FH-dependent complement evasion by disease-causing meningococcal strains with absent fHbp genes or frameshift mutations

Vaccine

Volumn 31, Issue 38, 2013, Pages 4192-4199

  Giuntini, Serena ^a   Vu, David M ^a   Granoff, Dan M ^a  

^a CHILDREN S HOSPITAL OAKLAND RESEARCH INSTITUTE   (United States)

Author keywords

Complement; Factor H; FHbp; Neisseria meningitidis; NspA; Transgenic rat; Vaccine

Indexed keywords

BACTERIAL ANTIGEN; COMPLEMENT FACTOR H; MENINGOCOCCUS VACCINE; VIRULENCE FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GENE; BACTERIAL SURVIVAL; COMPLEMENT FIXATION; COMPLEMENT SYSTEM; CONTROLLED STUDY; DOWN REGULATION; FHBP GENE; FLOW CYTOMETRY; FRAMESHIFT MUTATION; IMMUNE EVASION; MENINGOCOCCEMIA; NEISSERIA MENINGITIDIS; NONHUMAN; NSPA GENE; PATHOGENESIS; PRIORITY JOURNAL; RAT; TRANSGENIC RAT;

COMPLEMENT; FACTOR H; FACTOR H-BINDING PROTEIN; FH; FHBP; NEISSERIA MENINGITIDIS; NEISSERIA SURFACE PROTEIN A; NSPA; TRANSGENIC RAT; VACCINE;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; COMPLEMENT FACTOR H; FLOW CYTOMETRY; FRAMESHIFT MUTATION; HOST-PATHOGEN INTERACTIONS; HUMANS; LIPOPOLYSACCHARIDES; MENINGOCOCCAL INFECTIONS; NEISSERIA MENINGITIDIS, SEROGROUP B; RATS; RATS, TRANSGENIC;

EID: 84881551209     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2013.06.009     Document Type: Article

References (46)

