Effect of complement Factor H on antibody repertoire and protection elicited by meningococcal capsular group B vaccines containing Factor H binding protein

References

• Finne J, Leinonen M, Makela PH. Antigenic similarities between brain components and bacteria causing meningitis. Implications for vaccine development and pathogenesis. Lancet. 1983;2:355–57. doi:10.1016/s0140-6736(83)90340-9.
   PubMed Web of Science ®Google Scholar
• Tettelin H, Saunders NJ, Heidelberg J, Jeffries AC, Nelson KE, Eisen JA, Ketchum KA, Hood DW, Peden JF, Dodson RJ, et al. Complete genome sequence of Neisseria meningitidis serogroup B strain MC58. Science. 2000;287:1809–15. doi:10.1126/science.287.5459.1809.
   PubMed Web of Science ®Google Scholar
• Pizza M, Scarlato V, Masignani V, Giuliani MM, Arico B, Comanducci M, Jennings GT, Baldi L, Bartolini E, Capecchi B, et al. Identification of vaccine candidates against serogroup B meningococcus by whole-genome sequencing. Science. 2000;287:1816–20. doi:10.1126/science.287.5459.1816.
   PubMed Web of Science ®Google Scholar
• Granoff DM. Commentary: European medicines agency recommends approval of a broadly protective vaccine against serogroup B meningococcal disease. Pediatr Infect Dis J. 2013;32:372–73. doi:10.1097/INF.0b013e318282942f.
   PubMed Web of Science ®Google Scholar
• Giuliani MM, Adu-Bobie J, Comanducci M, Arico B, Savino S, Santini L, Brunelli B, Bambini S, Biolchi A, Capecchi B, et al. A universal vaccine for serogroup B meningococcus. Proc Natl Acad Sci USA. 2006;103:10834–39. doi:10.1073/pnas.0603940103.
   PubMed Web of Science ®Google Scholar
• Jiang HQ, Hoiseth SK, Harris SL, McNeil LK, Zhu D, Tan C, Scott AA, Alexander K, Mason K, Miller L, et al. Broad vaccine coverage predicted for a bivalent recombinant factor H binding protein based vaccine to prevent serogroup B meningococcal disease. Vaccine. 2010;28:6086–93. doi:10.1016/j.vaccine.2010.06.083.
   PubMed Web of Science ®Google Scholar
• Bai X, Findlow J, Borrow R. Recombinant protein meningococcal serogroup B vaccine combined with outer membrane vesicles. Expert Opin Biol Ther. 2011;11:969–85. doi:10.1517/14712598.2011.585965.
   PubMed Web of Science ®Google Scholar
• Masignani V, Comanducci M, Giuliani MM, Bambini S, Adu-Bobie J, Arico B, Brunelli B, Pieri A, Santini L, Savino S, et al. Vaccination against Neisseria meningitidis using three variants of the lipoprotein GNA1870. J Exp Med. 2003;197:789–99. doi:10.1084/jem.20021911.
   PubMed Web of Science ®Google Scholar
• Fletcher LD, Bernfield L, Barniak V, Farley JE, Howell A, Knauf M, Ooi P, Smith RP, Weise P, Wetherell M, et al. Vaccine potential of the Neisseria meningitidis 2086 lipoprotein. Infect Immun. 2004;72:2088–100. doi:10.1128/IAI.72.4.2088-2100.2004.
   PubMed Web of Science ®Google Scholar
• Su EL, Snape MD. A combination recombinant protein and outer membrane vesicle vaccine against serogroup B meningococcal disease. Expert Rev Vaccines. 2011;10:575–88. doi:10.1586/erv.11.32.
   PubMed Web of Science ®Google Scholar
• Findlow J. Meningococcal group B vaccines. Hum Vaccin Immunother. 2013;9:1387–88. doi:10.4161/hv.24689.
   PubMed Web of Science ®Google Scholar
• Esposito S, Principi N. Vaccine profile of 4CMenB: a four-component Neisseria meningitidis serogroup B vaccine. Expert Rev Vaccines. 2014;13:193–202. doi:10.1586/14760584.2014.874949.
   PubMed Web of Science ®Google Scholar
• Andrews SM, Pollard AJ. A vaccine against serogroup B Neisseria meningitidis: dealing with uncertainty. Lancet Infect Dis. 2014;14:426–34. doi:10.1016/S1473-3099(13)70341-4.
   PubMed Web of Science ®Google Scholar
• Seib KL, Scarselli M, Comanducci M, Toneatto D, Masignani V. Neisseria meningitidis factor H-binding protein fHbp: a key virulence factor and vaccine antigen. Expert Rev Vaccines. 2015;14:841–59. doi:10.1586/14760584.2015.1016915.
