Binding of complement factor H to loop 5 of porin protein 1A: A molecular mechanism of serum resistance of nonsialylated Neisseria gonorrhoeae

Journal of Experimental Medicine

Volumn 188, Issue 4, 1998, Pages 671-680

  Ram, Sanjay ^a   McQuillen, Daniel P ^a   Gulati, Sunita ^a   Elkins, Christopher ^b   Pangburn, Michael K ^c   Rice, Peter A ^a  

^a BOSTON MEDICAL CENTER   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c UNIVERSITY OF TEXAS HEALTH CENTER   (United States)

Author keywords

Factor H; Neisseria gonorrhoeae; Porin; Serum resistance

Indexed keywords

COMPLEMENT COMPONENT C3B; COMPLEMENT FACTOR H; DNA; OLIGOSACCHARIDE; PORIN;

ARTICLE; BINDING SITE; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; NEISSERIA GONORRHOEAE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; SIALYLATION;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; BLOOD BACTERICIDAL ACTIVITY; COMPLEMENT FACTOR H; HUMANS; MOLECULAR SEQUENCE DATA; NEISSERIA GONORRHOEAE; PORINS; RABBITS; SIALIC ACIDS;

EID: 0032541390     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.188.4.671     Document Type: Article

References (60)

1. Rice, P.A., W.M. McCormack, and D.L. Kasper. 1980. Natural serum bactericidal activity against Neisseria gonorrhoeae isolates from disseminated, locally invasive, and uncomplicated disease. J. Immunol. 124:2105-2109.
2. Rice, P.A., and D.L. Goldenberg. 1981. Clinical manifestations of disseminated infection caused by Neisseria gonorrhoeae are linked to differences in bactericidal reactivity of infecting strains. Ann. Intern. Med. 95:175-178.
3. O'Brien, J.P., D.L. Goldenberg, and P.A. Rice. 1983. Disseminated gonococcal infection: a prospective analysis of 49 patients and a review of pathophysiology and immune mechanisms. Medicine (Baltim.). 62:395-406.
4. Ward, M.E., P.J. Watt, and A.A. Glynn. 1970. Gonococci in urethral exudates possess a virulence factor lost on subculture. Nature. 227:382-384.
5. Nairn, C.A., J.A. Cole, P.V. Patel, N.J. Parsons, J.E. Fox, and H. Smith. 1988. Cytidine 5′-monophospho-N-acetylneuraminic acid or a related compound is the low Mr factor from human red blood cells which induces gonococcal resistance to killing by human serum. J. Gen. Microbiol. 134: 3295-3306.
6. Parsons, N.J., P.V. Patel, E.L. Tan, J.R. Andrade, C.A. Nairn, M. Goldner, J.A. Cole, and H. Smith. 1988. Cytidine 5′-monophospho-N-acetyl neuraminic acid and a low molecular weight factor from human blood cells induce lipopolysaccharide alteration in gonococci when conferring resistance to killing by human serum. Microb. Pathog. 5:303-309.
7. Ram, S., A.K. Sharma, S.D. Simpson, S. Gulati, D.P. McQuillen, M.K. Pangburn, and P.A. Rice. 1998. A novel sialic acid binding site on factor H mediates serum resistance of sialylated Neisseria gonorrhoeae. J. Exp. Med. 187:743-752.
8. Knapp, J.S., M.R. Tam, R.C Nowinski, K.K. Holmes, and E.G. Sandstrom. 1984. Serological classification of Neisseria gonorrhoeae with use of monoclonal antibodies to gonococcal outer membrane protein I. J. Infect. Dis. 150:44-48.
9. Blake, M.S., E.C. Gotschlich, and J. Swanson. 1981. Effects of proteolytic enzymes on the outer membrane proteins of Neisseria gonorrhoeae. Inject. Immun. 33:212-222.
10. Sandstrom, E.G., K.C. Chen, and T.M. Buchanan. 1982. Serology of Neisseria gonorrhoeae: coagglutination serogroups WI and WII/III correspond to different outer membrane protein I molecules. Infect. Immun. 38:462-470.
