Mannose-Binding Lectin Binds to Two Major Outer Membrane Proteins, Opacity Protein and Porin, of Neisseria meningitidis

Journal of Immunology

Volumn 172, Issue 6, 2004, Pages 3784-3792

  Estabrook, Michele M ^a,b   Jack, Dominic L ^c   Klein, Nigel J ^d   Jarvis, Gary A ^a,b  

^a SAN FRANCISCO VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF SHEFFIELD   (United Kingdom)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; COMPLEMENT; LIPOOLIGOSACCHARIDE; MANNOSE; MANNOSE BINDING LECTIN; MONOCLONAL ANTIBODY; N ACETYLGLUCOSAMINE; OPACITY PROTEIN; OUTER MEMBRANE PROTEIN; PORIN; PORIN B; SUGAR; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL CELL; BACTERICIDAL ACTIVITY; COMPLEMENT ACTIVATION; DOT HYBRIDIZATION; ENZYME LINKED IMMUNOSORBENT ASSAY; ESCHERICHIA COLI; IMMUNOBLOTTING; NEISSERIA MENINGITIDIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OPSONIZATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PURIFICATION;

EID: 1542724425     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.172.6.3784     Document Type: Article

References (78)

1. Estabrook, M. M., N. C. Christopher, J. M. Griffiss, C. J. Baker, and R. E. Mandrell. 1992. Sialylation and human neutrophil killing of group C Neisseria meningitidis. J. Infect. Dis. 166:1079.
2. Estabrook, M. M., J. M. Griffiss, and G. A. Jarvis. 1997. Sialylation of Neisseria meningitidis lipooligosaccharide inhibits serum bactericidal activity by masking lacto-N-neotetraose. Infect. Immun. 65:4436.
3. Estabrook, M. M., D. Zhou, and M. A. Apicella. 1998. Nonopsonic phagocytosis of group C Neisseria meningitidis by human neutrophils. Infect. Immun. 66:1028.
4. Holmskov, U. L. 2000. Collectins and collectin receptors in innate immunity. APMIS 108:7.
5. Tabona, P., A. Mellor, and J. A. Summerfield. 1995. Mannose binding protein is involved in first-line host defence: evidence from transgenic mice. Immunology 85:153.
6. Densen, P., J. M. Weiler, J. M. Griffiss, and L. G. Hoffmann. 1987. Familial properdin deficiency and fatal meningococcemia: correction of the bactericidal defect by vaccination. N. Engl. J. Med. 316:922.
7. Jarvis, G. A., and N. A. Vedros. 1987. Sialic acid of group B Neisseria meningitidis regulates alternative complement pathway activation. Infect. Immun. 55:174.
8. Jack, D. L., N. J. Klein, and M. W. Turner. 2001. Mannose-binding lectin: targeting the microbial world for complement attack and opsonophagocytosis. Immunol. Rev. 180:86.
9. Sastry, K., G. A. Herman, L. Day, E. Deignan, G. Bruns, C. C. Morton, and R. A. Ezekowitz. 1989. The human mannose-binding protein gene: exon structure reveals its evolutionary relationship to a human pulmonary surfactant gene and localization to chromosome 10. J. Exp. Med. 170:1175.
10. Taylor, M. E., P. M. Brickell, R. K. Craig, and J. A. Summerfield. 1989. Structure and evolutionary origin of the gene encoding a human serum mannose-binding protein. Biochem. J. 262:763.
11. Weis, W. I., K. Drickamer, and W. A. Hendrickson. 1992. Structure of a C-type mannose-binding protein complexed with an oligosaccharide. Nature 360:127.
12. Weis, W. I., and K. Drickamer. 1994. Trimeric structure of a C-type mannose-binding protein. Structure 2:1227.
13. Matsushita, M., and T. Fujita. 1992. Activation of the classical complement pathway by mannose-binding protein in association with a novel C1s-like serine protease. J. Exp. Med. 176:1497.
