Inhibition of the classical pathway of complement by meningococcal capsular polysaccharides

Journal of Immunology

Volumn 193, Issue 4, 2014, Pages 1855-1863

  Agarwal, Sarika ^a   Vasudhev, Shreekant ^a   DeOliveira, Rosane B ^a   Ram, Sanjay ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL POLYSACCHARIDE; COMPLEMENT COMPONENT C1; COMPLEMENT COMPONENT C1Q; COMPLEMENT COMPONENT C4; COMPLEMENT COMPONENT C4B; COMPLEMENT FACTOR H; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; MENINGOCOCCUS VACCINE; SIALIC ACID;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANTIGEN BINDING; ARTICLE; BACTERIAL CAPSULE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERICIDAL ACTIVITY; BACTERIUM ISOLATE; CELL ENCAPSULATION; COMPLEMENT CLASSICAL PATHWAY; COMPLEMENT DEPENDENT CYTOTOXICITY; COMPLEMENT DEPOSITION; COMPLEMENT INHIBITION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DILUTION; FLOW CYTOMETRY; MENINGOCOCCOSIS; MULTILOCUS SEQUENCE TYPING; NEISSERIA MENINGITIDIS; NONHUMAN; NUCLEOPHILICITY; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; SIALYLATION; SUPERNATANT; WESTERN BLOTTING;

ANTIBODIES, MONOCLONAL; ANTIGENS, BACTERIAL; BACTERIAL CAPSULES; BACTERIAL PROTEINS; COMPLEMENT C1Q; COMPLEMENT C4B; COMPLEMENT PATHWAY, CLASSICAL; HUMANS; IMMUNE EVASION; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; LIPOPOLYSACCHARIDES; NEISSERIA MENINGITIDIS; PORINS;

EID: 84905974907     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1303177     Document Type: Article

References (66)

1. Flexner, S. 1913. The results of the serum treatment in thirteen hundred cases of epidemic meningitis. J. Exp. Med. 17: 553-576.
2. Flexner, S. , and J. W. Jobling. 1908. An analysis of four hundred cases of epidemic meningitis treated with the anti-meningitis serum. J. Exp. Med. 10: 690-733.
3. Goldschneider, I. , E. C. Gotschlich, and M. S. Artenstein. 1969. Human immunity to the meningococcus. I. The role of humoral antibodies. J. Exp. Med. 129: 1307-1326.
4. Jones, G. R. , J. N. Williams, M. Christodoulides, K. Jolley, and J. E. Heckels. 2000. Lack of immunity in university students before an outbreak of serogroup C meningococcal infection. J. Infect. Dis. 181: 1172-1175.
5. Yazdankhah, S. P. , and D. A. Caugant. 2004. Neisseria meningitidis: an overview of the carriage state. J. Med. Microbiol. 53: 821-832.
6. Goldschneider, I. , E. C. Gotschlich, and M. S. Artenstein. 1969. Human immunity to the meningococcus. II. Development of natural immunity. J. Exp. Med. 129: 1327-1348.
7. Findlow, H. , U. Vogel, J. E. Mueller, A. Curry, B. M. Njanpop-Lafourcade, H. Claus, S. J. Gray, S. Yaro, Y. Traoré, L. Sangaré, et al. 2007. Three cases of invasive meningococcal disease caused by a capsule null locus strain circulating among healthy carriers in Burkina Faso. J. Infect. Dis. 195: 1071-1077.
8. Hoang, L. M. , E. Thomas, S. Tyler, A. J. Pollard, G. Stephens, L. Gustafson, A. McNabb, I. Pocock, R. Tsang, and R. Tan. 2005. Rapid and fatal meningococcal disease due to a strain of Neisseria meningitidis containing the capsule null locus. Clin. Infect. Dis. 40: e38-e42.
9. Vogel, U. , H. Claus, L. von M̈uller, D. Bunjes, J. Elias, and M. Frosch. 2004. Bacteremia in an immunocompromised patient caused by a commensal Neisseria meningitidis strain harboring the capsule null locus (cnl). J. Clin. Microbiol. 42: 2898-2901.
