Crystal Structure of the Hyperthermophilic Inorganic Pyrophosphatase from the Archaeon Pyrococcus horikoshii

Biophysical Journal

Volumn 86, Issue 1 I, 2004, Pages 420-427

  Liu, Binbin ^a,c   Bartlam, Mark ^a,c   Gao, Renjun ^b   Zhou, Weihong ^a   Pang, Hai ^a   Liu, Yiwei ^a   Feng, Yan ^b   Rao, Zihe ^a,c  

^a TSINGHUA UNIVERSITY   (China)

^b JILIN UNIVERSITY   (China)

^c INSTITUTE OF BIOPHYSICS   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; INORGANIC PYROPHOSPHATASE;

ARTICLE; BACTERIAL GENE; CARBOXY TERMINAL SEQUENCE; COMPARATIVE STUDY; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; ENZYME ANALYSIS; ENZYME STRUCTURE; ESCHERICHIA COLI; NONHUMAN; PYROCOCCUS; PYROCOCCUS HORIKOSHII; SULFOLOBUS ACIDOCALDARIUS; THERMOPHILIC BACTERIUM; THERMOSTABILITY; THERMUS THERMOPHILUS;

ARCHAEA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; PYROCOCCUS; PYROCOCCUS HORIKOSHII; SULFOLOBUS ACIDOCALDARIUS; THERMUS; THERMUS THERMOPHILUS; TRIXIS;

EID: 0346057934     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(04)74118-1     Document Type: Article

References (40)

