Catalysing new reactions during evolution: Economy of residues and mechanism

Journal of Molecular Biology

Volumn 331, Issue 4, 2003, Pages 829-860

  Bartlett, Gail J ^a,b   Borkakoti, Neera ^c,e   Thornton, Janet M ^a,b,d  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^c ROCHE PRODUCTS LTD   (United Kingdom)

^d UNIVERSITY OF LONDON   (United Kingdom)

^e MEDIVIR AB   (Sweden)

Author keywords

Active site; Catalytic mechanism; Enzyme evolution; Enzyme reaction

Indexed keywords

AMINODEOXYCHORISMATE LYASE; CHAPERONE; CYCLOMALTODEXTRIN GLUCANOTRANSFERASE; DEHYDROQUINATE SYNTHASE; DETHIOBIOTIN SYNTHASE; DEXTRO AMINO ACID AMINOTRANSFERASE; DNA 3 METHYLADENINE GLYCOSYLASE II; ENDONUCLEASE III; ENDONUCLEASE IV; ENZYME; FUCULOSEPHOSPHATE ALDOLASE; GLYCEROL DEHYDROGENASE; GUANOSINE DIPHOSPHATE MANNOSE 4,6 DEHYDRATASE; HYDROLASE; ISOCITRATE LYASE; METAL ION; OLIGO 1,6 GLUCOSIDASE; OROTIDINE 5' PHOSPHATE DECARBOXYLASE; PHOSPHOENOLPYRUVATE MUTASE; PHOSPHOLIPASE A2; PHOSPHOLIPASE A2 INHIBITOR; PROTEIN DISULFIDE ISOMERASE; RIBULOSE 5 PHOSPHATE EPIMERASE; RIBULOSE PHOSPHATE 3 EPIMERASE; SUPEROXIDE DISMUTASE; SUPEROXIDE DISMUTASE COPPER CHAPERONE; THIOREDOXIN; UNCLASSIFIED DRUG; URIDINE DIPHOSPHATE GLUCOSE 4 EPIMERASE; URIDINE DIPHOSPHATE HEXOSE 1 PHOSPHATE URIDYLYLTRANFERASE; XYLOSE ISOMERASE;

ARTICLE; CATALYSIS; ENZYME ACTIVITY; ENZYME STRUCTURE; EVOLUTION; EVOLUTIONARY HOMOLOGY; PRIORITY JOURNAL; PROTEIN FUNCTION; STRUCTURE ANALYSIS;

EID: 0041624350     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(03)00734-4     Document Type: Article

References (101)

