Subtilases: The superfamily of subtilisin-like serine proteases

Protein Science

Volumn 6, Issue 3, 1997, Pages 501-523

  Siezen, Roland J ^a   Leunissen, Jack A M ^b  

^a NIZO FOOD RESEARCH   (Netherlands)

^b RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

Author keywords

homology modeling; sequence alignment; serine protease; subtilase; subtilisin family

Indexed keywords

CALCIUM BINDING PROTEIN; SERINE PROTEINASE; SUBTILISIN;

AMINO ACID SEQUENCE; DNA SEQUENCE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME SPECIFICITY; PRIORITY JOURNAL; PROTEIN BINDING; REVIEW; SEQUENCE HOMOLOGY;

EID: 0030896832     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1002/pro.5560060301     Document Type: Review

References (76)

1. Abraham LD, Breuil C. 1995. Factors affecting autolysis of a subtilisin-like serine proteinase secreted by Ophiostoma piceae and identification of the cleavage site. Biochim Biophys Acta 1245:76-84.
2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol 215:403-410.
3. Balaban NP, Sharipova MR, Itskovich EL, Leshchinskaya IB, Rudenskaya GN. 1994. Secreted serine protease from the spore-forming bacterium Bacillus intermedius 3-19. Biochemistry (Moscow) 59:1033-1038.
4. Ballinger MD, Tom J, Wells JA. 1995. Designing subtilisin BPN' to cleave substrates containing dibasic residues. Biochemistry 34:13312-13319.
5. Barr PJ. 1991. Mammalian subtilisins: The long-sought dibasic processing endoproteases. Cell 66:1-3.
6. Barrett AJ, Rawlings ND. 1995. Families and clans of serine peptidases. Arch Biochem Biophys 318:247-250.
7. Benjannet S, Lusson L, Hamelin J, Savaria D, Chrétien M, Seidah NG. 1995. Structure-function studies on the biosynthesis and bioactivity of the precursor convertase PC2 and the formation of the PC2/7B2 complex. FEBS Lett 362:151-155.
8. Berti PJ, Storer AC. 1995. Alignment/phylogeny of the papain superfamily of cysteine proteases. J Mol Biol 246:273-283.
9. Betzel C, Belleman M, Pal GP, Bajorath J, Saenger W, Wilson KS. 1988a. X-ray and model-building studies on the specificity of the active site of proteinase K. Proteins Struct Funct Genet 4:157-164.
10. Betzel C, Pal GP, Saenger W. 1988b. Three-dimensional structure of proteinase K at 0.15 nm resolution. Eur J Biochem 178:155-171.
11. Booth MC, Bogie ChP, Sahl HG, Siezen RJ, Hatter KL, Gilmore MS. 1996. Structural analysis and proteolytic activation of Enterococcus faecalis cytolysin, a novel lantibiotic. Mol Microbiol 21:1175-1184.
12. Bruinenberg PG, Doesburg P, Alting AC, Exterkate FA, Vos WM de, Siezen RJ. 1994a. Evidence for a large dispensable segment in the subtilisin-like catalytic domain of the Lactococcus lactis cell-envelope proteinase. Protein Eng 7:991-996.
13. Bruinenberg PG, Vos WM de, Siezen RJ. 1994b. Prevention of C-terminal autoprocessing of Lactococcus lactis SK11 cell-envelope proteinase by engineering of an essential surface loop. Biochem J 302:957-963.
14. Burton KS, Wood DA, Thurston CF, Barker PJ. 1993. Purification and characterization of a serine proteinase from senescent sporophores of the commercial mushroom Agaricus bisporus. J Gen Microbiol 139:1379-1386.
15. Carter P, Wells JA. 1990. Functional interaction among catalytic residues in subtilisin BPN'. Proteins Struct Function Genet 7:335-342.
16. Chestukhina GG, Zagnit'ko OP, Revina LP, Klepikova FS, Stepanov VM. 1986. Extracellular serine proteinases from subspecies of Bacillus thuringiensis evolve much more slowly than the corresponding δ-endotoxins. Biochemistry (Moscow) 51:1472-1479.
