Complement inhibitor C4b-binding protein - Friend or foe in the innate immune system?

Molecular Immunology

Volumn 40, Issue 18, 2004, Pages 1333-1346

  Blom, Anna M ^a   Villoutreix, Bruno O ^b   Dahlbäck, Björn ^a  

^a LUND UNIVERSITY HOSPITAL   (Sweden)

^b INSERM   (France)

Author keywords

Activated complement factor 3; Activated complement factor 4; C3b; C4b; C4b binding protein; C4BP; CCP; Complement control protein domain; Complement receptor 1; CR1; DAF; Decay accelerating factor; EGF; Epidermal growth factor; FH; Gla; carboxyglutamic acid

Indexed keywords

COMPLEMENT COMPONENT C4 BINDING PROTEIN;

APOPTOSIS; B LYMPHOCYTE; BACTERIAL INFECTION; BINDING SITE; CATABOLISM; CELL ACTIVATION; CELL MEMBRANE; CELL SURFACE; CELL SURVIVAL; COMPUTER ANALYSIS; ELECTRON MICROSCOPY; ENDOPLASMIC RETICULUM; ENDOTHELIUM CELL; HEMOLYSIS; HUMAN; IMMUNE SYSTEM; IMMUNOPATHOGENESIS; INFLAMMATION; MACROPHAGE; MEMBRANE BINDING; MUTATION; NONHUMAN; PHAGOCYTOSIS; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; REGULATORY MECHANISM; REVIEW; RISK FACTOR; SERUM RESPONSIVE ELEMENT; WILD TYPE; XENOTRANSPLANTATION;

BORDETELLA; BORDETELLA PERTUSSIS; CANDIDA; CANDIDA ALBICANS; ESCHERICHIA COLI; NEISSERIA; NEISSERIA GONORRHOEAE; STREPTOCOCCUS PYOGENES;

EID: 1842557722     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2003.12.002     Document Type: Article

References (132)

1. Accardo P., Sanchez Corral P., Criado O., Garcia E., Rodriguez de Cordoba S. Binding of human complement component C4b-binding protein (C4BP) to Streptococcus pyogenes involves the C4b-binding site. J. Immunol. 157:1996;4935-4939.
2. Adams, E.M., Brown, M.C., Nunge, M., Krych, M., Atkinson, J.P., 1991. J. Immunol. 147, 3005-3011.
3. Åkerström B., Lindqvist A., Lindahl G. Binding properties of protein Arp, a bacterial IgA-receptor. Mol. Immunol. 28:1991;349-357.
4. Alsenz J., Lambris J.D., Schulz T.F., Dierich M.P. Localization of the complement-component-C3b-binding site and the cofactor activity for factor I in the 38. kDa tryptic fragment of factor H Biochem. J. 224:1984;389-398.
5. Anderson H.A., Maylock C.A., Williams J.A., Paweletz C.P., Shu H., Shacter E. Serum-derived protein S binds to phosphatidylserine and stimulates the phagocytosis of apoptotic cells. Science. 4:2003;87-91.
6. Andersson A., Dahlbäck B., Hanson C., Hillarp A., Levan G., Szpirer J., Szpirer C. Genes for C4b-binding protein alpha- and beta-chains (C4BPA and C4BPB) are located on chromosome 1, band 1q32, in humans and on chromosome 13 in rats. Somat. Cell. Mol. Genet. 16:1990;493-500.
7. Banchereau J., Bazan F., Blanchard D., Briere F., Galizzi J.P., van Kooten C., Liu Y.J., Rousset F., Saeland S. The CD40 antigen and its ligand. Annu. Rev. Immunol. 12:1994;881-922.
8. Barlow P.N., Steinkasserer A., Norman D.G., Kieffer B., Wiles A.P., Sim R.B., Campbell I.D. Solution structure of a pair of complement modules by nuclear magnetic resonance. J. Mol. Biol. 232:1993;268-284.
9. Barnum S.R., Dahlbäck B. C4b-binding protein, a regulatory component of the classical pathway of complement, is an acute-phase protein and is elevated in systemic lupus erythematosus. Complement Inflamm. 7:1990;71-77.
