Complement-resistance mechanisms of bacteria

Microbes and Infection

Volumn 1, Issue 10, 1999, Pages 785-794

  Riina Rautemaa, Seppo Meri ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

Author keywords

GPI; Salmonella; Streptococcus; Vaccine; Virulence

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; MEMBRANE PROTEIN; MEMBRANE RECEPTOR; PEPTIDOGLYCAN;

ANTIGEN RECOGNITION; BACTERIAL MEMBRANE; BACTERIAL VIRULENCE; BACTERIOLYSIS; BACTERIUM; COMPLEMENT ACTIVATION; COMPLEMENT INHIBITION; COMPLEMENT SYSTEM; NONHUMAN; OPSONIZATION; PATHOGENICITY; PHAGOCYTOSIS; PRIORITY JOURNAL; REVIEW; SALMONELLA; STREPTOCOCCUS;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; POSIBACTERIA; SALMONELLA; STREPTOCOCCUS;

EID: 0032707516     PISSN: 12864579     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1286-4579(99)80081-1     Document Type: Review

References (91)

1. Brown E.J., Joiner K.A., Frank M.M., The role of complement in host resistance to bacteria, Springer Semin. Immunopathol. 6 (1983) 349-360.
2. Fearon D.T., The complement system and adaptive immunity, Semin. Immunol. 10 (1998) 355-361.
3. Born J., Bhakdi S., Does complement kill E. coli by producing transmural pores? Immunology 59 (1986) 139-145.
4. Joiner K.A., Schmetz M.A., Sanders M.E., Murray T.G., Hammer C.H., Dourmashkin R., Frank M.M., Multimeric complement component C9 is necessary for killing of Escherichia colt J5 by terminal attack complex C5b-9, Proc. Natl. Acad. Sci. USA 82 (1985) 4808-4812.
5. Tomlinson S., Taylor P.W., Morgan B.P., Luzio J.P., Killing of Gram-negative bacteria by complement, Biochem. J. 263 (1989) 505-511.
6. Morgan B.P., Meri S., Membrane proteins that protect against complement lysis, Springer Semin. Immunopathol. 15 (1994) 369-396.
7. Davies A., Simmons D.L., Hale G., Harrison R.A., Tighe H., Lachmann P.J., Waldmann H., CD59 an LY-6-like protein expressed in human lymphoid cells regulates the action of the complement membrane attack complex on homologous cells, J. Exp. Med. 170 (1989) 637-654.
8. Meri S., Morgan B.P., Davies A., Daniels R.H., Olavesen M.G., Waldmann H., Lachmann P.J., Human protectin (CD59) an 18000-20000 MW complement lysis restricting factor inhibits C5b-8 catalysed insertion of C9 into lipid bilayers, Immunology 71 (1990) 1-9.
9. Rollins S.A., Sims P.J., The complement-inhibitory activity of CD59 resides in its capacity to block incorporation of C9 into membrane C5b-9, J. Immunol. 144 (1990) 3478-3483.
10. Medof M.E., Walter E.I., Rutgers J.L., Knowles D.M., Nussenzweig V., Identification of the complement decayaccelerating factor (DAF) on epithelium and glandular cells and in body fluids, J. Exp. Med. 165 (1987) 848-864.
11. Lehto T., Meri S., Interactions of soluble CD59 with terminal complement complexes, J. Immunol. 151 (1993) 4941-4949.
12. Meri S., Lehto T., Sutton C.W., Tyynelä J., Baumann M., Structural composition and functional characterization of soluble CD59: heterogeneity of the oligosaccharide and glycophosphoinositol (GPI) anchor revealed by laser-desorption mass spectrometric analysis, Biochem. J. 316 (1996) 923-935.
13. Väkevä A., Jauhiainen M., Ehnholm C., Lehto T., Meri S., High-density lipoproteins can act as carriers of glycophosphoinositol lipid-anchored CD59 in human plasma, Immunology 82 (1994) 28-33.
14. Kooyman D.L., Byrne G.W., Me Clellan S., Nielsen D., Tone M., Waldmann H., Coffman T.M., McCurry K.R., Platt J.L., Logan J.S., In vivo transfer of GPI-linked complement restriction factors from erythrocytes to the endothelium, Science 269 (1995) 89-92.
15. Isaacs S.N., Kotwal G.J., Moss B., Vaccinia virus complement-control protein prevents antibody-dependent complement-enhanced neutralization of infectivity and contributes to virulence, Proc. Natl. Acad. Sci. USA 89 (1992) 628-632.
