Insights into the molecular basis of thermal stability from the analysis of ion-pair networks in the glutamate dehydrogenase family

European Journal of Biochemistry

Volumn 255, Issue 2, 1998, Pages 336-346

  Yip, Kitty S P ^a   Britton, K Linda ^a   Stillman, Timothy J ^a   Lebbink, Joyce ^b   De Vos, Willem M ^b   Robb, Frank T ^c   Vetriani, Constantino ^c   Maeder, Dennis ^a   Rice, David W ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b WAGENINGEN UNIVERSITY   (Netherlands)

^c UNIVERSITY OF MARYLAND   (United States)

Author keywords

Archaea; Glutamate dehydrogenase; Homology modeling; Ion pair network; Thermal stability

Indexed keywords

GLUTAMATE DEHYDROGENASE;

ARTICLE; CLOSTRIDIUM; ENZYME ACTIVITY; ENZYME STRUCTURE; ESCHERICHIA COLI; MODEL; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PYROCOCCUS; SEQUENCE HOMOLOGY; STRAIN DIFFERENCE; THERMOSTABILITY;

EID: 0032528267     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1327.1998.2550336.x     Document Type: Article

References (52)

1. Flam, F. (1994) The chemistry of life at the margins, Science 265, 471-472.
2. Adams, M. W. W. & Kelly, R. M. (1995) Enzymes from microorganisms in extreme environments, Chem. Eng. News 73, December 18, 32-42.
3. Woese, C. R., Kandler, O. & Wheelis, M. L. (1990) Towards a natural system of organisms: Proposal for the domains; Archaea, Bacteria and Eucarya, Proc. Natl Acad. Sci. USA 87, 4576-4579.
4. Vihinen, M. (1987) Relationship of protein flexibility to thermostability, Protein Eng. 1, 481-485.
5. Mathews, B. W., Nicholson, H. & Becktel, W. J. (1987) Enhanced protein thermostability from site-directed mutations that decrease the entropy of unfolding, Proc. Natl Acad. Sci. USA 84, 6663-6667.
6. Day, M. W., Hsu, B. T., Joshua-tor, L., Park, J.-B., Zhou, Z. H., Adams, M. W. W. & Rees, D. (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.
7. Kelly, C. A., Nishiyama, M., Ohnishi, Y., Beppu, T. & Birktoft, J. J. (1993) Determinants of protein thermostability observed in the 1.9 Å crystal structure of malate dehydrogenase from the thermophilic bacterium Thermus flavus, Biochemistry 32, 3913-3922.
8. Perutz, M. F. & Raidt, H. (1975) Stereochemical basis of heat stability in bacterial ferredoxins and in haemoglobin A2, Nature 255, 256-259.
9. Perutz, M. F. (1978) Electrostatic effects in proteins, Science 201, 1187-1191.
10. Britton, K. L., Baker, P. J., Borges, K. M. M., Engel, P. C., Pasquo, A., Rice, D. W., Robb, F., Scandurra, R., Stillman, T. J. & 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.
11. Russell, R. J. M., Hough, D. W., Danson, M. J. & Taylor, G. L. (1994) The crystal structure of citrate synthase from the thermophilic archaeon Thermoplasma acidophilum, Structure 2, 1157-1167.
12. 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 mutations and its relation to the hydrophobic effect, Science 255, 178-183.
13. Völkl, P., Markiewicz, P., Stetter, K. O. & Miller, J. (1994) The sequence of a subtilisin-type protease (aerolysin) from the hyperthermophilic archaeum Pyrobaculum aerophilum reveals sites important to thermostability, Protein Sci. 3, 1329-1340.
14. Chan, M. K., Mukland, S., Kletzin, A., Adams, M. W. W. & Rees, D. C. (1995) Structure of a hyperthermophilic tungstopterin enzyme, aldehyde ferredoxin oxidoreductase, Science 267, 1463-1469.
15. Tesfay, H. S., Amelunxen, R. E. & Goldberg, I. D. (1989) Nucleotide-sequences of genes encoding heat-stable and heat-labile glyceraldehyde-3-phosphate dehydrogenases - Amino acid sequence and protein stability. Gene (Amst.) 82, 237-248.
