An unusual route to thermostability disclosed by the comparison of Thermus thermophilus and Escherichia coli inorganic pyrophosphatases

Protein Science

Volumn 5, Issue 6, 1996, Pages 1014-1025

  Salminen, Tiina ^a,b   Teplyakov, Alexei ^c   Kankare, Jussi ^b   Cooperman, Barry S ^d   Lahti, Reijo ^a   Goldman, Adrian ^a,b  

^a UNIVERSITY OF TURKU   (Finland)

^b TURKU CENTRE FOR BIOTECHNOLOGY   (Finland)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

inorganic pyrophosphatase; protein structure; structural analysis; thermostability

Indexed keywords

ARTICLE; CARBOXY TERMINAL SEQUENCE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME BINDING; ESCHERICHIA COLI; HYDROGEN BOND; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STRUCTURE; THERMOSTABILITY; THERMUS THERMOPHILUS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; THERMUS THERMOPHILUS;

EID: 0029896617     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1002/pro.5560050604     Document Type: Article

References (56)

1. Argos P, Rossmann MG, Grau UM, Zuber H, Frank G, Tratschin JD. 1979. Thermal stability and protein structure. Biochemistry 18:5698-5703.
2. Barlow DJ, Thornton JM. 1983. Ion-pairs in proteins. J Mol Biol 168: 857-885.
3. Baykov AA, Dudarenkov VY, Kasho VN, Käpyla J, Salminen T, Hyytiä T, Cooperman B, Goldman A, Lahti R. 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.
4. ++ dependence. Biochemistry. Forthcoming.
5. Baykov AA, Shestakov AS, Kasho VN, Vener AV, Ivanov AH. 1990. Kinetics and thermodynamics of catalysis by the inorganic pyrophosphatase of Escherichia coli in both directions. Eur J Biochem 194:879-887.
6. Bernstein FC, Koetzle TF, Williams GJB, Meyer EF Jr, Brice MD, Rodgers JR, Kennard O, Shimanouchi T, Tasumi M. 1977. The Protein Data Bank: A computer-based archival file for macromolecular structures. J Mol Biol 112:535-542.
7. Blaber M, Zhang Xj, Matthews BW. 1993. Structural basis of amino acid α helix propensity. Science 260:1631-1640.
8. Brunger AT. 1992. X-PLOR, version 3.1. A system for X-ray crystallography and NMR. New Haven, Connecticut: Yale University Press.
9. Brunger AT, Kuriyan J, Karplus M. 1987. Crystallographic R factor refinement by molecular dynamics. Science 255:458-460.
10. Buerger MJ, Arnold H, Fischer W, Langtet GA. 1987. In: Hahn T, ed. International tables for crystallography, 2nd ed, vol A. Dordrecht, Germany: D. Reidel Publishing Company, pp 506-507.
11. Chakrabartty A, Kortemme T, Baldwin RL. 1994. Helix propensities of the amino acids measured in alanine-based peptides without helix-stabilizing side-chain interactions. Protein Sci 3:843-852.
12. Chan MK, Mukund S, Kietzin A, Adams MWW, Rees DC. 1995. Structure of a hyperthermophilic tungstopterin enzyme, aldehyde ferredoxin oxidoreductase. Science 267:1463-1469.
13. Chen J, Brevet A, Fromant M, Lévèque F, Schmitter JM, Blanquet S, Plateau P. 1990. Pyrophosphatase is essential for growth of Escherichia coli. J Bacteriol 172:5686-5689.
14. Cooperman BS. 1982. The mechanism of action of yeast inorganic pyrophosphatase. Methods Enzymol 87:526-548.
15. Creamer TP, Rose GD. 1994. Alpha-helix-forming propensities in peptides and proteins. Proteins Struct Funct Genet 19:85-97.
16. Delboni LF, Mande SC, Remier-Delrue 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.