   PubMed Web of Science ®Google Scholar
• Gandhi A, Balmer P, York LJ. Characteristics of a new meningococcal serogroup B vaccine, bivalent rLP2086 (MenB-FHbp; Trumenba(R)). Postgrad Med. 2016;128:548–56. doi:10.1080/00325481.2016.1203238.
   PubMed Web of Science ®Google Scholar
• Mascioni A, Moy FJ, McNeil LK, Murphy E, Bentley BE, Camarda R, Dilts DA, Fink PS, Gusarova V, Hoiseth SK, et al. NMR dynamics and antibody recognition of the meningococcal lipidated outer membrane protein LP2086 in micellar solution. Biochim Biophys Acta. 2010;1798:87–93. doi:10.1016/j.bbamem.2009.09.021.
   PubMed Web of Science ®Google Scholar
• Goldschneider I, Gotschlich EC, Artenstein MS. Human immunity to the meningococcus. I. The role of humoral antibodies. J Exp Med. 1969;129:1307–26. doi:10.1084/jem.129.6.1307.
   PubMed Web of Science ®Google Scholar
• Konar M, Granoff DM, Beernink PT. Importance of inhibition of binding of complement factor H for serum bactericidal antibody responses to meningococcal factor H-binding protein vaccines. J Infect Dis. 2013;208:627–36. doi:10.1093/infdis/jit239.
   PubMed Web of Science ®Google Scholar
• Brunelli B, Del Tordello E, Palumbo E, Biolchi A, Bambini S, Comanducci M, Muzzi A, Pizza M, Rappuoli R, Donnelly JJ, et al. Influence of sequence variability on bactericidal activity sera induced by Factor H binding protein variant 1.1. Vaccine. 2011;29:1072–81. doi:10.1016/j.vaccine.2010.11.064.
   PubMed Web of Science ®Google Scholar
• Snape MD, Dawson T, Oster P, Evans A, John TM, Ohene-Kena B, Findlow J, Yu L-M, Borrow R, Ypma E, 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:e71–9. doi:10.1097/INF.0b013e3181f59f6d.
   PubMed Web of Science ®Google Scholar
• Findlow J, Borrow R, Snape MD, Dawson T, Holland A, John TM, Evans A, Telford KL, Ypma E, Toneatto D, 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;51:1127–37. doi:10.1086/656741.
   PubMed Web of Science ®Google Scholar
• Richmond PC, Nissen MD, Marshall HS, Lambert SB, Roberton D, Gruber WC, Jones TR, Arora A. A bivalent Neisseria meningitidis recombinant lipidated factor H binding protein vaccine in young adults: results of a randomised, controlled, dose-escalation phase 1 trial. Vaccine. 2012;30:6163–74. doi:10.1016/j.vaccine.2012.07.065.
   PubMed Web of Science ®Google Scholar
• Marshall HS, Richmond PC, Nissen MD, Jiang Q, Anderson AS, Jansen KU, Reynolds G, Ziegler JB, Harris SL, Jones TR, 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;31:1061–68. doi:10.1097/INF.0b013e31826327e4.
   PubMed Web of Science ®Google Scholar
• Perez JL, Absalon J, Beeslaar J, Balmer P, Jansen KU, Jones TR, Harris S, York LJ, Jiang Q, Radley D, et al. From research to licensure and beyond: clinical development of MenB-FHbp, a broadly protective meningococcal B vaccine. Expert Rev Vaccines. 2018;17:461–77. doi:10.1080/14760584.2018.1483726.
   PubMed Web of Science ®Google Scholar
• Giuntini S, Lujan E, Gibani MM, Dold C, Rollier CS, Pollard AJ, Granoff DM. Serum bactericidal antibody responses of adults immunized with the MenB-4C vaccine against genetically diverse serogroup B meningococci. Clin Vaccine Immunol. 2017;5:e00430–16.
   Google Scholar
• Lujan E, Partridge E, Giuntini S, Ram S, Granoff DM. Breadth and duration of meningococcal serum bactericidal activity in health care workers and microbiologists immunized with the MenB-FHbp vaccine. Clin Vaccine Immunol. 2017;24:e00121–17. doi:10.1128/CVI.00121-17.
   PubMed Web of Science ®Google Scholar
• Welsch JA, Senders S, Essink B, Klein T, Smolenov I, Pedotti P, Barbi S, Verma B, Toneatto D. Breadth of coverage against a panel of 110 invasive disease isolates, immunogenicity and safety for 2 and 3 doses of an investigational MenABCWY vaccine in US adolescents - results from a randomized, controlled, observer-blind phase II study. Vaccine. 2018;36:5309–17. doi:10.1016/j.vaccine.2018.07.016.