1. Babbitt P., Gerlt J. Understanding enzyme superfamilies. Chemistry as the fundamental determinant in the evolution of new catalytic activities. J. Biol. Chem. 272:1997;30591-30594.
2. Todd A., Orengo C., Thornton J. Evolution of function in protein superfamilies, from a structural perspective. J. Mol. Biol. 307:2001;1113-1143.
3. Anantharaman V., Aravind L., Koonin E. Emergence of diverse bio-chemical activities in evolutionarily conserved structural scaffolds of proteins. Curr. Opin. Chem. Biol. 7:2003;12-20.
4. Petsko G.A., Kenyon G.L., Gerlt J.A., Ringe D., Kozarich J.W. On the origin of enzymatic species. Trends Biochem. Sci. 18:1993;372-376.
5. Gerlt J., Babbitt P. Mechanistically diverse enzyme superfamilies: the importance of chemistry in the evolution of catalysis. Curr. Opin. Chem. Biol. 2:1998;607-612.
6. Gerlt J., Babbitt P. Divergent evolution of enzymatic function: mechanistically diverse superfamilies and functionally distinct suprafamilies. Annu. Rev. Biochem. 70:2001;209-246.
7. Babbitt P.C., Hasson M.S., Wedekind J.E., Palmer D.R., Barrett W.C., Reed G.H., et al. The enolase superfamily: a general strategy for enzyme-catalyzed abstraction of the alpha-protons of carboxylic acids. Biochemistry. 35:1996;16489-16501.
8. Lee M., Lenman M., Banas A., Bafor M., Singh S., Schweizer M., et al. Identification of non-heme diiron proteins that catalyze triple bond and epoxy group formation. Science. 280:1998;915-918.
9. Aravind L., Galperin M., Koonin E. The catalytic domain of the P-type ATPase has the haloacid dehalogenase fold. Trends Biochem. Sci. 23:1998;127-129.
10. Schofield C., Zhang Z. Structural and mechanistic studies on 2-oxoglutarate-dependent oxygenases and related enzymes. Curr. Opin. Struct. Biol. 9:1999;722-731.
11. Murzin A.G. Can homologous proteins evolve different enzymatic activities? Trends Biochem. Sci. 18:1993;403-405.
12. Todd A.E., Orengo C.A., Thornton J.M. Plasticity of enzyme active-sites. Trends Biochem. Sci. 27:2002;419-426.
13. Webb, E. (1992). Enzyme Nomenclature. Recommendations of the Nomenclature Committee of the International Union of Biochemistry and Molecular Biology. Academic Press, New York.
14. Bartlett G.J., Porter C.T., Borkakoti N., Thornton J.M. Analysis of catalytic residues in enzyme active-sites. J. Mol. Biol. 324:2002;105-121.
15. Altschul S., Madden T., Schaffer A., Zhang J., Zhang Z., Miller W., Lipman D. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl. Acids Res. 25:1997;3389-3402.
16. Berman H.M., Battistuz T., Bhat T.N., Bluhm W.F., Bourne P.E., Burkhardt K., et al. The Protein Data Bank. Acta Crystallog. sect. D. 58:2002;899-907.
17. Krissinel, E. & Henrick, K. (2003). Secondary structure matching (SSM), a tool for protein structure comparison in 3D. Proteins: Struct. Funct. Genet. In the press.
18. Kemmink J., Darby N.J., Dijkstra K., Nilges M., Creighton T.E. Structure determination of the n-terminal thioredoxin-like domain of protein disulfide isomerase using multidimensional heteronuclear 13C/15N NMR spectroscopy. Biochemistry. 35:1996;7684-7691.
19. Westerlund B., Saarinen M., Person B., Ramaswamy S., Eaker D., Eklund H. Crystallographic investigation of the dependence of calcium and phosphate ions for notexin. FEBS Letters. 403:1997;51-56.
20. Scott D.L., Sigler P.B. Structure and catalytic mechanism of secretory phospholipases A2. Advan. Protein Chem. 45:1994;53-88.
