Current strategies for probing substrate specificity of proteases

Current Medicinal Chemistry

Volumn 17, Issue 33, 2010, Pages 3968-3995

  Poreba, M ^a   Drag, M ^a,b  

^a WROCLAW UNIVERSITY OF TECHNOLOGY   (Poland)

^b BURNHAM INSTITUTE   (United States)

Author keywords

Combinatorial; Fluorogenic; Library; Positional scanning substrate combinatorial library; Protease; Substrate; Substrate specificity

Indexed keywords

BLOOD CLOTTING FACTOR 10A; BLOOD CLOTTING FACTOR 7A; BROMELAIN; CASPASE 11; CASPASE 14; CASPASE 2; CASPASE 3; CASPASE 4; CASPASE 5; CASPASE 6; CASPASE 7; CASPASE 8; CASPASE 9; CATHEPSIN B; CATHEPSIN F; CATHEPSIN K; CATHEPSIN L; CATHEPSIN S; CATHEPSIN V; CHYMASE; CHYMOTRYPSIN; CRUZIPAIN; FALCIPAIN 2; GRANZYME B; HEPSIN; INTERLEUKIN 1BETA CONVERTING ENZYME; LEGUMAIN; PROTEINASE; PROTEINASE INHIBITOR; UNINDEXED DRUG;

BACTERIOPHAGE; CARBOXY TERMINAL SEQUENCE; CLINICAL TRIAL (TOPIC); COMBINATORIAL LIBRARY; DNA MICROARRAY; ENZYME SPECIFICITY; ENZYME STRUCTURE; ENZYME SUBSTRATE; ENZYME SUBSTRATE COMPLEX; HUMAN; MOLECULAR PROBE; NONHUMAN; PROTEIN LOCALIZATION; PROTEIN MICROARRAY; PROTEIN MOTIF; PROTEOMICS; REVIEW; SCREENING; SOLID;

COMBINATORIAL CHEMISTRY TECHNIQUES; DRUG DESIGN; DRUG DISCOVERY; HUMANS; PEPTIDE HYDROLASES; PEPTIDE LIBRARY; SUBSTRATE SPECIFICITY;

EID: 79251491023     PISSN: 09298673     EISSN: None     Source Type: Journal    
DOI: 10.2174/092986710793205381     Document Type: Review

References (167)

1. Turk, B. Targeting proteases: Successes, failures and future prospects. Nat. Rev. Drug Discov., 2006, 5(9), 785-799.
2. Denault, J.B.; Salvesen, G.S. Apoptotic caspase activation and activity. Methods Mol. Biol., 2008, 414, 191-220.
3. Bennett, B.; Ratnoff, O.D. The normal coagulation mechanism. Med. Clin. North Am., 1972, 56(1), 95-104.
4. Coussens, L.M.; Fingleton, B.; Matrisian, L.M. Matrix metalloproteinase inhibitors and cancer: Trials and tribulations. Science, 2002, 295(5564), 2387-2392.
5. Overall, C.M.; Lopez-Otin, C. Strategies for MMP inhibition in cancer: Innovations for the post-trial era. Nat. Rev. Cancer, 2002, 2(9), 657-672.
6. Joyce, J.A.; Hanahan, D. Multiple roles for cysteine cathepsins in cancer. Cell Cycle, 2004, 3(12), 1516-1619.
7. Schechter, I.; Berger, A. On the size of the active site in proteases. I. Papain. Biochem. Biophys. Res. Commun., 1967, 27(2), 157-162.
8. Thornberry, N.A.; Rano, T.A.; Peterson, E.P.; Rasper, D.M.; Timkey, T.; Garcia-Calvo, M.; Houtzager, V.M.; Nordstrom, P.A.; Roy, S.; Vaillancourt, J.P.; Chapman, K.T.; Nicholson, D.W. A combinatorial approach defines specificities of members of the caspase family and granzyme B. Functional relationships established for key mediators of apoptosis. J. Biol. Chem., 1997, 272(29), 17907-17911.
9. Drag, M.; Salvesen, G.S. DeSUMOylating enzymes-SENPs. IUBMB Life, 2008, 60(11), 734-742.
10. Drag, M.; Mikolajczyk, J.; Bekes, M.; Reyes-Turcu, F.E.; Ellman, J.A.; Wilkinson, K.D.; Salvesen, G.S. Positional-scanning fluorigenic substrate libraries reveal unexpected specificity determinants of DUBs (deubiquitinating enzymes). Biochem. J., 2008, 415(3), 367-375.
11. Rawlings, N.D.; Morton, F.R.; Kok, C.Y.; Kong, J.; Barrett, A.J. MEROPS: The peptidase database. Nucleic Acids Res., 2008, 36(Database issue), D320-325.
12. Lim, M.D.; Craik, C.S. Using specificity to strategically target proteases. Bioorg. Med. Chem., 2009, 17(3), 1094-1100.
13. Petrassi, H.M.; Williams, J.A.; Li, J.; Tumanut, C.; Ek, J.; Nakai, T.; Masick, B.; Backes, B.J.; Harris, J.L. A strategy to profile prime and non-prime proteolytic substrate specificity. Bioorg. Med. Chem. Lett., 2005, 15(12), 3162-3166.
14. Diamond, S.L. Methods for mapping protease specificity. Curr. Opin. Chem. Biol., 2007, 11(1), 46-51.
15. Abbenante, G.; Fairlie, D.P. Protease inhibitors in the clinic. Med. Chem., 2005, 1(1), 71-104.
16. Adams, J.; Kauffman, M. Development of the proteasome inhibitor Velcade (Bortezomib). Cancer Invest., 2004, 22(2), 304-311.
17. Leiting, B.; Pryor, K.D.; Wu, J.K.; Marsilio, F.; Patel, R.A.; Craik, C.S.; Ellman, J.A.; Cummings, R.T.; Thornberry, N.A. Catalytic properties and inhibition of proline-specific dipeptidyl peptidases II, IV and VII. Biochem. J., 2003, 371(Pt 2), 525-532.
18. Ostresh, J.M.; Winkle, J.H.; Hamashin, V.T.; Houghten, R.A. Peptide Libraries - Determination of Relative Reaction-Rates of Protected Amino-Acids in Competitive Couplings. Biopolymers, 1994, 34(12), 1681-1689.
