Oligomeric integrity - The structural key to thermal stability in bacterial alcohol dehydrogenases

Protein Science

Volumn 8, Issue 6, 1999, Pages 1241-1249

  Korkhin, Yakov ^a,c   Kalb, A Joseph ^a   Peretz, Moshe ^a   Bogin, Oren ^a   Burstein, Yigal ^a   Frolow, Felix ^a,b  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b TEL AVIV UNIVERSITY   (Israel)

^c YALE UNIVERSITY   (United States)

Author keywords

Alcohol dehydrogenase; Crystal structure; Mutagenesis; Oligomers; Thermal stability

Indexed keywords

ALCOHOL DEHYDROGENASE; BACTERIAL ENZYME;

ARTICLE; CLOSTRIDIUM; ENZYME ACTIVITY; ENZYME STABILITY; HYDROGEN BOND; MOLECULAR INTERACTION; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN QUATERNARY STRUCTURE; THERMOSTABILITY;

EID: 0032989134     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.8.6.1241     Document Type: Article

References (50)

1. Argos P, Rossmann MG, Grau UM, Suborn H, Frank G, Tratschin JD. 1979. Thermal stability and protein structure. Biochemistry 18:5698-5703.
2. Bogin O, Peretz M, Hacham Y, Korkhin Y, Frolow F, Kalb(Gilboa) AJ, Burstein Y. 1998. Enhanced thermal stability of Clostridium beijerinckii alcohol dehydrogenase after strategic substitution of amino acid residues with prolines from the homologous thermophilic Thermoanaerobacter brockii alcohol dehydrogenase. Protein Sci 7:1156-1163.
3. Bogin O, Peretz M, Korkhin Y, Frolow F, Kalb(Gilboa) AJ, Burstein Y. 1996. Thermostabilization of Clostridium beijerinckii alcohol dehydrogenase by site-directed mutagenesis. Protein Sci 5(Suppl 1):81.
4. Burstein Y, Bogin O, Korkhin Y, Peretz M, Kalb(Gilboa) AJ, Frolow F. 1997. Oligomeric integrity - The structural key to thermal stability in bacterial alcohol dehydrogenases. Protein Sci 6(Suppl 1):83.
5. Chen JS. 1995. Alcohol dehydrogenase: Multiplicity and relatedness in the solvent-producing clostridia. FEMS Microbiol Rev 17:263-273.
6. Davies GJ, Gamblin SJ, Littlechild JA, Watson HC. 1993. The structure of a thermally stable 3-phosphoglycerate kinase and a comparison with its mesophilic equivalent. Proteins 15:283-289.
7. Delboni LF, Mande SC, Rentierdelrue F, Mainfroid V, Turley S, Vellieux FMD, Martial JA, Hol WGJ. 1995. Crystal structure of recombinant triosephosphate isomerase from Bacillus stearothermophilus. An analysis of potential thermostability factors in six isomerases with known three-dimensional structures points to the importance of hydrophobic interactions. Protein Sci 4:2594-2604.
8. Hennig M, Darimont B, Sterner R, Kirschner K, Jansonius JN. 1995. 2.0-Angstrom structure of indole-3-glycerol phosphate synthase from the hyperthermophile Sulfolobus solfataricus - Possible determinants of protein stability. Structure 3:1295-1306.
9. 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.
10. Hol WGJ, van Duijnen PT, Berendsen HJC. 1978. The α-helix dipole and the properties of proteins. Nature 273:443-446.
11. Horovitz A, Serrano L, Avron B, Bycroft M, Fersht AR. 1990. Strength and cooperativity of contributions of surface salt bridges to protein stability. J Mol Biol 216:1031-1044.
12. Hurley JH, Baase WA, Matthews BW. 1992. Design and structural analysis of alternative hydrophobic core packing arrangements in bacteriophage T4 lysozyme. J Mol Biol 224:1143-1159.
13. Imada K, Sato M, Tanaka N, Katsube Y, Matsuura 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.
14. Jaenicke R. 1996. Glyceraldehyde-3-phosphate dehydrogenase from Thermologa maritima: Strategies of protein stabilization. FEMS Microbiol Rev 18:215-224.
