Properdin is critical for antibody-dependent bactericidal activity against Neisseria gonorrhoeae that recruit C4b-binding protein

Journal of Immunology

Volumn 188, Issue 7, 2012, Pages 3416-3425

  Gulati, Sunita ^a   Agarwal, Sarika ^a   Vasudhev, Shreekant ^a   Rice, Peter A ^a   Ram, Sanjay ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT COMPONENT C3; COMPLEMENT COMPONENT C4B BINDING PROTEIN; EPITOPE; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 2C7; PROPERDIN; UNCLASSIFIED DRUG;

ADULT; ARTICLE; BACTERIAL STRAIN; BACTERIUM MUTANT; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMAN; MALE; NEISSERIA GONORRHOEAE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; SERUM; VOLUNTEER; WESTERN BLOTTING;

ADULT; ANIMALS; ANTIBODIES, BACTERIAL; ANTIBODY SPECIFICITY; ANTIGENS, BACTERIAL; BACTERIAL VACCINES; COMPLEMENT PATHWAY, ALTERNATIVE; COMPLEMENT PATHWAY, CLASSICAL; EPITOPES; HISTOCOMPATIBILITY ANTIGENS; HUMANS; LIPOPOLYSACCHARIDES; MALE; MICE; NEISSERIA GONORRHOEAE; PORINS; PROPERDIN; VIRULENCE;

EID: 84859417279     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1102746     Document Type: Article

References (70)

1. Centers for Disease Control and Prevention. 2011. Gonorrhea-CDC Fact Sheet. Centers for Disease Control and Prevention, Atlanta, GA.
2. Holmes, K. K., G. W. Counts, and H. N. Beaty. 1971. Disseminated gonococcal infection. Ann. Intern. Med. 74: 979-993.
3. Knapp, J. S., and K. K. Holmes. 1975. Disseminated gonococcal infections caused by Neisseria gonorrhoeae with unique nutritional requirements. J. Infect. Dis. 132: 204-208.
4. 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 (Baltimore) 62: 395-406. (Pubitemid 14201911)
5. 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. (Pubitemid 11039821)
6. Tapsall, J. W., F. Ndowa, D. A. Lewis, and M. Unemo. 2009. Meeting the public health challenge of multidrug- and extensively drug-resistant Neisseria gonorrhoeae. Expert Rev. Anti Infect. Ther. 7: 821-834.
7. Blake, M. S., and L. M. Wetzler. 1995. Vaccines for gonorrhea: where are we on the curve? Trends Microbiol. 3: 469-474.
8. Johnson, S. C., R. C. Chung, C. D. Deal, J. W. Boslego, J. C. Sadoff, S. W. Wood, C. C. Brinton, Jr., and E. C. Tramont. 1991. Human immunization with Pgh 3-2 gonococcal pilus results in cross-reactive antibody to the cyanogen bromide fragment-2 of pilin. J. Infect. Dis. 163: 128-134.
9. Buchanan, T. M., D. A. Eschenbach, J. S. Knapp, and K. K. Holmes. 1980. Gonococcal salpingitis is less likely to recur with Neisseria gonorrhoeae of the same principal outer membrane protein antigenic type. Am. J. Obstet. Gynecol. 138: 978-980. (Pubitemid 11198975)
10. Plummer, F. A., J. N. Simonsen, H. Chubb, L. Slaney, J. Kimata, M. Bosire, J. O. Ndinya-Achola, and E. N. Ngugi. 1989. Epidemiologic evidence for the development of serovar-specific immunity after gonococcal infection. J. Clin. Invest. 83: 1472-1476. (Pubitemid 19124099)
11. Plummer, F. A., H. Chubb, J. N. Simonsen, M. Bosire, L. Slaney, N. J. Nagelkerke, I. Maclean, J. O. Ndinya-Achola, P. Waiyaki, and R. C. Brunham. 1994. Antibodies to opacity proteins (Opa) correlate with a reduced risk of gonococcal salpingitis. J. Clin. Invest. 93: 1748-1755. (Pubitemid 24116417)
12. 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. (Pubitemid 16196043)
13. Rice, P. A., H. E. Vayo, M. R. Tam, and M. S. Blake. 1986. Immunoglobulin G antibodies directed against protein III block killing of serum-resistant Neisseria gonorrhoeae by immune serum. J. Exp. Med. 164: 1735-1748. (Pubitemid 17184201)
14. 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.