19. Acharya, A.N.; Ostresh, J.M.; Houghten, R.A. Determination of isokinetic ratios necessary for equimolar incorporation of carboxylic acids in the solid-phase synthesis of mixture-based combinatorial libraries. Biopolymers, 2002, 65(1), 32-39.
20. Furka, A.; Sebestyen, F.; Asgedom, M.; Dibo, G. General method for rapid synthesis of multicomponent peptide mixtures. Int. J. Pept. Protein Res., 1991, 37(6), 487-493.
21. Lam, K.S.; Salmon, S.E.; Hersh, E.M.; Hruby, V.J.; Kazmierski, W.M.; Knapp, R.J. A new type of synthetic peptide library for identifying ligand-binding activity. Nature, 1991, 354(6348), 82-84.
22. Houghten, R.A.; Pinilla, C.; Blondelle, S.E.; Appel, J.R.; Dooley, C.T.; Cuervo, J.H. Generation and use of synthetic peptide combinatorial libraries for basic research and drug discovery. Nature, 1991, 354(6348), 84-86.
23. Pinilla, C.; Appel, J.R.; Blanc, P.; Houghten, R.A. Rapid identification of high affinity peptide ligands using positional scanning synthetic peptide combinatorial libraries. Biotechniques, 1992, 13(6), 901-905.
24. Owens, R.A.; Gesellchen, P.D.; Houchins, B.J.; DiMarchi, R.D. The rapid identification of HIV protease inhibitors through the synthesis and screening of defined peptide mixtures. Biochem. Biophys. Res. Commun., 1991, 181(1), 402-408.
25. Rano, T.A.; Timkey, T.; Peterson, E.P.; Rotonda, J.; Nicholson, D.W.; Becker, J.W.; Chapman, K.T.; Thornberry, N.A. A combinatorial approach for determining protease specificities: Application to interleukin-1beta converting enzyme (ICE). Chem. Biol., 1997, 4(2), 149-155.
26. Butenas, S.; Orfeo, T.; Lawson, J.H.; Mann, K.G. Aminonaphthalenesulfonamides, a new class of modifiable fluorescent detecting groups and their use in substrates for serine protease enzymes. Biochemistry, 1992, 31(23), 5399-5411.
27. Cai, S.X.; Zhang, H.Z.; Guastella, J.; Drewe, J.; Yang, W.; Weber, E. Design and synthesis of rhodamine 110 derivative and caspase-3 substrate for enzyme and cell-based fluorescent assay. Bioorg. Med. Chem. Lett., 2001, 11(1), 39-42.
28. Sleath, P.R.; Hendrickson, R.C.; Kronheim, S.R.; March, C.J.; Black, R.A. Substrate specificity of the protease that processes human interleukin-1 beta. J. Biol. Chem., 1990, 265(24), 14526-14528.
29. Thornberry, N.A.; Molineaux, S.M. Interleukin-1 beta converting enzyme: A novel cysteine protease required for IL-1 beta production and implicated in programmed cell death. Protein Sci., 1995, 4(1), 3-12.
30. Thornberry, N.A.; Chapman, K.T.; Nicholson, D.W. Determination of caspase specificities using a peptide combinatorial library. Methods Enzymol., 2000, 322, 100-110.
31. Edwards, P.D.; Mauger, R.C.; Cottrell, K.M.; Morris, F.X.; Pine, K.K.; Sylvester, M.A.; Scott, C.W.; Furlong, S.T. Synthesis and enzymatic evaluation of a P1 arginine aminocoumarin substrate library for trypsin-like serine proteases. Bioorg. Med. Chem. Lett., 2000, 10(20), 2291-2294.
32. Backes, B.J.; Harris, J.L.; Leonetti, F.; Craik, C.S.; Ellman, J.A. Synthesis of positional-scanning libraries of fluorogenic peptide substrates to define the extended substrate specificity of plasmin and thrombin. Nat. Biotechnol., 2000, 18(2), 187-193.
33. Harris, J.L.; Backes, B.J.; Leonetti, F.; Mahrus, S.; Ellman, J.A.; Craik, C.S. Rapid and general profiling of protease specificity by using combinatorial fluorogenic substrate libraries. Proc. Natl. Acad. Sci. U S A, 2000, 97(14), 7754-7759.
34. Maly, D.J.; Leonetti, F.; Backes, B.J.; Dauber, D.S.; Harris, J.L.; Craik, C.S.; Ellman, J.A. Expedient solid-phase synthesis of fluorogenic protease substrates using the 7-amino-4- carbamoylmethylcoumarin (ACC) fluorophore. J. Org. Chem., 2002, 67(3), 910-915.
35. Zhu, Q.; Li, D.B.; Uttamchandani, M.; Yao, S.Q. Facile synthesis of 7-amino-4-carbamoylmethylcoumarin (ACC)-containing solid supports and their corresponding fluorogenic protease substrates. Bioorg. Med. Chem. Lett., 2003, 13(6), 1033-1036.
36. Choe, Y.; Leonetti, F.; Greenbaum, D.C.; Lecaille, F.; Bogyo, M.; Bromme, D.; Ellman, J.A.; Craik, C.S. Substrate profiling of cysteine proteases using a combinatorial peptide library identifies functionally unique specificities. J. Biol. Chem., 2006, 281(18), 12824-12832.
37. Debela, M.; Magdolen, V.; Schechter, N.; Valachova, M.; Lottspeich, F.; Craik, C.S.; Choe, Y.; Bode, W.; Goettig, P. Specificity profiling of seven human tissue kallikreins reveals individual subsite preferences. J. Biol. Chem., 2006, 281(35), 25678-25688.
38. Lee, D.; Adams, J.L.; Brandt, M.; DeWolf, W.E. Jr.; Keller, P.M.; Levy, M.A. A substrate combinatorial array for caspases. Bioorg. Med. Chem. Lett., 1999, 9(12), 1667-1672.
39. Kang, S.J.; Wang, S.; Hara, H.; Peterson, E.P.; Namura, S.; Amin- Hanjani, S.; Huang, Z.; Srinivasan, A.; Tomaselli, K.J.; Thornberry, N.A.; Moskowitz, M.A.; Yuan, J. Dual role of caspase-11 in mediating activation of caspase-1 and caspase-3 under pathological conditions. J. Cell. Biol., 2000, 149(3), 613-622.
