Is allostery an intrinsic property of all dynamic proteins?

Proteins: Structure, Function and Genetics

Volumn 57, Issue 3, 2004, Pages 433-443

  Gunasekaran, K ^a   Ma, Buyong ^a   Nussinov, Ruth ^a,b  

^a SAIC FREDERICK INC   (United States)

^b TEL AVIV UNIVERSITY   (Israel)

Author keywords

Allosteric transition; Allostery; Conformational ensembles; Drug discovery; Energy landscape; Function; Population redistribution

Indexed keywords

6 PHOSPHOFRUCTOKINASE; ASPARTATE CARBAMOYLTRANSFERASE; G PROTEIN COUPLED RECEPTOR; GLYCOGEN; HEMOGLOBIN; LIGAND; MYOGLOBIN; OLIGOMER; PROTEIN; PROTEIN SUBUNIT; RNA DIRECTED DNA POLYMERASE; SYNAPTOPHYSIN; THROMBIN;

ALLOSTERISM; AMINO ACID SEQUENCE; BINDING SITE; CHANNEL GATING; DRUG DESIGN; DRUG PROTEIN BINDING; ENZYME KINETICS; MOLECULAR DYNAMICS; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN STRUCTURE; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; SIMULATION;

ALLOSTERIC REGULATION; ALLOSTERIC SITE; DRUG DESIGN; PROTEIN CONFORMATION; PROTEINS;

EID: 6344219895     PISSN: 08873585     EISSN: None     Source Type: Journal    
DOI: 10.1002/prot.20232     Document Type: Review

References (98)