15. Jaenicke R, Böhm G. 1998. The stability of proteins in extreme environments. Curr Opin Struct Biol 8:738-748.
16. Kabsch W, Sander C. 1983. Dictionary of protein secondary structure: Pattern of recognition of hydrogen-bonded and geometrical features. Biopolymers 22:2577-2637.
17. Kallwass HKW, Surewicz WK, Parris W, Macfariane ELA, Luyten MA, Kay CM, Gold M, Jones JB. 1992. Singe amino acid substitutions can further increase the stability of a thermophilic L-lactate dehydrogenase. Protein Eng 5:769-774.
18. Kelly CA, Nishiyama M, Ohnishi Y, Beppu T, Birktoft JJ. 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.
19. Kirino H, Aoki M, Aoshima M, Hayashi Y, Ohba M, Yamagishi A, Wakagi T, Oshima T. 1994. Hydrophobic interaction at the subunit interface contributes to the thermostability of 3-isopropylmalate dehydrogenase from an extreme thermophile, Thermus thermophilus. Eur J Biochem 220:275-281.
20. Korkhin Y, Frolow F, Bogin O, Peretz M, Kalb(Gilboa) AJ, Burstein Y. 1996. Crystalline alcohol dehydrogenases from the mesophilic bacterium Clostridium beijerinckii and the thermophilic bacterium Thermoanaerobium brockii: Preparation, characterization and molecular symmetry. Acta Crystallogr D52:882-886.
21. Korkhin Y, Kalb(Gilboa) AJ, Peretz M, Bogin O, Burstein Y, Frolow F. 1998. NADP-dependent bacterial alcohol dehydrogenases: Crystal structure, cofactor binding and cofactor specificity of the ADHs of Clostridium beijerinckii and Thermoanaerobacter brockii. J Mol Biol 278:965-979.
22. Korndorfer I, Steipe B, Huber R, Tomschy A, Jaenicke R. 1995. The crystal structure of holo-glyceraldehyde-3-phosphate dehydrogenase from the hyperthermophilic bacterium Thermotoga maritima at 2.5 Å resolution. J Mol Biol 246:511-521.
23. Kraulis P. 1991. MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures. J Appl Crystallogr 24:946-950.
24. Lamed RJ, Zeikus JG. 1981. Novel NADP-linked alcohol-aldehyde/ketone oxidoreductase in thermophilic ethanologenic bacteria. Biochem J 795:183-190.
25. MacBeath G, Kast P, Hilvert D. 1998. Redesigning enzyme topology by directed evolution. Science 279:1958-1961.
26. Matthews BW, Nicholson H, Becktel WJ. 1987. Enhanced protein thermostability from site-directed mutations that decrease the entropy of unfolding. Proc Natl Acad Sci USA 84:6663-6667.
27. Matthews BW, Weaver LH, Kester WR. 1974. The conformation of thermolysin. J Biol Chem 249:8030-8044.
28. Merritt EA, Murphy ME. 1994. RASTER 3D version 2.0. A program for photo-realistic molecular graphics. Acta Crystallogr D50:869-873.
29. Moriyama H, Onodera K, Sakurai M, Tanaka N, Kirino KH, Oshima T, Katsube Y. 1995. The crystal structures of mutated 3-isopropylmalate dehydrogenase from Thermus thermophilus HB8 and their relationship to the thermostability of the enzyme. J Biochem (Tokyo) 117:408-413.
30. Nicholls A, Sharp K, Honig B. 1991. Protein folding and association - Insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins 11:281-296.
31. Nicholson H, Becktel WJ, Matthews BW. 1988. Enhanced protein thermostability from designed mutations that interact with alpha-helix dipoles. Nature 226:651-656.
32. Peretz M, Bogin O, Tel-Or S, Cohen A, Li G, Chen J-S, Burstein Y. 1997. Molecular cloning, nucleotide sequencing, and expression of genes encoding alcohol dehydrogenases from the thermophile Thermoanaerobacter brockii and the mesophile Clostridium beijerinckii. Anaerobe 3:259-270.