40. Park, K.; Kuechle, M.K.; Choe, Y.; Craik, C.S.; Lawrence, O.T.; Presland, R.B. Expression and characterization of constitutively active human caspase-14. Biochem. Biophys. Res. Commun., 2006, 347(4), 941-948.
41. Raymond, W.W.; Ruggles, S.W.; Craik, C.S.; Caughey, G.H. Albumin is a substrate of human chymase. Prediction by combinatorial peptide screening and development of a selective inhibitor based on the albumin cleavage site. J. Biol. Chem., 2003, 278(36), 34517-34524.
42. Lucas, J.J.; Hayes, G.R.; Kalsi, H.K.; Gilbert, R.O.; Choe, Y.; Craik, C.S.; Singh, B.N. Characterization of a cysteine protease from Tritrichomonas foetus that induces host-cell apoptosis. Arch. Biochem. Biophys., 2008, 477(2), 239-243.
43. Mathieu, M.A.; Bogyo, M.; Caffrey, C.R.; Choe, Y.; Lee, J.; Chapman, H.; Sajid, M.; Craik, C.S.; McKerrow, J.H. Substrate specificity of schistosome versus human legumain determined by P1-P3 peptide libraries. Mol. Biochem. Parasitol., 2002, 121(1), 99-105.
44. Li, J.; Lim, S.P.; Beer, D.; Patel, V.; Wen, D.; Tumanut, C.; Tully, D.C.; Williams, J.A.; Jiricek, J.; Priestle, J.P.; Harris, J.L.; Vasudevan, S.G. Functional profiling of recombinant NS3 proteases from all four serotypes of dengue virus using tetrapeptide and octapeptide substrate libraries. J. Biol. Chem., 2005, 280(31), 28766-28774.
45. Snipas, S.J.; Drag, M.; Stennicke, H.R.; Salvesen, G.S. Activation mechanism and substrate specificity of the Drosophila initiator caspase DRONC. Cell Death Differ., 2008, 15(5), 938-945.
46. Larsen, K.S.; Ostergaard, H.; Bjelke, J.R.; Olsen, O.H.; Rasmussen, H.B.; Christensen, L.; Kragelund, B.B.; Stennicke, H.R. Engineering the substrate and inhibitor specificities of human coagulation Factor VIIa. Biochem. J., 2007, 405(3), 429-438.
47. Furlong, S.T.; Mauger, R.C.; Strimpler, A.M.; Liu, Y.P.; Morris, F.X.; Edwards, P.D. Synthesis and physical characterization of a P1 arginine combinatorial library, and its application to the determination of the substrate specificity of serine peptidases. Bioorg. Med. Chem., 2002, 10(11), 3637-3647.
48. Subramanian, S.; Hardt, M.; Choe, Y.; Niles, R.K.; Johansen, E.B.; Legac, J.; Gut, J.; Kerr, I.D.; Craik, C.S.; Rosenthal, P.J. Hemoglobin cleavage site-specificity of the Plasmodium falciparum cysteine proteases falcipain-2 and falcipain-3. PLoS One, 2009, 4(4), e5156.
49. Edosada, C.Y.; Quan, C.; Wiesmann, C.; Tran, T.; Sutherlin, D.; Reynolds, M.; Elliott, J.M.; Raab, H.; Fairbrother, W.; Wolf, B.B. Selective inhibition of fibroblast activation protein protease based on dipeptide substrate specificity. J. Biol. Chem., 2006, 281(11), 7437-7444.
50. Ruggles, S.W.; Fletterick, R.J.; Craik, C.S. Characterization of structural determinants of granzyme B reveals potent mediators of extended substrate specificity. J. Biol. Chem., 2004, 279(29), 30751-30759.
51. Mahrus, S.; Kisiel, W.; Craik, C.S. Granzyme M is a regulatory protease that inactivates proteinase inhibitor 9, an endogenous inhibitor of granzyme B. J. Biol. Chem., 2004, 279(52), 54275-54282.
52. Herter, S.; Piper, D.E.; Aaron, W.; Gabriele, T.; Cutler, G.; Cao, P.; Bhatt, A.S.; Choe, Y.; Craik, C.S.; Walker, N.; Meininger, D.; Hoey, T.; Austin, R.J. Hepatocyte growth factor is a preferred in vitro substrate for human hepsin, a membrane-anchored serine protease implicated in prostate and ovarian cancers. Biochem. J., 2005, 390(Pt 1), 125-136.
53. Janssen, S.; Jakobsen, C.M.; Rosen, D.M.; Ricklis, R.M.; Reineke, U.; Christensen, S.B.; Lilja, H.; Denmeade, S.R. Screening a combinatorial peptide library to develop a human glandular kallikrein 2-activated prodrug as targeted therapy for prostate cancer. Mol. Cancer Ther., 2004, 3(11), 1439-1450.
54. Salter, J.P.; Choe, Y.; Albrecht, H.; Franklin, C.; Lim, K.C.; Craik, C.S.; McKerrow, J.H. Cercarial elastase is encoded by a functionally conserved gene family across multiple species of schistosomes. J. Biol. Chem., 2002, 277(27), 24618-24624.
55. Borgono, C.A.; Gavigan, J.A.; Alves, J.; Bowles, B.; Harris, J.L.; Sotiropoulou, G.; Diamandis, E.P. Defining the extended substrate specificity of kallikrein 1-related peptidases. Biol. Chem., 2007, 388(11), 1215-1225.
56. Marnett, A.B.; Nomura, A.M.; Shimba, N.; Ortiz de Montellano, P.R.; Craik, C.S. Communication between the active sites and dimer interface of a herpesvirus protease revealed by a transitionstate inhibitor. Proc. Natl. Acad. Sci. U.S.A., 2004, 101(18), 6870-6875.
57. Sexton, K.B.; Witte, M.D.; Blum, G.; Bogyo, M. Design of cellpermeable, fluorescent activity-based probes for the lysosomal cysteine protease asparaginyl endopeptidase (AEP)/legumain. Bioorg. Med. Chem. Lett., 2007, 17(3), 649-653.
58. Takeuchi, T.; Harris, J.L.; Huang, W.; Yan, K.W.; Coughlin, S.R.; Craik, C.S. Cellular localization of membrane-type serine protease 1 and identification of protease-activated receptor-2 and singlechain urokinase-type plasminogen activator as substrates. J. Biol. Chem., 2000, 275(34), 26333-26342.
