Insights into the molecular basis of thermal stability from the structure determination of Pyrococcus furiosus glutamate dehydrogenase

FEMS Microbiology Reviews

Volumn 18, Issue 2-3, 1996, Pages 105-117

  Rice, D W ^a   Yip, K S P ^a   Stillman, T J ^a   Britton, K L ^a   Fuentes, A ^b   Connerton, I ^b   Pasquo, A ^c   Scandurra, R ^c   Engel, P C ^d  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b INSTITUTE OF FOOD RESEARCH   (United Kingdom)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Archaea; Glutamate dehydrogenase; Hyperthermophile; Ion pair network; Pytococcus furiosus; Thermal stability; X ray crystallography

Indexed keywords

GLUTAMATE DEHYDROGENASE;

CONFERENCE PAPER; ENZYME STABILITY; ENZYME STRUCTURE; NONHUMAN; PROTEIN FOLDING; PYROCOCCUS; THERMOPHILIC BACTERIUM;

ARCHAEA; BACTERIA (MICROORGANISMS); CLOSTRIDIUM; ESCHERICHIA COLI; NEUROSPORA CRASSA; PYROCOCCUS; PYROCOCCUS FURIOSUS;

EID: 0029993239     PISSN: 01686445     EISSN: None     Source Type: Journal    
DOI: 10.1016/0168-6445(96)00005-8     Document Type: Conference Paper

References (43)

