The role of oligomerization and cooperative regulation in protein function: The case of tryptophan synthase

PLoS Computational Biology

Volumn 6, Issue 11, 2010, Pages

  Qaiser Fatmi, M ^a   Chang, Chia En A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BIOCHEMISTRY; COARSE-GRAINED MODELING; CONFORMATIONS; DIMERS; LIGANDS; MOLECULAR DYNAMICS; MONOMERS; OLIGOMERIZATION; SUBSTRATES;

BROWNIAN DYNAMIC SIMULATIONS; COLOCALIZATION; COOPERATIVE REGULATION; DIMERIC UNITS; ISOLATED MONOMERS; OLIGOMERIZATIONS; PROTEIN COMPLEXES; PROTEIN CONFORMATION; PROTEIN FUNCTIONS; TRYPTOPHAN SYNTHASE;

PROTEINS;

TRYPTOPHAN; TRYPTOPHAN SYNTHASE; AMINO ACID; BACTERIAL PROTEIN; INDOLE; INDOLE DERIVATIVE; PROTEIN SUBUNIT;

ALLOSTERISM; AMINO ACID SYNTHESIS; ARTICLE; CATALYSIS; COMPUTER SIMULATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME CONFORMATION; ENZYME STABILITY; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; LIGAND BINDING; MOLECULAR DYNAMICS; OLIGOMERIZATION; PROTEIN FUNCTION; CHEMISTRY; ENZYMOLOGY; HYDROGEN BOND; METABOLISM; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; SALMONELLA TYPHIMURIUM; THERMODYNAMICS;

ALLOSTERIC REGULATION; AMINO ACIDS; BACTERIAL PROTEINS; HYDROGEN BONDING; INDOLES; MOLECULAR DYNAMICS SIMULATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEIN SUBUNITS; SALMONELLA TYPHIMURIUM; THERMODYNAMICS; TRYPTOPHAN SYNTHASE;

EID: 78649648352     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1000994     Document Type: Article

References (83)