17. Fitzgerald PMD. 1988. MERLOT, an integrated package of computer programs for the determination of crystal structures by molecular replacement. J Appl Crystallogr 20:886-891.
18. Fleischmann RD, Adams MD, White O, Clayton RA, Kirkness EF, Kerlavage AR, Bult CJ, Tomb JF, Dougherty BA, Merrick JM, Mckenney K, Sutton G, Fitzhugh W, Fields CA, Gocayne JD, Scott JD, Shirley R, Liu LI, Glodek A, Kelley JM, Weidman JF, Phillips CA, Spriggs T, Hedblom E, Cotton MD, Utterback TR, Hanna MC, Nguyen DT, Saudek DM, Brandon RC, Fine LD, Fritchman JL, Fuhrmann JL, Geoghagen NSM, Gnehm CL, McDonald LA, Small KV, Fraser CM, Smith HO, Venter JC. 1995. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269:4-69-512.
19. Fraser CM, Gocayne JD, White O, Adams MD, Clayton RA, Fleischmann RD, Bult CJ, Kerlavage AR, Sutton G, Kelley JM, Fritchman JL, Weidman JF, Small KV, Sandusky M, Fuhrmann JL, Nguyen DT, Utterback TR, Saudek DM, Phillips CA, Merrick JM, Tomb JF, Dougherty BA, Bott KF, Hu PC, Lucier TS, Peterson SN, Smith HO, Hutchison CA III, Venter JC. 1995. The minimal gene complement of Mycoplasma genitalium. Science 270:397-403.
20. Heikinheimo P, Salminen T, Cooperman B, Lahti R, Goldman A 1995. New crystal forms of E. coli and S. cerevisiae soluble inorganic pyrophosphatases. Acta Crystallogr D 51:399-401.
21. Hendrickson WA, Konnert JH. 1981. Stereochemically restrained crystallographic least-squares refinement of macromolecular structures. In: Srinivasan R, ed. Biomolecular structure, conformation, function and evolution, vol 1. Oxford, UK: Pergamon Press, pp 43-57.
22. Hennig M, Darimont B, Sterner R, Kirschner K, Jansonius JN. 1995. 2.0 Å structure of indole-3-glycerolphosphate synthase from the hyperthermophile Sulfolobus solfataricus: Possible determinants of protein stability. Structure 3:1295-1306.
23. +-A possible model for enzymatic phosphoryl transfer. Biochemistry 29:5172-5179.
24. Höhne WE, Wessner H, Kuranova IP, Oblomova GV. 1988. Kinetic characterization of a thermostable inorganic pyrophosphatase from Thermus thermophilus. Biomed Biochim Acta 47:941-947.
25. Honig B, Nicholls A. 1995. Classical electrostatics in biology and chemistry. Science 268:1144-1149.
26. Ichiba T, Shibasaki T, Iizuka E, Hachimori A, Samejima T. 1988. Cation-induced thermostability of yeast and Escherichia coli pyrophosphatases. Biochem Cell Biol 66:25-31.
27. Ichiba T, Takenaka O, Samejima T, Hachimori A. 1990. Primary structure of the inorganic pyrophosphatase from thermophilic bacterium PS-3. J Biochem 108:572-578.
28. Jones TA, Zou JY, Cowan SW, Kjeldgaard M. 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.
29. Kankare J, Salminen T, Lahti R, Cooperman BS, Baykov AA, Goldman A. 1996a. Crystallographic identification of metal-binding sites in E. coli inorganic pyrophosphatase. Biochemistry. Forthcoming.
30. Kankare J, Salminen T, Lahti R, Cooperman BS, Baykov AA, Goldman A. 1996b. The structure of E. coli inorganic pyrophosphatase at 2.2 Å resolution Acta Crystallogr D. Forthcoming.
31. Khechinashvili NN, Janin J, Rodier F. 1995. Thermodynamics of the temperature-induced unfolding of globular proteins. Protein Sci 4:1315-1324.
32. Kleywegt GJ, Jones TA. 1994. Detection, delineation, measurement and display of cavities in macromolecular structures. Acta Crystallogr D 50: 178-185.
33. 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 245:511-521.