14. Thiel, S., T. Vorup-Jensen, C. M. Stover, W. Schwaeble, S. B. Laursen, K. Foulsen, A. C. Willis, P. Eggleton, S. Hansen, U. Holmskov, K. B. Reid, and J. C. Jensenius. 1997. A second serine protease associated with mannan-binding lectin that activates complement. Nature 386:506.
15. Dahl, M. R., S. Thiel, M. Matsushita, G. Fugita, A. C. Willis, T. Christensen, T. Vorup-Jensen, and J. C. Jensenius. 2001. MASP-3 and its association with direct complexes of the mannan-binding lectin complement activation pathway. Immunity 15:127.
16. Stover, C. M., S. Thiel, M. Thelen, N. J. Lynch, T. Vorup-Jensen, J. C. Jensenius, and W. J. Schwaeble. 1999. Two constituents of the initiation complex of the mannan-binding lectin activation pathway of complement are encoded by a single structural gene. J. Immunol. 162:3481.
17. Malhotra, R., S. Thiel, K. B. Reid, and R. B. Sim. 1990. Human leukocyte C1q receptor binds other soluble proteins with collagen domains. J. Exp. Med. 172:955.
18. Ghiran, I., S. F. Barbashov, L. B. Klickstein, S. W. Tas, J. C. Jensenius, and A. Nicholson-Weller. 2000. Complement receptor 1/CD35 is a receptor for mannan-binding lectin. J. Exp. Med. 192:1797.
19. Nepomuceno, R. R., and A. J. Tenner. 1998. C1qRp, the C1q receptor that enhances phagocytosis is detected specifically in human cells of myeloid lineage, endothelial cells, and platelets. J. Immunol. 160:1929.
20. Jack, D. L., R. C. Read, A. J. Tenner, and N. J. Klein. 2001. Mannose-binding lectin regulates the inflammatory response of human professional phagocytes to Neisseria meningitidis serogroup B. J. Infect. Dis. 184:1152.
21. Garred, P., H. O. Madsen, A. Svejgaard, and T. E. Michaelsen. 1999. Mannose-binding lectin and meningococcal disease. Lancet 354:336.
22. Hibberd, M. L., M. Sumiya, J. A. Summerfield, R. Booy, and M. Levin. 1999. Association of variants of the gene for mannose-binding lectin with susceptibility to meningococcal disease. Meningococcal Research Group. Lancet 353:1049.
23. Jack, D. L., A. W. Dodds, N. Anwar, C. A. Ison, A. Law, M. Frosch, M. W. Turner, and N. J. Klein. 1998. Activation of complement by mannose-binding lectin on isogenic mutants of Neisseria meningitidis serogroup B. J. Immunol. 160:1346.
24. Jack, D. L., G. A. Jarvis, C. L. Booth, M. W. Turner, and N. J. Klein. 2001. Mannose-binding lectin accelerates complement activation and serum killing of Neisseria meningitidis serogroup C. J. Infect. Dis. 184:836.
25. van Emmerik, L. C., E. J. Kuijper, C. A. Fijen, J. Dankert, and S. Thiel. 1994. Binding of mannan-binding protein to various bacterial pathogens of meningitis. Clin. Exp. Immunol. 97:411.
26. Griffiss, J. 1995. The role of bacterial lipooligosaccharides in the pathogenesis of human disease. Trends Glycosci. Glycotechnol. 7:461.
27. Griffiss, J., B. L. Brandt, N. B. Saunders, and W. Zollinger. 2000. Structural relationships and sialylation among meningococcal L1, L8, and L3,7 lipooligosaccharide serotypes. J. Biol. Chem. 275:9716.
28. Mandrell, R., and M. Apicella. 1993. Lipooligosaccharides (LOS) of mucosal pathogens: molecular mimicry and host-modification of LOS. Immunobiology 187:382.
29. Elkins, C., N. H. Carbonetti, V. A. Varela, D. Stirewalt, D. G. Klapper, and P. F. Sparling. 1992. Antibodies to N-terminal peptides of gonococcal porin are bactericidal when gonococcal lipoopolysaccharide is not sialylated. Mol. Microbiol. 6:2517.
