Refined crystal structure of a superoxide dismutase from the hyperthermophilic archaeon Sulfolobus acidocaldarius at 2.2 Å resolution

Journal of Molecular Biology

Volumn 285, Issue 2, 1999, Pages 689-702

  Knapp, Stefan ^a   Kardinahl, Simone ^b   Hellgren, Niklas ^a   Tibbelin, Gudrun ^a   Schäfer, Günter ^b   Ladenstein, Rudolf ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UNIVERSITY OF LÜBECK   (Germany)

Author keywords

Archaea; Protein structure; Sulfolobus acidocaldarius; Superoxide dismutase; Thermostability

Indexed keywords

SUPEROXIDE DISMUTASE;

ARCHAEBACTERIUM; ARTICLE; COMPARATIVE STUDY; CRYSTAL STRUCTURE; HYDROPHOBICITY; MYCOPLASMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; SULFOLOBUS ACIDOCALDARIUS; THERMOSTABILITY; THERMUS THERMOPHILUS;

AQUIFEX PYROPHILUS; ARCHAEA; BACTERIA (MICROORGANISMS); MYCOPLASMA; MYCOPLASMA TUBERCULOSIS; NEGIBACTERIA; SULFOLOBUS ACIDOCALDARIUS; THERMUS THERMOPHILUS;

EID: 0033555252     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1998.2344     Document Type: Article

References (66)