1. Cohn A.C., MacNeil J.R., Harrison L.H., Hatcher C., Theodore J., Schmidt M., et al. Changes in Neisseria meningitidis disease epidemiology in the United States, 1998-2007: implications for prevention of meningococcal disease. Clin Infect Dis 2010, 50:184-191.
2. Campbell H., Andrews N., Borrow R., Trotter C., Miller E. Updated postlicensure surveillance of the meningococcal C conjugate vaccine in England and Wales: effectiveness, validation of serological correlates of protection, and modeling predictions of the duration of herd immunity. Clin Vaccine Immunol 2010, 17:840-847.
3. Trotter C.L., Ramsay M.E. Vaccination against meningococcal disease in Europe: review and recommendations for the use of conjugate vaccines. FEMS Microbiol Rev 2007, 31:101-107.
4. Trotter C.L., Chandra M., Cano R., Larrauri A., Ramsay M.E., Brehony C., et al. A surveillance network for meningococcal disease in Europe. FEMS Microbiol Rev 2007, 31:27-36.
5. Finne J., Leinonen M., Makela P.H. Antigenic similarities between brain components and bacteria causing meningitis. Implications for vaccine development and pathogenesis. Lancet 1983, 2:355-357.
6. Gossger N., Snape M.D., Yu L.M., Finn A., Bona G., Esposito S., et al. Immunogenicity and tolerability of recombinant serogroup B meningococcal vaccine administered with or without routine infant vaccinations according to different immunization schedules: a randomized controlled trial. JAMA 2012, 307:573-582.
7. Snape M.D., Dawson T., Oster P., Evans A., John T.M., Ohene-Kena B., et al. Immunogenicity of two investigational serogroup B meningococcal vaccines in the first year of life: a randomized comparative trial. Pediatr Infect Dis J 2010, 29:e71-e79.
8. Findlow J., Borrow R., Snape M.D., Dawson T., Holland A., John T.M., et al. Multicenter, open-label, randomized phase II controlled trial of an investigational recombinant meningococcal serogroup B vaccine with and without outer membrane vesicles, administered in infancy. Clin Infect Dis 2010, 51:1127-1137.
9. Richmond P.C., Marshall H.S., Nissen M.D., Jiang Q., Jansen K.U., Garces-Sanchez M., et al. Safety, immunogenicity, and tolerability of meningococcal serogroup B bivalent recombinant lipoprotein 2086 vaccine in healthy adolescents: a randomised, single-blind, placebo-controlled, phase 2 trial. Lancet Infect Dis 2012, 12:597-607.
10. Marshall H.S., Richmond P.C., Nissen M.D., Jiang Q., Anderson A.S., Jansen K.U., et al. Safety and immunogenicity of a meningococcal B bivalent rLP2086 vaccine in healthy toddlers aged 18-36 months: a phase 1 randomized controlled clinical trial. Pediatr Infect Dis J 2012, 31:1061-1068.
11. Granoff D.M. European Medicines Agency Recommends Approval of a Broadly Protective Vaccine against Serogroup B Meningococcal Disease. Pediatr Infect Dis J 2012, 32:372-373.
12. Madico G., Welsch J.A., Lewis L.A., McNaughton A., Perlman D.H., Costello C.E., et al. The meningococcal vaccine candidate GNA1870 binds the complement regulatory protein factor H and enhances serum resistance. J Immunol 2006, 177:501-510.
13. Granoff D.M., Welsch J.A., Ram S. Binding of complement factor H (fH) to Neisseria meningitidis is specific for human fH and inhibits complement activation by rat and rabbit sera. Infect Immun 2009, 77:764-769.
14. Welsch J.A., Ram S., Koeberling O., Granoff D.M. Complement-dependent synergistic bactericidal activity of antibodies against factor H-binding protein, a sparsely distributed meningococcal vaccine antigen. J Infect Dis 2008, 197:1053-1061.
15. Welsch J.A., Ram S., Factor H. Neisserial pathogenesis. Vaccine 2008, 26(Suppl. 8):I40-I45.
16. Vu D.M., Shaughnessy J., Lewis L.A., Ram S., Rice P.A., Granoff D.M. Enhanced bacteremia in human factor H transgenic rats infected by Neisseria meningitidis. Infect Immun 2012, 80:643-650.
17. Masignani V., Comanducci M., Giuliani M.M., Bambini S., Adu-Bobie J., Arico B., et al. Vaccination against Neisseria meningitidis using three variants of the lipoprotein GNA1870. J Exp Med 2003, 197:789-799.
18. Beernink P.T., Leipus A., Granoff D.M. Rapid genetic grouping of factor H-binding protein (genome-derived neisserial antigen 1870), a promising group B meningococcal vaccine candidate. Clin Vaccine Immunol 2006, 13:758-763.
19. Murphy E., Andrew L., Lee K.L., Dilts D.A., Nunez L., Fink P.S., et al. Sequence diversity of the factor H binding protein vaccine candidate in epidemiologically relevant strains of serogroup B Neisseria meningitidis. J Infect Dis 2009, 200:379-389.
20. Lucidarme J., Tan L., Exley R.M., Findlow J., Borrow R., Tang C.M. Characterization of Neisseria meningitidis isolates that do not express the virulence factor and vaccine antigen factor H binding protein. Clin Vaccine Immunol 2011, 18:1002-1014.
21. Pajon R., Beernink P.T., Granoff D.M. Design of meningococcal factor h binding protein mutant vaccines that do not bind human complement factor h. Infect Immun 2012, 80:2667-2677.
22. Sacchi C.T., Lemos A.P., Whitney A.M., Solari C.A., Brandt M.E., Melles C.E., et al. Correlation between serological and sequencing analyses of the PorB outer membrane protein in the Neisseria meningitidis serotyping system. Clin Diagn Lab Immunol 1998, 5:348-354.
