The crystal structure of an Fe-superoxide dismutase from the hyperthermophile Aquifex pyrophilus at 1.9 Å resolution: Structural basis for thermostability

Journal of Molecular Biology

Volumn 270, Issue 2, 1997, Pages 259-274

  Lim, Jae Hwan ^b   Yu, Yeon Gyu ^b   Han, Ye Sun ^b   Cho, Seung Je ^b   Ahn, Byung Yoon ^b   Kim, Sung Hou ^b   Cho, Yunje ^a  

^a Korea Institute of Science and Technology   (South Korea)

^b NONE

Author keywords

Aquifex pyrophilus; Hyperthermophile; Ion pair; Superoxide dismutase; Thermostability

Indexed keywords

IRON COMPLEX; MONOMER; SUPEROXIDE DISMUTASE; TETRAMER;

ARTICLE; CARBOXY TERMINAL SEQUENCE; COMPARATIVE STUDY; CRYSTAL STRUCTURE; HYPERTHERMIA; NONHUMAN; PRIORITY JOURNAL; PROTEIN QUATERNARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; R FACTOR; THERMOPHILIC BACTERIUM; THERMOSTABILITY;

AQUIFEX PYROPHILUS; BACTERIA (MICROORGANISMS);

EID: 0030748521     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1997.1105     Document Type: Article

References (44)