   PubMed Web of Science ®Google Scholar
• Donnelly J, Medini D, Boccadifuoco G, Biolchi A, Ward J, Frasch C, Moxon ER, Stella M, Comanducci M, Bambini S, et al. Qualitative and quantitative assessment of meningococcal antigens to evaluate the potential strain coverage of protein-based vaccines. Proc Natl Acad Sci USA. 2010;107:19490–95. doi:10.1073/pnas.1013758107.
   PubMed Web of Science ®Google Scholar
• Harris SL, Donald RG, Hawkins JC, Tan C, O’Neill R, McNeil LK, Perez JL, Anderson AS, Jansen KU, Jones TR. Neisseria meningitidis serogroup B vaccine, bivalent rLP2086, induces broad serum bactericidal activity against diverse invasive disease strains including outbreak strains. Pediatr Infect Dis J. 2017;36:216–23. doi:10.1097/INF.0000000000001399.
   PubMed Web of Science ®Google Scholar
• Harris SL, Tan C, Andrew L, Hao L, Liberator PA, Absalon J, Anderson AS, Jones TR. The bivalent factor H binding protein meningococcal serogroup B vaccine elicits bactericidal antibodies against representative non-serogroup B meningococci. Vaccine. 2018;36:6867–74. doi:10.1016/j.vaccine.2018.05.081.
   PubMed Web of Science ®Google Scholar
• Pajon R, Fergus AM, Koeberling O, Caugant DA, Granoff DM. Meningococcal factor H binding proteins in epidemic strains from Africa: implications for vaccine development. PLoS Negl Trop Dis. 2011;5:e1302. doi:10.1371/journal.pntd.0001370.
   PubMed Web of Science ®Google Scholar
• Ladhani SN, Campbell H, Parikh SR, Saliba V, Borrow R, Ramsay M. The introduction of the meningococcal B (MenB) vaccine (Bexsero®) into the national infant immunisation programme–new challenges for public health. J Infect. 2015;71:611–14. doi:10.1016/j.jinf.2015.09.035.
   PubMed Web of Science ®Google Scholar
• McNamara LA, Shumate AM, Johnsen P, MacNeil JR, Patel M, Bhavsar T, Cohn AC, Dinitz-Sklar J, Duffy J, Finnie J, et al. First use of a serogroup B meningococcal vaccine in the US in response to a university outbreak. Pediatrics. 2015;135:798–804. doi:10.1542/peds.2014-4015.
   PubMed Web of Science ®Google Scholar
• Folaranmi T, Rubin L, Martin SW, Patel M, MacNeil JR, Centers for disease C. Use of serogroup B meningococcal vaccines in persons aged >/=10 years at increased risk for serogroup B meningococcal disease: recommendations of the advisory committee on immunization practices, 2015. MMWR Morb Mortal Wkly Rep. 2015;64:608–12.
   PubMed Web of Science ®Google Scholar
• Beernink PT, Shaughnessy J, Braga EM, Liu Q, Rice PA, Ram S, Granoff DM. A meningococcal factor H binding protein mutant that eliminates factor H binding enhances protective antibody responses to vaccination. J Immunol. 2011;186:3606–14. doi:10.4049/jimmunol.1003470.
   PubMed Web of Science ®Google Scholar
• Costa I, Pajon R, Granoff DM. Human factor H (FH) impairs protective meningococcal anti-FHbp antibody responses and the antibodies enhance FH binding. mBio. 2014;5:e01625–14. doi:10.1128/mBio.01625-14.
   PubMed Web of Science ®Google Scholar
• Granoff DM, Costa I, Konar M, Giuntini S, Van Rompay KK, Beernink PT. Binding of complement Factor H (FH) decreases protective anti-FH binding protein antibody responses of infant rhesus macaques immunized with a meningococcal serogroup B vaccine. J Infect Dis. 2015;212:784–92. doi:10.1093/infdis/jiv081.
   PubMed Web of Science ®Google Scholar
• Schneider MC, Prosser BE, Caesar JJ, Kugelberg E, Li S, Zhang Q, Quoraishi S, Lovett JE, Deane JE, Sim RB, et al. Neisseria meningitidis recruits factor H using protein mimicry of host carbohydrates. Nature. 2009;458:890–93. doi:10.1038/nature07769.
   PubMed Web of Science ®Google Scholar
• Meri S, Jordens M, Jarva H. Microbial complement inhibitors as vaccines. Vaccine. 2008;26(Suppl 8):I113–7. doi:10.1016/j.vaccine.2008.11.058.