11. Danielsson, D., H. Faruki, D. Dyer, and P.F. Sparling. 1986. Recombination near the antibiotic resistance locus penB results in antigenic variation of gonococcal outer membrane protein I. Infect. Immun. 52:529-533.
12. Bygdeman, S.M., P.A. Mardh, and E.G. Sandstrom. 1984. Susceptibility of Neisseria gonorrhoeae to rifampicin and thiamphenicol: correlation with protein I antigenic determinants. Sex. Transm. Dis. 11:366-370.
13. Hildebrandt, J.F., L.W. Mayer, S.P. Wang, and T.M. Buchanan. 1978. Neisseria gonorrhoeae acquire a new principal outer-membrane protein when transformed to resistance to serum bactericidal activity. Infect. Immun. 20:267-273.
14. Buchanan, T.M., and J.F. Hildebrandt. 1981. Antigen-specific serotyping of Neisseria gonorrhoeae: characterization based upon principal outer membrane protein. Inject. Immun. 32:985-994.
15. 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.
16. Griffiss, J.M., J.P. O'Brien, R. Yamasaki, G.D. Williams, P.A. Rice, and H. Schneider. 1987. Physical heterogeneity of Neisserial lipooligosaccharides reflects oligosaccharides that differ in apparent molecular weight, chemical composition, and antigenic expression. Infect. Immun. 55:1792-1800.
17. Schneider, H., C.A. Hammack, M.A. Apicella, and J.M. Griffiss. 1988. Instability of expression of lipooligosaccharides and their epitopes in Neisseria gonorrhoeae. Infect. Immun. 56: 942-946.
18. Carbonetti, N.H., and P.F. Sparling. 1987. Molecular cloning and characterization of the structural gene for protein I, the major outer membrane protein of Neisseria gonorrhoeae. Proc. Natl. Acad. Sci. USA. 84:9084-9098.
19. Gotschlich, E.C., M.E. Seiff, M.S. Blake, and M. Koomey. 1987. Porin protein of Neisseria gonorrhoeae: cloning and gene structure. Proc. Natl. Acad. Sci. USA. 84:8135-8139.
20. Carbonetti, N.H., V.I. Simnad, H.S. Seifert, M. So, and P.F. Sparling. 1988. Genetics of protein I of Neisseria gonorrhoeae: construction of hybrid ponns [published erratum appears in Proc. Natl. Acad. Sci. USA. 1989 Feb;86(4):1317]. Proc. Natl. Acad. Sci. USA. 85:6841-6845.
21. Horstmann, R.D., H.J. Sievertsen, J. Knobloch, and V.A. Fischetti. 1988. Antiphagocytic activity of streptococcal M protein: selective binding of complement control protein factor H. Proc. Natl. Acad. Sci. USA. 85:1657-1661.
22. Fischetti, V.A., R.D. Horstmann, and V. Pancholi. 1995. Location of the complement factor H binding site on streptococcal M6 protein. Infect. Immun. 63:149-153.
23. China, B., M.P. Sory, B.T. N'Guyen, M. De Bruyere, and G.R. Cornelis. 1993. Role of the YadA protein in prevention of opsonization of Yersinia enterocolitica by C3b molecules. Infect. Immun. 61:3129-3136.
24. Sadlon, T.A., S.J. Parker, and D.L. Gordon. 1994. Regulation of C3 deposition on gp120 coated CD4 positive cells by decay accelerating factor and factor H. Immunol. Cell Biol. 72: 461-470.
25. Pinter, C., A.G. Siccardi, L. Lopalco, R. Longhi, and A. Clivio. 1995. HIV glycoprotein 41 and complement factor H interact with each other and share functional as well as antigenic homology. AIDS Res. Hum. Retroviruses. 11:971-980.
26. Pinter, C., A.G. Siccardi, R. Longhi, and A. Clivio. 1995. Direct interaction of complement factor H with the C1 domain of HIV type 1 glycoprotein 120. AIDS Res. Hum. Retroviruses. 11:577-588.
27. Carbonetti, N., V. Simnad, C. Elkins, and P.F. Sparling. 1990. Construction of isogenic gonococci with variable porin structure: effects on susceptibility to human serum and antibiotics. Mol. Microbiol. 4:1009-1018.