15. Virji, M., and J. E. Heckels. 1989. Location of a blocking epitope on outermembrane protein III of Neisseria gonorrhoeae by synthetic peptide analysis. J. Gen. Microbiol. 135: 1895-1899. (Pubitemid 19197056)
16. Plummer, F. A., H. Chubb, J. N. Simonsen, M. Bosire, L. Slaney, I. Maclean, J. O. Ndinya-Achola, P. Waiyaki, and R. C. Brunham. 1993. Antibody to Rmp (outer membrane protein 3) increases susceptibility to gonococcal infection. J. Clin. Invest. 91: 339-343. (Pubitemid 23037289)
17. Edwards, J. L., and M. A. Apicella. 2002. The role of lipooligosaccharide in Neisseria gonorrhoeae pathogenesis of cervical epithelia: lipid A serves as a C3 acceptor molecule. Cell. Microbiol. 4: 585-598.
18. 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: 460-472. (Pubitemid 32718510)
19. Harvey, H. A., N. Porat, C. A. Campbell, M. Jennings, B. W. Gibson, N. J. Phillips, M. A. Apicella, and M. S. Blake. 2000. Gonococcal lipooligosaccharide is a ligand for the asialoglycoprotein receptor on human sperm. Mol. Microbiol. 36: 1059-1070. (Pubitemid 30330678)
20. Lucas, C. E., K. E. Hagman, J. C. Levin, D. C. Stein, and W. M. Shafer. 1995. Importance of lipooligosaccharide structure in determining gonococcal resistance to hydrophobic antimicrobial agents resulting from the mtr efflux system. Mol. Microbiol. 16: 1001-1009.
21. Quan, D. N., M. D. Cooper, J. L. Potter, M. H. Roberts, H. Cheng, and G. A. Jarvis. 2008. TREM-2 binds to lipooligosaccharides of Neisseria gonorrhoeae and is expressed on reproductive tract epithelial cells. Mucosal Immunol. 1: 229-238. (Pubitemid 351541308)
22. Shafer,W. M., A. Datta, V. S. Kolli, M. M. Rahman, J. T. Balthazar, L. E. Martin, W. L. Veal, D. S. Stephens, and R. Carlson. 2002. Phase variable changes in genes lgtA and lgtC within the lgtABCDE operon of Neisseria gonorrhoeae can modulate gonococcal susceptibility to normal human serum. J. Endotoxin Res. 8: 47-58. (Pubitemid 34234780)
23. Shafer, W. M., K. Joiner, L. F. Guymon, M. S. Cohen, and P. F. Sparling. 1984. Serum sensitivity of Neisseria gonorrhoeae: the role of lipopolysaccharide. J. Infect. Dis. 149: 175-183. (Pubitemid 14198918)
24. Song, W., L. Ma, R. Chen, and D. C. Stein. 2000. Role of lipooligosaccharide in Opa-independent invasion of Neisseria gonorrhoeae into human epithelial cells. J. Exp. Med. 191: 949-960.