16. Albrecht J.C., Nicholas J., Cameron K.R., Newman C., Fleckenstein B., Honess R.W., Herpervirus saimiri has a gene specifying a homologue of the cellular membrane glycoprotein CD59, Virology 190 (1992) 527-530.
17. Tenner A.J., Ziccardi R.J., Cooper N.R., Antibody-independent Cl activation by E. coli, J. Immunol. 133 (1984) 886-891.
18. Joiner K.A., Hammer C.H., Brown E.J., Cole R.J., Frank M.M., 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. 155 (1982) 797-808.
19. Joiner K.A., Grossman N., Schmetz M., Leive L., C3 binds preferentially to long-chain lipopolysaccharide during alternative pathway activation by Salmonella Montevideo, J. Immunol. 136 (1986) 710-715.
20. Grossman N., Svenson S.B., Leive L., Lindberg A.A., Salmonella O antigen-specific oligosaccharide-octyl conjugates activate complement via the alternative pathway at different rates depending on the structure of the O antigen, Mol. Immunol. 27 (1990) 859-865.
21. Merino S., Camprubi S., Alberti S., Benedi V.J., Tomas J.M., Mechanisms of Klebsiella pneumoniae resistance to complement-mediated killing, Infect. Immun. 60 (1992) 2529-2535.
22. Vishwanath S., Hackstadt T., Lipopolysaccharide phase variation determines the complement-mediated serum susceptibility of Coxiella burnetii, Infect. Immun. 56 (1988) 40-44.
23. Fearon D.T., Regulation by membrane sialic acid of betalH-dependent decay-dissociation of amplification C3 convertase of the alternative complement pathway, Proc. Natl. Acad. Sci. USA 75 (1978) 1971-1975.
24. Pangburn M.K., Müller-Eberhard H.J., Complement C3 convertase: cell surface restriction of β1H control and generation of restriction on neuraminidase-treated cells, Proc. Natl. Acad. Sci. USA 75 (1978) 2416-2420.
25. Meri S., Pangburn M.K., A mechanism of activation of the alternative complement pathway by the classical pathway: protection of C3b from inactivation by covalent attachment to C4b, Eur. J. Immunol. 20 (1990) 2555-2561.
26. Mandrell R.E., Lesse A.J., Sugai J.V., Shero M., Griffiss J.M., Cole J.A., Parsons N.J., Smith H., Morse S.A., Apicella M.A., In vitro and in vivo modification of Neisseria gonorrhoeae lipooligosaccharide epitope structure by sialylationj. Exp. Med. 171 (1990) 1649-1664.
27. Jarvis G.A., Analysis of C3 deposition and degradation on Neisseria meningitidis and Neisseria gonorrhoeae, Infect. Immun. 62 (1994) 1755-1760.
28. VanPutten J.P., Phase variation of lipopolysaccharide directs interconversion of invasive and immuno-resistant phenotypes of Neisseria gonorrhoeae, EMBO J. 12 (1993) 4043-4051.
29. 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 (1998) 743-752.
30. Estabrook M.M., Griffiss J.M., Jarvis G.A., Sialylation of Neisseria meningitidis lipooligosaccharide inhibits serum bactericidal activity by masking lacto-N-neotetraose, Infect. Immun. 65 (1997) 4436-4444.
31. Egan A.M., Gordon D.L., Burkholderia pseudomallei activates complement and is ingested but not killed by polymorphonuclear leukocytes, Infect. Immun. 64 (1996) 4952-4959.
32. Joiner K.A., Hammer C.H., Brown E.J., Frank M.M., Studies on the mechanism of bacterial resistance to complement-mediated killing. II. 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. 155 (1982) 809-819.
33. Wilkinson B.J., Sisson S.P., Kim Y., Peterson P.K., Localization of the third component of complement on the cell wall of encapsulated Staphylococcus aureus M: implications for the mechanism of resistance to phagocytosis, Infect. Immun. 26 (1979) 1159-1163.
34. Winkelstein J.A., Abramovitz A.S., Tomasz A., Activation of C3 via the alternative complement pathway results in fixation of C3b to the pneumococcal cell wall, J. Immunol. 124 (1980) 2502-2506.
