Pressure-induced thermostabilization of glutamate dehydrogenase from the hyperthermophile Pyrococcus furiosus

Protein Science

Volumn 8, Issue 5, 1999, Pages 1056-1063

  Sun, Michael M C ^a   Tolliday, Nicola ^b   Vetriani, Costantino ^b   Robb, Frank T ^b   Clark, Douglas S ^a  

^a University of California   (United States)

^b UNIVERSITY OF MARYLAND BIOTECHNOLOGY INSTITUTE   (United States)

Author keywords

Electron spin resonance; Glutamate dehydrogenase; Glycerol; Pressure; Pyrococcus furiosus; Stability; Temperature

Indexed keywords

GLUTAMATE DEHYDROGENASE; GLYCEROL; RECOMBINANT ENZYME; TETRAPEPTIDE;

ARTICLE; ELECTRON SPIN RESONANCE; ENVIRONMENTAL TEMPERATURE; ENZYME ANALYSIS; HYPERBARISM; KINETICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN STRUCTURE; PYROCOCCUS FURIOSUS; STRUCTURE ANALYSIS; TEMPERATURE DEPENDENCE; THERMAL ANALYSIS; THERMOSTABILITY;

BACTERIA (MICROORGANISMS); PYROCOCCUS FURIOSUS;

EID: 0032926175     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.8.5.1056     Document Type: Article

References (61)