1. Woolf PJ, Linderman JJ (2003) Self organization of membrane proteins via dimerization. Biophys Chem 104: 217-227.
2. Marianayagam NJ, Sunde M, Matthews JM (2004) The power of two: protein dimerization in biology. Trends Biochem Sci 29: 618-625.
3. Meng GY, Fronzes R, Chandran V, Remaut H, Waksman G (2009) Protein oligomerization in the bacterial outer membrane. Mol Membr Biol 26: 136-145.
4. Ali MH, Imperiali B (2005) Protein oligomerization: How and why. Bioorgan Med Chem 13: 5013-5020.
5. Brinda KV, Vishveshwara S (2005) Oligomeric protein structure networks: insights into protein-protein interactions. BMC Bioinformatics 6: doi:10.1186/1471-2105-6-296.
6. Cui Q, Karplus M (2008) Allostery and cooperativity revisited. Protein Sci 17: 1295-1307.
7. Koshland DE, Hamadani K (2002) Proteomics and models for enzyme cooperativity. J Biol Chem 277: 46841-46844.
8. Whitty A (2008) Cooperativity and biological complexity. Nat Chem Biol 4: 435-439.
9. Tsai CJ, Del Sol A, Nussinov R (2009) Protein allostery, signal transmission and dynamics: a classification scheme of allosteric mechanisms. Mol Biosyst 5: 207-216.
10. Bahar I, Chennubhotla C, Tobi D (2007) Intrinsic dynamics of enzymes in the unbound state and, relation to allosteric regulation. Curr Opin Struct Biol 17: 633-640.
11. Liu T, Whitten ST, Hilser VJ (2007) Functional residues serve a dominant role in mediating the cooperativity of the protein ensemble. Proc Natl Acad of Sci USA 104: 4347-4352.
12. Mittermaier AK, Kay LE (2009) Observing biological dynamics at atomic resolution using NMR. Trends Biochem Sci 34: 601-611.
13. Gorfe AA, Lu BZ, Yu ZY, McCammon JA (2009) Enzymatic Activity versus Structural Dynamics: The Case of Acetylcholinesterase Tetramer. Biophys J 97: 897-905.
14. Wolf-Watz M, Thai V, Henzler-Wildman K, Hadjipavlou G, Eisenmesser EZ, et al. (2004) Linkage between dynamics and catalysis in a thermophilicmesophilic enzyme pair. Nat Struct Mol Biol 11: 945-949.
15. Kale S, Jordan F (2009) Conformational Ensemble Modulates Cooperativity in the Rate-determining Catalytic Step in the E1 Component of the Escherichia coli Pyruvate Dehydrogenase Multienzyme Complex. J Biol Chem 284: 33122-33129.
16. Arora K, Brooks CL (2007) Large-scale allosteric conformational transitions of adenylate kinase appear to involve a population-shift mechanism. Proc Nat Acad Sci USA 104: 18496-18501.
17. Lee MC, Deng JX, Briggs JM, Duan Y (2005) Large-scale conformational dynamics of the HIV-1 integrase core domain and its catalytic loop mutants. Biophys J 88: 3133-3146.
18. Rhee S, Miles EW, Mozzarelli A, Davies DR (1998) Cryocrystallography and microspectrophotometry of a mutant (alpha D60N) tryptophan synthase alpha(2)beta(2) complex reveals allosteric roles of alpha Asp6O. Biochemistry 37: 10653-10659.
19. Ogasahara K, Hiraga K, Ito W, Miles EW, Yutani K (1992) Origin of the mutual activation of the alpha-subunit and beta-2-subunit 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: 5222-5228.
20. Rowlett R, Yang LH, Ahmed SA, McPhie P, Jhee KH, et al. (1998) Mutations in the contact region between the alpha and beta subunits of tryptophan synthase alter subunit interaction and intersubunit communication. Biochemistry 37: 2961-2968.
21. Spyrakis F, Raboni S, Cozzini P, Bettati S, Mozzarelli A (2006) Allosteric communication between alpha and beta subunits of tryptophan synthase: Modelling the open-closed transition of the alpha subunit. Biochim Biophys Acta 1764: 1102-1109.
22. Dunn MF, Niks D, Ngo H, Barends TRM, Schlichting I (2008) Tryptophan synthase: the workings of a channeling nanomachine. Trends Biochem Sci 33: 254-264.
23. Raboni S, Bettati S, Mozzarelli A (2009) Tryptophan synthase: a mine for enzymologists. Cell Mol Life Sci 66: 2391-2403.
24. Grishin NV, Phillips MA, Goldsmith EJ (1995) Modeling of the spatial structure of eukaryotic ornithine decarboxylases. Protein Sci 4: 1291-1304.
25. Marabotti A, De Biase D, Tramonti A, Bettati S, Mozzarelli A (2001) Allosteric communication of tryptophan synthase - Functional and regulatory properties of the beta S178P mutant. J Biol Chem 276: 17747-17753.
26. Miles EW (1991) Structural basis for catalysis by tryptophan synthase. Adv Enzymol RAMB 64: 93-172.
27. Miles EW (1995) Tryptophan synthase structure, function, and protein engineering. Sub-cell Biochem 24: 207-254.
28. Weischet WO, Kirschner K (1976) Steady-state kinetic studies of synthesis of indoleglycerol phosphate catalyzed by alpha subunit of tryptophan synthase from escherichia-coli - comparison with alpha-2-beta-2-complex. Eur J Biochem 65: 375-385.
