Understanding allosteric and cooperative interactions in enzymes

FEBS Journal

Volumn 281, Issue 2, 2014, Pages 621-632

  Cornish Bowden, Athel ^a  

^a AIX MARSEILLE UNIVERSITÉ   (France)

Author keywords

allosteric model; allostery; Changeux; cooperativity; feedback regulation; Filmer; Jacob; Koshland; Monod; N methy; sequential model; Wyman

Indexed keywords

6 PHOSPHOFRUCTOKINASE; ASPARTATE CARBAMOYLTRANSFERASE; G PROTEIN COUPLED RECEPTOR; GLUTAMATE RECEPTOR; LIGAND GATED ION CHANNEL; MEMBRANE PROTEIN; NICOTINIC RECEPTOR;

ALLOSTERISM; BINDING SITE; CATALYSIS; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME REGULATION; ENZYME SPECIFICITY; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; EQUILIBRIUM CONSTANT; MICHAELIS MENTEN KINETICS; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; REVIEW; SYNAPTIC TRANSMISSION; SYSTEMS BIOLOGY;

ALLOSTERIC MODEL; ALLOSTERY; CHANGEUX; COOPERATIVITY; FEEDBACK REGULATION; FILMER; JACOB; KOSHLAND; MONOD; NÉMETHY; SEQUENTIAL MODEL; WYMAN;

ALGORITHMS; ALLOSTERIC REGULATION; ENZYMES; FEEDBACK, PHYSIOLOGICAL; KINETICS; MODELS, CHEMICAL; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; SUBSTRATE SPECIFICITY;

EID: 84892818561     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12469     Document Type: Review

References (115)