10. Berggård K., Johnsson E., Mooi F.R., Lindahl G. Bordetella pertussis binds the human complement regulator C4BP: role of filamentous hemagglutinin. Infect. Immunol. 65:1997;3638-3643.
11. Berggård K., Lindahl G., Dahlbäck B., Blom A.M. Bordetella pertussis binds to human C4b-binding protein (C4BP) at a site similar to that used by the natural ligand C4b. Eur. J. Immunol. 31:2001;2771-2780.
12. Blom A.M., Berggård K., Webb J.H., Lindahl G., Villoutreix B.O., Dahlbäck B. Human C4b-binding protein has overlapping but not identical binding sites for C4b and streptococcal M proteins. J. Immunol. 164:2000a;5328-5336.
13. Blom A.M., Covell D.G., Wallqvist A., Dahlbäck B., Villoutreix B.O. The C4b-binding protein-protein S interaction is hydrophobic in nature. Biochim. Biophys. Acta. 1388:1998;181-189.
14. Blom A.M., Foltyn-Zadura A., Villoutreix B.O., Dahlbäck B. Positively charged amino acids at the interface between α-chain CCP1 and CCP2 of C4BP are required for regulation of the classical C3-convertase. Mol. Immunol. 37:2000b;445-453.
15. Blom A.M., Kask L., Dahlbäck B. Structural requirements for the complement regulatory activities of C4BP. J. Biol. Chem. 276:2001a;27136-27144.
16. Blom A.M., Kask L., Dahlbäck B. CCP1-4 of the C4b-binding protein a-chain are required for factor I mediated cleavage of C3b. Mol. Immunol. 39:2003a;547-556.
17. Blom, A.M., Kask, L., Ramesh, B., Hillarp, A., 2003b. Regulation of factor I cofactor activity of C4b-protein and factor H by zinc. Arch. Biochem. Biophys. 418, 108-118.
18. Blom A.M., Rytkönen A., Vasquez P., Lindahl G., Dahlbäck B., Jonsson A.-B. A novel interaction between type IV pili of Neisseria gonorrhoeae and the human complement regulator C4b-binding protein. J. Immunol. 166:2001b;6764-6770.
19. Blom A.M., Webb J., Villoutreix B.O., Dahlbäck B. A cluster of positively charged amino acids in the N-terminal modules of the C4BP a-chain is crucial for C4b binding and factor I cofactor function. J. Biol. Chem. 274:1999;19237-19245.
20. Boerger L.M., Morris P.C., Thurnau G.R.T.E.C., Comp P.C. Oral contraceptives and gender affect protein S status. Blood. 69:1987;692-694.
21. Brodbeck W.G., Liu D., Sperry J., Mold C., Medof M.E. Localization of classical and alternative pathway regulatory activity within the decay accelerating factor. J. Immunol. 156:1996;2528-2533.
22. Brodeur S., Angelini F., Bacharier L.B., Blom A.M., Mizoguchi E., Fujiwara H., Dahlbäck B., Plebani A., Tsitsikov E., Geha R.S. C4b-binding protein (C4BP) activates B cells through the CD40 receptor. Immunity. 18:2003;837-848.
23. Burge J., Nicholson-Weller A., Austen K.F. Isolation of C4-binding protein from guinea pig plasma and demonstration of its function as a control protein of the classical pathway C3 convertase. J. Immunol. 126:1981;232-235.
24. Calderhead D.M., Kosaka Y., Manning E.M., Noelle R.J. CD40-CD154 interactions in B-cell signaling. Curr. Top. Microbiol. Immunol. 245:2000;73-99.
25. Carlsson F., Berggård K., Stalhammar-Carlemalm M., Lindahl G. Evasion of phagocytosis through cooperation between two ligand-binding regions in Streptococcus pyogenes M protein. J. Exp. Med. 198:2003;1057-1068.
26. Casciola-Rosen L.A., Anhalt G., Rosen A. Autoantigens targeted in systemic lupus erythematosus are clustered in two populations of surface structures on apoptotic keratinocytes. J. Exp. Med. 179:1994;1317-1330.
