Structures of complement component C3 provide insights into the function and evolution of immunity

Nature

Volumn 437, Issue 7058, 2005, Pages 505-511

  Janssen, Bert J C ^a   Huizinga, Eric G ^a   Raaijmakers, Hans C A ^a   Roos, Anja ^b   Daha, Mohamed R ^b   Nilsson Ekdahl, Kristina ^c,d   Nilsson, Bo ^c   Gros, Piet ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UPPSALA UNIVERSITY HOSPITAL   (Sweden)

^d LINNAEUS UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTIVE SYSTEMS; CRYSTAL STRUCTURE; ESTERS; HYDROLYSIS;

ADAPTIVE IMMUNITY; MAMMALIAN COMPLEMENT SYSTEM; THIOESTER GROUP;

IMMUNIZATION;

ALPHA 2 MACROGLOBULIN; COMPLEMENT COMPONENT C3; COMPLEMENT COMPONENT C3C; THIOESTER; CLASSICAL COMPLEMENT PATHWAY C3 C5 CONVERTASE;

MEDICINE;

ALPHA CHAIN; ARTICLE; BETA CHAIN; COMPLEMENT ACTIVATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; COVALENT BOND; CRYSTAL STRUCTURE; EVOLUTION; HUMAN; IMMUNITY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; PROTEIN INTERACTION; PROTEIN STRUCTURE; REGULATORY MECHANISM; BIOLOGICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; IMMUNOLOGY; METABOLISM; MOLECULAR EVOLUTION; PROTEIN TERTIARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

MAMMALIA;

COMPLEMENT ACTIVATION; COMPLEMENT C3; COMPLEMENT C3-C5 CONVERTASES; COMPLEMENT C3C; CRYSTALLOGRAPHY, X-RAY; EVOLUTION, MOLECULAR; HUMANS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; PROTEIN STRUCTURE, TERTIARY;

EID: 25644452794     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature04005     Document Type: Article

References (51)

