Selectivity of propeptide-enzyme interaction in cathepsin L-like cysteine proteases

Biological Chemistry

Volumn 390, Issue 2, 2009, Pages 167-174

  Schilling, Klaus ^a   Körner, Alexandra ^a   Sehmisch, Saskia ^a   Kreusch, Annett ^a   Kleint, Ramona ^a   Benedix, Yvonne ^a   Schlabrakowski, Anne ^a,b   Wiederanders, Bernd ^a  

^a JENA UNIVERSITY HOSPITAL   (Germany)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Cathepsin L like endopeptidases; Inhibition; Intramolecular chaperone; Proregion; Refolding

Indexed keywords

CATHEPSIN K; CATHEPSIN L; CATHEPSIN S; CYSTEINE PROTEINASE; PROTEINASE;

ARTICLE; CROSS REACTION; ENZYME ACTIVITY; LATENT PERIOD; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; TAXONOMY; X RAY ANALYSIS;

ANIMALS; CATHEPSINS; CYSTEINE ENDOPEPTIDASES; ENZYME PRECURSORS; ESCHERICHIA COLI; HYDROGEN-ION CONCENTRATION; KINETICS; MODELS, MOLECULAR; PROTEIN FOLDING; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY; SUBSTRATE SPECIFICITY;

EID: 59949084805     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/BC.2009.023     Document Type: Article

References (40)