59. Lopez-Garcia, B.; Marcos, J.F.; Abad, C.; Perez-Paya, E. Stabilisation of mixed peptide/lipid complexes in selective antifungal hexapeptides. Biochim. Biophys. Acta, 2004, 1660(1-2), 131-137.
60. Shipway, A.; Danahay, H.; Williams, J.A.; Tully, D.C.; Backes, B.J.; Harris, J.L. Biochemical characterization of prostasin, a channel activating protease. Biochem. Biophys. Res. Commun., 2004, 324(2), 953-963.
61. Goetz, D.H.; Choe, Y.; Hansell, E.; Chen, Y.T.; McDowell, M.; Jonsson, C.B.; Roush, W.R.; McKerrow, J.; Craik, C.S. Substrate specificity profiling and identification of a new class of inhibitor for the major protease of the SARS coronavirus. Biochemistry, 2007, 46(30), 8744-8752.
62. Drag, M.; Mikolajczyk, J.; Krishnakumar, I.M.; Huang, Z.; Salvesen, G.S. Activity profiling of human deSUMOylating enzymes (SENPs) with synthetic substrates suggests an unexpected specificity of two newly characterized members of the family. Biochem. J., 2008, 409(2), 461-469.
63. Dubin, G.; Stec-Niemczyk, J.; Kisielewska, M.; Pustelny, K.; Popowicz, G.M.; Bista, M.; Kantyka, T.; Boulware, K.T.; Stennicke, H.R.; Czarna, A.; Phopaisarn, M.; Daugherty, P.S.; Thogersen, I.B.; Enghild, J.J.; Thornberry, N.; Dubin, A.; Potempa, J. Enzymatic activity of the Staphylococcus aureus SplB serine protease is induced by substrates containing the sequence Trp-Glu-Leu- Gln. J. Mol. Biol., 2008, 379(2), 343-356.
64. Tian, Y.; Sohar, I.; Taylor, J.W.; Lobel, P. Determination of the substrate specificity of tripeptidyl-peptidase I using combinatorial peptide libraries and development of improved fluorogenic substrates. J. Biol. Chem., 2006, 281(10), 6559-6572.
65. Harris, J.L.; Niles, A.; Burdick, K.; Maffitt, M.; Backes, B.J.; Ellman, J.A.; Kuntz, I.; Haak-Frendscho, M.; Craik, C.S. Definition of the extended substrate specificity determinants for beta-tryptases I and II. J. Biol. Chem., 2001, 276(37), 34941-34947.
66. Drag, M.; Bogyo, M.; Ellman, J.A.; Salvesen, G.S. Aminopeptidase fingerprints. An integrated approach for identification of good substrates and optimal inhibitors. J. Biol. Chem., 2010, 285, 3310-3318.
67. Walters, J.; Pop, C.; Scott, F.L.; Drag, M.; Swartz, P.; Mattos, C.; Salvesen, G.S.; Clark, A.C. A constitutively active and uninhibitable caspase-3 zymogen efficiently induces apoptosis. Biochem. J., 2009, 424, 335-345.
68. Wood, W.J.; Patterson, A.W.; Tsuruoka, H.; Jain, R.K.; Ellman, J.A. Substrate activity screening: A fragment-based method for the rapid identification of nonpeptidic protease inhibitors. J. Am. Chem. Soc., 2005, 127(44), 15521-15527.
69. Patterson, A.W.; Wood, W.J.; Hornsby, M.; Lesley, S.; Spraggon, G.; Ellman, J.A. Identification of selective, nonpeptidic nitrile inhibitors of cathepsin s using the substrate activity screening method. J. Med. Chem., 2006, 49(21), 6298-6307.
70. Patterson, A.W.; Wood, W.J.; Ellman, J.A. Substrate activity screening (SAS): A general procedure for the preparation and screening of a fragment-based non-peptidic protease substrate library for inhibitor discovery. Nat. Protoc., 2007, 2(2), 424-433.
71. Lesner, A.; Brzozowski, K.; Kupryszewski, G.; Rolka, K. Design, chemical synthesis and kinetic studies of trypsin chromogenic substrates based on the proteinase binding loop of Cucurbita maxima trypsin inhibitor (CMTI-III). Biochem. Biophys. Res. Commun., 2000, 269(1), 81-84.
72. Hojo, K.; Maeda, M.; Iguchi, S.; Smith, T.; Okamoto, H.; Kawasaki, K. Amino acids and peptides. XXXV. Facile preparation of pnitroanilide analogs by the solid-phase method. Chem. Pharm. Bull. (Tokyo), 2000, 48(11), 1740-1744.
73. Zablotna, E.; Dysasz, H.; Lesner, A.; Jaskiewicz, A.; Kazmierczak, K.; Miecznikowska, H.; Rolka, K. A simple method for selection of trypsin chromogenic substrates using combinatorial chemistry approach. Biochem. Biophys. Res. Commun., 2004, 319(1), 185-188.
74. Barrios, A.M.; Craik, C.S. Scanning the prime-site substrate specificity of proteolytic enzymes: A novel assay based on ligandenhanced lanthanide ion fluorescence. Bioorg. Med. Chem. Lett., 2002, 12(24), 3619-3623.
75. Salisbury, C.M.; Maly, D.J.; Ellman, J.A. Peptide microarrays for the determination of protease substrate specificity. J. Am. Chem. Soc., 2002, 124(50), 14868-14870.
76. Gosalia, D.N.; Diamond, S.L. Printing chemical libraries on microarrays for fluid phase nanoliter reactions. Proc. Natl. Acad. Sci. U S A, 2003, 100(15), 8721-8726.
77. Klibanov, A.M. Why are enzymes less active in organic solvents than in water? Trends Biotechnol., 1997, 15(3), 97-101.
78. Gosalia, D.N.; Salisbury, C.M.; Maly, D.J.; Ellman, J.A.; Diamond, S.L. Profiling serine protease substrate specificity with solution phase fluorogenic peptide microarrays. Proteomics, 2005, 5(5), 1292-1298.
79. Gosalia, D.N.; Salisbury, C.M.; Ellman, J.A.; Diamond, S.L. High throughput substrate specificity profiling of serine and cysteine proteases using solution-phase fluorogenic peptide microarrays. Mol. Cell Proteom., 2005, 4(5), 626-636.
