Engineering activity and stability of Thermotoga maritima glutamate dehydrogenase. I. Introduction of a six-residue ion-pair network in the hinge region

Journal of Molecular Biology

Volumn 280, Issue 2, 1998, Pages 287-296

  Lebbink, Joyce H G ^a   Knapp, Stefan ^b   Van Der Oost, John ^a   Rice, David ^c   Ladenstein, Rudolf ^b   De Vos, Willem M ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b KAROLINSKA INSTITUTE   (Sweden)

^c UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Glutamate dehydrogenase; Hinge ion pair networks; Pyrococcus furiosus; Thermostability; Thermotoga maritima

Indexed keywords

GLUTAMATE DEHYDROGENASE; GUANIDINE;

ARTICLE; DIFFERENTIAL SCANNING CALORIMETRY; ENZYME CONFORMATION; ENZYME STABILITY; GENETIC ENGINEERING; NONHUMAN; PRIORITY JOURNAL; PYROCOCCUS; SITE DIRECTED MUTAGENESIS; TEMPERATURE; THERMOPHILIC BACTERIUM;

EID: 0032504088     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1998.1870     Document Type: Article

References (33)

1. Bacon D.J., Anderson W.F. A fast algorithm for rendering space-filling molecule pictures. J. Mol. Graph. 6:1988;219-220
2. Baker P.J., Britton K.L., Engel P.C., Farrants G.W., Lilley K.S., Rice D.W., Stillman T.J. Subunit assembly and active site location in the structure of glutamate dehydrogenase. Proteins: Struct. Funct. Genet. 12:1992;75-86
3. Britton K.L., Baker P.J., Borges K.M.M., Engel P.C., Pasquo A., Rice D.W., Robb F.T., Scandurra R., Stillman T.J., Yip K.S.P. Insights into thermal stability from a comparison of the glutamate dehydrogenase from Pyrococcus furiosus andThermococcus litoralis. Eur. J. Biochem. 229:1995;688-695
4. Brünger A.T. X-PLOR (Version 3.1) Manual. 1992;Yale University Press, New Haven and London
5. Dao-pin S., Sauer U., Nicholson H., Matthews B.W. Contributions of engineered surface salt bridges to the stability of T4 lysozyme determined by directed mutagenesis. Biochemistry. 30:1991;7142-7153
6. Eggen R.I.L., Geerling A.C.M., Waldkötter K., Antranikian G., de Vos W.M. The glutamate dehydrogenase-encoding gene of the hyperthermophilic archaeon Pyrococcus furiosus sequence, transcription and analysis of the deduced amino acid sequence. Gene. 132:1993;143-148
7. Engh R.H., Huber R. Accurate bond and angle parameters for X-ray protein structure refinement. Acta Crystallog. sect A. 47:1991;392-400
8. Fiala G., Stetter K.O. Pyrococcus furiosus sp. nov. represents a novel genus of marine heterotrophic archaebacteria growing optimally at 100°C. Arch. Microbiol. 145:1986;56-61
9. Gibson T.J. PhD thesis. 1984;Cambridge University, Cambridge
10. Gill S.C., von Hippel P.H. Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem. 182:1989;319-326
11. Hennig M., Darimont B., Sterner R., Kirschner K., Jansonius J.N. 2.0 Å structure of indole-3-glycerol phosphate synthase from the hyperthermophile Sulfolobus solfataricus possible determinants of protein stability. Structure. 3:1995;1295-1306
12. Hennig M., Sterner R., Kirschner K., Jansonius J.N. Crystal structure at 2.0 Å resolution of phosphoribosyl anthranilate isomerase from the hyperthermophile Thermotoga maritima possible determinants of protein stability. Biochemistry. 36:1997;6009-6016
13. Horovitz A., Serrano L., Avron B., Bycroft M., Fersht A.R. Strength and cooperativity of contributions of surface salt bridges to protein stability. J. Mol. Biol. 216:1990;1031-1044
14. Klump H., Di Ruggiero J., Kessel M., Park J-B., Adams M.W.W., Robb F.T. Glutamate dehydrogenase from the hyperthermophile Pyrococcus furiosus. Thermal denaturation and activation. J. Biol. Chem. 267:1992;22681-22685
15. Knapp S., de Vos W.M., Rice D.W., Ladenstein R. Crystal structure of glutamate dehydrogenase from the hyperthermophilic eubacterium Thermotoga maritima at 3.0 Å resolution. J. Mol. Biol. 267:1997;916-932
