Structural basis for specificity of papain-like cysteine protease proregions toward their cognate enzymes

Proteins: Structure, Function and Genetics

Volumn 32, Issue 4, 1998, Pages 504-514

  Groves, Matthew R ^a   Coulombe, René ^b   Jenkins, John ^c   Cygler, Miroslaw ^b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^c INSTITUTE OF FOOD RESEARCH   (United Kingdom)

Author keywords

Caricain; Cathepsin L; Cysteine protease; Inhibition; Zymogens

Indexed keywords

CATHEPSIN L; CYSTEINE PROTEINASE; ENZYME PRECURSOR;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; ENZYME INHIBITION; ENZYME SPECIFICITY; ENZYME STRUCTURE; PRIORITY JOURNAL; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; BINDING SITES; CATHEPSINS; CYSTEINE ENDOPEPTIDASES; ENZYME PRECURSORS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PAPAIN; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 0031826072     PISSN: 08873585     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0134(19980901)32:4<504::AID-PROT8>3.0.CO;2-F     Document Type: Article

References (37)

1. Yagel, S., Warner, A.H., Nellans, H.N., Lala, P.K., Waghorne, C., Denhardt, D.T. Suppression by cathepsin L inhibitors of the invasion of amnion membranes by murine cancer cells. Cancer Res. 49:3553-3557, 1989.
2. Sloane, B.F., Honn, K.V. Cysteine proteinases and metastasis. Cancer Metastasis Rev. 3:249-263, 1984.
3. Esser, R.E., Angelo, R.A., Murphey, M.D., et al. Cysteine proteinase inhibitors decrease articular cartilage and bone destruction in chronic inflammatory arthritis. Arthritis Rheum. 37:236-247, 1994.
4. Esser, R.E., Watts, L.M., Angelo, R.A., Thornburg, L.P., Prior, J.J., Palmer, J.T. The effects of fluoromethyl ketone inhibitors of cathepsin B on adjuvant induced arthritis. J. Rheumatol. 20:1176-1183, 1993.
5. Cataldo, A.M., Paskevich, P.A., Kominami, E., Nixon, R.A. Lysosomal hydrolases of different classes are abnormally distributed in brains of patients with Alzheimer disease. Proc. Natl. Acad. Sci. USA 88:10998-11002, 1991 [erratum in 89:2509, 1992].
6. Vaes, G., Delaisse, J.M., Eeckhout, Y. Relative roles of collagenase and lysosomal cysteine-proteinases in bone resorption. Matrix Suppl. 1:383-388, 1992.
7. Kalsheker, N.A., Deam, S., Chambers, L., Sreedharan, S., Brocklehurst, K., Lomas, D.A. The house dust mite allergen Der p1 catalytically inactivates alpha 1-antitrypsin by specific reactive centre loop cleavage: A mechanism that promotes airway inflammation and asthma. Biochem. Biophys. Res. Commun. 221:59-61, 1996.
8. Bond, J.S., Butler, P.E. Intracellular proteases. Annu. Rev. Biochem. 56:333-364, 1987.
9. Votta, B.J., Levy, M.A., Badger, A., Bradbeer, G., Dodds, R.A., James, I.E., Thompson, S., Bossard, M.Y., Carr, T., Connor, J.R., Tomaszek, T.A., Szewczuk, L., Drake, F.H., Weber, D.F., Gowen, M. Peptide aldehyde inhibitors of cathepsin K inhibit bone resorption both in vitro and in vivo. J Bone Miner. Res. 12:1396-1406, 1997.
10. Azaryan, A.V., Hook, V.Y. Distinct properties of prohormone thiol protease (PTP) compared to cathepsins B, L, and H: Evidence for PTP as a novel cysteine protease. Arch. Biochem. Biophys. 314:171-177, 1994.
11. Drenth, J., Jansonius, J.N., Koekoek, R., Swen, H.M., Wolthers, B.G. Structure of papain. Nature 218:929-932, 1968.
12. Demuth, H.U. Recent developments in inhibiting cysteine and serine proteases. J. Enzym. Inhib. 3:249-278, 1990.
13. Otto, H.H., Schirmeister, T. Cysteine proteases and their inhibitors. Chem. Rev. 97:133-171, 1997.
14. Fox, T., de Miguel, E., Mort, J.S., Storer, A.C. Potent slow-binding inhibition of cathepsin B by its propeptide. Biochemistry 31:12571-12576, 1992.
15. Taylor, M.A.J., Baker, K.C., Briggs, G.S., et al. Recombinant pro-regions from papain and papaya proteinase IV-are selective high affinity inhibitors of the mature papaya enzymes. Protein Eng. 8:59-62, 1995.
16. Carmona, E., Dufour, E., Plouffe, C., et al. Potency and selectivity of the cathepsin L propeptide as an inhibitor of cysteine proteases. Biochemistry 35:8149-8157, 1996.