33. Peretz M, Burstein Y. 1989. Amino acid sequence of alcohol dehydrogenase from the thermophilic bacterium Thermoanaerobium brockii. Biochemistry 28:6549-6555.
34. Perutz MF. 1978. Electrostatic effects in proteins. Science 207:1187-1191.
35. Perutz MF, Raidt H. 1975. Stereochemical basis of heat stability in bacterial ferredoxins and in haemoglobin A2. Nature 255:256-259.
36. Russell RJ, Hough DW, Danson MJ, Taylor GL. 1994. The crystal structure of citrate synthase from the thermophilic archaeon Thermoplasma acidophilum. Structure 2:1157-1167.
37. Salminen T, Teplyakov A, Kankare J, Cooperman BS, Lahti RAG. 1996. An unusual route to thermostability disclosed by the comparison of Thermus thermophilus and Escherichia coli inorganic pyrophosphatases. Protein Sci 5:1014-1025.
38. Sterner R, Vogl T, Hinz HJ, Penz F, Hoff R, Foll R, Decker H. 1995. Extreme thermostability of tarantula hemocyanin. FEBS Lett 364:9-12.
39. Tanner JJ, Hecht RM, Krause KL. 1996. Determinants of enzyme thermostability observed in the molecular structure of Thermus aquaticus D-glyceraldehyde-3-phosphate dehydrogenase at 2.5 angstrom resolution. Biochemistry 35:2597-2609.
40. Tomschy A, Böhm G, Jaenicke R. 1994. The effect of ion pairs on the thermal stability of D-glyceraldehyde 3-phosphate dehydrogenase from the hyperthermophilic bacterium Thermotoga maritima. Protein Eng 7:1471-1478.
41. Van den Burg B, Vriend G, Veltman OR, Venema G, Eijsink VG. 1998. Engineering an enzyme to resist boiling. Proc Natl Acad Sci USA 95:2056-2060.
42. Vetriani C, Maeder DL, Tolliday N, Yip KSP, Stillman TJ, Britton KL, Rice DW, Klump HH, Robb FT. 1998. Protein thermostability above 100 °C: A key role for ionic interactions. Proc Natl Acad Sci USA 95:12300-12305.
43. Villeret V, Clantin B, Tricot C, Legrain C, Roovers M, Stalon V, Glansdorff N, Van Beeumen J. 1998. The crystal structure of Pyrococcus furiosus omithine carbamoyltransferase reveals a key role for oligomerization in enzyme stability at extremely high temperatures. Proc Natl Acad Sci USA 95:2801-2806.
44. Vriend G. 1990. WHATIF: A molecular modeling and drug design program. J Mol Graph 8:52-56.
45. Walker JE, Wonacott AJ, Harris JI. 1980. Heat stability of a tetrameric enzyme, D-glyceraldehyde-3-phosphate dehydrogenase. Eur J Biochem 108:581-586.
46. Wallon G, Kryger G, Lovett ST, Oshima T, Ringe D, Petsko GA. 1997. Crystal structures of Escherichia coli and Salmonella typhimurium 3-isopropylmalate dehydrogenase and comparison with their thermophilic counterpart from Thermus thermophilus. J Mol Biol 266:1016-1031.
47. Watanabe K, Chishiro K, Kitamura K, Suzuki Y. 1991. Proline residues responsible for thermostability occur with high frequency in the loop regions of an extremely thermostable oligo-1,6-glucosidase from Bacillus thermoglucosidasius KP1006. J Biol Chem 266:24287-24294.
48. Watanabe K, Masuda T, Ohashi H, Mihara H, Suzuki Y. 1994. Multiple proline substitutions cumulatively thermostabilize Bacillus cereus ATCC7064 oligo-1,6-glucosidase. Irrefragable proof supporting the proline rule. Eur J Biochem 226:277-283.
49. Yip KSP, Stillman TJ, Britton KL, Artymiuk PJ, Baker PJ, Sedelnikova SE, Engel PC, Pasquo A, Chiaraluce R, Consalvi V, Scandurra R, Rice DW. 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.
50. Zeikus JG, Hegge PW, Anderson MA. 1979. Thermoanaerobium brockii gen. nov. and sp. nov., A new chemoorganotrophic, caldoactive, anaerobic bacterium. Arch Microbial 122:41-48.