1. Avaeva, S., S. Kurilova, T. Nazarova, E. Rodina, N. Vorobyeva, V. Sklyankina, O. Grigorjeva, E. Harutyunyan, V. Oganessyan, K. Wilson, M. Dauter, R. Huber, and T. Mather. 1997. Crystal structure of Escherichia coli inorganic pyrophosphatase complexed with SO4(2-). Ligand-induced molecular asymmetry. FEBS Lett. 410:502-508.
2. Baykov, A. A., V. Y. Dudarenkov, J. Kapyla, T. Salminen, T. Hyytia, V. N. Kasho, S. Husgafvel, B. S. Cooperman, A. Goldman, and R. Lahti. 1995. Dissociation of hexameric Escherichia coli inorganic pyrophosphatase into trimers on His-136→Gln or His-140→Gln substitution and its effect on enzyme catalytic properties. J Biol Chem. 270:30804-30812.
3. Brunger, A. T., P. D. Adams, G. M. Clore, W. L. DeLano, P. Gros, R. W. Grosse-Kunstleve, J. S. Jiang, J. Kuszewski, M. Nilges, N. S. Pannu, R. J. Read, L. M. Rice, T. Simonson, and G. L. Warren. 1998. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D. 54:905-921.
4. Chen, J., A. Brevet, M. Fromant, F. Leveque, J. M. Schmitter, S. Blanquet, and P. Plateau. 1990. Pyrophosphatase is essential for growth of Escherichia coli. J. Bacteriol. 172:5686-5689.
5. Daggett, V., and M. Levitt. 1993. Protein unfolding pathways explored through molecular dynamics simulations. J. Mol. Biol. 232:600-619.
6. DeDecker, B. S., R. O'Brien, P. J. Fleming, J. H. Geiger, S. P. Jackson, and P. B. Sigler. 1996. The crystal structure of a hyperthermophilic archaeal TATA-box binding protein. J. Mol. Biol. 264:1072-1084.
7. Hansen, T., C. Urbanke, V. M. Leppanen, A. Goldman, K. Brandenburg, and G. Schafer. 1999. The extreme thermostable pyrophosphatase from Sulfolobus acidocaldarius: enzymatic and comparative biophysical characterization. Arch. Biochem. Biophys. 363:135-147.
8. Harris, J. I., J. D. Hocking, M. J. Runswick, K. Suzuki, and J. E. Walker. 1980. D-glyceraldehyde-3-phosphate dehydrogenase. The purification and characterisation of the enzyme from the thermophiles Bacillus stearothermophilus and Thermus aquaticus. Eur. J. Biochem. 108:535-547.
9. Heikinheimo, P., V. Tuominen, A. K. Ahonen, A. Teplyakov, B. S. Cooperman, A. A. Baykov, R. Lahti, and A. Goldman. 2001. Toward a quantum-mechanical description of metal-assisted phosphoryl transfer in pyrophosphatase. Proc. Natl. Acad. Sci. USA. 98:3121-3126.
10. Hennig, M., B. Darimont, R. Sterner, K. Kirschner, and J. N. Jansonius. 1995. 2.0 A structure of indole-3-glycerol phosphate synthase from the hyperthermophile Sulfolobus solfataricus: possible determinants of protein stability. Structure. 3:1295-1306.
11. Hennig, M., R. Sterner, K. Kirschner, and J. N. Jansonius. 1997. Crystal structure at 2.0 A resolution of phosphoribosyl anthranilate isomerase from the hyperthermophile Thermotoga maritima: possible determinants of protein stability. Biochemistry. 36:6009-6016.
12. Hyytia, T., P. Halonen, A. Salminen, A. Goldman, R. Lahti, and B. S. Cooperman. 2001. Ligand binding sites in Escherichia coli inorganic pyrophosphatase: effects of active site mutations. Biochemistry. 40:4645-4653.
13. Ichiba, T., T. Shibasaki, E. Iizuka, A. Hachimori, and T. Samejima. 1998. Cation-induced thermostability of yeast and Escherichia coli pyrophosphatases. Biochem. Cell Biol. 66:25-31.
14. Jones, T. A., J. Y. Zou, S. W. Cowan, and M. Kjeldgaard. 1991. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A. 47:110-119.
15. Kallwass, H. K., W. K. Surewicz, W. Parris, E. L. Macfarlane, M. A. Luyten, C. M. Kay, M. Gold, and J. B. Jones. 1992. Single amino acid substitutions can further increase the stability of a thermophilic L-lactate dehydrogenase. Protein Eng. 5:769-774.
16. Kankare, J., G. S. Neal, T. Salminen, T. Glumhoff, B. S. Cooperman, R. Lahti, and A. Goldman. 1994. The structure of E. coli soluble inorganic pyrophosphatase at 2.7 A resolution. Protein Eng. 7:823-830.
17. Kelly, C. A., M. Nishiyama, Y. Ohnishi, T. Beppu, and J. J. Birktoft. 1993. Determinants of protein thermostability observed in the 1.9-A crystal structure of malate dehydrogenase from the thermophilic bacterium Thermus flavus. Biochemistry. 32:3913-3922.
18. Komdorfer, I., B. Steipe, R. Huber, A. Tomschy, and R. Jaenicke. 1995. The crystal structure of holo-glyceraldehyde-3-phosphate dehydrogenase from the thermophilic bacterium Thermotoga aquaticus DNA polymerase at 2.5 A resolution. J. Mol. Biol. 246:511-521.
19. Lahti, R. 1983. Microbial inorganic pyrophosphatases. Microbiol. Rev. 47:169-179.
