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Bacterial Complement Escape

  • Chapter
Pathogen-Derived Immunomodulatory Molecules

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 666))

Abstract

Complement activation is a crucial step in our innate immune defense against invading bacteria. Complement proteins can quickly recognize invading bacteria and subsequenly label them for phagocytosis or kill them by direct lysis. In order to survive in the human host, bacterial pathogens have evolved a number of excreted and membrane-bound proteins that interfere with several steps of the complement cascade. In this chapter we summarize the most successful complement-modulating strategies by human bacterial pathogens.

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References

  1. Walport MJ. Complement. First of two parts. N Engl J Med 2001; 344(14):1058–1066.

    Article  CAS  PubMed  Google Scholar 

  2. Walport MJ. Complement. Second of two parts. N Engl J Med 2001; 344(15):1140–1144.

    Article  CAS  PubMed  Google Scholar 

  3. Gasque P. Complement: a unique innate immune sensor for danger signals. Mol Immunol 2004; 41(11):1089–1098.

    Article  CAS  PubMed  Google Scholar 

  4. Song WC, Sarrias MR, Lambris JD. Complement and innate immunity. Immunopharmacology 2000; 49(1–2):187–198.

    Article  CAS  PubMed  Google Scholar 

  5. Ramm LE, Whitlow MB, Mayer MM. Transmembrane channel formation by complement: functional analysis of the number of C5b6, C7, C8 and C9 molecules required for a single channel. Proc Natl Acad Sci USA 1982; 79(15):4751–4755.

    Article  CAS  PubMed  Google Scholar 

  6. Kirkitadze MD, Barlow PN. Structure and flexibility of the multiple domain proteins that regulate complement activation. Immunol Rev 2001; 180:146–161.

    Article  CAS  PubMed  Google Scholar 

  7. Sahu A, Lambris JD. Structure and biology of complement protein C3, a connecting link between innate and acquired immunity. Immunol Rev 2001; 180:35–48.

    Article  CAS  PubMed  Google Scholar 

  8. Duncan AR, Winter G. The binding site for C1q on IgG. Nature 1988; 332(6166):738–740.

    Article  CAS  PubMed  Google Scholar 

  9. Dodds AW, Sim RB, Porter RR et al. Activation of the first component of human complement (C1) by antibody-antigen aggregates. Biochem J 1978; 175(2):383–390.

    CAS  PubMed  Google Scholar 

  10. Sim RB, Laich A. Serine proteases of the complement system. Biochem Soc Trans 2000; 28(5):545–550.

    CAS  PubMed  Google Scholar 

  11. Law SK, Dodds AW. The internal thioester and the covalent binding properties of the complement proteins C3 and C4. Protein Sci 1997; 6(2):263–274.

    CAS  PubMed  Google Scholar 

  12. Matsushita M, Fujita T. Ficolins and the lectin complement pathway. Immunol Rev 2001; 180:78–85.

    Article  CAS  PubMed  Google Scholar 

  13. Fujita T, Matsushita M, Endo Y. The lectin-complement pathway—its role in innate immunity and evolution. Immunol Rev 2004; 198:185–202.

    Article  CAS  PubMed  Google Scholar 

  14. Holmskov U, Thiel S, Jensenius JC. Collections and ficolins: humoral lectins of the innate immune defense. Annu Rev Immunol 2003; 21:547–578.

    Article  CAS  PubMed  Google Scholar 

  15. Matsushita M, Fujita T. Cleavage of the third component of complement (C3) by mannose-binding protein-associated serine protease (MASP) with subsequent complement activation. Immunobiology 1995; 194(4–5):443–448.

    CAS  PubMed  Google Scholar 

  16. Krarup A, Wallis R, Presanis JS et al. Simultaneous activation of complement and coagulation by MBL-associated serine protease 2. PLoS ONE 2007; 2(7):e623.

    Article  PubMed  CAS  Google Scholar 

  17. Ponnuraj K, Xu Y, Macon K et al. Structural analysis of engineered Bb fragment of complement factor B: insights into the activation mechanism of the alternative pathway C3-convertase. Mol Cell 2004; l4(1):17–28.

    Article  Google Scholar 

  18. Xu Y, Narayana SV, Volanakis JE. Structural biology of the alternative pathway convertase. Immunol Rev 2001; 180:123–135.

    Article  CAS  PubMed  Google Scholar 

  19. Hourcade DE. The role of properdin in the assembly of the alternative pathway C3 convertases of complement. J Biol Chem 2006; 281(4):2128–2132.

    Article  CAS  PubMed  Google Scholar 

  20. Janssen BJ, Huizinga EG, Raaijmakers HC et al. Structures of complement component C3 provide insights into the function and evolution of immunity. Nature 2005; 437(7058):505–511.

    Article  CAS  PubMed  Google Scholar 

  21. Lambris JD. The multifunctional role of C3, the third component of complement. Immunol Today 1988; 9(12):387–393.

    Article  CAS  PubMed  Google Scholar 

  22. Pangburn MK, Rawal N. Structure and function of complement C5 convertase enzymes. Biochem Soc Trans 2002; 30(Pt 6):1006–1010.

