A double-headed cathepsin B inhibitor devoid of warhead

Protein Science

Volumn 17, Issue 12, 2008, Pages 2145-2155

  Schenker, Patricia ^a   Alfarano, Pietro ^a   Kolb, Peter ^a   Caflisch, Amedeo ^a   Baici, Antonio ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Cysteine peptidases; Docking; Endopeptidase; Enzyme kinetics; Exopeptidase; Inhibition; Occluding loop

Indexed keywords

CATHEPSIN B; CATHEPSIN B INHIBITOR; EXOPEPTIDASE;

ARTICLE; CHEMICAL STRUCTURE; ENZYME ACTIVITY; HYDROGEN BOND; KINETICS; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN DEGRADATION;

AMINO ACID SEQUENCE; BINDING, COMPETITIVE; CATHEPSIN B; COMPUTER SIMULATION; KINETICS; MOLECULAR SEQUENCE DATA; PEPTIDE LIBRARY; PROTEASE INHIBITORS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; THIAZOLIDINES;

EID: 56749161390     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1110/ps.037341.108     Document Type: Article

References (63)

1. Aronson Jr., N.N. and Barrett, A.J. 1978. The specificity of cathepsin B. Hydrolysis of glucagon at the C-terminus by a peptidyldipeptidase mechanism. Biochem. J. 171: 759-765.
2. Baici, A. 1981. The specific velocity plot. A graphical method for determining inhibition parameters for both linear and hyperbolic enzyme inhibitors. Eur. J. Biochem. 119: 9-14.
3. Baici, A. 1998. Inhibition of extracellular matrix-degrading endopeptidases: Problems, comments, and hypotheses. Biol. Chem. 379: 1007-1018.
4. Baici, A., Hörler, D., Lang, A., Merlin, C., and Kissling, R. 1995a. Cathepsin B in osteoarthritis: Zonal variation of enzyme activity in human femoral head cartilage. Ann. Rheum. Dis. 54: 281-288.
5. Baici, A., Lang, A., Hörler, D., Kissling, R., and Merlin, C. 1995b. Cathepsin B in osteoarthritis: Cytochemical and histochemical analysis of human femoral head cartilage. Ann. Rheum. Dis. 54: 289-297.
6. Baici, A., Szedlacsek, S.E., Früh, H., and Michel, B.A. 1996. pH-Dependent hysteretic behaviour of human myeloblastin (leucocyte proteinase 3). Biochem. J. 317: 901-905.
7. Baici, A., Müntener, K., Willimann, A., and Zwicky, R. 2006. Regulation of human cathepsin B by alternative mRNA splicing: Homeostasis, fatal errors and cell death. Biol. Chem. 387: 1017-1021.
8. Barrett, A.J. 1980. Fluorimetric assays for cathepsin B and cathepsin H with methylcoumarylamide substrates. Biochem. J. 187: 909-912.
9. Bond, J.S. and Barrett, A.J. 1980. Degradation of fructose-1,6- bisphosphate aldolase by cathepsin B. A further example of peptidyldipeptidase activity of this proteinase. Biochem. J. 189: 17-25.
10. Bröker, L.E., Kruyt, F.A.E., and Giaccone, G. 2005. Cell death independent of caspases: A review. Clin. Cancer Res. 11: 3155-3162.
11. Brooks, B.R., Bruccoleri, R.E., Olafson, B.D., States, D.J., Swaminathan, S., and Karplus, M. 1983. CHARMM: A program for macromolecular energy, minimization, and dynamics calculations. J. Comput. Chem. 4: 187-217.
12. Budin, N., Majeux, N., and Caflisch, A. 2001. Fragment-based flexible ligand docking by evolutionary optimization. Biol. Chem. 382: 1365-1372.
13. Buxser, S. and Vroegop, S. 2005. Calculating the probability of detection for inhibitors in enzymatic or binding reactions in high-throughput screening. Anal. Biochem. 340: 1-13.
