Phosphoribosyl anthranilate isomerase from Thermotoga maritima is an extremely stable and active homodimer

Protein Science

Volumn 5, Issue 10, 1996, Pages 2000-2008

  Sterner, Reinhard ^a   Kleemann, Gerd R ^a   Szadkowski, Halina ^a   Lustig, Ariel ^a   Hennig, Michael ^a,b   Kirschner, Kasper ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b F HOFFMANN LA ROCHE LTD   (Switzerland)

Author keywords

( )8 barrel proteins; hyperthermophile; labile substrate; steady state kinetics; thermostability; tryptophan biosynthesis

Indexed keywords

ISOMERASE;

ARTICLE; ENZYME ACTIVITY; ENZYME STABILITY; HIGH TEMPERATURE; NONHUMAN; PRIORITY JOURNAL; STEADY STATE; THERMOPHILIC BACTERIUM; THERMOSTABILITY;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; THERMOTOGA MARITIMA;

EID: 0029912086     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1002/pro.5560051006     Document Type: Article

References (62)

1. Achenbach-Richter L, Gupta R, Stetter KO, Woese CR. 1987. Were the original eubacteria thermophiles? System Appl Microbiol 9:34-39.
2. Adams MWW. 1993. Enzymes and proteins from organisms that grow near and above 100 °C. Annu Rev Microbiol 47:627-658.
3. Bisswanger H, Kirschner K, Cohn W, Hager V, Hansson E. 1979. N-(5-phosphoribosyl)anthranilate isomerase-indoleglycerol-phosphale synthase. 1. A substrate analogue binds to two different binding sites on the bifunctional enzyme from Escherichia coli. Biochemistry 18:5946-5953.
4. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254.
5. Braus GH, Luger K, Paravicini G, Schmidheini T, Kirschner K, Hütter R. 1988. The role of the TRP1 gene in yeast tryptophan biosynthesis. J Biol Chem 263:7868-7875.
6. Bujard H, Gentz R, Lanzer M, Stüber D, Müller M, Ibrahimi I, Häuptle MT, Dobberstein B. 1987. A T5 promoter-based transcription-translation system for the analysis of proteins in vitro and in vivo. Methods Enzymol 155:416-433.
7. Casabadan MY. 1976. Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and mu. J Mol Biol 104:541-555.
8. Cavagnero S, Zhou ZH, Adams MWW, Chan SI. 1995. Response of rubredoxin from Pyrococcus furiosus to environmental changes: Implications for the origin of hyperthermostability. Biochemistry 34:9865-9873.
9. Cohn W, Kirschner K, Paul C. 1979. N-(5-phosphoribosyl)anthranilate isomerase-indoleglycerol-phosphate synthase. 2. Fast-reaction studies show that a fluorescent substrate analogue binds independently to two different sites. Biochemistry 18:5953-5959.
10. Crawford IP. 1989. Evolution of a biosynthetic pathway: The tryptophan paradigm. Annu Rev Microbiol 43:567-600.
11. Creighton TE. 1968. The nonenzymatic preparation in solution of N-(5′-Phosphoribosyl)anthranilic acid, an intermediate in tryptophan biosynthesis. J Biol Chem 243:5605-5609.
12. Creighton TE. 1970. N-(5′-phosphoribosyl)anthranilate isomerase-indol-3-glycerol phosphate synthetase of tryptophan biosynthesis. Relationship between the two activities of the enzyme from Escherichia coli. Biochem J 120:699-707.
13. Creighton TC, Yanofsky C. 1966. Indole-3-glycerol phosphate synthetase of Escherichia coli, an enzyme of the tryptophan operon. J Biol Chem 241:4616-4624.
14. Darimont B, Sterner R. 1994. Sequence, assembly and evolution of a primordial ferredoxin from Thermotoga maritima. EMBO J 13:1772-1781.
15. Eberhard M, Tsai-Pflugfelder M, Bolewska K, Hommel U, Kirschner K. 1995. Indoleglycerol phosphate synthase-phosphoribosyl anthranilate isomerase: Comparison of the bifunctional enzyme from Escherichia coli with engineered monofunctional domains. Biochemistry 34:5419-5428.
16. Enatsu T, Crawford IP. 1968. Enzymes of the tryptophan synthetic pathway in Pseudomonas putida. J Bacteriol 95:107-112.
17. Engel AM, Cejka Z, Lupas A, Lottspeich F, Baumeister W. 1992. Isolation and cloning of Ompα, a coiled-coil protein spanning the periplasmic space of the ancestral eubacterium Thermotoga maritima. EMBO J 11:4369-4378.
18. Fink AL, Calciano LJ, Goto Y, Kurotsu T, Palleros DR. 1994. Classification of acid denaturation of proteins: Intermediates and unfolded states. Biochemistry 33:12504-12511.
