Biosynthesis of Thiamin Pyrophosphate.

The biosynthesis of thiamin pyrophosphate (TPP) in prokaryotes, as represented by the Escherichia coli and the Bacillus subtilis pathways, is summarized in this review. The thiazole heterocycle is formed by the convergence of three separate pathways. First, the condensation of glyceraldehyde 3-phosphate and pyruvate, catalyzed by 1-deoxy-D-xylulose 5-phosphate synthase (Dxs), gives 1-deoxy-D-xylulose 5-phosphate (DXP). Next, the sulfur carrier protein ThiS-COO- is converted to its carboxyterminal thiocarboxylate in reactions catalyzed by ThiF, ThiI, and NifS (ThiF and IscS in B. subtilis). Finally, tyrosine (glycine in B. subtilis) is converted to dehydroglycine by ThiH (ThiO in B. subtilis). Thiazole synthase (ThiG) catalyzes the complex condensation of ThiS-COSH, dehydroglycine, and DXP to give a thiazole tautomer, which is then aromatized to carboxythiazole phosphate by TenI (B. subtilis). Hydroxymethyl pyrimidine phosphate (HMP-P) is formed by a complicated rearrangement reaction of 5-aminoimidazole ribotide (AIR) catalyzed by ThiC. ThiD then generates hydroxymethyl pyrimidine pyrophosphate. The coupling of the two heterocycles and decarboxylation, catalyzed by thiamin phosphate synthase (ThiE), gives thiamin phosphate. A final phosphorylation, catalyzed by ThiL, completes the biosynthesis of TPP, the biologically active form of the cofactor. This review reviews the current status of mechanistic and structural studies on the enzymes involved in this pathway. The availability of multiple orthologs of the thiamin biosynthetic enzymes has also greatly facilitated structural studies, and most of the thiamin biosynthetic and salvage enzymes have now been structurally characterized.

[1]  C. Kinsland,et al.  Structural studies of thiamin monophosphate kinase in complex with substrates and products. , 2008, Biochemistry.

[2]  T. Begley,et al.  Mutagenesis studies on TenA: a thiamin salvage enzyme from Bacillus subtilis. , 2008, Bioorganic chemistry.

[3]  Tadhg P Begley,et al.  Structural similarities between thiamin-binding protein and thiaminase-I suggest a common ancestor. , 2008, Biochemistry.

[4]  P. Roach,et al.  Thiazole Synthase from Escherichia coli , 2007, Journal of Biological Chemistry.

[5]  G. Mazzucchelli,et al.  Discovery of a natural thiamine adenine nucleotide. , 2007, Nature chemical biology.

[6]  T. Begley,et al.  Thiamin phosphate synthase: the rate of pyrimidine carbocation formation. , 2007, Journal of the American Chemical Society.

[7]  A. Chatterjee,et al.  Biosynthesis of thiamin thiazole in eukaryotes: conversion of NAD to an advanced intermediate. , 2007, Journal of the American Chemical Society.

[8]  Juan Miranda-Ríos,et al.  The THI-box riboswitch, or how RNA binds thiamin pyrophosphate. , 2007, Structure.

[9]  L. Tong,et al.  Crystal Structure of 1-Deoxy-d-xylulose 5-Phosphate Synthase, a Crucial Enzyme for Isoprenoids Biosynthesis* , 2007, Journal of Biological Chemistry.

[10]  F. McLafferty,et al.  Biosynthesis of the Thioquinolobactin Siderophore: an Interesting Variation on Sulfur Transfer , 2007, Journal of bacteriology.

[11]  N. Kunishima,et al.  Purification, crystallization and preliminary crystallographic analysis of the putative thiamine-biosynthesis protein PH1313 from Pyrococcus horikoshii OT3. , 2007, Acta crystallographica. Section F, Structural biology and crystallization communications.

[12]  A. Ferré-D’Amaré,et al.  Crystal structures of the thi-box riboswitch bound to thiamine pyrophosphate analogs reveal adaptive RNA-small molecule recognition. , 2006, Structure.

[13]  A. Chatterjee,et al.  Structural insights into the function of the thiamin biosynthetic enzyme Thi4 from Saccharomyces cerevisiae. , 2006, Biochemistry.

[14]  A. Serganov,et al.  Structural basis for gene regulation by a thiamine pyrophosphate-sensing riboswitch , 2006, Nature.

[15]  A. Chatterjee,et al.  Thiamin biosynthesis in eukaryotes: characterization of the enzyme-bound product of thiazole synthase from Saccharomyces cerevisiae and its implications in thiazole biosynthesis. , 2006, Journal of the American Chemical Society.

[16]  T. Begley.  Cofactor Biosynthesis: An Organic Chemist′s Treasure Trove , 2006 .

