Mutational analysis of a surface area that is critical for the thermal stability of thermolysin-like proteases

European Journal of Biochemistry

Volumn 248, Issue 2, 1997, Pages 433-440

  Veltman, Oene R ^a   Vriend, Gert ^b   Hardy, Florence ^c   Mansfeld, Johanna ^d   Van Den Burg, Bertus ^a   Venema, Gerard ^a   Eijsink, Vincent G H ^e  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^c UNIVERSITÉ DE CERGY PONTOISE   (France)

^d MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^e NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

Author keywords

Autolysis; Calcium binding; Thermal stability; Thermolysin; Unfolding pathway

Indexed keywords

THERMOLYSIN;

AMINO ACID SEQUENCE; ARTICLE; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME STRUCTURE; GEOBACILLUS STEAROTHERMOPHILUS; MUTAGENESIS; PRIORITY JOURNAL; THERMOSTABILITY;

GEOBACILLUS STEAROTHERMOPHILUS;

EID: 0030963842     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1432-1033.1997.00433.x     Document Type: Article

References (60)

1. Dahlquist, F. W., Long, J. W. & Bigbee, W. L. (1976) Role of calcium in the thermal stability of thermolysin, Biochemistry 15, 1103-1111.
2. Roche, R. S. & Voordouw, G. (1978) The structural and functional roles of metal ions in thermolysin, CRC Crit. Rev. Biochem. 5, 1-23.
3. Matthews, B. W., Jansonius, J. N., Colman, P. M., Schoenborn, B. P. & Dupourque, D. (1972) Three dimensional structure of thermolysin, Nature 238, 37-42.
4. Holmes, M. A. & Matthews, B. W. (1982) Structure of thermolysin refined at 1.6 Å resolution, J. Mol. Biol. 160, 623-639.
5. Stark, W., Pauptit, R. A., Wilson, K. S. & Jansonius, J. N. (1992) The structure of neutral protease of Bacillus cereus at 0.2 nm resolution, Eur. J. Biochem. 207, 781-791.
6. Vriend, G. & Eijsink, V. G. H. (1993) Prediction and analysis of structure, stability and unfolding of thermolysin-like proteases, J. Comput.-Aided Mol. Des. 7, 367-396.
7. Van den Burg, B., Enequist, H. G., Van der Haar, M. E., Eijsink, V. G. H., Stulp, B. K. & Venema, G. (1991) A highly thermostable neutral protease from Bacillus caldolyticus: cloning and expression of the gene in Bacillus subtilis and characterization of the gene product, J. Bacteriol. 173, 4107-4115.
8. Imanaka, T., Shibazaki, M. & Takagi, M. (1986) A new way of enhancing the thermostability of proteins, Nature 324, 695-697.
9. Eijsink, V. G. H., Veltman, O. R., Aukema, W., Vriend, G. & Venema, G. (1995) Structural determinants of the stability of thermolysin-like proteinases, Nat. Struct. Biol. 2, 374-379.
10. Frigerio, F., Margarit, I., Nogarotto, R., de Filippis, V. & Grandi, G. (1996) Cumulative stabilizing effects of hydrophobic interactions on the surface of the neutral protease from Bacillus subtilis, Protein Eng. 9, 439-446.
11. Veltman, O. R., Vriend, G., Middelhoven, P. J., Van den Burg, B., Venema, G. & Eijsink, V. G. H. (1996) Analysis of structural determinants of the stability of thermolysin-like proteases by molecular modeling and site-directed mutagenesis, Protein Eng. 9, 1181-1189.
12. Heinrikson, R. L. (1977) Applications of thermolysin in protein structural analysis, Methods Enzymol. 47, 175-189.
13. Stoeva, S. & Kleinschmid, T. (1989) Proteolytic specificity of the neutral zinc proteinase of Bacillus mesentericus strain 76 determined by digestion of an α-globulin strain, Biol. Chem. Hoppe-Seyler 370, 1139-1143.
14. Fontana, A. (1988). Structure and stability of thermophilic enzymes. Studies on thermolysin, Biophys. Chem. 29, 181-193.
15. 2+-binding loop into subtilisin BPN′, Biochemistry 31, 7796-7801.
16. Kidokoro, S., Miki, Y., Endo, K., Wada, A., Nagao, H., Miyake, T., Aoyama, A., Yoneya, T., Kai, K. & Ooe, S. (1995) Remarkable activity enhancement of thermolysin mutants, FEBS Lett. 367, 73-76.
17. Hardy, F., Vriend, G., Veltman, O. R., Van der Vinne, B., Venema, G. & Eijsink, V. G. H. (1993) Stabilization of Bacillus stearothermophilus neutral protease by introduction of prolines, FEBS Lett. 317, 89-92.
