Allosteric communication between alpha and beta subunits of tryptophan synthase: Modelling the open-closed transition of the alpha subunit

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1764, Issue 6, 2006, Pages 1102-1109

  Spyrakis, Francesca ^a   Raboni, Samanta ^a   Cozzini, Pietro ^a   Bettati, Stefano ^a   Mozzarelli, Andrea ^a  

^a UNIVERSITY OF PARMA   (Italy)

Author keywords

Allosteric communication; Dynamic simulation; HINT; Open closed transition; Pyridoxal 5 phosphate

Indexed keywords

ALANINE; GLYCINE; PHENYLALANINE; PROLINE; SERINE; TRYPTOPHAN SYNTHASE; VALINE;

ALLOSTERISM; ALPHA CHAIN; ARTICLE; BETA CHAIN; CATALYSIS; CORRELATION ANALYSIS; ENTHALPY; ENTROPY; ENZYME ACTIVE SITE; ENZYME CONFORMATION; ENZYME STRUCTURE; ENZYME SUBSTRATE; HYDROGEN BOND; LIGAND BINDING; MOLECULAR DYNAMICS; MOLECULAR MODEL; MUTATIONAL ANALYSIS; PHASE TRANSITION; PRIORITY JOURNAL; PROTEIN DEGRADATION; SIGNAL TRANSDUCTION; SIMULATION; STRUCTURAL PROTEOMICS;

ALLOSTERIC SITE; BINDING SITES; COMPUTER SIMULATION; HYDROGEN BONDING; LIGANDS; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MUTATION; OXYGEN; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; SALMONELLA TYPHIMURIUM; THERMODYNAMICS; TRYPTOPHAN SYNTHASE;

EID: 33745185519     PISSN: 15709639     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbapap.2006.03.005     Document Type: Article

References (59)