10. Caugant, D. A. , and M. C. Maiden. 2009. Meningococcal carriage and disease: population biology and evolution. Vaccine 27(Suppl. 2): B64-B70.
11. Claus, H. , M. C. Maiden, D. J. Wilson, N. D. McCarthy, K. A. Jolley, R. Urwin, F. Hessler, M. Frosch, and U. Vogel. 2005. Genetic analysis of meningococci carried by children and young adults. J. Infect. Dis. 191: 1263-1271.
12. Masignani, V. , M. Comanducci, M. M. Giuliani, S. Bambini, J. Adu-Bobie, B. Arico, B. Brunelli, A. Pieri, L. Santini, S. Savino, et al. 2003. Vaccination against Neisseria meningitidis using three variants of the lipoprotein GNA1870. J. Exp. Med. 197: 789-799.
13. Fletcher, L. D. , L. Bernfield, V. Barniak, J. E. Farley, A. Howell, M. Knauf, P. Ooi, R. P. Smith, P. Weise, M. Wetherell, et al. 2004. Vaccine potential of the Neisseria meningitidis 2086 lipoprotein. Infect. Immun. 72: 2088-2100.
14. Madico, G. , J. A. Welsch, L. A. Lewis, A. McNaughton, D. H. Perlman, C. E. Costello, J. Ngampasutadol, U. Vogel, D. M. Granoff, and S. Ram. 2006. The meningococcal vaccine candidate GNA1870 binds the complement regulatory protein factor H and enhances serum resistance. J. Immunol. 177: 501-510.
15. Schneider, M. C. , B. E. Prosser, J. J. Caesar, E. Kugelberg, S. Li, Q. Zhang, S. Quoraishi, J. E. Lovett, J. E. Deane, R. B. Sim, et al. 2009. Neisseria meningitidis recruits factor H using protein mimicry of host carbohydrates. Nature 458: 890-893.
16. Seib, K. L. , D. Serruto, F. Oriente, I. Delany, J. Adu-Bobie, D. Veggi, B. Aricò, R. Rappuoli, and M. Pizza. 2009. Factor H-binding protein is important for meningococcal survival in human whole blood and serum and in the presence of the antimicrobial peptide LL-37. Infect. Immun. 77: 292-299.
17. Gorringe, A. R. , and R. Pajón. 2012. Bexsero: a multicomponent vaccine for prevention of meningococcal disease. Hum. Vaccin. Immunother. 8: 174-183.
18. Lewis, L. A. , J. Ngampasutadol, R. Wallace, J. E. Reid, U. Vogel, and S. Ram. 2010. The meningococcal vaccine candidate neisserial surface protein A (NspA) binds to factor H and enhances meningococcal resistance to complement. PLoS Pathog. 6: e1001027.
19. Lewis, L. A. , D. M. Vu, S. Vasudhev, J. Shaughnessy, D. M. Granoff, and S. Ram. 2013. Factor H-dependent alternative pathway inhibition mediated by porin B contributes to virulence of Neisseria meningitidis. MBio 4: e00339-e13.
20. Lewis, L. A. , M. Carter, and S. Ram. 2012. The relative roles of factor H binding protein, neisserial surface protein A, and lipooligosaccharide sialylation in regulation of the alternative pathway of complement on meningococci. J. Immunol. 188: 5063-5072.
21. Hammerschmidt, S. , C. Birkholz, U. Zähringer, B. D. Robertson, J. van Putten, O. Ebeling, and M. Frosch. 1994. Contribution of genes from the capsule gene complex (cps) to lipooligosaccharide biosynthesis and serum resistance in Neisseria meningitidis. Mol. Microbiol. 11: 885-896.
22. Kahler, C. M. , L. E. Martin, G. C. Shih, M. M. Rahman, R. W. Carlson, and D. S. Stephens. 1998. The (a2-8)-linked polysialic acid capsule and lipooligosaccharide structure both contribute to the ability of serogroup B Neisseria meningitidis to resist the bactericidal activity of normal human serum. Infect. Immun. 66: 5939-5947.
