Stability of mutant serpin/furin complexes: Dependence on pH and regulation at the deacylation step

Protein Science

Volumn 14, Issue 2, 2005, Pages 303-315

  Dufour, Erick K ^a   Désilets, Antoine ^a   Longpré, Jean Michel ^a   Leduc, Richard ^a  

^a UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

Convertases; Furin; Protease inhibitors; Serine proteases; Serpin mechanism; 1 antitrypsin; 1 antichymotrypsin

Indexed keywords

ALPHA 1 ANTICHYMOTRYPSIN; ALPHA 1 ANTITRYPSIN; COMPLEMENTARY DNA; FURIN; MUTANT PROTEIN; RECOMBINANT PROTEIN; SERINE PROTEINASE; SERINE PROTEINASE INHIBITOR;

ARTICLE; COMPLEX FORMATION; DEACYLATION; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; KIDNEY CELL; KINETICS; PH; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PURIFICATION; SITE DIRECTED MUTAGENESIS; STOICHIOMETRY;

EID: 13244260693     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.04843305     Document Type: Article

References (51)

1. Anderson, E.D., Molloy, S.S., Jean, F., Fei, H., Shimamura, S., and Thomas, G. 2002. The ordered and compartment-specific autoproteolytic removal of the furin intramolecular chaperone is required for enzyme activation. J. Biol. Chem. 277: 12879-12890.
2. Angliker, H. 1995. Synthesis of tight binding inhibitors and their action on the proprotein-processing enzyme furin. J. Med. Chem. 38: 4014-4018.
3. Bergeron, F., Leduc, R., and Day, R. 2000. Subtilase-like pro-protein convertases: From molecular specificity to therapeutic applications. J. Mol. Endocrinol. 24: 1-22.
4. Bieth, J.G. 1995. Theoretical and practical aspects of proteinase inhibition kinetics. Methods Enzymol. 248: 59-84.
5. Boudreault, A., Gauthier, D., and Lazure, C. 1998. Proprotein convertase PC1/ 3-related peptides are potent slow tight-binding inhibitors of murine PC1/3 and Hfurin. J. Biol. Chem. 273: 31574-31580.
6. Bravo, D.A., Gleason, J.B., Sanchez, R.I., Roth, R.A., and Fuller, R.S. 1994. Accurate and efficient cleavage of the human insulin proreceptor by the human proprotein-processing protease furin. Characterization and kinetic parameters using the purified, secreted soluble protease expressed by a recombinant baculovirus. J. Biol. Chem. 269: 25830-25837.
7. Calugaru, S.V., Swanson, R., and Olson, S.T. 2001. The pH dependence of serpin-proteinase complex dissociation reveals a mechanism of complex stabilization involving inactive and active conformational states of the proteinase which are perturbable by calcium. J. Biol. Chem. 276: 32446-32455.
8. Cameron, A., Appel, J., Houghten, R.A., and Lindberg, I. 2000. Polyarginines are potent furin inhibitors. J. Biol. Chem. 275: 36741-36749.
9. Chiron, M.F., Fryling, C.M., and FitzGerald, D.J. 1994. Cleavage of pseudomonas exotoxin and diphtheria toxin by a furin-like enzyme prepared from beef liver. J. Biol. Chem. 269: 18167-18176.
10. Collier, R.J. and Young, J.A. 2003. Anthrax toxin. Annu. Rev. Cell Dev. Biol. 19: 45-70.
11. Cooperman, B.S., Stavridi, E., Nickbarg, E., Rescorla, E., Schlechter, N.M., and Rubin, H. 1993. Antichymotrypsin interaction with chymotrypsin. Partitioning of the complex. J. Biol. Chem. 268: 23616-23625.
12. Corboy, M.J. and Draper, R.K. 1997. Elevation of vacuolar pH inhibits the cytotoxic activity of furin-cleaved exotoxin A. Infect. Immun. 65: 2240-2242.
13. Denault, J.B. 2000. "Etude de la région riche en cystéine de la convertase de mammifère humaine SPC1/furine." Ph.D. thesis, Université de Sherbrooke, Sherbrooke, Québec, Canada.
14. Denault, J.B., Lazure, C., Day, R., and Leduc, R. 2000. Comparative characterization of two forms of recombinant human SPC1 secreted from Schneider 2 cells. Protein Expr. Purif. 19: 113-124.