1. Back JF, Oakenfull D, Smith MB. 1979. Increased thermal stability of proteins in the presence of sugars and polyols. Biochemistry 18:5191-5196.
2. Balny C, Masson P, Travers F. 1989. Some recent aspects of the use of high-pressure for protein investigations in solution. High Press Res 2:1-28.
3. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254.
4. Britton KL, Baker PJ, Borges KMM, Engel PC, Pasquo A, Rice DW, Robb FT, Scandurra R, Stillman TJ, Yip KSP. 1995. Insights into thermal stability from a comparison of the glutamate dehydrogenases from Pyrococcus furiosus and Thermococcus litoralis. Eur J Biochem 229:688-695.
5. Butler SL, Falke JJ. 1996. Effects of protein stabilizing agents on thermal backbone motions: A disulfide trapping study. Biochemistry 35:10595-10600.
6. Calhoun DB, Englander SW. 1985. Internal protein motions, concentrated glycerol, and hydrogen exchange studied in myoglobin. Biochemistry 24:2095-2100.
7. Carreras CW, Naber N, Cooke R, Santi DV. 1994. A C-terminal conformational equilibrium in thymidylate synthase observed by electron paramagnetic resonance spectroscopy. Biochemistry 33:2011-2077.
8. Cioni P, Strambini GB. 1994. Pressure effects on protein flexibility monomeric proteins. J Mol Biol 242:291-301.
9. Cioni P, Strambini GB. 1996. Pressure effects on the structure of oligomeric proteins prior to subunit dissociation. J Mol Biol 263:789-799.
10. Consalvi V, Chiaraluce R, Politi L, Vaccaro R, De Rosa M, Scandurra R. 1991. Extremely thermostable glutamate dehydrogenase from the hyperthermophilic archaebacterium Pyrococcus furiosus. Eur J Biochem 202:1189-1196.
11. Cooper A. 1976. Thermodynamic fluctuations in protein molecules. Proc Natl Acad Sci USA 75:2740-2741.
12. Daniel RM, Dines M, Petach HH. 1996. The denaturation and degradation of stable enzymes at high temperatures. Biochem J 317:1-11.
13. Day MW, Hsu BT, Joshua-Tor L, Park JB, Zhou ZH, Adams MWW, Rees DC. 1992. X-ray crystal structures of the oxidized and reduced forms of the rubredoxin from the marine hyperthermophilic archaebacterium Pyrococcus furiosus. Protein Sci 1:1494-1507.
14. DiRuggiero J, Robb FT. 1995. Expression and in vitro assembly of recombinant glutamate dehydrogenase from the hyperthermophilic archaeon Pyrococcus furiosus. Appl Environ Microbiol 61:159-164.
15. Eggen RIL, Geerling ACM, Waldkotter K, Antranikian G, de Vos WM. 1993. The glutamate dehydrogenase-encoding gene of the hyperthermophilic archaeon Pyrococcus furiosus: Sequence, transcription, and analysis of the deduced amino acid sequence. Gene 132:143-148.
16. Eriksson AE, Baase WA, Wozniak JA, Matthews BW. 1992a. A cavity-containing mutant of T4 lysozyme is stabilized by buried benzene. Nature 355:371-373.
17. Eriksson AE, Baase WA, Zhang XJ, Heinz DW, Blaber M, Baldwin EP, Matthews BW. 1992b. Response of a protein structure to cavity-creating mutations and its relation to the hydrophobic effect. Science 255:178-183.
18. Fiala G, Stetter KO. 1986. Pyrococcus furiosus sp. nov. represents a novel genus of marine heterotrophic archaebacteria growing optimally at 100°C. Arch Microbiol 145:56-61.
19. Frauenfelder H, Alberding NA, Ansari A, Braunstein D, Cowen BR. 1990. Protein and pressures. J Phys Chem 94:1024-1037.
20. Gekko K, Hasegawa Y. 1986. Compressibility-structure relationship of globular proteins. Biochemistry 25:6563-6571.
21. Gekko K, Hasegawa Y. 1989. Effect of temperature on the compressibility of native globular proteins. J Phys Chem 93:426-429.
22. Gekko K, Timasheff SN. 1981a. Mechanism of protein stabilization by glycerol: Preferential hydration in glycerol-water mixtures. Biochemistry 20:4667-4676.
23. Gekko K, Timasheff SN. 1981b. Thermodynamic and kinetic examination of protein stabilization by glycerol. Biochemistry 20:4677-4686.
24. Gekko K, Yamagami K. 1991. Flexibility of food proteins as revealed by compressibility. J Agric Food Chem 59:57-62.
25. Gregory RB. 1988. The influence of glycerol on hydrogen isotope exchange in lysozyme. Biopolymers 27:1699-1709.
26. Gross M, Auerbach G, Jaenicke R. 1993. The catalytic activities of monomeric enzymes show complex pressure dependence. FEBS Lett 527:256-260.
27. Gross M, Jaenicke R. 1994. Proteins under pressure. The influence of high hydrostatic pressure on structure, function and assembly of proteins and protein complexes. Eur J Biochem 221:617-630.
28. Hei DJ, Clark DS. 1994. Pressure stabilization of proteins from extreme thermophiles. Appl Environ Microbiol 60:932-939.
29. Hennig M, Sterner R, Kirschner K, Jansonius JN. 1997. Crystal structure at 2.0 Å resolution of phosphoribosyl anthranilate isomerase from the hyperthermophile Thermotoga maritima: Possible determinants of protein stability. Biochemistry 36:6009-6016.
30. Heremans L, Heremans K. 1989a. Pressure effects of the Raman spectrum of proteins: Stability of the salt bridge in trypsin and elastase. J Mol Struct 214:305-314.
31. Heremans L, Heremans K. 1989b. Raman spectroscopy study of the changes in secondary structure of chymotrypsin: Effect of pH and pressure on the salt bridge. Biochim Biophys Acta 999:192-197.
32. Hubbard SJ, Gross KH, Argos P. 1994. Intramolecular cavities in globular proteins. Protein Eng 7:613-626.
