Commercial proteases: Present and future

FEBS Letters

Volumn 587, Issue 8, 2013, Pages 1155-1163

  Li, Qing ^a   Yi, Li ^a   Marek, Peter ^a   Iverson, Brent L ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Alkaline protease; Commercial protease; Protease engineering; Therapeutic protease

Indexed keywords

DETERGENT; PROTEINASE;

BIOTECHNOLOGY; CANCER RESEARCH; COMPUTER AIDED DESIGN; DRUG DESIGN; ENZYME SPECIFICITY; ENZYME SYNTHESIS; FOOD PROCESSING; HIGH THROUGHPUT SCREENING; HUMAN; INDUSTRY; LAUNDRY; LEATHER INDUSTRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ENGINEERING; PROTEIN FUNCTION; REVIEW;

CHEMICAL INDUSTRY; COMPUTATIONAL BIOLOGY; DIRECTED MOLECULAR EVOLUTION; DRUG INDUSTRY; FOOD INDUSTRY; FORECASTING; HUMANS; PEPTIDE HYDROLASES; PROTEIN ENGINEERING;

EID: 84876066165     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2012.12.019     Document Type: Review

References (94)

1. O. Schilling, and C. Overall Proteome-derived, database-searchable peptide libraries for identifying protease cleavage sites Nat. Biotechnol. 26 2008 685 694
2. A.B. Marnett, and C. Craik Papa's got a brand new tag: advances in identification of proteases and their substrates Trends Biotechnol. 23 2005 59 64
3. C. López-Otín, and J.S. Bond Proteases: multifunctional enzymes in life and disease J. Biol. Chem. 283 2008 30433 30437
4. C. Craik, M. Page, and E. Madison Proteases as therapeutics Biochem. J. 435 2011 1 17
5. A.R. Khan, and M.N. James Molecular mechanisms for the conversion of zymogens to active proteolytic enzymes Protein Sci. 7 1998 815 836
6. D.W. Wolan, J.A. Zorn, D.C. Gray, and J.A. Wells Small-molecule activators of a proenzyme Science 326 2009 853 858
7. K. Hasumi, S. Yamamichi, and T. Harada Small-molecule modulators of zymogen activation in the fibrinolytic and coagulation systems FEBS J. 277 2010 3675 3687
8. D.M. Mitrea, L.S. Parsons, and S.N. Loh Engineering an artificial zymogen by alternate frame protein folding Proc. Natl. Acad. Sci. USA 107 2010 2824 2829
9. P. Plainkum, S.M. Fuchs, S. Wiyakrutta, and R.T. Raines Creation of a zymogen Nat. Struct. Biol. 10 2003 115 119
10. V. Quesada, G.R. Ordóñez, L.M. Sánchez, X.S. Puente, and C. López-Otín The Degradome database: mammalian proteases and diseases of proteolysis Nucleic Acids Res. 37 2009 D239 D243
11. X.S. Puente, L.M. Sánchez, C.M. Overall, and C. López-Otín Human and mouse proteases: a comparative genomic approach Nat. Rev. Genet. 4 2003 544 558
12. A. Sumantha, C. Larroche, and P. Ashok Microbiology and industrial biotechnology of food-grade proteases: a perspective Food Technol. Biotechnol. 44 2006 211 220
13. P.N. Bryan Protein engineering of subtilisin Biochim. Biophys. Acta 1543 2000 203 222
14. K. Dill Dominant forces in protein folding Biochemistry 29 1990 7133 7155
15. H. Takagi, T. Takahashi, H. Momose, M. Inouye, Y. Maeda, H. Matsuzawa, and T. Ohta 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 1990 6874 6878
16. M. Pantoliano, R. Ladner, P. Bryan, M. Rollence, J. Wood, and T. Poulos Protein engineering of subtilisin BPN′: enhanced stabilization through the introduction of two cysteines to form a disulfide bond Biochemistry 26 1987 2077 2082
17. C. Mitchinson, and J. Wells Protein engineering of disulfide bonds in subtilisin BPN′ Biochemistry 28 1989 4807 4815
18. D. Estell, T. Graycar, and J. Wells Engineering an enzyme by site-directed mutagenesis to be resistant to chemical oxidation J. Biol. Chem. 260 1985 6518 6521