1. Koshl Jr. D.E., Ray Jr. W.J., and Erwin M.J. Protein structure and enzyme action. Fed. Proc. 17 (1958) 1145-1150
2. Gutteridge A., and Thornton J. Conformational change in substrate binding, catalysis and product release: an open and shut case?. FEBS Lett. 567 (2004) 67-73
3. Goldbeter A., and Koshland Jr. D.E. An amplified sensitivity arising from covalent modification in biological systems. Proc. Natl. Acad. Sci. U. S. A. 78 (1981) 6840-6844
4. Goh C.S., Milburn D., and Gerstein M. Conformational changes associated with protein-protein interactions. Curr. Opin. Struct. Biol. 14 (2004) 104-109
5. Swain J.F., and Gierasch L.M. The changing landscape of protein allostery. Curr. Opin. Struct. Biol. 16 (2006) 102-108
6. Stieglitz K., Stec B., Baker D.P., and Kantrowitz E.R. Monitoring the transition from the T to the R state in E. coli aspartate transcarbamoylase by X-ray crystallography: crystal structures of the E50A mutant enzyme in four distinct allosteric states. J. Mol. Biol. 341 (2004) 853-868
7. Perutz M. Mechanisms of Cooperativity and Allosteric Regulation in Proteins (1989), Cambridge University Press, Cambridge
8. Monod J., Wyman J., and Changeux J.P. On the nature of allosteric transitions: a plausible model. J. Mol. Biol. 12 (1965) 88-118
9. Koshland Jr. D.E., Nemethy G., and Filmer D. Comparison of experimental binding data and theoretical models in proteins containing subunits. Biochemistry 5 (1966) 365-385
10. Changeux J.P., and Edelstein S.J. Allosteric mechanisms of signal transduction. Science 308 (2005) 1424-1428
11. Pan P., Woehl E., and Dunn M.F. Protein architecture, dynamics and allostery in tryptophan synthase channeling. Trends Biochem. Sci. 22 (1997) 22-27
12. Ruvinov S.B., Yang X.J., Parris K.D., Banik U., Ahmed S.A., Miles E.W., and Sackett D.L. 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 (1995) 6357-6369
13. Miles E.W. Tryptophan synthase. Structure, function, and protein engineering. Subcell. Biochem. 24 (1995) 207-254
14. Miles E.W. Structural basis for catalysis by tryptophan synthase. Adv. Enzymol. Relat. Areas Mol. Biol. 64 (1991) 93-172
15. Peracchi A., Mozzarelli A., and Rossi G.L. Monovalent cations affect dynamic and functional properties of the tryptophan synthase alpha 2 beta 2 complex. Biochemistry 34 (1995) 9459-9465
16. Peracchi A., Bettati S., Mozzarelli A., Rossi G.L., Miles E.W., and Dunn M.F. Allosteric regulation of tryptophan synthase: effects of pH, temperature, and alpha-subunit ligands on the equilibrium distribution of pyridoxal 5′-phosphate-l-serine intermediates. Biochemistry 35 (1996) 1872-1880
17. Fan Y.X., McPhie P., and Miles E.W. 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 (2000) 4692-4703
18. Dunn M.F., Aguilar V., Brzovic P., Drewe W.F., Houben K.F., Leja C.A., and Roy M. The tryptophan synthase bienzyme complex transfers indole between the alpha- and beta-sites via a 25-30 Å long tunnel. Biochemistry 29 (1990) 8598-8607
19. Anderson K.S., Miles E.W., and Johnson K.A. Serine modulates substrate channeling in tryptophan synthase. A novel intersubunit triggering mechanism. J. Biol. Chem. 266 (1991) 8020-8033
20. Strambini G.B., Cioni P., Peracchi A., and Mozzarelli A. Conformational changes and subunit communication in tryptophan synthase: effect of substrates and substrate analogs. Biochemistry 31 (1992) 7535-7542
21. Ferrari D., Niks D., Yang L.H., Miles E.W., and Dunn M.F. Allosteric communication in the tryptophan synthase bienzyme complex: roles of the beta-subunit aspartate 305-arginine 141 salt bridge. Biochemistry 42 (2003) 7807-7818
22. Osborne A., Teng Q., Miles E.W., and Phillips R.S. Detection of open and closed conformations of tryptophan synthase by 15N-heteronuclear single-quantum coherence nuclear magnetic resonance of bound 1-15N-l-tryptophan. J. Biol. Chem. 278 (2003) 44083-44090
23. Rhee S., Parris K.D., Hyde C.C., Ahmed S.A., Miles E.W., and Davies D.R. Crystal structures of a mutant (betaK87T) tryptophan synthase alpha2beta2 complex with ligands bound to the active sites of the alpha- and beta-subunits reveal ligand-induced conformational changes. Biochemistry 36 (1997) 7664-7680
