Synthesis of positional-scanning libraries of fluorogenic peptide substrates to define the extended substrate specificity of plasmin and thrombin

Nature Biotechnology

Volumn 18, Issue 2, 2000, Pages 187-193

  Backes, Bradley J ^a,b   Harris, Jennifer L ^c   Leonetti, Francesco ^a   Craik, Charles S ^c   Ellman, Jonathan A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b GENOMICS INSTITUTE OF THE NOVARTIS RESEARCH FOUNDATION   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Blood coagulation; Combinatorial libraries; Molecular recognition; Proteinase; Serine protease

Indexed keywords

PLASMIN; THROMBIN;

ANALYTIC METHOD; ARTICLE; BINDING SITE; BLOOD CLOTTING; DERIVATIZATION; DNA LIBRARY; ENZYME ACTIVE SITE; ENZYME SPECIFICITY; ENZYME SUBSTRATE; HYDROPHOBICITY; MOLECULAR RECOGNITION; NONHUMAN; PEPTIDE SYNTHESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION;

AMINO ACID SEQUENCE; COMBINATORIAL CHEMISTRY TECHNIQUES; COMPUTER SIMULATION; FLUORESCENT DYES; MODELS, MOLECULAR; OLIGOPEPTIDES; PLASMIN; SUBSTRATE SPECIFICITY; THROMBIN;

EID: 0033951198     PISSN: 10870156     EISSN: None     Source Type: Journal    
DOI: 10.1038/72642     Document Type: Article

References (56)