21. Hart P.J., Balbirnie M.M., Ogihara N.L., Nersissian A.M., Weiss M.S., Valentine J.S., Eisenberg D. A structure-based mechanism for copper-zinc superoxide dismutase. Biochemistry. 38:1999;2167-2178.
22. Holmgren A. Thioredoxin structure and mechanism: conformational changes on oxidation of the active site sulfhydryls to a disulfide. Structure. 3:1995;239-243.
23. Devedjiev Y., Popov A., Atanasov B., Bartunik H.D. X-ray structure at 1.76 resolution of a polypeptide phospholipase a2 inhibitor. J. Mol. Biol. 266:1997;160-172.
24. Lamb A.L., Wernimont A.K., O'Halloran T.V., Rosenzweig A.C. Crystal structure of the second domain of the human copper chaperone for superoxide dismutase. Biochemistry. 39:2000;1589-1595.
25. Lamb A.L., Halloran T.V., Rosenzweig A.C. Heterodimeric structure of superoxide dismutase in complex with its metallochaperone. Nature Struct. Biol. 8:2001;751-755.
26. Kraulis P.J. Molscript: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24:1991;946-950.
27. Wedekind J.E., Frey P.A., Rayment I. The structure of nucleotidylated histidine-166 of galactose-1-phosphate uridylytransferase provides insight into phosphoryl group transfer. Biochemistry. 35:1996;11560-11569.
28. Geeganage S., Frey P.A. Significance of metal ions in galactose-1-phosphate uridylyltransferase: an essential structural zinc and a nonessential structural iron. Biochemistry. 38:1999;13398-13406.
29. Harris P., Poulsen N.J.C., Jensen K.F., Larsen S. Structural basis for the catalytic mechanism of a proficient enzyme: orotidine 5′-monophosphate decarboxylase. Biochemistry. 39:2000;4217-4224.
30. Appleby T.C., Kinsland C., Begley T.P., Ealick S.E. The crystal structure and mechanism of orotidine 5′-monophosphate decarboxylase. Proc. Natl Acad. Sci. USA. 97:2000;2005-2010.
31. Joerger A.C., Gosse C., Fessner W.D., Schulz G.E. Catalytic action of fuculose 1-phosphate aldolase (class II) as derived from structure-directed mutagenesis. Biochemistry. 39:2000;6033-6041.
32. Lima C.D., Klein M.G., Hendrickson W.A. Structure-based analysis of catalysis and substrate definition in the protein family. Science. 278:1997;286-290.
33. Kopp J., Kopriva S., Suss K.H., Schulz G.E. Structure and mechanism of the amphibolic enzyme-ribulose-5-phosphate 3-epimerase from potato chloroplasts. J. Mol. Biol. 287:1999;761-771.
34. Samuel J., Luo Y., Morgan P.M., Strynadka N.C., Tanner M.E. Catalysis and binding in-ribulose-5-phosphate 4-epimerase: a comparison with-fuculose-1-phosphate aldolase. Biochemistry. 40:2001;14772-14780.
35. Somoza J.R., Menon S., Schmidt H., Joseph-McCarthy D., Dessen A., Stahl M.L., et al. Structural and kinetic analysis of Escherichia coli GDP-mannose 4,6 dehydratase provides insights into the enzyme's catalytic mechanism and regulation by GDP-fucose. Struct. Fold. Des. 8:2000;123-135.
36. Gerratana B., Cleland W.W., Frey P.A. Mechanistic roles of Thr134, Tyr160, and Lys164 in the reaction catalysed by dTDP-glucose 4,6-dehydratase. Biochemistry. 40:2001;9187-9195.
37. Allard S.T., Beis K., Giraud M.F., Hegeman A.D., Gross J.W., Wilmouth R.C., et al. Toward a structural understanding of the dehydratase mechanism. Structure (Camb.). 10:2002;81-92.
38. Labahn J., Scharer O.D., Long A., Ezaz-Nikpay K., Verdine G.L., Ellenberger T.E. Structural basis for the excision repair of alkylation-damaged DNA. Cell. 86:1996;321-329.