29. Kriechbaumer V, Weigang L, Fiesselmann A, Letzel T, Frey M, et al. (2008) Characterisation of the tryptophan synthase a subunit in maize. BMC Plant Biol 8: doi:10.1186/1471-2229-8-44.
30. Yamagata Y, Ogasahara K, Hioki Y, Lee SJ, Nakagawa A, et al. (2001) Entropic stabilization of the tryptophan synthase alpha-subunit from a hyperthermophile, Pyrococcus furiosus - X-ray analysis and calorimetry. J Biol Chem 276: 11062-11071.
31. Hioki Y, Ogasahara K, Lee SJ, Ma JC, Ishida M, et al. (2004) The crystal structure of the tryptophan synthase beta(2) subunit from the hyperthermophile Pyrococcus furiosus - Investigation of stabilization factors. Eur J Biochem 271: 2624-2635.
32. Asada Y, Sawano M, Ogasahara K, Nakamura J, Ota M, et al. (2005) Stabilization mechanism of the tryptophan synthase alpha-subunit from Thermus thermophilus HB8: X-ray crystallographic analysis and calorimetry. J Biochem 138: 343-353.
33. Gierl A, Frey M (2001) Evolution of benzoxazinone biosynthesis and indole production in maize. Planta 213: 493-498.
34. Kulik V, Hartmann E, Weyand M, Frey M, Gierl A, et al. (2005) 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: 608-620.
35. Onufriev A, Bashford D, Case DA (2000) Modification of the generalized Born model suitable for macromolecules. J Phys Chem B 104: 3712-3720.
36. Hornak V, Okur A, Rizzo RC, Simmerling C (2006) HIV-1 protease flaps spontaneously open and reclose in molecular dynamics simulations. Proc Nat Acad Sci USA 103: 915-920.
37. Ngo H, Harris R, Kimmich N, Casino P, Niks D, et al. (2007) Synthesis and characterization of allosteric probes of substrate channeling in the tryptophan synthase bienzyme complex. Biochemistry 46: 7713-7727.
38. Barends TRM, Domratcheva T, Kulik V, Blumenstein L, Niks D, et al. (2008) Structure and mechanistic implications of a tryptophan synthase quinonold intermediate. Chembiochem 9: 1024-1028.
39. Case DA, Cheatham TE, Darden T, Gohlke H, Luo R, et al. (2005) The Amber biomolecular simulation programs. J Comput Chem 26: 1668-1688.
40. Weyand M, Schlichting I (1999) Crystal structure of wild-type tryptophan synthase complexed with the natural substrate indole-3-glycerol phosphate. Biochemistry 38: 16469-16480.
41. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, et al. (2005) Scalable molecular dynamics with NAMD. J Comput Chem 26: 1781-1802.
42. Morris GM, Huey R, Lindstrom W, Sanner MF, Belew RK, et al. (2009) AutoDock4 and AutoDockTools4: Automated Docking with Selective Receptor Flexibility. J Comput Chem 30: 2785-2791.
43. Wang JM, Wolf RM, Caldwell JW, Kollman PA, Case DA (2004) Development and testing of a general amber force field. J Comput Chem 25: 1157-1174.
44. Hornak V, Abel R, Okur A, Strockbine B, Roitberg A, et al. (2006) Comparison of multiple amber force fields and development of improved protein backbone parameters. Proteins 65: 712-725.
45. Wang JM, Wang W, Kollman PA, Case DA (2006) Automatic atom type and bond type perception in molecular mechanical calculations. J Mol Graph Model 25: 247-260.
46. Song YF, Gunner MR (2009) Using Multiconformation Continuum Electrostatics to Compare Chloride Binding Motifs in alpha-Amylase, Human Serum Albumin, and Omp32. J Mol Biol 387: 840-856.
47. Fatmi MQ, Ai R, Chang CEA (2009) Synergistic Regulation and Ligand- Induced Conformational Changes of Tryptophan Synthase. Biochemistry 48: 9921-9931.
48. Humphrey W, Dalke A, Schulten K (1996) VMD: Visual molecular dynamics. J Mol Graphics 14: 33-38.
49. McClendon CL, Friedland G, Mobley DL, Amirkhani H, Jacobson MP (2009) Quantifying Correlations Between Allosteric Sites in Thermodynamic Ensembles. J Chem Theory Comput 5: 2486-2502.
50. Grant BJ, Rodrigues APC, ElSawy KM, McCammon JA, Caves LSD (2006) Bio3d: an R package for the comparative analysis of protein structures. Bioinformatics 22: 2695-2696.
51. Ai R, Fatmi MQ, Chang CA (2010) T-Analyst: a program for efficient analysis of protein conformational changes by torsion angles. J Comput Aid Mol Des 24: 819-827.
52. Tozzini V, McCammon JA (2005) A coarse grained model for the dynamics of flap opening in HIV-1 protease. Chem Phys Lett 413: 123-128.
53. Chang CE, Shen T, Trylska J, Tozzini V, McCammon JA (2006) Gated binding of ligands to HIV-1 protease: Brownian dynamics simulations in a coarsegrained model. Biophys J 90: 3880-3885.
54. Tozzini V, Trylska J, Chang CE, McCammon JA (2007) Flap opening dynamics in HIV-1 protease explored with a coarse-grained model. J Struct Biol 157: 606-615.