1. Matthews, D.J. & Wells, J.A. Substrate phage: selection of protease substrates by monovalent phage display. Science 260, 1113-1117 (1993).
2. Ding, L. et al. Origins of the specificity of tissue-type plasminogen activator. Proc. Natl. Acad. Sci. USA 92, 7627-7631 (1995).
3. Bevan, A., Brenner, C. & Fuller, R.S. Quantitative assessment of enzyme specificity in vivo: P2 recognition by Kex2 protease defined in a genetic system. Proc. Natl. Acad. Sci. USA 95, 10384-10389 (1998).
4. Lustig, K.D. et al. Small pool expression screening: identification of genes involved in cell cycle control, apoptosis, and early development. Methods Enzymol. 283, 83-99 (1997).
5. Kothakota, S. et al. Caspase-3-generated fragment of gelsolin: effector of morphological change in apoptosis. Science 278, 294-298 (1997).
6. Petithory, J.R., Masiarz, F.R., Kirsch, J.F., Santi, D.V. & Malcolm, B.A. A rapid method for determination of endoproteinase substrate specificity: specificity of the 3C proteinase from hepatitis A virus. Proc. Natl. Acad. Sci. USA 88, 11510-11514 (1991).
7. Birkett, A.J. et al. Determination of enzyme specificity in a complex mixture of peptide substrates by N-terminal sequence analysis. Anal. Biochem. 196, 137-143 (1991).
8. Berman, J. et al. Rapid optimization of enzyme substrates using defined substrate mixtures. J. Biol. Chem. 267, 1434-1437 (1992).
9. McGeehan, G.M. et al. Characterization of the peptide substrate specificities of interstitial collagenase and 92-kDa gelatinase. Implications for substrate optimization. J. Biol. Chem. 269, 32814-32820 (1994).
10. Schellenberger, V., Turck, C.W., Hedstrom, L. & Rutter, W.J. Mapping the S' subsites of serine proteases using acyl transfer to mixtures of peptide nucleophiles. Biochemistry 32, 4349-4353 (1993).
11. Lam, K.S. & Lebl, M. Synthesis of a one-bead one-compound combinatorial peptide library. Methods Mol. Biol. 87, 1-6 (1998).
12. Meldal, M., Svendsen, I., Breddam, K. & Auzanneau, F.I. Portion-mixing peptide libraries of quenched fluorogenic substrates for complete subsite mapping of endoprotease specificity. Proc. Natl. Acad. Sci.USA 91, 3314-3318 (1994).
13. Meldal, M. et al. 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. Peptide Sci. 4, 83-91 (1998).
14. 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. Combinatorial Chem. VI, 509-523 (1999).
15. Del Nery, E. et al. Characterization of the substrate specificity of the major cysteine protease (cruzipain) from Trypanosoma cruzi using a portion-mixing combinatorial library and fluorogenic peptides. Biochem. J. 323, 427-433 (1997).
16. Dooley, C.T. & Houghten, R.A. Synthesis and screening of positional scanning combinatorial libraries. Methods Mol. Biol. 87, 13-24 (1998).
17. 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 13, 901-905 (1992).
18. Rano, T.A. et al. A combinatorial approach for determining protease specificities: application to interleukin-1beta converting enzyme (ICE). Chem.Biol. 4, 149-155 (1997).
19. Thornberry, N.A. et al. 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. 272, 17907-17911 (1997).
20. Schechter, I., Berger, A. On the size of the active site in proteases. I. Papain. Biochem. Biophys. Chem. Commun. 27, 157-162 (1968).
21. Backes, B.J. & Ellman, J.A. An alkane sulfonamide "safety-catch" linker for solid-phase synthesis. J. Org. Chem. 64, 2322-2330 (1999).
22. 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 34, 1681-1689 (1994).
23. Wang, X., Lin, X., Loy, J.A., Tang, J. & Zhang, X.C. Crystal structure of the catalytic domain of human plasmin complexed with streptokinase. Science 281, 1662-1665 (1998).
24. Bode, W. et al. The refined 1.9 Å crystal structure of human α-thrombin: interaction with D-Phe-Pro-Arg chloromethylkelone and significance of the Tyr-Pro-Pro-Trp insertion segment. EMBO J. 8, 3467-3475 (1989).
25. Thomas, K.A., Smith, G.M., Thomas, T.B. & Feldmann, R.J. Electronic distributions within protein phenylalanine aromatic rings are reflected by the three-dimensional oxygen atom environments. Proc. Natl. Acad. Sci.USA 79, 4843-4847 (1982).
26. Burley, S.K. & Petsko, G.A. Amino-aromatic interactions in proteins. FEBS Lett. 203, 139-143 (1986).
27. Gillmor, S.A., Craik, C.S. & Fletterick, R.J. Structural determinants of specificity in the cysteine protease cruzain. Protein Sci. 6, 1603-1611 (1997).
28. Omar, M.N. & Mann, K.G. Inactivation of factor Va by plasmin. J. Biol. Chem. 262, 9750-9755 (1987).
29. McKee, P.A., Andersen, J.C. & Switzer, M.E. Molecular structural studies of human factor VIII. Ann. NY Acad. Sci. 240, 8-33 (1975).
30. Gundersen, D., Traan-Thang, C., Sordat, B., Mourali, F. & Reuegg, C. Plasmin-induced proteolysis of tenascin-C: modulation by T lymphocyte-derived urokinase-type plasminogen activator and effect on T lymphocyte adhesion, activation, and cell clustering. J.Immunol. 158, 1051-1060 (1997).
