Plasminogen activator inhibitor 1 is an intracellular inhibitor of furin proprotein convertase

Journal of Cell Science

Volumn 124, Issue 8, 2011, Pages 1224-1230

  Bernot, Denis ^a   Stalin, Jimmy ^a   Stocker, Pierre ^b   Bonardo, Bernadette ^a   Scroyen, Ilse ^a   Alessi, Marie Christine ^a   Peiretti, Franck ^a  

^a INSERM   (France)

^b AIX MARSEILLE UNIVERSITÉ   (France)

Author keywords

ADAM17; Convertase; Furin; Golgi; Insulin receptor; PAI 1

Indexed keywords

ADAM PROTEIN; ADAM17 PROTEIN; FURIN; INSULIN RECEPTOR; PLASMINOGEN ACTIVATOR INHIBITOR 1; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME INHIBITOR COMPLEX; METABOLIC DISORDER; METABOLIC SYNDROME X; NON INSULIN DEPENDENT DIABETES MELLITUS; PRIORITY JOURNAL;

CELL LINE; ENZYME INHIBITORS; FURIN; GOLGI APPARATUS; HUMANS; INTRACELLULAR SPACE; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 79953151795     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.079889     Document Type: Article

References (53)

1. Alessi, M. C. and Juhan-Vague, I. (2008). Metabolic syndrome, haemostasis and thrombosis. Thromb. Haemost. 99, 995-1000.
2. Alessi, M. C., Peiretti, F., Morange, P., Henry, M., Nalbone, G. and Juhan-Vague, I. (1997). Production of plasminogen activator inhibitor 1 by human adipose tissue: possible link between visceral fat accumulation and vascular disease. Diabetes 46, 860-867.
3. Alessi, M. C., Poggi, M. and Juhan-Vague, I. (2007). Plasminogen activator inhibitor-1, adipose tissue and insulin resistance. Curr. Opin. Lipidol. 18, 240-245.
4. Anderson, E. D., Thomas, L., Hayflick, J. S. and Thomas, G. (1993). Inhibition of HIV-1 gp160-dependent membrane fusion by a furin-directed alpha 1-antitrypsin variant. J. Biol. Chem. 268, 24887-24891.
5. Anderson, E. D., VanSlyke, J. K., Thulin, C. D., Jean, F. and Thomas, G. (1997). Activation of the furin endoprotease is a multiple-step process: requirements for acidification and internal propeptide cleavage. EMBO J. 16, 1508-1518.
6. Benjannet, S., Savaria, D., Laslop, A., Munzer, J. S., Chretien, M., Marcinkiewicz, M. and Seidah, N. G. (1997). Alpha1-antitrypsin Portland inhibits processing of precursors mediated by proprotein convertases primarily within the constitutive secretory pathway. J. Biol. Chem. 272, 26210-26218.
7. Black, R. A., Rauch, C. T., Kozlosky, C. J., Peschon, J. J., Slack, J. L., Wolfson, M. F., Castner, B. J., Stocking, K. L., Reddy, P., Srinivasan, S. et al. (1997). A metalloproteinase disintegrin that releases tumour-necrosis factor-alpha from cells. Nature 385, 729-733.
8. Brennan, S. O. and Nakayama, K. (1994). Furin has the proalbumin substrate specificity and serpin inhibitory properties of an in situ hepatic convertase. FEBS Lett. 338, 147-151.
9. Coppola, J. M., Hamilton, C. A., Bhojani, M. S., Larsen, M. J., Ross, B. D. and Rehemtulla, A. (2007). Identification of inhibitors using a cell-based assay for monitoring Golgi-resident protease activity. Anal. Biochem. 364, 19-29.
10. 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.
11. Dupont, D. M., Madsen, J. B., Kristensen, T., Bodker, J. S., Blouse, G. E., Wind, T. and Andreasen, P. A. (2009). Biochemical properties of plasminogen activator inhibitor-1. Front. Biosci. 14, 1337-1361.
