Crystal Structure of the catalytic domain of human complement C1s: A serine protease with a handle

EMBO Journal

Volumn 19, Issue 8, 2000, Pages 1755-1765

  Gaboriaud, Christine ^a   Rossi, Véronique ^a   Bally, Isabelle ^a   Arlaud, Gérard J ^a   Fontecilla Camps, Juan Carlos ^a  

^a CEA GRENOBLE   (France)

Author keywords

Complement; Modular structure; Molecular recognition; Serine protease; Substrate specificity

Indexed keywords

COMPLEMENT COMPONENT C1; COMPLEMENT COMPONENT C2; COMPLEMENT COMPONENT C4; POLYPEPTIDE; PROLINE; SERINE PROTEINASE; TYROSINE;

ARTICLE; COMPLEMENT ACTIVATION; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME SUBSTRATE COMPLEX; EXTRACELLULAR SPACE; HUMAN; HUMAN CELL; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN TERTIARY STRUCTURE;

EID: 0034678903     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/19.8.1755     Document Type: Article

References (66)

1. Arlaud, G.J. and Thielens, N. (1993) Human complement serine proteases C1r and C1s and their proenzymes. Methods Enzymol., 223, 61-82.
2. Arlaud, G.J., Colomb, M.G. and Gagnon, J. (1987) A functional model of the human Cl complex. Immunol. Today, 8, 106-111.
3. Arlaud, G.J., Volanakis, J.E., Thielens, N.M., Narayana, S.V.L., Rossi, V. and Xu, Y, (1998) The atypical serine proteases of the complement system. Adv. Immunol., 69, 249-307.
4. Banner, D.W., D'Arcy, A., Chene, C., Winkler, F.K., Guha, A., Konigsherg, W.H., Nemerson, Y. and Kirchhofer, D. (1996) The crystal structure of the complex of blood coagulation factor VIIa with soluble tissue factor. Nature, 380, 41-46.
5. Barlow, P.N., Norman, D.G., Steinkasserer, A., Horne, T.J., Pearce, J., Driscoll, P.C., Sim, R.B. and Campbell, I.D. (1992) Solution structure of the fifth repeat of factor H: a second example of the complement control protein module. Biochemistry, 31, 3626-3634.
6. Barlow, P.N., Steinkasserer, A., Norman, D.G., Kieffer, B., Wiles, A.P., Sim, R.B. and Campbell, I.D. (1993) Solution structure of a pair of complement modules by nuclear magnetic resonance. J. Mol. Biol., 232, 268-284.
7. Bateman, A., Birney, E., Durbin, R., Eddy, S.R., Finn, R.D. and Sonnhammer, E.L. (1999) Pfam 3.1: 1313 multiple alignments and profile HMMs match the majority of proteins. Nucleic Acids Res., 27, 260-262.
8. Bernstein, F.C., Koetzle, T.F., Williams, G.J., Meyer, E.E., Jr. Brice, M.D., Rodgers, J.R., Kennard, O., Shimanouchi, T. and Tasumi, M. (1977) The Protein Data Bank: a computer-based archival file for macromolecular structures. J. Mol. Biol., 112, 535-542.
9. Bode, W. and Huber, R. (1992) Natural protein proteinase inhibitors and their interaction with proteinases. Eur. J. Biochem., 204, 433-451.
10. Bode, W., Brandstetter, H., Mather, T. and Stubbs, M.T. (1997) Comparative analysis of haemostatic proteinases: structural aspects of thrombin, factor Xa, factor IXa and protein C. Thromb. Haemost., 78, 501-511.
11. Bork, P. and Beckmann, G. (1993) The CUB domain. A widespread module in developmentally regulated proteins. J. Mol. Biol., 231, 539-545.
12. Brandstetter, H., Bauer, M., Huber, R., Lollar, P. and Bode, W. (1995) X-ray structure of clotting factor IXa: active site and module structure related to Xase activity and hemophilia B. Proc. Natl Acad. Sci. USA, 92, 9796-9800.
13. Brünger, A.T. (1992) X-PLOR version 3.1, a System for X-ray Crystallography and NMR. Yale University Press, New Haven, CT.
14. Burmeister, W.P. (2000) Structural changes in a cryo-cooled protein crystal due to radiation damage. Acta Crystallogr. D, 56, 328-341.
15. Casasnovas, J.M., Larvie, M. and Stehle, T. (1999) Crystal structure of two CD46 domains reveals an extended measles virus-binding surface. EMBO J., 18, 2911-2922.
16. Cooper, N.R. (1985) The classical complement pathway: activation and regulation of the first complement component. Adv. Immunol., 37, 151-216.
17. Dalmasso, A.P. (1992) The complement system in xenotransplantation. Immunopharmacology, 24, 149-160.
18. +-induced allosteric regulation of catalytic activity in serine proteases. Proc. Natl Acad. Sci. USA, 93, 10653-10656.
19. Dobryszycka, W. (1997) Biological functions of haptoglobin - new pieces to an old puzzle. Eur. J. Clin. Chem. Clin. Biochem., 35, 647-654.