23. Abad R., Alcala B., Salcedo C., Enriquez R., Uria M.J., Diez P., et al. Sequencing of the porB gene: a step toward a true characterization of Neisseria meningitidis. Clin Vaccine Immunol 2006, 13:1087-1091.
24. Lewis L.A., Carter M., Ram S. 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 2012, 188:5063-5072.
25. Lewis L.A., Ngampasutadol J., Wallace R., Reid J.E., Vogel U., Ram S. The meningococcal vaccine candidate neisserial surface protein A (NspA) binds to factor H and enhances meningococcal resistance to complement. PLoS Pathog 2010, 6:e1001027.
26. Moe G.R., Zuno-Mitchell P., Lee S.S., Lucas A.H., Granoff D.M. Functional activity of anti-neisserial surface protein A monoclonal antibodies against strains of Neisseria meningitidis serogroup B. Infect Immun 2001, 69:3762-3771.
27. Giuntini S., Reason D.C., Granoff D.M. Complement-mediated bactericidal activity of anti-factor H binding protein monoclonal antibodies against the meningococcus relies upon blocking factor H binding. Infect Immun 2011, 79:3751-3759.
28. Mandrell R.E., Kim J.J., John C.M., Gibson B.W., Sugai J.V., Apicella M.A., et al. Endogenous sialylation of the lipooligosaccharides of Neisseria meningitidis. J Bacteriol 1991, 173:2823-2832.
29. Granoff D.M., Bartoloni A., Ricci S., Gallo E., Rosa D., Ravenscroft N., et al. Bactericidal monoclonal antibodies that define unique meningococcal B polysaccharide epitopes that do not cross-react with human polysialic acid. J Immunol 1998, 160:5028-5036.
30. Moe G.R., Zuno-Mitchell P., Hammond S.N., Granoff D.M. Sequential immunization with vesicles prepared from heterologous Neisseria meningitidis strains elicits broadly protective serum antibodies to group B strains. Infect Immun 2002, 70:6021-6031.
31. Vu D.M., Pajon R., Reason D.C., Granoff D.M. A broadly cross-reactive monoclonal antibody against an epitope on the N-terminus of meningococcal fHbp. Sci Rep 2012, 2:341.
32. Beernink P.T., Shaughnessy J., Braga E.M., Liu Q., Rice P.A., Ram S., et al. A meningococcal factor H binding protein mutant that eliminates factor H binding enhances protective antibody responses to vaccination. J Immunol 2011, 186:3606-3614.
33. Welsch J.A., Granoff D. Naturally acquired passive protective activity against Neisseria meningitidis Group C in the absence of serum bactericidal activity. Infect Immun 2004, 72:5903-5909.
34. Tsang R.S., Law D.K., Tsai C., Ng L. Detection of the lst gene in different serogroups and LOS immunotypes of Neisseria meningitidis. FEMS Microbiol Lett 2001, 199:203-206.
35. Smith H., Parsons N.J., Cole J.A. Sialylation of neisserial lipopolysaccharide: a major influence on pathogenicity. Microb Pathog 1995, 19:365-377.
36. Borrow R., Carlone G.M., Rosenstein N., Blake M., Feavers I., Martin D., et al. Neisseria meningitidis group B correlates of protection and assay standardization - international meeting report Emory University, Atlanta, Georgia, United States, 16-17 March 2005. Vaccine 2006, 24:5093-5107.
37. Schneider M.C., Exley R.M., Ram S., Sim R.B., Tang C.M. Interactions between Neisseria meningitidis and the complement system. Trends Microbiol 2007, 15:233-240.
38. Schneider M.C., Exley R.M., Chan H., Feavers I., Kang Y.H., Sim R.B., et al. Functional significance of factor H binding to Neisseria meningitidis. J Immunol 2006, 176:7566-7575.
39. Lu D., Silhan J., Macdonald J.T., Carpenter E.P., Jensen K., Tang C.M., et al. Structural basis for the recognition and cleavage of abasic DNA in Neisseria meningitidis. Proc Natl Acad Sci U S A 2012, 42:16852-16857.
40. Quattroni P., Li Y., Lucchesi D., Lucas S., Hood D.W., Herrmann M., et al. Galectin-3 binds Neisseria meningitidis and increases interaction with phagocytic cells. Cell Microbiol 2012, 14:1657-1675.
41. Fletcher L.D., Bernfield L., Barniak V., Farley J.E., Howell A., Knauf M., et al. Vaccine potential of the Neisseria meningitidis 2086 lipoprotein. Infect Immun 2004, 72:2088-2100.
42. Seib K.L., Serruto D., Oriente F., Delany I., Adu-Bobie J., Veggi D., et al. 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 2009, 77:292-299.
43. Seib K.L., Brunelli B., Brogioni B., Palumbo E., Bambini S., Muzzi A., et al. Characterization of diverse subvariants of the meningococcal factor H (fH) binding protein for their ability to bind fH, to mediate serum resistance, and to induce bactericidal antibodies. Infect Immun 2011, 79:970-981.
44. Dunphy K.Y., Beernink P.T., Brogioni B., Granoff D.M. Effect of factor H-binding protein sequence variation on factor H binding and survival of Neisseria meningitidis in human blood. Infect Immun 2011, 79:353-359.
45. Giuntini S., Reason D.C., Granoff D.M. Combined roles of human IgG subclass, alternative complement pathway activation, and epitope density in the bactericidal activity of antibodies to meningococcal factor h binding protein. Infect Immun 2012, 80:187-194.
46. Gray S.J., Trotter C.L., Ramsay M.E., Guiver M., Fox A.J., Borrow R., et al. Epidemiology of meningococcal disease in England and Wales 1993/94 to 2003/04: contribution and experiences of the Meningococcal reference unit. J Med Microbiol 2006, 55:887-896.