1. Billington, C.J., Mason, P., Magny, M.C., and Mort, J.S. (2000). The slow-binding inhibition of cathepsin K by its propeptide. Biochem. Biophys. Res. Commun. 276, 924-929.
2. Brinkworth, R.I., Tort, J.F., Brindley, P.J., and Dalton, J.P. (2000). Phylogenetic relationships and theoretical model of human cathepsin W (lymphopain), a cysteine proteinase from cytotoxic T lymphocytes. Int. J. Biochem. Cell Biol. 32, 373-384.
3. Buevich, A.V., Shinde, U.P., Inouye, M., and Baum, J. (2001). Backbone dynamics of the natively unfolded pro-peptide of subtilisin by heteronuclear NMR relaxation studies. J. Biomol. NMR 20, 233-249.
4. Carmona, E., Dufour, E., Plouffe, C., Takebe, S., Mason, P., Mort, J.S., and Menard, R. (1996). Potency and selectivity of the cathepsin L propeptide as an inhibitor of cysteine proteases. Biochemistry 35, 8149-8157.
5. Coulombe, R., Grochulski, P., Sivaraman, J., Menard, R., Mort, J.S., and Cygler, M. (1996). Structure of human procathepsin L reveals the molecular basis of inhibition by the prosegment. EMBO J. 15, 5492-5503.
6. Fonovic, M., Brömme, D., Turk, V., and Turk, B. (2004). Human cathepsin F: expression in baculovirus system, characterization and inhibition by protein inhibitors. Biol. Chem. 385, 505-509.
7. Fu, X., Inouye, M., and Shinde, U. (2000). Folding pathway mediated by an intramolecular chaperone. The inhibitory and chaperone functions of the subtilisin propeptide are not obligatorily linked. J. Biol. Chem. 275, 16871-16878.
8. Guay, J., Falgueyret, J.P., Ducret, A., Percival, M.D., and Mancini, J.A. (2000). Potency and selectivity of inhibition of cathepsin K, L and S by their respective propeptides. Eur. J. Biochem. 267, 6311-6318.
9. Hou, W.S., Bromme, D., Zhao, Y., Mehler, E., Dushey, C., Weinstein, H., Miranda, C.S., Fraga, C., Greig, F., Carey, J., et al. (1999). Characterization of novel cathepsin K mutations in the pro and mature polypeptide regions causing pycnodysostosis. J. Clin. Invest. 103, 731-738.
10. Jaswal, S.S., Sohl, J.L., Davis, J.H., and Agard, D.A. (2002). Energetic landscape of alpha-lytic protease optimizes longevity through kinetic stability. Nature 415, 343-346.
11. Jaswal, S.S., Truhlar, S.M.E., Dill, K.A., and Agard, D.A. (2005). Comprehensive analysis of protein folding activation thermodynamics reveals a universal behavior violated by kinetically stable proteases. J. Mol. Biol. 347, 355-366.
12. Jerala, R., Zerovnik, E., Kidric, J., and Turk, V. (1998). pH-induced conformational transitions of the propeptide of human cathepsin L - a role for a molten globule state in zymogen activation. J. Biol. Chem. 273, 11498-11504.
13. Karrer, K.M., Peiffer, S.L., and DiTomas, M.E. (1993). Two distinct gene subfamilies within the family of cysteine protease genes. Proc. Natl. Acad. Sci. USA 90, 3063-3067.
14. Kaulmann, G., Palm, G.J., Schilling, K., Hilgenfeld, R., and Wiederanders, B. (2003). An unfolding/refolding step helps in the crystallization of a poorly soluble protein. Acta Cryst. D Biol. Cryst. 59, 1243-1245.
15. Kaulmann, G., Palm, G.J., Schilling, K., Hilgenfeld, R., and Wiederanders, B. (2006). The crystal structure of a Cys25→Ala mutant of human procathepsin S elucidates enzyme-prosequence interactions. Protein Sci. 15, 2619-2629.
16. Kirschke, H. and Wiederanders, B. (1994). Cathepsin S and related lysosomal endopeptidases. Methods Enzymol. 244, 500-511.
17. Kojima, S., Yanai, H., and Miura, K.-i. (2001). Accelerated refolding of subtilisin BPN9 by tertiary-structure-forming mutants of its propeptide. J. Biochem. 130, 471-474.
18. Kramer, G., Paul, A., Kreusch, A., Schüler, S., Wiederanders, B., and Schilling, K. (2007). Optimized folding and activation of recombinant procathepsin L and S produced in Escherichia coli. Protein Exp. Purif. 54, 147-156.
19. LaLonde, J.M., Zhao, B., Janson, C.A., D'Alessio, K.J., Mc-Queney, M.S., Orsini, M.J., Debouck, C.M., and Smith, W.W. (1999). The crystal structure of human procathepsin K. Biochemistry 38, 862-869.
20. Linnevers, C.J., McGrath, M.E., Armstrong, R., Mistry, F.R., Barnes, M.G., Klaus, J.L., Palmer, J.T., Katz, B.A., and Bromme, D. (1997). Expression of human cathepsin K in Pichia pastoris and preliminary crystallographic studies of an inhibitor complex. Protein Sci. 6, 919-921.
21. Marie-Claire, C., Yabuta, Y., Suefuji, K., Matsuzawa, H., and Shinde, U. (2001). Folding pathway mediated by an intramolecular chaperone: the structural and functional characterization of the aqualysin. J. Mol. Biol. 305, 151-165.
22. Maubach, G., Schilling, K., Rommerskirch, W., Wenz, I., Schultz, J.E., Weber, E., and Wiederanders, B. (1997). The inhibition of cathepsin S by its propeptide - specificity and mechanism of action. Eur. J. Biochem. 250, 745-750.
23. Morrison, J. and Welsch, C. (1988). The behaviour and significance of slow-binding enzyme inhibitors. In: Adv. Enzymol. vol. 61, A. Meister, ed. (New York, USA: John Wiley & Sons), pp. 201-301.
24. Pietschmann, S., Fehn, M., Kaulmann, G., Wenz, I., Wiederanders, B., and Schilling, K. (2002). Foldase function of the cathepsin S proregion is strictly based upon its domain structure. Biol. Chem. 383, 1453-1458.
25. Rasch, D. (1996). Software for selection procedures. 40 years of statistical selection theory, Part II. J. Statist. Planning Inference 54, 345-358.
26. Rasch, D., Verdooren, L.R., and Gowers, J.I. (1999). Fundamentals in the Design and Analysis of Experiments (München-Wien-Oldenburg: Oldenburg Wissenschaftsverlag GmbH).
27. Schilling, K., Pietschmann, S., Fehn, M., Wenz, I., and Wiederanders, B. (2001). Folding incompetence of cathepsin L-like cysteine proteases may be compensated by the highly conserved, domain-building N-terminal extension of the proregion. Biol. Chem. 382, 859-865.
28. Schittkowski, K. (2001). Parameter Estimation in Dynamical Systems with EASY-Fit. Program for Parameter Estimation in Dynamical Systems (Bayreuth, Germany).
29. Sivaraman, J., Lalumiere, M., Menard, R., and Cygler, M. (1999). Crystal structure of wild-type human procathepsin K. Protein Sci. 8, 283-290.
30. Smith, S.M. and Gottesman, M.M. (1989). Activity and deletion analysis of recombinant human cathepsin L expressed in Escherichia coli. J. Biol. Chem. 264, 20487-20495.
31. Subbian, E., Yabuta, Y., and Shinde, U. (2004). Positive selection dictates the choice between kinetic and thermodynamic protein folding and stability in subtilases. Biochemistry 43, 14348-14360.
32. Subbian, E., Yabuta, Y., and Shinde, U.P. (2005). Folding pathway mediated by an intramolecular chaperone: intrinsically unstructured propeptide modulates stochastic activation of subtilisin. J. Mol. Biol. 347, 367-383.
33. Tao, K., Stearns, N.A., Dong, J., Wu, Q.L., and Sahagian, G.G. (1994). The proregion of cathepsin L is required for proper folding, stability, and ER exit. Arch. Biochem. Biophys. 311, 19-27.
34. Tobbell, D.A., Middleton, B.J., Raines, S., Needham, M.R., Taylor, I.W., Beveridge, J.Y., and Abbott, W.M. (2002). Identification of in vitro folding conditions for procathepsin S and cathepsin S using fractional factorial screens. Protein Exp. Purif. 24, 242-254.
35. Truhlar, S.M.E. and Agard, D.A. (2005). The folding landscape of an a-lytic protease variant reveals the role of a conserved b-hairpin in the development of kinetic stability. Proteins 61, 105-114.
36. Wang, B., Shi, G.P., Yao, P.M., Li, Z., Chapman, H.A., and Bromme, D. (1998). Human cathepsin F. Molecular cloning, functional expression, tissue localization, and enzymatic characterization. J. Biol. Chem. 273, 32000-32008.
37. Wiederanders, B., Kaulmann, G., and Schilling, K. (2003). Functions of propeptide parts in cysteine proteases. Curr. Protein Pept. Sci. 4, 309-326.
38. Willis, M.S., Hogan, J.K., Prabhakar, P., Liu, X., Tsai, K., Wei, Y., and Fox, T. (2005). Investigation of protein refolding using a fractional factorial screen: a study of reagent effects and interactions. Protein Sci. 14, 1818-1826.
39. Yabuta, Y., Subbian, E., Oiry, C., and Shinde, U. (2003). Folding pathway mediated by an intramolecular chaperone. A functional peptide chaperone designed using sequence databases. J. Biol. Chem. 278, 15246-15251.
40. Yamamoto, Y., Watabe, S., Kageyama, T., and Takahashi, S.Y. (1999). Proregion of Bombyx mori cysteine proteinase functions as an intramolecular chaperone to promote proper folding of the mature enzyme. Arch. Insect Biochem. Physiol. 42, 167-178.