27. Criado Garcia O., Fernaud-Espinosa I., Bovolenta P., Sainz de la Cuesta R., Rodriguez de Cordoba S. Expression of the beta-chain of the complement regulator C4b-binding protein in human ovary. Eur. J. Cell. Biol. 78:1999;657-664.
28. Criado Garcia O., Sanchez Corral P., Rodriguez de Cordoba S. Isoforms of human C4b-binding protein. II. Differential modulation of the C4BPA and C4BPB genes by acute phase cytokines. J. Immunol. 155:1995;4037-4043.
29. Dahlbäck B. Purification of human C4b-binding protein and formation of its complex with vitamin K-dependent protein S. Biochem. J. 209:1983;847-856.
30. Dahlbäck B. Inhibition of protein Ca cofactor function of human and bovine protein S by C4b-binding protein. J. Biol. Chem. 261:1986;12022-12027.
31. Dahlbäck B., Stenflo J. High molecular weight complex in human plasma between vitamin K-dependent protein S and complement component C4b-binding protein. Proc. Natl. Acad. Sci. U.S.A. 78:1981;2512-2516.
32. Dahlbäck B., Smith C.A., Müller Eberhard H.J. Visualization of human C4b-binding protein and its complexes with vitamin K-dependent protein S and complement protein C4b. Proc. Natl. Acad. Sci. U.S.A. 80:1983;3461-3465.
33. Dahlbäck B., Wiedmer T., Sims P.J. Binding of anticoagulant vitamin K-dependent protein S to platelet-derived microparticles. Biochemistry. 31:1992;12769-12777.
34. Fair D.S., Marlar R.A. Biosynthesis and secretion of factor VII, protein C, protein S, and the protein C inhibitor from a human hepatoma cell line. Blood. 67:1986;64-70.
35. Fair D.S., Marlar R.A., Levin E.G. Human endothelial cells synthesize protein S. Blood. 67:1986;1168-1171.
36. Fearon D.T. The complement system and adaptive immunity. Seminars in Immunol. 10:1998;355-361.
37. Fearon D.T., Locksley R.M. The instructive role of innate immunity in the acquired immune response. Science. 272:1996;50-53.
38. Fischetti V.A. Streptococcal M protein: molecular design and biological behavior. Clin. Microbiol. Rev. 2:1989;285-314.
39. Fishelson Z., Attali G., Mevorach D. Complement and apoptosis. Mol. Immunol. 38:2001;207-219.
40. Fisher-Hoch S.P., Hutwagner L. Opportunistic candidiasis: an epidemic of the 1980s. Clin. Infect. Dis. 21:1995;897-904.
41. Frick I.M., Akesson P., Cooney J., Sjobring U., Schmidt K.H., Gomi H., Hattori S., Tagawa C., Kishimoto F., Bjorck L. Protein H-a surface protein of Streptococcus pyogenes with separate binding sites for IgG and albumin. Mol. Microbiol. 12:1994;143-151.
42. Frithz E., Heden L.O., Lindahl G. Extensive sequence homology between IgA receptor and M proteins in Streptococcus pyogenes. Mol. Microbiol. 3:1989;1111-1119.
43. Fujita T., Nussenzweig V. The role of C4-binding protein and b1H in proteolysis of C4b and C3b. J. Exp. Med. 150:1979;267-276.
44. Fukui A., Yuasa-Nakagawa T., Murakami Y., Funami K., Kishi N., Matsuda T., Fujita T., Seya T., Nagasawa S. Mapping of the sites responsible for factor I-cofactor activity for cleavage of c3b and c4b on human c4b-binding protein (c4bp) by deletion mutagenesis. J. Biochem. (Tokyo). 132:2002;719-728.
45. Garcia de Frutos P., Alim R.I., Härdig Y., Zöller B., Dahlbäck B. Differential regulation of alpha and beta chains of C4b-binding protein during acute-phase response resulting in stable plasma levels of free anticoagulant protein S. Blood. 84:1994;815-822.
46. Garcia de Frutos P., Dahlbäck B. cDNA structure of rabbit C4b-binding protein alpha-chain: preserved sequence motive in complement regulatory protein modules which bind C4b. Biochim. Biophys. Acta. 1261:1995;285-289.
