MASP-1 and MASP-2 do not activate pro-factor D in resting human blood, whereas MASP-3 is a potential activator: Kinetic analysis involving specific MASP-1 and MASP-2 inhibitors

Journal of Immunology

Volumn 196, Issue 2, 2016, Pages 857-865

  Oroszlán, Gábor ^a   Kortvely, Elod ^b   Szakács, Dávid ^c   Kocsis, Andrea ^a   Dammeier, Sascha ^b   Zeck, Anne ^b   Ueffing, Marius ^b   Závodszky, Péter ^a   Pál, Gábor ^c   Gál, Péter ^a   Dobo, József ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c EÖTVÖS LORÁND UNIVERSITY   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

ALANYLPROPYLPROPYLARGINYLGLYCYLARGININE; AMINO ACID; COMPLEMENT FACTOR D; MANNAN BINDING LECTIN ASSOCIATED SERINE PROTEINASE; PROTEIN MASP 1; PROTEIN MASP 2; PROTEIN MASP 3; SERINE PROTEINASE INHIBITOR; THROMBIN; UNCLASSIFIED DRUG; COMPLEMENT FACTOR D, HUMAN; ENZYME INHIBITOR; MASP1 PROTEIN, HUMAN; MASP2 PROTEIN, HUMAN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BLOOD CLOTTING; BLOOD SAMPLING; CARBOXY TERMINAL SEQUENCE; COMPLEMENT ACTIVATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PURIFICATION; FLUORESCENCE ANALYSIS; HUMAN; INSECT CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; COMPLEMENT ALTERNATIVE PATHWAY; IMMUNOLOGY; MASS SPECTROMETRY; METABOLISM;

COMPLEMENT FACTOR D; COMPLEMENT PATHWAY, ALTERNATIVE; ENZYME INHIBITORS; HUMANS; MANNOSE-BINDING PROTEIN-ASSOCIATED SERINE PROTEASES; MASS SPECTROMETRY;

EID: 84954193454     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1501717     Document Type: Article

References (39)