30. de Vries, F. P., R. Cole, J. Dankert, M. Frosch, and J. P. van Putten. 1998. Neisseric meningitidis producing the Opc adhesin binds epithelial cell proteoglycan receptors. Mol. Microbiol. 27:1203.
31. Virji, M., K. Makepeace, D. J. Ferguson, M. Achtman, J. Sarkari, and E. R. Moxon. 1992. Expression of the Opc protein correlates with invasion of epithelial and endothelial cells by Neisseria meningitidis. Mol. Microbiol. 6:2785.
32. Virji, M., K. Makepeace, D. J. Ferguson, M. Achtman, and E. R. Moxon. 1993. Meningococcal Opa and Opc proteins: their role in colonization and invasion of human epithelial and endothelial cells. Mol. Microbiol. 10:499.
33. Neth, O., D. L. Jack, A. W. Dodds, H. Holzel, N. J. Klein, and M. W. Turner. 2000. Mannose-binding lectin binds to a range of clinically relevant microorganisms and promotes complement deposition. Infect. Immun. 68:688.
34. Patrick, C. C., G. T. Furuta, M. M. Estabrook, M. S. Blake, and C. J. Baker. 1993. Variation in phenotypic expression of the Opa outer membrane protein and lipooligosaccharide of Neisseria meningitidis serogroup C causing periorbital cellulitis and bacteremia. Clin. Infect. Dis. 16:523.
35. Griffiss, J. M., and D. K. Goroff. 1981. Immunological cross-reaction between a naturally occurring galactan, agarose, and an LPS locus for immune lysis of Neisseria meningitidis by human sera. Clin. Exp. Immunol. 43:20.
36. Kilpatrick, D. C. 1997. Isolation of human mannan binding lectin, serum amyloid P component and related factors from Cohn fraction III. Transfus. Med. 7:289.
37. Neth, O., D. L. Jack, M. Johnson, N. J. Klein, and M. W. Turner. 2002. Enhancement of complement activation and opsonophagocytosis by complexes of mannose-binding lectin with mannose-binding lectin-associated serine protease after binding to Staphylococcus aureus. J. Immunol. 169:4430.
38. Schneider, H., J. M. Griffiss, G. D. Williams, and G. B. Pier. 1982. Immunological basis of serum resistance of Neisseria gonorrhoeae. J. Gen. Microbiol. 128:13.
39. Westphal, O., and K. Jann. 1965. Bacterial lipopolysaccharides, extraction with phenol-water and further applications of the procedure. In Methods in Carbohydrate Chemistry, Vol. 5. R. L. Whistler, ed. Academic Press, New York, p. 83.
40. Zollinger, W. D., R. E. Mandrell, J. M. Griffiss, P. Altieri, and S. Berman. 1979. Complex of meningococcal group B polysaccharide and type 2 outer membrane protein immunogenic in man. J. Clin. Invest. 63:836.
41. Estabrook, M. M., R. E. Mandrell, M. A. Apicella, and J. M. Griffiss. 1990. Measurement of the human immune response to meningococcal lipooligosaccharide antigens by using serum to inhibit monoclonal antibody binding to purified lipooligosaccharide. Infect. Immun. 58:2204.
42. Estabrook, M. M., C. J. Baker, and J. M. Griffiss. 1993. The immune response of children to meningococcal lipooligosaccharides during disseminated disease is directed primarily against two monoclonal antibody-defined epitopes. J. Infect. Dis. 167:966.
43. Collard, C. D., A. Väkevä, M. A. Morrissey, A. Agah, S. A. Rollins, W. R. Reenstra, J. A. Buras, S. Meri, and G. L. Stahl. 2000. Complement activation after oxidative stress: role of the lectin complement pathway. Am. J. Pathol. 156:1549.
44. Schneider, H., T. L. Hale, W. D. Zollinger, R. Seid, Jr., C. A. Hammack, and J. M. Griffiss. 1984. Heterogeneity of molecular size and antigenic expression within lipooligosaccharides of individual strains of Neisseria gonorrhoeae and Neisseria meningitidis. Infect. Immun. 45:544.