47. Gershov D., Kim S., Brot N., Elkon K.B. C-reactive protein binds to apoptotic cells, protects the cells from assembly of the terminal complement components, and sustains an anti-inflammatory innate immune response: implications for systemic autoimmunity. J. Exp. Med. 192:2000;1353-1363.
48. Gigli I., Fujita T., Nussenzweig V. Modulation of the classical pathway C3 convertase by plasma protein C4b binding and C3b inactivator. Proc. Natl. Acad. Sci. U.S.A. 76:1979;6596-6600.
49. Gordon D.L., Kaufman R.M., Blackmore T.K., Kwong J., Lublin D.M. Identification of complement regulatory domains in human factor H. J. Immunol. 155:1995;348-356.
50. Härdig Y., Dahlbäck B. The amino-terminal module of the C4b-binding protein beta-chain contains the protein S binding site. J. Biol. Chem. 271:1996;20861-20867.
51. Härdig Y., Rezaie A., Dahlbäck B. High affinity binding of human vitamin K-dependent protein S to a truncated recombinant beta-chain of C4b-binding protein expressed in Escherichia coli. J. Biol. Chem. 268:1993;3033-3036.
52. He X., Shen L., Malmborg A.C., Smith K.J., Dahlbäck B., Linse S. Binding site for C4b-binding protein in vitamin K-dependent protein S fully contained in carboxy-terminal laminin-G-type repeats: a study using recombinant factor IX-protein S chimeras and surface plasmon resonance. Biochemistry. 36:1997;3745-3754.
53. Heath D.G., Cleary P.P. Fc-receptor and M-protein genes of group A streptococci are products of gene duplication. Proc. Natl. Acad. Sci. U.S.A. 86:1989;4741-4745.
54. Hessing M., Vlooswijk R.A., Hackeng T.M., Kanters D., Bouma B.N. The localization of heparin-binding fragments on human C4b-binding protein. J. Immunol. 144:1990;204-208.
55. Hillarp A., Dahlbäck B. Novel subunit in C4b-binding protein required for protein S binding. J. Biol. Chem. 263:1988;12759-12764.
56. Hillarp A., Dahlbäck B. Cloning of cDNA coding for the beta chain of human complement component C4b-binding protein: sequence homology with the alpha chain. Proc. Natl. Acad. Sci. U.S.A. 87:1990;1183-1187.
57. Hillarp A., Hessing M., Dahlbäck B. Protein S binding in relation to the subunit composition of human C4b-binding protein. FEBS Lett. 259:1989;53-56.
58. Hillarp A., Thern A., Dahlbäck B. Bovine C4b binding protein: molecular cloning of the alpha- and beta-chains provides structural background for lack of complex formation with protein S. J. Immunol. 153:1994;4190-4199.
59. Hillarp A., Wiklund H., Thern A., Dahlbäck B. Molecular cloning of rat C4b binding protein alpha- and beta-chains: structural and functional relationships among human, bovine, rabbit, mouse, and rat proteins. J. Immunol. 158:1997;1315-1323.
60. Hoffmann J.A., Kafatos F.C., Janeway C.A., Ezekowitz R.A. Phylogenetic perspectives in innate immunity. Science. 284:1999;1313-1318.
61. Holmberg M.T., Blom A.M., Meri S. Regulation of complement classical pathway by association of c4b- binding protein to the surfaces of sk-ov-3 and caov-3 ovarian adenocarcinoma cells. J. Immunol. 167:2001;935-939.
62. Hourcade D., Garcia A.D., Post T.W., Taillon Miller P., Holers V.M., Wagner L.M., Bora N.S., Atkinson J.P. Analysis of the human regulators of complement activation (RCA) gene cluster with yeast artificial chromosomes (YACs). Genomics. 12:1992;289-300.
63. Iwata, K., Seya, T., Yanagi, Y., Pesando, J.M., Johnson, P.M., Okabe, M., Ueda, S., Ariga, H., Nagasawa, S., 1995. J. Biol. Chem. 270, 15148-15152.