    CAS  PubMed  Google Scholar 

  23. Rawal N, Pangburn MK. Structure/function of C5 convertases of complement. Int Immunopharmacol 2001; 1(3):415–422.

    Article  CAS  PubMed  Google Scholar 

  24. Joiner K, Brown E, Hammer C et al. Studies on the mechanism of bacterial resistance to complement-mediated killing. III. C5b-9 deposits stably on rough and Type 7S. pneumoniae without causing bacterial killing. J Immunol 1983; 130(2):845–849.

    CAS  PubMed  Google Scholar 

  25. Davies A, Lachmann PJ. Membrane defence against complement lysis: the structure and biological properties of CD59. Immunol Res 1993; 12(3):258–275.

    Article  CAS  PubMed  Google Scholar 

  26. Foster TJ. Immune evasion by staphylococci. Nat Rev Microbiol 2005; 3(12):948–958.

    Article  CAS  PubMed  Google Scholar 

  27. Rooijakkers SH, van Kessel KP, van Strijp JA. Staphylococcal innate immune evasion. Trends Microbiol 2005; 13(12):596–601.

    Article  CAS  PubMed  Google Scholar 

  28. Rooijakkers SH, van Strijp JA. Bacterial complement evasion. Mol Immunol 2007; 44(1–3):23–32.

    Article  CAS  PubMed  Google Scholar 

  29. Silverman GJ, Goodyear CS, Siegel DL. On the mechanism of staphylococcal protein A immunomodulation. Transfusion 2005; 45(2):274–280.

    Article  CAS  PubMed  Google Scholar 

  30. Forsgren A, Sjoquist J. “Protein A” from S. aureus. I. Pseudo-immune reaction with human gamma-globulin. J Immunol 1966; 97(6):822–827.

    CAS  PubMed  Google Scholar 

  31. Goward CR, Scawen MD, Murphy JP et al. Molecular evolution of bacterial cell-surface proteins. Trends Biochem Sci 1993; 18(4):136–140.

    Article  CAS  PubMed  Google Scholar 

  32. Zhang L, Jacobsson K, Vasi J et al. A second IgG-binding protein in Staphylococcus aureus. Microbiology 1998; 144(Pt 4):985–991.

    Article  CAS  PubMed  Google Scholar 

  33. Burman J, Leung E, Isenman DE et al. Interaction of human complement with Sbi, a staphylococcal immunoglobulin-binding protein. Mol Immunol 2007; 44(16):3982

    Article  Google Scholar 

  34. Rooijakkers SH, van Wamel WJ, Ruyken M et al. Anti-opsonic properties of staphylokinase. Microbes Infect 2005; 7(3):476–484.

    Article  CAS  PubMed  Google Scholar 

  35. Harpel PC, Sullivan R, Chang TS. Binding and activation of plasminogen on immobilized immunoglobulin G. Identification of the plasmin-derived Fab as the plasminogen-binding fragment. J Biol Chem 1989; 264(1):616–624.

    CAS  PubMed  Google Scholar 

  36. Seya T, Nagasawa S, Matsukura M et al. Generation of C3d,g and C3d by urokinase-treated plasma in association with fibrinolysis. Complement 1985; 2(2–3):165–174.

    CAS  PubMed  Google Scholar 

  37. Fitzgerald JR, Reid SD, Ruotsalainen E et al. Genome diversification in Staphylococcus aureus: Molecular evolution of a highly variable chromosomal region encoding the Staphylococcal exotoxin-like family of proteins. Infect Immun 2003; 71(5):2827–2838.

    Article  CAS  PubMed  Google Scholar 

  38. Langley R, Wines B, Willoughby N et al. The staphylococcal superantigen-like protein 7 binds IgA and complement C5 and inhibits IgA-Fc alpha RI binding and serum killing of bacteria. J Immunol 2005; 174(5):2926–2933.

    CAS  PubMed  Google Scholar 

  39. de Haas CJ, Veldkamp KE, Peschel A et al. Chemotaxis inhibitory protein of Staphylococcus aureus, a bacterial antiinflammatory agent. J Exp Med 2004; 199(5):687–695.

    Article  PubMed  Google Scholar 

  40. Rooijakkers SH, Ruyken M, Roos A et al. Immune evasion by a staphylococcal complement inhibitor that acts on C3 convertases. Nat Immunol 2005; 6(9):920–927.

    Article  CAS  PubMed  Google Scholar 

  41. Rooijakkers SH, Ruyken M, van RJ et al. Early expression of SCIN and CHIPS drives instant immune evasion by Staphylococcus aureus. Cell Microbiol 2006; 8(8):1282–1293.

    Article  CAS  PubMed  Google Scholar 

  42. Rooijakkers SH, Milder FJ, Bardoel BW et al. Staphylococcal complement inhibitor: structure and active sites. J Immunol 2007; 179(5):2989–2998.

    CAS  PubMed  Google Scholar 

  43. Jongerius I, Kohl J, Pandey MK et al. Staphylococcal complement evasion by various convertase-blocking molecules. J Exp Med 2007; 204(10):2461–2471.