19. H. Gron, L. Bech, S. Branner, and K. Breddam A highly active and oxidation-resistant subtilisin-like enzyme produced by a combination of site-directed mutagenesis and chemical modification Eur. J. Biochem. 194 1990 897 901
20. H. Wright Nonenzymatic deamidation of asparaginyl and glutaminyl residues in proteins Crit. Rev. Biochem. Mol. Biol. 26 1991 1 52
21. L. Narhi, Y. Stabinsky, M. Levitt, L. Miller, R. Sachdev, S. Finley, S. Park, C. Kolvenbach, T. Arakawa, and M. Zukowski Enhanced stability of subtilisin by three point mutations Biotechnol. Appl. Biochem. 13 1991 12 24
22. C. Smith, H. Toogood, H. Baker, R. Daniel, and E. Baker Calcium-mediated thermostability in the subtilisin superfamily: the crystal structure of Bacillus Ak.1 protease at 1.8 Å resolution J. Mol. Biol. 294 1999 1027 1040
23. M. Pantoliano, M. Whitlow, J. Wood, M. Rollence, B. Finzel, G. Gilliland, T. Poulos, and P. Bryan The engineering of binding affinity at metal ion binding sites for the stabilization of proteins: subtilisin as a test case Biochemistry 27 1988 8311 8317
24. S. Strausberg, P. Alexander, D. Gallagher, G. Gilliland, B. Barnett, and P. Bryan Directed evolution of a subtilisin with calcium-independent stability Bio/Technology 13 1995 669 673
25. S. Strausberg, B. Ruan, K. Fisher, P. Alexander, and P. Bryan Directed coevolution of stability and catalytic activity in calcium-free subtilisin Biochemistry 44 2005 3272 3279
26. A. Klibanov Improving enzymes by using them in organic solvents Nature 409 2001 241 246
27. F. Bordusa Proteases in organic synthesis Chem. Rev. 102 2002 4817 4868
28. I. Filippova, and E. Lysogorskaia Modified proteinases in peptide synthesis in organic media Bioorg. Khim. 29 2003 544 550
29. S. Riva, M. Nonini, G. Ottolina, and B. Danieli Subtilisin-catalyzed esterification of di- and oligosaccharides containing a d-fructose moiety Carbohyd. Res. 314 1998 259 266
30. M. Gupta Enzyme function in organic solvents Eur. J. Biochem. 203 1992 25 32
31. K. Chen, and F. Arnold Enzyme engineering for nonaqueous solvents: random mutagenesis to enhance activity of subtilisin E in polar organic media Bio/Technology 9 1991 1073 1077
32. K. Chen, and F. Arnold Tuning the activity of an enzyme for unusual environments: sequential random mutagenesis of subtilisin E for catalysis in dimethylformamide Proc. Natl. Acad. Sci. USA 90 1993 5618 5622
33. S. Desai, and V. Hentz Collagenase Clostridium histolyticum for Dupuytren's contracture Expert Opin. Biol. Ther. 10 2010 1395 1404
34. E. Persson, M. Kjalke, and O. Olsen Rational design of coagulation factor VIIa variants with substantially increased intrinsic activity Proc. Natl. Acad. Sci. USA 98 2001 13583 13588
35. S. Harvey, M. Stone, M. Martinez, and G. Nelsestuen Mutagenesis of the gamma-carboxyglutamic acid domain of human factor VII to generate maximum enhancement of the membrane contact site J. Biol. Chem. 278 2003 8363 8369
36. P. Comp, R. Jacocks, G. Ferrell, and C. Esmon Activation of protein C in vivo J. Clin. Invest. 70 1982 127 134
37. S. Hanson, J. Griffin, L. Harker, A. Kelly, C. Esmon, and A. Gruber Antithrombotic effects of thrombin-induced activation of endogenous protein C in primates J. Clin. Invest. 92 1993 2003 2012
38. C. Gibbs, S. Coutre, M. Tsiang, W. Li, A. Jain, K. Dunn, V. Law, C. Mao, S. Matsumura, and S. Mejza Conversion of thrombin into an anticoagulant by protein engineering Nature 378 1995 413 416