19. Fontana A. 1988. Structure and stability of thermophilic enzymes. Studies on thermolysin. Biophys Chem 29:181-193.
20. Hennig M, Darimont B, Sterner R, Kirschner K, Jansonius JN. 1995. 2.0 Å structure of indole-3-glycerol phosphate synthase from the hyperthermophile Sulfolobus solfataricus: Possible determinants of protein stability. Structure 3:1295-1306.
21. Hensel R, Fabry S, Biro J, Bogedain C, Jakob I, Siebers B. 1994. Glyceraldehyde-3-phosphate dehydrogenases from Archaea: Objects for studying protein thermoadaptation. Biocatalysis 11:151-164.
22. Hensel R, König H. 1988. Thermoadaptation of methanogenic bacteria by intracellular ion concentration. FEMS Microbiol Lett 49:75-79.
23. Hess D, Krüger K, Knappik A, Palm P, Hensel R. 1995. Dimeric 3-phosphoglycerate kinases from hyperthermophilic Archaea. Cloning, sequencing and expression of the 3-phosphoglycerate kinase gene of Pyrococcus woesei in Escherichia coli and characterization of the protein. Structural and functional comparison with the 3-phosphoglycerate kinase of Methanothermus fervidus. Eur J Biochem 233:227-237.
24. Hoch SO, Anagnostopoulos C, Crawford IP. 1969. Enzymes of the tryptophan operon of Bacillus subtilis. Biochem Biophys Res Commun 35:838-844.
25. Hommel U, Eberhard M, Kirschner K. 1995. Phosphoribosl anthranilate isomerase catalyzes a reversible Amadori reaction. Biochemistry 34:5429-5439.
26. Hommel U, Lustig A, Kirschner K. 1989. Purification and characterization of yeast anthranilate phosphoribosyltransferase. Eur J Biochem 180:33-40.
27. Huber R, Langworthy TA, König H, Thomm M, Woese CR, Sleytr UB, Stetter 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.
28. Jackson EN, Yanofsky C. 1973. The region between the operator and first structural gene of the tryptophan operon of Escherichia coli may have a regulatory function. J Mol Biol 76:89-101.
29. Jaenicke R. 1996. Stability and folding of ultrastable proteins: Eye lens crystallins and enzymes from thermophiles. FASEB J 10:84-92.
30. Kabsch W. 1988. Evaluation of single-crystal X-ray diffraction data from a position-sensitive detector. J Appl Crystallogr 21:916-924.
31. Kim CW, Markiewicz P, Lee JJ, Schierle CF, Miller JH. 1993. Studies of the hyperthermophile Thermotoga maritima by random sequencing of cDNA and genomic libraries. J Mol Biol 231:960-981.
32. Kirschner K, Szadkowski H, Jardetzky TS, Hager V. 1987. Phosphoribosylanthranilate isomerase-indoleglycerol phosphate synthase from Escherichia coli. Methods Enzymol 142:386-397.
33. Kohlhoff M, Dahm A, Hensel R. 1996. Tetrameric triosephosphate isomerase from hyperthermophilic Archaea. FEBS Lett 383:245-250.
34. Lämmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
35. Larralde R, Robertson MP, Miller SL. 1995. Rates of decomposition of ribose and other sugars: Implications for chemical evolution. Proc Natl Acad Sci USA 92:8158-8160.
36. Levine RL, Federici MM. 1982. Quantitation of aromatic residues in proteins: Model compounds for second-derivative spectroscopy. Biochemistry 21:2600-2606.
37. Liebl W, Feil R, Gabelsberger J, Kellermann J, Schleifer KH. 1992. Purification and characterization of a novel thermostable 4-α-glucanotransferase of Thermotoga maritima cloned in Escherichia coli. Eur J Biochem 207:81-88.
38. Martins LO, Santos H. 1995. Accumulation of mannosylglycerate and di-myoinisitol-phosphate by Pyrococcus furiosus in response to salinity and temperature. Appl Environ Microbiol 61:3299-3303.
39. 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.
40. Priestle JP, Grütter MG, White JL, Vincent MG, Kania M, Wilson E, Jardetzky TS, Kirschner K, Jansonius JN. 1987. Three-dimensional structure of the bifunctional enzyme N-(5′-phosphoribosyl)anthranilate isomerase-indole-3-glycerol-phosphate synthase from Escherichia coli. Proc Natl Acad Sci USA 84:5690-5694.
41. Reardon D, Farber GK. 1995. The structure and evolution of α/β barrel proteins. FASEB J 9:497-503.
42. Rehaber V, Jaenicke R. 1992. Stability and reconstitution of D-glyceraldehyde3-phosphate dehydrogenase from the hyperthermophilic eubacterium Thermotoga maritima. J Biol Chem 267:10999-11006.