    Article  CAS  PubMed  Google Scholar 

  44. Hammel M, Sfyroera G, Pyrpassopoulos S et al. Characterization of Ehp, a secreted complement inhibitory protein from Staphylococcus aureus. J Biol Chem 2007; 282(41):30051–30061.

    Article  CAS  PubMed  Google Scholar 

  45. Boden MK, Flock JI. Cloning and characterization of a gene for a 19 kDa fibrinogen-binding protein from Staphylococcus aureus. Mol Microbiol 1994; 12(4):599–606.

    Article  CAS  PubMed  Google Scholar 

  46. Hammel M, Sfyroera G, Ricklin D et al. A structural basis for complement inhibition by Staphylococcus aureus. Nat Immunol 2007; 8(4):430–437.

    Article  CAS  PubMed  Google Scholar 

  47. Lee LY, Liang X, Hook M et al. Identification and characterization of the C3 binding domain of the Staphylococcus aureus extracellular fibrinogen-binding protein (Efb). J Biol Chem 2004; 279(49):50710–50716.

    Article  CAS  PubMed  Google Scholar 

  48. Jarva H, Jokiranta TS, Wurzner R et al. Complement resistance mechanisms of streptococci. Mol Immunol 2003; 40(2–4):95–107.

    Article  CAS  PubMed  Google Scholar 

  49. Kraiczy P, Wurzner R. Complement escape of human pathogenic bacteria by acquisition of complement regulators. Mol Immunol 2006; 43:31–44.

    Article  CAS  PubMed  Google Scholar 

  50. Nizet V. Understanding how leading bacterial pathogens subvert innate immunity to reveal novel therapeutic targets. J Allergy Clin Immunol 2007; 120(1):13–22.

    Article  CAS  PubMed  Google Scholar 

  51. Peréz-Caballero D, García-Laorden I, Cortés G et al. Interaction between complement regulators and Streptococcus pyogenes: binding of C4b-binding protein and factor H/factor H-like protein 1 to M18 strains involves two different cell surface molecules. J Immunol 2004; 173(11):6899–6904.

    PubMed  Google Scholar 

  52. Thern A, Stenberg L, Dahlback B et al. Ig-binding surface proteins of Streptococcus pyogenes also bind human C4b-binding protein (C4BP), a regulatory component of the complement system. J Immunol 1995; 154(1):375–386.

    CAS  PubMed  Google Scholar 

  53. Pandiripally V, Gregory E, Cue D. Acquisition of regulators of complement activation by Streptococcus pyogenes serotype M1. Infect Immun 2002; 70(11):6206–6214.

    Article  CAS  PubMed  Google Scholar 

  54. Pandiripally V, Wei L, Skerka C et al. Recruitment of complement factor H-like protein 1 promotes intracellular invasion by group A streptococci. Infect Immun 2003; 71(12):7119–7128.

    Article  CAS  PubMed  Google Scholar 

  55. Caswell CC, Han R, Hovis KM et al. The Scl1 protein of M6-type group A Streptococcus binds the human complement regulatory protein, factor H and inhibits the alternative pathway of complement. Mol Microbiol 2008; 67(3):584–596.

    Article  CAS  PubMed  Google Scholar 

  56. Courtney HS, Hasty DL, Dale JB. Anti-phagocytic mechanisms of Streptococcus pyogenes: binding of fibrinogen to M-related protein. Mol Microbiol 2006; 59(3):936–947.

    Article  CAS  PubMed  Google Scholar 

  57. Weineisen M, Sjobring U, Fallman M et al. Streptococcal M5 protein prevents neutrophil phagocytosis by interfering with CD11b/CD18 receptor-mediated association and signaling. J Immunol 2004; 172(6):3798–3807.

    CAS  PubMed  Google Scholar 

  58. Lei B, DcLeo FR, Hoe NP et al. Evasion of human innate and acquired immunity by a bacterial homolog of CD11b that inhibits opsonophagocytosis. Nat Med 2001; 7(12):1298–1305.

    Article  CAS  PubMed  Google Scholar 

  59. Akesson P, Sjoholm AG, Bjorck L. Protein SIC, a novel extracellular protein of Streptococcus pyogenes interfering with complement function. J Biol Chem 1996; 271(2):1081–1088.

    Article  CAS  PubMed  Google Scholar 

  60. Fernie-King BA, Seilly DJ, Willers C et al. Streptococcal inhibitor of complement (SIC) inhibits the membrane attack complex by preventing uptake of C567 onto cell membranes. Immunology 2001; 103(3):390–398.

    Article  CAS  PubMed  Google Scholar 

  61. Hartas J, Sriprakash KS. Streptococcus pyogenes strains containing emml2 and emm55 possess a novel gene coding for distantly related SIC protein. Microb Pathog 1999; 26(1):25–33.

    Article  CAS  PubMed  Google Scholar 

  62. von Pawel-Rammingen U, Johansson BP, Bjorck L. IdeS, a novel streptococcal cysteine proteinase with unique specificity for immunoglobulin G. EMBO J 2002; 21(7):1607–1615.