17. Creemers JWM, Siezen RJ, Roebroek AJM, Ayoubi TAY, Heylebroeck D, Van de Ven WJM. 1993. Modulation of furin-mediated proprotein processing activity by site-directed mutagenesis. J Biol Chem 268:21826-21834.
18. Davail S, Feller G, Narinx E, Gerday C. 1994. Cold adaptation of proteins. J Biol Chem 269:17448-17453.
19. Devereux J, Haeberli P, Smithies O. 1984. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12:387-395.
20. Durham DR. 1993. The elastolytic properties of subtilisin GX from alkalophilic Bacillus sp. strain 6644 provides a means of differentiation from other subtilisins. Biochem Biophys Res Commun 194:1365-1370.
21. Felsenstein J. 1993. PHYLIP (Phylogeny Inference Package) version 3.5c. Distributed by the author. Seattle, Department of Genetics, University of Washington.
22. Freeman SA, Peek K, Prescott M, Daniel R. 1993. Characterization of a chelator-resistant proteinase from Thermus strain Rt4A2. Biochem J 295:463-369.
23. Gallagher T, Bryan P, Gilliland GL. 1993. Calcium-independent subtilisin by design. Proteins 16:205-213.
24. Gallagher T, Gilliland G, Wang L, Bryan P. 1995. The prosegment-subtilisin BPN' complex: Crystal structure of a specific 'foldase.' Structure 3:907-914.
25. Gaucher GM, Stevenson KJ. 1976. Thermomycolin. Methods Enzymol 45:415-433.
26. Greer J. 1990. Comparative modeling methods: Application to the family of mammalian serine proteases. Proteins Struct Funct Genet 7:317-334.
27. Gron H, Meldal M, Breddam K. 1992. Extensive comparison of the substrate preferences of two subtilisins as determined with peptide substrates which are based on the principle of intramolecular quenching. Biochemistry 31:6011-6018.
28. Gros P, Betzel Ch, Dauter Z, Wilson KS, Hol WGJ. 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.
29. Hazes B, Dijkstra BW. 1988. Model building of disulfide bonds in proteins with known three-dimensional structure. Protein Eng 2:119-125.
30. Heinz DW, Priestle JP, Rahuel J, Wilson KS, Grütter MG. 1991. Refined crystal structures of subtilisin Novo in complex with wild-type and two mutant eglins: Comparison with other serine proteinase inhibitor complexes. J Mol Biol 217:353-371.
31. Heringa J, Argos P, Egmond MR, Vlieg J de. 1995. Increasing thermal stability of subtilisin from mutations suggested by strongly interacting side-chain clusters. Protein Eng 8:21-30.
32. Jukes TH, Cantor CR. 1969. Evolution of protein molecules. In: Munro HN, ed. Mammalian protein metabolism, vol. III. New York: Academic Press. pp 21-132.
33. Kabsch W, Sander C. 1983. Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22:2577-2637.
34. Katz B, Kossiakoff AA. 1990. Crystal structures of subtilisin BPN' variants containing disulfide bonds and cavities: Concerted structural rearrangements induced by mutagenesis. Proteins Struct Funct Genet 7:343-357.
35. Kimura M. 1983. The neutral theory of molecular evolution. Cambridge, UK: Cambridge University Press.
36. Kraulis PJ. 1991. MOLSCRIPT: A program to produce both detailed and schematic plots of protein structure. J Appl Crystal 24:946-950.
37. Kunitate A, Okamoto M, Ohmori I. 1989. Purification and characterization of a thermostable serine protease from Bacillus thuringiensis. Agric Biol Chem 53:3251-3256.
38. Kwon ST, 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.
39. Kwon YT, Kim JO, Moon SY, Lee HH, Rho HM. 1994. Extracellular alkaline proteases from alkalophilic Vibrio metschnikovii strain RH530. Biotech Lett 16:413-418.
