Ligand-induced changes in the conformational stability and flexibility of glutamate dehydrogenase and their role in catalysis and regulation

Protein Science

Volumn 19, Issue 10, 2010, Pages 1820-1829

  Wacker, Sarah A ^a   Bradley, Michael J ^b   Marion, Jimmy ^a   Bell, Ellis ^a  

^a UNIVERSITY OF RICHMOND   (United States)

^b GUSTAVUS ADOLPHUS COLLEGE   (United States)

Author keywords

Allosteric regulation; Glutamate dehydrogenase; Ligand induced changes; Local flexibility; Protein stability

Indexed keywords

GLUTAMATE DEHYDROGENASE; GLUTAMIC ACID; GUANIDINE; NORVALINE; TRYPSIN;

ALLOSTERISM; ARTICLE; CATALYSIS; CONFORMATIONAL TRANSITION; ENZYME KINETICS; ENZYME REGULATION; ENZYME STABILITY; PRIORITY JOURNAL;

ALLOSTERIC REGULATION; ANIMALS; BIOCATALYSIS; CALORIMETRY, DIFFERENTIAL SCANNING; CATTLE; CIRCULAR DICHROISM; ENZYME ACTIVATION; ENZYME STABILITY; GLUTAMATE DEHYDROGENASE; GLUTAMIC ACID; GUANIDINE; HOT TEMPERATURE; KINETICS; LIGANDS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; SUBSTRATE SPECIFICITY; VALINE;

BOVINAE;

EID: 77957295549     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.459     Document Type: Article

References (44)