80. Vijayendran, R.A.; Leckband, D.E. A quantitative assessment of heterogeneity for surface-immobilized proteins. Anal. Chem., 2001, 73(3), 471-480.
81. Johnson, C.P.; Jensen, I.E.; Prakasam, A.; Vijayendran, R.; Leckband, D. Engineered protein a for the orientational control of immobilized proteins. Bioconjug. Chem., 2003, 14(5), 974-978.
82. Zaks, A.; Klibanov, A.M. The effect of water on enzyme action in organic media. J. Biol. Chem., 1988, 263(17), 8017-8021.
83. Winssinger, N.; Damoiseaux, R.; Tully, D.C.; Geierstanger, B.H.; Burdick, K.; Harris, J.L. PNA-encoded protease substrate microarrays. Chem. Biol., 2004, 11(10), 1351-1360.
84. Yaron, A.; Carmel, A.; Katchalski-Katzir, E. Intramolecularly quenched fluorogenic substrates for hydrolytic enzymes. Anal. Biochem., 1979, 95(1), 228-235.
85. Meldal, M.; Breddam, K. Anthranilamide and nitrotyrosine as a donor-acceptor pair in internally quenched fluorescent substrates for endopeptidases: Multicolumn peptide synthesis of enzyme substrates for subtilisin Carlsberg and pepsin. Anal. Biochem., 1991, 195(1), 141-147.
86. Matayoshi, E.D.; Wang, G.T.; Krafft, G.A.; Erickson, J. Novel fluorogenic substrates for assaying retroviral proteases by resonance energy transfer. Science, 1990, 247(4945), 954-958.
87. Nagase, H.; Fields, C.G.; Fields, G.B. Design and characterization of a fluorogenic substrate selectively hydrolyzed by stromelysin 1 (matrix metalloproteinase-3). J. Biol. Chem., 1994, 269(33), 20952-20957.
88. Chagas, J.R.; Juliano, L.; Prado, E.S. Intramolecularly quenched fluorogenic tetrapeptide substrates for tissue and plasma kallikreins. Anal. Biochem., 1991, 192(2), 419-425.
89. Stocker, W.; Ng, M.; Auld, D.S. Fluorescent oligopeptide substrates for kinetic characterization of the specificity of Astacus protease. Biochemistry, 1990, 29(45), 10418-10425.
90. Barrett, A.J.; Knight, C.G.; Brown, M.A.; Tisljar, U. A continuous fluorimetric assay for clostridial collagenase and Pz-peptidase activity. Biochem. J., 1989, 260(1), 259-263.
91. Maggiora, L.L.; Smith, C.W.; Zhang, Z.Y. A general method for the preparation of internally quenched fluorogenic protease substrates using solid-phase peptide synthesis. J. Med. Chem., 1992, 35(21), 3727-3730.
92. Pope, A.J.; Haupts, U.M.; Moore, K.J. Homogeneous fluorescence readouts for miniaturized high-throughput screening: Theory and practice. Drug Discov. Today, 1999, 4(8), 350-362.
93. Meldal, M.; Svendsen, I.; Breddam, K.; Auzanneau, F.I. Portionmixing peptide libraries of quenched fluorogenic substrates for complete subsite mapping of endoprotease specificity. Proc. Natl. Acad. Sci. U.S.A., 1994, 91(8), 3314-3318.
94. St Hilaire, P.M.; Alves, L.C.; Sanderson, S.J.; Mottram, J.C.; Juliano, M.A.; Juliano, L.; Coombs, G.H.; Meldal, M. The substrate specificity of a recombinant cysteine protease from Leishmania mexicana: Application of a combinatorial peptide library approach. Chembiochem, 2000, 1(2), 115-122.
95. St Hilaire, P.M.; Alves, L.C.; Herrera, F.; Renil, M.; Sanderson, S.J.; Mottram, J.C.; Coombs, G.H.; Juliano, M.A.; Juliano, L.; Arevalo, J.; Meldal, M. Solid-phase library synthesis, screening, and selection of tight-binding reduced peptide bond inhibitors of a recombinant Leishmania mexicana cysteine protease B. J. Med. Chem., 2002, 45(10), 1971-1982.
96. Meldal, M.; Svendsen, I. Direct Visualization of Enzyme-Inhibitors Using a Portion Mixing Inhibitor Library Containing a Quenched Fluorogenic Peptide Substrate .1. Inhibitors for Subtilisin Carlsberg. J. Chem. Soc. Perk. T 1, 1995(12), 1591-1596.
97. Meldal, M.; Svendsen, I.B.; Juliano, L.; Juliano, M.A.; Nery, E.D.; Scharfstein, J. Inhibition of cruzipain visualized in a fluorescence quenched solid-phase inhibitor library assay. D-amino acid inhibitors for cruzipain, cathepsin B and cathepsin L. J. Pept. Sci., 1998, 4(2), 83-91.
98. Graven, A.; St Hilaire, P.M.; Sanderson, S.J.; Mottram, J.C.; Coombs, G.H.; Meldal, M. Combinatorial library of peptide isosters based on Diels-Alder reactions: Identification of novel inhibitors against a recombinant cysteine protease from Leishmania mexicana. J. Comb. Chem., 2001, 3(5), 441-452.
99. Buchardt, J.; Schiodt, C.B.; Krog-Jensen, C.; Delaisse, J.M.; Foged, N.T.; Meldal, M. Solid phase combinatorial library of phosphinic peptides for discovery of matrix metalloproteinase inhibitors. J. Comb. Chem., 2000, 2(6), 624-638.
100. Alves, L.C.; Melo, R.L.; Sanderson, S.J.; Mottram, J.C.; Coombs, G.H.; Caliendo, G.; Santagada, V.; Juliano, L.; Juliano, M.A. S1 subsite specificity of a recombinant cysteine proteinase, CPB, of Leishmania mexicana compared with cruzain, human cathepsin L and papain using substrates containing non-natural basic amino acids. Eur. J. Biochem., 2001, 268(5), 1206-1212. (Pubitemid 32231872)
101. Stennicke, H.R.; Renatus, M.; Meldal, M.; Salvesen, G.S. Internally quenched fluorescent peptide substrates disclose the subsite preferences of human caspases 1, 3, 6, 7 and 8. Biochem. J., 2000, 350 Pt 2, 563-568.
