The levels of the lectin pathway serine protease MASP-1 and its complex formation with C1 inhibitor are linked to the severity of hereditary angioedema

Journal of Immunology

Volumn 195, Issue 8, 2015, Pages 3596-3604

  Hansen, Cecilie Bo ^a   Csuka, Dorottya ^b   Munthe Fog, Lea ^a   Varga, Lilian ^b   Farkas, Henriette ^b   Hansen, Karin Møller ^a   Koch, Claus ^c   Skjødt, Karsten ^c   Garred, Peter ^a   Skjoedt, Mikkel Ole ^a  

^a Mental Health Services CPH   (Denmark)

^b SEMMELWEIS UNIVERSITY OF MEDICINE   (Hungary)

^c UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT COMPONENT C1S INHIBITOR; COMPLEMENT COMPONENT C3; COMPLEMENT COMPONENT C4; FICOLIN; FICOLIN 3; LECTIN; MANNAN BINDING LECTIN; MANNAN BINDING LECTIN ASSOCIATED SERINE PROTEINASE; MANNAN BINDING LECTIN ASSOCIATED SERINE PROTEINASE 1; MANNAN BINDING LECTIN ASSOCIATED SERINE PROTEINASE 2; MICROTUBULE ASSOCIATED PROTEIN 1; UNCLASSIFIED DRUG; MASP1 PROTEIN, HUMAN; MULTIPROTEIN COMPLEX; SERPING1 PROTEIN, HUMAN;

ADULT; ANGIONEUROTIC EDEMA; ARTICLE; BINDING AFFINITY; BLOOD SAMPLING; COMPARATIVE STUDY; COMPLEX FORMATION; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE SEVERITY; ENZYME ACTIVATION; ENZYME BINDING; ENZYME BLOOD LEVEL; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMAN; MAJOR CLINICAL STUDY; MALE; MOLECULAR DYNAMICS; PATHOPHYSIOLOGY; PRECIPITATION; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; BLOOD; CLINICAL TRIAL; IMMUNOLOGY; INJURY SCALE; METABOLISM; MIDDLE AGED; PATHOLOGY;

ADULT; ANGIOEDEMAS, HEREDITARY; COMPLEMENT C1 INACTIVATOR PROTEINS; COMPLEMENT C4; FEMALE; HUMANS; MALE; MANNOSE-BINDING PROTEIN-ASSOCIATED SERINE PROTEASES; MIDDLE AGED; MULTIPROTEIN COMPLEXES; TRAUMA SEVERITY INDICES;

EID: 84943551989     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1402838     Document Type: Article

References (35)