25. Zhang, P., O. Schwartz, M. Pantelic, G. Li, Q. Knazze, C. Nobile, M. Radovich, J. He, S. C. Hong, J. Klena, and T. Chen. 2006. DC-SIGN (CD209) recognition of Neisseria gonorrhoeae is circumvented by lipooligosaccharide variation. J. Leukoc. Biol. 79: 731-738. (Pubitemid 44835605)
26. Gregg, C. R., A. P. Johnson, D. Taylor-Robinson, M. A. Melly, and Z. A. McGee. 1981. Host species-specific damage to oviduct mucosa by Neisseria gonorrhoeae lipopolysaccharide. Infect. Immun. 34: 1056-1058. (Pubitemid 12247210)
27. Densen, P., W. D. Zollinger, S. Gulati, and P. A. Rice. 1988. Antibodies against Neisseria gonorrhoeae lipooligosaccharide antigens stimulate neutrophil chemotaxis. 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. 511-518.
28. Schmidt, K. A., H. Schneider, J. A. Lindstrom, J. W. Boslego, R. A. Warren, L. Van de Verg, C. D. Deal, J. B. McClain, and J. M. Griffiss. 2001. Experimental gonococcal urethritis and reinfection with homologous gonococci in male volunteers. Sex. Transm. Dis. 28: 555-564. (Pubitemid 32937563)
29. Yamasaki, R., H. Koshino, S. Kurono, Y. Nishinaka, D. P. McQuillen, A. Kume, S. Gulati, and P. A. Rice. 1999. Structural and immunochemical characterization of a Neisseria gonorrhoeae epitope defined by a monoclonal antibody 2C7; the antibody recognizes a conserved epitope on specific lipo-oligosaccharides in spite of the presence of human carbohydrate epitopes. J. Biol. Chem. 274: 36550-36558.
30. Gulati, S., J. Ngampasutadol, R. Yamasaki, D. P. McQuillen, and P. A. Rice. 2001. Strategies for mimicking Neisserial saccharide epitopes as vaccines. Int. Rev. Immunol. 20: 229-250. (Pubitemid 33119078)
31. Ngampasutadol, J., P. A. Rice, M. T. Walsh, and S. Gulati. 2006. Characterization of a peptide vaccine candidate mimicking an oligosaccharide epitope of Neisseria gonorrhoeae and resultant immune responses and function. Vaccine 24: 157-170. (Pubitemid 41753003)
32. Ricklin, D., G. Hajishengallis, K. Yang, and J. D. Lambris. 2010. Complement: a key system for immune surveillance and homeostasis. Nat. Immunol. 11: 785-797.
33. Walport, M. J. 2001. Complement. First of two parts. N. Engl. J. Med. 344: 1058-1066.
34. Ingwer, I., B. H. Petersen, and G. Brooks. 1978. Serum bactericidal action and activation of the classic and alternate complement pathways by Neisseria gonorrhoeae. J. Lab. Clin. Med. 92: 211-220. (Pubitemid 8400107)
35. Lewis, L. A., B. Choudhury, J. T. Balthazar, L. E. Martin, S. Ram, P. A. Rice, D. S. Stephens, R. Carlson, and W. M. Shafer. 2009. Phosphoethanolamine substitution of lipid A and resistance of Neisseria gonorrhoeae to cationic antimicrobial peptides and complement-mediated killing by normal human serum. Infect. Immun. 77: 1112-1120.
36. Fearon, D. T., and K. F. Austen. 1975. Properdin: binding to C3b and stabilization of the C3b-dependent C3 convertase. J. Exp. Med. 142: 856-863.
37. Wirthmueller, U., B. Dewald, M. Thelen, M. K. Schäfer, C. Stover, K. Whaley, J. North, P. Eggleton, K. B. Reid, and W. J. Schwaeble. 1997. Properdin, a positive regulator of complement activation, is released from secondary granules of stimulated peripheral blood neutrophils. J. Immunol. 158: 4444-4451. (Pubitemid 127483949)
38. Price, R. J., and B. Boettcher. 1979. The presence of complement in human cervical mucus and its possible relevance to infertility in women with complement-dependent sperm-immobilizing antibodies. Fertil. Steril. 32: 61-66. (Pubitemid 9187969)
39. Edwards, J. L., E. J. Brown, S. Uk-Nham, J. G. Cannon, M. S. Blake, and M. A. Apicella. 2002. A co-operative interaction between Neisseria gonorrhoeae and complement receptor 3 mediates infection of primary cervical epithelial cells. Cell. Microbiol. 4: 571-584.