[17]  N. Ban,et al.  Structure of the Eukaryotic Thiamine Pyrophosphate Riboswitch with Its Regulatory Ligand , 2006, Science.

[18]  F. McLafferty,et al.  Biosynthesis of thiamin thiazole: determination of the regiochemistry of the S/O acyl shift by using 1,4-dideoxy-D-xylulose-5-phosphate. , 2006, Angewandte Chemie.

[19]  E. Mueller.  Trafficking in persulfides: delivering sulfur in biosynthetic pathways , 2006, Nature chemical biology.

[20]  Tadhg P Begley,et al.  Structure of the Escherichia coli ThiS-ThiF complex, a key component of the sulfur transfer system in thiamin biosynthesis. , 2006, Biochemistry.

[21]  T. Henkin,et al.  From Ribosome to Riboswitch: Control of Gene Expression in Bacteria by RNA Structural Rearrangements , 2006, Critical reviews in biochemistry and molecular biology.

[22]  E. Koonin,et al.  Crystal structure of Bacillus anthracis ThiI, a tRNA-modifying enzyme containing the predicted RNA-binding THUMP domain. , 2005, Journal of molecular biology.

[23]  R. D. Walter,et al.  Vitamin B1 de novo synthesis in the human malaria parasite Plasmodium falciparum depends on external provision of 4-amino-5-hydroxymethyl-2-methylpyrimidine , 2006, Biological chemistry.

[24]  P. Dorrestein,et al.  Reconstitution of a new cysteine biosynthetic pathway in Mycobacterium tuberculosis. , 2005, Journal of the American Chemical Society.

[25]  B. Schulman,et al.  Structural analysis of Escherichia coli ThiF. , 2005, Journal of molecular biology.

[26]  W. Winkler.  Metabolic monitoring by bacterial mRNAs , 2005, Archives of Microbiology.

[27]  T. Begley,et al.  Structural characterization of the regulatory proteins TenA and TenI from Bacillus subtilis and identification of TenA as a thiaminase II. , 2005, Biochemistry.

[28]  A. Joachimiak,et al.  The structure and ligand binding properties of the B. subtilis YkoF gene product, a member of a novel family of thiamin/HMP-binding proteins. , 2004, Journal of molecular biology.

[29]  P. Dorrestein,et al.  The biosynthesis of the thiazole phosphate moiety of thiamin: the sulfur transfer mediated by the sulfur carrier protein ThiS. , 2004, Chemistry & biology.

[30]  R. Mehl,et al.  Biosynthesis of the thiamin pyrimidine: the reconstitution of a remarkable rearrangement reaction. , 2004, Organic & biomolecular chemistry.

[31]  Pieter C Dorrestein,et al.  Thiamin biosynthesis in Bacillus subtilis: structure of the thiazole synthase/sulfur carrier protein complex. , 2004, Biochemistry.

[32]  Olga Vassieva,et al.  Identification of the Two Missing Bacterial Genes Involved in Thiamine Salvage: Thiamine Pyrophosphokinase and Thiamine Kinase , 2004, Journal of bacteriology.

[33]  Giangthy N. Ton,et al.  Substrate Specificity for 4-Thiouridine Modification in Escherichia coli* , 2004, Journal of Biological Chemistry.

[34]  J. Perkins,et al.  Production of thiamin by fermentation , 2004 .

[35]  P. Roach,et al.  Thiamine Biosynthesis in Escherichia coli , 2004, Journal of Biological Chemistry.

[36]  Sean V. Taylor,et al.  The biosynthesis of the thiazole phosphate moiety of thiamin (vitamin B1): the early steps catalyzed by thiazole synthase. , 2004, Journal of the American Chemical Society.

[37]  E. Settembre,et al.  Structural biology of enzymes of the thiamin biosynthesis pathway. , 2003, Current opinion in structural biology.

[38]  R. Wightman,et al.  The THI5 gene family of Saccharomyces cerevisiae: distribution of homologues among the hemiascomycetes and functional redundancy in the aerobic biosynthesis of thiamin from pyridoxine. , 2003, Microbiology.

[39]  Jeffrey E. Barrick,et al.  Riboswitches Control Fundamental Biochemical Pathways in Bacillus subtilis and Other Bacteria , 2003, Cell.

[40]  P. Roach,et al.  Thiamine biosynthesis in Escherichia coli: isolation and initial characterisation of the ThiGH complex , 2003, FEBS letters.

[41]  P. Dorrestein,et al.  Structural and mechanistic studies on ThiO, a glycine oxidase essential for thiamin biosynthesis in Bacillus subtilis. , 2003, Biochemistry.