23. Mackinnon, F. G. , R. Borrow, A. R. Gorringe, A. J. Fox, D. M. Jones, and A. Robinson. 1993. Demonstration of lipooligosaccharide immunotype and capsule as virulence factors for Neisseria meningitidis using an infant mouse intranasal infection model. Microb. Pathog. 15: 359-366.
24. Vogel, U. , S. Hammerschmidt, and M. Frosch. 1996. Sialic acids of both the capsule and the sialylated lipooligosaccharide of Neisseria meningitis serogroup B are prerequisites for virulence of meningococci in the infant rat. Med. Microbiol. Immunol. (Berl. ) 185: 81-87.
25. Fearon, D. T. 1978. Regulation by membrane sialic acid of beta1H-dependent decay-dissociation of amplification C3 convertase of the alternative complement pathway. Proc. Natl. Acad. Sci. USA 75: 1971-1975.
26. Meri, S. , and M. K. Pangburn. 1990. 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: 3982-3986.
27. Severi, E. , D. W. Hood, and G. H. Thomas. 2007. Sialic acid utilization by bacterial pathogens. Microbiology 153: 2817-2822.
28. Varki, A. , and P. Gagneux. 2012. Multifarious roles of sialic acids in immunity. Ann. N. Y. Acad. Sci. 1253: 16-36.
29. Jarvis, G. A. 1994. Analysis of C3 deposition and degradation on Neisseria meningitidis and Neisseria gonorrhoeae. Infect. Immun. 62: 1755-1760.
30. Jarvis, G. A. , and N. A. Vedros. 1987. Sialic acid of group B Neisseria meningitidis regulates alternative complement pathway activation. Infect. Immun. 55: 174-180.
31. Vogel, U. , H. Claus, G. Heinze, and M. Frosch. 1997. Functional characterization of an isogenic meningococcal a-2,3-sialyltransferase mutant: the role of lipooligosaccharide sialylation for serum resistance in serogroup B meningococci. Med. Microbiol. Immunol. (Berl. ) 186: 159-166.
32. Vogel, U. , H. Claus, G. Heinze, and M. Frosch. 1999. Role of lipopolysaccharide sialylation in serum resistance of serogroup B and C meningococcal disease isolates. Infect. Immun. 67: 954-957.
33. Ram, S. , L. A. Lewis, and S. Agarwal. 2011. Meningococcal group W-135 and Y capsular polysaccharides paradoxically enhance activation of the alternative pathway of complement. J. Biol. Chem. 286: 8297-8307.
34. Harrison, O. B. , H. Claus, Y. Jiang, J. S. Bennett, H. B. Bratcher, K. A. Jolley, C. Corton, R. Care, J. T. Poolman, W. D. Zollinger, et al. 2013. Description and nomenclature of Neisseria meningitidis capsule locus. Emerg. Infect. Dis. 19: 566-573.
35. Welsch, J. A. , R. Rossi, M. Comanducci, and D. M. Granoff. 2004. Protective activity of monoclonal antibodies to genome-derived neisserial antigen 1870, a Neisseria meningitidis candidate vaccine. J. Immunol. 172: 5606-5615.
36. Ray, T. D. , L. A. Lewis, S. Gulati, P. A. Rice, and S. Ram. 2011. Novel blocking human IgG directed against the pentapeptide repeat motifs of Neisseria meningitidis Lip/H. 8 and Laz lipoproteins. J. Immunol. 186: 4881-4894.
37. Apicella, M. A. , K. M. Bennett, C. A. Hermerath, and D. E. Roberts. 1981. Monoclonal antibody analysis of lipopolysaccharide from Neisseria gonorrhoeae and Neisseria meningitidis. Infect. Immun. 34: 751-756.