40. McQuillen, D. P., S. Gulati, S. Ram, A. K. Turner, D. B. Jani, T. C. Heeren, and P. A. Rice. 1999. Complement processing and immunoglobulin binding to Neisseria gonorrhoeae determined in vitro simulates in vivo effects. J. Infect. Dis. 179: 124-135. (Pubitemid 29028347)
41. 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, eds. Kluwer Academic Publishers, Dordrecht, The Netherlands, p. 569-574.
42. 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 the gonococcal lipooligosaccharide. J. Biol. Chem. 269: 30345-30351.
43. Ram, S., M. Cullinane, A. M. Blom, S. Gulati, D. P. McQuillen, B. G. Monks, C. O'Connell, R. Boden, C. Elkins, M. K. Pangburn, et al. 2001. Binding of C4bbinding protein to porin: a molecular mechanism of serum resistance of Neisseria gonorrhoeae. J. Exp. Med. 193: 281-295. (Pubitemid 32524512)
44. Ram, S., D. P. McQuillen, S. Gulati, C. Elkins, M. K. Pangburn, and P. A. Rice. 1998. 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. 188: 671-680. (Pubitemid 28387930)
45. Cohen, M. S., J. G. Cannon, A. E. Jerse, L. M. Charniga, S. F. Isbey, and L. G. Whicker. 1994. Human experimentation with Neisseria gonorrhoeae: rationale, methods, and implications for the biology of infection and vaccine development. J. Infect. Dis. 169: 532-537. (Pubitemid 24062994)
46. Densen, P., S. Gulati, and P. A. Rice. 1987. Specificity of antibodies against Neisseria gonorrhoeae that stimulate neutrophil chemotaxis. Role of antibodies directed against lipooligosaccharides. J. Clin. Invest. 80: 78-87. (Pubitemid 17097519)
47. 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. (Pubitemid 28115190)
48. Banerjee, A., R. Wang, S. N. Uljon, P. A. Rice, E. C. Gotschlich, and D. C. Stein. 1998. Identification of the gene (lgtG) encoding the lipooligosaccharide beta chain synthesizing glucosyl transferase from Neisseria gonorrhoeae. Proc. Natl. Acad. Sci. USA 95: 10872-10877. (Pubitemid 28413161)
49. 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.
50. Rice, P. A., E. W. Hook, M. S. Blake, R. S. Kaslow, S. Gulati, P. K. Kohl, M. VanRadden, and T. M. Buchanan. 1994. A possible influence of vaccine induced Por, LOS, and Rmp antibodies on the outcome of intraurethral challenge with Neisseria gonorrhoeae. In Proceedings of the Ninth International Pathogenic Neisseria Conference. J. S. Evans, S. E. Yost, M. C. Maiden, and I. M. Feavers, eds, Winchester, London, p. 483-484.
51. Gulati, S., D. P. McQuillen, R. E. Mandrell, D. B. Jani, and P. A. Rice. 1996. Immunogenicity of Neisseria gonorrhoeae lipooligosaccharide epitope 2C7, widely expressed in vivo with no immunochemical similarity to human glycosphingolipids. [Published erratum appears in 1997 J. Infect. Dis. 175: 1027.] J. Infect. Dis. 174: 1223-1237. (Pubitemid 26393901)
52. Mandrell, R., H. Schneider, M. Apicella, W. Zollinger, P. A. Rice, and J. M. Griffiss. 1986. Antigenic and physical diversity of Neisseria gonorrhoeae lipooligosaccharides. Infect. Immun. 54: 63-69. (Pubitemid 16021214)
53. Agarwal, S., V. P. Ferreira, C. Cortes, M. K. Pangburn, P. A. Rice, and S. Ram. 2010. An evaluation of the role of properdin in alternative pathway activation on Neisseria meningitidis and Neisseria gonorrhoeae. J. Immunol. 185: 507-516.
