The tryptophan synthase α2β2 complex: A model for substrate channeling, allosteric communication, and pyridoxal phosphate catalysis

Journal of Biological Chemistry

Volumn 288, Issue 14, 2013, Pages 10084-10091

  Miles, Edith Wilson ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOSTERIC COMMUNICATION; INDEPENDENT RESEARCH; MULTI-PROTEIN COMPLEX; MULTIENZYME COMPLEXES; NATIONAL INSTITUTES OF HEALTH; SALMONELLA TYPHIMURIUM; SUBSTRATE CHANNELINGS; THREE-DIMENSIONAL STRUCTURE;

AMINO ACIDS; CATALYSIS; CHEMICAL MODIFICATION; COMMUNICATION; RESEARCH; SALMONELLA;

ENZYMES;

ASPARTIC ACID; CARBOXYLYASE; L ASPARTATE BETA CARBOXYLASE; PYRIDOXAL 5 PHOSPHATE; TRYPTOPHAN SYNTHASE; TRYPTOPHAN SYNTHASE ALPHA2BETA2; UNCLASSIFIED DRUG;

ALLOSTERISM; CATALYSIS; CHEMICAL MODIFICATION; CRYSTALLIZATION; ENZYME ACTIVITY; ENZYME PURIFICATION; ENZYME REGULATION; ENZYME STRUCTURE; EUKARYOTE; HEALTH CARE ORGANIZATION; NATIONAL INSTITUES OF HEALTH; NONHUMAN; PRIORITY JOURNAL; PROKARYOTE; PROTEIN DEGRADATION; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; SALMONELLA TYPHIMURIUM; X RAY CRYSTALLOGRAPHY;

ALLOSTERIC SITE; BACTERIAL PROTEINS; BIOCHEMISTRY; CATALYSIS; HISTORY, 20TH CENTURY; HUMANS; PHOSPHORIC MONOESTER HYDROLASES; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PYRIDOXAL PHOSPHATE; SALMONELLA TYPHIMURIUM; TRYPTOPHAN SYNTHASE; UNITED STATES;

BACTERIA (MICROORGANISMS); EUKARYOTA; PROKARYOTA; SALMONELLA TYPHIMURIUM;

EID: 84875993616     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.X113.463331     Document Type: Review

References (36)