28. 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 lipopolysaccharide is not sialylated. Mol. Microbiol. 6: 2617-2628.
29. Mandrell, R., A. Apicella, J. Boslego, R. Chung, P. Rice, and J.M. Griffiss. 1988. Human immune response to monoclonal antibody-defined epitopes of Neisseria gonorrhoeae lipooligosaccharides. In Gonococci and Meningococci. J.T. Poolman, H. Zanen, T. Mayer, J. Heckels, P.H. Makela, H. Smith, and C. Beuvery, editors. Kluwer Academic Publishers, Dordrecht, Netherlands. 569-574.
30. Yamasaki, R., D.E. Kerwood, H. Schneider, K.P. Quinn, J.M. Griffiss, and R.E. Mandrell. 1994. The structure of lipooligosaccharide produced by Neisseria gonorrhoeae, strain 15253, isolated from a patient with disseminated infection: evidence for a new glycosylation pathway of gonococcal lipooligosaccharide. J. Biol. Chem. 269:30345-30351.
31. Densen, P., S. Gulati, and P.A. Rice. 1987. Specificity of antibodies against Neisseria gonorrhoeae that stimulate neutrophil chemotaxis. J. Clin. Invest. 80:78-87.
32. Rice, P.A., and D.L. Kasper. 1982. Characterization of serum resistance of Neisseria gonorrhoeae that disseminate: roles of blocking antibody and gonococcal outer membrane proteins. J. Clin. Invest. 70:157-167.
33. Maness, M.J., and P.F. Sparling. 1973. Multiple antibiotic resistance due to a single mutation in Neisseria gonorrhoeae. J. Infect. Dis. 128:321-330.
34. Meyer, T.F., N. Mlawer, and M. So. 1982. Pilus expression in Neisseria gonorrhoeae involves chromosomal rearrangement. Cell. 30:45-52.
35. Schneider, H., J.M. Griffiss, G.D. Williams, and G.B. Pier. 1982. Immunological basis of serum resistance of Neisseria gonorrhoeae. J. Gen. Microbiol. 128:13-22.
36. McQuillen, D.P., S. Gulati, and P.A. Rice. 1994. Complement-mediated bacterial killing assays. Methods Enzymol. 236: 137-147.
37. Pangburn, M.K., R.D. Schreiber, and H.J. Muller-Eberhard. 1977. Human complement C3b inactivator: isolation, characterization, and demonstration of an absolute requirement for the serum protein beta1H for cleavage of C3b and C4b in solution. J. Exp. Med. 146:257-270.
38. Iida, K., K. Mitomo, T. Fujita, and N. Tamura. 1987. Characterization of three monoclonal antibodies against C3 with selective specificities. Immunology. 62:413-117.
39. Kolb, W.P., P.R. Morrow, and J.D. Tamerius. 1989. Ba and Bb fragments of factor B activation: fragment production, biological activities, neoepitope expression and quantitation in clinical samples. Complement Inflamm. 6:175-204.
40. Apicella, M.A., R.E. Mandrell, M. Shero, M.E. Wilson, J.M. Griffiss, G.F. Brooks, C. Lammel, J.F. Breen, and P.A. Rice. 1990. Modification by sialic acid of Neisseria gonorrhoeae lipooligosaccharide epitope expression in human urethral exudates: an immunoelectron microscopic analysis. J. Infect. Dis. 162:506-512.
41. Cannon, J.G., W.J. Black, I. Nachamkin, and P.W. Stewart. 1984. Monoclonal antibody that recognizes an outer membrane antigen common to the pathogenic Neisseria species but not to most nonpathogenic Neisseria species. Infect. Immun. 43:994-999.
42. Sambrook, J., E.F. Fritsch, and T. Maniatis. 1989. Molecular Cloning: A Laboratory Manual. 2nd edition. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
43. 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. 60:3620-3629.