40. Larcher G, Cimon B, Symoens F, Tronchin G, Charbasse D, Bouchara J-P. 1996. A 33 kDa serine proteinase from Scedosporium apiospermum. Biochem J 315:119-126.
41. Lavrenova GI, Gul'nik SV, Kalugar SV, Borovikova VP, Revina LP, Stepanov VM. 1984. Extracellular acid serine proteinase D of Streptomyces rutgersensis. Biochemistry (Moscow) 49:447-454.
42. Lilley G, Stewart DJ, Kortt AA. 1992. Amino acid and DNA sequences of an extracellular basic protease of Dichelobacter nodosus show that it is a member of the subtilisin family of proteases. Eur J Biochem 210:13-21.
43. Lipkind G, Gong Q, Steiner DF. 1995. Molecular modeling of the substrate specificity of prohormone convertases SPC2 and SPC3. J Biol Chem 270:13277-13284.
44. Lo RYC, Strathdee CA, Shewen PE, Cooney BJ. 1991. Molecular studies of Ssa1, a serotype-specific antigen of Pasteurella haemolytica A1. Infect Immun 59:3398-3406.
45. Matsumura M, Signor G, Matthews BW. 1989. Substantial increase of protein stability by multiple disulphide bonds. Nature 342:291-293.
46. McPhalen CA, James MNG. 1988. Structural comparison of two serine proteinase-protein inhibitor complexes: Eglin-C-subtilisin Carlsberg and CI-2-subtilisin Novo. Biochemistry 27:6582-6598.
47. Meyer C, Bierbaum G, Heidrich C, Reis M, Süling J, Iglesias-Wind MI, Kempter C, Molitor E, Sahl HG. 1995. Nucleotide sequence analysis of the lantibiotic gene cluster and functional analysis of PepP and PepC. Eur J Biochem 232:478-489.
48. Mitchinson C, Wells JA. 1989. Protein engineering of disulfide bonds in subtilisin BPN'. Biochemistry 28:4807-4815.
49. Murphy JM, Walton JD. 1996. Three extracellular proteases from Cochliobolus carbonum: Cloning and targeted disruption of ALP1. Mol Plant-Microbe Interact 9:290-297.
50. Pantoliano MW, Ladner RC, Bryan PN, Rollence ML, Wood JF, Poulos TL. 1987. Protein engineering of subtilisin BPN': Enhanced stabilization through the introduction of two cysteines to form a disulfide bond. Biochemistry 26:2077-2082.
51. Pearson WR, Lipman DJ. 1988. Improved tools for biological sequence comparison. Proc Natl Acad Sci USA 85:2444-2448.
52. Perona JJ, Craik CS. 1995. Structural basis of substrate specificity in the serine proteases. Protein Sci 4:337-360.
53. Rawlings ND, Barrett AJ. 1994. Families of serine peptidases. Methods Enzymol 244:19-61.
54. Rypniewski WR, Perrakis A, Vorgias CE, Wilson KS. 1994. Evolutionary divergence and conservation of trypsin. Protein Eng 7:57-64.
55. Sahl HG, Jack RW, Bierbaum G. 1995. Biosynthesis and biological activities of lantibiotics with unique post-translational modifications. Eur J Biochem 230:827-853.
56. Saitou N, Nei M. 1987. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406-425.
57. Schlechter I, Berger A. 1967. On the size of the active site in proteases. I. Papain. Biochem Biophys Res Commun 27:157-162.
58. Schmidt BF, Woodhouse L, Adams RM, Ward T, Mainzer SE, Lad PJ. 1995. Alkalophilic Bacillus sp. strain LG12 has a series of serine protease genes. Appl Environ Microbiol 61:4490-4493.
59. Segers R, Butt TM, Keen JN, Kerry BR, Peberdy JF. 1995. The subtilisins of the invertebrate mycopathogens Verticillium chlamydosporium and Metarhizium anisopliae are serologically and functionally related. FEMS Microbiol Lett 126:227-232.
60. Shimogaki H, Takeuchi K, Nishino T, Ohdera M, Kudo T, Ohba K, Iwama M, Irie M. 1991. Purification and properties of a novel surface-active agent-and alkaline-resistant protease from Bacillus sp. Y. Agric Biol Chem 55:2251-2258.
