Understanding the Importance of Protein Structure to Nature's Routes for Divergent Evolution in TIM Barrel Enzymes

Accounts of Chemical Research

Volumn 37, Issue 3, 2004, Pages 149-158

  Wise, Eric L ^a   Rayment, Ivan ^a,b,c  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

^c Department of Biochemistry ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CATALYSIS; ENZYME ACTIVE SITE; ENZYME SPECIFICITY; GENE DUPLICATION; GENETIC VARIABILITY; PROTEIN STRUCTURE; REACTION ANALYSIS;

BINDING SITES; ENZYMES; EVOLUTION, MOLECULAR; MODELS, MOLECULAR; PROTEIN CONFORMATION;

EID: 1642342177     PISSN: 00014842     EISSN: None     Source Type: Journal    
DOI: 10.1021/ar030250v     Document Type: Article

References (52)

1. Gerlt, J. A.; Babbitt, P. C. Divergent Evolution of Enzymatic Function: Mechanistically Diverse Superfamilies and Functionally Distinct Suprafamilies. Annu. Rev. Biochem. 2001, 70, 209-246.
2. O'Brien, P. J.; Herschlag, D. Catalytic promiscuity and the evolution of new enzymatic activities. Chem. Biol. 1999, 6, R91-R105.
3. Jensen, R. A. Enzyme recruitment in evolution of new function. Annu. Rev. Microbiol. 1976, 30, 409-425.
4. Henn-Sax, M.; Thoma, R.; Schmidt, S.; Hennig, M.; Kirschner, K.; Sterner, R. Two (betaalpha)(8)-barrel enzymes of histidine and tryptophan biosynthesis have similar reaction mechanisms and common strategies for protecting their labile substrates. Biochemistry 2002, 41, 12032-12042.
5. Babbitt, P. C.; Hasson, M.S.; Wedekind, J. E.; Palmer, D. R.; Barrett, W. C.; Reed, G. H.; Rayment, I.; Ringe, D.; Kenyon, G. L.; Gerlt, J. A. The enolase superfamily: a general strategy for enzyme-catalyzed abstraction of the alpha-protons of carboxylic acids. Biochemistry 1996, 35, 16489-16501.
6. Todd, A. E.; Orengo, C. A.; Thornton, J. M. Evolution of protein function, from a structural perspective. Curr. Opin. Chem. Biol. 1999, 3, 548-556.
7. 8-barrel enzymes that catalyze unrelated reactions: orotidine 5′-monophosphate decarboxylase and 3-keto-L-gulonate 6-phosphate decarboxylase. Biochemistry 2002, 41, 3861-3869.
8. Bartlett, G. J.; Borkakoti, N.; Thornton, J. M. Catalysing new reactions during evolution: economy of residues and mechanism. J. Mol. Biol. 2003, 331, 829-860.
9. Nagano, N.; Orengo, C. A.; Thornton, J. M. One fold with many functions: the evolutionary relationships between TIM barrel families based on their sequences, structures and functions. J. Mol. Biol. 2002, 321, 741-765.
10. Horowitz, N. H. On the evolution of biochemical syntheses. Proc. Natl. Acad. Sci. U.S.A. 1945, 31, 153-157.
11. Gerlt, J. A.; Raushel, F. M. Evolution of function in (beta/alpha)-(8)-barrel enzymes. Curr. Opin. Chem. Biol. 2003, 7, 252-264.
12. Gerlt, J. A. New wine from old barrels. Nat. Struct. Biol. 2000, 7, 171-173.
13. Lazcano, A.; Miller, S. L. On the origin of metabolic pathways. J. Mol. Evol. 1999, 49, 424-431.
14. Ycas, M. On earlier states of the biochemical system. J. Theor. Biol. 1974, 44, 145-160.
15. Horowitz, N. H. The evolution of biochemical syntheses-retrospect and prospect. In Evolving Genes and Proteins; Bryson, V., Vogel, H. J., Eds.; Academic Press: New York, 1965; pp 15-23.
16. Wilmanns, M.; Hyde, C. C.; Davies, D. R.; Kirschner, K.; Jansonius, J. N. Structural conservation in parallel beta/alpha-barrel enzymes that catalyze three sequential reactions in the pathway of tryptophan biosynthesis. Biochemistry 1991, 30, 9161-9169.
