Revisiting the mechanism of the autoactivation of the complement protease C1r in the C1 complex: Structure of the active catalytic region of C1r

Molecular Immunology

Volumn 45, Issue 6, 2008, Pages 1752-1760

  Kardos, József ^a,b   Harmat, Veronika ^a   Palló, Anna ^a,d   Barabás, Orsolya ^a   Szilágyi, Katalin ^b   Gráf, László ^a   Náray Szabó, Gábor ^a   Goto, Yuji ^c   Závodszky, Péter ^b   Gál, Péter ^b  

^a EÖTVÖS LORÁND UNIVERSITY   (Hungary)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^c OSAKA UNIVERSITY   (Japan)

^d CHEMICAL RESEARCH CENTER   (Hungary)

Author keywords

C1r catalytic domain; Complement control protein; Complement system; Mechanism of C1r autoactivation; Modular serine protease

Indexed keywords

ARGININE; ASPARTIC ACID; ENZYME; ENZYME PRECURSOR; SERINE PROTEINASE;

AMINO TERMINAL SEQUENCE; ARTICLE; CATALYSIS; COMPLEMENT ACTIVATION; COMPLEX FORMATION; CRYSTAL STRUCTURE; CRYSTALLIZATION; HUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN STRUCTURE;

CATALYTIC DOMAIN; COMPLEMENT C1R; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; HUMANS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 38949188247     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2007.09.031     Document Type: Article

References (40)