44. Qi, H.L., J.Y. Tai, and M.S. Blake. 1994. Expression of large amounts of Neisserial porin proteins in Escherichia coli and refolding of the proteins into native tnmers. Infect. Immun. 62: 2432-2439.
45. Zar, J.H. 1984. Biostatistical Analysis. 2nd edition. Prentice-Hall, Inc., Englewood Cliffs, NJ. 718 pp.
46. Pangburn, M.K., R.D. Schreiber, and H.J. Muller-Eberhard. 1983. C3b deposition during activation of the alternative complement pathway and the effect of deposition on the activating surface. J. Immunol. 131:1930-1935.
47. Elkins, C., K.B. Barkley, N.H. Carbonetti, A.J. Coimbre, and P.F. Sparling. 1994. Immunobiology of purified recombinant outer membrane ponn protein I of Neisseria gonorrhoeae. Mol. Micobiol. 14:1059-1075.
48. Parker, C.J., R.N. Frame, and M.R. Elstad. 1988. Vitronectin (S protein) augments the functional activity of monocyte receptors for IgG and complement C3b. Blood. 71:86-93.
49. Sim, E., A.B. Wood, L.M. Hsiung, and R.B. Sim. 1981. Pattern of degradation of human complement fragment, C3b. FEBS Lett. 132:55-60.
50. Whaley, K., and S. Ruddy. 1976. Modulation of the alternative complement pathways by beta 1 H globulin. J. Exp. Med. 144:1147-1163.
51. McGregor, J.A., J.I. French, W. Jones, K. Milligan, P.J. McKinney, E. Patterson, and R. Parker. 1994. Bacterial vaginosis is associated with prematurity and vaginal fluid mucinase and sialidase: results of a controlled trial of topical clindamycin cream. Am J. Obstet. Gynecol. 170:1048-1060.
52. Briseiden, A.M., B.J. Moncla, C.E. Stevens, and S.L. Hillier. 1992. Sialidases (neuraminidases) in bacterial vaginosis and bacterial vaginosis-associated microflora. J. Clin. Microbiol. 30: 663-666.
53. Paulesu, L., and G.P. Pessina. 1982. Cyclic changes of sialidase in human cervical mucus. Int. J. Biochem. 14:561-563.
54. Cooke, S.J., K. Jolley, C.A. Ison, H. Young, and J.E. Heckels. 1998. Naturally occurring isolates of Neisseria gonorrhoeae, which display anomalous serovar properties, express PIA/PIB hybrid porins, deletions in PIB or PIA molecules. FEMS Microbiol. Lett. 162:75-82.
55. Danielsson, D., H. Faruki, D. Dyer, and P.F. Sparling. 1983. Recombination near the antibiotic resistance locus penB results in antigenic variation of gonococcal outer membrane-protein I. Infect. Immun. 52:529-533.
56. Gigli, I., T. Fujita, and V. Nussenzweig. 1979. Modulation of the classical pathway C3 convertase by plasma proteins C4 binding protein and C3b inactivator. Proc. Natl. Acad. Sci. USA. 76:6596-6600.
57. Wetzler, L.M., M.S. Blake, K. Barry, and E.G. Gotschlich. 1992. Gonococcal porin vaccine evaluation: comparison of Por proteosomes, liposomes, and blebs isolated from rmp deletion mutants. J. Infect. Dis. 166:551-555.
58. Gulati, S., P.A. Rice, M. Blake, S.K. Sarafian, S.A. Morse, M.J. Quentin-Millet, and F. Arminjon. 1991. Antibody responses in six volunteers immunized with a gonococcal protein I vaccine. In Neisseriae 1990. M. Achtmann, P. Kohl, C. Marchai, G. Morelli, A. Seiler and B. Thiesen, editors. Walter de Gruyter & Co., Berlin, Germany. 229-234.
59. Joiner, K.A., R. Scales, K.A. Warren, M.M. Frank, and P.A. Rice. 1985. Mechanism of action of blocking immunoglobulin G for Neisseria gonorrhoeae. J. Clin. Invest. 76:1765-1772.
60. Virji, M., and J.E. Heckels. 1988. Nonbactericidal antibodies against Neisseria gonorrhoeae: evaluation of their blocking effect on bactericidal antibodies directed against outer membrane antigens. J. Gen. Microbiol. 134:2703-2711.