1. Albert T., Dao-pin S., Wilson K., Wozniak J. A., Cook S. P., Matthews B. W. Contributions of hydrogen bonds of Thr157 to the thermodynamic stability of phage T4 lysozyme. Nature. 330:1987;41-46.
2. Anderson D. E., Becktel W. J., Dahlquist F. W. pH-Induced denaturation of proteins: a single salt bridge contributes 3-5 kcal/mol to the free energy of folding of T4 lysozyme. Biochemistry. 29:1990;2403-2408.
3. Auerbach G., Ostendorp R., Prade L., Korndörfer I., Dams T., Huber R., Jaenicke R. Lactate dehydrogenase from the hyperthermophilic bacterium Thermotoga maritima: the crystal structure at 2.1 Å resolution reveals strategies for intrinsic protein stabilization. Structure. 6:1998;769-781.
4. Bode W., Schirmer T. Determination of the protein content of crystals formed by Mastigocladus laminosus C-phycocyanin,Chroomonas spec. phycocyanin-645 and modified human fibrinogen using an improved Ficoll density gradient method. Biol. Chem. 366:1985;287-295.
5. Bordo D., Djinovic-Carugo K., Bolognesi M. Conserved patterns in superoxide dismutase structure. J. Mol. Biol. 238:1994;366-386.
6. Borgstahl G. E. O., Parge H. E., Hickey M. J., Beyer W. F., Hellewell R. A., Tainer J. A. The structure of human mitochondrial manganese superoxide dismutase reveals a novel tetrameric interface of two 4-helix bundles. Cell. 71:1992;107-118.
7. Brünger A. T. Extension of molecular replacement: a new strategy based on Patterson correlation refinement. Acta Crystallog. sect. A. 46:1990;46-57.
8. Brünger A. T. X-PLOR (version 3.1) Manual. 1992a;Yale University Press, New Haven and London.
9. Brünger A. T. Free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature. 255:1992b;472-475.
10. Carlson M. RIBBON 2.0. J. Appl. Crystallog. 24:1991;958-961.
11. Chan M. K., Mukund S., Kletzin A., Adams M. W. W., Rees D. C. Structure of a hyperthermophilic tungstopterin enzyme, aldehyde ferredoxine oxidoreductase. Science. 267:1995;1463-1469.
12. Acta Crystallog. sect. D. 50:1994;760-763.
13. 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 Ångstroms resolution reveals novel dimer-dimer interactions. J. Mol. Biol. 246:1995;531-544.
14. Dao-pin S., Sauer U., Nicholson H., Matthews B. W. Contributions of 13 engineered surface salt bridges to the stability of T4 lysozyme determined by directed mutagenesis. Biochemistry. 30:1991;7142-7153.
15. Engh R. A., Huber R. Accurate bond and angle parameters for X-ray protein structure refinement. Acta Crystallog. sect. A. 47:1991;392-400.
16. Fuginaga M., Read R. J. Experiences with a new translation function program. J. Appl. Crystallog. 20:1987;517-521.
17. Getzoff E. D., Tainer J. A., Stempien M. M., Bell G. I., Hallewell R. A. Evolution of Cu, Zn superoxide dismutases and the greek-key β-barrel structural motive. Proteins: Struct. Funct. Genet. 5:1989;322-336.
18. Hecht K., Wrba A., Jaenike R. Catalytic properties of thermophilic LDH and halophilic MDH at high temperature and low water activity. Eur. J. Biochem. 183:1990;69-74.
19. Hennig M., Darimont B., Sterner R., Kirschner K., Jansonius J. N. 2.0 Å structure of indole-3-glycerol phosphate synthase from the hyperthermophile Sulfolobus solfataricus: possible determinants of protein stability. Structure. 3:1995;1295-1306.
20. Horovitz A., Serrano L., Avron B., Bycroft M., Fersht A. R. Strength and co-operativity of surface salt bridges to protein stability. J. Mol. Biol. 216:1990;1031-1044.
21. Hunter T., Ikebukuro K., Bannister W. H., Bannister J. V., Hunter G. The conserved residues tyrosine 34 is essential for maximal activity of iron-superoxide dismutase from Escherichia coli. Biochemistry. 36:1997;4925-4933.
22. Jones, T. A. Kjeldgaard, M. 1991, O-The manual, Uppsala, Sweden.
23. Kabsch W., Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen bonded and geometrical features. Biopolymers. 22:1983;2577-2637.
24. Kardinahl S., Schmidt C. L., Petersen A., Schäfer G. Isolation, characterization and crystallization of an iron-superoxide dismutase from the cren-archaeon Sulfolobus acidocaldarius. FEMS Microbiol. Letters. 138:1996;65-70.
25. Kelly C. A., Nishiyama M., Ohnishi Y., Beppu T., Birktoft J. J. Determinants of protein stability in the 1.9 Å crystal structure of malate dehydrogenase from the thermophilic bacterium Thermus flavus. Biochemistry. 32:1993;3913-3922.
26. Kirby T. W., Lancaster J. R., Fridovich I. Isolation and characterization of the iron-containing superoxide dismutase of Methanobacterium bryantii. Arch. Biochem. Biophys. 210:1981;140-148.
27. Klenk H. P., Schleper C., Schwass V., Brudler R. Nucleotide sequence, transcription and phylogeny of the gene encoding the superoxid dismutase of Sulfolobus acidocaldarius. Biochim. Biophys. Acta. 1174:1993;95-98.
28. Kleywegt, G. J. Jones, T. A. 1993a, Masks made easy, ESF/CCP4 Newsletter, 28, 56, 59.
29. Kleywegt G. J., Jones T. A. Biomolecular speleology. ESF/CCP4. Newsletter. 29:1993b;26-28.
30. Kleywegt G. J., Jones T. A. Halloween, masks and bones. From First Map to Final Model. 1994;. p. 59-66.
31. Knapp S., de-Vos W., Rice D. W., Ladenstein R. Crystal structure of glutamate dehydrogenase from the hyperthermophilic eubacterium Thermotoga maritima at 3.0 Å resolution. J. Mol. Biol. 267:1997;916-932.
32. Korndörfer I., Steipe B., Huber R., Tomschy A., Jaenicke R. The crystal structure of holo-glyceraldehyde-3-phosphate dehydrogenase from the hyperthermophilic bacteriumThermotoga maritima at 2.5 Å resolution. J. Mol. Biol. 246:1995;511-521.
