Distinct Binding and Immunogenic Properties of the Gonococcal Homologue of Meningococcal Factor H Binding Protein

PLoS Pathogens

Volumn 9, Issue 8, 2013, Pages

  Jongerius, Ilse ^a   Lavender, Hayley ^a   Tan, Lionel ^b   Ruivo, Nicola ^b   Exley, Rachel M ^a   Caesar, Joseph J E ^a   Lea, Susan M ^a   Johnson, Steven ^a   Tang, Christoph M ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT FACTOR H; BACTERIAL ANTIGEN; BACTERIAL PROTEIN; FACTOR H-BINDING PROTEIN, NEISSERIA MENINGITIDIS; MENINGOCOCCUS VACCINE;

ANIMAL EXPERIMENT; ARTICLE; BACTERICIDAL ACTIVITY; BINDING AFFINITY; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; IMMUNE RESPONSE; IMMUNOGENICITY; NEISSERIA GONORRHOEAE; NEISSERIA MENINGITIDIS; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PURIFICATION; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; SERUM BACTERICIDAL ACTIVITY; SURFACE PLASMON RESONANCE; WESTERN BLOTTING; AMINO ACID SUBSTITUTION; GENETICS; IMMUNOLOGY;

AMINO ACID SUBSTITUTION; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; MENINGOCOCCAL VACCINES; NEISSERIA GONORRHOEAE; NEISSERIA MENINGITIDIS, SEROGROUP A; NEISSERIA MENINGITIDIS, SEROGROUP B; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84883376289     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003528     Document Type: Article

References (46)