1. Carroll, M. C. The complement system in regulation of adaptive immunity. Nature Immunol. 5, 981-986 (2004).
2. Walport, M. J. Complement. First of two parts. N. Engl. J. Med. 344, 1058-1066 (2001);
3. Complement. Second of two parts. N. Engl. J. Med. 344, 1140-1144 (2001).
4. Sunyer, J. O., Zarkadis, I. K. & Lambris, J. D. Complement diversity: a mechanism for generating immune diversity? Immunol. Today 19, 519-523 (1998).
5. Levashina, E. A. et al. Conserved role of a complement-like protein in phagocytosis revealed by dsRNA knockout in cultured cells of the mosquito, Anopheles gambiae. Cell 104, 709-718 (2001).
6. Budd, A., Blandin, S., Levashina, E. A. & Gibson, T. J. Bacterial α2-macroglobulins: colonization factors acquired by horizontal gene transfer from the metazoan genome? Genome Biol. 5, R38 (2004).
7. Bokisch, V. A., Muller-Eberhard, H. J. & Cochrane, C. G. Isolation of a fragment (C3a) of the third component of human complement containing anaphylatoxin and chemotactic activity and description of an anaphylatoxin inactivator of human serum. J. Exp. Med. 129, 1109-1130 (1969).
8. Tack, B. F., Harrison, R. A., Janatova, J., Thomas, M. L. & Prahl, J. W. Evidence for presence of an internal thiolester bond in third component of human complement. Proc. Natl Acad. Sci. USA 77, 5764-5768 (1980).
9. Lambris, J. D. The multifunctional role of C3, the third component of complement. Immunol. Today 9, 387-393 (1988).
10. Law, S. K., Lichtenberg, N. A. & Levine, R. P. Evidence for an ester linkage between the labile binding site of C3b and receptive surfaces. J. Immunol. 123, 1388-1394 (1979).
11. Muller-Eberhard, H. J. & Gotze, O. C3 proactivator convertase and its mode of & action. J. Exp. Med. 135, 1003-1008 (1972).
12. Fishelson, Z., Pangburn, M. K. & Muller-Eberhard, H. J. Characterization of the initial C3 convertase of the alternative pathway of human complement. J. Immunol. 132, 1430-1434 (1984).
13. Pangburn, M. K., Schreiber, R. D. & Muller-Eberhard, H. J. Human complement C3b inactivator: isolation, characterization, and demonstration of an absolute requirement for the serum protein β1H for cleavage of C3b and C4b in solution. J. Exp. Med. 146, 257-270 (1977).
14. Ross, G. D., Lambris, J. D., Cain, J. A. & Newman, S. L. Generation of three different fragments of bound C3 with purified factor I or serum. I. Requirements for factor H vs CR1 cofactor activity. J. Immunol. 129, 2051-2060 (1982).
15. Seya, T., Turner, J. R. & Atkinson, J. P. Purification and characterization of a membrane protein (gp45-70) that is a cofactor for cleavage of C3b and C4b. J. Exp. Med. 163, 837-855 (1986).
16. Harrison, R. A. & Lachmann, P. J. Novel cleavage products of the third component of human complement. Mol. Immunol. 17, 219-228 (1980).
17. Lachmann, P. J., Pangburn, M. K. & Oldroyd, R. G. Breakdown of C3 after complement activation. Identification of a new fragment C3g, using monoclonal antibodies. J. Exp. Med. 156, 205-216 (1982).
18. Collaborative Computational Project, Number 4, The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D 50, 760-763 (1994).
19. Nagar, B., Jones, R. G., Diefenbach, R. J., Isenman, D. E. & Rini, J. M. X-ray crystal structure of C3d: a C3 fragment and ligand for complement receptor 2. Science 280, 1277-1281 (1998).
20. Storoni, L. C., McCoy, A. J. & Read, R. J. Likelihood-enhanced fast rotation functions. Acta Crystallogr. D 60, 432-438 (2004).
21. de Bruijn, M. H. & Fey, G. H. Human complement component C3: cDNA coding sequence and derived primary structure. Proc. Natl Acad. Sci. USA 82, 708-712 (1985).
22. Huber, R., Scholze, H., Paques, E. P. & Deisenhofer, J. Crystal structure analysis and molecular model of human C3a anaphylatoxin. Hoppe-Seyler's Z. Physiol. Chem. 361, 1389-1399 (1980).
23. Jenner, L., Husted, L., Thirup, S., Sottrup-Jensen, L. & Nyborg, J. Crystal structure of the receptor-binding domain of α2-macroglobulin. Structure 6, 595-604 (1998).
24. Thomas, M. L., Janatova, J., Gray, W. R. & Tack, B. F. Third component of human complement: localization of the internal thiolester bond. Proc. Natl Acad. Sci. USA 79, 1054-1058 (1982).
25. Bramham, J. et al. Functional insights from the structure of the multifunctional C345C domain of C5 of complement. J. Biol. Chem. 280, 10636-10645 (2005).
26. Taniguchi-Sidle, A. & Isenman, D. E. Interactions of human complement component C3 with factor B and with complement receptors type 1 (CR1, CD35) and type 3 (CR3, CD11b/CD18) involve an acidic sequence at the N-terminus of C3 alpha'-chain. J. Immunol. 153, 5285-5302 (1994).