35. Taylor P.W., Robinson M.K., Determinants that increase the serum resistance of Escherichia coli, Infect. Immun. 29 (1980) 278-280.
36. Thakker M., Park J.S., Carey V., Lee J.C., Staphylococcus aureus serotype 5 capsular polysaccharide is antiphagocytic and enhances bacterial virulence in a murine bacteremia model, Infect. Immun. 66 (1998) 5183-5189.
37. Corn P.G., Anders J., Takala A.K., Kayhty H., Hoiseth S.K., Genes involved in Haemophilus influenzae type b capsule expression are frequently amplified, J. Infect. Dis. 167 (1993) 356-364.
38. Noel G.J., Brittingham A., Granato A.A., Mosser D.M., Effect of amplification of the Cap b locus on complementmediated bacteriolysis and opsonization of type b Haemophilus influenzae, Infect. Immun. 64 (1996) 4769-4775.
39. Craven D.E., Peppier M.S., Frasch C.E., Mocca L.F., McGrath P.P., Washington G., Adherence of isolates of Neisseria meningitidis from patients and carriers to human buccal epithelial cells, J. Infect. Dis. 142 (1980) 556-568.
40. Marques M.B., Kasper D.L., Pangburn M.K., Wessels M.R., Prevention of C3 deposition by capsular polysaccharide is a virulence mechanism of type III group B streptococci, Infect. Immun. 60 (1992) 3986-3993.
41. Meri S., Pangburn M.K., Discrimination between activators and nonactivators of the alternative pathway of complement: regulation via a sialic acid/polyanion binding site on factor H, Proc. Natl. Acad. Sci. USA 87 (1990) 3982-3986.
42. Ward C.K., Inzana T.J., Resistance of Actinobacillus pleuropneumoniae to bactericidal antibody and complement is mediated by capsular polysaccharide and blocking antibody specific for lipopolysaccharide, J. Immunol. 153 (1994) 2110-2121.
43. Mold C., Gewurz H., Inhibitory effect of C-reactive protein on alternative C pathway activation by liposomes and Streptococcus pneumoniae, J. Immunol. 127 (1981) 2089-2092.
44. Aronen M., Lehto T., Meri S., Regulation of alternative pathway complement activation by an interaction of C-reactive protein with factor H, Immunol. Infect. Dis. 3 (1993) 83-87.
45. Weis J.J., Law S.K., Levine R.P., Cleary P.P., Resistance to phagocytosis by group A streptococci: failure of deposited complement opsonins to interact with cellular receptors, J. Immunol. 134 (1985) 500-505.
46. Whitnack E., Dale J.B., Beachey E.H., Common protective antigens of group A streptococcal M proteins masked by fibrinogen, J. Exp. Med. 159 (1984) 1201-1212.
47. Fischetti V.A., Streptococcal M protein: molecular design and biological behavior, Clin. Microb. Rev. 2 (1989) 285-314.
48. Horstmann R.D., Sievertsen HJ., Knobloch J., Fischetti V.A., Anuphagocytic activity of streptococcal M protein: selective binding of complement control protein factor H, Proc. Natl. Acad. Sci. USA 85 (1988) 1657-1661.
49. 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.
50. Them A., Wastfelt M., Lindahl G., Expression of two different antiphagocytic M proteins by Streptococcus pyogenes of the OF+ lineage, J. Immunol. 160 (1998) 860-869.
51. Johnsson E., Andersson G., Lindahl G., Heden L.O., Identification of the IgA-binding region in streptococcal protein Arp, J. Immunol. 153 (1994) 3557-3564.
52. Berge A., Kihlberg B.M., Sjoholm A.G., Bjorck L., Streptococcal protein H forms soluble complement-activating complexes with IgG but inhibits complement activation by IgG-coated targets, J. Biol. Chem. 272 (1997) 20774-20781.
53. Them A., Stenberg L., Dahlback B., Lindahl G., Igbinding 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.
54. Johnsson E., Them A., Dahlback B., Heden L.O., Wikstrom 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.