43. Rudolph J, Stubbe J. 1995. Investigation of the mechanism of phosphoribosylamine transfer from glutamine phosphoribosylpyrophosphate amidotransferase to glycinamide ribonucleotide synthetase. Biochemistry 34:2241-2250.
44. Sambrook J, Fritsch EF, Maniatis E. 1989. Molecular cloning: A laboratory manual. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
45. Sanangelantoni AM, Forlani G, Ambroselli F, Cammarano P, Tiboni O. 1992. The glnA gene of the extremely thermophilic eubacterium Thermotoga maritima: Cloning, primary structure, and expression in Escherichia coli. J Gen Microbiol 138:383-393.
46. Scholz S, Sonnenbichler J, Schäfer W, Hensel R. 1992. Di-myo-inisitol-1′,1′-phosphate: A new inositol phosphate isolated from Pyrococcus woesei. FEBS Lett 306:239-242.
47. Schurig H, Beaucamp N, Ostendorp R, Jaenicke R, Adler E, Knowles JR. 1995a. Phosphoglycerate kinase and triosephosphate isomerase from the hyperthermophilic bacterium Thermotoga maritima form a covalent bifunctional enzyme complex. EMBO J 14:442-451.
48. Schurig H, Rutkat K, Rachel R, Jaenicke R. 1995b. Octameric enolase from the hyperthermophilic bacterium Thermotoga maritima: Purification, characterization, and image processing. Protein Sci 4:228-236.
49. Srivastava DK, Smolen P, Betts GF, Fukushima T, Spivey HO, Bernhard SA. 1989. Direct transfer of NADH between alpha-glycerol phosphate dehydrogenase and lactate dehydrogenase: Fact or misinterpretation? Proc Natl Acad Sci USA 86:6464-6468.
50. 8-Barrel proteins of tryptophan biosynthesis in the hyperthermophile Thermotoga maritima. EMBO J 14:4395-4402.
51. Stetter KO, Fiala G, Huber G, Huber R, Segerer A. 1990. Hyperthermophilic microorganisms. FEMS Microbiol Rev 75:117-124.
52. Stoll VS, Blanchard JS. 1990. Buffers: Principle and practice. Methods Enzymol 182:24-38.
53. Stüber D, Matile H, Garotta G. 1990. System for high-level production in Escherichia coli and rapid purification of recombinant proteins: Application to epitope mapping, preparation of antibodies, and structure-function analysis. In: Lefkovits I, Pernis B, eds. Immunological methods, vol IV. Orlando, Florida: Academic Press. pp 121-152.
54. Tiboni O, Sanangelantoni AM, Cammarano P, Di Pasquale G, Sora S. 1989. Expression in Escherichia coli of the tuf gene from the extremely thermophilic eubacterium Thermotoga maritima: Purification of the Thermotoga elongation Factor Tu by thermal denaturation of the mesophile host cell proteins. System Appl Microbiol 12:127-133.
55. Tomschy A, Glockshuber R, Jaenicke R. 1993. Functional expression of D-glyceraldehyde-3-phosphate dehydrogenase from the hyperthermophilic eubacterium Thermotoga maritima in Escherichia coli. Eur J Biochem 214:43-50.
56. Vieille C, Hess JM, Kelly RM, Zeikus JG. 1995. xylA cloning and sequencing and biochemical characterization of xylose isomerase from Thermotoga neapolitana. Appl Environ Microbiol 61:1867-1875.
57. Wilmanns M, Priestle JP, Niermann T, Jansonius JN. 1992. Three-dimensional structure of the bifunctional enzyme phosphoribosylanthranilate isomerase:indoleglycerolphosphate synthase from Escherichia coli refined at 2.0 A° resolution. J Mol Biol 223:477-507.
58. Winterhalter C, Heinrich P, Candussio A, Wich G, Liebl W. 1995. Identification of a novel cellulose-binding domain within the multidomain 120 kDa xylanase XynA of the hyperthermophilic bacterium Thermotoga maritima. Mol Microbiol 15:431-444.
59. Woese CR, Kandler O, Wheelis ML. 1990. Towards a natural system of organisms: Proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci USA 87:4576-4579.
60. Wrba A, Jaenicke R, Huber R, Stetter KO. 1990a. Lactate dehydrogenase from the extreme thermophile Thermotoga maritima. Eur J Biochem 188:195-201.
61. Wrba A, Schweiger A, Schultes V, Jaenicke R, Zavodszky P. 1990b. Extremely thermostable D-glyceraldehyde-3-phosphate dehydrogenase from the eubacterium Thermotoga maritima. Biochemistry 29:7584-7592.
62. Yaylayan V, Huyghues-Despointes A. 1994. Chemistry of Amadori rearrangement products: Analysis, synthesis, kinetics, reactions, and spectroscopic properties. Crit Rev Food Sci Nutr 34:321-369.