39. Hollis T., Ichikawa Y., Ellenberger T. DNA bending and a flip-out mechanism for base excision by the helix-hairpin-helix DNA glycosylase, Escherichia coli alka. EMBO J. 19:2000;758-766.
40. Carpenter E.P., Hawkins A.R., Frost J.W., Brown K.A. Structure of dehydroquinate synthase reveals an active site capable of multistep catalysis. Nature. 394:1998;299-302.
41. Liu Y., Thoden J.B., Kim J., Berger E., Gulick A.M., Ruzicka F.J., et al. Mechanistic roles of Tyrosine 149 and Serine 124 in UDP-galactose 4-epimerase from Escherichia coli. Biochemistry. 36:1997;10675-10684.
42. Thoden J.B., Hegeman A.D., Wesenberg G., Chapeau M.C., Frey P.A., Holden H.M. Structural analysis of UDP-sugar binding to UDP-galactose 4-epimerase from Escherichia coli. Biochemistry. 36:1997;6294-6304.
43. Thayer M.M., Ahern H., Xing D., Cunningham R.P., Tainer J.A. Novel DNA binding motifs in the DNA repair enzyme endonuclease III crystal structure. EMBO J. 14:1995;4108-4120.
44. Ruzheninikov S.N., Burke J., Sedelnikova S., Baker P.J., Taylor R., Bullough P.A., et al. Glycerol dehydrogenase. Structure, specificity, and mechanism of a family polyol dehydrogenase. Structure (Camb.). 9:2001;789-802.
45. Srinivasan V., Ma K., Adams M.W., Newton M.G., Rose J.P., Wang B.C. Towards the crystal structure of glycerol dehydrogenase from Thermotoga maritima. Acta. Crystallog. sect. D. 58:2002;867-869.
46. Huang K., Li Z., Jia Y., Dunaway-Mariano D., Herzberg O. Helix swapping between two alpha/beta barrels: crystal structure of phosphoenolpyruvate mutase with bound Mg(2+)-oxalate. Struct. Fold. Des. 7:1999;539-548.
47. Hosfield D.J., Guan Y., Haas B.J., Cunningham R.P., Tainer J.A. Structure of the DNA repair enzyme endonuclease IV and its DNA complex: double-nucleotide flipping at abasic sites and three-metal-ion catalysis. Cell. 98:1999;397-408.
48. Watanabe K., Hata Y., Kizaki H., Katsube Y., Suzuki Y. The refined crystal structure of Bacillus cereus oligo-1,6-glucosidase at 2.0 Å resolution: structural characterization of proline-substitution sites for protein thermostabilization. J. Mol. Biol. 269:1997;142-153.
49. Sharma V., Sharma S., zu K., Bentrup H., McKinney J.D., Russell D.G. Jr, et al. Structure of isocitrate lyase, a persistence factor of Mycobacterium tuberculosis. Nature Struct. Biol. 7:2000;663-668.
50. Collyer C.A., Henrick K., Blow D.M. Mechanism for aldose-ketose interconversion by D-xylose isomerase involving ring opening followed by a 1,2-hydride shift. J. Mol. Biol. 212:1990;211-235.
51. Blow D.M., Collyer C.A., Goldberg J.D., Smart O.S. Structure and mechanism of D-xylose isomerase. Faraday Discuss. 1992;67-73.
52. Strokopytov B., Knegtel R.M., Penninga D., Rozeboom H.J., KalK K.H., Dijkuizen L., Dijkstra B.W. Structure of cyclodextrin glycosyl-transferase complexed with a maltononaose inhibitor at 2.6 angstrom resolution. Implications for product specificity. Biochemistry. 35:1996;4241-4249.
53. Uitdehaag J., van der Veen B.A., Dijkhuizen L., Dijkstra B.W. Catalytic mechanism and product specificity of cyclodextrin glycosyltransferase, a prototypical transglycosylase from the alpha-amylase family. Enzyme Microb. Technol. 30:2002;295-304.
54. Sugio S., Kashima A., Kishimoto K., Peisach D., Petsko G.A., Ringe D., et al. Crystal structures of L201A mutant of D-amino acid aminotransferase at 2.0 Å resolution: implication of the structural role of Leu201 in transamination. Protein Eng. 11:1998;613-619.