38. Apicella, M. A. , M. Shero, G. A. Jarvis, J. M. Griffiss, R. E. Mandrell, and H. Schneider. 1987. Phenotypic variation in epitope expression of the Neisseria gonorrhoeae lipooligosaccharide. Infect. Immun. 55: 1755-1761.
39. Giuntini, S. , D. C. Reason, and D. M. Granoff. 2012. Combined roles of human IgG subclass, alternative complement pathway activation, and epitope density on bactericidal activity of antibodies to meningococcal factor H binding protein. Infect. Immun. 80: 187-194.
40. Gulati, S. , S. Agarwal, S. Vasudhev, P. A. Rice, and S. Ram. 2012. Properdin is critical for antibody-dependent bactericidal activity against Neisseria gonorrhoeae that recruit C4b-binding protein. J. Immunol. 188: 3416-3425.
41. Lewis, L. A. , S. Ram, A. Prasad, S. Gulati, S. Getzlaff, A. M. Blom, U. Vogel, and P. A. Rice. 2008. Defining targets for complement components C4b and C3b on the pathogenic neisseriae. Infect. Immun. 76: 339-350.
42. Ram, S. , A. D. Cox, J. C. Wright, U. Vogel, S. Getzlaff, R. Boden, J. Li, J. S. Plested, S. Meri, S. Gulati, et al. 2003. Neisserial lipooligosaccharide is a target for complement component C4b. Inner core phosphoethanolamine residues define C4b linkage specificity. J. Biol. Chem. 278: 50853-50862.
43. Carroll, M. C. , D. M. Fathallah, L. Bergamaschini, E. M. Alicot, and D. E. Isenman. 1990. Substitution of a single amino acid (aspartic acid for histidine) converts the functional activity of human complement C4B to C4A. Proc. Natl. Acad. Sci. USA 87: 6868-6872.
44. Isenman, D. E. , and J. R. Young. 1986. Covalent binding properties of the C4A and C4B isotypes of the fourth component of human complement on several C1-bearing cell surfaces. J. Immunol. 136: 2542-2550.
45. Merino, S. , S. Camprubí, S. Albertí, V. J. Benedí, and J. M. Tomás. 1992. Mechanisms of Klebsiella pneumoniae resistance to complement-mediated killing. Infect. Immun. 60: 2529-2535.
46. Joiner, K. A. , R. C. Goldman, C. H. Hammer, L. Leive, and M. M. Frank. 1983. Studies of the mechanism of bacterial resistance to complement-mediated killing. V. IgG and F(ab9)2 mediate killing of E. coli 0111B4 by the alternative complement pathway without increasing C5b-9 deposition. J. Immunol. 131: 2563-2569.
47. Rawal, N. , and M. K. Pangburn. 2003. Formation of high affinity C5 convertase of the classical pathway of complement. J. Biol. Chem. 278: 38476-38483.
48. McNeil, L. K. , E. Murphy, X. J. Zhao, S. Guttmann, S. L. Harris, A. A. Scott, C. Tan, M. Mack, I. DaSilva, K. Alexander, et al. 2009. Detection of LP2086 on the cell surface of Neisseria meningitidis and its accessibility in the presence of serogroup B capsular polysaccharide. Vaccine 27: 3417-3421.
49. Jarva, H. , S. Ram, U. Vogel, A. M. Blom, and S. Meri. 2005. Binding of the complement inhibitor C4bp to serogroup B Neisseria meningitidis. J. Immunol. 174: 6299-6307.
50. Diebolder, C. A. , F. J. Beurskens, R. N. de Jong, R. I. Koning, K. Strumane, M. A. Lindorfer, M. Voorhorst, D. Ugurlar, S. Rosati, A. J. Heck, et al. 2014. Complement is activated by IgG hexamers assembled at the cell surface. Science 343: 1260-1263.
51. Burton, D. R. , J. Boyd, A. D. Brampton, S. B. Easterbrook-Smith, E. J. Emanuel, J. Novotny, T. W. Rademacher, M. R. van Schravendijk, M. J. Sternberg, and R. A. Dwek. 1980. The Clq receptor site on immunoglobulin G. Nature 288: 338-344.