15. Denault, J., Bissonnette, L., Longpre, J., Charest, G., Lavigne, P., and Leduc, R. 2002. Ectodomain shedding of furin: Kinetics and role of the cysteine-rich region. FEBS Lett. 527: 309-314.
16. de Wit, T.R. and van Mourik, J.A. 2001. Biosynthesis, processing and secretion of von Willebrand factor: Biological implications. Best Pract. Res. Clin. Haematol. 14: 241-255.
17. Djie, M.Z., Le Bonniec, B.F., Hopkins, P.C., Hipler, K., and Stone, S.R. 1996. Role of the P2 residue in determining the specificity of serpins. Biochemistry 35: 11461-11469.
18. Dufour, E.K., Denault, J.B., Hopkins, P.C., and Leduc, R. 1998. Serpin-like properties of α1-antitrypsin Portland towards furin convertase. FEBS Lett. 426: 41-46.
19. Dufour, E.K., Denault, J.B., Bissonnette, L., Hopkins, P.C., Lavigne, P., and Leduc, R. 2001. The contribution of arginine residues within the P6-P1 region of α 1-antitrypsin to its reaction with furin. J. Biol. Chem. 276: 38971-38979.
20. Elliott, P.R., Lomas, D.A., Carrell, R.W., and Abrahams, J.P. 1996. Inhibitory conformation of the reactive loop of α 1-antitrypsin. Nat. Struct. Biol. 3: 676-681.
21. Elliott, P.R., Abrahams, J.P., and Lomas, D.A. 1998. Wild-type α 1-antitrypsin is in the canonical inhibitory conformation. J. Mol. Biol. 275: 419-425.
22. Gettins, P.G. 2002. Serpin structure, mechanism, and function. Chem. Rev. 102: 4751-4804.
23. Gron, H., Meldal, M., and Breddam, K. 1992. Extensive comparison of the substrate preferences of two subtilisins as determined with peptide substrates which are based on the principle of intramolecular quenching. Biochemistry 31: 6011-6018.
24. Han, J.H., Cote, H.C., and Tollefsen, D.M. 1997. Inhibition of meizothrombin and meizothrombin(desF1) by heparin cofactor II. J. Biol. Chem. 272: 28660-28665.
25. Henrich, S., Cameron, A., Bourenkov, G.P., Kiefersauer, R., Huber, R., Lindberg, I., Bode, W., and Than, M.E. 2003. The crystal structure of the proprotein processing proteinase furin explains its stringent specificity. Nat. Struct. Biol. 10: 520-526.
26. Hopkins, P.C. and Stone, S.R. 1995. The contribution of the conserved hinge region residues of α1-antitrypsin to its reaction with elastase. Biochemistry 34: 15872-15879.
27. Huntington, J.A., Read, R.J., and Carrell, R.W. 2000. Structure of a serpin-protease complex shows inhibition by deformation. Nature 407: 923-926.
28. Jean, F., Stella, K., Thomas, L., Liu, G., Xiang, Y., Reason, A.J., and Thomas, G. 1998. α1-Antitrypsin Portland, a bioengineered serpin highly selective for furin: Application as an antipathogenic agent. Proc. Natl. Acad. Sci. 95: 7293-7298.
29. Johnson, D. and Travis, J. 1978. Structural evidence for methionine at the reactive site of human α-1-proteinase inhibitor. J. Biol. Chem. 253: 7142-7144.
30. Komiyama, T. and Fuller, R.S. 2000. Engineered eglin c variants inhibit yeast and human proprotein processing proteases, Kex2 and furin. Biochemistry 39: 15156-15165.
31. Komiyama, T., VanderLugt, B., Fugere, M., Day, R., Kaufman, R.J., and Fuller, R.S. 2003. Optimization of protease-inhibitor interactions by randomizing adventitious contacts. Proc. Natl. Acad. Sci. 100: 8205-8210.
32. Krysan, D.J., Rockwell, N.C., and Fuller, R.S. 1999. Quantitative characterization of furin specificity. Energetics of substrate discrimination using an internally consistent set of hexapeptidyl methylcoumarinamides. J. Biol. Chem. 274: 23229-23234.