55. Peisach D., Chipman D.M., Ophem V.P.W., Manning J.M., Ringe D. Crystallographic study of steps along the reaction pathway of D-amino acid aminotransferase. Biochemistry. 37:1998;4958-4967.
56. van Ophem P.W., Peisach D., Erickson S.D., Soda K., Ringe D., Manning J.M. Effects of the E177k mutation in-amino acid transaminase. Studies on an essential coenzyme anchoring group that contributes to stereochemical fidelity. Biochemistry. 38:1999;1323-1331.
57. Yang G., Sandalova T., Lohman K., Lindqvist Y., Rendina A.R. Active site mutants of Escherichia coli dethiobiotin synthetase: effects of mutations on enzyme catalytic and structural properties. Biochemistry. 36:1997;4751-4760.
58. Kack H., Sandmark J., Gibson K.J., Schneider G., Lindqvist Y. Crystal structure of two quaternary complexes of dethiobiotin synthetase, enzyme-MgADP-AlF3-diaminopelargonic acid and enzyme-MgADP-dethiobiotin-phosphate; implications for catalysis. Protein Sci. 7:1998;2560-2566.
59. Carfi A., Duee E., Paul-Soto R., Galleni M., Frere J.M., Dideberg O. X-ray structure of the ZnII beta-lactamase from Bacteroides fragilis in an orthorhombic crystal form. Acta Crystallog. sect. D. 54:1998;45-57.
60. Nakai T., Mizutani H., Miyahara I., Hirotsu K., Takeda S., Jhee K.H., et al. Three-dimensional structure of 4-amino-4-deoxychorismate lyase from Escherichia coli. J. Biochem. (Tokyo). 128:2000;29-38.
61. Schlessman J.L., Woo D., Joshua-Tor L., Howard J.B., Rees D.C. Conformational variability in structures of the nitrogenase iron proteins from Azotobacter vinelandii and Clostridium pasteurianum. J. Mol. Biol. 280:1998;669-685.
62. Frazao C., Silva G., Gomes C.M., Matias P., Coelho R., Sieker L., et al. Structure of a dioxygen reduction enzyme from Desulfovibrio gigas. Nature Struct. Biol. 7:2000;1041-1045.
63. Mancia F., Smith G.A., Evans P.R. Crystal structure of substrate complexes of methylmalonyl-CoA mutase. Biochemistry. 38:1999;7999-8005.
64. Marsh E.N., Drennan C.L. Adenosylcobalamin-dependent isomerases: new insights into structure and mechanism. Curr. Opin. Chem. Biol. 5:2001;499-505.
65. Tesmer J.J., Klem T.J., Deras M.L., Davisson V.J., Smith J.L. The crystal structure of GMP synthetase reveals a novel catalytic triad and is a structural paradigm for two enzyme families. Nature Struct. Biol. 3:1996;74-86.
66. Benning M.M., Haller T., Gerlt J.A., Holden H.M. New reactions in the crotonase superfamily: structure of methylmalonyl CoA decarboxylase from Escherichia coli. Biochemistry. 39:2000;4630-4639.
67. Drennan C.L., Huang S., Drummond J.T., Matthews R.G., Lidwig M.L. How a protein binds B12: 3.0 Å X-ray structure of B12-binding domains of methionine synthase. Science. 266:1994;1669-1674.
68. Knochel T., Ivens A., Hester G., Gonzalez A., Bauerle R., Wilmanns M., et al. The crystal structure of anthranilate synthase from Sulfolobus solfataricus: functional implications. Proc. Natl Acad. Sci. USA. 96:1999;9479-9484.
69. Yang G., Liu R.Q., Taylor K.L., Xiang H., Price J., Dunaway-Mariano D. Identification of active site residues essential to 4-chlorobenzoyl-coenzyme dehalogenase catalysis by chemical modification and site directed mutagenesis. Biochemistry. 35:1996;10879-10885.
