A Unified View of "How Allostery Works"

PLoS Computational Biology

Volumn 10, Issue 2, 2014, Pages

  Tsai, Chung Jung ^a   Nussinov, Ruth ^a,b  

^a FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^b TEL AVIV UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

FREE ENERGY;

ALLOSTERIC MECHANISMS; ALLOSTERY; BASIC SCIENCE; CANCER PROGRESSION; DRUG DISCOVERY; LIVING CELL; ONCOGENICS; PRACTICAL IMPORTANCE; QUANTITATIVE MATHEMATICAL MODEL; STRUCTURAL MECHANISMS;

BINDING SITES;

ALLOSTERISM; ARTICLE; BINDING AFFINITY; BINDING SITE; CHEMICAL STRUCTURE; CONFORMATIONAL TRANSITION; DRUG DESIGN; MATHEMATICAL MODEL; QUALITATIVE RESEARCH; QUANTITATIVE STUDY; SIGNAL DETECTION; SIGNAL TRANSDUCTION; SYNTHESIS; THERMODYNAMICS; BIOLOGICAL MODEL; BIOLOGY;

LIGAND;

ALLOSTERIC REGULATION; ALLOSTERIC SITE; COMPUTATIONAL BIOLOGY; LIGANDS; MODELS, BIOLOGICAL; SIGNAL TRANSDUCTION; THERMODYNAMICS;

EID: 84895745240     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003394     Document Type: Article

References (62)