1. Monod J, Wyman J, Changeux JP (1965) On the nature of allosteric transitions: a plausible model. J Mol Biol 12:88-118.
2. Koshland DE, Nemethy G, Filmer D (1966) Comparison of experimental binding data and theoretical models in proteins containing subunits. Biochemistry 5:365-385.
3. Dalziel K, Engel PC (1968) Antagonists homotropic interactions as a possible explanation of coenzyme activation of glutamate dehydrogenase. FEBS Lett 1:349-352.
4. Weber G (1972) Ligand binding and internal equilibria in proteins. Biochemistry 11:864-878.
5. Lakowicz JR, Weber G (1973) Quenching of fluorescence by oxygen: a probe for structural fluctuations in macromolecules. Biochemistry 12:4161-4170.
6. +. Biochim Biophys Acta 309:237-242.
7. Boyer PD (1998) A perspective of the binding change mechanism for ATP synthesis. FASEB J 3:2164-2178.
8. Ma J, Flynn TC, Cui Q, Leslie AG, Walker JE, Karplus M (2002) A dynamic analysis of the rotation mechanism for conformational change in F(1)-ATPase. Structure 10:921-931.
9. Beernink PT, Endrizzi JA, Alber T, Schachman HK (1999) Assessment of the allosteric mechanism of aspartate transcarbamoylase based on the crystalline structure of the unregulated catalytic subunit. Proc Natl Acad Sci USA 96:5388-5393. (Pubitemid 29234627)
10. 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 induced cell migration. Proc Natl Acad Sci USA 97:5077-5082. (Pubitemid 30313674)
11. Liang ZX, Lee T, Resing KA, Ahn NG, Klinman JP (2004) Thermal-activated protein mobility and its correlation with catalysis in thermophilic alcohol dehydrogenase. Proc Natl Acad Sci USA 101:9556-9561. (Pubitemid 38869274)
12. Ceccarelli C, Liang ZX, Strickler M, Prehna G, Goldstein BM, Klinman JP, Bahnson BJ (2004) Crystal structure and amide H/D exchange of binary complexes of alcohol dehydrogenase from Bacillus stearothermophilus: insight into thermostability and cofactor binding. Biochemistry 43:5266-5277. (Pubitemid 38620918)
13. Knapp MJ, Klinman JP (2002) Environmentally coupled hydrogen tunneling: linking catalysis to dynamics. Eur J Biochem 269:3113-3121.
14. Kohen A, Cannio, R, Bartolucci, S, Klinman JP (1999) Enzyme dynamics and hydrogen tunnelling in a thermophilic alcohol dehydrogenase. Nature 399:496-499.
15. Alhambra C, Corchado JC, Sanchez ML, Gao J, Truhlar DG (2000) Quantum dynamics of hydride transfer in enzyme catalysis. J Am Chem Soc 122:8197-8203.
16. Kraut DA, Carroll KS, Herschlag D (2003) Challenges in enzyme mechanism and energetics. Ann Rev Biochem 72:517-571.
17. Kern D, Zuiderweg ERP (2003) The role of dynamics in allosteric regulation. Curr Opin Struct Biol 13:748-757.
18. Swain JF, Gierasch LM (2006) The changing landscape of protein allostery. Curr Opin Struct Biol 16:102-108.
19. Benkovic SJ, Hammes-Schiffer S (2003) A perspective on enzyme catalysis. Science 301:1196-1202.
20. Vendruscolo M, Dobson CM (2006) Structural biology. Dynamic visions of enzymatic reactions. Science 313:1586-1587.
21. Hammes-Schiffer S, Benkovic SJ (2006) Relating protein motion to catalysis. Annu Rev Biochem 75:519-541.
22. Henzler-Wildman K, Kern D (2007) Dynamic personalities of proteins. Nature 450:964-972.
23. Karplus M, Kuriyan J (2005) Molecular dynamics and protein function. Proc Natl Acad Sci USA 102:6679-6685.
24. Thompson JR, Bell JK, Bratt J, Grant GA, Banaszak L (2005) Vmax regulation through domain and subunit changes. The active form of phosphoglycerate dehydrogenase. Biochemistry 44:5763-5773.
25. Kaplan NO, Ciotti MM, Stolzenbach FE (1956) Reaction of pyridine nucleotide analogues with dehydrogenases. J Biol Chem 221:833-841.
26. Appella E, Tomkins GM (1966) The subunits of bovine liver glutamate dehydrogenase: demonstration of a single peptide chain. J Biol Chem 18:77-89.
27. Alex S, Bell JE (1980) Dual nucleotide specificity of bovine glutamate dehydrogenase: the role of negative cooperativity. Biochem J 191:299-304.
28. Bell ET, LiMuti C, Renz CL, Bell JE (1985) Negative co-operativity in glutamate dehydrogenase: involvement of the 2-position in glutamate in the induction of conformational changes. Biochem J 225:209-217.
29. LiMuti C, Bell JE (1983) A steady-state random-order mechanism for the oxidative deamination of norvaline by glutamate dehydrogenase. Biochem J 211:99-107.
30. Bell ET, Bell JE (1984) Catalytic activity of bovine glutamate dehydrogenase requires a hexamer structure. Biochem J 217:327-330.
31. Frieden C (1965) Glutamate dehydrogenase VI: survey of purine nucleotide and other effects on the enzyme from various sources. J Biol Chem 240:2028-2037.
32. Bailey J, Bell ET, Bell JE (1982) Regulation of bovine glutamate dehydrogenase: the effects of pH and ADP. J Biol Chem 247:5579-5583.
33. Peterson PE, Smith TJ (1999) The structure of bovine glutamate dehydrogenase provides insights into the mechanism of allostery. Struct Fold Des 7:769-782.
34. Smith TJ, Peterson PE, Schmidt T, Fang J, Stanley CA (2001) Structures of bovine glutamate dehydrogenase complexes elucidate the mechanism of purine regulation. J Mol Biol 307:707-720.
35. Smith TJ, Schmidt T, Fang J, Wu J, Siuzdak G, Stanley CA (2002) The structure of apo human glutamate dehydrogenase details subunit communication and allostery. J Mol Biol 318:765-777.
36. MacMullen C, Fang J, Hsu BY, Kelly A, de Lonlay-Debeney P, Saudubray JM, Ganguly A, Smith TJ, Stanley CA (2001) Hyperinsulinism/hyperammonemia syndrome in children with regulatory mutations in the inhibitory guanosine triphosphate-binding domain of glutamate dehydrogenase. J Clin Endocrinol Metab 86:1782-1787. (Pubitemid 32374938)
37. Fang J, Hsu BY, MacMullen CM, Poncz M, Smith TJ, Stanley CA (2002) Expression, purification and characterization of human glutamate dehydrogenase (GDH) allosteric regulatory mutations. Biochem J 363:81-87. (Pubitemid 34280615)
38. Fisher HF, Bard JR, Prough RA (1970) Transient-state intermediates involved in the hydride transfer step of the glutamate dehydrogenase reaction. Biochem Biophys Res Commun 41:601-607.
39. Engel PC, Dalziel K (1969) Kinetic studies of glutamate dehydrogenase with glutamate and norvaline as substrates. Biochem J 115:621-631.
40. Tashiro R, Inoue T, Shimozawa R (1982) Subunit dissociation and unfolding of bovine liver glutamate dehydrogenase induced by guanidine. Biochim Biophys Acta 706:129-135.
41. Dalziel K, Egan RR (1972) The binding of oxidized coenzymes by glutamate dehydrogenase and the effects of glutarate and purine nucleotides. Biochem J 126:975-984.
42. Rife JE, Cleland WW (1980) Kinetic mechanism of glutamate dehydrogenase. Biochemistry 19:2321-2328.
43. Hartshorn SR, Shiner VJ, Jr (1972) Calculation of H/D carbon-12/carbon-13, and carbon-12/carbon-14 fractionation factors from valence force fields derived for a series of simple organic molecules. J Am Chem Soc 94:9002-9012.
44. Schimerlik MI, Rife JE, Cleland WW (1972) Equilibrium perturbation by isotope substitution. Biochemistry 14:5347-5354.