34. Korolev S, Nayal M, Barnes WM, Cera Ed, Waksman G. 1995. Crystal structure of the large fragment of Thermos aquaticus DNA polymerase I at 2.5 Å resolution: Structural basis for thermostability. Proc Natl Acad Sci USA 92:9264-9268.
35. Kraulis PJ. 1991. MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures. J Appl Crystallogr 24:946-950.
36. Kuranova IP, Oblomova GV, Konareva NV. 1987. Inorganic pyrophosphatase from the extremely thermophilic bacterium Thermus thermophilus HB8. Biokhimiya 295:1013-1016.
37. Lahti R. 1983. Microbial inorganic pyrophosphates. Microbiol Rev 47: 169-179.
38. Laskowski RA, MacArthur MV, Moss DS, Thornton JM. 1993. PROCHECK: A program to check the stereochemical quality of protein structures. J Appl Crystallogr 26:283-291.
39. Lundin M, Baltscheffsky H, Ronne H. 1991. Yeast PPA2 gene encodes a mitochondrial inorganic pyrophosphatase that is essential for mitochondrial function. J Biol Chem 206:12168-12172.
40. Menendez-Arias L, Argos P. 1989. Engineering protein thermal stability - Sequence statistics point to residue substitution in alpha-helices. J Mol Biol 206:397-406.
41. Meyer W, Moll R, Kath Th, Schafer G. 1995. Purification, cloning, and sequencing of archebacterial pyrophosphatase from the extreme thermoacidophile Sulfolobus acidocaldarius. Arch Biochem Biophys 319: 149-156.
42. Nicholls A, Sharp KA, Honig B. 1991. Protein folding and association: Insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins Struct Funct Genet 11:281-296.
43. Nicholson H, Anderson PE, Dao-pin S, Matthews BW. 1991. Analysis of interactions between charged side chains and the α-helix dipole using designed thermostable mutants of phage T4 lysozyme. Biochemistry 30:9816-9828.
44. Nojima H, Hon-nami K, Oshima T, Noda H. 1978. Reversible thermal unfolding of thermostable cytochrome c-552. J Mol Biol 122:33-42.
45. O'Neil KT, DeGrado WF. 1990. A thermodynamic scale for the helix-forming tendencies of the commonly occurring amino acids. Science 250:646-651.
46. Perutz M, Raidt H. 1975. Stereochemical basis of heat stability in bacterial ferredoxins and in hemoglobin A2. Nature 255:256-259.
47. Richards FM. 1974. The interpretation of protein structures: Total volume, group volume distributions and packing density. J Mol Biol 82:1-14.
48. Richards FM. 1977. Areas, volumes, packing and protein structure. Annu Rev Biophys Bioeng 6:151-175.
49. Richter OMH, Schafer G. 1992. Cloning and sequencing of the gene for the cytoplasmic inorganic pyrophosphatase from the thermoacidophilic archaebacterium Thermoplasma acidophilum. Eur J Biochem 209:350-355.
50. Russell RJM, Hough DW, Danson MJ, Taylor GL. 1994. The crystal structure of citrate synthase from the thermophilic Archaeon, Thermoplasma acidophilum. Structure 2:1157-1167.
51. Serrano L, Fersht AR. 1989. Capping and α-helix stability. Nature 342: 296-299.
52. 1. Biochemistry 31:725-732.
53. Teplyakov A, Obmolova G, Wilson KS, Ishii K, Kaji H, Samejima T, Kuranova I. 1994. Crystal structure of inorganic pyrophosphatase from Thermus thermophilus. Protein Sci 3:1098-1107.
54. Terzyan SS, Voronova AA, Smirnova EA, Kuranova IP, Nekrasov YV, Arutyunyan ÉG, Vainshtein BK, Hohne W, Hansen G. 1984. Spatial structure of yeast inorganic pyrophosphatase at a resolution of 3 Å. Bioorg Khim 10:1469-1482
55. Vriend G. 1990. WHAT IF: A molecular modeling and drug design program. J Mol Graphics 8:52-56.
56. 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.