[42]  M. Gelfand,et al.  Comparative Genomics of Thiamin Biosynthesis in Procaryotes , 2002, The Journal of Biological Chemistry.

[43]  Evgeny Nudler,et al.  Sensing Small Molecules by Nascent RNA A Mechanism to Control Transcription in Bacteria , 2002, Cell.

[44]  Ronald R. Breaker,et al.  Thiamine derivatives bind messenger RNAs directly to regulate bacterial gene expression , 2002, Nature.

[45]  Ali Nahvi,et al.  Genetic control by a metabolite binding mRNA. , 2002, Chemistry & biology.

[46]  C. Lima.  Analysis of the E. coli NifS CsdB protein at 2.0 A reveals the structural basis for perselenide and persulfide intermediate formation. , 2002, Journal of molecular biology.

[47]  Tadhg P Begley,et al.  Crystal structure of 4-amino-5-hydroxymethyl-2-methylpyrimidine phosphate kinase from Salmonella typhimurium at 2.3 A resolution. , 2002, Structure.

[48]  H. Schindelin,et al.  Mechanism of ubiquitin activation revealed by the structure of a bacterial MoeB–MoaD complex , 2001, Nature.

[49]  O. Dym,et al.  Sequence‐structure analysis of FAD‐containing proteins , 2001, Protein science : a publication of the Protein Society.

[50]  S E Ealick,et al.  Structural characterization of the enzyme-substrate, enzyme-intermediate, and enzyme-product complexes of thiamin phosphate synthase. , 2001, Biochemistry.

[51]  J. Miranda-Ríos,et al.  A conserved RNA structure (thi box) is involved in regulation of thiamin biosynthetic gene expression in bacteria , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[52]  L. Nicholson,et al.  Solution structure of ThiS and implications for the evolutionary roots of ubiquitin , 2001, Nature Structural Biology.

[53]  M. Hochstrasser,et al.  Evolution and function of ubiquitin-like protein-conjugation systems , 2000, Nature Cell Biology.

[54]  R. Schinazi,et al.  Human Herpesvirus 8 Open Reading Frame 21 Is a Thymidine and Thymidylate Kinase of Narrow Substrate Specificity That Efficiently Phosphorylates Zidovudine but Not Ganciclovir , 2000, Journal of Virology.

[55]  H. Chiu,et al.  Crystal structure of thiamin phosphate synthase from Bacillus subtilis at 1.25 A resolution. , 1999, Biochemistry.

[56]  D. Downs,et al.  thiBPQ Encodes an ABC Transporter Required for Transport of Thiamine and Thiamine Pyrophosphate inSalmonella typhimurium * , 1998, The Journal of Biological Chemistry.

[57]  B. Sayer,et al.  COMPARATIVE BIOGENETIC ANATOMY OF VITAMIN B1 : A 13C NMR INVESTIGATION OF THE BIOSYNTHESIS OF THIAMIN IN ESCHERICHIA COLI AND IN SACCHAROMYCES CEREVIS IAE , 1998 .

[58]  D. Downs,et al.  Identification and characterization of an operon in Salmonella typhimurium involved in thiamine biosynthesis , 1997, Journal of bacteriology.

[59]  R. White,et al.  Mechanism for the desulfurization of L-cysteine catalyzed by the nifS gene product. , 1994, Biochemistry.

[60]  Y. Kaneko,et al.  Isolation and characterization of a thiamin pyrophosphokinase gene, THI80, from Saccharomyces cerevisiae. , 1993, The Journal of biological chemistry.

[61]  K. Rajagopalan,et al.  The biosynthesis of molybdopterin in Escherichia coli. Purification and characterization of the converting factor. , 1993, The Journal of biological chemistry.

[62]  S. David,et al.  Conversion of 5-aminoimidazole ribotide to the pyrimidine of thiamin in enterobacteria: study of the pathway with specifically labeled samples of riboside. , 1990, Biochimica et biophysica acta.

[63]  S. David,et al.  Biosynthesis of thiamine: origin of the methyl carbon atom of the pyrimidine moiety in Salmonella typhimurium. , 1986, Biochemical and biophysical research communications.

[64]  D. Edmondson,et al.  Evidence for an aldehyde intermediate in the catalytic mechanism of thiamine oxidase. , 1985, Archives of biochemistry and biophysics.

[65]  B. Estramareix,et al.  Biosynthesis of thiamin: 5-aminoimidazole ribotide as the precursor of all the carbon atoms of the pyrimidine moiety , 1984 .

[66]  K. Yamada.  Biosynthesis of thiamin. Incorporation of a two-carbon fragment derived from ribose of 5-aminoimidazole ribotide into the pyrimidine moiety of thiamin , 1982 .