17. Taylor, M.A., Lee, M.J. Trypsin isolated from the midgut of the tobacco hornworm, Manduca sexta, is inhibited by synthetic pro-peptides in vitro. Biochem. Biophys. Res. Commun. 235:606-609, 1997.
18. Karrer, K.M., Peiffer, S.L., DiTomas, M.E. Two distinct gene subfamilies within the family of cysteine protease genes. Proc. Natl. Acad. Sci. USA 90:3063-3067, 1993.
19. Cygler, M., Sivaraman, J., Grochulski, P., Coulombe, R., Storer, A.C., Mort, J.S. Structure of rat procathepsin B: model for inhibition of cysteine protease activity by the proregion. Structure 4:405-416, 1996.
20. Turk, D., Podobnik, M., Kuhelj, R., Dolinar, M., Turk, V. Crystal structures of human procathepsin B at 3.2 and 3.3 Angstroms resolution reveal an interaction motif between a papain-like cysteine protease and its propeptide. FEBS Lett. 384:211-214, 1996.
21. Podobnik, M., Kuhelj, R., Turk, V., Turk, D. Crystal structure of the wild-type human procathepsin B at 2.5 A resolution reveals the native active site of a papain-like cysteine protease zymogen. J. Mol. Biol. 271:774-788, 1997.
22. Groves, M.R., Taylor, M.A.J., Scott, M., Cummings, N.J., Pickersgill, R.W., Jenkins, J.A. The prosequence of procaricain forms an alpha-helical domain that prevents access to the substrate-binding cleft. Structure 4:1193-1203, 1996.
23. Coulombe, R., Grochulski, P., Sivaraman, J., Menard, R., Mort, J.S., Cygler, M. Structure of human procathepsin L reveals the molecular basis of inhibition by the prosegment. EMBO J. 15:5492-5503, 1996.
24. Bryan, P., Wang, L., Hoskins, J., et al. Catalysis of a protein folding reaction: mechanistic implications of the 2.0 A structure of the subtilisin-prodomain complex. Biochemistry 34:10310-10318, 1995.
25. Baker, D., Sohl, J.L., Agard, D.A. A protein-folding reaction under kinetic control. Nature 356:263-265, 1992.
26. Phillips, M.A., Rutter, W.J. Role of the prodomain in folding and secretion of rat pancreatic carboxypeptidase A1. Biochemistry 35:6771-6776, 1996.
27. Ramos, C., Winther, J.R., Kielland-Brandt, M.C. Requirement of the propeptide for in vivo formation of active yeast carboxypeptidase Y. J. Biol. Chem. 269:7006-7012, 1994.
28. Tao, K., Stearns, N.A., Dong, J., Wu, Q.L., Sahagian, G.G. The proregion of cathepsin L is required for proper folding, stability, and ER exit. Arch. Biochem. Biophys. 311:19-27, 1994.
29. Mach, L., Mort, J.S., Glossl, J. Noncovalent complexes between the lysosomal proteinase cathepsin B and its propeptide account for stable, extracellular, high molecular mass forms of the enzyme. J. Biol. Chem. 269:13036-13040, 1994.
30. McIntyre, G.F., Erickson, A.H. The lysosomal proenzyme receptor that binds procathepsin L to microsomal membranes at pH 5 is a 43-kDa integral membrane protein. Proc. Natl. Acad. Sci. USA 90:10588-10592, 1993.
31. McIntyre, G.F., Godbold, G.D., Erickson, A.H. The pH-dependent membrane association of procathepsin L is mediated by a 9-residue sequence within the propeptide. J. Biol. Chem. 269:567-572, 1994.
32. Musil, D., Zucic, D., Turk, D., et al. The refined 2.15 A X-ray crystal structure of human liver cathepsin B: the structural basis for its specificity. EMBO J. 10:2321-2330, 1991.
33. Turk, D., Podobnik, M., Popovic, T., et al. Crystal structure of cathepsin B inhibited with CA030 at 2.0-A resolution: A basis for the design of specific epoxysuccinyl inhibitors. Biochemistry 34:4791-4797, 1995.
34. Illy, C., Quraishi, O., Wang, J., Purisima, E., Vernet, T., Mort, J.S. Role of the occluding loop in cathepsin B activity. J. Biol. Chem. 272:1197-1202, 1997.
35. Vernet, T., Tessier, D.C., Chatellier, J., et al. Structural and functional roles of asparagine 175 in the cysteine protease papain. J. Biol. Chem. 270:16645-16652, 1995.
36. Pickersgill, R.W., Rizkallah, P., Harris, G.W., Goodenough, P.W. Determination of the structure of papaya protease omega. Acta Crystallogr. B. 47:766-771, 1991.
37. Chen, Y., Plouffe, C., Menard, R., Storer, A.C. Delineating functionally important regions and residues in the cathepsin B propeptide for inhibitory activity. FEBS Lett. 393:24-26, 1996.