102. Rosse, G.; Kueng, E.; Page, M.G.; Schauer-Vukasinovic, V.; Giller, T.; Lahm, H.W.; Hunziker, P.; Schlatter, D. Rapid identification of substrates for novel proteases using a combinatorial peptide library. J. Comb. Chem., 2000, 2(5), 461-466.
103. Oda, K.; Takahashi, T.; Takada, K.; Tsunemi, M.; Ng, K.K.; Hiraga, K.; Harada, S. Exploring the subsite-structure of vimelysin and thermolysin using FRETS-libraries. FEBS Lett., 2005, 579(22), 5013-5018.
104. Ekici, O.D.; Zhu, J.; Wah Chung, I.Y.; Paetzel, M.; Dalbey, R.E.; Pei, D. Profiling the substrate specificity of viral protease VP4 by a FRET-based peptide library approach. Biochemistry, 2009, 48(24), 5753-5759.
105. Mizuno, H.; Sawano, A.; Eli, P.; Hama, H.; Miyawaki, A. Red fluorescent protein from Discosoma as a fusion tag and a partner for fluorescence resonance energy transfer. Biochemistry, 2001, 40(8), 2502-2510.
106. Fretwell, J.F.; SM, K.I.; Cummings, J.M.; Selby, T.L. Characterization of a randomized FRET library for protease specificity determination. Mol. Biosyst., 2008, 4(8), 862-870.
107. Araujo, M.C.; Melo, R.L.; Cesari, M.H.; Juliano, M.A.; Juliano, L.; Carmona, A.K. Peptidase specificity characterization of C- and Nterminal catalytic sites of angiotensin I-converting enzyme. Biochemistry, 2000, 39(29), 8519-8525.
108. Bersanetti, P.A.; Andrade, M.C.; Casarini, D.E.; Juliano, M.A.; Nchinda, A.T.; Sturrock, E.D.; Juliano, L.; Carmona, A.K. Positional-scanning combinatorial libraries of fluorescence resonance energy transfer peptides for defining substrate specificity of the angiotensin I-converting enzyme and development of selective C-domain substrates. Biochemistry, 2004, 43(50), 15729-15736. (Pubitemid 39665072)
109. Sun, H.; Panicker, R.C.; Yao, S.Q. Activity based fingerprinting of proteases using FRET peptides. Biopolymers, 2007, 88(2), 141-149.
110. Hu, Y.; Webb, E.; Singh, J.; Morgan, B.A.; Gainor, J.A.; Gordon, T.D.; Siahaan, T.J. Rapid determination of substrate specificity of Clostridium histolyticum beta-collagenase using an immobilized peptide library. J. Biol. Chem., 2002, 277(10), 8366-8371.
111. Ramjee, M.K.; Flinn, N.S.; Pemberton, T.P.; Quibell, M.; Wang, Y.; Watts, J.P. Substrate mapping and inhibitor profiling of falcipain- 2, falcipain-3 and berghepain-2: Implications for peptidase anti-malarial drug discovery. Biochem. J., 2006, 399(1), 47-57.
112. Gron, H.; Meldal, M.; Breddam, K. Extensive comparison of the substrate preferences of two subtilisins as determined with peptide substrates which are based on the principle of intramolecular quenching. Biochemistry, 1992, 31(26), 6011-6018.
113. Thomas, D.A.; Francis, P.; Smith, C.; Ratcliffe, S.; Ede, N.J.; Kay, C.; Wayne, G.; Martin, S.L.; Moore, K.; Amour, A.; Hooper, N.M. A broad-spectrum fluorescence-based peptide library for the rapid identification of protease substrates. Proteomics, 2006, 6(7), 2112-2120.
114. Cuerrier, D.; Moldoveanu, T.; Davies, P.L. Determination of peptide substrate specificity for mu-calpain by a peptide library-based approach: The importance of primed side interactions. J. Biol. Chem., 2005, 280(49), 40632-40641.
115. Del Nery, E.; Alves, L.C.; Melo, R.L.; Cesari, M.H.; Juliano, L.; Juliano, M.A. Specificity of cathepsin B to fluorescent substrates containing benzyl side-chain-substituted amino acids at P1 subsite. J. Protein Chem., 2000, 19(1), 33-38.
116. Melo, R.L.; Alves, L.C.; Del Nery, E.; Juliano, L.; Juliano, M.A. Synthesis and hydrolysis by cysteine and serine proteases of short internally quenched fluorogenic peptides. Anal. Biochem., 2001, 293(1), 71-77.
117. Menard, R.; Carmona, E.; Plouffe, C.; Bromme, D.; Konishi, Y.; Lefebvre, J.; Storer, A.C. The specificity of the S1' subsite of cysteine proteases. FEBS Lett,, 1993, 328(1-2), 107-110.
118. Cezari, M.H.; Puzer, L.; Juliano, M.A.; Carmona, A.K.; Juliano, L. Cathepsin B carboxydipeptidase specificity analysis using internally quenched fluorescent peptides. Biochem. J., 2002, 368(Pt 1), 365-369.
119. Cotrin, S.S.; Puzer, L.; de Souza Judice, W.A.; Juliano, L.; Carmona, A.K.; Juliano, M.A. Positional-scanning combinatorial libraries of fluorescence resonance energy transfer peptides to define substrate specificity of carboxydipeptidases: Assays with human cathepsin B. Anal. Biochem., 2004, 335(2), 244-252. (Pubitemid 39535189)
120. Peterson, J.J.; Meares, C.F. Cathepsin substrates as cleavable peptide linkers in bioconjugates, selected from a fluorescence quench combinatorial library. Bioconjug. Chem., 1998, 9(5), 618-626.
121. Lesner, A.; Wysocka, M.; Guzow, K.; Wiczk, W.; Legowska, A.; Rolka, K. Development of sensitive cathepsin G fluorogenic substrate using combinatorial chemistry methods. Anal. Biochem., 2008, 375(2), 306-312.
122. Alves, M.F.; Puzer, L.; Cotrin, S.S.; Juliano, M.A.; Juliano, L.; Bromme, D.; Carmona, A.K. S3 to S3' subsite specificity of recombinant human cathepsin K and development of selective internally quenched fluorescent substrates. Biochem. J., 2003, 373(Pt 3), 981-986.
123. Puzer, L.; Cotrin, S.S.; Alves, M.F.; Egborge, T.; Araujo, M.S.; Juliano, M.A.; Juliano, L.; Bromme, D.; Carmona, A.K. Comparative substrate specificity analysis of recombinant human cathepsin V and cathepsin L. Arch. Biochem. Biophys., 2004, 430(2), 274-283.