14. Cathers, B.E., Barrett, C., Palmer, J.T., and Rydzewski, R.M. 2002. pH Dependence of inhibitors targeting the occluding loop of cathepsin B. Bioorg. Chem. 30: 264-275.
15. Cecchini, M., Kolb, P., Majeux, N., and Caflisch, A. 2004. Automated docking of highly flexible ligands by genetic algorithms: A critical assessment. J. Comput. Chem. 25: 412-422.
16. Cech, P. and Lehrer, R.I. 1984. Phagolysosomal pH of human neutrophils. Blood 63: 88-95.
17. Cotrin, S.S., Puzer, L., Judice, W.A.D., Juliano, L., Carmona, A.K., and Juliano, M.A. 2004. Positional-scanning combinatorial libraries of fluorescence resonance energy transfer peptides to define substrate specificity of carboxydipeptidases: Assays with human cathepsin B. Anal. Biochem. 335: 244-252.
18. Friedrichs, B., Tepel, C., Reinheckel, T., Deussing, J., von Figura, K., Herzog, V., Peters, C., Saftig, P., and Brix, K. 2003. Thyroid functions of mouse cathepsins B, K, and L. J. Clin. Invest. 111: 1733-1745.
19. Frlan, R. and Gobec, S. 2006. Inhibitors of cathepsin B. Curr. Med. Chem. 13: 2309-2327.
20. Gu, F. and Gruenberg, J. 2000. ARF1 regulates pH-dependent COP functions in the early endocytic pathway. J. Biol. Chem. 275: 8154-8160.
21. Hanada, K., Tamai, M., Yamagishi, M., Ohmura, S., Sawada, J., and Tanaka, I. 1978. Isolation and characterization of E-64, a new thiol protease inhibitor. Agric. Biol. Chem. 42: 523-528.
22. Huang, D.Z., Lüthi, U., Kolb, P., Edler, K., Cecchini, M., Audetat, S., Barberis, A., and Caflisch, A. 2005. Discovery of cell-permeable nonpeptide inhibitors of β-secretase by high-throughput docking and continuum electrostatics calculations. J. Med. Chem. 48: 5108-5111.
23. Huang, D.Z., Lüthi, U., Kolb, P., Cecchini, M., Barberis, A., and Caflisch, A. 2006. In silico discovery of β-secretase inhibitors. J. Am. Chem. Soc. 128: 5436-5443.
24. Illy, C., Quraishi, O., Wang, J., Purisima, E., Vernet, T., and Mort, J.S. 1997. Role of the occluding loop in cathepsin B activity. J. Biol. Chem. 272: 1197-1202.
25. Im, W., Beglov, D., and Roux, B. 1998. Continuum solvation model: Computation of electrostatic forces from numerical solutions to the Poisson-Boltzmann equation. Comput. Phys. Commun. 111: 59-75.
26. Irwin, J.J. and Shoichet, B.K. 2005. ZINC - a free database of commercially available compounds for virtual screening. J. Chem. Inf. Model. 45: 177-182.
27. Kolb, P. and Caflisch, A. 2006. Automatic and efficient decomposition of two-dimensional structures of small molecules for fragment-based high-throughput docking. J. Med. Chem. 49: 7384-7392.
28. Kolb, P., Huang, D., Dey, F., and Caflisch, A. 2008. Discovery of kinase inhibitors by high-throughput docking and scoring based on a transferable linear interaction energy model. J. Med. Chem. 51: 1179-1188.
29. Krupa, J.C., Hasnain, S., Nägler, D.K., Menard, R., and Mort, J.S. 2002. S2′ substrate specificity and the role of His110 and His111 in the exopeptidase activity of human cathepsin B. Biochem. J. 361: 613-619.
