Properties of a subtilisin-like proteinase from a psychrotrophic Vibrio species. Comparison with proteinase K and aqualysin I

European Journal of Biochemistry

Volumn 260, Issue 3, 1999, Pages 752-760

  Kristjánsson, Magnús M ^a   Magnússon, Ólafur ^a   Gudmundsson, Haflidi M ^a   Alfredsson, Gudni Á ^a   Matsuzawa, Hiroshi ^b  

^a UNIVERSITY OF ICELAND   (Iceland)

^b NONE

Author keywords

Aqualysin I; Cold adaptation; Proteinase K; Psychrotrophic; Subtilisin like proteinase; Vibrio

Indexed keywords

PROTEINASE; PROTEINASE K; SUBTILISIN;

ARTICLE; CATALYSIS; COLD ACCLIMATIZATION; DENATURATION; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME PURIFICATION; ENZYME STABILITY; OXIDATION; PH; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN STRUCTURE; SPECIES DIFFERENCE; SPECIES DIFFERENTIATION;

ADAPTATION, PHYSIOLOGICAL; AMINO ACID SEQUENCE; ASCOMYCOTA; BINDING SITES; DISULFIDES; ENDOPEPTIDASE K; ENZYME STABILITY; METHIONINE; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; PROTEIN CONFORMATION; SEQUENCE HOMOLOGY, AMINO ACID; SERINE ENDOPEPTIDASES; SUBSTRATE SPECIFICITY; SUBTILISINS; TEMPERATURE; THERMUS; VIBRIO;

EID: 0033559561     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1327.1999.00205.x     Document Type: Article

References (73)