17. Weyand, M.; Schlichting, I. Crystal structure of wild-type tryptophan synthase complexed with the natural substrate indole-3-glycerol phosphate. Biochemistry 1999, 38, 16469-16480.
18. Hennig, M.; Darimont, B. D.; Jansonius, J. N.; Kirschner, K. The catalytic mechanism of indole-3-glycerol phosphate synthase: crystal structures of complexes of the enzyme from Sulfolobus solfataricus with substrate analogue, substrate, and product. J. Mol. Biol. 2002, 319, 757-766.
19. Hommel, U.; Eberhard, M.; Kirschner, K. Phosphoribosyl anthranilate isomerase catalyzes a reversible amadori reaction. Biochemistry 1995, 34, 5429-5439.
20. Darimont, B.; Stehlin, C.; Szadkowski, H.; Kirschner, K. Mutational analysis of the active site of indoleglycerol phosphate synthase from Escherichia coli. Protein Sci 1998, 7, 1221-1232.
21. Rhee, S.; Miles, E. W.; Davies, D. R. Cryo-crystallography of a true substrate, indole-3-glycerol phosphate, bound to a mutant (alphaD60N) tryptophan synthase alpha2beta2 complex reveals the correct orientation of active site alphaGlu49. J. Biol. Chem. 1998, 273, 8553-8555.
22. Fani, R.; Lio, P.; Chiarelli, I.; Bazzicalupo, M. The evolution of the histidine biosynthetic genes in prokaryotes: a common ancestor for the hisA and hisF genes. J. Mol. Evol. 1994, 38, 489-495.
23. Lang, D.; Thoma, R.; Henn-Sax, M.; Sterner, R.; Wilmanns, M. Structural evidence for evolution of the beta/alpha barrel scaffold by gene duplication and fusion. Science 2000, 289, 1546-1550.
24. Hocker, B.; Beismann-Driemeyer, S.; Hettwer, S.; Lustig, A.; Sterner, R. Dissection of a (betaalpha)8-barrel enzyme into 2-folded halves. Nat. Struct. Biol. 2001, 8, 32-36.
25. Babbitt, P. C.; Gerlt, J. A. Understanding enzyme superfamilies. Chemistry As the fundamental determinant in the evolution of new catalytic activities. J. Biol. Chem. 1997, 272, 30591-30594.
26. Holm, L.; Sander, C. An evolutionary treasure: unification of a broad set of amidohydrolases related to urease. Proteins 1997, 28, 72-82.
27. Armstrong, R. N. Mechanistic diversity in a metalloenzyme superfamily. Biochemistry 2000, 39, 13625-13632.
28. 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. Acc. Chem. Res. 2001, 34, 145-157.
29. Neidhart, D. J.; Kenyon, G. L.; Gerlt, J. A.; Petsko, G. A. Mandelate racemase and muconate lactonizing enzyme are mechanistically distinct and structurally homologous. Nature 1990, 347, 692-694.
30. 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 A resolution. J. Mol. Biol. 1995, 254, 918-941.
31. Schmidt, D. M.; Hubbard, B. K.; Gerlt, J. A. Evolution of enzymatic activities in the enolase superfamily: functional assignment of unknown proteins in Bacillus subtilis and Escherichia coli as L-AlaD/L-Glu epimerases. Biochemistry 2001, 40, 15707-15715.
32. Larsen, T. M.; Wedekind, J. E.; Rayment, I.; Reed, G. H. A carboxylate oxygen of the substrate bridges the magnesium ions at the active site of enolase: structure of the yeast enzyme complexed with the equilibrium mixture of 2-phosphoglycerate and phosphoenolpyruvate at 1.8 A resolution. Biochemistry 1996, 35, 4349-4358.
33. Landro, J. A.; Gerlt, J. A.; Kozarich, J. W.; Koo, C. W.; Shah, V. J.; Kenyon, G. L.; Neidhart, D. J.; Fujita, S.; Petsko, G. A. 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 1994, 33, 635-643.
34. Gulick, A. M.; Hubbard, B. K.; Gerlt, J. A.; Rayment, I. Evolution of enzymatic activities in the enolase superfamily: identification of the general acid catalyst in the active site of D-glucarate dehydratase from Escherichia coli. Biochemistry 2001, 40, 10054-10062.
