Calcium-mediated thermostability in the subtilisin superfamily: The crystal structure of Bacillus Ak.1 protease at 1.8 Å resolution

Journal of Molecular Biology

Volumn 294, Issue 4, 1999, Pages 1027-1040

  Smith, Clyde A ^a   Toogood, Helen S ^b   Baker, Heather M ^a   Daniel, Roy M ^b   Baker, Edward N ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b UNIVERSITY OF WAIKATO   (New Zealand)

Author keywords

Calcium binding; Crystal structure; Serine protease; Subtilase family; Thermostability

Indexed keywords

BACTERIAL ENZYME; CALCIUM ION; DISULFIDE; PROTEINASE; SUBTILISIN;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; BACILLUS; BINDING SITE; CALCIUM BINDING; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME SUBSTRATE COMPLEX; HYDROPHOBICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DENATURATION; PROTEIN FAMILY; STEREOCHEMISTRY; THERMOSTABILITY;

BACILLUS SP.; BACTERIA (MICROORGANISMS);

EID: 0033544694     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1999.3291     Document Type: Article

References (54)

1. Bajorath J., Hinrichs W., Saenger W. The enzymatic activity of proteinase K is controlled by calcium. Eur. J. Biochem. 176:1988;441-447.
2. Barr P. J. Mammalian subtilisins: the long-sought dibasic processing endoproteases. Cell. 66:1991;1-3.
3. Bernstein F. C., Koetzle T. F., Williams G. J. B., Meyer E. F. J., Brice M. D., Rodgers J. R., Kennard O., Shimanouchi T., Tasumi M. Protein Data Bank: a computer based archival file for macromolecular structures. J. Mol. Biol. 112:1977;535-542.
4. Betzel C., Pal G. P., Saenger W. Three-dimensional structure of proteinase K at 0.15-nm resolution. Eur. J. Biochem. 178:1988;155-171.
5. Betzel C., Teplyakov A. V., Harutyunyan E. H., Saenger W., Wilson K. S. Thermitase and proteinase K: a comparison of the refined three-dimensional structures of the native enzymes. Protein Eng. 3:1990;161-172.
6. Betzel C., Klupsch S., Papendorf G., Hastrup S., Branner S., Wilson K. S. Crystal structure of the alkaline proteinase Savinase from Bacillus lentus at 1.4 Å resolution. J. Mol. Biol. 223:1992;427-445.
7. Bode W., Papamokos E., Musil D. The high-resolution X-ray crystal structure of the complex formed between subtilisin Carlsberg and eglin c, an elastase inhibitor from the leech Hirudo medicinalis. Structural analysis, subtilisin structure and interface geometry. Eur. J. Biochem. 166:1987;673-692.
8. Bott R., Ultsch M., Kossiakoff A., Graycar T., Katz B., Power S. The three-dimensional structure of Bacillus amyloliquefaciens subtilisin at 1.8 Å and an analysis of the structural consequences of peroxide inactivation. J. Biol. Chem. 263:1988;7895-7906.
9. 2+-binding loop into subtilisin BPN′ Biochemistry. 31:1992;7796-7801.
10. Briedigkeit L., Frömmel C. Calcium ion binding by thermitase. FEBS Letters. 253:1989;83-87.
11. Brocchieri L., Karlin S. Geometry of interplanar residue contacts in protein structures. Proc. Natl Acad. Sci. USA. 91:1994;9297-9301.
12. Bryan P., Alexander P., Strausberg S., Schwarz F., Wang L., Gilliland G., Gallagher D. T. Energetics of folding subtilisin BPN′ Biochemistry. 31:1992;4937-4945.
13. Brünger A. T. X-PLOR Version 3.1: A System for Crystallography and NMR. 1990;Yale University, New Haven.
14. Brünger A. T., Karplus M., Petsko G. A. Crystallographic refinement by simulated annealing: application to crambin. Acta Crystallog. sect. A. 45:1989;50-61.