64. Johnsson E., Andresson G., Lindahl G., Heden L.O. Identification of the IgA-binding region in streptococcal protein Arp. J. Immunol. 153:1994;3557-3564.
65. Johnsson E., Thern A., Dahlbäck B., Heden L.O., Wikström M., Lindahl G. A highly variable region in members of the streptococcal M protein family binds the human complement regulator C4BP. J. Immunol. 157:1996;3021-3029.
66. Jokiranta T.S., Hellwage J., Koistinen V., Zipfel P.F., Meri S. Each of the three binding sites on complement factor H interacts with a distinct site on C3b. J. Biol. Chem. 275:2000;27657-27662.
67. Kaidoh T., Natsuume-Sakai S., Takahashi M. Murine C4-binding protein: a rapid purification method by affinity chromatography. J. Immunol. 126:1981;463-467.
68. Kask L., Hillarp A., Ramesh B., Dahlbäck B., Blom A.M. Structural requirements for the intra-cellular subunit polymerization of the complement inhibitor C4b-binding protein. Biochemistry. 41:2002;9349-9357.
69. Katerov V., Andreev A., Schalen C., Totolian A.A. Protein F, a fibronectin-binding protein of Streptococcus pyogenes, also binds human fibrinogen: isolation of the protein and mapping of the binding region. Microbiology. 144(Pt 1):1998;119-126.
70. Kim K.S., Itabashi H., Gemski P., Sadoff J., Warren R.L., Cross A.S. The K1 capsule is the critical determinant in the development of Escherichia coli meningitis in the rat. J. Clin. Invest. 90:1992;897-905.
71. Klickstein L.B., Bartow T.J., Miletic V., Rabson L.D., Smith J.A., Fearon D.T. Identification of distinct C3b and C4b recognition sites in the human C3b/C4b receptor (CR1, CD35) by deletion mutagenesis. J. Exp. Med. 168:1988;1699-1717.
72. Kotarsky H., Hellwage J., Johnsson E., Skerka C., Svensson H.G., Lindahl G., Sjobring U., Zipfel P.F. Identification of a domain in human factor H and factor H-like protein-1 required for the interaction with streptococcal M proteins. J. Immunol. 160:1998;3349-3354.
73. Kristensen T., Ogata R.T., Chung L.P., Reid K.B., Tack B.F. cDNA structure of murine C4b-binding protein, a regulatory component of the serum complement system. Biochemistry. 26:1987;4668-4674.
74. Krych M., Clemenza L., Howdeshell D., Hauhart R., Hourcade D., Atkinson J.P. Analysis of the functional domains of complement receptor type 1 (C3b/C4b receptor CD35) by substitution mutagenesis. J. Biol. Chem. 269:1994;13273-13278.
75. Krych M., Hauhart R., Atkinson J.P. Structure-function analysis of the active sites of complement receptor type 1. J. Biol. Chem. 273:1998;8623-8629.
76. Krych M., Hourcade D., Atkinson J.P. Sites within the complement C3b/C4b receptor important for the specificity of ligand binding. Proc. Natl. Acad. Sci. U.S.A. 88:1991;4353-4357.
77. Kuhn S., Skerka C., Zipfel P.F. Mapping of the complement regulatory domains in the human factor H-like protein 1 and in factor H1. J. Immunol. 155:1995;5663-5670.
78. Kuhn S., Zipfel P.F. Mapping of the domains required for decay acceleration activity of the human factor H-like protein 1 and factor H. Eur. J. Immunol. 26:1996;2383-2387.
79. Lancefield R.C. Current knowledge of type-specific M antigens of group A streptococci. J. Immunol. 89:1962;307-313.
80. Lappin D.F., Whaley K. Interferon-induced transcriptional and post-transcriptional modulation of factor H and C4 binding-protein synthesis in human monocytes. Biochem. J. 271:1990;767-772.
81. Lindahl G., Sjöbring U., Johnsson E. Human complement regulators: a major target for pathogenic microorganisms. Curr. Opin. Immunol. 12:2000;44-51.
82. Malm J., Bennhagen R., Holmberg L., Dahlbäck B. Plasma concentrations of C4b-binding protein and vitamin K-dependent protein S in term and preterm infants: low levels of protein S-C4b-binding protein complexes. Br. J. Haematol. 68:1988a;445-449.