35. Miller, B. G.; Smiley, J. A.; Short, S. A.; Wolfenden, R. Activity of yeast orotidine-5′-phosphate decarboxylase in the absence of metals. J. Biol. Chem. 1999, 274, 23841-23843.
36. Yew, W. S.; Gerlt, J. A. Utilization of L-ascorbate by Escherichia coli K-12: assignments of functions to products of the yjf-sga and yia-sgb operons. J. Bacteriol. 2002, 184, 302-306.
37. 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. U.S.A. 2000, 97, 2005-2010.
38. Harris, P.; Navarro Poulsen, J. C.; Jensen, K. F.; Larsen, S. Structural basis for the catalytic mechanism of a proficient enzyme: orotidine 5′-monophosphate decarboxylase. Biochemistry 2000, 39, 4217-4224.
39. Miller, B. G.; Hassell, A. M.; Wolfenden, R.; Milburn, M. V.; Short, S. A. Anatomy of a proficient enzyme: the structure of orotidine 5′- monophosphate decarboxylase in the presence and absence of a potential transition state analog. Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 2011-2016.
40. Wu, N.; Mo, Y.; Gao, J.; Pai, E. F. Electrostatic stress in catalysis: structure and mechanism of the enzyme orotidine monophosphate decarboxylase. Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 2017-2022.
41. Miller, B. G.; Wolfenden, R. Catalytic proficiency: the unusual case of OMP decarboxylase. Annu. Rev. Biochem. 2002, 71, 847-885.
42. Begley, T. P.; Appleby, T. C.; Ealick, S. E. The structural basis for the remarkable catalytic proficiency of orotidine 5′-monophosphate decarboxylase. Curr. Opin. Struct. Biol. 2000, 10, 711-718.
43. Miller, B. G.; Snider, M. J.; Short, S. A.; Wolfenden, R. Contribution of enzyme-phosphoribosyl contacts to catalysis by orotidine 5′-phosphate decarboxylase. Biochemistry 2000, 39, 8113-8118.
44. Miller, B. G.; Snider, M. J.; Wolfenden, R.; Short, S. A. Dissecting a charged network at the active site of orotidine-5′-phosphate decarboxylase. J. Biol. Chem. 2001, 276, 15174-15176.
45. Wise, E.; Yew, W. S.; Gerlt, J. A.; Rayment, I. Structural Evidence for an Enediolate Intermediate in the Reaction Catalyzed by 3-ket-L-gulonate 6-phosphate decarboxylase, a member of the OMPDC Suprafamily. Biochemistry 2003, 42, 12133-12142.
46. Wise, E.; Yew, W. S.; Gerlt, J. A.; Rayment, I. Results not yet published.
47. Yew, W. S.; Wise, E.; Rayment, I.; Gerlt, J. A. Results not yet published, 2003.
48. Traut, T. W.; Temple, B. R. The chemistry of the reaction determines the invariant amino acids during the evolution and divergence of orotidine 5′-monophosphate decarboxylase. J. Biol. Chem. 2000, 275, 28675-28681.
49. Sahm, H.; Schutte, H.; Kula, M. R. Purification and properties of 3-hexulosephosphate synthase from Methylomonas M 15. Eur. J. Biochem. 1976, 66, 591-596.
50. Chen, Y. R.; Hartman, F. C.; Lu, T. Y.; Larimer, F. W. D-Ribulose-5-phosphate 3-epimerase: cloning and heterologous expression of the spinach gene, and purification and characterization of the recombinant enzyme. Plant Physiol. 1998, 118, 199-207.
51. Jelakovic, S.; Kopriva, S.; Suss, K. H.; Schulz, G. E. Structure and catalytic mechanism of the cytosolic D-ribulose-5-phosphate 3-epimerase from rice. J. Mol. Biol. 2003, 326, 127-135.
52. Kopp, J.; Kopriva, S.; Suss, K. H.; Schulz, G. E. Structure and mechanism of the amphibolic enzyme D-ribulose-5-phosphate 3-epimerase from potato chloroplasts. J. Mol. Biol. 1999, 287, 761-771.