1. Ambrus G., Gál P., Kojima M., Szilágyi K., Balczer J., Antal J., Gráf L., Laich A., Moffatt B., Schwaeble W., Sim R.B., and Závodszky P. Natural substrates and inhibitors of mannan-binding lectin-associated serine protease-1 and -2: a study on recombinant catalytic fragments. J. Immunol. 170 (2003) 1374-1382
2. Arlaud G.J., Barlow P.N., Gaboriaud C., Gros P., and Narayana S.V.L. Deciphering complement mechanisms: the contributions of structural biology. Mol. Immunol. 44 (2007) 3809-3822
3. Arlaud G.J., Chesne S., Villiers C.L., and Colomb M.G. A study on the structure and interactions of the C1 subcomponents C1r and C1s in the fluid phase. Biochem. Biophys. Acta 616 (1980) 105-115
4. Arlaud G.J., Gaboriaud C., Thielens N.M., Rossi V., Bersch B., Hernandez J.-F., and Fontecilla-Camps J.C. Structural biology of C1: dissection of a complex molecular mashinery. Immunol. Rev. 180 (2001) 136-145
5. Arlaud G.J., Gagnon J., Villiers C.L., and Colomb M.G. Molecular characterization of the catalytic domains of human complement serine protease C1r. Biochemistry 25 (1986) 5177-5182
6. Beinrohr L., Harmat V., Dobó J., Lo{combining double acute accent}rincz Zs., Gál P., and Závodszky P. C1 inhibitor serpin domain structure reveals the likely mechanism of heparin potentiation and conformational disease. J. Biol. Chem. 282 (2007) 21100-21109
7. Berman H.M., Westbrook J., Feng Z., Gilliland G., Bhat T.N., Weissig H., Shindyalov I.N., and Bourne P.E. The Protein Data Bank. Nucleic Acids Res. 28 (2000) 235-242
8. Bersch B., Hernandez J._F., Marion D., and Arlaud G.J. Solution structure of the epidermal growth factor-like module of human complement protease C1r, an atypical member of the EGF family. Biochemistry 37 (1998) 1204-1214
9. Budayova-Spano M., Grabarse W., Thielens N.M., Hillen H., Lacroix M., Schmidt M., Fontecilla-Camps J.C., Arlaud G.J., and Gaboriaud C. Monomeric structures of the zymogen and active catalytic domain of complement protease C1r: further insights into the C1 activation mechanism. Structure 10 (2002) 1509-1519
10. Budayova-Spano M., Lacroix M., Thielens N.M., Arlaud G.J., Fontecilla-Camps J.C., and Gaboriaud C. The crystal structure of the zymogen catalytic domain of complement protease C1r reveals that a disruptive mechanical stress is required to trigger activation of the C1 complex. EMBO J. 21 (2002) 231-239
11. 2-terminal calcium-binding domain of human complement C1s mediates the interaction of C1r with C1q. Biochemistry 29 (1990) 4613-4618
12. Collaborative Computational Project, Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D50 (1994) 760-763
13. DeLano W.L. The PyMOL Molecular Graphics System (2002), DeLano Scientific, San Carlos, CA, USA
14. Dobó J., Gál P., Szilágyi K., Cseh S., Lo{combining double acute accent}rincz Zs., Schumaker V.N., and Závodszky P. One active C1r subunit is sufficient for the activity of the complement c1 complex: stabilization of C1r in the zymogen form by point mutations. J. Immunol. 162 (1999) 1108-1112
15. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D60 (2004) 2126-2132
16. Evans P.R. Data reduction. Proceedings of the CCP4 Study Weekend on Data Collection and Processing (1993), CLRC Daresbury Laboratory, UK 114-122
17. Gaboriaud C., Juanhuix J., Gruez A., Lacroix M., Darnault C., Pignol D., Verger D., Fontecilla-Camps J.C., and Arlaud G.J. The crystal structure of the globular head of complement protein C1q provides a basis for its versatile recognition properties. J. Biol. Chem. 278 (2003) 46974-46982
18. Gaboriaud C., Rossi V., Bally I., Arlaud G.J., and Fontecilla-Camps J.C. Crystal structure of the catalytic domain of human complement C1s: a serine protease with a handle. EMBO J. 19 (2000) 1755-1765
19. Gaboriaud C., Thielens N.M., Gregory L.A., Rossi V., Fontecilla-Camps J.C., and Arlaud G.J. Structure and activation of the C1 complex of complement: unraveling the puzzle. Trends Immunol. 25 (2004) 368-373
20. Gál P., Barna L., Kocsis A., and Závodszky P. Serine proteases of the classical and lectin pathways: similarities and differences. Immunobiology 212 (2007) 267-277
21. Gál P., Harmat V., Kocsis A., Bián T., Barna L., Ambrus G., Végh B., Balczer J., Sim R.B., Náray-Szabó G., and Závodszky P. A true autoactivating enzyme. Structural insights into mannose-binding lectin-associated serine protease-2 activation. J. Biol. Chem. 280 (2005) 33435-33444
22. Gál P., Sárvári M., Szilágyi K., Závodszky P., and Schumaker V.N. Expression of hemolytically active human complement component C1r in insect cells using a baculovirus vector. Complement Inflamm. 6 (1989) 433-441
23. 2+-binding interaction domain of C1s. Insights into the assembly of the C1 complex of complement. J. Biol. Chem. 278 (2003) 32157-32164
24. Guex N., and Peitsch M.C. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18 (1997) 2714-2723
25. Kardos J., Gál P., Szilágyi L., Thielens N.M., Szilágyi K., Lo{combining double acute accent}rincz Zs., Kulcsár P., Gráf L., Arlaud G.J., and Závodszky P. The role of the individual domains in the structure and function of the catalytic region of a modular serine protease C1r. J. Immunol. 167 (2001) 5202-5208
26. Lacroix M., Ebel C., Kardos J., Dobó J., Gál P., Závodszky P., Arlaud G.J., and Thielens N.M. Assembly and enzymatic properties of the catalytic domain of human complement protease C1r. J. Biol. Chem. 276 (2001) 36233-36240
27. Laskowski R.A., MacArthur M.W., Moss D.S., and Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26 (1993) 283-291
28. Lee B., and Richards F.M. The interpretation of protein structures: estimation of static accessibility. J. Mol. Biol. 55 (1971) 379-400
29. Leslie, A.G.W., 1992. Recent changes to the MOSFLM package for processing film and image plate data. Joint CCP4 + ESF-EAMCB Newsletter on Protein Crystallography, No. 26.
30. Lorand, L., Mann, K.G., 1993. Proteolytic enzymes in coagulation, fibrinolysis, and complement activation. Methods Enzymol., v222. Academic Press, San Diego.
31. Murshudov G.N., Vagin A.A., and Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D53 (1997) 240-255
32. Perkins S.J. Models for the C1 complex determined by physical techniques. Behring Inst. Mitt. 84 (1989) 129-141
33. Perona J.J., and Craik C.S. Evolutionary divergence of substrate specificity within the chymotrypsin-like serine protease fold. J. Biol. Chem. 272 (1997) 29987-29990
34. Read R.J. Pushing the boundaries of molecular replacement with maximum likelihood. Acta Cryst. D57 (2001) 1373-1382
35. Rossi V., Bally I., Thielens N.M., Esser A.F., and Arlaud G.J. Baculovirus mediated expression of truncated modular fragments from the catalytic region of human complement serine protease C1s. Evidence for the involvment of both complement control protein modules in the recognition of the C4 protein substrate. J. Biol. Chem. 273 (1998) 1232-1239
36. Rossi V., Teillet F., Thielen N.M., Bally I., and Arlaud G.J. Functional characterization of complement proteases C1s/mannan-binding lectin-associated serine protease-2 (MASP-2) chimeras reveals the higher C4 recognition efficacy of the MASP-2 complement control protein modules. J. Biol. Chem. 280 (2005) 41811-41818
37. Schumaker V.N., Závodszky P., and Poon P.H. Activation of the first component of complement. Annu. Rev. Immunol. 5 (1987) 21-42
38. Winn M., Isupov M., and Murshudov G.N. Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallogr. D57 (2001) 122-133
39. Wong N.K.H., Kojima M., Dobó J., Ambrus G., and Sim R.B. Activities of the MBL-associated serine proteases (MASPs) and their regulation by natural inhibitors. Mol. Immunol. 36 (1999) 853-861
40. Ziccardi R.J. Spontaneous activation of the first component of human complement (C1) by an intramolecular autocatalytic mechanism. J. Immunol. 128 (1982) 2500-2504