54. McQuillen, D. P., S. Gulati, and P. A. Rice. 1994. Complement-mediated bacterial killing assays. Methods Enzymol. 236: 137-147. (Pubitemid 24283610)
55. 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.
56. Gulati, S., K. Sastry, J. C. Jensenius, P. A. Rice, and S. Ram. 2002. Regulation of the mannan-binding lectin pathway of complement on Neisseria gonorrhoeae by C1-inhibitor and alpha 2-macroglobulin. J. Immunol. 168: 4078-4086. (Pubitemid 34298415)
57. Ram, S., J. Ngampasutadol, A. D. Cox, A. M. Blom, L. A. Lewis, F. St Michael, J. Stupak, S. Gulati, and P. A. Rice. 2007. Heptose I glycan substitutions on Neisseria gonorrhoeae lipooligosaccharide influence C4b-binding protein binding and serum resistance. Infect. Immun. 75: 4071-4081. (Pubitemid 47206306)
58. Cannon, J. G. 1989. Conserved lipoproteins of pathogenic Neisseria species bearing the H.8 epitope: lipid-modified azurin and H.8 outer membrane protein. Clin. Microbiol. Rev. 2(Suppl): S1-S4.
59. 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. (Pubitemid 14192821)
60. Fearon, D. T., and K. F. Austen. 1977. Activation of the alternative complement pathway due to resistance of zymosan-bound amplification convertase to endogenous regulatory mechanisms. Proc. Natl. Acad. Sci. USA 74: 1683-1687. (Pubitemid 8087040)
61. Pillemer, L., L. Blum, I. H. Lepow, O. A. Ross, E. W. Todd, and A. C. Wardlaw. 1954. The properdin system and immunity. I. Demonstration and isolation of a new serum protein, properdin, and its role in immune phenomena. Science 120: 279-285.
62. 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.
63. Schneider, H., J. M. Griffiss, R. E. Mandrell, and G. A. Jarvis. 1985. Elaboration of a 3.6-kilodalton lipooligosaccharide, antibody against which is absent from human sera, is associated with serum resistance of Neisseria gonorrhoeae. Infect. Immun. 50: 672-677. (Pubitemid 16216857)
64. Figueroa, J., J. Andreoni, and P. Densen. 1993. Complement deficiency states and meningococcal disease. Immunol. Res. 12: 295-311. (Pubitemid 23357454)
65. Roantree, R. J., and L. A. Rantz. 1960. A Study of the Relationship of the Normal Bactericidal Activity of Human Serum to Bacterial Infection. J. Clin. Invest. 39: 72-81.
66. Figueroa, J. E., and P. Densen. 1991. Infectious diseases associated with complement deficiencies. Clin. Microbiol. Rev. 4: 359-395. (Pubitemid 21920404)
67. Ram, S., L. A. Lewis, and P. A. Rice. 2010. Infections of people with complement deficiencies and patients who have undergone splenectomy. Clin. Microbiol. Rev. 23: 740-780.
68. Tapsall, J. W. 2009. Neisseria gonorrhoeae and emerging resistance to extended spectrum cephalosporins. Curr. Opin. Infect. Dis. 22: 87-91.
69. Braconier, J. H., H. Odeberg, and A. G. Sjöholm. 1983. Granulocyte phagocytosis of Streptococcus pneumoniae in properdin-deficient serum. Infect. Immun. 40: 219-224. (Pubitemid 13163060)
70. Camous, L., L. Roumenina, S. Bigot, S. Brachemi, V. Frémeaux- Bacchi, P. Lesavre, and L. Halbwachs-Mecarelli. 2011. Complement alternative pathway acts as a positive feedback amplification of neutrophil activation. Blood 117: 1340-1349.