1. Monod J, Changeux J-P, Jacob F. Allosteric proteins and cellular control systems. J Mol Biol 1963;6:306-329.
2. Perutz M. Cooperativity and allosteric regulation in proteins. Cambridge, UK: Cambridge University Press; 1990.
3. Koshland DE Jr, Hamadani K. Proteomics and models for enzyme cooperativity. J Biol Chem. 2002;277:46841-46844.
4. Umbarger HE. The origin of a useful concept: feedback inhibition. Prot Sci 1992;1:1392-1395.
5. Monod J, Wyman J, Changeux J-P. On the nature of allosteric transitions: a plausible model. J Mol Biol 1965;12:88-118.
6. Koshland DE Jr, Nemethy G, Filmer D. Comparison of experimental binding data and theoretical models in proteins containing subunits. Biochemistry 1966;5:365-385.
7. Eigen M. Kinetics of reaction control and information transfer in enzymes and nucleic acids. Nobel Symp 1967;5:333-369.
8. Jardetzky O. Protein dynamics and conformational transitions in allosteric proteins. Prog Biophys Mol Biol. 1996;65:171-219.
9. Helmstaedt K, Krappmann S, Braus GH. Allosteric regulation of catalytic activity: Escherichia coli aspartate transcarbamoylase versus yeast chorismate mutase. Microbiol Mol Biol Rev 2001;65:404-421.
10. Yu EW, Koshland DE Jr. Propagating conformational changes over long (and short) distances in proteins. Proc Natl Acad USA 2001;98:9517-9520.
11. Ottemann KM, Xiao W, Shin YK, Koshland DE Jr. A piston model for transmembrane signaling of the aspartate receptor. Science 1999;285:1751-1754.
12. Weber G. Ligand binding and internal equilibrium in proteins. Biochemistry 1972;11:864-878
13. Volkman BF, Lipson D, Wemmer DE, Kern D. Two-state allosteric behavior in a single-domain signaling protein. Science 2001;291:2429-2433.
14. Malmendal A, Evenas J, Forsen S, Akke M. Structural dynamics in the C-terminal domain of calmodulin at low calcium levels. J Mol Biol 1999;293:883-899.
15. Martinez KL, Gohon Y, Corringer PJ, Tribet C, Merola F, Changeux JP, Popot JL. Allosteric transitions of Torpedo acetylcholine receptor in lipids, detergent and amphipols: molecular interactions vs. physical constraints. FEBS Lett 2002;528:251-256.
16. Christopoulos A. Allosteric binding sites on cell-surface receptors: novel targets for drug discovery. Nature Rev Drug Discov 2002;1:198-210.
17. Berger C, Weber-Bornhauser S, Eggenberger J, Hanes J, Pluckthun A, Bosshard HR. Antigen recognition by conformational selection. FEBS Lett 1999;450:149-153.
18. Ma B, Kumar S, Tsai CJ, Nussinov R. Folding funnels and binding mechanisms. Prot Eng 1999;12:713-720.
19. Ma B, Kumar S, Tsai CJ, Hu Z, Nussinov R. Transition state ensemble in enzyme catalysis: Possibility reality or necessity? J Theor Biol 1999;203:383-397.
20. Tsai C-J, Ma B, Nussinov R. Folding and binding cascades: shifts in energy landscapes. Proc Natl Acad Sci USA 1999;96:9970-9972.
21. Kumar S, Ma B, Tsai CJ, Sinha N, Nussinov R. Folding and binding cascades: dynamic landscapes and population shifts. Prot Sci 2000;9:10-19.
22. Carlson HA, McCammon JA. Accommodating protein flexibility in computational drug design. Mol Pharmacol 2000;57:213-218.
23. Sinha N, Nussinov R. Point mutations and sequence variability in proteins: redistributions of pre-existing populations. Proc Natl Acad Sci USA 2001;98:3139-3144.
24. Kenakin T. Efficacy at G-protein-coupled receptors. Nat Rev Drug Discov 2002;1:103-110.
25. Kenakin T, Onaran O. The ligand paradox between affinity and efficacy: can you be there and not make a difference? Trends Pharmacol Sci 2002;23:275-280.
26. Freire E. The propagation of binding interactions to remote sites in proteins: analysis of the binding of the monoclonal antibody D1.3 to lysozyme. Proc Natl Acad Sci USA 1999;96:10118-10122.
27. Kern D, Zuiderweg, ERP. The role of dynamics in allosteric regulation. Curr Opin Struct Biol 2003;13:748-757.
28. Pan H, Lee JC, Hilser VJ. Binding sites in Escherichia coli dihydrofolate reductase communicate by modulating the conformational ensemble. Proc Natl Acad Sci USA 2000;97:12020-12025.