    Article  Google Scholar 

  63. von Pawel-Rammingen U, Björck L. IdeS and SpeB: immunoglobulin-degrading cysteine proteinases of Streptococcus pyogenes. Curr Opin Microbiol 2003; 6(1):50–55.

    Article  CAS  Google Scholar 

  64. Tsao N, Tsai WH, Lin YS et al. Streptococcal pyrogenic exotoxin B cleaves properdin and inhibits complement-mediated opsonophagocytosis. Biochem Biophys Res Commun 2006; 339(3):779–784.

    Article  CAS  PubMed  Google Scholar 

  65. Kuo CF, Lin YS, Chuang WJ et al. Degrading Complement 3 by Streptococcal Pyrogenic Exotoxin B Inhibits Complement Activation and Neutrophil Opsonophagocytosis. Infect Immun 2008; 76(3):1116–1169.

    Article  CAS  Google Scholar 

  66. Terao Y, Mori Y, Yamaguchi M et al. Group A streptococcal cysteine protease degrades C3 (C3b) and contributes to evasion of innate immunity. J Biol Chem 2008; 283(10):6253–6260.

    Article  CAS  PubMed  Google Scholar 

  67. Wexler DE, Chenoweth DE, Cleary PP. Mechanism of action of the group A streptococcal C5a inactivator. Proc Natl Acad Sci USA 1985; 82(23):8144–8148.

    Article  CAS  PubMed  Google Scholar 

  68. Ji Y, McLandsborough L, Kondagunta A et al. C5a peptidase alters clearance and trafficking of group A streptococci by infected mice. Infect Immun 1996; 64(2):503–510.

    CAS  PubMed  Google Scholar 

  69. Areschoug T, Stalhammar-Carlemalm M, Karlsson I et al. Streptococcal beta protein has separate binding sites for human factor H and IgA-Fc. J Biol Chem 2002; 277(15):12642–12648.

    Article  CAS  PubMed  Google Scholar 

  70. Heden LO, Frithz E, Lindahl G. Molecular characterization of an IgA receptor from group B streptococci: sequence of the gene, identification of a proline-rich region with unique structure and isolation of N-terminal fragments with IgA-binding capacity. Eur J Immunol 1991; 21(6):1481–1490.

    Article  CAS  PubMed  Google Scholar 

  71. Chmouryguina I, Suvorov A, Ferrieri P et al. Conservation of the C5a peptidase genes in group A and B streptococci. Infect Immun 1996; 64(7):2387–2390.

    CAS  PubMed  Google Scholar 

  72. Bohnsack JF, Chang JK, Hill HR. Restricted ability of group B streptococcal C5a-ase to inactivate C5a prepared from different animal species. Infect Immun 1993; 61(4):1421–1426.

    CAS  PubMed  Google Scholar 

  73. Mitchell TJ, Andrew PW, Saunders FK et al. Complement activation and antibody binding by pneumolysin via a region of the toxin homologous to a human acute-phase protein. Mol Microbiol 1991; 5(8):1883–1888.

    Article  CAS  PubMed  Google Scholar 

  74. Paton JC, Rowan-Kelly B, Ferrante A. Activation of human complement by the pneumococcal toxin pneumolysin. Infect Immun 1984; 43(3):1085–1087.

    CAS  PubMed  Google Scholar 

  75. McDaniel LS, Yother J, Vijayakumar M et al. Use of insertional inactivation to facilitate studies of biological properties of pneumococcal surface protein A (PspA). J Exp Med 1987; 165(2):381–394.

    Article  CAS  PubMed  Google Scholar 

  76. Dave S, Brooks-Walter A, Pangburn MK et al. PspC, a pneumococcal surface protein, binds human factor H. Infect Immun 2001; 69(5):3435–3437.

    Article  CAS  PubMed  Google Scholar 

  77. Jarva H, Janulczyk R, Hellwage J et al. Streptococcus pneumoniae evades complement attack and opsonophagocytosis by expressing the pspC locus-encoded Hie protein that binds to short consensus repeats 8–11 of factor H. J Immunol 2002; 168(4):1886–1894.

    CAS  PubMed  Google Scholar 

  78. Kerr AR, Paterson GK, McCluskey J et al. The contribution of PspC to pneumococcal virulence varies between strains and is accomplished by both complement evasion and complement-independent mechanisms. Infect Immun 2006; 74(9):5319–5324.

    Article  CAS  PubMed  Google Scholar 

  79. Li J, Glover DT, Szalai AJ et al. PspA and PspC minimize immune adherence and transfer of pneumococci from erythrocytes to macrophages through their effects on complement activation. Infect Immun 2007; 75(12):5877–5885.

    Article  CAS  PubMed  Google Scholar 

  80. Merino S, Camprubi S, Alberti S et al. Mechanisms of Klebsiella pneumoniae resistance to complement-mediated killing. Infect Immun 1992; 60:2529–2535.

    CAS  PubMed  Google Scholar 

  81. Alberti S, Marques G, Hernandez-Alles S et al. Interaction between complement subcomponent C1q and the Klebsiella pneumoniae porin OmpK36. Infect Immun 1996; 64:4719–4725.

