Identification of serpin determinants of specificity and selectivity for furin inhibition through studies of α1PDX (α1-protease inhibitor portland)-serpin B8 and furin active-site loop chimeras

Journal of Biological Chemistry

Volumn 288, Issue 30, 2013, Pages 21802-21814

  Izaguirre, Gonzalo ^a   Qi, Lixin ^a   Lima, Mary ^a   Olson, Steven T ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOLOGY;

MICROCOMPUTERS;

ALPHA1 PROTEASE INHIBITOR PORTLAND; FURIN; SERINE PROTEINASE; SERPIN B8; UNCLASSIFIED DRUG;

ARTICLE; BETA SHEET; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ENGINEERING; ENZYME SPECIFICITY; PRIORITY JOURNAL; PROTEIN DOMAIN; SEQUENCE ALIGNMENT;

Α1PDX; FURIN; PROPROTEIN CONVERTASE; PROTEASE; PROTEASE INHIBITOR; PROTEIN ENGINEERING; SERINE PROTEASE; SERPIN; SERPIN B8;

ALPHA 1-ANTITRYPSIN; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; BIOCATALYSIS; CATALYTIC DOMAIN; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FURIN; HUMANS; KINETICS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PROPROTEIN CONVERTASES; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SERPINS;

EID: 84881257896     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.462804     Document Type: Article

References (32)