33. Jaenicke R. 1991. Protein stability and molecular adaption to extreme conditions. Eur J Biochem 202:715-728.
34. Kellis JT Jr, Nyberg K, Fersht AR. 1989. Energetics of complementary side-chain packing in a protein hydrophobic core. Biochemistry 28:4914-4922.
35. Kellis JT Jr, Nyberg K, Sali D, Fersht AR. 1988. Contribution of hydrophobic interactions to protein stability. Nature 555:784-786.
36. Klump H, DiRuggiero J, Kessel M, Park JB, Adams MWW, Robb FT. 1992. Glutamate dehydrogenase from the hyperthermophile Pyrococcus furiosus. J Biol Chem 267:22681-22685.
37. Kyte J, Doolittle RF. 1982. A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105-132.
38. Macedo-Ribeiro S, Darimont B, Reinhard S, Huber R. 1996. Small structural changes account for the high thermostability of 1[4Fe-4S] ferrodoxin from the hyperthermophilic bacterium Thermotoga maritima. Structure 4:1291-1301.
39. Mchaourab HS, Lietzow MA, Kalman H, Hubbell WL. 1996. Motion of spinlabeled side-chains in T4 lysozyme: Correlation with protein structure and dynamics. Biochemistry 35:7692-7704.
40. Michels PC, Clark DS. 1992. Pressure dependence of enzyme catalysis. In: Adams MWW, Kelly RM, eds. Biocatalysis at extreme temperatures. Washington, DC: American Chemical Society, pp 1088-1121.
41. Michels PC, Clark DS. 1997. Pressure enhanced activity and stability of a hyperthermophilic protease from a deep-sea methanogen. Appl Environ Microbiol 63:3985-3991.
42. Michels PC, Hei D, Clark DS. 1996. Pressure effects on enzyme activity and stability at high temperatures. Adv Protein Chem 48:341-376.
43. Mozhaev VV, Lange R, Kudryashova EV, Balny C. 1996. Application of high hydrostatic pressure for increasing activity and stability of enzymes. Biotechnol Bioeng 52:320-331.
44. Pakula AA, Sauer RT. 1989. Genetic analysis of protein stability and function. Ann Rev Genet 23:289-310.
45. Priev A, Almagor A, Yedgar S, Gavish B. 1996. Glycerol decreases the volume and compressibility of protein interior. Biochemistry 35:2061-2066.
46. Qu K, Vaughn JL, Sienkiewicz A, Scholes CP, Fetrow JS. 1997. Kinetics and motional dynamics of spin-labeled yeast iso-1-cytochrome c: Stopped-flow electron paramagnetic resonance as a probe for protein folding/unfolding of the C-terminal helix spin-labeled at cysteine 102. Biochemistry 36:2884-2897.
47. Robb FT, Maeder DL. 1998. Novel evolutionary histories and adaptive features of proteins from hyperthermophiles. Curr Op Biotech 9:288-291.
48. Robb FT, Park JB, Adams MWW. 1992. Characterization of an extremely thermostable glutamate dehydrogenase: A key enzyme in the primary metabolism of the hyperthermophilic archaebacterium Pyrococcus furiosus. Biochim Biophy Acta 1120:267-272.
49. Russell RJM, Ferguson JMC, Hough DW, Danson MJ, Taylor GL. 1997. The crystal structure of citrate synthase from the hyperthermophilic archaeon Pyrococcus furiosus at 1.9 Å. Biochemistry 36:9983-9994.
50. Samarasighe SD, Campbell DM, Jonas A, Jonas J. 1992. High resolution NMR study of the pressure-induced unfolding of lysozyme. Biochemistry 31:7773-7778.
51. Schreier S, Polnaszek CF, Smith ICP. 1978. Spin labels in membranes: Problems in practice. Biochim Biophys Acta 515:375-436.
52. Singh N, Liu Z, Fisher HF. 1996. The existence of a hexameric intermediate with molten-globule-like properties in the thermal denaturation of bovine-liver glutamate dehydrogenase. Biophys Chem 63:27-36.
53. Teller JK, Smith RJ, McPherson MJ, Engel PC, Guest JR. 1992. The glutamate dehydrogenase gene of Clostridium symbiosum. Eur J Biochem 206:151-159.
54. Timasheff SN. 1993. The control of protein stability and association by weak interactions with water: How do solvents affect these processes? Annu Rev Biophys Biomol Struct 22:67-97.
55. Timasheff SN, Arakawa T. 1997. Stabilization of protein structure by solvents. In: Creighton TE, ed. Protein structure: A practical approach. Oxford, UK: Oxford University Press, pp 349-364.
56. Vetriani C, Maeder DL, Tolliday N, Yip K-S, Stillman TJ, Britton KL, Rice D, Klump HH, Robb FT. 1998. Protein thermostability above 100̊C: A key role for ionic interactions. Proc Natl Acad Sci USA 95:12300-12305.
57. Vihinen M. 1987. Relationship of protein flexibility to thermostability. Protein Eng 1:477-480.
58. Wang A, Robertson AD, Bolen DW. 1995. Effects of a naturally occurring compatible osmolyte on the internal dynamics of ribonuclease A. Biochemisny 34:15096-15104.
59. Weber G, Drickamer HG. 1983. The effect of high pressure upon proteins and other biomolecules. Quat Rev Biophys 16:89-112.
60. Yip KSP, Britton KL, Stillman TJ, Lebbink J, De Vos WM, Robb FT, Vetriani C, Maeder D, Rice DW. 1998. Insights into the molecular basis of thermal stability from the analysis of ion-pair networks in the glutamate dehydrogenase family. Eur J Biochem 255:336-346.
61. Yip KSP, Stillman TJ, Britton KL, Artymiuk PJ, Baker PJ, Sedelnikova SE, Engel PC, Pasquo A, Chiaraluce R, Consalvi V. 1995. The structure of Pyrococcus furiosus glutamate dehydrogenase reveals a key role for ion-pair networks in maintaining enzyme stability at extreme temperatures. Structure 3:1147-1158.