124. Alves, F.M.; Hirata, I.Y.; Gouvea, I.E.; Alves, M.F.; Meldal, M.; Bromme, D.; Juliano, L.; Juliano, M.A. Controlled peptide solvation in portion-mixing libraries of FRET peptides: Improved specificity determination for Dengue 2 virus NS2B-NS3 protease and human cathepsin S. J. Comb. Chem., 2007, 9(4), 627-634.
125. Diaz-Mochon, J.J.; Bialy, L.; Bradley, M. Dual colour, microarraybased, analysis of 10,000 protease substrates. Chem. Commun. (Camb), 2006(38), 3984-3986.
126. Niyomrattanakit, P.; Yahorava, S.; Mutule, I.; Mutulis, F.; Petrovska, R.; Prusis, P.; Katzenmeier, G.; Wikberg, J.E. Probing the substrate specificity of the dengue virus type 2 NS3 serine protease by using internally quenched fluorescent peptides. Biochem. J., 2006, 397(1), 203-211.
127. Davy, A.; Svendsen, I.; Sorensen, S.O.; Blom Sorensen, M.; Rouster, J.; Meldal, M.; Simpson, D.J.; Cameron-Mills, V. Substrate specificity of barley cysteine endoproteases EP-A and EP-B. Plant Physiol., 1998, 117(1), 255-261.
128. Ludeman, J.P.; Pike, R.N.; Bromfield, K.M.; Duggan, P.J.; Cianci, J.; Le Bonniec, B.; Whisstock, J.C.; Bottomley, S.P. Determination of the P1', P2' and P3' subsite-specificity of factor Xa. Int. J. Biochem. Cell. Biol., 2003, 35(2), 221-225.
129. Bianchini, E.P.; Louvain, V.B.; Marque, P.E.; Juliano, M.A.; Juliano, L.; Le Bonniec, B.F. Mapping of the catalytic groove preferences of factor Xa reveals an inadequate selectivity for its macromolecule substrates. J. Biol. Chem., 2002, 277(23), 20527-20534.
130. Tanskul, S.; Oda, K.; Oyama, H.; Noparatnaraporn, N.; Tsunemi, M.; Takada, K. Substrate specificity of alkaline serine proteinase isolated from photosynthetic bacterium, Rubrivivax gelatinosus KDDS1. Biochem. Biophys. Res. Commun., 2003, 309(3), 547-551.
131. Patterson-Ward, J.; Tedesco, J.; Hudak, J.; Fishovitz, J.; Becker, J.; Frase, H.; McNamara, K.; Lee, I. Utilization of synthetic peptides to evaluate the importance of substrate interaction at the proteolytic site of Escherichia coli Lon protease. Biochim. Biophys. Acta, 2009, 1794(9), 1355-1363.
132. Wysocka, M.; Lesner, A.; Guzow, K.; Mackiewicz, L.; Legowska, A.; Wiczk, W.; Rolka, K. Design of selective substrates of proteinase 3 using combinatorial chemistry methods. Anal. Biochem., 2008, 378(2), 208-215.
133. St Hilaire, P.M.; Willert, M.; Juliano, M.A.; Juliano, L.; Meldal, M. Fluorescence-quenched solid phase combinatorial libraries in the characterization of cysteine protease substrate specificity. J. Comb. Chem., 1999, 1(6), 509-523.
134. Agarkov, A.; Chauhan, S.; Lory, P.J.; Gilbertson, S.R.; Motin, V.L. Substrate specificity and screening of the integral membrane protease Pla. Bioorg. Med. Chem. Lett., 2008, 18(1), 427-431.
135. Ekici, O.D.; Karla, A.; Paetzel, M.; Lively, M.O.; Pei, D.; Dalbey, R.E. Altered -3 substrate specificity of Escherichia coli signal peptidase 1 mutants as revealed by screening a combinatorial peptide library. J. Biol. Chem., 2007, 282(1), 417-425.
136. Camargo, A.C.; Gomes, M.D.; Reichl, A.P.; Ferro, E.S.; Jacchieri, S.; Hirata, I.Y.; Juliano, L. Structural features that make oligopeptides susceptible substrates for hydrolysis by recombinant thimet oligopeptidase. Biochem. J., 1997, 324 ( Pt 2), 517-522.
137. Le Bonniec, B.F.; Myles, T.; Johnson, T.; Knight, C.G.; Tapparelli, C.; Stone, S.R. Characterization of the P2' and P3' specificities of thrombin using fluorescence-quenched substrates and mapping of the subsites by mutagenesis. Biochemistry, 1996, 35(22), 7114-7122.
138. Kumaresan, P.R.; Natarajan, A.; Song, A.; Wang, X.; Liu, R.; DeNardo, G.; DeNardo, S.; Lam, K.S. Development of tissue plasminogen activator specific "on demand cleavable" (odc) linkers for radioimmunotherapy by screening one-bead-one-compound combinatorial peptide libraries. Bioconjug. Chem., 2007, 18(1), 175-182.
139. Turk, B.E.; Huang, L.L.; Piro, E.T.; Cantley, L.C. Determination of protease cleavage site motifs using mixture-based oriented peptide libraries. Nat. Biotechnol., 2001, 19(7), 661-667.
140. Turk, B.E.; Cantley, L.C. Using peptide libraries to identify optimal cleavage motifs for proteolytic enzymes. Methods, 2004, 32(4), 398-405.
141. Arnold, D.; Keilholz, W.; Schild, H.; Dumrese, T.; Stevanovic, S.; Rammensee, H.G. Substrate specificity of cathepsins D and E determined by N-terminal and C-terminal sequencing of peptide pools. Eur. J. Biochem., 1997, 249(1), 171-179. (Pubitemid 27432611)
142. Bertenshaw, G.P.; Turk, B.E.; Hubbard, S.J.; Matters, G.L.; Bylander, J.E.; Crisman, J.M.; Cantley, L.C.; Bond, J.S. Marked differences between metalloproteases meprin A and B in substrate and peptide bond specificity. J. Biol. Chem., 2001, 276(16), 13248-13255.
143. Smith, M.M.; Shi, L.; Navre, M. Rapid identification of highly active and selective substrates for stromelysin and matrilysin using bacteriophage peptide display libraries. J. Biol. Chem., 1995, 270(12), 6440-6449.