1. 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
2. Walker, J. A., Molloy, S. S., Thomas, G., Sakaguchi, T., Yoshida, T., Chambers, T. M., and Kawaoka, Y. (1994) Sequence specificity of furin, a proprotein-processing endoprotease, for the hemagglutinin of a virulent avian influenza virus. J. Virol. 68, 1213-1218
3. Scamuffa, N., Calvo, F., Chrétien, M., Seidah, N. G., and Khatib, A. M. (2006) Proprotein convertases. Lessons from knockouts. FASEB J. 20, 1954-1963
4. Seidah, N. G., Mayer, G., Zaid, A., Rousselet, E., Nassoury, N., Poirier, S., Essalmani, R., and Prat, A. (2008) The activation and physiological functions of the proprotein convertases. Int. J. Biochem. Cell Biol. 40, 1111-1125
5. Artenstein, A. W., and Opal, S. M. (2011) Proprotein convertases in health and disease. N. Engl. J. Med. 365, 2507-2518
6. Seidah, N. G., and Prat, A. (2012) The biology and therapeutic targeting of the proprotein convertases. Nat. Rev. Drug Discov. 11, 367-383
7. Couture, F., D'Anjou, F., and Day, R. (2011) On the cutting edge of proprotein convertase pharmacology. From molecular concepts to clinical applications. Biomol. Concepts 2, 421-438
8. Fugère, M., and Day, R. (2002) Inhibitors of the subtilase-like pro-protein convertases (SPCs). Curr. Pharm. Des. 8, 549-562
9. Basak, A. (2005) Inhibitors of proprotein convertases. J. Mol. Med. 83, 844-855
10. Henrich, S., Lindberg, I., Bode, W., and Than, M. E. (2005) Proprotein convertase models based on the crystal structures of furin and kexin. Explanation of their specificity. J. Mol. Biol. 345, 211-227
11. 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
12. Lu, W., Zhang, W., Molloy, S. S., Thomas, G., Ryan, K., Chiang, Y., Anderson, S., and Laskowski, M., Jr. (1993) Arg15-Lys17-Arg18 turkey ovomucoid third domain inhibits human furin. J. Biol. Chem. 268, 14583-14585
13. Van Rompaey, L., Ayoubi, T., Van De Ven, W., and Marynen, P. (1997) Inhibition of intracellular proteolytic processing of soluble proproteins by an engineered2-macroglobulin containing a furin recognition sequence in the bait region. Biochem. J. 326, 507-514
14. Anderson, E. D., Thomas, L., Hayflick, J. S., and Thomas, G. (1993) Inhibition of HIV-1 gp160-dependent membrane fusion by a furin-directed α1-antitrypsin variant. J. Biol. Chem. 268, 24887-24891
15. Dahlen, J. R., Jean, F., Thomas, G., Foster, D. C., and Kisiel, W. (1998) Inhibition of soluble recombinant furin by human proteinase inhibitor 8. J. Biol. Chem. 273, 1851-1854
16. Osterwalder, T., Kuhnen, A., Leiserson, W. M., Kim, Y. S., and Keshishian, H. (2004) Drosophila serpin 4 functions as a neuroserpin-like inhibitor of subtilisin-like proprotein convertases. J. Neurosci. 24, 5482-5491
17. Richer, M. J., Keays, C. A., Waterhouse, J., Minhas, J., Hashimoto, C., and Jean, F. (2004) The Spn4 gene of Drosophila encodes a potent furin-directed secretory pathway serpin. Proc. Natl. Acad. Sci. U.S.A. 101, 10560-10565
18. Bentele, C., Krüger, O., Tödtmann, U., Oley, M., and Ragg, H. (2006) A proprotein convertase-inhibiting serpin with an endoplasmic reticulum targeting signal from Branchiostoma lanceolatum, a close relative of vertebrates. Biochem. J. 395, 449-456
19. Silverman, G. A., Bird, P. I., Carrell, R. W., Church, F. C., Coughlin, P. B., Gettins, P. G., Irving, J. A., Lomas, D. A., Luke, C. J., Moyer, R. W., Pemberton, P. A., Remold-O'Donnell, E., Salvesen, G. S., Travis, J., and Whisstock, J. C. (2001) The serpins are an expanding superfamily of structurally similar but functionally diverse proteins. Evolution, mechanism of inhibition, novel functions, and a revised nomenclature. J. Biol. Chem. 276, 33293-33296
20. Gettins, P. G., and Olson, S. T. (2009) Exosite determinants of serpin specificity. J. Biol. Chem. 284, 20441-20445
21. Strik, M. C., Bladergroen, B. A., Wouters, D., Kisiel, W., Hooijberg, J. H., Verlaan, A. R., Hordijk, P. L., Schneider, P., Hack, C. E., and Kummer, J. A. (2002) Distribution of the human intracellular serpin protease inhibitor 8 in human tissues. J. Histochem. Cytochem. 50, 1443-1454
22. Leblond, J., Laprise, M. H., Gaudreau, S., Grondin, F., Kisiel, W., and Dubois, C. M. (2006) The serpin proteinase inhibitor 8. An endogenous furin inhibitor released from human platelets. Thromb. Haemost. 95, 243-252
23. Gill, S. C., and von Hippel, P. H. (1989) Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem. 182, 319-326
24. Izaguirre, G., Rezaie, A. R., and Olson, S. T. (2009) Engineering functional antithrombin exosites inα1-proteinase inhibitor that specifically promote the inhibition of factor Xa and factor IXa. J. Biol. Chem. 284, 1550-1558
25. Kwon, K. S., Lee, S., and Yu, M. H. (1995) Refolding of α1-antitrypsin expressed as inclusion bodies in Escherichia coli. Characterization of aggregation. Biochim. Biophys. Acta 1247, 179-184
26. Pannell, R., Johnson, D., and Travis, J. (1974) Isolation and properties of human plasma α1-proteinase inhibitor. Biochemistry 13, 5439-5445
27. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685
28. Dufour, E. K., Denault, J. B., Hopkins, P. C., and Leduc, R. (1998) Serpinlike properties of α1-antitrypsin Portland towards furin convertase. FEBS Lett. 426, 41-46
29. 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 furin explains its stringent specificity. Nat. Struct. Biol. 10, 520-526
30. Horovitz, A. (1987) Non-additivity in protein-protein interactions. J. Mol. Biol. 196, 733-735
31. Di Cera, E. (1998) Site-specific thermodynamics: understanding cooperativity in molecular recognition. Chem. Rev. 98, 1563-1592
32. Dementiev, A., Simonovic, M., Volz, K., and Gettins, P. G. (2003) Canonical inhibitor-like interactions explain reactivity ofα1-proteinase inhibitor Pittsburgh and antithrombin with proteinases. J. Biol. Chem. 278, 37881-37887