83. Malm J., He X.H., Bjartell A., Shen L., Abrahamsson P.A., Dahlback B. Vitamin K-dependent protein S in Leydig cells of human testis. Biochem. J. 302:1994;845-850.
84. Malm J., Laurell M., Dahlbäck B. Changes in the plasma levels of vitamin K-dependent proteins C and S and of C4b-binding protein during pregnancy and oral contraception. Br. J. Haematol. 68:1988b;437-443.
85. McMichael J.C., Fiske M.J., Fredenburg R.A., Chakravarti D.N., VanDerMeid K.R., Barniak V., Caplan J., Bortell E., Baker S., Arumugham R., Chen D. Isolation and characterization of two proteins from Moraxella catarrhalis that bear a common epitope. Infect. Immun. 66:1998;4374-4381.
86. Melissari E., Nicolaides K.H., Scully M.F., Kakkar V.V. Protein S and C4b-binding protein in fetal and noenatal blood. Br. J. Haematol. 70:1988;199-203.
87. Meri, T., Blom, A.M., Hartmann, A., Lenk, D., Meri, S., Zipfel, P.F., 2004. The yeast and hyphal forms of Candida albicans bind complement regulator C4b-binding protein, submitted for publication.
88. Meri T., Hartmann A., Lenk D., Eck R., Wurzner R., Hellwage J., Meri S., Zipfel P.F. The yeast Candida albicans binds complement regulators factor H and FHL-1. Infect. Immun. 70:2002;5185-5192.
89. Moalic P., Gruel Y., Body G., Foloppe P., Delahousse B., Leroy J. Levels and plasma distribution of free and C4BP-bound protein s in human fetuses and full-term new borns. Thromb. Res. 49:1988;471-480.
90. Morfeldt E., Berggard K., Persson J., Drakenberg T., Johnsson E., Lindahl E., Linse S., Lindahl G. Isolated hypervariable regions derived from streptococcal M proteins specifically bind human C4b-binding protein: implications for antigenic variation. J. Immunol. 167:2001;3870-3877.
91. Morio T., Hanissian S., Geha R.S. Characterization of a 23. kDa protein associated with CD40 Proc. Natl. Acad. Sci. U.S.A. 92:1995;11633-11636.
92. Murphy T.F. Branhamella catarrhalis: epidemiology, surface antigenic structure, and immune response. Microbiol. Rev. 60:1996;267-279.
93. Nauta A.J., Trouw L.A., Daha M.R., Tijsma O., Nieuwland R., Schwaeble W.J., Gingras A.R., Mantovani A., Hack E.C., Roos A. Direct binding of C1q to apoptotic cells and cell blebs induces complement activation. Eur. J. Immunol. 32:2002;1726-1736.
94. Nelsestuen G.L., Kisiel W., Di Scipio R.G. Interaction of vitamin K dependent proteins with membranes. Biochemistry. 17:1978;2134-2138.
95. Niles M.J., Matsuuchi L., Koshland M.E. Polymer IgM assembly and secretion in lymphoid and nonlymphoid cell lines: evidence that J chain is required for pentamer IgM synthesis. Proc. Natl. Acad. Sci. U.S.A. 92:1995;2884-2888.
96. Nordström, T., Blom, A.M., Forsgren, A., K R., 2004. The emerging pathogen Moraxella catarrhalis interacts with complement inhibitor C4b-binding protein through ubiquitous surface proteins A1 and A2, submitted for publication.
97. Oettgen H.C. Regulation of the IgE isotype switch: new insights on cytokine signals and the functions of epsilon germline transcripts. Curr. Opin. Immunol. 12:2000;618-623.
98. Ogden C.A.A.D., Hoffman P.R., Bratton D., Ghebrehiwet B., Fadok V.A., Henson P.M. C1q and mannose-binding lectin engagement of cell surface calrticulin and CD91 initiates macropinocytosis and uptake of apoptotic cells. J. Exp. Med. 194:2001;781-795.
