E., McNicholas, S., Krissinel, E., Cowtan, K. & Noble, M. The CCP4 molecular-graphics project. Acta Crystallogr. D Biol. Crystallogr. 58, 1955-1957 (2002).
47. Martinez-Gomez, N.C. & Downs, D.M. 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 (2008).