1. Wilson, E. M., and Snell, E. E. (1962) Metabolism ofα-methylserine. I.α-Methylserine hydroxymethyltransferase. J. Biol. Chem. 237, 3171-3179
2. Wilson, E. M., and Snell, E. E. (1962) Metabolism of α- methylserine. II. Stereospecificity of α-methylserine hydroxymethyltransferase. J. Biol. Chem. 237, 3180-3184
3. Wilson, E. M., and Kornberg, H. L. (1963) Properties of crystalline L-aspartate 4-carboxy-lyase from Achromobacter sp. Biochem. J. 88, 578-587
4. Wilson, E. M., and Meister, A. (1966) Optical rotatory dispersion of L-aspartate β-decarboxylase and its derivatives. Biochemistry 5, 1166-1174
5. Miles, E. W., and Meister, A. (1967) The mechanism of the reaction of β-hydroxyaspartate with L-aspartate β-decarboxylase. A new type of pyridoxal 5′- phosphate-enzyme inhibition. Biochemistry 6, 1734-1743
6. Crawford, I. P, and Yanofsky, C. (1958) On the separation of the tryptophan synthetase of Escherichia coli into two protein components. Proc. Natl. Acad. Sci. U.S.A. 44, 1161-1170
7. Miles, E. W., Hatanaka, M., and Crawford, I. P. (1968) A new thiol-dependent transamination reaction catalyzed by the B protein of Escherichia coli tryptophan synthetase. Biochemistry 7, 2742-2753
8. Miles, E. W. (1970) The B protein of Escherichia coli tryptophan synthetase. I. Effects of sulfhydryl modification on enzymatic activities and subunit interaction. J. Biol. Chem. 245, 6016-6025
9. Miles, E. W., and Kumagai, H. (1974) Modification of essential histidyl residues of the β2 subunit of tryptophan synthetase by photo-oxidation in the presence of pyridoxal 5′-phosphate and L-serine and by diethylpyrocarbonate. J. Biol. Chem. 249, 2843-2851
10. Miles, E. W. (1977) Modification of histidyl residues in proteins by diethylpyrocarbonate. Methods Enzymol. 47, 431-442
11. Higgins, W., Fairwell, T., and Miles, E. W. (1979) An active proteolytic derivative of the α subunit of tryptophan synthase. Identification of the site of cleavage and characterization of the fragments. Biochemistry 18, 4827-4835
12. Miles, E. W., Yutani, K., and Ogasahara, K. (1982) Guanidine hydrochloride induced unfolding of the α subunit of tryptophan synthase and of the two α proteolytic fragments: evidence for stepwise unfolding of the two α domains. Biochemistry 21, 2586-2592
13. Kumagai, H., and Miles, E. W. (1971) The B protein of Escherichia coli tryptophan synthetase. II. Newß-elimination andβ-replacement reactions. Biochem. Biophys. Res. Commun. 44, 1271-1278
14. Phillips, R. S., Miles, E. W., and Cohen, L. A. (1984) Interactions of tryptophan synthase, tryptophanase, and pyridoxal phosphate with oxindolyl-L-alanine and 2,3-dihydro-L-tryptophan: support for an indolenine intermediate in tryptophan metabolism. Biochemistry 23, 6228-6234
15. Miles, E. W., Phillips, R. S., Yeh, H. J., and Cohen, L. A. (1986) Isomerization of (3S)-2,3-dihydro-5-fluoro-L-tryptophan and of 5-fluoro-L-tryptophan catalyzed by tryptophan synthase: studies using fluorine-19 nuclear magnetic resonance and difference spectroscopy. Biochemistry 25, 4240-4249
16. Adachi, O., Kohn, L. D., and Miles, E. W. (1974) Crystalline α2β2 complexes of tryptophan synthetase of Escherichia coli. A comparison between the native complex and the reconstituted complex. J. Biol. Chem. 249, 7756-7763
17. Adachi, O., and Miles, E. W. (1974)Arapid method for preparing crystallineß2 subunit of tryptophan synthetase of Escherichia coli in high yield. J. Biol. Chem. 249, 5430-5434
18. Ahmed, S. A., Miles, E. W., and Davies, D. R. (1985) Crystallization and preliminary x-ray crystallographic data of the tryptophan synthase α2β2 complex from Salmonella typhimurium. J. Biol. Chem. 260, 3716-3718
19. Ahmed, S. A., Hyde, C. C., Thomas, G., and Miles, E. W. (1987) Microcrystals of tryptophan synthase α2β2 complex from Salmonella typhimurium are catalytically active. Biochemistry 26, 5492-5498
20. Mozzarelli, A., Peracchi, A., Rossi, G. L., Ahmed, S. A., and Miles, E. W. (1989) Microspectrophotometric studies on single crystals of the tryptophan synthase α2β2 complex demonstrate formation of enzyme-substrate intermediates. J. Biol. Chem. 264, 15774-15780