1. Walport, M. J. 2001. Complement. First of two parts. N. Engl. J. Med. 344:1058-1066.
2. Walport, M. J. 2001. Complement. Second of two parts. N. Engl. J. Med. 344:1140-1144.
3. Terai, I., K. Kobayashi, M. Matsushita, and T. Fujita. 1997. Human serum mannose-binding lectin (MBL)-associated serine protease-1 (MASP-1): determination of levels in body fluids and identification of two forms in serum. Clin. Exp. Immunol. 110:317-323.
4. Thiel, S., T. Vorup-Jensen, C. M. Stover, W. Schwaeble, S. B. Laursen, K. Poulsen, A. C. Willis, P. Eggleton, S. Hansen, U. Holmskov, et al. 1997. A second serine protease associated with mannan-binding lectin that activates complement. Nature 386:506-510.
5. Dahl, M. R., S. Thiel, M. Matsushita, T. Fujita, A. C. Willis, T. Christensen, T. Vorup-Jensen, and J. C. Jensenius. 2001. MASP-3 and its association with distinct complexes of the mannan-binding lectin complement activation pathway. Immunity 15:127-135.
6. Takahashi, M., Y. Endo, T. Fujita, and M. Matsushita. 1999. A truncated form of mannose-binding lectin-associated serine protease (MASP)-2 expressed by alternative polyadenylation is a component of the lectin complement pathway. Int. Immunol. 11:859-863.
7. Skjoedt, M. O., T. Hummelshoj, Y. Palarasah, C. Honore, C. Koch, K. Skjodt, and P. Garred. 2010. A novel mannose-binding lectin/ficolin-associated protein is highly expressed in heart and skeletal muscle tissues and inhibits complement activation. J. Biol. Chem. 285:8234-8243.
8. Degn, S. E., A. G. Hansen, R. Steffensen, C. Jacobsen, J. C. Jensenius, and S. Thiel. 2009. MAp44, a human protein associated with pattern recognition molecules of the complement system and regulating the lectin pathway of complement activation. J. Immunol. 183:7371-7378.
9. Héja, D., A. Kocsis, J. Dobó, K. Szilágyi, R. Szász, P. Závodszky, G. Pál, and P. Gál. 2012. Revised mechanism of complement lectin-pathway activation revealing the role of serine protease MASP-1 as the exclusive activator of MASP-2. Proc. Natl. Acad. Sci. USA 109:10498-10503.
10. Héja, D., V. Harmat, K. Fodor, M. Wilmanns, J. Dobó, K. A. Kékesi, P. Závodszky, P. Gál, and G. Pál. 2012. Monospecific inhibitors show that both mannan-binding lectin-associated serine protease-1 (MASP-1) and -2 are essential for lectin pathway activation and reveal structural plasticity of MASP-2. J. Biol. Chem. 287:20290-20300.
11. Degn, S. E., L. Jensen, A. G. Hansen, D. Duman, M. Tekin, J. C. Jensenius, and S. Thiel. 2012. Mannan-binding lectin-associated serine protease (MASP)-1 is crucial for lectin pathway activation in human serum, whereas neither MASP-1 nor MASP-3 is required for alternative pathway function. J. Immunol. 189:3957-3969.
12. Davis, A. E., III, F. Lu, and P. Mejia. 2010. C1 inhibitor, a multi-functional serine protease inhibitor. Thromb. Haemost. 104:886-893.
13. Zuraw, B. L., J. A. Bernstein, D. M. Lang, T. Craig, D. Dreyfus, F. Hsieh, D. Khan, J. Sheikh, D. Weldon, D. I. Bernstein, et al. 2013. A focused parameter update: hereditary angioedema, acquired C1 inhibitor deficiency, and angiotensinconverting enzyme inhibitor-associated angioedema. J. Allergy Clin. Immunol. 131:1491-1493.e25.
14. Dobó, J., B. Major, K. A. Kékesi, I. Szabó, M. Megyeri, K. Hajela, G. Juhász, P. Závodszky, and P. Gál. 2011. Cleavage of kininogen and subsequent bradykinin release by the complement component: mannose-binding lectin-associated serine protease (MASP)-1. PLoS One 6:e20036.
15. Csuka, D., L. Munthe-Fog, M. O. Skjoedt, A. Kocsis, Z. Zotter, P. Gál, L. Varga, H. Farkas, G. Füst, and P. Garred. 2013. The role of ficolins and MASPs in hereditary angioedema due to C1-inhibitor deficiency. Mol. Immunol. 54:271-277.
16. Csuka, D., G. Füst, H. Farkas, and L. Varga. 2011. Parameters of the classical complement pathway predict disease severity in hereditary angioedema. Clin. Immunol. 139:85-93.
17. Csuka, D., L. Munthe-Fog, M. O. Skjoedt, E. Hein, J. T. Bay, L. Varga, G. Füst, and P. Garred. 2013. A novel assay to quantitate MASP-2/ficolin-3 complexes in serum. J. Immunol. Methods 387:237-244.