1. Neurath, H. (1989) The diversity of proteolytic enzymes. In Proteolytic Enzymes. A Practical Approach. (Beynon, R.J. & Bond, J.S., eds.), pp. 1-13. IRL Press, Oxford, USA.
2. Barrett, A.J. & Rawlings, N.D. (1995) Families and clans of serine peptidases. Arch. Biochem. Biophys. 318, 247-250.
3. Bott, R., Ultsch, M., Kossiakoff, A., Graycar, T., Katz, B. & Power, S. (1988) The three-dimensional structure of Bacillus amyloliquefaciens subtilisin at 1.8 Å and an analysis of the structural consequences of peroxide oxidation. J. Biol. Chem. 263, 7895-7906.
4. McPhalen, C.A. & James, M.N.G. (1988) Structural comparison of two serine proteinase-protein inhibitor complexes: eglin-C-subtilisin Carlsberg and CI-2-subtilisin Novo. Biochemistry 27, 6582-6598.
5. Bode, W., Papamokos, E. & Musil, D. (1987) 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. Eur. J. Biochem. 166, 673-692.
6. Betzel, C., Klupsch, S., Papendorf, G., Hastrup, S., Branner, S. & Wilson, K. (1992) Crystal structure of the alkaline proteinase savinase™ from Bacillus lentus at 1.4 Å resolution. J. Mol. Biol. 223, 427-445.
7. Gros, P., Betzel, C., Dauter, Z., Wilson, K.S. & Hol, W.G.J. (1989) 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, 347-367.
8. Teplyakov, A.V., Kuranova, I.P., Harutyunyan, E.H., Vainshtein, B.K., Frömmel, C., Höhne, W.E. & Wilson, K.S. (1990) Crystal structure of of thermitase at 1.4 Å. J. Mol. Biol. 214, 261-279.
9. Betzel, C., Pal, G.P. & Sanger, W. (1988) Three-dimensional structure of proteinase K at 0.15 nm resolution. Eur. J. Biochem. 178, 155-171.
10. Betzel, C., Teplyakov, A.V., Harutyunyan, E.H., Saenger, W. & Wilson, K.S. (1990) Thermitase and proteinase K: a comparison of the refined three-dimensional structures of the native enzymes. Protein Eng. 3, 161-172.
11. Müller, A., Hinrichs, W., Wolfs, W.M. & Sanger, W. (1994) Crystal structure of calcium-free proteinase K at 1.5-Å resolution. J. Biol. Chem. 269, 23108-23111.
12. Martin, J.R., Mulder, F.A.A., Karimi-Nejad, Y., van der Zwan, J., Mariani, M., Schipper, D. & Boelens, R. (1997) The solution structure of serine protease PB92 from Bacillus alcalophilus presents a rigid fold with a flexible substrate binding site. Structure 5, 521-532.
13. Wells, J.A. & Estell, D.A. (1988) Subtilisin- an enzyme designed to be engineered. Trends Biochem. Sci. 13, 291-297.
14. Carter, P. & Wells, J.A. (1990) Functional interaction among catalytic residues in subtilisin BPN'. Proteins 7, 335-342.
15. 2+ binding loop into subtilisin BPN'. Biochemistry 31, 7796-7801.
16. Strausberg, S., Alexander, P., Wang, L., Schwarz, F. & Bryan, P. (1993) Catalysis of a protein folding reaction: thermodynamic and kinetic analysis of subtilisin BPN' interactions with its propeptide fragment. Biochemistry 32, 8112-8119.
17. Rheinecker, M., Eder, J., Pandey, P.S. & Fersht, A.R. (1994) Variants of subtilisin BPN' with altered specificity profiles. Biochemistry 33, 221-225.
18. Pedersen, J.T., Olsen, O.H., Betzel, C., Eschenburg, S., Branner, S. & Hastrup, S. (1994) Cavity mutants of savinase™. Crystal structures and differential scanning calorimetry experiments give hints of the function of the buried water molecules in subtilisins. J. Mol. Biol. 242, 193-202.
19. Dambmann, C. & Aunstrup, K. (1981) The variety of serine proteases and their industrial significance. In Proteinases and Their Inhibitors, Structure, Function and Applied Aspects. (Turk, V. & Vitale, L.J., eds.), pp. 231-244. Pergamon Press, Oxford, USA.
20. Kristjánsson, M.M. & Kristjánsson, J.K. (1993) Proteinases from thermophilic microorganisms. Comments Agric. Food Chem. 3, 39-67.
21. Siezen, R.J., de Vos, W.M., Leunissen, J.A.M. & Dijkstra, W. (1991) Homology modelling and protein engineering strategy of subtilases, the family of subtilisin-like serine proteinases. Protein Eng. 4, 719-737.
22. Siezen, R.J. & Leunissen, J.A.M. (1997) Subtilases: the superfamily of subtilisin-like serine proteases. Protein Sci. 6, 501-523.
23. Jaenicke, R. & Zavodsky, P. (1990) Proteins under extreme physical conditions. FEBS Lett. 268, 344-349.
24. Jaenicke, R. (1991) Protein stability and molecular adaptation to extreme conditions. Eur. J. Biochem. 202, 715-728.
25. Adams, M.W.W., Perler, F.B. & Kelly, R.M. (1995) Extremoenzymes: expanding the limits of biocatalysis. Biotechnol. 13, 662-668.
26. Jaenicke, R., Schurig, H., Beaucamp, N. & Ostendorp, R. (1996) Structure and stability of hyperstable proteins: glycolytic enzymes from hyperthermophilic bacterium Thermotaga maritima. Adv. Protein Chem. 48, 181-269.
27. Kristjánsson, M.M. & Kinsella, J.E. (1991) Protein and enzyme stability; structural, thermodynamic and experimental aspects. Adv. Food Nutr. Res. 35, 237-316.