12. Gawlik, K., Shiryaev, S. A., Zhu, W., Motamedchaboki, K., Desjardins, R., Day, R., Remacle, A. G., Stec, B. and Strongin, A. Y. (2009). Autocatalytic activation of the furin zymogen requires removal of the emerging enzyme's N-terminus from the active site. PLoS One 4, e5031.
13. Gawlik, K., Remacle, A. G., Shiryaev, S. A., Golubkov, V. S., Ouyang, M., Wang, Y. and Strongin, A. Y. (2010). A femtomol range FRET biosensor reports exceedingly low levels of cell surface furin: implications for the processing of anthrax protective antigen. PLoS One 5, e11305.
14. Griffiths, S. L. and Grainger, D. J. (2006). Proposal of a novel diabetogenic mechanism involving the serpin PAI-1. BioEssays 28, 629-641.
15. Guimont, P., Grondin, F. and Dubois, C. M. (2007). Sox9-dependent transcriptional regulation of the proprotein convertase furin. Am. J. Physiol. Cell Physiol 293, C172-C183.
16. Jean, F., Stella, K., Thomas, L., Liu, G., Xiang, Y., Reason, A. J. and Thomas, G. (1998). alpha1-Antitrypsin Portland, a bioengineered serpin highly selective for furin: application as an antipathogenic agent. Proc. Natl. Acad. Sci. USA 95, 7293-7298.
17. Keijer, J., Linders, M., Wegman, J. J., Ehrlich, H. J., Mertens, K. and Pannekoek, H. (1991). On the target specificity of plasminogen activator inhibitor 1, the role of heparin, vitronectin, and the reactive site. Blood 78, 1254-1261.
18. Konkle, B. A., Schuster, S. J., Kelly, M. D., Harjes, K., Hassett, D. E., Bohrer, M. and Tavassoli, M. (1992). Plasminogen activator inhibitor-1 messenger RNA expression is induced in rat hepatocytes in vivo by dexamethasone. Blood 79, 2636-2642.
19. Kvassman, J. O., Lawrence, D. A. and Shore, J. D. (1995). The acid stabilization of plasminogen activator inhibitor-1 depends on protonation of a single group that affects loop insertion into beta-sheet A. J. Biol. Chem. 270, 27942-27947.
20. Langdown, J., Johnson, D. J., Baglin, T. P. and Huntington, J. A. (2004). Allosteric activation of antithrombin critically depends upon hinge region extension. J. Biol. Chem. 279, 47288-47297.
21. Laprise, M. H., Grondin, F., Cayer, P., McDonald, P. P. and Dubois, C. M. (2002). Furin gene (fur) regulation in differentiating human megakaryoblastic Dami cells: involvement of the proximal GATA recognition motif in the P1 promoter and impact on the maturation of furin substrates. Blood 100, 3578-3587.
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. 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.
24. Levin, E. G. (1983). Latent tissue plasminogen activator produced by human endothelial cells in culture: evidence for an enzyme-inhibitor complex. Proc. Natl. Acad. Sci. USA 80, 6804-6808.
25. Liang, X., Kanjanabuch, T., Mao, S. L., Hao, C. M., Tang, Y. W., Declerck, P. J., Hasty, A. H., Wasserman, D. H., Fogo, A. B. and Ma, L. J. (2006). Plasminogen activator inhibitor-1 modulates adipocyte differentiation. Am. J. Physiol. Endocrinol. Metab. 290, E103-E113.
26. Ma, G. M., Halayko, A. J., Stelmack, G. L., Zhu, F., Zhao, R., Hillier, C. T. and Shen, G. X. (2006). Effects of oxidized and glycated low-density lipoproteins on transcription and secretion of plasminogen activator inhibitor-1 in vascular endothelial cells. Cardiovasc. Pathol. 15, 3-10.