55. Scott EE, Gibson QH, Olson JS (2001) Mapping the pathways for O-2 entry into and exit from myoglobin. J Biol Chem 276: 5177-5188.
56. Ermak DL, McCammon JA (1978) Brownian dynamics with hydrodynamic interactions. J Chem Phys 69: 1352-1360.
57. Shen TY, Wong CF, McCammon JA (2001) Atomistic Brownian dynamics simulation of peptide phosphorylation. J Am Chem Soc 123: 9107-9111.
58. Panchenko AR, Wang J, Nienhaus GU, Wolynes PG (1995) Analysis of ligandbinding to heme-proteins using a fluctuating path description. J Phys Chem 99: 9278-9282.
59. Wang J, Wolynes P (1995) Intermittency of single-molecule reaction dynamics in fluctuating environments. Phys Rev Lett 74: 4317-4320.
60. Mazur J, Jernigan RL (1991) Distance-dependent dielectric-constants and their application to double-helical dna. Biopolymers 31: 1615-1629.
61. Vasilyev V (2002) Determination of the effective dielectric constant from the accurate solution of the Poisson equation. J Comput Chem 23: 1254-1265.
62. Luo R, David L, Gilson MK (2002) Accelerated Poisson-Boltzmann calculations for static and dynamic systems. J Comput Chem 23: 1244-1253.
63. Sitkoff D, Sharp KA, Honig B (1994) Accurate calculation of hydration freeenergies using macroscopic solvent models. J Phys Chem 98: 1978-1988.
64. Tan C, Tan YH, Luo R (2007) Implicit nonpolar solvent models. J Phys Chem B 111: 12263-12274.
65. Hnizdo V, Tan J, Killian BJ, Gilson MK (2008) Efficient calculation of configurational entropy from molecular simulations by combining the mutualinformation expansion and nearest-neighbor methods. J Comput Chem 29: 1605-1614.
66. Chang CEA, McLaughlin WA, Baron R, Wang W, McCammon JA (2008) Entropic contributions and the influence of the hydrophobic environment in promiscuous protein-protein association. Proc Nat Acad Sci USA 105: 7456-7461.
67. Meirovitch H (2007) Recent developments in methodologies for calculating the entropy and free energy of biological systems by computer simulation. Curr Opin Struct Biol 17: 181-186.
68. Dill KA, Bromberg S (2003) Molecular Driving Forces. London: Garland Science.
69. Hyde CC, Ahmed SA, Padlan EA, Miles EW, Davis DR (1988) Three- Dimensional Structure of the Tryptophan Synthase alpha2beta2 Multienzyme Complex from Salmonella typhimurium. J Biol Chem 263: 17857-17871.
70. Fidelak J, Juraszek J, Branduardi D, Bianciotto M, Gervasio FL (2010) Free- Energy-Based Methods for Binding Profile Determination in a Congeneric Series of CDK2 Inhibitors. J Phys Chem B 114: 9516-9524.
71. Mills M, Andricioaei I (2008) An experimentally guided umbrella sampling protocol for biomolecules. J Chem Phys 129: 114101-114113.
72. Khare SD, Dokholyan NV (2006) Common dynamical signatures of familial amyotrophic lateral sclerosis-associated structurally diverse Cu, Zn superoxide dismutase mutants. Proc Nat Acad Sci USA 103: 3147-3152.
73. Tarus B, Straub JE, Thirumalai D (2006) Dynamics of Asp23-Lys28 salt-bridge formation in A beta(10-35) monomers. J Am Chem Soc 128: 16159-16168.
74. Scott JD, Pawson T (2009) Cell Signaling in Space and Time: Where Proteins Come Together and When They're Apart. Science 326: 1220-1224.
75. Zhang J, Ma YL, Taylor SS, Tsien RY (2001) Genetically encoded reporters of protein kinase A activity reveal impact of substrate tethering. Proc Nat Acad Sci USA 98: 14997-15002.
76. Conrado RJ, Varner JD, DeLisa MP (2008) Engineering the spatial organization of metabolic enzymes: mimicking nature's synergy. Curr Opin Biotech 19: 492-499.
77. Zhou HX (2010) From Induced Fit to Conformational Selection: A Continuum of Binding Mechanism Controlled by the Timescale of Conformational Transitions. Biophys J 98: L15-L17.
78. Okazaki KI, Takada S (2008) Dynamic energy landscape view of coupled binding and protein conformational change: Induced-fit versus population-shift mechanisms. Proc Nat Acad Sci USA 105: 11182-11187.
79. Boehr DD, Nussinov R, Wright PE (2009) The role of dynamic conformational ensembles in biomolecular recognition. Nat Chem Biol 5: 789-796.
80. Xing JH (2007) Nonequilibrium dynamic mechanism for allosteric effect. Phys Rev Lett 99: 168103-168106.
81. Harris RM, Ngo H, Dunn MF (2005) Synergistic effects on escape of a ligand from the closed tryptophan synthase bienzyme complex. Biochemistry 44: 16886-16895.
82. Monticelli L, Kandasamy SK, Periole X, Larson RG, Tieleman DP, et al. (2008) The MARTINI coarse-grained force field: Extension to proteins. J Chem Theory Comput 4: 819-834.
83. Gopal SM, Mukherjee S, Cheng YM, Feig M (2010) PRIMO/PRIMONA: A coarse-grained model for proteins and nucleic acids that preserves near-atomistic accuracy. Proteins 78: 2187-2187.