52. Duncan, A. R. , and G. Winter. 1988. The binding site for C1q on IgG. Nature 332: 738-740.
53. Kojouharova, M. S. , M. G. Gadjeva, I. G. Tsacheva, A. Zlatarova, L. T. Roumenina, M. I. Tchorbadjieva, B. P. Atanasov, P. Waters, B. C. Urban, R. B. Sim, et al. 2004. Mutational analyses of the recombinant globular regions of human C1q A, B, and C chains suggest an essential role for arginine and histidine residues in the C1q-IgG interaction. J. Immunol. 172: 4351-4358.
54. Roumenina, L. T. , M. M. Ruseva, A. Zlatarova, R. Ghai, M. Kolev, N. Olova, M. Gadjeva, A. Agrawal, B. Bottazzi, A. Mantovani, et al. 2006. Interaction of C1q with IgG1, C-reactive protein and pentraxin 3: mutational studies using recombinant globular head modules of human C1q A, B, and C chains. Biochemistry 45: 4093-4104.
55. Uria, M. J. , Q. Zhang, Y. Li, A. Chan, R. M. Exley, B. Gollan, H. Chan, I. Feavers, A. Yarwood, R. Abad, et al. 2008. A generic mechanism in Neisseria meningitidis for enhanced resistance against bactericidal antibodies. J. Exp. Med. 205: 1423-1434.
56. Brown, E. J. , J. Ramsey, C. H. Hammer, and M. M. Frank. 1983. Surface modulation of classical pathway activation: C2 and C3 convertase formation and regulation on sheep, guinea pig, and human erythrocytes. J. Immunol. 131: 403-408.
57. Albertí, S. , G. Marqués, S. Camprubí, S. Merino, J. M. Tomás, F. Vivanco, and V. J. Benedí. 1993. C1q binding and activation of the complement classical pathway by Klebsiella pneumoniae outer membrane proteins. Infect. Immun. 61: 852-860.
58. Betz, S. J. , and H. Isliker. 1981. Antibody-independent interactions between Escherichia coli J5 and human complement components. J. Immunol. 127: 1748-1754.
59. Bredt, W. , B. Wellek, H. Brunner, and M. Loos. 1977. Interactions between mycoplasma pneumoniae and the first components of complement. Infect. Immun. 15: 7-12.
60. Clas, F. , and M. Loos. 1981. 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. 31: 1138-1144.
61. Mintz, C. S. , P. I. Arnold, W. Johnson, and D. R. Schultz. 1995. Antibodyindependent binding of complement component C1q by Legionella pneumophila. Infect. Immun. 63: 4939-4943.
62. Tenner, A. J. , R. J. Ziccardi, and N. R. Cooper. 1984. Antibody-independent C1 activation by E. coli. J. Immunol. 133: 886-891.
63. Schoen, C. , J. Weber-Lehmann, J. Blom, B. Joseph, A. Goesmann, A. Strittmatter, and M. Frosch. 2011. Whole-genome sequence of the transformable Neisseria meningitidis serogroup A strain WUE2594. J. Bacteriol. 193: 2064-2065.
64. Frasch, C. E. , W. D. Zollinger, and J. T. Poolman. 1985. Serotype antigens of Neisseria meningitidis and a proposed scheme for designation of serotypes. Rev. Infect. Dis. 7: 504-510.
65. Vogel, U. , G. Morelli, K. Zurth, H. Claus, E. Kriener, M. Achtman, and M. Frosch. 1998. Necessity of molecular techniques to distinguish between Neisseria meningitidis strains isolated from patients with meningococcal disease and from their healthy contacts. J. Clin. Microbiol. 36: 2465-2470.
66. Claus, H. , R. Borrow, M. Achtman, G. Morelli, C. Kantelberg, E. Longworth, M. Frosch, and U. Vogel. 2004. Genetics of capsule Oacetylation in serogroup C, W-135 and Y meningococci. Mol. Microbiol. 51: 227-239.