27. Ma, L. J., Mao, S. L., Taylor, K. L., Kanjanabuch, T., Guan, Y., Zhang, Y., Brown, N. J., Swift, L. L., McGuinness, O. P., Wasserman, D. H. et al. (2004). Prevention of obesity and insulin resistance in mice lacking plasminogen activator inhibitor 1. Diabetes 53, 336-346.
28. Molloy, S. S., Anderson, E. D., Jean, F. and Thomas, G. (1999). Bi-cycling the furin pathway: from TGN localization to pathogen activation and embryogenesis. Trends Cell Biol. 9, 28-35.
29. Moss, M. L., Jin, S. L., Milla, M. E., Bickett, D. M., Burkhart, W., Carter, H. L., Chen, W. J., Clay, W. C., Didsbury, J. R., Hassler, D. et al. (1997). Cloning of a disintegrin metalloproteinase that processes precursor tumour-necrosis factor-alpha. Nature 385, 733-736.
30. Oda, K., Misumi, Y., Ikehara, Y., Brennan, S. O., Hatsuzawa, K. and Nakayama, K. (1992). Proteolytic cleavages of proalbumin and complement Pro-C3 in vitro by a truncated soluble form of furin, a mammalian homologue of the yeast Kex2 protease. Biochem. Biophys. Res. Commun. 189, 1353-1361.
31. Oley, M., Letzel, M. C. and Ragg, H. (2004). Inhibition of furin by serpin Spn4A from Drosophila melanogaster. FEBS Lett. 577, 165-169.
32. Olson, S. T., Swanson, R., Day, D., Verhamme, I., Kvassman, J. and Shore, J. D. (2001). Resolution of Michaelis complex, acylation, and conformational change steps in the reactions of the serpin, plasminogen activator inhibitor-1, with tissue plasminogen activator and trypsin. Biochemistry 40, 11742-11756.
33. Peiretti, F., Canault, M., Deprez-Beauclair, P., Berthet, V., Bonardo, B., Juhan-Vague, I. and Nalbone, G. (2003). Intracellular maturation and transport of tumor necrosis factor alpha converting enzyme. Exp. Cell Res. 285, 278-285.
34. Reddy, P., Slack, J. L., Davis, R., Cerretti, D. P., Kozlosky, C. J., Blanton, R. A., Shows, D., Peschon, J. J. and Black, R. A. (2000). Functional analysis of the domain structure of tumor necrosis factor-alpha converting enzyme. J. Biol. Chem. 275, 14608-14614.
35. Robertson, B. J., Moehring, J. M. and Moehring, T. J. (1993). Defective processing of the insulin receptor in an endoprotease-deficient Chinese hamster cell strain is corrected by expression of mouse furin. J. Biol. Chem. 268, 24274-24277.
36. Roebroek, A. J., Schalken, J. A., Leunissen, J. A., Onnekink, C., Bloemers, H. P. and Van de Ven, W. J. (1986). Evolutionary conserved close linkage of the c-fes/fps protooncogene and genetic sequences encoding a receptor-like protein. EMBO J. 5, 2197-2202.
37. Schafer, K., Fujisawa, K., Konstantinides, S. and Loskutoff, D. J. (2001). Disruption of the plasminogen activator inhibitor 1 gene reduces the adiposity and improves the metabolic profile of genetically obese and diabetic ob/ob mice. FASEB J. 15, 1840-1842.
38. Schechter, I. and Berger, A. (1967). On the size of the active site in proteases. I. Papain. Biochem. Biophys. Res. Commun. 27, 157-162.
39. Seidah, N. G. and Chretien, M. (1999). Proprotein and prohormone convertases: a family of subtilases generating diverse bioactive polypeptides. Brain Res. 848, 45-62.