27. Sottrup-Jensen, L., Sand, O., Kristensen, L. & Fey, G. H. The α-macroglobulin bait region. Sequence diversity and localization of cleavage sites for proteinases in five mammalian α-macroglobulins. J. Biol. Chem. 264, 15781-15789 (1989).
28. Lagueux, M., Perrodou, E., Levashina, E. A., Capovilla, M. & Hoffmann, J. A. Constitutive expression of a complement-like protein in toll and JAK gain-of-function mutants of Drosophila. Proc. Natl Acad. Sci. USA 97, 11427-11432 (2000).
29. Ishii, N., Wadsworth, W. G., Stern, B. D., Culotti, J. G. & Hedgecock, E. M. UNC-6, a laminin-related protein, guides cell and pioneer axon migrations in C. elegans. Neuron 9, 873-881 (1992).
30. Sahu, A. & Lambris, J. D. Structure and biology of complement protein C3, a connecting link between innate and acquired immunity. Immunol. Rev. 180, 35-48 (2001).
31. Pangburn, M. K., Schreiber, R. D. & Muller-Eberhard, H. J. Formation of the initial C3 convertase of the alternative complement pathway. Acquisition of C3b-like activities by spontaneous hydrolysis of the putative thioester in native C3. J. Exp. Med. 154, 856-867 (1981).
32. Isenman, D. E., Kells, D. I., Cooper, N. R., Muller-Eberhard, H. J. & Pangburn, M. K. Nucleophilic modification of human complement protein C3: correlation of conformational changes with acquisition of C3b-like functional properties. Biochemistry 20, 4458-4467 (1981).
33. Pangburn, M. K. Spontaneous reformation of the intramolecular thioester in complement protein C3 and low temperature capture of a conformational intermediate capable of reformation. J. Biol. Chem. 267, 8584-8590 (1992).
34. Law, S. K. & Dodds, A. W. The internal thioester and the covalent binding properties of the complement proteins C3 and C4. Protein Sci. 6, 263-274 (1997).
35. Gadjeva, M. et al. The covalent binding reaction of complement component C3. J. Immunol. 161, 985-990 (1998).
36. Dodds, A. W., Ren, X. D., Willis, A. C. & Law, S. K. The reaction mechanism of the internal thioester in the human complement component C4. Nature 379, 177-179 (1996).
37. van den Elsen, J. M. et al. X-ray crystal structure of the C4d fragment of human complement component C4. J. Mol. Biol. 322, 1103-1115 (2002).
38. Qazi, U., Gettins, P. G. & Stoops, J. K. On the structural changes of native human α2-macroglobulin upon proteinase entrapment. Three-dimensional structure of the half-transformed molecule. J. Biol. Chem. 273, 8987-8993 (1998).
39. Daoudaki, M. E., Becherer, J. D. & Lambris, J. D. A 34-amino acid peptide of the third component of complement mediates properdin binding. J. Immunol. 140, 1577-1580 (1988).
40. Winters, M. S., Spellman, D. S. & Lambris, J. D. Solvent accessibility of native and hydrolyzed human complement protein 3 analyzed by hydrogen/deuterium exchange and mass spectrometry. J. Immunol. 174, 3469-3474 (2005).
41. Oran, A. E. & Isenman, D. E. Identification of residues within the 727-767 segment of human complement component C3 important for its interaction with factor H and with complement receptor 1 (CR1, CD35). J. Biol. Chem. 274, 5120-5130 (1999).
42. Lambris, J. D. et al. Dissection of CR1, factor H, membrane cofactor protein, and factor B binding and functional sites in the third complement component. J. Immunol. 156, 4821-4832 (1996).
43. Hammer, C. H., Wirtz, G. H., Renfer, L., Gresham, H. D. & Tack, B. F. Large scale isolation of functionally active components of the human complement system. J. Biol. Chem. 256, 3995-4006 (1981).
44. Otwinowski, Z. & Minor, W. Processing X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997).
45. Kabsch, W. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallogr. 26, 795-800 (1993).
46. Terwilliger, T. C. & Berendzen, J. Automated MAD and MIR structure solution. Acta Crystallogr. D 55, 849-861 (1999).
47. Kleywegt, G. J. & Jones, T. A. Software for handling macromolecular envelopes. Acta Crystallogr. D 55, 941-944 (1999).
48. Perrakis, A., Morris, R. & Lamzin, V. S. Automated protein model building combined with iterative structure refinement. Nature Strud. Biol. 6, 458-463 (1999).
49. Jones, T. A., Zou, J. Y., Cowan, S. W. & Kjeldgaard, M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47, 110-119 (1991).
50. Brunger, A. T. et al. Crystallography NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D 54, 905-921 (1998).
51. Solomon, K. R., Sharma, P., Chan, M., Morrison, P. T. & Finberg, R. W. CD109 represents a novel branch of the α2-macroglobulin/complement gene family. Gene 327, 171-183 (2004).