28. Zuber, H. (1988) Temperature adaptation of lactate dehydrogenase. Structural, functional and genetic aspects. Biophys. Chem. 29, 171-179.
29. Menéndez-Arias, L. & Argos, P. (1991) Engineering protein thermal stability. Sequence statistics point to residue substitutions in α-helices. J. Mol. Biol. 206, 397-406.
30. Franks, F. (1995) Protein destabilization at low temperatures. Adv. Prot. Chem. 46, 105-139.
31. Hochacha, P.W. & Somero, G.N. (1984) In Biochemical Adaptation, pp. 377-422. Princeton University Press, Princeton, New Jersey, USA.
32. Feller, G., Narinx, E., Arpigny, J.L., Aittaleb, M., Baise, E., Genicot, S. & Gerday, C. (1996) Enzymes from psychrophilic organisms. FEMS Microbiol. Lett. 18, 189-202.
33. Kristjánsson, M.M., Ásgeirsson, B. & Bjarnason, J.B. (1997) Serine proteinases from cold-adapted organisms. In Food Proteins and Lipids (Damodaran, S., ed.), pp. 27-46. Plenum Publishing Corporation, New York, USA.
34. Závodsky, P., Kardos, J., Svingor, Á. & Petsko, G.A. (1998) Adjustment of conformational flexibility is a key event in the thermal adaptation of proteins. Proc. Natl Acad. Sci. USA 95, 7406-7411.
35. Gerday, C., Aittaleb, M., Arpigny, J.L., Baise, E., Chessa, J.P., Garsoux, G., Petrescu, I. & Feller, G. (1997) Psychrophilic enzymes: a thermodynamic challenge. Biochem. Biophys. Acta 1342, 119-131.
36. Vihinen, M. (1987) Relationship of protein flexibility to thermostability. Protein Eng. 1, 477-480.
37. Shoichet, B., Baase, W.A., Kuroki, R. & Matthews, B.W. (1995) A relationship between protein stability and protein function. Proc. Natl Acad. Sci. USA. 92, 452-456.
38. Alvarez, M., Zeelen, J.P., Mainfroid, V., Rentier-Delrue, F., Martial, J.A., Wyns, L., Wierenga, R.K. & Maes, D. (1998) Triose-phosphate isomerase (TIM) of the psychrophilic bacterium Vibrio marinus. J. Biol. Chem. 273, 2199-2206.
39. Aghajari, N., Feller, G., Gerday, C. & Haser, R. (1998) Crystal structures of the psychrophilic α-amylase from Alteromonas haloplanctis in its native form and complexed with an inhibitor. Protein Sci. 7, 564-572.
40. Villeret, V., Chessa, J.P., Gerday, C. & van Beeumen, J. (1997) Preliminary crystal structure determination of the alkaline protease from the Antarctic Pseudomonas aeruginosa. Protein Sci. 6, 2462-2464.
41. Davail, S., Feller, G., Narinx, E. & Gerday, C. (1994) Cold adaptation of proteins. Purification, characterization, and sequence of the heat-labile subtilisin from the antarctic psychrophile Bacillus TA41. J. Biol. Chem. 269, 17448-17453.
42. Narinx, E., Baise, E. & Gerday, C. (1997) Subtilisin from psychrophilic antarctic bacteria: characterization and site-directed mutagenesis of residues possibly involved in the adaptation to cold. Protein Eng. 10, 1271-1279.
43. Feller, G., Lonhienne, T., Deroanne, C., Libioulle, C., van Beeumen, J. & Gerday, C. (1992) Purification, characterization and nucleotide sequence of the thermolabile α-amylase from the antarctic psychrotroph Alteromonas haloplanctis. J. Biol. Chem. 267, 5217-5221.
44. Feller, G., Payan, F., Theys, F., Qian, M., Haser, R. & Gerday, C. (1994) Stability and structural analysis of α-amylase from the antarctic psychrophile Alteromonas haloplanctis. Eur. J. Biochem. 222, 441-447.
45. Feller, G., Zekhnini, Z., Lamotte-Brasseur, J. & Gerday, C. (1997) Enzymes from cold-adapted microorganisms. The class C β-lactamase from the antarctic psychrophile Psychrobacter immobilis A5. Eur. J. Biochem. 244, 186-191.
46. Rentier-Delrue, F., Mande, S.C., Moyens, S., Terpstra, P., Mainfroid, V., Goraj, K., Lion, M., Hol, W.G.J. & Martial, J.A. (1993) Cloning and overexpression of the triosephosphate isomerase genes from psychrophilic and thermophilic bacteria. Structural comparison of the predicted protein sequences. J. Mol. Biol. 229, 85-93.
47. Wallon, G., Lovett, S.T., Magyar, C., Swingor, A., Szilagyi, A., Zavodsky, P., Ringe, D. & Petsko, G.A. (1997) Sequence and homology model of 3-isopropylmalate dehydrogenase from the psychrotrophic bacterium Vibrio sp. I5 suggest reasons for thermal instability. Protein Eng. 10, 665-672.
48. Gerike, U., Danson, M.J., Russel, N.J. & Hough, D.W. (1997) Sequencing and expression of the gene encoding a cold-active citrate synthase from an Antarctic bacterium, strain DS2-3R. Eur. J. Biochem. 248, 49-57.
49. Alfredsson, G.A., Gudmundsson, H.M., Xiang, J.Y. & Kristjansson, M.M. (1995) Subtilisin-like serine proteases from psychrophilic marine bacteria. J. Mar. Biotechnol. 3, 71-72.