1. Nussinov R, Tsai C-J, (2013) Allostery in disease and in drug discovery. Cell 153: 293-305.
2. Jura N, Zhang XW, Endres NF, Seeliger MA, Schindler T, et al. (2011) Catalytic control in the EGF receptor and its connection to general kinase regulatory mechanisms. Mol Cell 42: 9-22.
3. Jeffrey PD, Ruso AA, Polyak K, Gibbs E, Hurwitz J, et al. (1995) Mechanism of CDK activation revealed by the structure of a cyclinA-CDK2 complex. Nature 376: 313-320.
4. Blackmore NJ, Reichau S, Jiao W, Hutton RD, Baker EN, et al. (2013) Three sites and you are out: ternary synergistic allostery controls aromatic amino acid biosynthesis in mycobacterium tuberculosis. J Mol Biol 425: 1582-1592.
5. Tang S, Liao J-C, Dunn AR, Altman RB, Spudich JA, et al. (2007) Predicting allosteric communication in myosin via a pathway of conserved residues. J Mol Biol 373: 1361-1373.
6. Srinivasan S, Nwachukwu JC, Parent AA, Cavett V, Nowak J, et al. (2013) Ligand-binding dynamics rewire cellular signaling via estrogen receptor-alpha. Nat Chem Biol 9: 326-332.
7. Bruning JB, Parent AA, Gil G, Zhao M, Nowak J, et al. (2010) Coupling of receptor conformation and ligand orientation determine graded activity. Nat Chem Biol 6: 837-843.
8. Gardino AK, Villali J, Kivenson A, Lei M, Liu CF, et al. (2009) Transient non-native hydrogen bonds promote activation of a signaling protein. Cell 139: 1109-1118.
9. Volkman BF, Lipson D, Wemmer DE, Kern D, (2001) Two-state allosteric behavior in a single-domain signaling protein. Science 291: 2429-2433.
10. Frauenfelder H, Sligar SG, Wolynes PG, (1991) The energy landscapes and motions of proteins. Science 254: 1598-1603.
11. Fenton AW, (2008) Allostery: an illustrated definition for the 'second secret of life'. Trends Biochem Sci 33: 420-425.
12. Monod J, Changeux JP, Jacob F, (1963) Allosteric proteins and cellular control systems. J Mol Biol 6: 306-329.
13. Changeux J-P, (2012) Allostery and the Monod-Wyman-Changeux model after 50 years. Annu Rev Biophys 41: 103-133.
14. Hilser VJ, Wrabl JO, Motlagh HN, (2012) Structural and energetic basis of allostery. Annu Rev Biophys 41: 585-609.
15. Cui Q, Karplus M, (2008) Allostery and cooperativity revisited. Protein Sci 17: 1295-1307.
16. Sadowsky JD, Burlingame MA, Wolan DW, McClendon CL, Jacobson MP, et al. (2011) Turning a protein kinase on or off from a single allosteric site via disulfide trapping. Proc Natl Acad Sci U S A 108: 6056-6061.
17. Motlagh HN, Hilser VJ, (2012) Agonism/antagonism switching in allosteric ensembles. Proc Natl Acad Sci U S A 109: 4134-4139.
18. Ma JP, Karplus M, (1998) The allosteric mechanism of the chaperonin GroEL: A dynamic analysis. Proc Natl Acad Sci U S A 95: 8502-8507.
19. Kong YF, Ma JP, Karplus M, Lipscomb WN, (2006) The allosteric mechanism of yeast chorismate mutase: a dynamic analysis. J Mol Biol 356: 237-247.
20. Cecchini M, Houdusse A, Karplus M, (2008) Allosteric communication in myosin V: from small conformational changes to large directed movements. PLoS Comput Biol 4: e1000129.
21. Monod J, Wyman J, Changeux JP, (1965) On the nature of allosteric transitions: a plausible model. J Mol Biol 12: 88-118.
22. Perutz MF, (1970) Stereochemistry of cooperative effects in haemoglobin. Nature 228: 726-739.
23. Szabo A, Karplus M, (1972) A mathematical model for structure-function relations in hemoglobin. J Mol Biol 72: 163-197.
24. Eaton WA, Henry ER, Hofrichter J, Bettati S, Viappiani C, et al. (2007) Evolution of allosteric models for hemoglobin. IUBMB Life 59: 586-599.
25. Ciaccio C, Coletta A, De Saneti G, Marini S, Coletta M, (2008) Cooperativity and allostery in haemoglobin function. IUBMB Life 60: 112-123.
26. Yonetani T, Laberge M, (2008) Protein dynamics explain the allosteric behaviors of hemoglobin. Biochim Biophys Acta 1784: 1146-1158.
27. Gunasekaran K, Ma BY, Nussinov R, (2004) Is allostery an intrinsic property of all dynamic proteins? Proteins 57: 433-443.
28. Tsai CJ, Ma BY, Sham YY, Kumar S, Nussinov R, (2001) Structured disorder and conformational selection. Proteins 44: 418-427.
29. Kumar S, Ma BY, Tsai CJ, Sinha N, Nussinov R, (2000) Folding and binding cascades: Dynamic landscapes and population shifts. Protein Sci 9: 10-19.
30. Itoh K, Sasai M, (2011) Statistical mechanics of protein allostery: roles of backbone and side-chain structural fluctuations. J Chem Phys 134: 125102-125119.
31. Leach K, Sexton PM, Christopoulos A, (2007) Allosteric GPCR modulators: taking advantage of permissive receptor pharmacology. Trends Pharmacol Sci 28: 382-389.
32. Ehlert FJ, (2005) Analysis of allosterism in functional assays. J Pharmacol Exp Ther 315: 740-754.
33. Kenakin TP, (2009) '7TM receptor allostery: putting numbers to shapeshifting proteins. Trends Pharmacol Sci 30: 460-469.
34. Price MR, Baillie GL, Thomas A, Stevenson LA, Easson M, et al. (2005) Allosteric modulation of the cannabinoid CB1 receptor. Mol Pharmacol 68: 1484-1495.