1. Flam, F. (1994) The chemistry of life at the margins. Science 265, 471-472.
2. Maras, B., Consalvi, V., Chiaraluce, R., Politi, L., De Rosa, M., Bossa, F., Scandurra, R. and Barra, D. (1992) The protein sequence of glutamate dehydrogenase from Sulfulobus solfataricus, a thermoacidophilic archaebacterium. Eur. J. Biochem. 203, 81-87.
3. DiRuggiero, J. Robb, F.T., Jagus, R., Klump, H.H., Borges, K.M., Kessel, M. Mai, X. and Adams, M.W.W. (1993) Characterization, cloning and in vitro expression of the extremely thermostable glutamate dehydrogenase from the archaeon, ES4. J. Biol. Chem. 268, 17767-17774.
4. Ohshima, T. and Nishida, N. (1993) Purification and properties of extremely thermostable glutamate dehydrogenases from two hyperthermophilic Archaebacteria Pyrococcus woesei and Pyrococcus furiosus. Biosci. Biotech. Biochem. 57, 945-951.
5. Smith, E.L., Austen, B.M., Blumenthal, K.M. and Nyc, J.F. (1975) Glutamate dehydrogenases. In: The Enzymes (3rd Edn.) (Boyer, P.D. Ed.), Vol. 11, pp. 293-367, Academic Press, New York.
6. Baker, P.J., Britton, K.L., Engel, P.C., Farrants, G.W., Lilley, K.S., Rice, D.W. and Stillman, T.J. (1992) Subunit assembly and active site location in the structure of glutamate dehydrogenase. Proteins: Structure, Function and Genetics 12, 75-86.
7. Teller, J.K., Smith, R.M., McPherson, M.J., Engel, P.C. and Guest, J.R. (1992) The glutamate dehydrogenase gene of Clostridium symbiosum - cloning by polymerase chain reaction, sequence analysis and over-expression in Escherichia coli. Eur. J. Biochem. 206, 151-159.
8. McPherson, M.J. and Wootton, J.C. (1983) Complete nucleotide sequence of the Escherichia coli gdhA gene. Nucleic Acids Res. 11, 5257-5266.
9. Wootton, J.C., Chambers, G.K., Holder, A.A., Baron, A.J., Taylor, J.G., Fincham, J.R.S., Blumenthal, K.M., Moon, K., Smith, E.L. (1974) Amino-acid sequence of NADP-specific glutamate dehydrogenase of Neurospora crassa. Proc. Natl. Acad. Sci. USA 71, 4361-4365
10. Eggen, R.I.L., Geering, A.C.M., Waldkötter, K., Antranikan, G. and de Vos, W.M. (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.
11. 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. and Yip, K.S.P. (1995) Insights into thermal stability from a comparison of the glutamate dehydrogenase from Pyrococcus furiosus and Thermococcus litoralis. Eur. J. Biochem. 229, 688-695.
12. Wootton, J.C. (1974) The coenzyme-binding domains of glutamate dehydrogenases. Nature (Lond.) 252, 542-546.
13. Britton, K.L., Baker, P.J., Rice, D.W. and Stillman, T.J. (1992) Structural relationship between the hexameric and tetrameric family of glutamate dehydrogenases. Eur. J. Biochem. 209, 851-859.
14. Consalvi, V., Chiaraluce, R., Politi, L., Vaccaro, R., De Rosa, M. and Scandurra, R. (1991) Extremely thermostable glutamate denydrogenase from the hyperthermophilic archaebacterium Pyrococcus furiosus. Eur. J. Biochem. 202, 1189-1196.
15. Robb, F.T., Park, J.B. and Adams, M.W.W. (1992) Characterization of an extremely thermostable glutamate dehydrogenase; a key enzyme in the primary metabolism of the hyperthermophilic archaebacterium Pyrococcus furiosus. Biochim. Biophys. Acta 1120, 267-272.
16. Syed, S.E.H. (1987) Glutamate dehydrogenase from Clostridium symbiosum. PhD Thesis, University of Sheffield, England.
17. +-dependent glutamate dehydrogenase from Clostridium symbiosum. J. Mol. Biol. 181, 147-149.
18. Korber, F.C.F., Rizkallah, P.J., Attwood, T.K., Wootton, J.C., McPherson, M.J., North, A.C., Geddes, A.J., Abeysinghe, I.S.B., Baker, P.J., Dean, J.L., Engel, P.C., Stillman, T.J. and Rice, D.W. (1993) Crystallization of the NADP-dependent glutamate dehydrogenase from Escherichia coli. J. Mol. Biol. 234, 1270-1273.
19. Stillman, T.J., Yip, K.S.P., Rice, D.W., Fuentes, A.M. amd Connerton, I. (1995) Crystallisation and preliminary X-ray analysis of the NADP-specific glutamate dehydrogenase from Neurospora crassa. Acta Cryst. D51, 837-839.
20. Yip, K.S.P., Baker, P.J., Britton, K.L., Engel, P.C., Rice, D.W., Sedelnikova, S.E., Stillman, T.J., Pasquo, A., Chiaraluce, R., Consalvi, V. and Scandurra, R. (1995) Crystallization of the NAD(P)-dependent glutamate dehydrogenase from the hyperthermophilic Pyrococcus furiosus. Acta. Cryst. D51, 240-242.
21. Stillman, T.J., Baker, P.J., Britton, K.L. and Rice, D.W. (1993) Conformational flexibility in glutamate dehydrogenase. Role of water in substrate recognition and catalysis. J. Mol. Biol. 234, 1131-1139.
22. 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, V., Scandurra, R. and Rice, D.W. (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.
23. Ferrin, T.E., Huang, C.C., Jarvis, L.E. and Langridge, R. (1988) The MIDAS display system. J. Mol. Graphics 6, 62-69.
24. Rossmann, M.G., Moras, D. and Olsen, K.W. (1974) Chemical and biological evolution of a nucleotide-binding protein. Nature (Lond.) 250 194-199.
25. Laskowski, R.A., MacArthur, M.W., Moss, D.S. and Thornton, J.M. (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291.
26. Korndörfer, I., Steipe, B., Huber, R., Tomschy, A and Jaenicke, R. (1995) The crystal structure of holo-glyceraldehyde-3-phosphate dehydrogenase from the hyperthermophilic bacterium Thermotoga maritima at 2.5Å resolution. J. Mol. Biol. 246, 511-521.
27. Hennig, M., Darimont, B., Sterner, R., Kirschner, K., Jansonius, J.N. (1995) 2.0Å structure of indole-3-glycerolphosphate synthase from the hyperthermophile Sulfalobus snlfataricus: possible determinants of protein stability. Structure 3, 1295-1306.
28. Russell, R.J.M., Hough, D.W., Danson, M.J. and Taylor, G.L. (1994) The crystal structure of citrate synthase from the thermophilic archaeon. Thermoplasma acidophilum. Structure 2, 1157-1167.
29. Chan, M.K., Mukland, S., Kietzin, A., Adams, M.W.W. and Rees, D.C. (1995) Structure of a hyperthermophilic tungstopterin enzyme, aldehyde ferredoxin oxidoreductase. Science 267, 1463-1469.
30. Lee, B. and Richards, F.M. (1971) The interpretation of protein structures: estimation of static accessibility. J. Mol. Biol. 55, 379-400.
31. Miller S., Janin, J., Lesk, A.M. and Chothia, C. (1987) Interior surface of monomeric proteins. J. Mol. Biol. 196, 641-656.
32. 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. and Yip, K.S.P. (1995) Insights into thermal stability from a comparison of the glutamate dehydrogenase from Pyrococcus furiosus and Thermococcus litoralis. Eur. J. Biochem. 229, 688-695.
33. Harpaz, Y., Gerstein, M. and Chothia, C. (1994) Volume changes on protein folding. Structure 2, 641-649.
34. Eriksson, A.E., Baase, W.A., Zhang, X.-J., Heinz, D.W., Blaber, M, Baldwin, E.P., Matthews, B.W. (1992) Response of a protein structure to cavity-creating mutants and its relation to the hydrophobic effect. Science 255, 178-183.
35. Barlow, D.J. and Thornton, J.M. (1983) Ion pairs in proteins. J. Mol. Biol. 168, 857-885.
36. Kraulis, P.J., (1991) MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Cryst. 24, 946-950.
37. Day, M.W., Hsu, B.T., Joshuator, L., Park, J.B., Zhou, Z.H., Adams, M.W.W. and Rees, D.C. (1992) X-ray crystal structures of the oxidised and reduced forms of the rubredoxin from the marine hyperthermophilic archaebacterium Pyrococcus furiosus. Protein Sci. 1, 1494-1507.
38. Kelly, C.A., Nishiyama, M., Ohnishi, Y., Beppu, T. and Birktoft, J.J. (1993) Determinants of protein thermostability observed in the 1.9Å crystal structure of malate dehydrogenase from the thermophilic bacterium Thermus flavus. Biochemistry 32, 3913-3922.
39. Ishikawa, K., Okumura, M., Katayanagi, K., Kimura, S., Kanaya, S., Nakamura, H., Morikawa, K. (1993) Crystal structure of ribonuclease H from Thermus thermophilus HB8 refined at 2.8 Å resolution. J. Mol. Biol. 230, 529-542.
40. Perutz, M and Raidt, H. (1975) Stereochemical basis of heat stability in bacterial ferredoxins and in haemoglobin A2. Nature 255, 256-259.
41. Perutz, M.F. (1978) Electrostatic effects in proteins. Science 210, 1187-1191.
42. Honig, B. and Nicholls, A. (1995) Classical electrostatics in biology and chemistry. Science 268, 1144-1149.
43. Waldburger, C.D., Schildbach, J.F. and Sauer, R.T. (1995) Are buried saltbridges important for protein stability and conformational specificity? Nat. Struct. Biol. 2, 122-128.