    CAS  PubMed  Google Scholar 

  82. Merino S, Nogueras MM, Aguilar A et al. Activation of the complement classical pathway (C1q binding) by mesophilic Aeromonas hydrophila outer membrane protein. Infect Immun 1998; 66:3825–3831.

    CAS  PubMed  Google Scholar 

  83. Clas F, Loos M. Antibody-independent binding of the first component of complement (C1) and its subcomponent C1q to the S and R forms of Salmonella minnesota. Infect Immun 1981; 31:1138–1144.

    CAS  PubMed  Google Scholar 

  84. Tomas JM, Camprubi S, Merino S et al. Surface exposure of O1 serotype lipopolysaccharide in Klebsiella pneumoniae strains expressing different K antigens. Infect Immun 1991; 59:2006–2011.

    CAS  PubMed  Google Scholar 

  85. Alberti S, Marques G, Camprubi S et al. C1q binding and activation of the complement classical pathway by Klebsiella pneumoniae outer membrane proteins. Infect Immun 1993; 61:852–860.

    CAS  PubMed  Google Scholar 

  86. Eisenschenk FC, Houle JJ, Hoffmann EM. Mechanism of serum resistance among Brucella abortus isolates. Vet Microbiol 1999; 68:235–244.

    Article  CAS  PubMed  Google Scholar 

  87. Peak IR, Jennings MP, Hood DW et al. Tetrameric repeat units associated with virulence factor phase variation in Haemophilus also occur in Neisseria spp. and Moraxella catarrhalis. FEMS Microbiol Lett 1996; 137:109–114.

    Article  CAS  PubMed  Google Scholar 

  88. Peak IR, Jennings MP, Hood DW et al. Tetranucleotide repeats identify novel virulence determinant homologues in Neisseria meningitidis. Microb Pathog 1999; 26:13–23.

    Article  CAS  PubMed  Google Scholar 

  89. Saunders NJ, Peden JF, Hood DW et al. Simple sequence repeats in the Helicobacter pylori genome. Mol Microbiol 1998; 27:1091–1098.

    Article  CAS  PubMed  Google Scholar 

  90. Mandrell RE, Apicella MA. Lipo-oligosaccharides (LOS) of mucosal pathogens: molecular mimicry and host-modification of LOS. Immunobiology 1993; 187:382–402.

    CAS  PubMed  Google Scholar 

  91. Mandrell RE, Griffiss JM, Macher BA. Lipooligosaccharides (LOS) of Neisseria gonorrhoeae and Neisseria meningitidis have components that are immunochemically similar to precursors of human blood group antigens. Carbohydrate sequence specificity of the mouse monoclonal antibodies that recognize cross-reacting antigens on LOS and human erythrocytes. J Exp Med 1988; 168:107–126.

    Article  CAS  PubMed  Google Scholar 

  92. Yuki NK, Susuki M. Koga Y et al. Carbohydrate mimicry between human ganglioside GM1 and Campylobacter jejuni lipooligosaccharide causes Guillain-Barre syndrome. Proc Natl Acad Sci USA 2004; 101:11404–11409.

    Article  CAS  PubMed  Google Scholar 

  93. Edwards JL, Apicella MA. The role of lipooligosaccharide in Neisseria gonorrhoeae pathogenesis of cervical epithelia: lipid A serves as a C3 acceptor molecule. Cell Microbiol 2002; 4:585–598.

    Article  CAS  PubMed  Google Scholar 

  94. Ho DK, Ram S, Nelson KL et al. lgtC expression modulates resistance to C4b deposition on an invasive nontypeable Haemophilus influenzae. J Immunol 2007; 178:1002–1012.

    CAS  PubMed  Google Scholar 

  95. Lewis LA, Ram S, Prasad A et al. Defining targets for complement components C4b and C3b on the pathogenic neisseriae. Infect Immun 2008; 76:339–350.

    Article  CAS  PubMed  Google Scholar 

  96. Ram S, Cox AD, Wright JC et al. Neisserial lipooligosaccharide is a target for complement component C4b: Inner core phosphoethanolamine residues define C4b linkage specificity. J Biol Chem 2003; 278:50853–50862.

    Article  CAS  PubMed  Google Scholar 

  97. Madico G, Ngampasutadol J, Gulati S et al. Factor H Binding and Function in Sialylated Pathogenic Neisseriae is Influenced by Gonococcal, but Not Meningococcal, Porin. J Immunol 2007; 178:4489–4497.

    CAS  PubMed  Google Scholar 

  98. Hong YQ, Ghebrehiwet B. Effect of Pseudomonas aeruginosa elastase and alkaline protease on serum complement and isolated components C1q and C3. Clin Immunol Immunopathol 1992; 62:133–138.

    Article  CAS  PubMed  Google Scholar 

  99. Wolf U, Bauer D, Traub WH. Metalloproteases of Serratia liquefaciens: degradation of purified human serum proteins. Zentralbl Bakteriol 1991; 276:16–26.