1. Monod J, Changeux J-P, &, Jacob F, (1963) Allosteric proteins and cellular control systems. J Mol Biol 6, 306-329.
2. Changeux J-P, (1961) Feedback control mechanism of biosynthetic l -threonine deaminase by l -isoleucine. Cold Spring Harbor Symp Quant Biol 26, 313-318.
3. Monod J, &, Jacob F, (1961) General conclusions: teleonomic mechanisms in cellular metabolism, growth, and differentiation. Cold Spring Harbor Symp Quant Biol 26, 389-401.
4. Henri V, (1902) Théorie générale de l'action de quelques diastases. C R Hebd Séances Acad Sci 135, 916-919.
5. Henri V, (1903) Lois Générales de l'Action des Diastases. Hermann, Paris.
6. Michaelis L, &, Menten ML, (1913) Kinetik der Invertinwirkung. Biochem Z 49, 333-369.
7. Michaelis L, &, Pechstein H, (1914) Über die verschiedenartige Natur der Hemmungen der Invertasewirkung. Biochem Z 60, 79-90.
8. Michaelis L, &, Rona P, (1914) Die Wirkungs bedingenungen der Maltase aus Bierhefe: III. Über die Natur der verschiedenartigen Hemmungen der Fermentwirkungen. Biochem Z 60, 62-78.
9. Umbarger HE, (1956) Evidence for a negative-feedback mechanism in the biosynthesis of isoleucine. Science 123, 848.
10. Yates RA, &, Pardee AB, (1956) Control of pyrimidine biosynthesis in Escherichia coli by a feed-back mechanism. J Biol Chem 221, 757-770.
11. Martin RG, (1963) The first enzyme in histidine biosynthesis: the nature of the feedback inhibition by histidine. J Biol Chem 238, 257-268.
12. Pauling L, (1935) The oxygen equilibrium of hemoglobin and its structural interpretation. Proc Natl Acad Sci USA 21, 186-191.
13. Perutz MF, Rossmann MG, Cullis AF, Muirhead H, Will G, &, North ACT, (1960) Structure of hæmoglobin: a three-dimensional Fourier synthesis at 5.5-Å resolution, obtained by X-ray analysis. Nature 185, 416-422.
14. Monod J, Wyman J, &, Changeux J-P, (1965) On the nature of allosteric transitions-a plausible model. J Mol Biol 12, 88-118.
15. Wyman J, &, Allen DW, (1951) The problem of the heme interactions in hemoglobin and the basis of the Bohr effect. J Polym Sci 7, 499-518.
16. Koshland DE Jr, (1958) Application of a theory of enzyme specificity to protein synthesis. Proc Natl Acad Sci USA 44, 98-104.
17. Koshland DE Jr, (1959) Enzyme flexibility and enzyme action. J Cell Comp Physiol 54, 245-258.
18. Koshland DE Jr, (1996) How to get paid for having fun. Annu Rev Biochem 65, 1-13.
19. Fischer E, (1894) Einfluss der Configuration auf die Wirkung der Enzyme. Ber Deutsch Chem Gesellschaft 27, 2985-2993.
20. Changeux J-P, (1965) Sur les propriétés allostériques de la l -thréonine désaminase de biosynthèse. VI Discussion générale. Bull Soc Chim Biol 47, 281-300.
21. Changeux J-P, (1966) Responses of acetylcholinesterase from Torpedo marmorata to salts and curarizing drugs. Mol Pharmacol 2, 369-392.
22. Changeux J-P, (1969) Symmetry and cooperative properties of biological membranes. In Symmetry and Function of Biological Systems at the Macromolecular Level (, Engstrom A, &, Strandberg B, eds), pp. 235-256. Almqvist & Wiksell, Stockholm.
23. Changeux J-P, (2010) Allosteric receptors: from electric organ to cognition. Annu Rev Pharmacol Toxicol 50, 1-38.
24. Traynelis SF, Wollmuth LP, McBain CJ, Menniti FS, Vance KM, Ogden KK, Hansen KB, Yuan H, Myers SJ, &, Dingledine R, (2010) Glutamate receptor ion channels: structure, regulation, and function. Pharmacol Rev 62, 405-496.
25. Palczewski K, Kumasaka T, Hori T, Behnke CA, Motoshima H, Fox BA, Le Trong I, Teller DC, Okada T, Stenkamp RE, et al,. (2000) Crystal structure of rhodopsin: a G-protein-coupled receptor. Science 289, 739-745.
26. Murakami M, &, Kouyama T, (2008) Crystal structure of squid rhodopsin. Nature 453, 363-367.
27. Koshland DE Jr, Némethy G, &, Filmer D, (1966) Comparison of experimental binding data and theoretical models in proteins containing subunits. Biochemistry 5, 365-385.
28. Grant GA, (2012) Special Issue: allosteric regulation. Introduction. Arch Biochem Biophys 519, 67-68.
29. Cornish-Bowden A, (2012) Fundamentals of Enzyme Kinetics 4th edn. Wiley-VCH, Weinheim.
30. Haber JE, &, Koshland DE Jr, (1967) Relation of protein subunit interactions to the molecular species observed during cooperative binding of ligands. Proc Natl Acad Sci USA 58, 2087-2093.