30. Kuhelj, R., Dolinar, M., Pungercar, J., and Turk, V. 1995. The preparation of catalytically active human cathepsin B from its precursor expressed in Escherichia coli in the form of inclusion bodies. Eur. J. Biochem. 229: 533-539.
31. Kukor, Z., Mayerle, J., Krüger, B., Tóth, M., Steed, P.M., Halangk, W., Lerch, M.M., and Sahin-Tóth, M. 2002. Presence of cathepsin B in the human pancreatic secretory pathway and its role in trypsinogen activation during hereditary pancreatitis. J. Biol. Chem. 277: 21389-21396.
32. Lenarcic, B., Gabrijelcic, D., Rozman, B., Drobnic-Kosorok, M., and Turk, V. 1988. Human cathepsin B and cysteine proteinase inhibitors (CPIs) in inflammatory and metabolic joint diseases. Biol. Chem. Hoppe Seyler 369: 257-261.
33. Majeux, N., Scarsi, M., Apostolakis, J., Ehrhardt, C., and Caflisch, A. 1999. Exhaustive docking of molecular fragments with electrostatic solvation. Proteins 37: 88-105.
34. Matsumoto, K., Mizoue, K., Kitamura, K., Tse, W.C., Huber, C.P., and Ishida, T. 1999. Structural basis of inhibition of cysteine proteases by E-64 and its derivatives. Biopolymers 51: 99-107.
35. Matsunaga, Y., Saibara, T., Kido, H., and Katunuma, N. 1993. Participation of cathepsin B in processing of antigen presentation to MHC class II. FEBS Lett. 324: 325-330.
36. McKay, M.J., Offermann, M.K., Barrett, A.J., and Bond, J.S. 1983. Action of human liver cathepsin B on the oxidized insulin B chain. Biochem. J. 213: 467-471.
37. Michaud, S. and Gour, B.J. 1998. Cathepsin B inhibitors as potential anti-metastatic agents. Expert Opin. Ther. Pat. 8: 645-672.
38. Mohamed, M.M. and Sloane, B.F. 2006. Cysteine cathepsins: Multifunctional enzymes in cancer. Nat. Rev. Cancer 6: 764-775.
39. Momany, F.A. and Rone, R. 1992. Validation of the general purpose QUANTA®3.2/CHARMm® force field. J. Comput. Chem. 13: 888-900.
40. Mort, J.S. 2004. Cathepsin B. In Handbook of proteolytic enzymes, 2nd ed. (eds. A.J. Barrett and N.D. Rawlings, J.F.Woessner, Jr.), pp. 1079-1086. Elsevier, London, UK.
41. Mort, J.S., Magny, M.C., and Lee, E.R. 1998. Cathepsin B: An alternative protease for the generation of an aggrecan "metalloproteinase" cleavage neoepitope. Biochem. J. 335: 491-494.
42. Müntener, K., Zwicky, R., Csucs, G., and Baici, A. 2003. The alternative use of exons 2 and 3 in cathepsin B mRNA controls enzyme trafficking and triggers nuclear fragmentation in human cells. Histochem. Cell Biol. 119: 93-101.
43. Müntener, K., Zwicky, R., Csucs, G., Rohrer, J., and Baici, A. 2004. Exon skipping of cathepsin B: Mitochondrial targeting of a lysosomal peptidase provokes cell death. J. Biol. Chem. 279: 41012-41017.
44. Murata, M., Miyashita, S., Yokoo, C., Tamai, M., Hanada, K., Hatayama, K., Towatari, T., Nikawa, T., and Katunuma, N. 1991. Novel epoxysuccinyl peptides. Selective inhibitors of cathepsin B, in vitro. FEBS Lett. 280: 307-310.
45. Musil, D., Zucic, D., Turk, D., Engh, R.A., Mayr, I., Huber, R., Popovic, T., Turk, V., Towatari, T., Katunuma, N., et al. 1991. The refined 2.15 Å X-ray crystal structure of human liver cathepsin B: The structural basis for its specificity. EMBO J. 10: 2321-2330.