    CAS  PubMed  Google Scholar 

  100. Molla A, Akaike T, Maeda H. Inactivation of various proteinase inhibitors and the complement system in human plasma by the 56-kilodalton proteinase from Serratia marcescens. Infect Immun 1989; 57:1868–1871.

    CAS  PubMed  Google Scholar 

  101. Sodeinde OA, Subrahmanyam YV, Stark K et al. A surface protease and the invasive character of plague. Science 1992; 258:1004–1007.

    Article  CAS  PubMed  Google Scholar 

  102. Jagels MA, Travis J, Potempa J et al. Proteolytic inactivation of the leukocyte C5a receptor by proteinases derived from Porphyromonas gingivalis. Infect Immun 1996; 64:1984–1991.

    CAS  PubMed  Google Scholar 

  103. Discipio RG, Daffern PJ, Kawahara M et al. Cleavage of human complement component C5 by cysteine proteinases from Porphyromonas (Bacteroides) gingivalis. Prior oxidation of C5 augments proteinase digestion of C5. Immunology 1996; 87:660–667.

    Article  CAS  PubMed  Google Scholar 

  104. Jagels MA, Ember JA, Travis J et al. Cleavage of the human C5A receptor by proteinases derived from Porphyromonas gingivalis: cleavage of leukocyte C5a receptor. Adv Exp Med Biol 1996; 389:155–164.

    CAS  PubMed  Google Scholar 

  105. Schenkein HA, Fletcher HM, Bodnar M et al. Increased opsonization of a prtH-defective mutant of Porphyromonas gingivalis W83 is caused by reduced degradation of complement-derived opsonins. J Immunol 1995; 154:5331–5337.

    CAS  PubMed  Google Scholar 

  106. Grenier D. Inactivation of human serum bactericidal activity by a trypsinlike protease isolated from Porphyromonas gingivalis. Infect Immun 1992; 60:1854–1857.

    CAS  PubMed  Google Scholar 

  107. Popadiak K, Potempa J, Riesbeck K et al. Biphasic effect of gingipains from Porphyromonas gingivalis on the human complement system. J Immunol 2007; 178:7242–7250.

    CAS  PubMed  Google Scholar 

  108. Wingrove JA, DiScipio RG, Chen Z et al. Activation of complement components C3 and C5 by a cysteine proteinase (gingipain-1) from Porphyromonas (Bacteroides) gingivalis. J Biol Chem 1992; 267:18902–18907.

    CAS  PubMed  Google Scholar 

  109. Slaney JM, Curtis MA. Mechanisms of evasion of complement by Porphyromonas gingvalis. Front Biosci 2008; 13:188–196.

    Article  CAS  PubMed  Google Scholar 

  110. Slaney JM, Gallagher A, Aduse-Opoku J et al. Mechanisms of resistance of Porphyromonas gingivalis to killing by serum complement. Infect Immun 2006; 74:5352–5361.

    Article  CAS  PubMed  Google Scholar 

  111. Lathem WW, Price PA, Miller VL et al. A plasminogen-activating protease specifically controls the development of primary pneumonic plague. Science 2007; 315:509–513.

    Article  CAS  PubMed  Google Scholar 

  112. Blom AM, Rytkonen A, Vasquez P et al. A novel interaction between Type IV pili of Neisseria gonorrhoeae and the human complement regulator C4B-binding protein. J Immunol 2001; 166:6764–6770.

    CAS  PubMed  Google Scholar 

  113. Ram S, Cullinane M, Blom A et al. Binding of C4b-binding Protein to Porin: A molecular mechanism of serum resistance of Neisseria gonorrhoeae. J Exp Med 2001; 193:281–296.

    Article  CAS  PubMed  Google Scholar 

  114. Nordstrom T, Blom AM, Forsgren A et al. The emerging pathogen Moraxella catarrhalis interacts with complement inhibitor C4b binding protein through ubiquitous surface proteins A1 and A2. J Immunol 2004; 173:4598–4606.

    PubMed  Google Scholar 

  115. Attia AS, Ram S, Rice PA et al. Binding of vitronectin by the Moraxella catarrhalis UspA2 protein interferes with late stages of the complement cascade. Infect Immun 2006; 74:1597–1611.

    Article  CAS  PubMed  Google Scholar 

  116. Ngampasutadol J, Ram S, Blom AM et al. Human C4b-binding protein selectively interacts with Neisseria gonorrhoeae and results in species-specific infection. Proc Natl Acad Sci USA 2005; 102:17142–17147.

    Article  CAS  PubMed  Google Scholar 

  117. Arko RJ, Kraus SJ, Brown WJ et al. Neisseria gonorrhoeae: effects of systemic immunization on resistance of chimpanzees to urethral infection. J Infect Dis 1974; 130:160–164.

    CAS  PubMed  Google Scholar 

  118. Stevenson B, El-Hage N, Hines MA et al. Differential binding of host complement inhibitor factor H by Borrelia burgdorferi Erp surface proteins: a possible mechanism underlying the expansive host range of Lyme disease spirochetes. Infect Immun 2002; 70:491–497.