15. Burley S. K., Petsko G. A. Aromatic-aromatic interaction: a mechanism of protein structure stabilization. Science. 229:1985;23-28.
16. Acta Crystallog. sect. D. 50:1994;760-763.
17. Dauter Z., Betzel C., Genov N., Pipon N., Wilson K. S. Complex between the subtilisin from a mesophilic bacterium and the leech inhibitor eglin-C. Acta Crystallog. sect. B. 47:1991;707-730.
18. Drenth J., Hol W. G., Jansonius J. N., Koekoek R. Subtilisin novo. The three-dimensional structure and its comparison with subtilisin BPN'. Eur. J. Biochem. 26:1972;177-181.
19. Engh R. A., Huber R. Accurate bond and angle parameters for X-ray protein structure refinement. Acta Crystallog. sect. A. 47:1991;392-400.
20. Fersht A. R., Serrano L. Principles of protein stability derived from protein engineering experiments. Curr. Opin. Struct. Biol. 3:1993;75-83.
21. Frömmel C., Höhne W. E. Influence of calcium binding on the thermal stability of 'thermitase', a serine protease from Thermoactinomyces vulgaris. Biochim. Biophys. Acta. 670:1981;25-31.
22. Gros P., Betzel C., Dauter Z., Wilson K. S., Hol W. G. Molecular dynamics refinement of a thermitase-eglin-c complex at 1.98 Å resolution and comparison of two crystal forms that differ in calcium content. J. Mol. Biol. 210:1989;347-367.
23. Gros P., Kalk K. H., Hol W. G. Calcium binding to thermitase. Crystallographic studies of thermitase at 0, 5, and 100 mM calcium. J. Biol. Chem. 266:1991;2953-2961.
24. Hunter C. A., Singh J., Thornton J. M. π-π interactions: the geometry and energetics of phenylalanine-phenylalanine interactions in proteins. J. Mol. Biol. 218:1991;837-846.
25. Kingston R. L., Baker H. M., Baker E. N. Search designs for protein crystallization based on orthogonal arrays. Acta Crystallog. sect. D. 50:1994;429-440.
26. Knapp S., de Vos W. M., Rice D., 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.
27. Kraulis P. J. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structure. J. Appl. Crystallog. 24:1991;946-950.
28. Krishnaswamy S., Rossmann M. G. Structural refinement and analysis of Mengo virus. J. Mol. Biol. 211:1990;803-844.
29. Laskowski R., MacArthur M., Moss D., Thornton J. M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallog. 26:1993;283-291.
30. Luzzati V. Traitement statistiques des erreurs dans la determination des structures cristallines. Acta Crystallog. 5:1952;802-810.
31. MacIver B., McHale R. H., Saul D. J., Bergquist P. L. Cloning and sequencing of a serine proteinase gene from a thermophilic Bacillus species and its expression in Escherichia coli. Appl. Env. Microbiol. 60:1994;3981-3988.
32. Matthews B. W. Solvent content of protein crystals. J. Mol. Biol. 33:1968;491-497.
33. McPhalen C. A., James M. N. Structural comparison of two serine proteinase-protein inhibitor complexes: eglin-c-subtilisin Carlsberg and CI-2-subtilisin novo. Biochemistry. 27:1988;6582-6598.
34. McPhalen C. A., Schnebli H. P., James M. N. Crystal and molecular structure of the inhibitor eglin from leeches in complex with subtilisin Carlsberg. FEBS Letters. 188:1985;55-58.
35. Merritt E. A., Murphy M. E. P. Raster3D Version 2.0. A Program for photorealistic molecular graphics. Acta Crystallog. sect. D. 50:1994;869-873.