70. Benning M.M., Taylor K.L., Yang G., Xiang H., Wesenberg G., Dunaway-Mariano D., Holden H.M. Structure of 4-chlorobenzoyl coenzyme a dehalogenase determined to 1.8 Å resolution: an enzyme catalyst generated via adaptive mutation. Biochemistry. 35:1996;8103-8109.
71. Lebioda L., Stec B., Brewer J.M., Tykarska E. Inhibition of enolase: the crystal structures of enolase-Ca2(+)-2-phosphoglycerate and enolase-Zn2(+)-phosphoglycolate complexes at 2.2-Å resolution. Biochemistry. 30:1991;2823-2827.
72. Poyner R.R., Laughlin L.T., Sowa G.A., Reed G.H. Toward identification of acid/base catalysts in the active site of enolase: comparison of the properties of K345A, E168Q, and E211Q variants. Biochemistry. 35:1996;1692-1699.
73. Brewer J.M., Glover C.V., Holland M.J., Lebioda L. Effect of site-directed mutagenesis of His373 of yeast enolase on some of its physical and enzymatic properties. Biochim. Biophys. Acta. 1340:1997;88-96.
74. Landro J.A., Gerlt J.A., Kozarich J.W., Koo C.W., Shah V.J., Kenyon G.L., et al. The role of Lysine 166 in the mechanism of mandelate racemase from Pseudomonas putida: mechanistic and crystallographic evidence for stereospecific alkylation by (R)-alpha-phenylglycidate. Biochemistry. 33:1994;635-643.
75. Helin S., Kahn P.C., Guha B.L., Mallows D.G., Goldman A. The refined X-ray structure of muconate lactonizing enzyme from Pseudomonas putida PRS2000 at 1.85 Å resolution. J. Mol. Biol. 254:1995;918-941.
76. Bahnson B.J., Anderson V.E., Petsko G.A. Structural mechanism of enoyl-CoA hydratase: three atoms from a single water are added in either an E1cb stepwise or concerted fashion. Biochemistry. 41:2002;2621-2629.
77. Ridderstrom M., Cameron A.D., Jones T.A., Mannervik B. Involvement of an active site Zn2+ ligand in the catalytic mechanism of human glyoxalase. J. Biol. Chem. 273:1998;21623-21628.
78. Cameron A.D., Ridderstrom M., Olin B., Kavarana M.J., Creighton D.J., Mannervik B. Reaction mechanism of glyoxalase explored by an X-ray crystallographic analysis of the human enzyme in complex with a transition state analogue. Biochemistry. 38:1999;13480-13490.
79. Himo F., Siegbahn P.E. Catalytic mechanism of glyoxalase: a theoretical study. J. Am. Chem. Soc. 123:2001;10280-10289.
80. Charon M.H., Volbeda A., Chabriere E., Pieulle L., Fontecilla-Camps J.C. Structure and electron transfer mechanism of pyruvate:ferredoxin oxidoreductase. Curr. Opin. Struct. Biol. 9:1999;663-669.
81. Chabriere E., Vernede X., Guigliarelli B., Charon M.H., Hatchikian E.C., Fontecilla-Camps J.C. Crystal structure of the free radical intermediate of pyruvate:ferredoxin oxidoreductase. Science. 294:2001;2559-2563.
82. Sato N., Uragami Y., Nishizaki T., Takahashi Y., Sazaki G., Sugimoto K., et al. Crystal structures of the reaction intermediate and its homologue of an extradiol-cleaving catecholic dioxygenase. J. Mol. Biol. 321:2002;621-636.
83. McCarthy A.A., Baker H.M., Shewry S.C., Patchett M.L., Baker E.N. Crystal structure of methylmalonyl-coenzyme epimerase from P. shermanii: a novel enzymatic function on an ancient metal binding scaffold. Structure (Camb.). 9:2001;637-646.
84. Arjunan P., Umland T., Dyda F., Swaminathan S., Furey W., Sax M., et al. Crystal structure of the thiamin diphosphate-dependent enzyme pyruvate decarboxylase from the yeast Saccharomyces cerevisiae at 2.3 Å resolution. J. Mol. Biol. 256:1996;590-600.
85. Sergienko E.A., Jordan F. Catalytic acid-base groups in yeast pyruvate decarboxylase. 3. Steady-state kinetic model consistent with the behavior of both wild-type and variant enzymes at all relevant pH values. Biochemistry. 40:2001;7382-7403.