    Article  CAS  PubMed  Google Scholar 

  119. Bartra SS, Styer KL, O’Bryant DM et al. Resistance of Yersinia pestis to Complement-Dependent Killing is Mediated by the Ail Outer Membrane Protein. Infect Immun 2008; 76 (2):612–622.

    Article  CAS  PubMed  Google Scholar 

  120. Heffernan EJ, Reed S, Hackett J et al. Mechanism of resistance to complement-mediated killing of bacteria encoded by the Salmonella typhimurium virulence plasmid gene rck. J Clin Invest 1992; 90:953–964.

    Article  CAS  PubMed  Google Scholar 

  121. Bliska JB, Falkow S. Bacterial resistance to complement killing mediated by the Ail protein of Yersinia enterocolitica. Proc Natl Acad Sci USA 1992; 89:3561–3565.

    Article  CAS  PubMed  Google Scholar 

  122. Joiner KA, Hammer CH, Brown EJ et al. Studies on the mechanism of bacterial resistance to complement-mediated killing. I. Terminal complement components are deposited and released from Salmonella minnesota S218 without causing bacterial death. J Exp Med 1982; 155:797–808.

    Article  CAS  PubMed  Google Scholar 

  123. Joiner KA, Hammer CH, Brown EJ et al. Studies on the mechanism of bacterial resistance to complement-mediated killing. IL C8 and C9 release C5b67 from the surface of Salmonella minnesota S218 because the terminal complex does not insert into the bacterial outer membrane. J Exp Med 1982; 155:809–919.

    Article  CAS  PubMed  Google Scholar 

  124. Joiner KA, Warren KA, Hammer C et al. Bactericidal but not nonbactericidal C5b-9 is associated with distinctive outer membrane proteins in Neisseria gonorrhoeae. J Immunol 1985; 134:1920–1925.

    CAS  PubMed  Google Scholar 

  125. Pfeiffer R. Z Hyg Infektionskr 1895; 20:215.

    Google Scholar 

  126. Thomas L, Dingle JH. Investigations of meningococcal infection. III. Bactericidal action of normal and immune sera for the meningococcus. J Clin Invest 1943; 22:375–385.

    Article  CAS  PubMed  Google Scholar 

  127. Jarvis GA, Griffiss JM. Human IgA1 blockade of IgG-initiated lysis of Neisseria meningitidis is a function of antigen-binding fragment binding to the polysaccharide capsule. J Immunol 1991; 147:1962–1967.

    CAS  PubMed  Google Scholar 

  128. Selander B, Kayhty H, Wedege E et al. Vaccination responses to capsular polysaccharides of Neisseria meningitidis and Haemophilus influenzae Type b in two C2-deficient sisters: alternative pathway-mediated bacterial killing and evidence for a novel type of blocking IgG. J Clin Immunol 2000; 20:138–149.

    Article  CAS  PubMed  Google Scholar 

  129. Hall WH, Manion RE, Zinneman HH. Blocking serum lysis of Brucella abortus by hyperimmune rabbit immunoglubulin A. J Immunol 1971; 107:41–46.

    CAS  PubMed  Google Scholar 

  130. Glenchur H, Hall WH, Zinneman HH. Blocking antibodies in rabbits infected with Brucella melitensis. Proc Soc Exp Biol Med 1959; 101:422–425.

    CAS  PubMed  Google Scholar 

  131. Guttman RM, Waisbren BA. Bacterial blocking activity of specific IgG in chronic Pseudomonas aeruginosa infection. Clin Exp Immunol 1975; 19:121–130.

    CAS  PubMed  Google Scholar 

  132. Waisbren BA, Brown I. A factor in the serum of patients with persisting infection that inhibits the bactericidal activity of normal serum against the organism that is causing the infection. J Immunol 1966; 97:431–437.

    CAS  PubMed  Google Scholar 

  133. Joiner KA, Scales R, Warren KA et al. Mechanism of action of blocking immunoglobulin G for Neisseria gonorrhoeae. J Clin Invest 1985; 76:1765–1772.

    Article  CAS  PubMed  Google Scholar 

  134. Plummer FA, Chubb H, Simonsen JN et al. Antibody to Rmp (outer membrane protein 3) increases susceptibility to gonococcal infection. J Clin Invest 1993; 91:339–343.

    Article  CAS  PubMed  Google Scholar 

  135. Kraiczy P, Skerka C, Brade V et al. Further characterization of complement regulator-acquiring surface proteins of Borrelia burgdorferi. Infect Immun 2001; 69(12):7800–7809.

    Article  CAS  PubMed  Google Scholar 

  136. Alitalo A, Meri T, Lankinen H et al. Complement inhibitor factor H binding to Lyme disease spirochetes is mediated by inducible expression of multiple plasmid-encoded outer surface protein E paralogs. J Immunol 2002; 169(7):3847–3853.

    Google Scholar 

  137. Pausa M, Pellis V, Cinco M et al. Serum-resistant strains of Borrelia burgdorferi evade complement-mediated killing by expressing a CD59-like complement inhibitory molecule. J Immunol 2003; 170(6):3214–3222.

