Extremely thermostable L(+)-lactate dehydrogenase from Thermotoga maritima: Cloning, characterization, and crystallization of the recombinant enzyme in its tetrameric and octameric state

Protein Science

Volumn 5, Issue 5, 1996, Pages 862-873

  Ostendorp, Ralf ^a   Auerbach, Günter ^a   Jaenicke, Rainer ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

association; lactate dehydrogenase; thermophilism; thermostability; Thermotoga maritima

Indexed keywords

LACTATE DEHYDROGENASE;

ALPHA HELIX; ARTICLE; CRYSTALLIZATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME PURIFICATION; GLYCOLYSIS; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DENATURATION; THERMOPHILIC BACTERIUM; THERMOSTABILITY;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; THERMOTOGA MARITIMA;

EID: 0029923296     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1002/pro.5560050508     Document Type: Article

References (62)

1. Abad-Zapatero C, Griffith JP, Sussman JL, Rossmann MG. 1987. Refined crystal structure of dogfish M4 apo-lactate dehydrogenase. J Mol Biol 198:445-467.
2. Auerbach G. 1994. Aufklärung der Dreidimensionalen Struktur der LDH aus dem Hyperthermophilen Bakterium Thermotoga Maritima Mittels Homology Modelling. Regensburg: University of Regensburg.
3. Beaucamp N, Ostendorp R, Schurig H, Jaenicke R. 1995. Cloning, sequencing, expression and characterization of the gene encoding the 3-phosphoglycerate kinase-triosephosphate isomerase fusionprotein from Thermotoga maritima. Prot Pepl Lett 2:281-286.
4. Bohm G, Jaenicke R. 1992. Correlation functions as a tool for protein modeling and structure analysis. Protein Sci 1:1269-1278.
5. Bohm G, Jaenicke R. 1994. Relevance of sequence statistics for the properties of extremophilic proteins. Int J Pept Prot Res 43:97-106.
6. Chan WWC, Mort JS, Chong DKK, MacDonald PDM. 1973. Studies on protein subunits. J Biol Chem 248:2778-2784.
7. Chen YH, Yang JT, Martinez HM. 1972. Determination of the secondary structures of proteins by circular dichroism and optical rotatory dispersion. Biochemistry 11:4120-4131.
8. Clarke AR, Atkinson T, Holbrook JJ. 1989. From analysis to synthesis: New ligand binding sites on the lactate dehydrogenase framework. Trends Biochem Sci 14:101-105; 145-148.
9. Dams T. 1995. Vergleichende Charakterisierung von Tetramerer und Oktamerer L(+)-LDH aus dem Hyperthermophilen Bakterium Thermotoga Maritima. Regensburg: University of Regensburg.
10. Dayhoff MO, Barker WC, Hunt LT. 1983. Establishing homologies in protein sequences. Methods Enzymol 91:524-545.
11. Durchschlag H, Jaenicke R. 1982. Partial specific volume changes of proteins: Densirnetric studies. Biochem Biophys Res Commun 108:1074-1079.
12. Eisenberg H, Josephs R, Reisler E. 1976. Bovine liver glutamate dehydrogenase. Adv Prot Chem 30:101-181.
13. Garvie EI. 1980. Bacterial lactate dehydrogenases. Microbiol Rev 44:106-139.
14. Gill SC, von Hippel PH. 1989. Calculation of protein extinction coefficients from amino acid sequence data. Anal Biochem 182:319-326.
15. Gira R, Jaenicke R, Rudolph R. 1983. Dimers of porcine skeletal muscle lactate dehydrogenase produced by limited proteolysis during reassociation are enzymatically active in the presence of stabilizing salt. Biochemistry International 7:433-441.
16. Hensel R, Konig H. 1988. Thermoadaptation of methanogenic bacteria by intracellular ion concentration. FEMS Microbiol Lett 49:75-79.
17. Hermann R, Jaenicke R, Rudolph R. 1981. Analysis of the reconstitution of oligomeric enzymes by crosslinking with glutaraldehyde: Kinetics of reassociation of lactic dehydrogenase. Biochemistry 20:5195-5201.
18. Hubert M, Böhm G, Jaenicke R. 1993. Structural relationships of homologous proteins as a fundamental principle in homology modeling. Proteins Struct Funct Genet 77:138-151.