86. Obmolova G., Badet-Denisot M.A., Badet B., Teplyakov A. Crystallization and preliminary X-ray analysis of the two domains of glucosamine-6-phosphate synthase from Escherichia coli. J. Mol. Biol. 242:1994;703-705.
87. Teplyakov A., Obmolova G., Badet-Denisot M.A., Badet B. The mechanism of sugar phosphate isomerization by glucosamine 6-phosphate synthase. Protein Sci. 8:1999;596-602.
88. Martinez-Cruz L.A., Dreyer M.K., Boisvert D.C., Yokota H., Martinez-Chantar M.L., Kim R., Kim S.H. Crystal structure of MJ1247 protein from M. jannaschii at 2.0 Å resolution infers a molecular function of 3-hexulose-6-phosphate isomerase. Structure (Camb.). 10:2002;195-204.
89. Ito N., Phillips S.E., Yadav K.D., Knowles P.F. Crystal structure of a free radical enzyme, galactose oxidase. J. Mol. Biol. 238:1994;794-814.
90. Gaskell A., Crennell S., Taylor G. The three domains of a bacterial sialidase: a beta-propeller, an immunoglobulin module and a galactose-binding jelly-roll. Structure. 3:1995;1197-1205.
91. Bravo J., Verdaguer N., Tormo J., Betzel C., Switala J., Loewen P.C., Fita I. (May 15 Crystal structure of catalase hpii from Escherichia coli. Structure. 3:1995;491-502.
92. Du X., Choi I.G., Kim R., Wang W., Jancarik J., Yokota H., Kim S.H. Crystal structure of an intracellular protease from Pyrococcus horikoshii at 2 Å resolution. Proc. Natl Acad. Sci. USA. 97:2000;14079-14084.
93. McArthur A.G., Knodler L.A., Silberman J.D., Davids B.J., Gillin F.D., Sogin M.L. The evolutionary origins of eukaryotic protein disulfide isomerase domains: new evidence from the Amitochondriate protist Giardia lamblia. Mol. Biol. Evol. 18:2001;1455-1463.
94. Brenner C. Hint, Fhit, and GalT: function, structure, evolution, and mechanism of three branches of the histidine triad superfamily of nucleotide hydrolases and transferases. Biochemistry. 41:2002;9003-9014.
95. Holden H.M., Benning M.M., Haller T., Gerlt J.A. The crotonase superfamily: divergently related enzymes that catalyze different reactions involving acyl coenzyme a thioesters. Accts Chem. Res. 34:2001;145-157.
96. Clarkson J., Tonge P.J., Taylor K.L., Dunaway-Mariano D., Carey P.R. Raman study of the polarizing forces promoting catalysis in 4-chlorobenzoate-CoA dehalogenase. Biochemistry. 36:1997;10192-10199.
97. Thoden J.B., Wohlers T.M., Fridovich-Keil J.L., Holden H.M. Crystallographic evidence for Tyr157 functioning as the active site base in human UDP-galactose 4-epimerase. Biochemistry. 39:2000;5691-5701.
98. Hasson M.S., Muscate A., McLeish M.J., Polovnikova L.S., Gerlt J.A., Kenyon G.L., et al. The crystal structure of benzoylformate decarboxylase at 1.6 Å resolution: diversity of catalytic residues in thiamin diphosphate-dependent enzymes. Biochemistry. 37:1998;9918-9930.
99. Pearl F.M., Bennett C.F., Bray J.E., Harrison A.P., Martin N., Shepherd A., et al. The CATH database: an extended protein family resource for structural and functional genomics. Nucl. Acids Res. 31:2003;452-455.
100. Lo Conte L., Ailey B., Hubbard T., Brenner S., Murzin A., Chothia C. SCOP: a structural classification of proteins database. Nucl. Acids Res. 28:2000;257-259.
101. Tanner M. Understanding nature's strategies for enzyme-catalyzsed racemization and epimerization. Accts Chem. Res. 35:2002;237-246.