29. Gerstein M, Krebs W. A database of macromolecular motions. Nucleic Acids Res 1998;26:4280-4290.
30. Wang X, Kemp RG. Reaction path of phosphofructo-1-kinase is altered by mutagenesis and alternative substrates. Biochemistry 2001;40:3938-3942.
31. Ikeda Y, Taniguchi N, Noguchi T. Dominant negative role of the glutamic acid residue conserved in the pyruvate kinase M(1) isozyme in the heterotropic allosteric effect involving fructose-1,6-bisphosphate. J Biol Chem 2000;275:9150-9156.
32. Lim WA. The modular logic of signaling proteins: building allosteric switches from simple binding domains. Curr Opin Struct Biol 2002;12:61-68.
33. Falcon CM, Matthews KS. Engineered disulfide linking the hinge regions within lactose repressor dimer increases operator affinity decreases sequence selectivity and alters allostery. Biochemistry 2001;40:15650-15659.
34. Santamaria B, Estevez AM, Martinez-Costa OH, Aragon JJ. Creation of an allosteric phosphofructokinase starting with a nonallosteric enzyme. The case of dictyostelium discoideum phosphofructokinase. J Biol Chem 2002;277:1210-1216.
35. Frauenfelder H, McMahon BH, Austin RH, Chu K, Groves JT. The role of structure energy landscape dynamics and allostery in the enzymatic function of myoglobin. Proc Natl Acad Sci USA 2001;98:2370-2374.
36. Pargellis C, Tong L, Churchill L, Cirillo PF, Gilmore T, Graham AG, Grob PM, Hickey ER, Moss N, Pav S, Regan J. Inhibition of p38 MAP kinase by utilizing a novel allosteric binding site. Nat Struct Biol 2002;9:268-272.
37. Simon WA, Hofer HW. Allosteric and non-allosteric phosphofructokinases from Lactobacilli. Purification and properties of phosphofructokinases from L. plantarum and L. acidophilus. Biochim Biophys Acta 1977;481:450-462.
38. Uchikoba H, Fushinobu S, Wakagi T, Konno M, Taguchi H, Matsuzawa H. Crystal structure of non-allosteric L-lactate dehydrogenase from Lactobacillus pentosus at 2.3 A resolution: specific interactions at subunit interfaces. Proteins 2002;46:206-214.
39. Yonetani T, Park SI, Tsuneshige A, Imai K, Kanaori K. Global allostery model of hemoglobin. Modulation of O(2) affinity cooperativity and Bohr effect by heterotropic allosteric effectors. J Biol Chem 2002;277:34508-34520.
40. Krauss M, Korr D, Herrmann A, Hucho F. Binding properties of agonists and antagonists to distinct allosteric states of the nicotinic acetylcholine receptor are incompatible with a concerted model. J Biol Chem 2000;275:30196-30201.
41. Teague SJ. 2003. Implications of protein flexibility for drug discovery. Nat Rev Drug Discov 2003;2:527-541.
42. Demchenko AP. Recognition between flexible protein molecules: induced and assisted folding. J Mol Recognit 2001;14:42-61.
43. Kim KS, Woodward C. Protein internal flexibility and global stability: effect of urea on hydrogen exchange rates of bovine pancreatic trypsin inhibitor. Biochemistry 1993;32:9609-9613.
44. Woodward C. Is the slow exchange core the protein folding core? Trends Biochem Sci 1993;18:359-360.
45. Bai Y, Sosnick TR, Mayne L, Englander SW. Protein folding intermediates: native state hydrogen exchange. Science 1995;269:192-197.
46. Elber R, Karplus M. Multiple conformational states of proteins: a molecular dynamics analysis of myoglobin. Science 1987;235:318-321.
47. Kurbanov FT, Endrizzi JA, Schachman HK, Alber T. Control of flexibility in the allosteric regulation of aspartate transcarbamoylase. Prot Sci 2002;11(Suppl 1):43.
48. Endrizzi JA, Beernink PT, Alber T, Schachman HK. Binding of bisubstrate analog promotes large structural changes in the unregulated catalytic trimer of aspartate transcarbamoylase: Implications for allosteric regulation induced cell migration. Proc Natl Acad Sci USA 2000;97:5077-5082.
49. Barbar EJ, Norwood S, Hare M. Increase in flexibility upon dissociation of dynein light chain LC8 dimer as probed by NMR and mass spectrometry. Biophys J 2002;82:1701.