21. Hyde, C. C., Ahmed, S. A., Padlan, E. A., Miles, E. W., and Davies, D. R. (1988) Three-dimensional structure of the tryptophan synthase α2β2 multienzyme complex from Salmonella typhimurium. J. Biol. Chem. 263, 17857-17871
22. Dunn, M. F. (2012) Allosteric regulation of substrate channeling and catalysis in the tryptophan synthase bienzyme complex. Arch. Biochem. Biophys. 519, 154-166
23. Miles, E. W., McPhie, P., and Yutani, K. (1988) Evidence that glutamic acid 49 of tryptophan synthaseα subunit is a catalytic residue. Inactive mutant proteins substituted at position 49 bind ligands and transmit ligand-dependent effects to the β subunit. J. Biol. Chem. 263, 8611-8614
24. Nagata, S., Hyde, C. C., and Miles, E. W. (1989) The α subunit of tryptophan synthase. Evidence that aspartic acid 60 is a catalytic residue and that the double alteration of residues 175 and 211 in a second-site revertant restores the proper geometry of the substrate binding site. J. Biol. Chem. 264, 6288-6296
25. Rhee, S., Miles, E. W., Mozzarelli, A., and Davies, D. R. (1998) Cryocrystallography and microspectrophotometry of a mutant (αD60N) tryptophan synthase α2β2 complex reveals allosteric roles ofαAsp60. Biochemistry 37, 10653-10659
26. Miles, E. W., Kawasaki, H., Ahmed, S. A., Morita, H., Morita, H., and Nagata S. (1989) The β subunit of tryptophan synthase. Clarification of the roles of histidine 86, lysine 87, arginine 148, cysteine 170, and cysteine 230. J. Biol. Chem. 264, 6280-6287
27. Rhee, S., Parris, K. D., Hyde, C. C., Ahmed, S. A., Miles, E. W., and Davies, D. R. (1997) Crystal structures of a mutant (βK87T) tryptophan synthase α2β2 complex with ligands bound to the active sites of the α- and β-subunits reveal ligand-induced conformational changes. Biochemistry 36, 7664-7680
28. Brzović, P. S., Kayastha, A. M., Miles, E. W., and Dunn, M. F. (1992) Substitution of glutamic acid 109 by aspartic acid alters the substrate specificity and catalytic activity of the β-subunit in the tryptophan synthase bienzyme complex from Salmonella typhimurium. Biochemistry 31, 1180-1190
29. Brzović, P. S., Sawa, Y., Hyde, C. C., Miles, E. W., and Dunn, M. F. (1992) Evidence that mutations in a loop region of the α-subunit inhibit the transition from an open to a closed conformation in the tryptophan synthase bienzyme complex. J. Biol. Chem. 267, 13028-13038
30. Yang, X. J., and Miles, E. W. (1992) Threonine 183 and adjacent flexible loop residues in the tryptophan synthase α subunit have critical roles in modulating the enzymatic activities of the β subunit in the α2β2 complex. J. Biol. Chem. 267, 7520-7528
31. Anderson, K. S., Miles, E. W., and Johnson, K. A. (1991) Serine modulates substrate channeling in tryptophan synthase. A novel intersubunit triggering mechanism. J. Biol. Chem. 266, 8020-8033
32. Anderson, K. S., Kim, A. Y., Quillen, J. M., Sayers, E., Yang, X. J., and Miles, E. W. (1995) Kinetic characterization of channel impaired mutants of tryptophan synthase. J. Biol. Chem. 270, 29936-29944
33. Ruvinov, S. B., Yang, X. J., Parris, K. D., Banik, U., Ahmed, S. A., Miles, E. W., and Sackett, D. L. (1995) Ligand-mediated changes in the tryptophan synthase indole tunnel probed by Nile Red fluorescence with wild type, mutant, and chemically modified enzymes. J. Biol. Chem. 270, 6357-6369
34. Peracchi, A., Mozzarelli, A., and Rossi, G. L. (1995) Monovalent citations affect dynamic and functional properties of the tryptophan synthase α2β2 complex. Biochemistry 34, 9459-9465
35. Peracchi, A., Bettati, S., Mozzarelli, A., Rossi, G. L., Miles, E. W., and Dunn, M. F. (1996) Allosteric regulation of tryptophan synthase: effects of pH, temperature, and α-subunit ligands on the equilibrium distribution of pyridoxal 5′-phosphate-L-serine intermediates. Biochemistry 35, 1872-1880
36. Fan, Y. X., McPhie, P., and Miles, E. W. (2000) Regulation of tryptophan synthase by temperature, monovalent cations, and an allosteric ligand. Evidence from Arrhenius plots, absorption spectra, and primary kinetic isotope effects. Biochemistry 39, 4692-4703