24. Weyand M., Schlichting I., Herde P., Marabotti A., and Mozzarelli A. Crystal structure of the beta Ser178-Pro mutant of tryptophan synthase. A "knock-out" allosteric enzyme. J. Biol. Chem. 277 (2002) 10653-10660
25. Rhee S., Miles E.W., Mozzarelli A., and Davies D.R. Cryocrystallography and microspectrophotometry of a mutant (alpha D60N) tryptophan synthase alpha 2 beta 2 complex reveals allosteric roles of alpha Asp60. Biochemistry 37 (1998) 10653-10659
26. Weber-Ban E., Hur O., Bagwell C., Banik U., Yang L.H., Miles E.W., and Dunn M.F. Investigation of allosteric linkages in the regulation of tryptophan synthase: the roles of salt bridges and monovalent cations probed by site-directed mutation, optical spectroscopy, and kinetics. Biochemistry 40 (2001) 3497-3511
27. Brzovic P.S., Sawa Y., Hyde C.C., Miles E.W., and Dunn M.F. Evidence that mutations in a loop region of the alpha-subunit inhibit the transition from an open to a closed conformation in the tryptophan synthase bienzyme complex. J. Biol. Chem. 267 (1992) 13028-13038
28. Brzovic P.S., Ngo K., and Dunn M.F. Allosteric interactions coordinate catalytic activity between successive metabolic enzymes in the tryptophan synthase bienzyme complex. Biochemistry 31 (1992) 3831-3839
29. Marabotti A., De Biase D., Tramonti A., Bettati S., and Mozzarelli A. Allosteric communication of tryptophan synthase. Functional and regulatory properties of the beta S178P mutant. J. Biol. Chem. 276 (2001) 17747-17753
30. Kulik V., Hartmann E., Weyand M., Frey M., Gierl A., Niks D., Dunn M.F., and Schlichting I. On the structural basis of the catalytic mechanism and the regulation of the alpha subunit of tryptophan synthase from Salmonella typhimurium and BX1 from maize. Two evolutionarily related enzymes. J. Mol. Biol. 352 (2005) 608-620
31. Bahar I., and Jernigan R.L. Cooperative fluctuations and subunit communication in tryptophan synthase. Biochemistry 38 (1999) 3478-3490
32. Schneider T.R., Gerhardt E., Lee M., Liang P.H., Anderson K.S., and Schlichting I. Loop closure and intersubunit communication in tryptophan synthase. Biochemistry 37 (1998) 5394-5406
33. Raboni S., Pioselli B., Bettati S., and Mozzarelli A. The molecular pathway for the allosteric regulation of tryptophan synthase. Biochim. Biophys. Acta 1647 (2003) 157-160
34. Raboni S., Bettati S., and Mozzarelli A. Identification of the geometric requirements for allosteric communication between the alpha- and beta-subunits of tryptophan synthase. J. Biol. Chem. 280 (2005) 13450-13456
35. Xie G., Forst C., Bonner C., and Jensen R.A. Significance of two distinct types of tryptophan synthase beta chain in Bacteria, Archaea and higher plants. Genome Biol. 3 (2002) 1-13 (RESEARCH0004)
36. Weyand M., Schlichting I., Marabotti A., and Mozzarelli A. Crystal structures of a new class of allosteric effectors complexed to tryptophan synthase. J. Biol. Chem. 277 (2002) 10647-10652
37. Lee S.J., Ogasahara K., Ma J., Nishio K., Ishida M., Yamagata Y., Tsukihara T., and Yutani K. Conformational changes in the tryptophan synthase from a hyperthermophile upon alpha2beta2 complex formation: crystal structure of the complex. Biochemistry 44 (2005) 11417-11427
38. Miles E.W. The tryptophan synthase alpha 2 beta 2 complex. Cleavage of a flexible loop in the alpha subunit alters allosteric properties. J. Biol. Chem. 266 (1991) 10715-10718
39. Ruvinov S.B., and Miles E.W. Subunit communication in the tryptophan synthase alpha 2 beta 2 complex. Effects of beta subunit ligands on proteolytic cleavage of a flexible loop in the alpha subunit. FEBS Lett. 299 (1992) 197-200
40. Kellogg G.E., and Abraham D.J. Hydrophobicity: is LogP(o/w) more than the sum of its parts?. Eur. J. Med. Chem. 35 (2000) 651-661
41. Burnett J.C., Kellogg G.E., and Abraham D.J. Computational methodology for estimating changes in free energies of biomolecular association upon mutation. The importance of bound water in dimer-tetramer assembly for beta 37 mutant hemoglobins. Biochemistry 39 (2000) 1622-1633