20. Endo, Y., Takahashi, M., Nakao, M., Saiga, H., Sekine, H., Matsushita, M., Nonaka, M. and Fujita, T. (1998) Two lineages of mannose-binding lectin-associated serine protease (MASP) in vertebrates. J. Immunol., 161, 4924-4930.
21. Gaboriaud, C., Rossi, V., Fontecilia-Camps, J.C. and Arlaud, G.J. (1998) Evolutionary conserved rigid module-domain interactions can be detected at the sequence level: the examples of complement and blood coagulation proteases. J. Mol. Biol., 282, 459-470.
22. Gans, P., Rossi, V., Gaboriaud, C., Bally, I., Hernandez, J.F., Blackledge, M.J. and Arlaud, G.J. (1998) NMR structures of the C-terminal end of human complement serine protease C1s. Cell. Mol. Life Sci., 54, 171-178.
23. Guinto, E.R., Caccia, S., Rose, T., Fütterer, K., Waksman, G. and Di Cera, E. (1999) Unexpected crucial role of residue 225 in serine proteases. Proc. Natl Acad. Sci. USA, 96, 1852-1857.
24. Hubbard, S.J. and Thornton, J.M. (1993) 'NACCESS', Computer Program. Department of Biochemistry and Molecular Biology, University College London, UK.
25. Hwang, P.K. and Greer, J. (1980) Interaction between hemoglobin subunits in the hemoglobin.haptoglobin complex. J. Biol. Chem., 255, 3038-3041.
26. Jing, H., Macon, K., Moore, D., DeLucas, L.J., Volanakis, J.E. and Narayana, S.V.L. (1999) Structural basis of profactor D activation: from a highly flexible zymogen to a novel self-inhibited serine protease, complement factor D. EMBO J., 18, 804-814.
27. Jones, T.A, Zou, J.-Y., Cowan, S.W. and Kjeldgaard, M. (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A, 47, 110-119.
28. Kabsch, W. (1993) Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallogr., 26, 795-800.
29. Kirkitadze, M.D. et al. (1999) Independently melting modules and highly structured intermodular junctions within complement receptor type 1. Biochemistry, 38, 7019-7031.
30. Kraulis, P.J. (1991) MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr., 24, 946-950.
31. Lacroix, M., Rossi, V., Gaboriaud, C., Chevallier, S., Jaquinod, M., Thielens, N.M., Gagnon, J. and Arlaud, G.J. (1997) Structure and assembly of the catalytic region of human complement protease C1r: a three-dimensional model based on chemical cross-linking and homology modeling. Biochemistry, 36, 6270-6282.
32. Lamzin, V. and Wilson, K. (1993) Automated refinement of protein model. Acta Crystallogr. D, 49, 129-147.
33. Laskowski, R.A., MacArthur, M.W., Moss, D.S. and Thornton, J.M. (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr., 26, 283-291.
34. Mackinnon, C.M., Carter, P.E., Smyth, S.J., Dunbar, B. and Fothergill, J.E. (1987) Molecular cloning of cDNA for human complement component C1s. The complete amino acid sequence. Eur. J. Biochem., 169, 547-553.
35. Mather, T., Oganessyan, V., Hof, P., Huber, R., Foundling, S., Esmon, C. and Bode, W. (1996) The 2.8 Å crystal structure of Gla-domainless activated protein C. EMBO J., 15, 6822-6831.
36. Matsushita, M., Endo, Y., Nonaka, M. and Fujita, T. (1998) Complement-related serine proteases in tunicates and vertebrates. Curr. Opin. Immunol., 10, 29-35.
37. McDonald, I.K. and Thornton, J.M. (1994) Satisfying hydrogen bonding potential in proteins. J. Mol. Biol., 238, 777-793.
38. Merritt, E.A. and Bacon, D.J. (1997) Raster3D photorealistic molecular graphics. Methods Enzymol., 277, 505-524.
39. Mevorach, D., Mascarenhas, J.O., Gershov, D. and Elkon, K.B. (1998) Complement-dependent clearance of apoptotic cells by human macrophages. J. Exp. Med., 188, 2313-2320.
40. Murshudov, G.N., Vagin, A.A. and Dodson, E.J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D, 53, 240-255.
41. Muta, T., Miyata, T., Misumi, Y., Tokunaga, F., Nakamura, T., Toh, Y., Ikehara, Y. and Iwanaga, S. (1991) Limulus factor C. An endotoxin-sensitive serine protease zymogen with a mosaic structure of complement-like, epidermal growth factor-like and lectin-like domains. J. Biol. Chem., 26, 6554-6561.
42. Navaza, J. (1994) AMoRe: an automated package for molecular replacement. Acta Crystallogr. A, 50, 157-163.
43. Nicholls, A., Sharp, K.A. and Honig, B. (1991) Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins, 11, 281-296.
44. Padmanabhan, K., Padmanabhan, K.P., Tulinsky, A., Park, C.H., Bode, W., Huber, R., Blankenship, D.T., Cardin, A.D. and Kisiel, W. (1993) Structure of human Des (1-45) factor Xa at 2.2 Å resolution. J. Mol. Biol., 232, 947-966.