18. Munthe-Fog, L., T. Hummelshøj, C. Honoré, H. O. Madsen, H. Permin, and P. Garred. 2009. Immunodeficiency associated with FCN3 mutation and ficolin-3 deficiency. N. Engl. J. Med. 360:2637-2644.
19. Larsen, F., H. O. Madsen, R. B. Sim, C. Koch, and P. Garred. 2004. Diseaseassociated mutations in human mannose-binding lectin compromise oligomerization and activity of the final protein. J. Biol. Chem. 279:21302-21311.
20. Skjoedt, M. O., Y. Palarasah, L. Munthe-Fog, Y. Jie Ma, G. Weiss, K. Skjodt, C. Koch, and P. Garred. 2010. MBL-associated serine protease-3 circulates in high serum concentrations predominantly in complex with Ficolin-3 and regulates Ficolin-3 mediated complement activation. Immunobiology 215:921-931.
21. Skjoedt, M. O., T. Hummelshoj, Y. Palarasah, E. Hein, L. Munthe-Fog, C. Koch, K. Skjodt, and P. Garred. 2011. Serum concentration and interaction properties of MBL/ficolin associated protein-1. Immunobiology 216:625-632.
22. Hein, E., C. Honoré, M. O. Skjoedt, L. Munthe-Fog, T. Hummelshøj, and P. Garred. 2010. Functional analysis of Ficolin-3 mediated complement activation. PLoS One 5:e15443.
23. Laursen, I., P. Højrup, G. Houen, and M. Christiansen. 2008. Characterisation of the 1st SSI purified MBL standard. Clin. Chim. Acta 395:159-161.
24. Laursen, I., G. Houen, P. Højrup, N. Brouwer, L. B. Krogsøe, L. Blou, and P. R. Hansen. 2007. Second-generation nanofiltered plasma-derived mannan-binding lectin product: process and characteristics. Vox Sang. 92:338-350.
25. Zundel, S., S. Cseh, M. Lacroix, M. R. Dahl, M. Matsushita, J. P. Andrieu, W. J. Schwaeble, J. C. Jensenius, T. Fujita, G. J. Arlaud, and N. M. Thielens. 2004. Characterization of recombinant mannan-binding lectin-associated serine protease (MASP)-3 suggests an activation mechanism different from that of MASP-1 and MASP-2. J. Immunol. 172:4342-4350.
26. Matsushita, M., S. Thiel, J. C. Jensenius, I. Terai, and T. Fujita. 2000. Proteolytic activities of two types of mannose-binding lectin-associated serine protease. J. Immunol. 165:2637-2642.
27. Petersen, S. V., S. Thiel, and J. C. Jensenius. 2001. The mannan-binding lectin pathway of complement activation: biology and disease association. Mol. Immunol. 38:133-149.
28. Ambrus, G., P. Gál, M. Kojima, K. Szilágyi, J. Balczer, J. Antal, L. Gráf, A. Laich, B. E. Moffatt, W. Schwaeble, et al. 2003. Natural substrates and inhibitors of mannan-binding lectin-associated serine protease-1 and -2: a study on recombinant catalytic fragments. J. Immunol. 170:1374-1382.
29. Møller-Kristensen, M., J. C. Jensenius, L. Jensen, N. Thielens, V. Rossi, G. Arlaud, and S. Thiel. 2003. Levels of mannan-binding lectin-associated serine protease-2 in healthy individuals. J. Immunol. Methods 282:159-167.
30. Thiel, S., L. Jensen, S. E. Degn, H. J. Nielsen, P. Gál, J. Dobó, and J. C. Jensenius. 2012. Mannan-binding lectin (MBL)-associated serine protease-1 (MASP-1), a serine protease associated with humoral pattern-recognition molecules: normal and acute-phase levels in serum and stoichiometry of lectin pathway components. Clin. Exp. Immunol. 169:38-48.
31. Presanis, J. S., K. Hajela, G. Ambrus, P. Gál, and R. B. Sim. 2004. Differential substrate and inhibitor profiles for human MASP-1 and MASP-2. Mol. Immunol. 40:921-929.
32. Paréj, K., J. Dobó, P. Závodszky, and P. Gál. 2013. The control of the complement lectin pathway activation revisited: both C1-inhibitor and antithrombin are likely physiological inhibitors, while a2-macroglobulin is not. Mol. Immunol. 54:415-422.
33. Rossi, V., S. Cseh, I. Bally, N. M. Thielens, J. C. Jensenius, and G. J. Arlaud. 2001. Substrate specificities of recombinant mannan-binding lectin-associated serine proteases-1 and -2. J. Biol. Chem. 276:40880-40887.
34. Sim, R. B., G. J. Arlaud, and M. G. Colomb. 1979. C1 inhibitor-dependent dissociation of human complement component C1 bound to immune complexes. Biochem. J. 179:449-457.
35. Bowen, T., M. Cicardi, H. Farkas, K. Bork, H. J. Longhurst, B. Zuraw, E. Aygoeren-Pürsün, T. Craig, K. Binkley, J. Hebert, et al. 2010. 2010 International consensus algorithm for the diagnosis, therapy and management of hereditary angioedema. Allergy Asthma Clin. Immunol. 6:24.