31. Eigen M, (1968) New looks and outlooks on physical enzymology. Quart Rev Biophys 1, 3-33.
32. Cui Q, &, Karplus M, (2008) Allostery and cooperativity revisited. Protein Sci 17, 1295-1307.
33. Dyachenko R, Gruber R, Shimon L, Horovitz A, &, Sharon M, (2013) Allosteric mechanisms can be distinguished using structural mass spectrometry. Proc Natl Acad Sci USA 110, 7235-7239.
34. Morange M, (2012) What history tells us XXVII. A new life for allostery. J Biosci 37, 13-17.
35. Yudkin J, (1938) Enzyme variation in micro-organisms. Biol Rev Cambridge Phil Soc 13, 93-106.
36. Frieden C, &, Colman RF, (1967) Glutamate dehydrogenase concentration as a determinant in effect of purine nucleotides on enzymatic activity. J Biol Chem 242, 1705-1715.
37. Tomkins GM, &, Yielding KL, (1961) Regulation of enzymic activity of glutamic dehydrogenase mediated by changes in its structure. Cold Spring Harbor Symp Quant Biol 26, 331-341.
38. Frieden C, (1967) Treatment of enzyme kinetic data. II. Multisite case: comparison of allosteric models and a possible new mechanism. J Biol Chem 242, 4045-4052.
39. Nichol LW, Jackson WJH, &, Winzor DJ, (1967) A theoretical study of binding of small molecules to a polymerizing protein system: a model for allosteric effects. Biochemistry 6, 2449-2456.
40. Changeux JP, (1963) Allosteric interactions on biosynthetic l -threonine deaminase from E. coli K12. Cold Spring Harbor Symp Quant Biol 28, 497-504.
41. +-specific isocitrate dehydrogenase. Arch Biochem Biophys 519, 112-117.
42. Ferdinand W, (1966) Interpretation of non-hyperbolic rate curves for two-substrate enzymes: a possible mechanism for phosphofructokinase. Biochem J 98, 278-283.
43. Rabin BR, (1967) Co-operative effects in enzyme catalysis: a possible kinetic model based on substrate-induced conformation isomerization. Biochem J 102, 22C-23C.
44. Niemeyer H, Cárdenas ML, Rabajille E, Ureta T, Clark-Turri L, &, Peñaranda J, (1975) Sigmoidal kinetics of glucokinase. Enzyme 20, 321-333.
45. Storer AC, &, Cornish-Bowden A, (1976) Kinetics of rat-liver glucokinase: co-operative interactions with glucose at physiologically significant concentrations. Biochem J 159, 7-14.
46. Cárdenas ML, (1995) 'Glucokinase': its Regulation and Role in Liver Metabolism. R. G. Landes, Austin, TX.
47. Larion M, &, Miller BG, (2012) Homotropic allosteric regulation in monomeric mammalian glucokinase. Arch Biochem Biophys 519, 103-111.
48. Cárdenas ML, (2013) Michaelis and Menten and the long road to the discovery of cooperativity. FEBS Lett 587, 2767-2771.
49. Cornish-Bowden A, &, Cárdenas ML, (1987) Cooperativity in monomeric enzymes. J Theor Biol 124, 1-23.
50. Gohara DW, &, Di Cera E, (2011) Allostery in trypsin-like proteases suggests new therapeutic strategies. Trends Biotechnol 29, 577-585.
51. Khorchid A, &, Ikura M, (2002) How calpain is activated by calcium. Nat Struct Biol 9, 239-241.
52. Fischer EH, &, Krebs EG, (1955) Conversion of phosphorylase b to phosphorylase a in muscle extracts. J Biol Chem 216, 121-132.
53. Fischer EH, (2013) Cellular regulation by protein phosphorylation. Biochem Biophys Res Commun 430, 865-867.
54. Goldbeter A, &, Koshland DE Jr, (1981) An amplified sensitivity arising from covalent modification in biological systems. Proc Natl Acad Sci USA 78, 6840-6844.
55. Cárdenas ML, &, Cornish-Bowden A, (1989) Characteristics necessary for an interconvertible enzyme cascade to generate a highly sensitive response to an effector. Biochem J 257, 339-345.
56. Szedlacsek SE, Cárdenas ML, &, Cornish-Bowden A, (1992) Response coefficients of interconvertible enzyme cascades towards effectors that act on one or both modifier enzymes. Eur J Biochem 204, 807-813.
57. Xia T, Gray DW, &, Shiman R, (1994) Regulation of rat-liver phenylalanine-hydroxylase. III. Control of catalysis by (6R)-tetrahydrobiopterin and phenylalanine. J Biol Chem 269, 24657-24665.
58. Fitzpatrick PF, (2012) Allosteric regulation of phenylalanine hydroxylase. Arch Biochem Biophys 519, 194-201.
59. Palm DC, Rohwer JM, &, Hofmeyr JHS, (2013) Regulation of glycogen synthase from mammalian skeletal muscle: a unifying view of allosteric and covalent regulation. FEBS J 280, 2-27.