33. Lazure, C., Gauthier, D., Jean, F., Boudreault, A., Seidah, N.G., Bennett, H.P., and Hendy, G.N. 1998. In vitro cleavage of internally quenched fluorogenic human proparathyroid hormone and proparathyroid-related peptide substrates by furin. Generation of a potent inhibitor. J. Biol. Chem. 273: 8572-8580.
34. Leduc, R., Molloy, S.S., Thorne, B.A., and Thomas, G. 1992. Activation of human furin precursor processing endoprotease occurs by an intramolecular autoproteolytic cleavage. J. Biol. Chem. 267: 14304-14308.
35. Molloy, S.S., Bresnahan, P.A., Leppla, S.H., Klimpel, K.R., and Thomas, G. 1992. Human furin is a calcium-dependent serine endoprotease that recognizes the sequence Arg-X-X-Arg and efficiently cleaves anthrax toxin protective antigen. J. Biol. Chem. 267: 16396-16402.
36. Nash, P., McFadden, G., and Whitty, A. 2000. Application of linear free energy relationships to the serpin-proteinase inhibition mechanism. FEBS Lett. 475: 1-6.
37. Perona, J.J. and Craik, C.S. 1995. Structural basis of substrate specificity in the serine proteases. Protein Sci. 4: 337-360.
38. Plotnick, M.I., Samakur, M., Wang, Z.M., Liu, X., Rubin, H., Schlechter, N.M., and Selwood, T. 2002. Heterogeneity in serpin-protease complexes as demonstrated by differences in the mechanism of complex breakdown. Biochemistry 41: 334-342.
39. Rockwell, N.C., Krysan, D.J., Komiyama, T., and Fuller, R.S. 2002. Precursor processing by kex2/furin proteases. Chem. Rev. 102: 4525-4548.
40. Schechter, I. and Berger, A. 1967. On the size of the active site in proteases. I. Papain. Biochem. Biophys. Res. Commun. 27: 157-162.
41. Schechter, N.M., Plotnick, M., Selwood, T., Walter, M., and Rubin, H. 1997. Diverse effects of pH on the inhibition of human chymase by serpins. J. Biol. Chem. 272: 24499-24507.
42. Siezen, R.J. and Leunissen, J.A. 1997. Subtilases: The superfamily of subtilisin-like serine proteases. Protein Sci. 6: 501-523.
43. Siezen, R.J., Creemers, J.W., and Van de Ven, W.J. 1994. Homology modelling of the catalytic domain of human furin. A model for the eukaryotic subtilisin-like proprotein convertases. Eur. J. Biochem. 222: 255-266.
44. Stavridi, E.S., O'Malley, K., Lukacs, C.M., Moore, W.T., Lambris, J.D., Christianson, D.W., Rubin, H., and Cooperman, B.S. 1996. Structural change in α-chymotrypsin induced by complexation with α 1-antichymotrypsin as seen by enhanced sensitivity to proteolysis. Biochemistry 35: 10608-10615.
45. Steiner, D.F. 1998. The proprotein convertases. Curr. Opin. Chem. Biol. 2: 31-39.
46. Thomas, G. 2002. Furin at the cutting edge: From protein traffic to embryogenesis and disease. Nat. Rev. Mol. Cell Biol. 3: 753-766.
47. Van de Ven, W.J., Creemers, J.W., and Roebroek, A.J. 1991. Furin: The prototype mammalian subtilisin-like proprotein-processing enzyme. Endoproteolytic cleavage at paired basic residues of proproteins of the eukaryotic secretory pathway. Enzyme 45: 257-270.
48. Waley, S.G. 1985. Kinetics of suicide substrates. Practical procedures for determining parameters. Biochem. J. 222: 843-849.
49. Watanabe, T., Nakagawa, T., Ikemizu, J., Nagahama, M., Murakami, K., and Nakayama, K. 1992. Sequence requirements for precursor cleavage within the constitutive secretory pathway. J. Biol. Chem. 267: 8270-8274.
50. Wei, A., Rubin, H., Cooperman, B.S., and Christianson, D.W. 1994. Crystal structure of an uncleaved serpin reveals the conformation of an inhibitory reactive loop. Nat. Struct. Biol. 1: 251-258.
51. Wise, R.J., Barr, P.J., Wong, P.A., Kiefer, M.C., Brake, A.J., and Kaufman, R.J. 1990. Expression of a human proprotein processing enzyme: Correct cleavage of the von Willebrand factor precursor at a paired basic amino acid site. Proc. Natl Acad. Sci. 87: 9378-9382.