36. Miller H., Mande S. S., Parsonage D., Sarfaty S. H., Hol W. G., Claiborne A. An L40C mutation converts the cysteine-sulfenic acid redox center in enterococcal NADH peroxidase to a disulfide. Biochemistry. 34:1995;5180-5190.
37. Navaza J. AMoRe: an automated package for molecular replacement. Acta Crystallog. sect. A. 50:1994;157-163.
38. Neidhart D. J., Petsko G. A. The refined crystal structure of subtilisin Carlsberg at 2.5 Å resolution. Protein Eng. 2:1988;271-276.
39. Nicholls A., Sharp K. A., Honig B. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins: Struct. Funct. Genet. 11:1991;281-296.
40. Otwinowski Z. Oscillation data reduction program. Sawyer L., Isaacs N., Bailey S. Proceedings of the CCP4 Study Weekend: Data Collection and Processing. 1993;56-62 SERC Daresbury Laboratory, Daresbury.
41. Pantoliano M. W., Whitlow M., Wood J. F., Dodd S. W., Hardman K. D., Rollence M. L., Bryan P. N. Large increases in general stability for subtilisin BPN' through incremental changes in the free energy of unfolding. Biochemistry. 28:1989;7205-7213.
42. Peek K., Veitch D. P., Prescott M., Daniel R. M., MacIver B., Bergquist P. L. Some characteristics of a proteinase from a thermophilic Bacillus sp. expressed in Escherichia coli: comparison with the native enzyme and its processing in E. coli and in vitro. Appl. Environ. Microbiol. 59:1993;1168-1175.
43. Ramakrishnan C., Ramachandran G. N. Stereochemical criteria for polypeptide and protein chain conformation. Biophys. J. 5:1965;909-933.
44. Read R. J. Improved Fourier coefficients for maps using phases from partial structures with errors. Acta Crystallog. sect. A. 42:1986;140-149.
45. Shirai T., Suzuki A., Yamane T., Ashida T., Kobayashi T., Hitomi J., Ito S. High- resolution crystal structure of M-protease: phylogeny aided analysis of the high-alkaline adaptation mechanism. Protein Eng. 10:1997;627-634.
46. Siezen R. J., Leunissen J. A. M. Subtilases: the superfamily of subtilisin-like serine proteases. Protein Sci. 6:1997;501-523.
47. Siezen R. J., de Vos W. M., Leunissen J. A. M., Dijkstra B. W. Homology modelling and protein engineering strategy of subtilases, the family of subtilisin-like serine proteinases. Protein Eng. 4:1991;719-737.
48. Strausberg S., Alexander P., Wang L., Schwarz F., Bryan P. Catalysis of a protein folding reaction: thermodynamic and kinetic analysis of subtilisin BPN′ interactions with its propeptide fragment. Biochemistry. 32:1993;8112-8119.
49. Teplyakov A. V., Kuranova I. P., Harutyunyan E. H., Vainshtein B. K., Frömmel C., Höhne W. E., Wilson K. S. Crystal structure of thermitase at 1.4 Å resolution. J. Mol. Biol. 214:1990;261-279.
50. Thornton J. M. Disulphide bridges in globular proteins. J. Mol. Biol. 151:1981;261-287.
51. Tronrud D. E., Ten Eyck L. F., Matthews B. W. An efficient general-purpose least-squares refinement program for macromolecular structures. Acta Crystallog. sect. A. 43:1987;489-501.
52. Vogt G., Woell S., Argos P. Protein thermal stability, hydrogen bonds and ion pairs. J. Mol. Biol. 269:1997;631-643.
53. Wallon G., Kryger G., Lovett S. T., Oshima T., Ringe D., Petsko G. A. Crystal structure of Escherichia coli and Salmonella typhimurium 3-isopropylmalate dehydrogenase and comparison with their thermophilic counterpart from Thermus thermophilus. J. Mol. Biol. 226:1997;1016-1031.
54. Wells J. A., Estell D. A. Subtilisin - an enzyme designed to be engineered. Trends Biochem. Sci. 13:1988;291-297.