18. Fujii, M., Takagi, M., Imanaka, T. & Aiba, S. (1983) Molecular cloning of a thermostable neutral protease gene from Bacillus stearothermophilus in a vector plasmid and its expression in Bacillus stearothermophilus and Bacillus subtilis, J. Bacteriol. 154, 831-837.
19. Takagi, M., Imanaka, T. & Aiba, S. (1985) Nucleotide sequence and promoter region for the neutral protease gene from Bacillus stearothermophilus, J. Bacteriol. 163, 824-831.
20. Eijsink, V. G. H., Vriend, G., Van der Vinne, B., Hazes, B., Van den Burg, B. & Venema, G. (1992) Effects of changing the interaction between subdomains on the thermostability of Bacillus neutral proteases, Proteins 14, 224-236.
21. Wetmore, D. R., Wong, S.-L. & Roche, R. S. (1992) The role of the pro-sequence in the processing and secretion of the thermolysin-like neutral protease from Bacillus cereus, Mol. Microbiol. 6, 1593-1604.
22. Yang, M. Y., Ferrari, E. & Henner, D. J. (1984) Cloning of the neutral protease gene of Bacillus subtilis and the use of the cloned gene to create an in vitro-derived deletion mutation, J. Bacteriol. 173, 4107-4115.
23. Eijsink, V. G. H., Vriend, G., Van den Burg, B., Van der Zee, J. R., Veltman, O. R., Stulp, B. K. & Venema, G. (1992) Introduction of a stabilizing 10 amino acid residue β-hairpin in Bacillus subtilis neutral protease, Protein Eng. 5, 157-163.
24. Vriend, G. (1990) WHAT IF: a molecular modeling and drug design program, J. Mol. Graphics 8, 52-56.
25. Mosimann, S., Meleshko, R. & James, M. N. G. (1995) A critical assessment of comparative molecular modeling of tertiary structures of proteins, Proteins 23, 301-317.
26. De Filippis, V., Sander, C. & Vriend, G. (1994) Predicting local structural changes that result from point mutations, Protein Eng. 7, 1203-1208.
27. Chinea, G., Padron, G., Hooft, R. W. W., Sander, C. & Vriend, G. (1995) The use of position specific rotamers in model building by homology, Proteins 23, 415-421.
28. Van Gunsteren, W. & Berendsen, H. J. J. (1987) GROMOS, Groningen Molecular Simulation computer program package, BIOMOS, Biomolecular Software, Laboratory of Physical Chemistry, University of Groningen, The Netherlands.
29. McPhalen, C. A., Strynadka, N. C. J. & James, M. N. G. (1991) Calcium binding sites in proteins: a structural perspective, Adv. Protein Chem. 42, 77-144.
30. Matthews, B. W., Nicholson, H. & Becktel, W. J. (1987) Enhanced protein thermostability from site directed mutations that decrease the entropy of unfolding, Proc. Natl Acad. Sci. USA 84, 6663-6667.
31. Minor, D. L. & Kim, P. S. (1994) Measurement of the β-sheet forming propensities of amino acids, Nature 367, 660-663.
32. Van den Burg, B., Dijkstra, B. W., Vriend, G., Van der Vinne, B., Venema, G. & Eijsink, V. G. H. (1994) Protein stabilization by hydrophobic interactions at the surface, Eur. J. Biochem. 220, 981-985.
33. Pakula, A. A. & Sauer, R. T. (1990) Reverse hydrophobic effect relieved by amino acid substitutions at the surface, Nature 344, 363-364.
34. Bower, M. J., Cohen, F. E. & Dunbrack, R. L. (1997) Prediction of protein side-chain rotamers from a backbone-dependent rotamer library: a new homology modeling tool, J. Mol. Biol. 267, 1268-1282.
35. Matthews, B. W. (1993) Structural and genetic analysis of protein stability, Annu. Rev. Biochem. 62, 139-160.
36. Fersht, A. R. & Serrano, L. (1993) Principles of protein stability derived from protein engineering experiments, Curr. Opin. Struct. Biol. 3, 75-83.
37. Dao-pin, S., Sauer, U., Nicholson, H. & Matthews, B. W. (1991) Contributions of engineered salt bridges to the stability of T4 lysozyme determined by directed mutagenesis, Biochemistry 30, 7142-7153.
38. Sali, D., Bycroft, M. & Fersht, A. R. (1991) Surface electrostatic interactions contribute little to stability of barnase, J. Mol. Biol. 220, 779-788.
39. Richardson, J. S. & Richardson, D. C. (1988) Amino acid preferences for specific locations at the ends of alpha helices, Science 240, 1648-1652.
40. Serrano, L., Neira, J. L., Sancho, J. & Fersht, A. R. (1992) Effect of alanine versus glycine in alpha-helices on protein stability, Nature 356, 453-455.