45. Mandrell, R., J. Griffiss, and B. Macher. 1988. Lipooligosaccharides (LOS) of Neisseria gonorrhoeae and Neisseria meningitidis have components that are immunochemically similar to precursors of human blood group antigens: carbohydrate specificity of the mouse monoclonal antibodies that recognize cross-reacting antigens on LOS and human erythrocytes. J. Exp. Med. 168:107.
46. Achtman, M., M. Neibert, B. Crowe, W. Strittmatter, B. Kusecek, E. Weyse, M. Walsh, B. Slawig, G. Morelli, A. Moll, and M. Blake. 1988. Purification and characterization of eight class 5 outer membrane protein variants from a clone of Neisseria meningitidis serogroup A. J. Exp. Med. 168:507.
47. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389.
48. Gorby, G. L., A. F. Ehrhardt, M. A. Apicella, and C. Elkins. 2001. Invasion of human fallopian tube epithelium by Escherichia coli expressing combinations of a gonococcal porin, opacity-associated protein, and chimeric lipo-oligosaccharide. J. Infect. Dis. 184:460.
49. Lammel, C. J., A. E. Karu, and G. F. Brooks. 1988. Antigenic specificity and biological activity of a monoclonal antibody that is broadly cross reactive with gonococcal protein IIs. In Gonococci and Meningococci. J. T. Poolman, H. C. Zanen, T. F. Mayer, J. E. Heckels, P. R. H. Makela, H. Smith, and E. C. Beuvery, eds. Kluwer Academic Publishers, Dordrecht, The Netherlands, p. 737.
50. Ram, S., F. G. Mackinnon, S. Gulati, D. P. McQuillen, U. Vogel, M. Frosch, C. Elkins, H. K. Guttormsen, L. M. Wetzler, M. Oppermann, M. K. Pangburn, and P. A. Rice. 1999. The contrasting mechanisms of serum resistance of Neisseria gonorrhoeae and group B Neisseria meningitidis. Mol. Immunol. 36:915.
51. 2-macroglobulin. J. Immunol. 168:4178.
52. Jarvis, G. A., and J. M. Griffiss. 1989. Human IgA1 initiates complement-mediated killing of Neisseria meningitidis. J. Immunol. 143:1703.
53. Feavers, I. M., J. Suker, A. J. McKenna, A. B. Heath, and M. C. J. Maiden. 1992. Molecular analysis of the serotyping antigens of Neisseria meningitidis. Infect. Immun. 60:3620.
54. Murakami, K., E. C. Gotschlich, and M. E. Seiff. 1989. Cloning and characterization of the structural gene for the class 2 protein of Neisseria meningitidis. Infect. Immun. 57:2318.
55. Blake, M. S., C. M. Blake, M. A. Apicella, and R. E. Mandrell. 1995. Gonococcal opacity: lectin-like interactions between Opa proteins and lipooligosaccharide. Infect. Immun. 63:1434.
56. Hamadeh, R. M., M. M. Estabrook, P. Zhou, G. A. Jarvis, and J. M. Griffiss. 1995. Anti-Gal binds to pili of Neisseria meningitidis: the immunoglobulin A isotype blocks complement-mediated killing. Infect. Immun. 63:4900.
57. Blake, M. S., and E. C. Gotschlich. 1982. Purification and partial characterization of the major outer membrane protein of Neisseria gonorrhoeae. Infect. Immun. 36:277.
58. Blake, M. S., and E. C. Gotschlich. 1984. Purification and partial characterization of the opacity-associated proteins of Neisseria gonorrhoeae. J. Exp. Med. 159:452.
59. 2+-independent association with a C1s-like serine protease. Biochem. J. 319:329.
60. Wallis, R., and J. Y. Cheng. 1999. Molecular defects in variant forms of mannose-binding protein associated with immunodeficiency. J. Immunol. 163:4953.
61. McNeely, T. B., and J. D. Coonrod. 1994. Aggregation and opsonization of Type A but not Type B Hemophilus inluenzae by surfactant protein A. Am. J. Respir. Cell Mol. Biol. 11:114.