1. Adams M. W. W. Enzymes and proteins from organisms that grow near and above 100°C. Annu. Rev. Microbiol. 47:1993;627-658.
2. Barlow D. J., Thornton J. M. Ion-pairs in proteins. J. Mol. Biol. 168:1983;867-885.
3. Brünger A. T. X-PLOR Version 3.1. 1992;Yale University Press, New Haven and London.
4. Chan M. K., Mukund S., Kletzin A., Adams M. W. W., Rees D. C. Structure of a hyperthermophilic tungstopterin enzyme, aldehyde ferredoxin oxidoreductase. Science. 267:1995;1463-1469.
5. Cooper J. B., McIntyre K., Badasso M. O., Wood S. P., Zhang Y., Garbe T. R., Young D. X-ray structure analysis of the iron-dependent superoxide dismutase from Mycobacterium tuberculosis at 2.0 Å resolution reveals novel dimer-dimer interactions. J. Mol. Biol. 246:1995;531-544.
6. Dao-pin S., Anderson D. E., Baase W. A., Dahlquist F. W., Matthews B. W. Structural and thermodynamic consequences of burying a charged residue within the hydrophobic of T4 lysozyme. Biochemistry. 30:1991;11521-11529.
7. Delboni L. F. et al. 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. 4:1995;2594-2604.
8. Engh R. A., Huber R. Accurate bond and angle parameters for X-ray protein structure refinement. Acta Crystallog. sect. A. 47:1991;392-400.
9. Fee J. A. Superoxide, superoxide dismutases and oxygen toxicity. Metal ion Activation of Dioxygen. 1980;Wiley & Sons, New York.
10. Fridovich I. Superoxide and superoxide dismutases. Eichhorn G. L., Marzelli L. G. Advances in Inorganic Biochemistry. 1979;Elsevier, Amsterdam.
11. Hendsch Z. S., Tidor B. Do salt bridges stabilize proteins? A continuum electrostatic analysis. Protein Sci. 3:1994;211-226.
12. Hennig M., Darimont B., Sterner R., Kirschner K., Jansonius J. N. 2.0 Å structure of indole-3-glycerolphosphate synthetase from the hyperthermophile Sulfolobus solfataricus: possible determinants of protein stability. Structure. 3:1995;1295-1306.
13. Honig B., Nicholls A. Classical electrostatics in biology and chemistry. Science. 268:1995;1144-1149.
14. Huber R., Wilharm T., Huber D., Tricone A., Burggraf S., Koning H., Rachel R., Rockinger I., Fricke H., Stetter K. O. Aquifex pyrophilus gen. nov. sp. nov., represents a novel group of marine hyperthermophilic hydrogen-oxidizing bacteria. Syst. Appl. Microbiol. 15:1992;340-351.
15. Kabsch W., Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers. 22:1983;2577-2637.
16. Kleywegt G. T., Jones T. A. Detection, delineation, measurement and display of cavities in macromolecular structures. Acta Crystallog. sect. D. 50:1994;178-185.
17. Korolev S., Nayal M., Barnes W. M., Di Cera E., Waksman G. Crystal structure of the large fragment of Thermus aquaticus DNA polymerase I at 2.5 Å resolution: structural basis for thermostability. Proc. Natl Acad. Sci. USA. 92:1995;9264-9268.
18. Korndorfer I., Steipe B., Huber R., Tomschy A., Jaenicke R. The crystal structure of holo-glyceraldehyde-3-phosphate dehydrogenase from the hyperthermophilic bacterium Thermotoga maritima at 2.5 Å resolution. J. Mol. Biol. 246:1995;511-521.
19. Kraulis P. J. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24:1991;946-950.
20. Kusunose E., Ichihara K., Noda Y., Kusunose M. Superoxide dismutase from Mycobacterium tubrerculosis. J. Biochem. 80:1976;1343-1352.
21. Lah M. S., Dixon M. M., Pattridge K. A., Stallings W. C., Fee J. A., Ludwig M. L. Structure-function in Escherichia coli Iron Superoxide dismutase: comparisons with the manganese enzyme from Thermus thermophilus. Biochemistry. 34:1995;1646-1660.
22. Laskowski R. A., MacArther M. W., Moss D. S., Thornton J. M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallog. 26:1993;283-291.
23. Lim J.-H., Yu Y. G., Choi I.-G., Ryu J.-R., Ahn B.-Y., Kim S.-H., Han Y.-S. Cloning and expression of superoxide dismutase from Aquifex pyrophilus, a hyperthermophilic bacterium. FEBS Letters, 406:1997;142-146.
24. Ludwig M. L., Metztger A. L., Pattridge K. A., Stallings W. C. Manganese superoxide dismutase from Thermus thermophilus. A structural model refined at 1.8 Å resolution. J. Mol. Biol. 219:1991;335-358.
25. McCord J., Fridovich I. Superoxide dismutase. J. Biol. Chem. 244:1969;6049-6055.
26. Menendez-Arias L., Argos P. Engineering protein thermal stability. Sequence statistics point to residue substitutions in α-helices. J. Mol. Biol. 206:1989;397-406.
27. Mrabet N. T., Van den Broeck A., Van den brande I., Stanssens P., Laroche Y., Lambeir A.-M., Matthijssens G., Jenkins J., Chiadmi M., van Tilbeurgh H. Arginine residues as stabilizing elements in proteins. Biochemistry. 31:1992;2239-2253.
28. Navaza J. AMoRe: an automated package for molecular replacement. Acta Crystallog. sect. A. 50:1994;157-163.
29. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation method. Methods Enzymol. 276:1997;in the press.
30. Perutz M. F. Electrostastic effects in proteins. Science. 210:1978;1187-1191.
31. Perutz M., Raidt H. Stereochemical basis of heat stability in bacterial ferredoxins and in hemoglobin A2. Nature. 255:1975;255-259.
32. Richards F. M. Areas, volumes, packing and protein structure. Annu. Rev. Biophys. Bioeng. 6:1977;151-175.
33. Russel R. J. M., Hough D. W., Danson M. J., Taylor G. L. The crystal structure of citrate synthase from the thermophilic Archaeon, Thermoplasma acidophilum. Structure. 2:1994;1157-1167.
34. Sacks J. S. CHAIN: a crystallographic modelling program. J. Mol. Graph. 6:1988;224-225.
35. Sato S., Harris J. I. Superoxide dismutase from Thermus aquaticus. Eur. J. Biochem. 73:1977;373-381.
36. Sines J., Allison S., Wierzbicki A., McCammon J. A. Brownian dynamics simulation of the superoxide-superoxide disutase reaction: iron and manganase enzymes. J. Phys. Chem. 94:1990;959-961.
37. Stetter K. O., Fiala G., Huber G., Huber R., Segerer G. Hyperthermophilic microorganisms. FEMS Microbiol. Rev. 75:1990;117-124.
38. Stoddard B. L., Howell P. L., Ringe D., Petsko G. A. The 2.1 Å resolution structure of iron superoxide dismutase from Pseudomonas ovalis. Biochemistry. 29:1990;8885-8893.
39. Tanner J. J., Hecht R. M., Krause K. L. Determinants of enzyme thermostability observed in the molecular surface of Thermus aquaticus D-glyceraldehyde-3-phosphate dehydrogenase at 2.5 Å resolution. Biochemistry. 35:1996;2597-2609.
40. Tsai C.-J., Lin S. L., Wolfson H. J., Nussinov R. Studies of protein-protein interfaces: A statistical analysis of the hydrophobic effect. Protein Sci. 6:1997;53-64.
41. Waldburger C. D., Schildbach J. F., Sauer R. T. Are buried salt bridges important for protein stability and conformational specificity? Nature Struct. Biol. 2:1995;122-128.
42. Wishart D. S., Boyko R. F., Willard L., Richards F. M., Sykes B. D. SEQSEE: a comprehensive program suite for protein sequence analysis. Com. Appl. Biosci. 10:1994;121-132.
43. Xu D., Lin S. L., Nussinov R. Protein binding versus protein folding: the role of hydrophilic bridges in protein association. J. Mol. Biol. 265:1997;68-84.
44. Yip K. S. P., Stillman T. J., Britton K. L., Artymiuk P. J., Baker P. J., Sedelnikova S. E., Engel P. C., Pasquo A., Chiaraluce R., Consalvi V. The structure of Pyrococcus furiosus glutamate dehydrogenase reveals a key role for ion-pair networks in maintaining enzyme stability at extreme temperatures. Structure. 3:1995;1147-1158.