16. Korndörfer I., Steipe B., Huber R., Tomschy A., Jaenicke R. The crystal structure of holo-glyceraldehyde-3-phosphate dehydrogenase from the hyperthermophilic bacteriumThermotoga maritima at 2.5 Å resolution structural basis for thermostability. J. Mol. Biol. 246:1995;511-521
17. Kort R., Liebl W., Labedan B., Forterre P., Eggen R.I.L., de Vos W.M. Glutamate dehydrogenase from the hyperthermophilic bacterium Thermotoga maritima molecular characterization and phylogenetic implications. Extremophiles. 1:1997;52-60
18. Kraulis P.J. MOLSCRIPT a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24:1991;946-950
19. Kuipers O.P., Boot H.J., de Vos W.M. Improved site-directed mutagenesis method using PCR. Nucl. Acids Res. 19:1991;4558
20. Landt O., Grunert H., Hahn U. A general method for rapid site-directed mutagenesis using the polymerase chain reaction. Gene. 96:1990;125-128
21. Lebbink J.H.G., Eggen R.I.L., Geerling A.C.M., Consalvi V., Chiaraluce R., Scandurra R., de Vos W.M. Exchange of domains of glutamate dehydrogenase from the hyperthermophilic archaeon Pyrococcus furiosus and the mesophilic bacterium Clostridium difficile effects on catalysis, thermoactivity and stability. Protein Eng. 8:1995;1287-1294
22. Mead D.A., Szczesna-Skorupa E., Kemper B. Single-stranded DNA "blue" T7 promoter plasmids a versatile tandem promoter system for cloning and protein engineering. Protein Eng. 1:1986;67-74
23. Merrit E.A., Murphy M.E.P. Raster 3D version 2.0 a program for photorealistic molecular graphics. Acta Crystallog. sect. D. 50:1994;869-873
24. Neuner A., Yannasch H., Bellun S., Stetter K.O. Thermococcus litoralis sp. nov. a new species of extremely thermophilic marine archaebacteria. Arch. Microbiol. 153:1990;205-207
25. Pappenberger G., Schurig H., Jaenicke R. Disruption of an ionic network leads to accelerated thermal denaturation of D-glyceraldehyde-3-phosphate dehydrogenase from the hyperthermophilic bacterium Thermotoga maritima. J. Mol. Biol. 274:1997;676-683
26. Russell R.J.M., Ferguson J.M.C., Hough D.W., Danson M.J., Taylor G.L. The crystal structure of citrate synthase from the hyperthermophilic archaeon Pyrococcus furiosus at 1.9 Å resolution. Biochemistry. 36:1997;9983-9994
27. Spassov V.Z., Atanasov B.P. Spatial optimization of electrostatic interactions between the ionized groups in globular proteins. Protein Struct. Funct. Genet. 19:1994;222-229
28. Spassov V.Z., Karshikoff A.D., Ladenstein R. The optimization of protein-solvent interactions thermostability and the role of hydrophobic and electrostatic interactions. Protein Sci. 4:1995;1516-1527
29. Stillman T.J., Baker P.J., Britton K.L., Rice D.W. Conformational flexibility in glutamate dehydrogenase. The role of water in substrate recognition and catalysis. J. Mol. Biol. 234:1993;1131-1139
30. Tomschy A., Böhm G., Jaenicke R. The effect of ion-pairs on the thermal stability of D-glyceraldehyde-3-phosphate dehydrogenase from the hyperthermophilic bacterium Thermotoga maritima. Protein Eng. 7:1994;1471-1478
31. Turk D. PhD thesis. 1992;Technical University, München
32. Yip K.S.P., Stillman T.J., Britton K.L., Artymiuk P.J., Baker P.J., Sedelnikova S.E., Engel P.C., Pasquo A., Chiaraluce R., Consalvi R., Scandurra R., Rice D.W. The structure of Pyrococcus furiosus glutamate dehydrogenase reveals a key role for ion-pair networks in maintaining enzyme stability at extreme temperatures. Structure. 3:1995;1147-1158
33. Yip K.S.P., Britton K.L., Stillman T.J., Lebbink J.H.G., de Vos W.M., Robb F.T., Rice D.W. Insights into the molecular basis of thermostability from the analysis of ion-pair networks in the glutamate dehydrogenase family. Eur. J. Biochem. 1998;. In the press