16. Suzuki, Y., Hatagaki, K. & Oda, H. (1991) A hyperthermostable pullulanase produced by an extreme thermophile, Bacillus flavocaldarius KP 1228, and evidence for the proline theory of increasing protein thermostability, Appl. Microbiol. Biotechnol. 34, 707-714.
17. Matsumura, M., Signor, G. & Matthews, B. W. (1989) Substantial increase of protein stability by multiple disulphide bonds, Nature 342, 291-293.
18. Imada, K., Sato, M., Tanaka, N., Katsube, Y., Matsura, Y. & Oshima, T. (1991) Three dimensional structure of a highly thermostable enzyme, 3-Isopropylmalate dehydrogenase of Thermus thermophilus at 2.2 Å resolution, J. Mol. Biol. 222, 725-738.
19. Hurley, J. H., Baase, W. A. & Matthews, B. W. (1992) Design and structural analysis of alternative core packing arrangements in Bacteriophage T4 Lysozyme, J. Mol. Biol. 224, 1144-1159.
20. Anderson, D. E., Hurley, J. H., Nicholson, H., Baase, W. A. & Matthews, B. W. (1993) Hydrophobic core repacking and aromatic-aromatic interaction in the thermostable mutant of T4 lysozyme Ser117→Phe, Protein Sci. 2, 1285-1290.
21. Waldburger, C. D., Schildbach, J. F. & Sauer, R. T. (1995) Are buried salt bridges important for protein stability and conformational specificity? Struct. Biol. 2, 122-128.
22. Pauptit, R. A., Karlsson, R., Picot, D., Jenkins, J. A., Niklaus-Reimer, A.-S. & Jansonius, J. N. (1988) Crystal structure of neutral protease from Bacillus cereus refined at 3.0 resolution and comrison with the homologous but more thermostable enzyme thermolysin, J. Mol. Biol. 199, 525-537.
23. Creighton, T. E. (1985) The problem of how and why proteins adopt folded conformations, J. Phys. Chem. 89, 2452-2459.
24. Boyer, P. D. (1975) The enzymes 11, 3rd edn, Academic Press, New York.
25. Hudson, R. C. & Daniel, R. M. (1993) L-Glutamate dehydrogenases: distribution, properties and mechanism, Comp. Biochem. Physiol. B 106, 767-792.
26. Fiala, G. & Stetter, K. O. (1986) Pyrococcus furiosus sp. nov. represents a novel genus of marine heterotrophic archaebacteria growing optimally at 100°C, Arch. Microbiol. 145, 56-61.
27. 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.
28. Syed, S. E. H. (1987) Glutamate dehydrogenase from Clostridium symbiosum, PhD Thesis, University of Sheffield, UK.
29. 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. & Rice, D. W. (1995) The structure of Pyrococcus furiosus glutamate dehydrogenase reveals a key role for ion pairs networks in maintaining enzyme stability at extreme temperatures, Structure 3, 1147-1158.
30. Rice, D. W., Yip, K. S. P., Stillman, T. J., Britton, K. L., Fuentes, A., Connerton, I., Pasquo, A., Scandurra, R. & Engel, P. C. (1996) Insights into the molecular basis of thermal stability from the structure determination of Pyrococcus furiosus glutamate dehydrogenase, FEMS Microbiol. Rev. 18, 105-117.
31. +-linked glutamate dehydrogenase from E. coli, PhD Thesis, University of Sheffield, UK.
32. Fincham, J. R. S. & Garner, H. R. (1967) Effects of pH and temperature on the wild type and a mutant form of Neurospora glutamate dehydrogenase, J. Biochem. (Tokyo) 103, 705-708.
33. Anderson, B. M., Anderson, C. D., Van Tassell, R. L., Lyerly, D. M. & Wilkins, T. D. (1993) Purification and characterisation of Clostridium difficile, Arch. Biochem. Biophys. 300, 483-488.
34. Lebbink, J. H. G., Eggen, R. I. L., Geering, A. C. M., Consalvi, V., Chiaraluce, R., Scandurra, R. & de Vos, W. M. (1995) Exchange of domains of GluDH from the hyperthermophilic archaeon Pyrococcus furiosus and the mesophilic bacterium Clostridium difficile effects on catalysis, thermoactivity and stability, Protein Eng. 8, 1287-1294.