50. Lin, S.-J., Kim, D.-W., Ryugo, Y., Wakagi, T. & Matsuzawa, H. (1997) Increase of the protease activity of aqualysin I, a thermostable serine protease, by replacing Asn 219 near the catalytic residue Ser 222. Biosci. Biotech. Biochem. 61, 718-719.
51. DelMar, E.G., Largmann, C., Brodrick, J.W. & Geokas, M.C. (1979) A sensitive new substrate for chymotrypsin. Anal. Biochem. 99, 316-320.
52. Thannhauser, T.W., Konishi, Y. & Scheraga, H.A. (1984) Sensitive quantitative analysis of disulfide bonds in polypeptides and proteins. Anal Biochem. 138, 181-188.
53. Ellman, G.L. (1959) Tissue sulfhydryl groups. Arch. Biochem. Biophys. 82, 70-77.
54. Zaman, Z. & Verwilghen, R.L. (1979) Quantitation of proteins solubilized in sodium dodecyl sulfate-mercaptoethanol-Tris electrophoresis buffer. Anal. Biochem. 100, 64-69.
55. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
56. Jany, K.D., Lederer, G. & Mayer, B. (1986) Amino acid sequence of proteinase K from the mold Tritirachium album Limber. Proteinase K - a subtilisin-related enzyme with disulfide bonds. FEBS Lett. 199, 139-144.
57. Kwon, S.T., Terada, I., Matsuzawa, H. & Ohta, T. (1988) Nucleotide sequence of the gene for aqualysin I (a thermophilic alkaline serine protease) of Thermus aquaticus YT-1 and characteristics of the deduced primary structure of the enzyme. Eur. J. Biochem. 173, 491-497.
58. Deane, S.M., Robb, F.T., Robb, S.M. & Woods, D.R. (1989) Nucleotide sequence of the Vibrio alginolyticus calcium-dependent, detergent-resistant alkaline serine exoprotease A. Gene 76, 281-288.
59. Tsujibo, H., Miyamoto, K., Tanaka, K., Tainaka, K., Imada, C., Okami, Y. & Inamori, Y. (1993) Cloning and sequence of an alkaline serine protease-encoding gene from the marine bacterium Alteromonas sp. strain O-7. Gene 136, 247-251.
60. Jacobs, M., Eliasson, M., Uhlen, M. & Flock, J.I. (1985) Cloning, sequencing and expression of subtilisin Carlsberg from Bacillus licheniformis. Nucl. Acid Res. 13, 8913-8926.
61. Wells, J.A., Ferrari, E., Henner, D.J., Estell, D.A. & Chen, E.Y. (1983) Cloning, sequencing and secretion of Bacillus amyloliquefaciens subtilisin in Bacillus subtilis. Nucl. Acids Res. 11, 7911-7925.
62. Meloun, B., Baudys, M., Kostka, V., Hausdorf, G., Frömmel, C. & Höhne, W.E. (1985) Complete primary structure of thermitase from Thermoactinomyces vulgaris and its structural features related to the subtilisin-type proteinases. FEBS Lett. 183, 195-200.
63. Stauffer, C.E. & Etson, D. (1969) The effect on subtilisin activity of oxidizing a methionine residue. J. Biol. Chem. 244, 5333-5338.
64. Estell, D.A., Graycar, T.P. & Wells, J.A. (1985) Engineering an enzyme by site-directed mutagenesis to be resistant to chemical oxidation. J. Biol. Chem. 260, 6518-6521.
65. Hausdorf, G., Krüger, K., Kütter, G., Holzhütter, H.G., Frömmel, C. & Höhne, W. (1987) Oxidation of a methionine residue in subtilisin-type proteinases by the hydrogen peroxide/borate system - an active site-directed reaction. Biochem. Biophys. Acta 952, 20-26.
66. Matsuzawa, H., Tokugawa, K., Hamaoki, M., Mizoguchi, M., Taguchi, H., Terada, I., Kwon, S.T. & Ohta, T., (1988) Purification and characterization of aqualysin I (a thermophilic alkaline serine protease) produced by Thermus aquaticus YT-1. Eur. J. Biochem. 171, 441-447.
67. Terada, I., Kwon, S.T., Miyata, Y., Matsuzawa, H. & Ohta, T. (1990) Unique precursor structure of an extracellular protease, aqualysin I, with NH2- and COOH-terminal pro-sequences and its processing in Escherichia coli. J. Biol. Chem. 265, 6576-6581.
68. Kurosaka, K., Ohta, T. & Matsuzawa, H. (1996) A 38 kDa precursor protein of aqualysin I (a thermophilic subtilisin-type protease) with a C-terminal extended sequence: its purification and in vitro processing. Mol. Microbiol. 20, 385-389.
69. 2-terminal pro-region aids in the production of active aqualysin I (a thermophilic protease) without the COOH-terminal pro-sequence in Escherichia coli. FEMS Microbiol. Lett. 92, 73-78.
70. Lee, Y.-C., Koike, H., Taguchi, H., Ohta, T. & Matsuzawa, H. (1994) Requirement of a COOH-terminal pro-sequence for the extracellular secretion of aqualysin I (a thermophilic subtilisin-type protease) in Thermus thermophilus. FEMS Microbiol. Lett. 120, 69-74.
71. Kwon, S.T., Matsuzawa, H. & Ohta, T. (1988b) Determination of the position of the disulfide bonds in aqualysin I (a thermophilic alkaline serine protease) of Thermus aquaticus YT-1. J. Biochem. 104, 557-559.
72. Peitsch, M.C. (1996) PROMOD and SWISS-MODEL: Internet-based tools for automated comparative protein modelling. Biochem. Soc. Trans. 24, 274-279.
73. Srinivasan, N., Sowdhamini, R., Ramakrishnan, C. & Balaram, P. (1990) Conformation of disulfide bridges in proteins. Int. J. Peptide Protein Res. 36, 147-155.