61. Siezen RJ, Vos WM de, Leunissen JAM, Dijkstra BW. 1991. Homology modelling and protein engineering strategy of subtilases, the family of subtilisin-like serine proteases. Protein Eng 4:719-737.
62. Siezen RJ, Bruinenberg PG, Vos P, van Alen-Boerrigter IJ, Nijhuis M, Alting AC, Exterkate FA, Vos WM de. 1993. Engineering of the substrate binding region of the subtilisin-like, cell-envelope proteinase of Lactococcus lactis. Protein Eng 6:927-937.
63. Siezen RJ, Creemers JWM, van de Ven WJM. 1994. Homology modelling of the catalytic domain of human furin. A model for the eukaryotic subtilisin-like proprotein convertases. Eur J Biochem 222:255-266.
64. Siezen RJ, Rollema HS, Kuipers OP, Vos WM de. 1995a. Homology modelling of the Lactococcus lactis leader peptidase NisP and its interaction with the precursor of the lantibiotic nisin. Protein Eng 8:117-125.
65. Siezen RJ, Leunissen JAM, Shinde U. 1995b. Homology analysis of the propeptides of subtilisin-like serine proteases (subtilases). In: Shinde U, ed. Intramolecular chaperones and folding. Austin: R.G. Landes Company. pp 231-253.
66. Strongin AYa, Izotova LS, Abramov ZT, Gorodetsky DI, Ermakova LM, Baratova LA, Belyanova LP, Stepanov VM. 1978. Intracellular serine protease of Bacillus subtilis: Sequence homology with extracellular subtilisins. J Bacteriol 133:1401-1411.
67. Takagi H, Takahashi T, Momose H, Inouye M, Maeda Y, Matsuzawa H, Ohta T. 1990. Enhancement of the thermostability of subtilisin E by introduction of a disulfide bond engineered on the basis of structural comparison with a thermophilic serine protease. J Biol Chem 265:6874-6878.
68. Takeuchi Y, Noguchi S, Satow Y, Kojima S, Kumagai I, Miura K, Nakamura KT, Mitsui Y. 1991a. Molecular recognition at the active site of subtilisin BPN': Crystallographic studies using genetically engineered proteinaceous inhibitor SSI (Streptomyces subtilisin inhibitor). Protein Eng 4:501-508.
69. Takeuchi Y, Satow Y, Nakamura KT, Mitsui Y. 1991b. Refined crystal structure of the complex of subtilisin BPN' and Streptomyces subtilisin inhibitor at 1.8 Å resolution. J Mol Biol 221:309-325.
70. Tsujibo H, Miyamoto K, Hasegawa T, Inamori Y. 1990. Amino acid compositions and partial sequences of two types of alkaline serine proteases from Nocardiopsis dassonvillei subsp. prasina OPC-210. Agric Biol Chem 54:2177-2179.
71. van de Ven WJM, Voorberg J, Fontijn R, Pannekoek H, Ouweland AMW van den, Duijnhoven HLP van, Roebroek AJM, Siezen RJ. 1990 Furin is a subtilisin-like proprotein processing enzyme in higher eukaryotes. Mol Biol Rep 14:265-275.
72. van de Ven WJM, Roebroek AJM, Duijnhoven HLP van. 1993. Structure and function of eukaryotic proprotein processing enzymes of the subtilisin family of serine proteases. Crit Rev Oncogenesis 4:115-136.
73. van der Meer JR, Rollema HS, Siezen RJ, Kuipers OP, Vos WM de. 1994. Influence of amino acid substitutions in the nisin leader peptide on biosynthesis and secretion of nisin by Lactococcus lactis. J Biol Chem 269:3555-3562.
74. Wells JA, Powers DB. 1986. In vivo formation and stability of engineered disulfide bonds in subtilisin. J Biol Chem 261:6564-6570.
75. Wells JA, Powers DB, Bott RR, Graycar TP, Estell DA. 1987. Designing substrate specificity by protein engineering of electrostatic interactions. Proc Natl Acad Sci USA 84:1219-1223.
76. Zhou A, Paquet L, Mains E. 1995. Structural elements that direct specific processing of different mammalian subtilisin-like prohormone convertases. J Biol Chem 270:21509-21516.