39. E. Di Cera, and A. Cantwell Determinants of thrombin specificity Ann. N. Y. Acad. Sci. 936 2001 133 146
40. P. Gandhi, M. Page, Z. Chen, L. Bush-Pelc, and E. Di Cera Mechanism of the anticoagulant activity of thrombin mutant W215A/E217A J. Biol. Chem. 284 2009 24098 24105
41. A. Gruber, A. Cantwell, E. Di Cera, and S. Hanson The thrombin mutant W215A/E217A shows safe and potent anticoagulant and antithrombotic effects in vivo J. Biol. Chem. 277 2002 27581 27584
42. S. Opal Can we RESOLVE the treatment of sepsis? Lancet 369 2007 803 804
43. L. Mosnier, X. Yang, and J. Griffin Activated protein C mutant with minimal anticoagulant activity, normal cytoprotective activity, and preservation of thrombin activable fibrinolysis inhibitor-dependent cytoprotective functions J. Am. Chem. Soc. 282 2007 33022 33033
44. J.-S. Bae, L. Yang, C. Manithody, and A. Rezaie Engineering a disulfide bond to stabilize the calcium-binding loop of activated protein C eliminates its anticoagulant but not its protective signaling properties J. Biol. Chem. 282 2007 9251 9259
45. S. Harmon, R. Preston, F. Ni Ainle, J. Johnson, M. Cunningham, O. Smith, B. White, and J. O'Donnell Dissociation of activated protein C functions by elimination of protein S cofactor enhancement J. Biol. Chem. 283 2008 30531 30539
46. H. Pannekoek, H. Veerman, H. Lambers, P. Diergaarde, C. Verweij, A. van Zonneveld, and J. van Mourik Endothelial plasminogen activator inhibitor (PAI): a new member of the Serpin gene family EMBO J. 5 1986 2539 2544
47. E. Madison, E. Goldsmith, R. Gerard, M. Gething, and J. Sambrook Serpin-resistant mutants of human tissue-type plasminogen activator Nature 339 1989 721 724
48. C. Koh, and R. Kini Molecular diversity of anticoagulants from haematophagous animals Thromb. Haemost. 102 2009 437 453
49. G. Pasut, and F. Veronese State of the art in PEGylation: the great versatility achieved after forty years of research J. Control Release 161 2012 461 472
50. H. Stennicke, H. Ostergaard, R. Bayer, M. Kalo, K. Kinealy, P. Holm, B. Sorensen, D. Zopf, and S. Bjorn Generation and biochemical characterization of glycoPEGylated factor VIIa derivatives Thromb. Haemost. 100 2008 920 928
51. C. Negrier, K. Knobe, A. Tiede, P. Giangrande, and J. Moss Enhanced pharmacokinetic properties of a glycoPEGylated recombinant factor IX: a first human dose trial in patients with hemophilia B Blood 118 2011 2695 2701
52. S. Schulte Pioneering designs for recombinant coagulation factors Thromb. Res. 128 Suppl 1 2011 12
53. R. Benecke Clinical relevance of botulinum toxin immunogenicity BioDrugs 26 2012 9
54. D. Dressler Botulinum toxin drugs: future developments J. Neural Trs. 115 2008 575 577
55. E. Zambidis, and D. Scott Epitope-specific tolerance induction with an engineered immunoglobulin Proc. Natl. Acad. Sci. USA 93 1996 5019 5024
56. A. Basu, K. Yang, M. Wang, S. Liu, R. Chintala, T. Palm, H. Zhao, P. Peng, D. Wu, and Z. Zhang Structure-function engineering of interferon-beta-1b for improving stability, solubility, potency, immunogenicity, and pharmacokinetic properties by site-selective mono-PEGylation Bioconjugate Chem. 17 2006 618 630
57. A. von Delwig, D. Altmann, J. Isaacs, C. Harding, R. Holmdahl, N. McKie, and J. Robinson The impact of glycosylation on HLA-DR1-restricted T cell recognition of type II collagen in a mouse model Arthritis Rheum. 54 2006 482 491