55. Berggard K., Johnsson E., Mooi F.R., Lindahl G., Bordetella pertussis binds the human complement regulator C4BP: role of filamentous hemagglutinin, Infect. Immun. 65 (1997) 3638-3643.
56. Knapp J.S., Tarn M.R., Nowinski R.C., Holmes K.K., Sandstrom E.G., Serological classification of Neisseria gonorrhoeae with use of monoclonal antibodies to gonococcal outer membrane protein I, J. Infect. Dis. 150 (1984) 44-48.
57. 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 gonorrhoeas, J. Exp. Med. 188 (1998) 671-680.
58. James J.F., Swanson J., Studies on gonococcus infection. XIII. Occurrence of color/opacity colonial variants in clinical cultures, Infect. Immun. 19 (1978) 332-340.
59. Chen T., Swanson J., Wilson J., Belland R.J., Heparin protects Opa+ Neisseria gonorrhoeas from the bactericidal action of normal human serum, Infect. Immun. 63 (1995) 1790-1795.
60. Bliska J.B., Falkow S., Bacterial resistance to complement killing mediated by the Ail protein of Yersinia enterocolitica, Proc. Natl. Acad. Sci. USA 89 (1992) 3561-3565.
61. Pilz D., Vocke T., Heesemann J., Brade V., Mechanism of YadA-mediated serum resistance of Yersinia enterocolitica serotype O3, Infect. Immun. 60 (1992) 189-195.
62. China B., Sory M.P., N'guyen B.T., DeBruyere M., Cornelis G.R., Role of the YadA protein in prevention of opsonization of Yersinia enterocolitica by C3b molecules, Infect. Immun. 61 (1993) 3129-3136.
63. Rossi V., Tatar L.D., Beer K.B., Miller V.L., Esser A.F., Structural studies of Ail-mediated resistance of E. coli to killing by complement, Mol. Immunol. 35 (1998) 397.
64. Heffernan E.J., Wu L., Louie J., Okamoto S., Fierer J., Guiney D.G., Specificity of the complement resistance and cell association phenotypes encoded by the outer membrane protein genes rck from Salmonella typhimurium and ail from Yersinia enterocolitica, Infect. Immun. 62 (1994) 5183-5186.
65. Pramoonjago P., Kaneko M., Kinoshita T., Ohtsubo E., Takeda J., Hong K.S., Inagi R., Inoue K., Role of TraT protein an anticomplementary protein produced in Escherichia coli by R100 factor in serum resistance, J. Immunol. 148 (1992) 827-836.
66. Akesson P., Sjoholm A.G., Bjorck L., Protein SIC a novel extracellular protein of Streptococcuspyogenes interfering with complement function, J. Biol. Chem. 271 (1996) 1081-1088.
67. Schultz D.R., Miller K.D., Elastase of Pseudomonas aeruginosa: inactivation of complement components and complement-derived chemotactic and phagocytic factors, Infect. Immun. 10 (1974) 128-135.
68. Schenkein H.A., The effect of periodontal proteolytic Bacteroides species on proteins of the human complement systemj. Periodont. Res. 23 (1988) 187-192.
69. Chen Z., Potempa J., Polanowski A., Wikstrom M., Travis J., Purification and characterization of a 50-kDa cysteine proteinase (gingipain) from Porphyromonas gingivalis, J. Biol. Chem. 267 (1992) 18896-18901.
70. Schenkein H.A., Failure of Bacteroides gingivalis W83 to accumulate bound C3 following opsonization with serum, J. Periodont. Res. 24 (1989) 20-27.
71. Wingrove J.A., Discipio R.G., Chen Z., Potempa J., Travis J., Hugli T.E., Activation of complement components C3 and C5 by a cysteine proteinase (gingipain-1) from Porphyromonas (Bacteroides) gingivalis, J. Biol. Chem. 267 (1992) 18902-18907.
72. Takahashi S., Nagano Y., Nagano N., Hayashi O., Taguchi F., Okuwaki Y., Role of C5a-ase in group B streptococcal resistance to opsonophagocytic killing, Infect. Immun. 63 (1995) 4764-4769.
73. Kuusela P., Ullberg M., Saksela O., Kronvall G., Tissue-type plasminogen activator-mediated activation of plasminogen on the surface of group A C and G streptococci, Infect. Immun. 60 (1992) 196-201.
74. 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 (1982) 1054-1058.