41. Serrano, L., Sancho, J., Hirshberg, M. & Fersht, A. R. (1992) Alpha-helix stability in proteins, I. Empirical correlations concerning substitutions of side-chains at the N and C-caps and the replacement of alanine by glycine or serine at solvent exposed surfaces, J. Mol. Biol. 227, 544-559.
42. Bell, J. A., Becktel, W. J., Sauer, U., Baase, W. A. & Matthews, B. W. (1992) Dissection of helix capping in T4 lysozyme by structural and thermodynamic analysis of six amino acid substitutions at Thr59, Biochemistry 31, 3540-3596.
43. Harpaz, Y., Elmarsry, N., Fersht, A. R. & Henrick, K. (1994) Direct observation of better hydration at the N terminus of an alpha-helix with glycine rather than alanine as the N-cap residue, Proc. Natl Acad. Sci. USA 91, 311-315.
44. Mansfeld, J., Vriend, G., Dijkstra, B. W., Veltman, O. R., Van den Burg, B., Venema, G., Ulbrich-Hofmann, R. & Eijsink, V. G. H. (1997) Extreme stabilization of a thermolysin-like protease by an engineered disulfide bond, J. Biol. Chem. 272, 11152-11156.
45. Erwin, C. R., Barnett, B. L., Oliver, J. D. & Sullivan, J. F. (1990) Effects of salt bridges on the stability of subtilisin BPN′, Protein Eng. 4, 87-97.
46. Mitchinson, C. & Wells, J. A. (1989) Protein engineering of disulphide bonds in subtilisin BPN′, Biochemistry 28, 4807-4815.
47. Mitraki, A. & King, J. (1989) Protein folding intermediates and inclusion body formation, Biotechnology 7, 690-697.
48. Chrunyk, B. A. & Wetzel, R. (1993) Breakdown in the relationship between thermal and thermodynamic stability in an interleukin-1β point mutant modified in a surface loop, Protein Eng. 6, 733-738.
49. Pepys, M. B., Hawkins, P. N., Booth, D. R., Vigushin, D. M., Tennent, G. A., Soutar, A. K., Totty, N., Nguyen, O., Blake, C. C. F., Terry, C. J., Fesst, T. G., Zalin, A. M. & Hsuan, J. J. (1993) Human lysozyme gene mutations cause hereditary systemic amyloidosis, Nature 362, 553-557.
50. Serrano, L., Day, A. G. & Fersht, A. R. (1993) Step-wise mutation of barnase to binase: A procedure for engineering increased stability in proteins and an experimental analysis of the evolution of protein stability, J. Mol. Biol. 233, 305-312.
51. Argos, P., Rossmann, M. G., Grau, U. M., Zuber, H., Frank, G. & Tratschin, J. D. (1979) Thermal stability and protein structure, Biochemistry 18, 5698-5703.
52. Menéndez-Arias, L. & Argos, P. (1989) Engineering protein thermal stability. Sequence statistics point to residue substitutions in α-helices, J. Mol. Biol. 206, 397-406.
53. Eijsink, V. G. H. & Venema, G. (1994) Genes encoding extremely thermostable variants of neutral proteases, vectors and cells comprising these genes and proteases produced through these genes, vectors and/or cells, in particular the neutral proteases of Bacillus strearothermophilus and Bacillus thermoproteolyticus (thermolysin) and sequences and cells coding therefore, Patent application 94200182, 7 (Eur.).
54. Veltman, O. R., Vriend, G., Van den Burg, B., Hardy, F., Venema, G. & Eijsink, V. G. H. (1997) Engineering thermolysin-like proteases whose stability is largely independent of calcium, FEBS Lett. 405, 241-244.
55. Vita, C., Fontana, A. & Jaenicke, R. (1989) Folding of thermolysin fragments. Hydrodynamic properties of isolated domains and subdomains, Eur. J. Biochem. 183, 513-518.
56. Corbett, E. J. T., Ahmad, F. & Roche, R. S. (1986) Domain unfolding and the stability of thermolysin in guanidine hydrochloride, Biochem. Cell. Biol. 64, 953-961.
57. Daniel, R. M., Dines, M. & Petach, H. H. (1996) The denaturation and degradation of stable enzymes at high temperatures, Biochem. J. 317, 1-11
58. Carson, M. (1987) Ribbon models for macromolecules, J. Mol. Graphics 5, 103-106.
59. Kühn, S. & Fortnagel, P. (1993) Molecular cloning and nucleotide sequence of the gene encoding a calcium-dependent exoproteinase from Bacillus megaterium ATCC 14581, J. Gen. Microbiol. 139, 39-47.
60. Chumakov, V. N., Azimova, M. I., Zaitsev, D. A. & Gabriélyan, A. V. (1995) Analysis of the structural basis of thermostability of secreted Bacillary metalloproteinases with model chimeric enzymes, Mol. Biol. 29, 578-583.