50. van Aalten DMF, Crielaard W, Hellinger KJ, Joshua-Tor L. Conformational substates in different crystal forms of the photoactive yellow protein: correlation with theoretical and experimental flexibility. Prot Sci 2000;9:64-72.
51. Hammes GG. Multiple conformational changes in enzyme catalysis. Biochemistry 2002;41:8221-8228.
52. Sundberg EJ, Mariuzza RA. Luxury accommodations: the expanding role of structural plasticity in protein-protein interactions. Structure Fold Des 2000;8:R137-R142.
53. DeLano WL, Ultsch MH, de Vos AM, Wells JA. Convergent solutions to binding at a protein-protein interface. Science 2000;287:1279-1283.
54. Ma JP, Sigler PB, Xu ZH, Karplus MA. A dynamic model for the allosteric mechanism of GroEL. J Mol Biol 2000;302:303-313.
55. Ma B, Wolfson H, Nussinov R. Protein functional epitopes: hot spots dynamics and combinatorial libraries. Curr Opin Struct Biol 2001;11:364-369.
56. Roberts EL, Shu N, Howard MJ, Broadhurst RW, Chapman-Smith A, Wallace JC, Morris T, Cronan JE Jr, Perham RN. Solution structures of apo and holo biotinyl domains from acetyl coenzyme A carboxylase of Escherichia coli determined by triple-resonance nuclear magnetic resonance spectroscopy. Biochemistry 1999;38:5045-5053.
57. Zhao D, Arrowsmith CH, Jia X, Jardetzky O. Refined solution structures of the Escherichia coli trp holo- and aporepressor. J Mol Biol 1993;229:735-746.
58. Gunasekaran K, Ma B, Ramakrishnan B, Qasba PK, Nussinov R. The interdependence of backbone flexibility residue conservation and enzyme function: A case study on β1,4-galactosyltransferase-I. Biochemistry 2003;42:3674-3687.
59. Ramakrishnan B, Balaji PV, Qasba PK. Crystal structure of β1,4-galactosyltransferase complex with UDP-gal reveals an oligosaccharide acceptor binding site. J Mol Biol 2002;318:491-502.
60. Lindner AB, Eshhar Z, Tawfik DS. Conformational changes affect binding and catalysis by ester-hydrolyzing antibodies. J Mol Biol 1999;285:421-430.
61. Steitz TA, Shoham M, Bennett WS Jr. Structural dynamics of yeast hexokinase during catalysis. Philos Trans R Soc Soc Lond (Biol) 1981;293:43-52.
62. Schachman HK. Can a simple model account for the allosteric transition of aspartate transcarbamoylase? J Biol Chem 1988;263:18583-18586.
63. Kantrowitz ER, Lipscomb WN. Escherichia coli aspartate transcarbamylase: the relation between structure and function. Science 1988;241:669-674.
64. Kantrowitz ER, Lipscomb WN. Escherichia coli aspartate transcarbamylase: the molecular basis for a concerted allosteric transition. Trends Biochem Sci 1990;15:53-59.
65. Braig K, Otwinowski Z, Hegde R, Boisvert DC, Joachimiak A, Horwich AL, Sigler PB. The crystal structure of the bacterial chaperonin GroEL at 2.8Å. Nature 1994;371:578-586.
66. Xu Z, Horwich AL, Sigler PB. The crystal structure of the asymmetric GroEL-GroES-(ADP)7 chaperonin complex. Nature 1997;388:741-750.
67. Gierasch LM. Caught in the act: how ATP binding triggers cooperative conformational changes in a molecular machine. Mol Cell 2002;9:3-5.
68. Ranson NA, Farr GW, Roseman AM, Gowen B, Fenton WA, Horwich AL, Saibil HR. ATP-bound states of GroEL captured by cryo-electron microscopy. Cell 2001;107:869-879.
69. Cantor CR, Schimmel PR. Biophysical chemistry. Part III. The behavior of biological macromolecules Chapters 15 and 17 New York: W. H. Freeman; 1980.
70. Dickerson RE, Geis I. Hemoglobin: structure function evolution and pathology. Menlo Park, CA: Benjamin-Cummings; 1983.
71. Alberts B, Bray D, Lewis J, Raff M, Roberts K, Watson JD. Molecular biology of the cell, 3rd ed. New York: Garland Pub. New York; 1994.
72. Lazareno S, Birdsall N. Detection quantitation and verification of allosteric interactions of agents with labeled and unlabeled ligands at G protein-coupled receptors: interactions of strychnine and acetylcholine at muscarinic receptors. Mol Pharmacol 1995;48:362-378.
73. Galzi J-L, Changeux J-P. Neurotransmitter-gated ion channels as unconventional allosteric proteins. Curr Opin Struct Biol 1994;4:554-565.