35. Kort, R., Liebl, W., Labedan, B., Forterre, P., Eggen, R. I. L. & de Vos. W. M. (1997) Extremophiles, in the press.
36. Maras, B., Consalvi, V., Chiaraluce, R., Politi, L., De Rosa, M., Bossa, F., Scandurra, R. & Barra, D. (1992) The protein sequence of glutamate dehydrogenase from Sulfolobus solfataricus, a thermoacidophilic archaebacterium. Is the presence of N-ε-methyllysine related to thermostability? Eur. J. Biochem. 203, 81-87.
37. Ma, K., Robb, F. T. & Adams, M. W. W. (1994) Purification and characterisation of NADP-specific alcohol dehydrogenase and glutamate dehydrogenase from the hyperthermophilic archaeon Thermococcus litoralis, Appl. Environ. Microbiol. February. 562-568.
38. DiRuggiero, J., Robb, F. T., Jagus, R., Klump, H. H., Borges, K. M., Kessel, M., Mai, X. & Adams, M. W. W. (1993) Characterisation, cloning and in vitro expression of the extremely thermostable glutamate dehydrogenase from the hyperthermophilic archaeon, ES4, J. Biol. Chem. 268, 17767-17774.
39. Klump, H., DiRuggiero, J., Kessel, M., Park, J.-B., Adams, M. W. W. & Robb, F. T. (1992) Glutamate dehydrogenase from the hyperthermophilic Pyrococcus furiosus: Thermal denaturation and activation, J. Biol. Chem. 267, 22681-22685.
40. Baker, P. J., Britton, K. L., Engel, P. C., Farrants, G. W., Lilley, K. S., Rice, D. W. & Stillman, T. J. (1992) Subunit assembly and active site location in the structure of glutamate dehydrogenase, Proteins 12, 75-86.
41. + dependent glutamate dehydrogenase from Clostridium symbiosum, J. Mol. Biol. 181, 147-149.
42. McPherson, M. J. & Wootton, J. C. (1983) Complete nucleotide sequence of the Escherichia coli gdhA gene, Nucleic Acids Res. 11, 5257-5266.
43. Koherstein, R. & Sund, H. (1973) Studies of glutamate dehydrogenase. The influence of ADP, GTP, L-glutamate on the binding of the reduced coenzyme to beef liver GluDH, Eur. J. Biochem. 36, 545-552.
44. Menéndez-Arias, L. & Argos, P. (1989) Engineering protein thermal stability, J. Mol. Biol. 206, 397-406.
45. Teller, J. K., Smith, R. M., McPherson, M. J., Engel, P. C. & 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.
46. Kinnaird, J. H. & Fincham, J. R. S. (1983) The complete nucleotide sequence of the Neurospora crassa am (NADP-specific glutamate dehydrogenase) gene, Gene (Amst.) 26, 253-260.
47. Lyerly, D. M., Barroso, L. A. & Wilkins, T. D. (1991) Identification of the latex test-reactive protein of Clostridium difficile as glutamate dehydrogenase, J. Chem. Microbiol. 29, 2639-2642.
48. Snedecor, B., Chu, H. & Chen, H. (1991) Selection, expression, and nucleotide sequencing of the glutamate dehydrogenase gene of Peptostreptococcus asaccharolyticus, J. Bacteriol. 173, 6162-6167.
49. Eggen, R. I. L., Geerling, A. C. M., Waldkötter, K., Antranikan, G. & de Vos, W. M. (1993) The glutamate dehydrogenase encoding gene of the hyperthermophilic archacon Pyrococcus furiosus: sequence, transcription and analysis of the deduced amino acid sequence, Gene (Amst.) 132, 143-148.
50. Kraulis, P. J. (1991) MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24, 946-950.
51. Nicholls, A., Sharp, K. A. & Honig, B. (1991) Protein folding and association - Insights from the interfacial and thermodynamic properties of hydrocarbons, Proteins Struct. Funct. Genet. 11, 281-296.
52. Ferrin, T. E., Huang, C. C., Jarvis, L. E. & Langridge, R. (1988) The MIDAS display system, J. Mol. Graphics 6, 13-27.