60. Weinkam P, Pons J, &, Sali A, (2012) Structure-based model of allostery predicts coupling between distant sites. Proc Natl Acad Sci USA 109, 4875-4880.
61. Freiburger LA, Auclair K, &, Mittermaier AK, (2012) Van't Hoff global analyses of variable temperature isothermal titration calorimetry data. Thermochim Acta 527, 148-157.
62. Chow SS, Van Petegem F, &, Accili EA, (2012) Energetics of cyclic AMP binding to HCN channel C terminus reveal negative cooperativity. J Biol Chem 287, 600-606.
63. Cornish-Bowden A, (2013) The origins of enzyme kinetics. FEBS Lett 587, 2725-2730.
64. Bellelli A, &, Brunori M, (2011) Hemoglobin allostery: variations on the theme. Biochim Biophys Acta-Bioenerg 1807, 1262-1272.
65. Hofmeyr JHS, &, Cornish-Bowden A, (1997) The reversible Hill equation: how to incorporate cooperative enzymes into metabolic models. Comput Appl Biosci 13, 377-385.
66. Blangy D, Buc H, &, Monod J, (1968) Kinetics of allosteric interactions of phosphofructokinase from Escherichia coli. J Mol Biol 31, 13-35.
67. Kirtley ME, &, Koshland DE Jr, (1967) Models for cooperative effects in proteins containing subunits: effects of two interacting ligands. J Biol Chem 242, 4192-4205.
68. Cornish-Bowden A, &, Koshland DE Jr, (1970) Influence of binding domains on nature of subunit interactions in oligomeric proteins: application to unusual kinetic and binding patterns. J Biol Chem 245, 6241-6250.
69. Cornish-Bowden AJ, &, Koshland DE Jr, (1971) Quaternary structure of proteins composed of identical subunits. J Biol Chem 246, 3092-3102.
70. Briggs GE, &, Haldane JBS, (1925) A note on the kinetics of enzyme action. Biochem J 19, 338-339.
71. Hill AV, (1910) The possible effects of the aggregation of the molecules of haemoglobin on its dissociation curves. J Physiol (Lond) 40, iv-vii.
72. Popova SV, &, Selkov EE, (1975) Generalization of the model of Monod, Wyman and Changeux for the case of reversible monosubstrate reactions S ⇄ (R,T) ⇆ P. FEBS Lett 53, 269-273.
73. Ricard J, &, Noat G, (1985) Subunit coupling and kinetic cooperativity of polymeric enzymes: amplification, attenuation and inversion effects. J Theor Biol 117, 633-649.
74. Lísal J, &, Tuma R, (2005) Cooperative mechanism of RNA packaging motor. J Biol Chem 280, 23157-23164.
75. Kendrew JC, Dickerson RE, Strandberg BE, Hart RG, Davies DR, Phillips DC, &, Shore VC, (1960) Structure of myoglobin: three-dimensional Fourier synthesis at 2 Å resolution. Nature 185, 422-427.
76. Blake CCF, Koenig DF, Mair GA, North ACT, Phillips DC, &, Sarma VR, (1965) Structure of hen egg-white lysozyme: a three-dimensional Fourier synthesis at 2 Å resolution. Nature 206, 757-761.
77. Matthews BW, Sigler PB, Henderson R, &, Blow DM, (1967) Three-dimensional structure of tosyl-α-chymotrypsin. Nature 214, 652-656.
78. Wyckoff HW, Hardman KD, Allewell NM, Inagami T, Johnson LN, &, Richards FM, (1967) Structure of ribonuclease-S at 3.5 Å resolution. J Biol Chem 242, 3984-3988.
79. Dwek RA, Radda GK, Richards RE, &, Salmon AG, (1972) Probes for conformational transitions of phosphorylase a: effect of ligands studied by proton-relaxation enhancement, and chemical reactivities. Eur J Biochem 29, 509-514.
80. Dwek RA, Griffiths JR, Radda GK, &, Strauss U, (1972) A spin label probe for conformational change on conversion of phosphorylase b to phosphorylase a. FEBS Lett 28, 161-164.
81. Brewster AI, Hruby VJ, Spatola AF, &, Bovey FA, (1973) Carbon-13 nuclear magnetic resonance spectroscopy of oxytocin, related oligopeptides, and selected analogs. Biochemistry 12, 1643-1649.
82. 3 and consideration of its properties. Nature 249, 425-429.
83. Hubbell WL, Cafiso DS, &, Altenbach C, (2000) Identifying conformational changes with site directed spin labeling. Nat Struct Biol 7, 735-739.
84. Lorenzi M, Puppo C, Lebrun R, Lignon S, Roubaud V, Martinho M, Mileo E, Tordo P, Marque SRA, Gontero B, et al,. (2011) Tyrosine-targeted spin labeling and EPR spectroscopy: an alternative strategy for studying structural transitions in proteins. Angew Chem Int Edn 50, 9108-9111.
85. Ogawa S, &, McConnell HM, (1967) Spin-label study of hemoglobin conformations in solution. Proc Natl Acad Sci USA 58, 19-28.