33. 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.
34. Kroll J. S., Langford P. R., Loynds B. M. Copper-zinc superoxide dismutases of Haemophilus influenzae and H. parainfluenzae. J. Bacteriol. 173:1991;7449-7457.
35. Kusunose E., Ichihara K., Noda Y., Kusunose M. Superoxide dismutase from Mycobacterium tuberculosis. J. Biochem. 80:1976;1343-1352.
36. Lah M. S., Dixon M. M., Pattridge K. A., Stallings W., Fee J. A., Ludwig M. L. Structure-Function in Escherichia coli iron superoxide dismutase: comparisons with the manganese enzyme fromThermus thermophilus. Biochemistry. 34:1995;1646-1660.
37. Laskowski R. A., MacArthur 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.
38. Lavelle K. F., McAdam M. E., Fielden E. M., Roberts P. B. A pulse-radiolysis study of the catalytic mechanism of the iron-containing superoxide dismutase from Photobacterium leiognathi. Biochem. J. 161:1977;3-11.
39. Lim J.-H., Yu Y. G., Han Y. S., Cho S., Ahn B.-Y., Kim S.-H., Cho Y. The crystal structure of an Fe-Superoxide dismutase from the hyperthermophile Aquifex pyrophilus at 1.9 Å resolution: structural basis for thermostability. J. Mol. Biol. 270:1997;259-274.
40. Ludwig M. L., Metzger 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.
41. Matthews B. W. Solvent content of protein crystals. J. Mol. Biol. 33:1968;491-497.
42. Matthews B. W. Structural and genetic analysis of protein stability. Annu. Rev. Biochem. 62:1993;139-160.
43. McAdam M. E., Fox R. A., Lavelle F., Fielden E. M. A pulse-radiolysis study of the catalytic mechanism of the manganese-containing superoxide dismutase from Bacillus stearothennophilus. A kinetic model for the enzyme action. Biochem. J. 165:1977;71-79.
44. Nicholls A., Sharp K., Honig B. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins: Struct. Funct. Genet. 11:1991;281-296.
45. Nicolson H., Becktel W. J., Matthews B. W. Enhanced protein thermostability from designed mutations that interact with alpha-helix dipols. Nature. 336:1988;651-656.
46. Nicolson H., Anderson D. E., Dao-pin S., Matthews B. W. Analysis of the interaction between charged side chains and the a-helix dipole using designed thermostable mutants of Phage T4 lysozyme. Biochemistry. 30:1991;9816-9828.
47. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:1997;307-326.
48. Parker M. W., Blake C. C. F. Crystal structure of manganese superoxide dismutase from Bacillus stearothermophilus at 2.4 Å resolution. J. Mol. Biol. 199:1988;649-661.
49. Perutz F. M., Raidt H. Stereochemical basis of heat stability in bacterial ferredoxins and in haemoglobin A2. Nature. 255:1975;256-259.
50. Ramachandran G. N., Sasisekharan V. Conformation of polypeptides and proteins. Advan. Protein Chem. 23:1968;283-437.
51. Russell R. J. M., Hough D. W., Danson M. J., Garry L. T. The crystal structure of citrate synthase from the thermophilic archaeon Thermoplasma acidophilum. Structure. 2:1994;1157-1167.
52. Sato S., Harris J. I. Superoxide dismutase from Thermus aquaticus. Eur. J. Biochem. 73:1977;373-381.
53. Schmidt M., Meier B., Parak F. X-ray structure of the cambialistic superoxide dismutase from Propionibacterium shermanii active with Fe or Mn. J. Bioinorg. Chem. 1:1997;532-541.
54. Searcy K. B., Searcy D. G. Superoxide dismutase from the archaebacterium Thermoplasma acidophilum. Biochim. Biophys. Acta. 670:1981;39-46.
55. Sines J., Allison S., Wierzbicki A., McCammon J. A. Brownian dynamics simulation of the superoxide-superoxide dismutase reaction: iron and manganese enzymes. J. Phys. Chem. 94:1990;959-961.
56. Spassov V. Z., Karshikoff A. D., Ladenstein R. The optimization of protein-solvent interactions: thermostability and the role of hydrophobic interactions. Protein Sci. 4:1995;1516-1527.
57. Stallings W. C., Powers T. B., Pattridge K. A., Fee J. A., Ludwig M. L. Iron superoxide dismutase from Escherichia coli at 3.1-Å resolution: a structure unlike that of copper/zinc protein at both monomer and dimer levels. Proc. Natl Acad. Sci. USA. 80:1983;3884-3888.
58. Stallings W. C., Pattridge K. A., Strong R. K., Ludwig M. L. The structure of manganese superoxide dismutase from Thermus thermophilus at 2.4 Å resolution. J. Biol. Chem. 260:1985;16424-16432.
59. Steinman H. M., Ely B. Copper-zinc superoxide dismutase of Caulobacter crescentus: cloning, sequencing and mapping of the gene and periplasmic location of the enzyme. J. Bacteriol. 172:1990;2901-2910.
60. 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.
61. Takao M., Oikawa A., Yasui A. Characterization of a superoxide dismutase gene from the archaebacterium. Methanobacterium thermoautotrophicum. Arch. Biochem. Biophys. 283:1990;210-216.
62. Tanner J. J., Hecht R. M., Krause K. L. Determinants of enzyme thermostability observed in the molecular surface of Thermus aquaticus D-glycer-aldehyde-3-phosphate dehydrogenase at 2.5 Å resolution. Biochemistry. 35:1996;2597-2609.
63. Vihinen M. Relationship of protein flexibility to thermostability. Protein Eng. 1:1987;477-480.
64. Vriend G. WHATIF-The Manual. 1995.
65. 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., Scandurra R., Rice D. W. 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.
66. Youn H.-D., Kim E.-J., Roe J.-H., Hah Y. C., Kang S.-O. A novel nickel-containing superoxide dismutase from Streptomyces spp. Biochem. J. 318:1996;889-896.