1. Van DM, Brandtzaeg P, van der Meer JW, (2000) Update on meningococcal disease with emphasis on pathogenesis and clinical management. Clin Microbiol Rev 13: 144-66.
2. Yazdankhah SP, Caugant DA, (2004) Neisseria meningitidis: an overview of the carriage state. J Med Microbiol 53: 821-832.
3. Rosenstein NE, Perkins BA, Stephens DS, Popovic T, Hughes JM, (2001) Meningococcal disease. N Engl J Med 344: 1378-1388.
4. Stephens DS, Greenwood B, Brandtzaeg P, (2007) Epidemic meningitis, meningococcaemia, and Neisseria meningitidis. Lancet 369: 2196-2210.
5. Trotter CL, Ramsay ME, (2007) Vaccination against meningococcal disease in Europe: review and recommendations for the use of conjugate vaccines. FEMS Microbiol Rev 31: 101-107.
6. Finne J, Leinonen M, Makela PH, (1983) Antigenic similarities between brain components and bacteria causing meningitis. Implications for vaccine development and pathogenesis. Lancet 2: 355-357.
7. Oster P, O'Hallahan J, Aaberge I, Tilman S, Ypma E, et al. (2007) Immunogenicity and safety of a strain-specific MenB OMV vaccine delivered to under 5-year olds in New Zealand. Vaccine 25: 3075-3079.
8. Masignani V, Comanducci M, Giuliani MM, Bambini S, Adu-Bobie J, et al. (2003) Vaccination against Neisseria meningitidis using three variants of the lipoprotein GNA1870. J Exp Med 197: 789-799.
9. Fletcher LD, Bernfield L, Barniak V, Farley JE, Howell A, et al. (2004) Vaccine potential of the Neisseria meningitidis 2086 lipoprotein. Infect Immun 72: 2088-2100.
10. Schneider MC, Exley RM, Chan H, Feavers I, Kang YH, et al. (2006) Functional significance of factor H binding to Neisseria meningitidis. J Immunol 176: 7566-7575.
11. Madico G, Welsch JA, Lewis LA, McNaughton A, Perlman DH, et al. (2006) The meningococcal vaccine candidate GNA1870 binds the complement regulatory protein factor H and enhances serum resistance. J Immunol 177: 501-510.
12. Schneider MC, Prosser BE, Caesar JJ, Kugelberg E, Li S, et al. (2009) Neisseria meningitidis recruits factor H using protein mimicry of host carbohydrates. Nature 458: 890-893.
13. Johnson S, Tan L, van der Veen S, Caesar J, Goicoechea De Jorge E, et al. (2012) Design and Evaluation of Meningococcal Vaccines through Structure-Based Modification of Host and Pathogen Molecules. PLoS Pathog 8: e1002981.
14. Seib KL, Brunelli B, Brogioni B, Palumbo E, Bambini S, et al. (2011) 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 79: 970-981.
15. Ram S, McQuillen DP, Gulati S, Elkins C, Pangburn MK, et al. (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.
16. Hadad R, Jacobsson S, Pizza M, Rappuoli R, Fredlund H, et al. (2012) Novel meningococcal 4CMenB vaccine antigens- prevalence and polymorphisms of the encoding genes in Neisseria gonorrhoeae. APMIS 120: 750-760.
17. Welsch JA, Ram S, (2008) Factor H and Neisserial pathogenesis. Vaccine 26 Suppl 8: I40-I45.
18. Shell DM, Chiles L, Judd RC, Seal S, Rest RF, (2002) The Neisseria lipooligosaccharide-specific alpha-2,3-sialyltransferase is a surface-exposed outer membrane protein. Infect Immun 70: 3744-3751.
19. Lucidarme J, Comanducci M, Findlow J, Gray SJ, Kaczmarski EB, et al. (2010) Characterization of fHbp, nhba (gna2132), nadA, porA, and sequence type in group B meningococcal case isolates collected in England and Wales during January 2008 and potential coverage of an investigational group B meningococcal vaccine. Clin Vaccine Immunol 17: 919-929.
20. Schneider MC, Exley RM, Ram S, Sim RB, Tang CM, (2007) Interactions between Neisseria meningitidis and the complement system. Trends Microbiol 15: 233-240.
21. Schielke S, Frosch M, Kurzai O, (2010) Virulence determinants involved in differential host niche adaptation of Neisseria meningitidis and Neisseria gonorrhoeae. Med Microbiol Immunol 199: 185-196.
22. Shaughnessy J, Ram S, Bhattacharjee A, Pedrosa J, Tran C, et al. (2011) Molecular characterization of the interaction between sialylated Neisseria gonorrhoeae and factor H. J Biol Chem 286: 22235-22242.
23. Kahler CM, Martin LE, Shih GC, Rahman MM, Carlson RW, et al. (1998) The (alpha2→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.
24. Nairn CA, Cole JA, Patel PV, Parsons NJ, Fox JE, et al. (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.
25. Fox AJ, Jones DM, Scotland SM, Rowe B, Smith A, et al. (1989) Serum killing of meningococci and several other gram-negative bacterial species is not decreased by incubating them with cytidine 5′-monophospho-N-acetyl neuraminic acid. Microb Pathog 7: 317-318.
26. Madico G, Ngampasutadol J, Gulati S, Vogel U, Rice PA, et al. (2007) Factor H binding and function in sialylated pathogenic neisseriae is influenced by gonococcal, but not meningococcal, porin. J Immunol 178: 4489-4497.
27. Vogel U, Frosch M, (1999) Mechanisms of neisserial serum resistance. Mol Microbiol 32: 1133-1139.
28. Ram S, Cullinane M, Blom AM, Gulati S, McQuillen DP, et al. (2001) C4bp binding to porin mediates stable serum resistance of Neisseria gonorrhoeae. Int Immunopharmacol 1: 423-432.
29. Ram S, Cullinane M, Blom AM, Gulati S, McQuillen DP, et al. (2001) Binding of C4b-binding protein to porin: a molecular mechanism of serum resistance of Neisseria gonorrhoeae. J Exp Med 193: 281-295.
30. Seib KL, Serruto D, Oriente F, Delany I, Adu-Bobie J, et al. (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.
31. Veggi D, Gentile MA, Cantini F, Lo SP, Nardi-Dei V, et al. (2012) The Factor H Binding Protein of Neisseria meningitidis Interacts with Xenosiderophores in Vitro. Biochemistry 51: 9384-9393.
32. Richmond PC, Marshall HS, Nissen MD, Jiang Q, Jansen KU, et al. (2012) 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 12: 597-607.
33. Santolaya ME, O'Ryan ML, Valenzuela MT, Prado V, Vergara R, et al. (2012) Immunogenicity and tolerability of a multicomponent meningococcal serogroup B (4CMenB) vaccine in healthy adolescents in Chile: a phase 2b/3 randomised, observer-blind, placebo-controlled study. Lancet 379: 617-624.
34. Gossger N, Snape MD, Yu LM, Finn A, Bona G, et al. (2012) 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 307: 573-582.
35. Giuliani MM, Adu-Bobie J, Comanducci M, Arico B, Savino S, et al. (2006) A universal vaccine for serogroup B meningococcus. Proc Natl Acad Sci U S A 103: 10834-10839.
36. Maslanka SE, Gheesling LL, Libutti DE, Donaldson KB, Harakeh HS, et al. (1997) Standardization and a multilaboratory comparison of Neisseria meningitidis serogroup A and C serum bactericidal assays. The Multilaboratory Study Group. Clin Diagn Lab Immunol 4: 156-167.
37. Lewis LA, Ngampasutadol J, Wallace R, Reid JE, Vogel U, et al. (2010) The meningococcal vaccine candidate neisserial surface protein A (NspA) binds to factor H and enhances meningococcal resistance to complement. PLoS Pathog 6: e1001027.
38. Beernink PT, Granoff DM, (2008) Bactericidal antibody responses induced by meningococcal recombinant chimeric factor H-binding protein vaccines. Infect Immun 76: 2568-2575.
39. Scarselli M, Arico B, Brunelli B, Savino S, Di MF, et al. (2011) Rational design of a meningococcal antigen inducing broad protective immunity. Sci Transl Med 3: 91.
40. Beernink PT, Granoff DM, (2009) The modular architecture of meningococcal factor H-binding protein. Microbiology 155: 2873-2883.
41. Carroll MC, (2004) The complement system in B cell regulation. Mol Immunol 41: 141-146.
42. Zipfel PF, Skerka C, Hellwage J, Jokiranta ST, Meri S, et al. (2002) Factor H family proteins: on complement, microbes and human diseases. Biochem Soc Trans 30: 971-978.
43. Beernink PT, Shaughnessy J, Braga EM, Liu Q, Rice PA, et al. (2011) A meningococcal factor H binding protein mutant that eliminates factor H binding enhances protective antibody responses to vaccination. J Immunol 186: 3606-3614.
44. Lucidarme J, Tan L, Exley RM, Findlow J, Borrow R, et al. (2011) Characterization of Neisseria meningitidis isolates that do not express the virulence factor and vaccine antigen factor H binding protein. Clin Vaccine Immunol 18: 1002-1014.
45. Mehr IJ, Seifert HS, (1998) Differential roles of homologous recombination pathways in Neisseria gonorrhoeae pilin antigenic variation, DNA transformation and DNA repair. Mol Microbiol 30: 697-710.
46. Exley RM, Shaw J, Mowe E, Sun YH, West NP, et al. (2005) Available carbon source influences the resistance of Neisseria meningitidis against complement. J Exp Med 201: 1637-1645.