99. Perkins S.J., Chung L.P., Reid K.B. Unusual ultrastructure of complement component C4b-binding protein of human complement by synchrotron X-ray scattering and hydrodynamic analysis. Biochem. J. 233:1986;799-807.
100. Pfaller M., Wenzel R. Impact of the changing epidemiology of fungal infections in the 1990s. Eur. J. Clin. Microbiol. Infect. Dis. 11:1992;287-291.
101. Prasadarao N.V., Blom A.M., Villoutreix B.O., Linsangan L.C. A novel interaction of outer membrane protein A with C4b-binding protein mediates serum resitance of Escherichia coli K1. J. Immunol. 169:2002;6352-6360.
102. Ram S., Cullinane M., Blom A.M., Gulati S., McQuillen D.P., Monks B.G., O' Connell C., Boden R., Elkins C., Pangburn M.K., Dahlbäck B., Rice P.A. Binding of C4b-binding protein to porin: a molecular mechanism of serum resistance of Neisseria gonorrhoeae. J. Exp. Med. 193:2001;281-296.
103. Ram S., McQuillen D.P., Gulati S., Elkins C., Pangburn M.K., Rice P.A. Binding of complement factor H to loop 5 of porin protein 1A: a molecular mechanism of serum resistance of nonsialylated Neisseria gonorrhoeae. J. Exp. Med. 4:1998a;671-680.
104. Ram S., Sharma A.K., Simpson S.D., Gulati S., McQuillen D.P., Pangburn M.K., Rice P.A. A novel sialic acid binding site on factor H mediates serum resistance of sialylated Neisseria gonorrhoeae. J. Exp. Med. 187:1998b;743-752.
105. Rodriguez de Cordoba S., Perez Blas M., Ramos Ruiz R., Sanchez Corral P., Pardo Manuel de Villena F., Rey Campos J. The gene coding for the beta-chain of C4b-binding protein (C4BPB) has become a pseudogene in the mouse. Genomics. 21:1994;501-509.
106. Saeki T., Hirose S., Nukatsuka M., Kusunoki Y., Nagasawa S. Evidence that C4b-binding protein is an acute phase protein. Biochem. Biophys. Res. Commun. 164:1989;1446-1451.
107. Sahu A., Pangburn M.K. Identification of multiple sites of interaction between heparin and the complement system. Mol. Immunol. 30:1993;679-684.
108. Sanchez Corral P., Criado Garcia O., Rodriguez de Cordoba S. Isoforms of human C4b-binding protein. I: molecular basis for the C4BP isoform pattern and its variations in human plasma. J. Immunol. 155:1995;4030-4036.
109. Savill J., Dransfield I., Gregory C., Haslett C. A blast from the past: clearance of apoptotic cells regulates immune responses. Nat. Rev. Immunol. 2:2002;965-975.
110. Scharfstein J., Ferreira A., Gigli I., Nussenzweig V. Human C4b-binding protein, isolation and characterization. J. Exp. Med. 148:1978;207-222.
111. Schneider L.C. X-linked hyper IgM syndrome. Clin. Rev. Allergy Immunol. 19:2000;205-215.
112. Schwalbe R.A., Dahlbäck B., Nelsestuen G.L. Independent association of serum amyloid P component, protein S, and complement C4b with complement C4b-binding protein and subsequent association of the complex with membranes. J. Biol. Chem. 265:1990;21749-21757.
113. Schwalbe R.A., Ryan J., Stern D.M., Kisiel W., Dahlback B., Nelsestuen G.L. Protein structural requirements and properties of membrane binding by gamma-carboxyglutamic acid-containing plasma proteins and peptides. J. Biol. Chem. 264:1989;20288-20296.
114. Seya T., Holers V.M., Atkinson J.P. Purification and functional analysis of the polymorphic variants of the C3b/C4b receptor (CR1) and comparison with H, C4b-binding protein (C4bp), and decay accelerating factor (DAF). J. Immunol. 135:1985;2661-2667.
115. Seya T., Nakamura K., Masaki T., Ichihara-Itoh C., Matsumoto M., Nagasawa S. Human factor H and C4b-binding protein serve as factor I cofactors both encompassing inactivation of C3b and C4b. Mol. Immunol. 32:1995;355-360.