75. Jarvis G.A., Griffiss J.M., Human IgAl blockade of IgG-initiated lysis of Neisseria meningitidis is a function of antigen-binding fragment binding to the polysaccharide capsule, J. Immunol. 147 (1991) 1962-1967.
76. Joiner K.A., Scales R., Warren K.A., Frank M.M., Rice P.A., Mechanism of action of blocking immunoglobulin G for Neisseria gonorrhoeae, J. Clin. Invest. 76 (1985) 1765-1772.
77. Hamadeh R.M., Jarvis G.A., Galili U., Mandrell R.E., Zhou P., Griffiss J.M., Human natural anti-Gal IgG regulates alternative complement pathway activation on bacterial surfaces, J. Clin. Invest. 89 (1992) 1223-1235.
78. Hoffmann E.M., Houle J.J., Contradictory roles for antibody and complement in the interaction of Brucella abortus with its host, Crit. Rev. Microbiol. 21 (1995) 153-163.
79. Schlesinger L.S., Horwitz M.A., Phagocytosis of Mycobacterium leprae by human monocyte-derived macrophages is mediated by complement receptors CRI (CD35) CR3 (GD11b/CD18) and CR4 (GD11c/CD18) and IFN-gamma activation inhibits complement receptor function and phagocytosis of this bacterium, J. Immunol. 147 (1991) 1983-1994.
80. Schorey J.S., Carroll M.C., Brown E.J., A macrophage invasion mechanism of pathogenic mycobacteria, Science 277 (1997) 1091-1093.
81. Kaul A., Nowicki B.J., Martens M.G., Goluszko P., Hart A., Nagamani M., Kumar D., Pham T.Q., Nowicki S., Decay-accelerating factor is expressed in the human endometrium and may serve as the attachment ligand for Dr pili of Escherichia coli, Am. J. Reprod. Immunol. 32 (1994) 194-199.
82. Nowicki B., Hart A., Coyne K.E., Lublin D.M., Nowicki S., Short consensus repeat-3 domain of recombinant decayaccelerating factor is recognized by Escherichia coli recombinant Dr adhesin in a model of a cell-cell interaction, J. Exp. Med. 178 (1993) 2115-2121.
83. Rautemaa R., Jarvis G.A., Marnila P., Meri S., Acquired resistance of Escherichia coli to complement lysis by binding of glycophosphoinositol-anchored protectin (CD59), Infect. Immun. 66 (1998) 1928-1933.
84. Beachey E.H., Dale J.B., Simpson W.A., Evans J.D., Knox K.W., Ofek I., Wicken A.J., Erythrocyte binding properties of streptococcal lipoteichoic acids, Infect. Immun. 23 (1979) 618-625.
85. Hummell D.S., Winkelstein J.A., Bacterial lipoteichoic acid sensitizes host cells for destruction by autologous complement, J. Clin. Invest. 77 (1986) 1533-1538.
86. Kochi S.K., Johnson R.C., Dalmasso A.P., Facilitation of complement-dependent killing of the Lyme disease spirochete Borrelia burgdorferi by specific immunoglobulin G Fab antibody fragments, Infect. Immun. 61 (1993) 2532-2536.
87. Breitner-Ruddock S., Wurzner R., Schulze J., Brade V., Heterogeneity in the complement-dependent bacteriolysis within the species of Borrelia burgdorferi, Med. Microb. Immunol. 185 (1997) 253-260.
88. Verduin C.M., Jansze M., Hoi C., Mollnes T.E., Verhoef J., VanDijk H., Differences in complement activation between complement-resistant and complement-sensitive Moraxella (Branhamella) catarrhalis strains occur at the level of membrane attack complex formation, Infect. Immun. 62 (1994) 589-595.
89. Joiner K.A., Warren K.A., Brown E.J., Swanson J., Frank M.M., Studies on the mechanism of bacterial resistance to complement-mediated killing. IV. C5b-9 forms high molecular weight complexes with bacterial outer membrane constituents on serum-resistant but not on serum-sensitive Neisseria gonorrhoeae, J. Immunol. 131 (1983) 1443-1451.
90. Wexler D.E., Chenoweth D.E., deary P.P., Mechanism of action of the group A streptococcal C5a inactivator. Proc. Natl. Acad. Sci. USA 82 (1985) 8144-8148.
91. O'Connor S.P., Cleary P.P., In vivo Streptococcus pyogenes C5a peptidase activity: analysis using transposon- and nitrosoguanidine-induced mutants, J. Infect. Dis. 156 (1987) 495-504.