58. S. Tangri, B. Mothe, J. Eisenbraun, J. Sidney, S. Southwood, K. Briggs, J. Zinckgraf, P. Bilsel, M. Newman, and R. Chesnut Rationally engineered therapeutic proteins with reduced immunogenicity J. Immunol. 174 2005 3187 3196
59. G. Winter, A. Fersht, A. Wilkinson, M. Zoller, and M. Smith Redesigning enzyme structure by site-directed mutagenesis: tyrosyl tRNA synthetase and ATP binding Nature 299 1982 756 758
60. L.D. Cabrita, D. Gilis, A.L. Robertson, Y. Dehouck, M. Rooman, and S.P. Bottomley Enhancing the stability and solubility of TEV protease using in silico design Protein Sci. 16 2007 2360 2367
61. R.B. Kapust, J. Tozser, J.D. Fox, D.E. Anderson, S. Cherry, T.D. Copeland, and D.S. Waugh Tobacco etch virus protease: mechanism of autolysis and rational design of stable mutants with wild-type catalytic proficiency Protein Eng. 14 2001 993 1000
62. L. Hedstrom, L. Szilagyi, and W.J. Rutter Converting trypsin to chymotrypsin: the role of surface loops Science 255 1992 1249 1253
63. C. Craik, C. Largman, T. Fletcher, S. Roczniak, P. Barr, R. Fletterick, and W. Rutter Redesigning trypsin: alteration of substrate specificity Science 228 1985 291 297
64. T. Kurth, D. Ullmann, H. Jakubke, and L. Hedstrom Converting trypsin to chymotrypsin: structural determinants of S1′ specificity Biochemistry 36 1997 10098 10104
65. T. Kurth, S. Grahn, M. Thormann, D. Ullmann, H. Hofmann, H. Jakubke, and L. Hedstrom Engineering the S1′ subsite of trypsin: design of a protease which cleaves between dibasic residues Biochemistry 37 1998 11434 11440
66. M. Ballinger, J. Tom, and J. Wells Designing subtilisin BPN′ to cleave substrates containing dibasic residues Biochemistry 34 1995 13312 13319
67. M. Ballinger, J. Tom, and J. Wells Furilisin: a variant of subtilisin BPN′ engineered for cleaving tribasic substrates Biochemistry 35 1996 13579 13585
68. H. Mei, Y. Liaw, Y. Li, D. Wang, H. Takagi, and Y. Tsai Engineering subtilisin YaB: restriction of substrate specificity by the substitution of Gly124 and Gly151 with Ala Protein Eng. 11 1998 109 117
69. P. Carter, B. Nilsson, J. Burnier, D. Burdick, and J. Wells Engineering subtilisin BPN′ for site-specific proteolysis Proteins 6 1989 240 248
70. M. Rheinnecker, G. Baker, J. Eder, and A. Fersht Engineering a novel specificity in subtilisin BPN′ Biochemistry 32 1993 1199 1203
71. M. Rheinnecker, J. Eder, P. Pandey, and A. Fersht Variants of subtilisin BPN′ with altered specificity profiles Biochemistry 33 1994 221 225
72. E.J. Lim, S. Sampath, J. Coll-Rodriguez, J. Schmidt, K. Ray, and D.W. Rodgers Swapping the substrate specificities of the neuropeptidases neurolysin and thimet oligopeptidase J. Biol. Chem. 282 2007 9722 9732
73. K. Olesen, and K. Breddam Increase of the P1 Lys/Leu substrate preference of carboxypeptidase Y by rational design based on known primary and tertiary structures of serine carboxypeptidases Biochemistry 34 1995 15689 15699
74. T. Shintani, K. Nomura, and E. Ichishima Engineering of porcine pepsin. Alteration of S1 substrate specificity of pepsin to those of fungal aspartic proteinases by site-directed mutagenesis J. Biol. Chem. 272 1997 18855 18861
75. H. Khouri, T. Vernet, R. Menard, F. Parlati, P. Laflamme, D. Tessier, B. Gour-Salin, D. Thomas, and A. Storer Engineering of papain: selective alteration of substrate specificity by site-directed mutagenesis Biochemistry 30 1991 8929 8936