144. Matthews, D.J.; Wells, J.A. Substrate phage: Selection of protease substrates by monovalent phage display. Science, 1993, 260(5111), 1113-1117.
145. Harris, J.L.; Peterson, E.P.; Hudig, D.; Thornberry, N.A.; Craik, C.S. Definition and redesign of the extended substrate specificity of granzyme B. J. Biol. Chem., 1998, 273(42), 27364-27373.
146. Huang, C.; Wong, G.W.; Ghildyal, N.; Gurish, M.F.; Sali, A.; Matsumoto, R.; Qiu, W.T.; Stevens, R.L. The tryptase, mouse mast cell protease 7, exhibits anticoagulant activity in vivo and in vitro due to its ability to degrade fibrinogen in the presence of the diverse array of protease inhibitors in plasma. J. Biol. Chem., 1997, 272(50), 31885-31893.
147. Kridel, S.J.; Chen, E.; Smith, J.W. A substrate phage enzymelinked immunosorbent assay to profile panels of proteases. Anal. Biochem., 2001, 294(2), 176-184.
148. Beck, Z.Q.; Lin, Y.C.; Elder, J.H. Molecular basis for the relative substrate specificity of human immunodeficiency virus type 1 and feline immunodeficiency virus proteases. J. Virol., 2001, 75(19), 9458-9469.
149. Hervio, L.S.; Coombs, G.S.; Bergstrom, R.C.; Trivedi, K.; Corey, D.R.; Madison, E.L. Negative selectivity and the evolution of protease cascades: The specificity of plasmin for peptide and protein substrates. Chem. Biol., 2000, 7(6), 443-453.
150. Deng, S.J.; Bickett, D.M.; Mitchell, J.L.; Lambert, M.H.; Blackburn, R.K.; Carter, H.L. 3rd; Neugebauer, J.; Pahel, G.; Weiner, M.P.; Moss, M.L. Substrate specificity of human collagenase 3 assessed using a phage-displayed peptide library. J. Biol. Chem., 2000, 275(40), 31422-31427.
151. Chen, E.I.; Kridel, S.J.; Howard, E.W.; Li, W.; Godzik, A.; Smith, J.W. A unique substrate recognition profile for matrix metalloproteinase- 2. J. Biol. Chem., 2002, 277(6), 4485-4491.
152. Ohkubo, S.; Miyadera, K.; Sugimoto, Y.; Matsuo, K.; Wierzba, K.; Yamada, Y. Substrate phage as a tool to identify novel substrate sequences of proteases. Comb. Chem. High Throughput Screen., 2001, 4(7), 573-583.
153. Matthews, D.J.; Goodman, L.J.; Gorman, C.M.; Wells, J.A. A survey of furin substrate specificity using substrate phage display. Protein Sci., 1994, 3(8), 1197-1205.
154. Vindigni, A.; Dang, Q.D.; Di Cera, E. Site-specific dissection of substrate recognition by thrombin. Nat. Biotechnol., 1997, 15(9), 891-895.
155. Coombs, G.S.; Bergstrom, R.C.; Pellequer, J.L.; Baker, S.I.; Navre, M.; Smith, M.M.; Tainer, J.A.; Madison, E.L.; Corey, D.R. Substrate specificity of prostate-specific antigen (PSA). Chem. Biol., 1998, 5(9), 475-488.
156. Dall'Acqua, W.; Halin, C.; Rodrigues, M.L.; Carter, P. Elastase substrate specificity tailored through substrate-assisted catalysis and phage display. Protein Eng., 1999, 12(11), 981-987.
157. Lopez-Otin, C.; Overall, C.M. Protease degradomics: A new challenge for proteomics. Nat. Rev. Mol. Cell Biol., 2002, 3(7), 509-519.
158. Dix, M.M.; Simon, G.M.; Cravatt, B.F. Global mapping of the topography and magnitude of proteolytic events in apoptosis. Cell, 2008, 134(4), 679-691.
159. Mahrus, S.; Trinidad, J.C.; Barkan, D.T.; Sali, A.; Burlingame, A.L.; Wells, J.A. Global sequencing of proteolytic cleavage sites in apoptosis by specific labeling of protein N termini. Cell, 2008, 134(5), 866-876.
160. Enoksson, M.; Li, J.; Ivancic, M.M.; Timmer, J.C.; Wildfang, E.; Eroshkin, A.; Salvesen, G.S.; Tao, W.A. Identification of proteolytic cleavage sites by quantitative proteomics. J. Proteome Res., 2007, 6(7), 2850-2858.
161. Timmer, J.C.; Zhu, W.; Pop, C.; Regan, T.; Snipas, S.J.; Eroshkin, A.M.; Riedl, S.J.; Salvesen, G.S. Structural and kinetic determinants of protease substrates. Nat. Struct. Mol. Biol., 2009, 16(10), 1101-1108.
162. Timmer, J.C.; Enoksson, M.; Wildfang, E.; Zhu, W.; Igarashi, Y.; Denault, J.B.; Ma, Y.; Dummitt, B.; Chang, Y.H.; Mast, A.E.; Eroshkin, A.; Smith, J.W.; Tao, W.A.; Salvesen, G.S. Profiling constitutive proteolytic events in vivo. Biochem. J., 2007, 407(1), 41-48.
163. Butler, G.S.; Overall, C.M. Updated biological roles for matrix metalloproteinases and new "intracellular" substrates revealed by degradomics. Biochemistry, 2009, 48(46), 10830-10845.
164. Schilling, O.; Overall, C.M. Proteomic discovery of protease substrates. Curr. Opin. Chem. Biol., 2007, 11(1), 36-45.
165. Dean, R.A.; Overall, C.M. Proteomics discovery of metalloproteinase substrates in the cellular context by iTRAQ labeling reveals a diverse MMP-2 substrate degradome. Mol. Cell Proteomics, 2007, 6(4), 611-623.
166. Dean, R.A.; Smith, D.; Overall, C.M. Proteomic identification of cellular protease substrates using isobaric tags for relative and absolute quantification (iTRAQ). Curr. Protoc. Prot. Sci., 2007, Chapter 21, Unit 21 18.
167. Schilling, O.; Overall, C.M. Proteome-derived, database-searchable peptide libraries for identifying protease cleavage sites. Nat. Biotechnol., 2008, 26(6), 685-694.