86. Kacser H, &, Burns JA, (1973) The control of flux. Symp Soc Expt Biol 27, 65-104.
87. Kacser H, Burns JA, &, Fell DA, (1995) The control of flux. Biochem Soc Trans 23, 341-366.
88. Hofmeyr JHS, &, Cornish-Bowden A, (1991) Quantitative assessment of regulation in metabolic systems. Eur J Biochem 200, 223-236.
89. Hofmeyr JHS, &, Cornish-Bowden A, (2000) Regulating the cellular economy of supply and demand. FEBS Lett 476, 47-51.
90. Cornish-Bowden A, Hofmeyr JHS, &, Cárdenas ML, (1995) Strategies for manipulating metabolic fluxes in biotechnology. Bioorg Chem 23, 439-449.
91. Cornish-Bowden A, &, Cárdenas ML, (2001) Information transfer in metabolic pathways: effects of irreversible steps in computer models. Eur J Biochem 268, 6616-6624.
92. Conway A, &, Koshland DE Jr, (1968) Negative cooperativity in enzyme action. Binding of diphosphopyridine nucleotide to glyceraldehyde 3-phosphate dehydrogenase. Biochemistry 7, 4011-4023.
93. Dalziel K, &, Engel PC, (1968) Antagonistic homotropic interactions as a possible explanation of coenzyme activation of glutamate dehydrogenase. FEBS Lett 1, 349-352.
94. Wyman J, (1967) Allosteric linkage. J Am Chem Soc 89, 2202-2218.
95. Wyman J, (1984) Linkage graphs: a study in the thermodynamics of macromolecules. Q Rev Biophys 17, 453-488.
96. Horovitz A, &, Willison KR, (2005) Allosteric regulation of chaperonins. Curr Opin Struct Biol 15, 646-651.
97. Levitzki A, &, Koshland DE Jr, (1969) Negative cooperativity in regulatory enzymes. Proc Natl Acad Sci USA 62, 1121-1128.
98. Levitzki A, (1974) Negative cooperativity in clustered receptors as a possible basis for membrane action. J Theor Biol 44, 367-372.
99. Cornish-Bowden A, (1975) The physiological significance of negative cooperativity. J Theor Biol 51, 233-235.
100. Atkinson DE, (1977) Cellular Energy Metabolism and its Regulation. Academic Press, New York.
101. Cornish-Bowden A, (2013) The physiological significance of negative cooperativity revisited. J Theor Biol 319, 144-147.
102. Changeux J-P, (2012) Allostery and the Monod-Wyman-Changeux Model after 50 years. Annu Rev Biophys 41, 103-133.
103. Gerhart JC, &, Schachman HK, (1965) Distinct subunits for regulation and catalytic activity of aspartate transcarbamylase. Biochemistry 4, 1054-1062.
104. Changeux J-P, Gerhart JC, &, Schachman HK, (1968) Allosteric interactions in aspartate transcarbamylase. I. Binding of specific ligands to native enzyme and its isolated subunits. Biochemistry 7, 531-538.
105. Winlund CC, &, Chamberlin MJ, (1970) Binding of cytidine triphosphate to aspartate transcarbamylase. Biochem Biophys Res Commun 40, 43-49.
106. Kantrowitz ER, (2012) Allostery and cooperativity in Escherichia coli aspartate transcarbamoylase. Arch Biochem Biophys 519, 81-90.
107. Wiley DC, Evans DR, Warren SG, McMurray CH, Edwards BF, Franks WA, &, Lipscomb WN, (1972) The 5.5 Å resolution structure of the regulatory enzyme, asparate transcarbamylase. Cold Spring Harbor Symp Quant Biol 36, 285-290.
108. Heng S, Stieglitz KA, Eldo J, Xia J, Cardia JP, &, Kantrowitz ER, (2006) T-state inhibitors of E. coli aspartate transcarbamoylase that prevent the allosteric transition. Biochemistry 45, 10062-10071.
109. Endrizzi JA, Beernink PT, Alber T, &, Schachman HK, (2000) Binding of bisubstrate analog promotes large structural changes in the unregulated catalytic trimer of aspartate transcarbamoylase: implications for allosteric regulation. Proc Natl Acad Sci USA 97, 5077-5082.
110. Colquhoun D, &, Lape R, (2012) Allosteric coupling in ligand-gated ion channels. J Gen Physiol 140, 599-612.
111. Auerbach A, (2012) Thinking in cycles: MWC is a good model for acetylcholine receptor channels. J Physiol (Lond) 590, 93-98.
112. Saibil HR, Fenton WA, Clare DK, &, Horwich AL, (2013) Structure and allostery of the chaperonin GroEL. J Mol Biol 425, 1476-1487.
113. Canagarajah BJ, Ren X, Bonifacino JS, &, Hurley JH, (2013) The clathrin adaptor complexes as a paradigm for membrane-associated allostery. Protein Sci 22, 517-529.
114. Noble D, (2008) The Music of Life: Biology beyond Genes. Oxford University Press, Oxford.
115. Changeux J-P, (2011) 50th anniversary of the word 'allosteric'. Protein Sci 20, 1119-1124.