    CAS  PubMed  Google Scholar 

  138. McDowell JV, Wolfgang J, Tran E et al. Comprehensive analysis of the factor h binding capabilities of borrelia species associated with lyme disease: delineation of two distinct classes of factor H binding proteins. Infect Immun 2003; 71(6):3597–3602.

    Article  CAS  PubMed  Google Scholar 

  139. Hovis KM, McDowell JV, Griffin L et al. Identification and characterization of a linear-plasmid-encoded factor H-binding protein (FhbA) of the relapsing fever spirochete Borrelia hermsii. J Bacteriol 2004; 186(9):2612–2618.

    Article  CAS  PubMed  Google Scholar 

  140. Meri T, Cutler SJ, Blom AM et al. Relapsing fever spirochetes Borrelia recurrentis and B. Duttonii acquire complement regulators C4b-binding protein and factor H. ti Infect Immun 2006; 74(7):4157–4163.

    Article  CAS  Google Scholar 

  141. McDowell JV, Frederick J, Stamm L et al. Identification of the gene encoding the FhbB protein of Treponema denticola, a highly unique factor H-like protein 1 binding protein. Infect Immun 2007; 75(2):1050–1054.

    Article  CAS  PubMed  Google Scholar 

  142. McDowell JV, Lankford J, Stamm L et al. Demonstration of factor H-like protein 1 binding to Treponema denticola, a pathogen associated with periodontal disease in humans. Infect Immun 2005; 73(11):7126–7132.

    Article  CAS  PubMed  Google Scholar 

  143. Gros P, Milder FJ, Janssen BJ. Complement driven by conformational changes. Nat Rev Immunol 2008; 8(1):48–58.

    Article  CAS  PubMed  Google Scholar 

  144. Marr N, Luu RA, Fernandez RC. Bordetella pertussis binds human C1 esterase inhibitor during the virulent phase, to evade complement-mediated killing. J Infect Dis 2007; 195:585–588.

    Article  CAS  PubMed  Google Scholar 

  145. China B, Sory MP, N’Guyen BT et al. Role of the YadA protein in prevention of opsonization of Yersinia enterocolitica by C3b molecules. Infect Immun 1993; 61:3129–3136.

    CAS  PubMed  Google Scholar 

  146. Ram S, McQuillen DP, Gulati S et al. 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 1998; 188:671–680.

    Article  CAS  PubMed  Google Scholar 

  147. Madico G, Welsch JA, Lewis LA et al. The meningococcal vaccine candidate GNA1870 binds the complement regulatory protein factor H and enhances serum resistance. J Immunol 2006; 177:501–510.

    CAS  PubMed  Google Scholar 

  148. Kunert A, Losse J, Gruszin C et al. Immune evasion of the human pathogen Pseudomonas aeruginosa: elongation factor Tuf is a factor H and plasminogen binding protein. J Immunol 2007; 179:2979–2988.

    CAS  PubMed  Google Scholar 

  149. Prasadarao NV, Blom AM, Villoutreix BO et al. A novel interaction of outer membrane protein A with C4b binding protein mediates serum resistance of Escherichia coli K1. J Immunol 2002; 169:6352–6360.

    CAS  PubMed  Google Scholar 

  150. Berggard K, Johnsson E, Mooi FR et al. Bordetella pertussis binds the human complement regulator C4BP: role of filamentous hemagglutinin. Infect Immun 1997; 65:3638–3643.

    CAS  PubMed  Google Scholar 

  151. Jarva H, Ram S, Vogel U et al. Binding of the complement inhibitor C4bp to serogroup B Neisseria meningitidis. J Immunol 2005; 174:6299–6307.

    CAS  PubMed  Google Scholar 

  152. Hallstrom T, Jarva H, Riesbeck K et al. Interaction with C4b-binding protein contributes to nontypeable Haemophilus influenzae serum resistance. J Immunol 2007; 178:6359–6366.

    PubMed  Google Scholar 

  153. Hallstrom T, Trajkovska E, Forsgren A et al. Haemophilus influenzae surface fibrils contribute to serum resistance by interacting with vitronectin. J Immunol 2006; 177:430–436.

    PubMed  Google Scholar 

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Authors and Affiliations

  1. Medical Microbiology, HP G04.614, University Medical Center Utrecht, The Netherlands

    Ilse Jongerius & Suzan Rooijakkers

  2. Division of Infectious Diseases and Immunology, University of Massachusetts Medical School, Worcester, Massachusetts, USA

    Sanjay Ram

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  1. Ilse Jongerius
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  2. Sanjay Ram
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Correspondence to Suzan Rooijakkers .

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  1. Inflammation and Immunity Group, Institute of Molecular Medicine, Trinity College, Dublin, Ireland

    Padraic G. Fallon BSc, MSc, PhD

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Jongerius, I., Ram, S., Rooijakkers, S. (2009). Bacterial Complement Escape. In: Fallon, P.G. (eds) Pathogen-Derived Immunomodulatory Molecules. Advances in Experimental Medicine and Biology, vol 666. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-1601-3_3

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