45. Parry, M.A, Fernandez-Catalan, C., Bergner, A., Huber, R., Hopfner, K.P., Schlott, B., Guhrs, K.H. and Bode, W. (1998) The ternary microplasmin-staphylokinase-microplasmin complex is a proteinase-cofactor-substrate complex in action. Nature Struct. Biol., 10, 917-923.
46. Perona, J.J. and Craik, C.S. (1997) Evolutionary divergence of substrate specificity within the chymotrypsin-like serine protease fold. J. Biol. Chem., 272, 29987-29990.
47. Perrakis, A., Morris, R. and Lamzin, V.S. (1999) Automated protein model building combined with iterative structure refinement. Nature Struct. Biol., 6, 458-463.
48. Pétillot., Y. et al. (1995) Analysis of the N-linked oligosaccharides of human CIs using electrospray ionisation mass spectrometry. FEBS Lett., 358, 323-328.
49. Reid, K.B.M. and Day, A.J. (1989) Structure-function relationships of the complement components. Immunol. Today, 10, 177-180.
50. Rogers, J. et al. (1992) Complement activation by β-amyloid in Alzheimer disease. Proc. Natl Acad. Sci. USA, 89, 10016-10020.
51. Rossi, V., Gaboriaud, C., Lacroix, M., Ulrich, J., Fontecilla-Camps, J.C., Gagnon, J. and Arlaud, G.J. (1995) Structure of the catalytic region of human complement protease C1s: study by chemical cross-linking and three-dimensional homology modeling. Biochemistry, 34, 7311-7321.
52. Rossi, V., Bally, I., Thielens, N.M., Esser, A.F. and Arlaud, G.J. (1998) Baculovirus-mediated expression of truncated modular fragments from the catalytic region of human complement serine protease C1s. Evidence for the involvement of both complement control protein modules in the recognition of the C4 protein substrate. J. Biol. Chem., 273, 1232-1239.
53. Sato, T., Endo, Y., Matsushita, M. and Fujita, T. (1994) Molecular characterization of a novel serine protease involved in activation of the complement system by mannose-binding protein. Int. Immunol., 6, 665-669.
54. Schumaker, V.N., Hanson, D.C., Kilchherr, E., Phillips, M.L. and Poon, P.H. (1986) A molecular mechanism for the activation of the first component of complement by immune complexes. Mol. Immunol, 23, 557-565.
55. Smith, A.B., Esko, J.D. and Hajduk, S.L. (1995) Killing of trypanosomes by the human haptoglobin related protein. Science, 268, 284-286.
56. Thiel, S. et al. (1997) A second serine protease associated with mannan-binding lectin that activates complement. Nature, 386, 506-510.
57. 2-terminal α fragments of human complement proteases C1r and C1s. J. Biol. Chem., 265, 14469-14475.
58. Tosi, M, Duponchel, C., Meo, T. and Julier, C. (1987) Complete cDNA sequence of human complement C1s and close physical linkage of the homologous genes C1s and C1r. Biochemistry, 26, 8516-8524.
59. Tosi, M., Duponchel, C., Meo, T. and Couture-Tosi, E. (1989) Complement genes C1r and C1s feature an intronless serine protein domain closely related to haptoglobin. J. Mol. Biol., 208, 709-714.
60. van de Locht, A., Bode, W., Huber, R., Le Bonniec, B.F., Stone, S.R., Esmon, C.T. and Stubbs, M.T. (1997) The thrombin E192Q-BPTI complex reveals gross structural rearrangements: implications for the interaction with antithrombin and thrombomodulin. EMBO J., 16, 2977-2984.
61. Vernède, X. and Fontecilla-Camps, J.C. (1999) A method to stabilize reduced and/or gas-treated protein crystals by flash-cooling under a controlled atmosphere. J. Appl. Crystallogr., 32, 505-509.
62. Volanakis, J.E. and Narayana, S.V.L. (1996) Complement factor D, a novel serine protease. Protein Sci., 5, 553-564.
63. Wallace, A.C., Laskowski, R.A. and Thornton, J.M. (1995) LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions. Protein Eng., 8, 127-134.
64. Weiss, V., Fauser, C. and Engel, J. (1986) Functional model of sub-component Cl of human complement. J. Mol. Biol., 189, 573-581.
65. Wiles, A.P., Shaw, G., Bright, J., Perczel, A., Campbell, I.D. and Barlow, P.N. (1997) NMR studies of a viral protein that mimics the regulators of complement activation. J. Mol. Biol., 272, 253-265.
66. Zahedi, R., Wisnieski, J. and Davis, A.E., III (1997) Role of the P2 residue of complement 1 inhibitor (Ala443) in determination of target protease specificity: inhibition of complement and contact system proteases. J. Immunol., 159, 983-988.