1. Merle, N. S., S. E. Church, V. Fremeaux-Bacchi, and L. T. Roumenina. 2015. Complement System Part I-Molecular Mechanisms of Activation and Regulation. Front. Immunol. 6: 262.
2. Thiel, S. 2007. Complement activating soluble pattern recognition molecules with collagen-like regions, mannan-binding lectin, ficolins and associated proteins. Mol. Immunol. 44: 3875-3888.
3. Gál, P., J. Dobó, P. Závodszky, and R. B. Sim. 2009. Early complement proteases: C1r, C1s and MASPs. A structural insight into activation and functions. Mol. Immunol. 46: 2745-2752.
4. Henriksen, M. L., K. L. Madsen, K. Skjoedt, and S. Hansen. 2014. Calcium-sensitive immunoaffinity chromatography: Gentle and highly specific retrieval of a scarce plasma antigen, collectin-LK (CL-LK). J. Immunol. Methods 413: 25-31.
5. Beltrame, M. H., A. B. Boldt, S. J. Catarino, H. C. Mendes, S. E. Boschmann, I. Goeldner, and I. Messias-Reason. 2015. MBL-associated serine proteases (MASPs) and infectious diseases. Mol. Immunol. 67: 85-100.
6. 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
7. Megyeri, M., V. Harmat, B. Major, Á. Végh, J. Balczer, D. Héja, K. Szilágyi, D. Datz, G. Pál, P. Závodszky, et al. 2013. Quantitative characterization of the activation steps of mannan-binding lectin (MBL)-associated serine proteases (MASPs) points to the central role of MASP-1 in the initiation of the complement lectin pathway. J. Biol. Chem. 288: 8922-8934.
8. Dobó, J., V. Harmat, L. Beinrohr, E. Sebestyén, P. Závodszky, and P. Gál. 2009. MASP-1, a promiscuous complement protease: structure of its catalytic region reveals the basis of its broad specificity. J. Immunol. 183: 1207-1214.
9. Dobó, J., V. Schroeder, L. Jenny, L. Cervenak, P. Závodszky, and P. Gál. 2014. Multiple roles of complement MASP-1 at the interface of innate immune response and coagulation. Mol. Immunol. 61: 69-78.
10. Megyeri, M., V. Makó, L. Beinrohr, Z. Doleschall, Z. Prohászka, L. Cervenak, P. Z ávodszky, and P. Gál. 2009. Complement protease MASP-1 activates human endothelial cells: PAR4 activation is a link between complement and endothelial function. J. Immunol. 183: 3409-3416.
11. Jenny, L., J. Dobó, P. Gál, and V. Schroeder. 2015. MASP-1 of the complement system promotes clotting via prothrombin activation. Mol. Immunol. 65: 398-405.
12. Takahashi, M., Y. Ishida, D. Iwaki, K. Kanno, T. Suzuki, Y. Endo, Y. Homma, and T. Fujita. 2010. Essential role of mannose-binding lectin-associated serine protease-1 in activation of the complement factor D. J. Exp. Med. 207: 29-37.
13. Iwaki, D., K. Kanno, M. Takahashi, Y. Endo, M. Matsushita, and T. Fujita. 2011. The role of mannose-binding lectin-associated serine protease-3 in activation of the alternative complement pathway. J. Immunol. 187: 3751-3758.
14. Forneris, F., D. Ricklin, J. Wu, A. Tzekou, R. S. Wallace, J. D. Lambris, and P. Gros. 2010. Structures of C3b in complex with factors B and D give insight into complement convertase formation. Science 330: 1816-1820.
15. Lesavre, P. H., and H. J. Müller-Eberhard. 1978. Mechanism of action of factor D of the alternative complement pathway. J. Exp. Med. 148: 1498-1509.
16. Johnson, D. M., J. Gagnon, and K. B. Reid. 1980. Factor D of the alternative pathway of human complement. Purification, alignment and N-terminal amino acid sequences of the major cyanogen bromide fragments, and localization of the serine residue at the active site. Biochem. J. 187: 863-874.
17. Fearon, D. T., K. F. Austen, and S. Ruddy. 1974. Properdin factor D: characterization of its active site and isolation of the precursor form. J. Exp. Med. 139: 355-366.
18. Volanakis, J. E., and S. V. Narayana. 1996. Complement factor D, a novel serine protease. Protein Sci. 5: 553-564.
19. Barnum, S. R., and J. E. Volanakis. 1985. In vitro biosynthesis of complement protein D by U937 cells. J. Immunol. 134: 1799-1803.
20. Kim, S., S. V. Narayana, and J. E. Volanakis. 1994. Mutational analysis of the substrate binding site of human complement factor D. Biochemistry 33: 14393-14399.
21. Yamauchi, Y., J. W. Stevens, K. J. Macon, and J. E. Volanakis. 1994. Recombinant and native zymogen forms of human complement factor D. J. Immunol. 152: 3645-3653.
22. 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.
23. Degn, S. E., J. C. Jensenius, and S. Thiel. 2014. The pro-factor D cleaving activity of MASP-1/-3 is not required for alternative pathway function. J. Immunol. 192: 5447-5448.
24. Takahashi, M., H. Sekine, and T. Fujita. 2014. Comment on "the pro-factor D cleaving activity of MASP-1/-3 is not required for alternative pathway function". J. Immunol. 192: 5448-5449.
25. Ruseva, M. M., M. Takahashi, T. Fujita, and M. C. Pickering. 2014. C3 dysregulation due to factor H deficiency is mannan-binding lectin-associated serine proteases (MASP)-1 and MASP-3 independent in vivo. Clin. Exp. Immunol. 176: 84-92.
26. Dobó, J., V. Harmat, E. Sebestyén, L. Beinrohr, P. Závodszky, and P. Gál. 2008. Purification, crystallization and preliminary X-ray analysis of human mannose-binding lectin-associated serine protease-1 (MASP-1) catalytic region. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 64: 781-784.
27. 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.
28. Megyeri, M., P. K. Jani, E. Kajdácsi, J. Dobó, E. Schwaner, B. Major, J. Rigó, Jr., P. Z ávodszky, S. Thiel, L. Cervenak, and P. Gál. 2014. Serum MASP-1 in complex with MBL activates endothelial cells. Mol. Immunol. 59: 39-45.
29. Gál, P., V. Harmat, A. Kocsis, T. Bián, L. Barna, G. Ambrus, B. Végh, J. Balczer, R. B. Sim, G. Náray-Szabó, and P. Závodszky. 2005. A true autoactivating enzyme. Structural insight into mannose-binding lectin-associated serine protease-2 activations. J. Biol. Chem. 280: 33435-33444.
30. Héja, D., V. Harmat, K. Fodor, M. Wilmanns, J. Dobó, K. A. Kékesi, P. Z ávodszky, 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.
31. 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.
32. 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.
33. Petersen, T. N., S. Brunak, G. von Heijne, and H. Nielsen. 2011. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 8: 785-786.
34. Wu, X., I. Hutson, A. Akk, C. Pham, D. Hourcade, C. Harris, and J. P. Atkinson. 2015. Factor D deficiency in a genetically mutant mouse strain that lacks adipose tissue (15th European Meeting on Complement in Human Disease 2015, Uppsala, Sweden). Mol. Immunol. 67: 195.
35. Takahashi, M., H. Sekine, Y. Endo, W. J. Schwaeble, and T. Fujita. 2014. MASP-3 is the main converting enzyme for complement factor D (XXV International Complement Workshop, 2014, Rio de Janeiro, Brazil). Mol. Immunol. 61: 280-281.
36. 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.
37. 2-macroglobulin is not. Mol. Immunol. 54: 415-422.
38. Hansen, C. B., D. Csuka, L. Munthe-Fog, L. Varga, H. Farkas, K. M. Hansen, C. Koch, K. Skjødt, P. Garred, and M.-O. Skjoedt. 2015. 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. J. Immunol. 195: 3596-3604.
39. 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.