76. D. Bromme, P. Bonneau, P. Lachance, and A. Storer Engineering the S2 subsite specificity of human cathepsin S to a cathepsin L- and cathepsin B-like specificity J. Biol. Chem. 269 1994 30238 30242
77. P. Scarborough, and B. Dunn Redesign of the substrate specificity of human cathepsin D: the dominant role of position 287 in the S2 subsite Protein Eng. 7 1994 495 502
78. T. Tanaka, H. Matsuzawa, and T. Ohta Engineering of S2 site of aqualysin I: alteration of P2 specificity by excluding P2 side chain Biochemistry 37 1998 17402 17407
79. T.L. O'Loughlin, D.N. Greene, and I. Matsumura Diversification and specialization of HIV protease function during in vitro evolution Mol. Biol. Evol. 23 2006 764 772
80. K.D. Verhoeven, O.C. Altstadt, and S.N. Savinov Intracellular detection and evolution of site-specific proteases using a genetic selection system Appl. Biochem. Biotechnol. 166 2012 1340 1354
81. N. Varadarajan, J. Gam, M.J. Olsen, G. Georgiou, and B.L. Iverson Engineering of protease variants exhibiting high catalytic activity and exquisite substrate selectivity Proc. Natl. Acad. Sci. USA 102 2005 6855 6860
82. N. Varadarajan, S. Rodriguez, B.Y. Hwang, G. Georgiou, and B.L. Iverson Highly active and selective endopeptidases with programmed substrate specificities Nat. Chem. Biol. 4 2008 290 294
83. F. Kohler A yeast-based growth assay for the analysis of site-specific proteases Nucleic Acids Res. 31 2003 e16
84. N. Varadarajan, G. Georgiou, and B.L. Iverson An engineered protease that cleaves specifically after sulfated tyrosine Angew. Chem.; Int. Ed. Engl. 47 2008 7861 7863
85. N. Varadarajan, M. Pogson, G. Georgiou, and B.L. Iverson Proteases that can distinguish among different post-translational forms of tyrosine engineered using multicolor flow cytometry J. Am. Chem. Soc. 131 2009 18186 18190
86. Z. Knight, J. Garrison, K. Chan, D. King, and K. Shokat A remodelled protease that cleaves phosphotyrosine substrates J. Am. Chem. Soc. 129 2007 11672 11673
87. G. Kostallas, and P. Samuelson Novel fluorescence-assisted whole-cell assay for engineering and characterization of proteases and their substrates Appl. Environ. Microbiol. 76 2010 7500 7508
88. P.S. Daugherty Protein engineering with bacterial display Curr. Opin. Struct. Biol. 17 2007 474 480
89. M. Pogson, G. Georgiou, and B.L. Iverson Engineering next generation proteases Curr. Opin. Biotechnol. 20 2009 390 397
90. S. Sellamuthu, B.H. Shin, E.S. Lee, S.H. Rho, W. Hwang, Y.J. Lee, H.E. Han, J.I. Kim, and W.J. Park Engineering of protease variants exhibiting altered substrate specificity Biochem. Biophys. Res. Commun. 371 2008 122 126
91. S. Sellamuthu, B.H. Shin, H.E. Han, S.M. Park, H.J. Oh, S.H. Rho, Y.J. Lee, and W.J. Park An engineered viral protease exhibiting substrate specificity for a polyglutamine stretch prevents polyglutamine-induced neuronal cell death PLoS ONE 6 2011 e22554
92. D. Gray, S. Mahrus, and J. Wells Activation of specific apoptotic caspases with an engineered small-molecule-activated protease Cell 142 2010 637 646
93. O. Erster, J. Thomas, J. Hamzah, A. Jabaiah, J. Getz, T. Schoep, S. Hall, E. Ruoslahti, and P. Daugherty Site-specific targeting of antibody activity in vivo mediated by disease-associated proteases J. Control Release 161 2012 804 812
94. T. Jiang, E. Olson, Q. Nguyen, M. Roy, P. Jennings, and R. Tsien Tumor imaging by means of proteolytic activation of cell-penetrating peptides Proc. Natl. Acad. Sci. USA 101 2004 17867 17872