42. Cozzini P., Fornabaio M., Marabotti A., Abraham D.J., Kellogg G.E., and Mozzarelli A. Simple, intuitive calculations of free energy of binding for protein-ligand complexes. 1. Models without explicit constrained water. J. Med. Chem. 45 (2002) 2469-2483
43. Fornabaio M., Cozzini P., Mozzarelli A., Abraham D.J., and Kellogg G.E. Simple, intuitive calculations of free energy of binding for protein-ligand complexes. 2. Computational titration and pH effects in molecular models of neuraminidase-inhibitor complexes. J. Med. Chem. 46 (2003) 4487-4500
44. Fornabaio M., Spyrakis F., Mozzarelli A., Cozzini P., Abraham D.J., and Kellogg G.E. Simple, intuitive calculations of free energy of binding for protein-ligand complexes. 3. The free energy contribution of structural water molecules in HIV-1 protease complexes. J. Med. Chem. 47 (2004) 4507-4516
45. Spyrakis F., Fornabaio M., Cozzini P., Mozzarelli A., Abraham D.J., and Kellogg G.E. Computational titration analysis of a multiprotic HIV-1 protease-ligand complex. J. Am. Chem. Soc. 126 (2004) 11764-11765
46. White D., and Bovill M. Molecular mechanics calculations on alkanes and non-conjugated alkanes. J. Chem. Soc. Perkin II 12 (1977) 1610-1623
47. Vinter J.G., Davis A., and Saunders M.R. Strategic approaches to drug design: I. An integrated software framework for molecular modelling. J. Comput. Aided Mol. Des. 1 (1987) 31-51
48. Clark M., and Cramer R.D. Validation of the general purpose Tripos 5.2 force field. J. Comput. Chem. 10 (1989) 982-1012
49. Verlet L. Computer "experiments" on classical fluids: I. Thermodynamical properties of Lennard-Jones molecules. Phys. Rev. 159 (1967) 98-103
50. Keil M., Exner T.E., and Brickmann J. Pattern recognition strategies for molecular surfaces: III. Binding site prediction with a neural network. J. Comput. Chem. 25 (2004) 779-789
51. Cozzini P., Fornabaio M., Marabotti A., Abraham D.J., Kellogg G.E., and Mozzarelli A. Free energy of ligand binding to protein: evaluation of the contribution of water molecules by computational methods. Curr. Med. Chem. 11 (2004) 3093-3118
52. Joseph D., Petsko G.A., and Karplus M. Anatomy of a conformational change: hinged "lid" motion of the triosephosphate isomerase loop. Science 249 (1990) 1425-1428
53. Ogasahara K., Hiraga K., Ito W., Miles E.W., and Yutani K. Origin of the mutual activation of the alpha and beta 2 subunits in the alpha 2 beta 2 complex of tryptophan synthase. Effect of alanine or glycine substitutions at proline residues in the alpha subunit. J. Biol. Chem. 267 (1992) 5222-5228
54. Rowlett R., Yang L.H., Ahmed S.A., McPhie P., Jhee K.H., and Miles E.W. Mutations in the contact region between the alpha and beta subunits of tryptophan synthase alter subunit interaction and intersubunit communication. Biochemistry 37 (1998) 2961-2968
55. Yang X.J., and Miles E.W. Threonine 183 and adjacent flexible loop residues in the tryptophan synthase alpha subunit have critical roles in modulating the enzymatic activities of the beta subunit in the alpha 2 beta 2 complex. J. Biol. Chem. 267 (1992) 7520-7528
56. Brzovic P.S., Hyde C.C., Miles E.W., and Dunn M.F. Characterization of the functional role of a flexible loop in the alpha-subunit of tryptophan synthase from Salmonella typhimurium by rapid-scanning, stopped-flow spectroscopy and site-directed mutagenesis. Biochemistry 32 (1993) 10404-10413
57. Kulik V., Weyand M., Seidel R., Niks D., Arac D., Dunn M.F., and Schlichting I. On the role of alphaThr183 in the allosteric regulation and catalytic mechanism of tryptophan synthase. J. Mol. Biol. 324 (2002) 677-690
58. Nishio K., Morimoto Y., Ishizuka M., Ogasahara K., Tsukihara T., and Yutani K. Conformational changes in the alpha-subunit coupled to binding of the beta 2-subunit of tryptophan synthase from Escherichia coli: crystal structure of the tryptophan synthase alpha-subunit alone. Biochemistry 44 (2005) 1184-1192
59. Derreumaux P., and Schlick T. The loop opening/closing motion of the enzyme triosephosphate isomerase. Biophys. J. 74 (1998) 72-81