62. Dehio, C., S. D. Gray-Owen, and T. F. Meyer. 1998. The role of neisserial Opa proteins in interactions with host cells. Trends Microbiol. 6:489.
63. Aho, E. L., J. A. Dempsey, M. M. Hobbs, D. G. Klapper, and J. G. Cannon. 1991. Characterization of the opa (class 5) gene family of Neisseria meningitidis. Mol. Microbiol. 5:1429.
64. Malomy, B., G. Morelli, B. Kusecek, J. Kolberg, and M. Achtman. 1998. Sequence diversity, predicted two-dimensional protein structure, and epitope mapping of neisserial Opa proteins. J. Bacteriol. 180:1323.
65. Nassif, X., C. Pujol, P. Morand, and E. Eugene. 1999. Interactions of pathogenic neisseria with host cells: is it possible to assemble the puzzle? Mol. Microbiol. 32:1124.
66. Muenzner, P., C. Dehio, T. Fujiwara, M. Achtman, T. F. Meyer, and S. D. Gray-Owen. 2000. Carcinoembryonic antigen family receptor specificity of Neisseria meningitidis Opa variants influences adherence to and invasion of proinflammatory cytokine-activated endothelial cells. Infect. Immun. 68:3601.
67. McNeil, G., and M. Virji. 1997. Phenotypic variants of meningococci and their potential in phagocytic interactions: the influence of opacity proteins, pili, PilC and surface sialic acids. Microb. Pathog. 22:295.
68. Bjerknes, R., H. K. Guttormsen, C. O. Solberg, and L. M. Wetzler. 1995. Neisserial porins inhibit human neutrophil actin polymerization, degranulation, opsonin receptor expression, and phagocytosis but prime the neutrophils to increase their oxidative burst. Infect. Immun. 63:160.
69. Massari, P., P. Heneke, Y. Ho, E. Latz, D. T. Golenbock, and L. M. Wetzler. 2002. Cutting edge: Immune stimulation by neisserial porins is Toll-like receptor 2 and MyD88 dependent. J. Immunol. 168:1533.
70. Massari, P., Y. Ho, and J. M. Wetzler. 2000. Neisseria meningitidis porin PorB interacts with mitochondria and protects cells from apoptosis. Proc. Natl. Acad. Sci. USA 97:9070.
71. Muller, A., D. Gunther, F. Dux, M. Naumann, T. F. Meyer, and T. Rudel. 1999. Neisserial porin (PorB) causes rapid calcium influx in target cells and induces apoptosis by the activation of cystein proteases. EMBO J. 18:339.
72. Kristensen, T., R. A. Wetsel, and B. F. Tack. 1986. Structural analysis of human complement protein H: homology with C4b binding protein, β2-glycoprotein 1, and the Ba fragment of B2. J. Immunol. 136:3407.
73. Reid, K. B., and A. J. Day. 1989. Structure-function relationships of the complement components. Immunol. Today 10:177.
74. Kahler, C. M., and D. S. Stephens. 1998. Genetic basis for biosynthesis, structure, and function of meningococcal lipooligosaccharide (endotoxin). Crit. Rev. Microbiol. 24:281.
75. Griffiss, J. M., and H. Schneider. 1999. The chemistry and biology of lipooligosaccharides: the endotoxins of bacteria of the respiratory and genital mucosae. In Endotoxin in Health and Disease. H. Brade, S. M. Opal, S. N. Vogel, and D. C. Morrison, eds. Marcel Dekker, New York, p. 179.
76. Di Fabio, J., F. Michon, J. R. Brisson, and H. Jennings. 1990. Structure of the L1 and L6 core oligosaccharide epitopes of Neisseria meningitidis. Can. J. Chem. 68:1029.
77. Poolman, J., C. Hopman, and H. Zanen. 1982. Problems in the definition of meningococcal serotypes. FEMS Microbiol. Lett. 13:339.
78. Zollinger, W. D., and R. E. Mandrell. 1977. Outer-membrane protein and lipopolysaccharide serotyping of Neisseria meningitidis by inhibition of a solid-phase radioimmunoassay. Infect. Immun. 18:424.