116. Simmonds R.E., Zöller B., Ireland H., Thompson E., de Frutos P.G., Dahlbäck B., Lane D.A. Genetic and phenotypic analysis of a large (122-member) protein S-deficient kindred provides an explanation for the familial coexistence of type I and type III plasma phenotypes. Blood. 89:1997;4364-4370.
117. Stenberg L., O'Toole P.W., Mestecky J., Lindahl G. Molecular characterization of protein Sir, a streptococcal cell surface protein that binds both immunoglobulin A and immunoglobulin G. J. Biol. Chem. 269:1994;13458-13464.
118. Thern A., Stenberg L., Dahlbäck B., Lindahl G. Ig-binding surface proteins of Streptococcus pyogenes also bind human C4b-binding protein (C4BP), a regulatory component of the complement system. J. Immunol. 154:1995;375-386.
119. van de Poel R.H., Meijers J.C., Bouma B.N. Interaction between protein S and complement C4b-binding protein (C4BP): affinity studies using chimeras containing c4bp beta-chain short consensus repeats. J. Biol. Chem. 274:1999;15144-15150.
120. Van Wijnen M., Stam J.G., Chang G.T., Meijers J.C., Reitsma P.H., Bertina R.M., Bouma B.N. Characterization of mini-protein S, a recombinant variant of protein S that lacks the sex hormone binding globulin-like domain. Biochem. J. 330:1998;389-396.
121. Villoutreix B.O., Blom A.M., Webb J., Dahlbäck B. The complement regulator C4b-binding protein analyzed by molecular modeling, bioinformatics and computer-aided experimental design. Immunopharmacology. 42:1999;121-134.
122. Walport M.J. Complement first of two parts. N. Eng. J. Med. 344:2001;1058-1066.
123. Walport M.J. Complement and systemic lupus erythematosus. Arthritis Res. 4(Suppl. 3):2002;S279-S293.
124. Webb J.H., Blom A.M., Dahlbäck B. Vitamin K-dependent protein S localizing complement regulator C4b-binding protein to the surface of apoptotic cells. J. Immunol. 169:2002;2580-2586.
125. Webb J.H., Blom A.M., Dahlbäck B. The binding of protein S and the protein S-C4BP complex to neutrophils is apoptosis-dependent. Blood Coagul. Fibrinolysis. 14:2003a;355-359.
126. Webb J.H., Villoutreix B.O., Dahlback B., Blom A.M. Localization of a hydrophobic binding site for anticoagulant protein S on the beta-chain of complement regulator C4b-binding protein. J. Biol. Chem. 276:2001;4330-4337.
127. Webb J.H., Villoutreix B.O., Dahlbäck B., Blom A.M. Role of CCP2 of the C4b-binding protein beta-chain in protein S binding evaluated by mutagenesis and monoclonal antibodies. Eur. J. Immunol. 270:2003b;93-100.
128. Weiser J.N., Gotschlich E.C. Outer membrane protein A (OmpA) contributes to serum resistance and pathogenicity of Escherichia coli K-1. Infect. Immun. 59:1991;2252-2258.
129. Westein E., Denis C.V., Bouma B.N., Lenting P.J. The alpha-chains of C4b-binding protein mediate complex formation with low density lipoprotein receptor-related protein. J. Biol. Chem. 277:2002;2511-2516.
130. Ziccardi R.J., Dahlbäck B., Müller Eberhard H.J. Characterization of the interaction of human C4b-binding protein with physiological ligands. J. Biol. Chem. 259:1984;13674-13679.
131. Zipfel P.F., Skerka C., Hellwage J., Jokiranta S.T., Meri S., Brade V., Kraiczy P., Noris M., Remuzzi G. Factor H family proteins: on complement, microbes and human diseases. Biochem. Soc. Trans. 30:2002;971-978.
132. Zöller B., Garcia de Frutos P., Dahlbäck B. Evaluation of the relationship between protein S and C4b-binding protein isoforms in hereditary protein S deficiency demonstrating type I and type III deficiencies to be phenotypic variants of the same genetic disease. Blood. 85:1995;3524-3531.