19. Holbrook JJ, Liljas A, Steindel SJ, Rossmann MG. 1975. Lactate dehydrogenase. In: Boyer PD, ed. The enzymes. New York: Academic Press. pp 191-292.
20. Huber R, Langworthy TA, König H, Thomm M, Woese CR, Sleytr UB, Steuer KO. 1986. Thermotoga maritima sp. nov. represents a new genus of unique extremely thermophilic eubacteria growing up to 90 °C. Arch Microbiol 144:324-333.
21. Iwata S, Kamata K, Yoshida S, Minowa T, Ohta T. 1994. T and R states in the crystals of bacterial L-lactate dehydrogenase reveal the mechanism for allosteric control. Struct Biol 1:176-185.
22. Iwata S, Ohta T. 1993. Molecular basis of allosteric activation of bacterial L-lactate dehydrogenase. J Mol Biol 230:21-27.
23. Jaenicke R. 1981. Enzymes under extremes of physical conditions. Annu Rev Biophys Bioeng 10:1-67.
24. Jaenicke R. 1991. Protein stability and molecular adaptation to extreme conditions. Eur J Biochem 202:715-728.
25. Jaenicke R, Schurig H, Beaucamp N, Ostendorp R. 1996. Structure and stability of hyperstable proteins: Glycolytic enzymes from the hyperthermophilic bacterium Thermoroga maritime. Adv Prot Chem. Forthcoming.
26. Kabsch W, Sander C. 1983. Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22:2577-2637.
27. Kallwass HKW, Surewicz WK, Parris W, Macfarlane ELA, LuytenMA, Kay CM, Gold M, Jones JB. 1992. Single amino acid substitutions can further increase the stability of a thermophilic L-lactate dehydrogenase. Protein Eng 5:769-774.
28. 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.
29. Kotik M, Zuber H. 1992. Evidence for temperature-dependent conformational changes in the L-lactate dehydrogenase from Bacillus stearothermophilus. Biochemistry 31:7787-7795.
30. Kotik M, Zuber H. 1993. Mutations that significantly change the stability, flexibility and quaternary structure of the L-lactate dehydrogenase from Bacillus megaterium. Eur J Biochem 211:267-280.
31. Kraulis PJ. 1991. MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures. J Appl Crystallogr 24:946-950.
32. Laskowski RA, MacArthur MW, Moss DS, Thornton JM. 1993. PROCHECK: A program to check the stereochemical quality of protein structures. J Appl Crystallogr 26:283-291.
33. Leibrock E, Bayer P, Lüdemann HD. 1995. Nonenzymatic hydrolysis of adenosinetriphosphate (ATP) at high temperatures and high pressures. Biophys Chem 54:175-180.
34. Menendez-Arias L, Argos P. 1989. Engineering protein thermal stability. Sequence statistics point to residue substitutions in α-helices. J Mol Biol 206:397-406.
35. Muller K, Seifert T, Jaenicke R. 1984. High pressure dissociation of lactate dehydrogenase from Bacillus stearothermophilus and reconstitution of the enzyme after denaturation in 6 M guanidine hydrochioride. Eur Biophys J 11:87-94.
36. Needleman SB, Wunsch CD. 1970. A general method applicable to the search for similarities in the amino acid sequence of two proteins. J Mol Biol 48:443-453.
37. Nojima H, Noda H. 1979. Kinetics of thermal unfolding and refolding of thermostable phosphoglycerate kinase. J Biochem 86:1055-1065.
38. Ostendorp R, Liebl W, Schurig H, Jaenicke R. 1993. The L-lactate dehydrogenase gene of the hyperthermophilic bacterium Thermotoga maritima cloned by complementation in Escherichia coli. Eur J Biochem 216: 709-715.
39. Ott M. 1996. Dynamische Lichtstreuung an Proteinen: Faltung und Assoziatiom. Regensburg: University of Regenshurg.
40. Pace CN. 1986. Determination and analysis of urea and guanidine hydrochloride denaturation curves. Methods Enzymol 131:266-280.
41. Perutz MF, Raidt H. 1975. Stereochemical basis of heat stability in bacterial ferredoxins and in haemoglobin A2. Nature 255:256-259.
42. Ravot G, Magot M, Fardeau ML, Patel BKC, Prensier O, Egan A, Garcia JL, Ollivier B. 1995. Thermotoga elfii sp. nov., a novel thermophilic bacterium from an African oil-producing well. Int J Syst Bact 45:308-314.