20. Laskowski, R. A., M. W. MacArthur, D. S. Moss, and J. M. Thornton. 1993. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26:283-291.
21. Leppanen, V. M., H. Nummelin, T. Hansen, and R. Lahti. 1999. Sulfolobus acidocaldarius inorganic pyrophosphatase: structure, thermostability, and effect of metal ion in an archael pyrophosphatase. Protein Sci. 8:1218-1231.
22. MacBeath, G., P. Kast, and D. Hilvert. 1998. A small, thermostable, and monofunctional chorismate mutase from the archaeon Methanococcus jannaschii. Biochemistry. 37:10062-10073.
23. Masuda, H., T. Uchiumi, M. Wada, T. Ichiba, and A. Hachimori. 2002. Effects of replacement of prolines with alanines on the catalytic activity and thermostability of inorganic pyrophosphatase from thermophilic bacterium PS-3. J. Biochem. (Tokyo). 131:53-58.
24. Matthews, B. W., H. Nicholson, and W. J. Becktel. 1987. Enhanced protein thermostability from site-directed mutations that decrease the entropy of unfolding. Proc. Natl. Acad. Sci. USA. 84:6663-6667.
25. Nakamura, H. 1996. Roles of electrostatic interaction in proteins. Q. Rev. Biophys. 29:1-90.
26. Nojima, H., K. Hon-Nami, T. Oshima, and H. Noda. 1978. Reversible thermal unfolding of thermostable cytochrome c-552. J. Mol. Biol. 122:33-42.
27. Otwinowski, Z., and W. Minor. 1997. Processing of x-ray diffraction data collected in oscillation mode. In: Macromolecular Crystallography, part A. C. W. Carter Jr. and R. M. Sweet, editors. Academic Press. 307-326.
28. Perutz, M., and H. Raidt. 1975. Stereochemical basis of heat thermostability in bacterial ferredoxins and in hemoglobin A2. Nature. 255:256-259.
29. Pfeil, W., V. E. Bychkova, and O. B. Ptitsyn. 1986. Physical nature of the phase transition in globular proteins. Calorimetric study of human alpha-lactalbumin. FEBS Lett. 198:287-291.
30. Richter, O. M., and G. Schafer. 1992. Purification and enzymic characterization of the cytoplasmic pyrophosphatase from the thermoacidophilic archaebacterium Thermoplasma acidophilum. Eur. J. Biochem. 209:343-349.
31. Sakon, J., W. S. Adney, M. E. Himmel, S. R. Thomas, and P. A. Karplus. 1996. Crystal structure of thermostable family 5 endocellulase E1 from Acidothermus cellulolyticus in complex with cellotetraose. Biochemistry. 35:10648-10660.
32. Salminen, T., A. Teplyakov, J. Kankare, B. S. Cooperman, R. Lahti, and A. Goldman. 1996. An unusual route to thermostability disclosed by the comparison of Thermus thermophilus and Escherichia coli inorganic pyrophosphatases. Protein Sci. 5:1014-1025.
33. Scholtz, J. M., H. Qian, V. H. Robbins, and R. L. Baldwin. 1993. The energetics of ion-pair and hydrogen-bonding interactions in a helical peptide. Biochemistry. 32:9668-9676.
34. Sterner, R., T. Vogl, H. J. Hinz, F. Penz, R. Hoff, R. Foll, and H. Decker. 1995. Extreme thermostability of tarantula hemocyanin. FEBS Lett. 364:9-12.
35. Teplyakov, A., G. Obmolova, K. S. Wilson, K. Ishii, H. Kaji, T. Samejima, and I. Kuranova. 1994. Crystal structure of inorganic pyrophosphatase from Thermus thermophilus. Protein Sci. 3:1098-1107.
36. Vander Horn, P. B., M. C. Davis, J. J. Cunniff, C. Ruan, B. F. McArdle, S. B. Samols, J. Szasz, G. Hu, K. M. Hujer, S. T. Domke, S. R. Brummet, R. B. Moffet, and C. W. Fuller. 1997. Thermo Sequenase DNA polymerase and T. acidophilum pyrophosphatase: new thermostable enzymes for DNA sequencing. Biotechniques 22(4):758-762, 764-765.
37. Vetriani, C., D. L. Maeder, N. Tolliday, K. S. Yip, T. J. Stillman, K. L. Britton, D. W. Rice, H. H. Klump, and F. T. Robb. 1998. Protein thermostability above 100 degreesC: a key role for ionic interactions. Proc. Natl. Acad. Sci. USA. 95:12300-12305.
38. Villeret, V., B. Clantin, C. Tricot, C. Legrain, M. Roovers, V. Stalon, N. Glansdorff, and J. Van Beeumen. 1998. The crystal structure of Pyrococcus furiosus ornithine carbamoyltransferase reveals a key role for oligomerization in enzyme stability at extremely high temperatures. Proc. Natl. Acad. Sci. USA. 95:2801-2806.
39. Walker, J. E., A. J. Wonacott, and J. I. Harris. 1980. Heat stability of a tetrameric enzyme, D-glyceraldehyde-3-phosphate dehydrogenase. Eur. J. Biochem. 108:581-586.
40. Yip, K. S., T. J. Stillman, K. L. Britton, P. J. Artymiuk, P. J. Baker, S. E. Sedelnikova, P. C. Engel, A. Pasquo, R. Chiaraluce, and V. Consalvi. 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.