46. Nägler, D.K., Storer, A.C., Portaro, F.C.V., Carmona, E., Juliano, L., and Menard, R. 1997. Major increase in endopeptidase activity of human cathepsin B upon removal of occluding loop contacts. Biochemistry 36: 12608-12615.
47. Nycander, M., Estrada, S., Mort, J.S., Abrahamson, M., and Björk, I. 1998. Two-step mechanism of inhibition of cathepsin B by cystatin C due to displacement of the proteinase occluding loop. FEBS Lett. 422: 61-64.
48. Okamura-Oho, Y., Zhang, S.Q., Callahan, J.W., Murata, M., Oshima, A., and Suzuki, Y. 1997. Maturation and degradation of β-galactosidase in the post-Golgi compartment are regulated by cathepsin B and a non-cysteine protease. FEBS Lett. 419: 231-234.
49. Otto, H.H. and Schirmeister, T. 1997. Cysteine proteases and their inhibitors. Chem. Rev. 97: 133-171.
50. Palmier, M.O. and Van Doren, S.R. 2007. Rapid determination of enzyme kinetics from fluorescence: Overcoming the inner filter effect. Anal. Biochem. 371: 43-51.
51. Pavlova, A., Krupa, J.C., Mort, J.S., Abrahamson, M., and Björk, I. 2000. Cystatin inhibition of cathepsin B requires dislocation of the proteinase occluding loop. Demonstration by release of loop anchoring through mutation of His110. FEBS Lett. 487: 156-160.
52. Quraishi, O., Nägler, D.K., Fox, T., Sivaraman, J., Cygler, M., Mort, J.S., and Storer, A.C. 1999. The occluding loop in cathepsin B defines the pH dependence of inhibition by its propeptide. Biochemistry 38: 5017-5023.
53. Rawlings, N.D., Tolle, D.P., and Barrett, A.J. 2004. MEROPS: The peptidase database (http://merops.sanger.ac.uk). Nucleic Acids Res. 32: D160-D164.
54. Rofstad, E.K., Mathiesen, B., Kindem, K., and Galappathi, K. 2006. Acidic extracellular pH promotes experimental metastasis of human melanoma cells in athymic nude mice. Cancer Res. 66: 6699-6707.
55. Rowan, A.D., Feng, R., Konishi, Y., and Mort, J.S. 1993. Demonstration by electrospray mass spectrometry that the peptidylpeptidase activity of cathepsin B is capable of rat cathepsin B C-terminal processing. Biochem. J. 294: 923-927.
56. Schechter, I. and Berger, A. 1967. On the size of the active sites in proteases. I. Papain. Biochem. Biophys. Res. Commun. 27: 157-162.
57. Schwabe, C. 1975. A fluorescence assay for proteolytic enzymes. Anal. Biochem. 53: 484-490.
58. Selwyn, M.J. 1965. A simple test for inactivation of an enzyme during assay. Biochim. Biophys. Acta 105: 193-195.
59. Shoichet, B.K. 2006. Screening in a spirit haunted world. Drug Discov. Today 11: 607-615.
60. Takahashi, T., Dehdarani, A.H., Yonezawa, S., and Tang, J. 1986. Porcine spleen cathepsin B is an exopeptidase. J. Biol. Chem. 261: 9375-9381.
61. Turk, D., Podobnik, M., Kuhelj, R., Dolinar, M., and Turk, V. 1996. Crystal structures of human procathepsin B at 3.2 and 3.3 Å resolution reveal an interaction motif between a papain-like cysteine protease and its propeptide. FEBS Lett. 384: 211-214.
62. Yan, S.Q. and Sloane, B.F. 2003. Molecular regulation of human cathepsin B: Implication in pathologies. Biol. Chem. 384: 845-854.
63. Zwicky, R., Müntener, K., Csucs, G., Goldring, M.B., and Baici, A. 2003. Exploring the role of 5′-alternative splicing and of the 3′-untranslated region of cathepsin B mRNA. Biol. Chem. 384: 1007-1018.