43. Rehaber V, Jaenicke R. 1992. Stability and reconstitution of D-glyceraldehyde-3-phosphate dehydrogenase from the hyperthermophilic eubacterium Thermotoga maritima. J Biol Chem 267:10999-11006.
44. Rossmann MG, Liljas A, Brändén CI, Banaszak LJ. 1975. Evolutionary and structural relationships among dehydrogenases. In: Boyer PD, ed. The enzymes. New York: Academic Press, pp 61-102.
45. Rost B, Sander C. 1994. Combining evolutionary information and neural networks to predict protein secondary structure. Proteins Struct Funct Genet 19:55-72.
46. Rudolph R, Jaenicke R. 1977. Kinetics of reassociation and reactivation of pig-muscle lactic dehydrogenase after acid dissociation. Eur J Biochem 63:409-417.
47. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: A laboratory manual. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
48. Sanger F, Micklen F, Coulson AR. 1977. DNA sequencing with chain termination inhibitors. Proc Natl Acad Sci USA 74:5463-5467.
49. Schurig H, Rutkat K, Rachel R, Jaenicke R. 1995. Octameric enolase from the hyperthermophilic bacterium Thermoioga maritima: Purification, characterization, and image processing. Protein Sci 4:228-236.
50. Skerra A, Pfitzinger I, Plückthun A. 1991. The functional expression of antibody Fv fragments in Escherichia coli: Improved vectors and a generally applicable purification technique. Bio/Technology 9:273-278.
51. Studier FW, Moffatt BA. 1986. Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J Mol Biol 189: 113-130.
52. Taylor WR. 1988. Pattern matching methods in protein sequence comparison and structure prediction. Protein Eng 2:77-86.
53. Tomschy A, Glockshuber R, Jaenicke R. 1993. Functional expression of Dglyceraldehyde-3-phosphate dehydrogenase from the hyperthermophilic eubacterium Thermotoga maritima in Escherichia coli: Authenticity and kinetic properties of the recombinant enzyme. Eur J Biochem 214:43-50.
54. Wigley DB, Clarke AR, Dunn CR, Barstow DA, Atkinson T, Chia WN, Muirhead H, Holbrook JJ. 1987. The engineering of a more thermally stable lactate dehydrogenase by reduction of the area of water-accessible hydrophobic surface. Biochim Biophys Acta 916:145-148.
55. Wigley DB, Gamblin SJ, Turkenburg JP, Dodson EJ, Piontek K, Muirhead H, Holbrook JJ. 1992. Structure of a ternary complex of an allosteric lactate dehydrogenase from Bacillus stearothermophilus at 2.5 Å resolution. J Mol Biol 223:317-335
56. Wrba A, Jaenicke R, Huber R, Stetter KO. 1990a. Lactate dehydrogenase from the extreme thermophile Thermotoga maritima. Eur J Biochem 188:195-201.
57. Wrba A, Schweiger A, Schultes V, Jaenicke R, Závodszky P. 1990b. Extremely thermostable D-glyceraldehyde-3-phosphate dehydrogenase from the eubacterium Thermotoga maritima. Biochemistry 29:7584-7592.
58. Yphantis DA. 1964. Equilibrium ultracentrifugation of dilute solutions. Biochemistry 3:297-317.
59. Zettlmeissl G, Rudolph R, Jaenicke R. 1982. Rate-determining folding and association reactions on the reconstitution pathway of porcine skeletal muscle lactic dehydrogenase after denaturation by guanidine hydrochloride. Biochemistry 21:3946-3950.
60. Zuber H. 1988. Temperature adaptation of lactate dehydrogenase Structural, functional and genetic aspects. Biophys Chem 29:171-179.
61. Zulli F, Schneller R, Urfer R, Zuber H. 1991. Engineering thermostability and activity of lactate dehydrogenases from bacilli. Biol Chem Hoppe-Seyler 372:363-312.
62. Zulli F, Weber H, Zuber H. 1990. Analysis of structural elements responsible for the differences in thermostability and activation by fructose 1,6-bisphosphate in the lactate dehydrogenases from B. stearothermophilus and B. caldolyticus by protein engineering. Biol Chem Hoppe-Seyler 371:655-662.