74. Ellis J. Allosteric binding site on muscarinic receptors. Drug Dev Res 1997;40:193-204.
75. Rose RB, Craik CS, Stroud RM. Domain flexibility in retroviral proteases: Structural implications for drug resistant mutations. Biochemistry 1998;37:2607-2621.
76. Gulnik S, Erickson JW, Xie D. HIV protease: enzyme function and drug resistance. Vitam Horm 2000;58:213-256.
77. Luque I, Freire E. Structural stability of binding sites: consequences for binding affinity and allosteric effects. Proteins 2000;(Suppl 4):63-71.
78. Freire E. Can allosteric regulation be predicted from structure? Proc Natl Acad Sci USA 2000;97:1168-11682.
79. Hilser VJ, Freire E. Structure based calculation of the equilibrium folding pathway of proteins. Correlation with hydrogen exchange protection factors. J Mol Biol 1996;262:756-772.
80. Temiz NA, Bahar I. Inhibitor binding alters the directions of domain motions in HIV-1 reverse transcriptase. Proteins 2002;49:61-70.
81. Kurt N, Scott WR, Schiffer CA, Haliloglu T. Cooperative fluctuations of unliganded and substrate-bound HIV-1 protease: a structure-based analysis on a variety of conformations from crystallography and molecular dynamics simulations. Proteins 2003;51:409-422.
82. Lockless SW, Ranganathan R. Evolutionarily conserved pathways of energetic connectivity in protein families. Science 1999;286:295-299.
83. Suel GM, Lockless SW, Wall MA, Ranganathan R. Evolutionarily conserved networks of residues mediate allosteric communication in proteins. Nat Struct Biol 2003;10:56-69.
84. Piana S, Parrinello M, Carloni P. Role of conformational fluctuations in the enzymatic reaction of HIV-1 protease. J Mol Biol 2002;319:567-583.
85. Piana S, Carloni P, Rothlisberger U. Drug resistance in HIV-1 protease: flexibility-assisted mechanism of compensatory mutations. Prot Sci 2002;11:2393-2402.
86. Gunasekaran K, Ma B, Nussinov R. Triggering loops and enzyme function: identification of loops that trigger and modulate movements. J Mol Biol 2003;332:143-159.
87. Gunasekaran K, Nussinov R. Modulating functional loop movements: the role of highly conserved residues in the correlated loop motions. Chem Bio Chem 2004;5:224-230.
88. Schotte F, Lim M, Jackson TA, Smirnov AV, Soman J, Olson JS, Phillips GN Jr, Wulff M, Anfinrud PA. Watching a protein as it functions with 150-ps time-resolved x-ray crystallography. Science 2003;300:1944-1947.
89. Rippin TM, Freund SM, Veprintsev DB, Fersht AR. Recognition of DNA by p53 core domain and location of intermolecular contacts of cooperative binding. J Mol Biol 2002;319:351-358.
90. Schon O, Friedler A, Bycroft M, Freund SM, Fersht AR. Molecular mechanism of the interaction between MDM2 and p53. J Mol Biol 2002;323:491-501.
91. Friedler A, Veprintsev DB, Hansson LO, Fersht AR. Kinetic instability of p53 core domain mutants: implications for rescue by small molecules. J Biol Chem 2003;278:24108-24112.
92. Rippin TM, Bykov VJ, Freund SM. Selivanova G, Wiman KG, Fersht AR. Characterization of the p53-rescue drug CP-31398 in vitro and in living cells. Oncogene 2002;21:2119-2129.
93. Hudson JW, Golding GB, Crerar MM. Evolution of allosteric control in glycogen phosphorylase. J Mol Biol 1993;234:700-721.
94. Oikonomakos NG. Glycogen phosphorylase as a molecular target for type 2 diabetes therapy. Curr Protein Pept Sci 2002;3:561-586.
95. Fredenburgh JC, Stafford AR, Weitz JI. Evidence for allosteric linkage between exosites 1 and 2 of thrombin. J Biol Chem 1997;272:25493-25499.
96. Bell CE, Lewis M. The Lac repressor: a second generation of structural and functional studies. Curr Opin Struct Biol 2001;11:19-25.
97. Helmstaedt K, Krappmann S, Braus GH. Allosteric regulation of catalytic activity: Escherichia coli aspartate transcarbamoylase versus yeast chorismate mutase. Microbiol Mol Biol Rev 2001;65:404-421.
98. Tronchet JM, Seman M. Nonnucleoside inhibitors of HIV-1 reverse transcriptase: from the biology of reverse transcription to molecular design. Curr Top Med Chem 2003;3:1496-1511.