35. May LT, Leach K, Sexton PM, Christopoulos A, (2007) Allosteric modulation of G protein-coupled receptors. Annu Rev Pharmacol Toxicol 47: 1-51.
36. Leff P, (1995) The two-state model of receptor activation. Trends Pharmacol Sci 16: 89-97.
37. Tsai CJ, Kumar S, Ma BY, Nussinov R, (1999) Folding funnels, binding funnels, and protein function. Protein Sci 8: 1181-1190.
38. Deupi X, Kobilka BK, (2010) Energy landscapes as a tool to integrate GPCR structure, dynamics, and function. Physiology 25: 293-303.
39. Yu EW, Koshland DE, (2001) Propagating conformational changes over long (and short) distances in proteins. Proc Natl Acad Sci U S A 98: 9517-9520.
40. Gardino AK, Kern D (2007) Functional dynamics of response regulators using NMR relaxation techniques. In: Simon MI, Crane BR, Crane A, editors. Two-component signaling systems, Pt B. pp. 149-165.
41. Palmer AG, Kroenke CD, Loria JP, (2001) Nuclear magnetic resonance methods for quantifying microsecond-to-millisecond motions in biological macromolecules. Methods Enzymol 339: 204-238.
42. Manley G, Loria JP, (2012) NMR insights into protein allostery. Arch Biochem Biophys 519: 223-231.
43. del Sol A, Tsai CJ, Ma BY, Nussinov R, (2009) The origin of allosteric functional modulation: multiple pre-existing pathways. Structure 17: 1042-1050.
44. Suel GM, Lockless SW, Wall MA, Ranganathan R, (2003) Evolutionarily conserved networks of residues mediate allosteric communication in proteins. Nat Struct Biol 10: 59-69.
45. Laine E, Auclair C, Tchertanov L, (2012) Allosteric communication across the native and mutated KIT receptor tyrosine kinase. PLoS Comput Biol 8: e1002661.
46. Weinkam P, Chen YC, Pons J, Sali A, (2013) Impact of mutations on the allosteric conformational equilibrium. J Mol Biol 425: 647-661.
47. Dixit A, Verkhivker GM, (2011) Computational modeling of allosteric communication reveals organizing principles of mutation-induced signaling in ABL and EGFR kinases. PLoS Comput Biol 7: e1002179.
48. Kaya C, Armutlulu A, Ekesan S, Haliloglu T, (2013) MCPath: Monte Carlo path generation approach to predict likely allosteric pathways and functional residues. Nucleic Acids Res 41: W249-W255.
49. Rodriguez GJ, Yao R, Lichtarge O, Wensel TG, (2010) Evolution-guided discovery and recoding of allosteric pathway specificity determinants in psychoactive bioamine receptors. Proc Natl Acad Sci U S A 107: 7787-7792.
50. Fischer S, Olsen KW, Nam K, Karplus M, (2011) Unsuspected pathway of the allosteric transition in hemoglobin. Proc Natl Acad Sci U S A 108: 5608-5613.
51. Atilgan AR, Turgut D, Atilgan C, (2007) Screened nonbonded interactions in native proteins manipulate optimal paths for robust residue communication. Biophys J 92: 3052-3062.
52. Mitternacht S, Berezovsky IN, (2011) Coherent conformational degrees of freedom as a structural basis for allosteric communication. PLoS Comput Biol 7: e1002301.
53. Selvaratnam R, Chowdhury S, VanSchouwen B, Melacini G, (2011) Mapping allostery through the covariance analysis of NMR chemical shifts. Proc Natl Acad Sci U S A 108: 6133-6138.
54. Neubig RR, Spedding M, Kenakin T, Christopoulos A, (2003) International Union of Pharmacology Committee on Receptor Nomenclature and Drug Classification. XXXVIII. Update on terms and symbols in quantitative pharmacology. Pharmacol Rev 55: 597-606.
55. Liu J, Nussinov R, (2008) Allosteric effects in the marginally stable von Hippel-Lindau tumor suppressor protein and allostery-based rescue mutant design. Proc Natl Acad Sci U S A 105: 901-906.
56. Reiter E, Ahn S, Shukla AK, Lefkowitz RJ, (2012) Molecular mechanism of beta-arrestin-biased agonism at seven-transmembrane receptors. Annu Rev Pharmacol Toxicol 52: 179-197.
57. Ehlert FJ, Roeske WR, Gee KW, Yamamura HI, (1983) An allosteric model for benzodiazepine receptor function. Biochem Pharmacol 32: 2375-2383.
58. Christopoulos A, (2002) Allosteric binding sites on cell-surface receptors: novel targets for drug discovery. Nat Revi Drug Discove 1: 198-210.
59. Stockton JM, Birdsall NJM, Burgen ASV, Hulme EC, (1983) Modification of the binding properties of muscarinic receptors by gallamine. Mol Pharmacol 23: 551-557.
60. Webby CJ, Jiao WT, Hutton RD, Blackmore NJ, Baker HM, et al. (2010) Synergistic allostery, a sophisticated regulatory network for the control of aromatic amino acid biosynthesis in mycobacterium tuberculosis. J Biol Chem 285: 30567-30576.
61. Hall DA, (2000) Modeling the functional effects of allosteric modulators at pharmacological receptors: an extension of the two-state model of receptor activation. Mol Pharmacol 58: 1412-1423.
62. Ehlert FJ, Griffin MT, (2008) Two-state models and the analysis of the allosteric effect of gallamine at the M-2 muscarinic receptor. J Pharmacol Exp Ther 325: 1039-1060.