31. Campbell, P.G. & Andress, D.L. Plasmin degradation of insulin-like growth factor-binding protein-5 (IGFBP-5): regulation by IGFBP-5-(201-218). Am. J. Physiol. 273, E996-1004 (1997).
32. Tsirka, S.E., Bugge, T.H., Degen, J.L. & Strickland, S. Neuronal death in the central nervous system demonstrates a non-fibrin substrate for plasmin (published erratum appears in Proc Natl Acad Sci USA 26, 14976, 1997). Proc. Natl. Acad. Sci. USA 94, 9779-9781 (1997).
33. Pryzdial, E.L., Lavigne, N., Dupuis, N. & Kessler, G.E. Plasmin converts factor X from coagulation zymogen to fibrinolysis cofactor J. Biol. Chem. 274, 8500-8505 (1999).
34. Kuliopulos, A. et al. Plasmin desensitization of the PAR1 thrombin receptor: kinetics, sites of truncation, and implications for thrombolytic therapy. Biochemistry 38, 4572-4585 (1999).
35. Kost, C., Benner, K., Stockmann, A., Linder, D. & Preissner, K.T. Limited plasmin proteolysis of vitronectin. Characterization of the adhesion protein as morphoregulatory and angiostatin-binding factor. Eur. J. Biochem. 236, 682-688 (1996).
36. Chain, D., Kreizman, T., Shapira, H. & Shaltiel, S. Plasmin cleavage of vitronectin. Identification of the site and consequent attenuation in binding plasminogen activator inhibitor-1. FEBS Lett. 285, 251-256 (1991).
37. Novak, J.F., Hayes, J.D. & Nishimoto, S.K. Plasmin-mediated proteolysis of osteocalcin. J.Bone Mineral Res. 12, 1035-1042 (1997).
38. Pozsgay, M. et al. Study of the specificity of thrombin with tripeptidyl-p-nitroanilide substrates. Eur. J. Biochem. 115, 491-495 (1981).
39. Bode, W., Turk, D. & Karshikov, A. The refined 1.9-Å X-ray crystal structure of D-Phe-Pro-Arg chloromethylketone-inhibited human alpha-thrombin: structure analysis, overall structure, electrostatic properties, detailed active-site geometry, and structure-function relationships. Protein Sci. 1, 426-471 (1992).
40. Le Bonniec, B.F. et al. Characterization of the P2′ and P3′ specificities of thrombin using fluorescence-quenched substrates and mapping of the subsites by mutagenesis. Biochemistry 35, 7114-7122 (1996).
41. Vindigni, A., Dang, Q.D. & Di Cera, E. Site-specific dissection of substrate recognition by thrombin. Nat. Biotechnol. 15, 891-895 (1997).
42. Lottenberg, R., Hall, J.A., Blinder, M., Binder, E.P. & Jackson, C.M. The action of thrombin on peptide p-nitroanilide substrates. Substrate selectivity and examination of hydrolysis under different reaction conditions. Biochim. Biophys. Acta 742, 539-557 (1983).
43. Kawabata, S. et al. Highly sensitive peptide-4-methylcoumaryl-7-amide substrates for blood-clotting proteases and trypsin. Eur. J. Biochem. 172, 17-25 (1988).
44. Mathews, I.I. et al. Crystallographic structures of thrombin complexed with thrombin receptor peptides: existence of expected and novel binding modes. Biochemistry 33, 3266-3279 (1994).
45. Vu, T.K.. Wheaton, V.I., Hung, D.T., Charo, I. & Coughlin, S.R. Domains specifying thrombin-receptor interaction. Nature 353, 674-677 (1991).
46. Pittman, D.D., Tomkinson, K.N., Michnick, D., Selighsohn, U. & Kaufman, R.J. Posttranslational sulfation of factor V is required for efficient thrombin cleavage and activation and for full procoagulant activity. Biochemistry 33, 6952-6959 (1994).
47. Keller, F.G., Ortel, T.L., Quinn-Allen, M.A. & Kane, W.H. Thrombin-catalyzed activation of recombinant human factor V. Biochemistry 34, 4118-4124 (1995).
48. Stubbs, M.T. & Bode, W. A model for the specificity of fibrinogen cleavage by thrombin. Semin. Thrombosis Hemostasis 19, 344-351 (1993).
49. Ehrlich, H.J. et al. Recombinant human protein C derivatives: altered response to calcium resulting in enhanced activation by thrombin. EMBO J. 9, 2367-2373 (1990).
50. Bunin, B.A. The combinatorial index. xvii, 322 (Academic, San Diego; 1998).
51. Still, W.C., Kahn, M. & Mitra, A. Rapid chromatographic technique for preparative separations with moderate resolution. J. Org. Chem. 43, 2923-2925 (1978).
52. Robbins, K.C., Summaria, L. & Wohl, R.C. Human plasmin. Methods Enzymol. C 80, 379-387 (1981).
53. Fenton, J.W.d., Fasco, M.J. & Stackrow, A.B. Human thrombins. Production, evaluation, and properties of alpha-thrombin. J. Biol. Chem. 252, 3587-3598 (1977).
54. Jameson, G., Roberts, D.V., Adams, R.W., Kyle, W.S., & Elmore, D.T. Determination of the operational molarity of solutions of bovine alpha-chymotrypsin, trypsin, thrombin and factor Xa by spectrofluorimetric titration. Biochem. J. 131, 107-117 (1973).
55. Zimmerman, M., Ashe, B., Yurewicz, E. & Patel, G. Sensitive assay for trypsin, elastase, and chymotrypsin using fluorogenic substrates. Anal. Biochem. 78, 47-51 (1977).
56. Bernstein, F.C. et al. The Protein Data Bank: a computer-based archival file for macromolecular structures. J. Mol. Biol. 112, 535 (1977).