40. Serino, M., Menghini, R., Fiorentino, L., Amoruso, R., Mauriello, A., Lauro, D., Sbraccia, P., Hribal, M. L., Lauro, R. and Federici, M. (2007). Mice heterozygous for tumor necrosis factor-alpha converting enzyme are protected from obesity-induced insulin resistance and diabetes. Diabetes 56, 2541-2546.
41. Shapiro, J., Sciaky, N., Lee, J., Bosshart, H., Angeletti, R. H. and Bonifacino, J. S. (1997). Localization of endogenous furin in cultured cell lines. J. Histochem. Cytochem. 45, 3-12.
42. Solomon, K. A., Pesti, N., Wu, G. and Newton, R. C. (1999). Cutting edge: a dominant negative form of TNF-alpha converting enzyme inhibits proTNF and TNFRII secretion. J. Immunol. 163, 4105-4108.
43. Srour, N., Lebel, A., McMahon, S., Fournier, I., Fugere, M., Day, R. and Dubois, C. M. (2003). TACE/ADAM-17 maturation and activation of sheddase activity require proprotein convertase activity. FEBS Lett. 554, 275-283.
44. Takahashi, S., Kasai, K., Hatsuzawa, K., Kitamura, N., Misumi, Y., Ikehara, Y., Murakami, K. and Nakayama, K. (1993). A mutation of furin causes the lack of precursor-processing activity in human colon carcinoma LoVo cells. Biochem. Biophys. Res. Commun. 195, 1019-1026.
45. Thomas, G. (2002). Furin at the cutting edge: from protein traffic to embryogenesis and disease. Nat. Rev. Mol. Cell Biol. 3, 753-766.
46. Thorsen, S., Philips, M., Selmer, J., Lecander, I. and Astedt, B. (1988). Kinetics of inhibition of tissue-type and urokinase-type plasminogen activator by plasminogenactivator inhibitor type 1 and type 2. Eur. J. Biochem. 175, 33-39.
47. van de Ven, W. J., Voorberg, J., Fontijn, R., Pannekoek, H., van den Ouweland, A. M., van Duijnhoven, H. L., Roebroek, A. J. and Siezen, R. J. (1990). Furin is a subtilisinlike proprotein processing enzyme in higher eukaryotes. Mol. Biol. Rep. 14, 265-275.
48. Vleugels, N., Leys, J., Knockaert, I. and Declerck, P. J. (2000). Effect of stabilizing versus destabilizing interactions on plasminogen activator inhibitor-1. Thromb. Haemost. 84, 871-875.
49. Wasley, L. C., Rehemtulla, A., Bristol, J. A. and Kaufman, R. J. (1993). PACE/furin can process the vitamin K-dependent pro-factor IX precursor within the secretory pathway. J. Biol. Chem. 268, 8458-8465.
50. Williams, J. F., McClain, D. A., Dull, T. J., Ullrich, A. and Olefsky, J. M. (1990). Characterization of an insulin receptor mutant lacking the subunit processing site. J. Biol. Chem. 265, 8463-8469.
51. Xu, H., Hirosumi, J., Uysal, K. T., Guler, A. D. and Hotamisligil, G. S. (2002a). Exclusive action of transmembrane TNF alpha in adipose tissue leads to reduced adipose mass and local but not systemic insulin resistance. Endocrinology 143, 1502-1511.
52. Xu, H., Uysal, K. T., Becherer, J. D., Arner, P. and Hotamisligil, G. S. (2002b). Altered tumor necrosis factor-alpha (TNF-alpha) processing in adipocytes and increased expression of transmembrane TNF-alpha in obesity. Diabetes 51, 1876-1883.
53. Yamashita, T., Dai, Q., Suzuki, Y., Ihara, H., Mogami, H., Koide, T., Castellino, F. and Urano, T. (2006). Plasminogen activator inhibitor 1 forms a stable non-acyl enzyme inhibitor complex with tissue plasminogen activator. J. Thromb. Haemost. 4, Supplement S1, 165-165.