Rational modulation of conformational fluctuations in adenylate kinase reveals a local unfolding mechanism for allostery and functional adaptation in proteins

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 40, 2009, Pages 16984-16989

  Schrank, Travis P ^a,b   Bolen, D Wayne ^a   Hilser, Vincent J ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

^b W M Keck Center for Computational and Structural Biology   (United States)

Author keywords

Dynamics; Isothermal titration calorimetry; Native state ensemble; Thermodynamics

Indexed keywords

ADENYLATE KINASE; GLYCINE; PROTEIN;

ADAPTATION; ALLOSTERISM; ARTICLE; BINDING AFFINITY; CONFORMATION; CONTROLLED STUDY; ENZYME BINDING; ESCHERICHIA COLI; MODULATION; MUTATION; NONHUMAN; PRIORITY JOURNAL; SURFACE PROPERTY; TEMPERATURE ACCLIMATIZATION; X RAY CRYSTALLOGRAPHY;

ADENYLATE KINASE; ALGORITHMS; ALLOSTERIC REGULATION; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; MUTATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; STRUCTURE-ACTIVITY RELATIONSHIP; THERMODYNAMICS;

ESCHERICHIA COLI;

EID: 70350131719     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0906510106     Document Type: Article

References (29)

1. Hvidt A, Linderstrom-Lang K (1954) Exchange of hydrogen atoms in insulin with deuterium atoms in aqueous solutions. Biochim Biophys Acta 14:574-575.
2. Henzler-Wildman KA, et al. (2007) A hierarchy of timescales in protein dynamics is linked to enzyme catalysis. Nature 450:913-916.
3. Frederick KK, Marlow MS, Valentine KG, Wand AJ (2007) Conformational entropy in molecular recognition by proteins. Nature 448:325-329.
4. Popovych N, Sun S, Ebright RH, Kalodimos CG (2006) Dynamically driven protein allostery. Nat Struct Mol Biol 13:831-838.
5. Feller G, Gerday C (2003) Psychrophilic enzymes: Hot topics in cold adaptation. Nat Rev Microbiol 1:200-208.
6. Fields PA, Somero GN (1998) Hot spots in cold adaptation: localized increases in conformational flexibility in lactate dehydrogenase A4 orthologs of Antarctic noto-thenioid fishes. Proc Natl Acad Sci USA 95:11476-11481.
7. Shapiro YE, Sinev MA, Sineva EV, Tugarinov V, Meirovitch E (2000) Backbone dynamics of escherichia coli adenylate kinase at the extreme stages of the catalytic cycle studied by (15)N NMR relaxation. Biochemistry 39:6634-6644. (Pubitemid 30353995)
8. Wolf-Watz M, et al. (2004) Linkage between dynamics and catalysis in a thermophilic-mesophilic enzyme pair. Nat Struct Mol Biol 11:945-949. (Pubitemid 39315297)
9. Hanson JA, et al. (2007) Illuminating the mechanistic roles of enzyme conformational dynamics. Proc Natl Acad Sci USA 104:18055-18060.
10. Müller CW, Schulz GE (1992) Structure of the complex between adenylate kinase from Escherichia coli and the inhibitor Ap5A refined at 1.9 A resolution. A model for a catalytic transition state. J Mol Biol 224:159-177.
11. Müller CW, Schlauderer GJ, Reinstein J, Schulz GE (1996) Adenylate kinase motions during catalysis: an energetic counterweight balancing substrate binding. Structure 4:147-156. (Pubitemid 126658978)
12. Rundqvist L, et al. (2009) Noncooperative folding of subdomains in adenylate kinase. Biochemistry 48:1911-1927.
13. D'Aquino JA, et al. (1996) The magnitude of the backbone conformational entropy change in protein folding. Proteins 25:143-156.
14. Adén J, Wolf-Watz M (2007) NMR identification of transient complexes critical to adenylate kinase catalysis. J Am Chem Soc 129:14003-14012. (Pubitemid 350106092)
15. Eftink MR, Anusiem AC, Biltonen RL (1983) Enthalpy-entropy compensation and heat capacity changes for protein-ligand interactions: general thermodynamic models and data for the binding of nucleotides to ribonuclease A. Biochemistry 22:3884-3896.
16. Lumry R, Biltonen R (1966) Validity of the "two-state" hypothesis for conformational transitions of proteins. Biopolymers 4:917-944.
17. Pan H, Lee JC, Hilser VJ (2000) Binding sites in Escherichia coli dihydrofolate reductase communicate by modulating the conformational ensemble. Proc Natl Acad Sci USA 97:12020-12025. (Pubitemid 30815131)
18. Cooper A, Dryden DT (1984) Allostery without conformational change. A plausible model. Eur Biophys J 11:103-109.
19. Hilser VJ, Freire E (1996) Structure-based calculation of the equilibrium folding pathway of proteins. Correlation with hydrogen exchange protection factors. J Mol Biol 262:756-772.
20. Arora K, Brooks CL (2007) Large-scale allosteric conformational transitions of adenylate kinase appear to involve a population-shift mechanism. Proc Natl Acad Sci USA 104:18496-18501. (Pubitemid 350210725)
21. Whitford PC, Miyashita O, Levy Y, Onuchic JN (2007) Conformational transitions of adenylate kinase: switching by cracking. J Mol Biol 366:1661-1671. (Pubitemid 46215597)
22. Bae E, Phillips GN (2006) Roles of static and dynamic domains in stability and catalysis of adenylate kinase. Proc Natl Acad Sci USA 103:2132-2137. (Pubitemid 43271635)
23. Deng H, et al. (1994) Source of catalysis in the lactate dehydrogenase system. Ground-state interactions in the enzyme-substrate complex. Biochemistry 33:2297-2305. (Pubitemid 24099631)
24. Aghajari N, Feller G, Gerday C, Haser R (1998) Structures of the psychrophilic Alteromonas haloplanctis α-amylase give insights into cold adaptation at a molecular level. Structure 6:1503-1516. (Pubitemid 29000528)
25. Závodszky P, Kardos J, Svingor, Petsko GA(1998) Adjustment of conformational flexibility is a key event in the thermal adaptation of proteins. Proc Natl Acad Sci USA 95:7406-7411.
26. Röthlisberger D, et al. (2008) Kemp elimination catalysts by computational enzyme design. Nature 453:190-195. (Pubitemid 351667979)
27. Sinev MA, Sineva EV, Ittah V, Haas E (1996) Domain closure in adenylate kinase. Biochemistry 35:6425-6437.
28. Reinstein J, Brune M, Wittinghofer A (1988) Mutations in the nucleotide binding loop of adenylate kinase of Escherichia coli. Biochemistry 27:4712-4720.
29. Burlacu-Miron S, Gilles AM, Popescu A, Bârzu O, Craescu CT (1999) Multinuclear magnetic resonance studies of Escherichia coli adenylate kinase in free and bound forms. Resonance assignment, secondary structure and ligand binding. Eur J Biochem 264:765-774. (Pubitemid 29437205)