   PubMed Web of Science ®Google Scholar
• Granoff DM, Welsch JA, 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;77:764–69. doi:10.1128/IAI.01191-08.
   PubMed Web of Science ®Google Scholar
• Beernink PT, Shaughnessy J, Stefek H, Ram S, Granoff DM. Heterogeneity in rhesus macaque complement factor H binding to meningococcal factor H binding protein (FHbp) informs selection of primates to assess immunogenicity of FHbp-based vaccines. Clin Vaccine Immunol. 2014;21:1505–11. doi:10.1128/CVI.00517-14.
   PubMed Web of Science ®Google Scholar
• Konar M, Beernink PT, Granoff DM. A newly-identified polymorphism in rhesus macaque complement Factor H modulates binding affinity for meningococcal FHbp. PLoS One. 2015;10:e0135996. doi:10.1371/journal.pone.0135996.
   PubMed Web of Science ®Google Scholar
• Granoff DM, Giuntini S, Gowans FA, Lujan E, Sharkey K, Beernink PT. Enhanced protective antibody to a mutant meningococcal factor H-binding protein with low-factor H binding. JCI Insight. 2016;1:e88907. doi:10.1172/jci.insight.88907.
   PubMed Web of Science ®Google Scholar
• Giuliani MM, Biolchi A, Serruto D, Ferlicca F, Vienken K, Oster P, Rappuoli R, Pizza M, Donnelly J. Measuring antigen-specific bactericidal responses to a multicomponent vaccine against serogroup B meningococcus. Vaccine. 2010;28:5023–30. doi:10.1016/j.vaccine.2010.05.014.
   PubMed Web of Science ®Google Scholar
• Ufret-Vincenty RL, Aredo B, Liu X, McMahon A, Chen PW, Sun H, Niederkorn JY, Kedzierski W. Transgenic mice expressing variants of complement factor H develop AMD-like retinal findings. Invest Ophthalmol Vis Sci. 2010;51:5878–87. doi:10.1167/iovs.09-4457.
   PubMed Web of Science ®Google Scholar
• Granoff DM, Ram S, Beernink PT. Does binding of complement factor H to the meningococcal vaccine antigen, factor H binding protein, decrease protective serum antibody responses? Clin Vaccine Immunol. 2013;20:1099–107. doi:10.1128/CVI.00260-13.
   PubMed Web of Science ®Google Scholar
• Koeberling O, Seubert A, Santos G, Colaprico A, Ugozzoli M, Donnelly J, Granoff DM. Immunogenicity of a meningococcal native outer membrane vesicle vaccine with attenuated endotoxin and over-expressed factor H binding protein in infant rhesus monkeys. Vaccine. 2011;29:4728–34. doi:10.1016/j.vaccine.2011.04.095.
   PubMed Web of Science ®Google Scholar
• Giuntini S, Beernink PT, Granoff DM. Effect of complement factor H on anti-FHbp serum bactericidal antibody responses of infant rhesus macaques boosted with a licensed meningococcal serogroup B vaccine. Vaccine. 2015;33:7168–75. doi:10.1016/j.vaccine.2015.10.135.
   PubMed Web of Science ®Google Scholar
• Mascioni A, Bentley BE, Camarda R, Dilts DA, Fink P, Gusarova V, Hoiseth SK, Jacob J, Lin SL, Malakian K, et al. Structural basis for the immunogenic properties of the meningococcal vaccine candidate LP2086. J Biol Chem. 2009;284:8738–46. doi:10.1074/jbc.M808831200.
   PubMed Web of Science ®Google Scholar
• Cendron L, Veggi D, Girardi E, Zanotti G. Structure of the uncomplexed Neisseria meningitidis factor H-binding protein fHbp (rLP2086). Acta Crystallogr Sect F Struct Biol Cryst Commun. 2011;67:531–35. doi:10.1107/S1744309111006154.
   PubMedGoogle Scholar
• Johnson S, Tan L, van der Veen S, Caesar J, Goicoechea De Jorge E, Harding RJ, Bai X, Exley RM, Ward PN, Ruivo N, et al. Design and evaluation of meningococcal vaccines through structure-based modification of host and pathogen molecules. PLoS Pathog. 2012;8:e1002981. doi:10.1371/journal.ppat.1002981.
   PubMed Web of Science ®Google Scholar
• Konar M, Pajon R, Beernink PT. A meningcoccal vaccine antigen engineered to increase thermal stability and stabilize protective epitopes. Proc Natl Acad Sci USA. 2015;112:14823–28. doi:10.1073/pnas.1507829112.
   PubMed Web of Science ®Google Scholar
• Pajon R, Beernink PT, Granoff DM. Design of meningococcal factor H binding protein mutant vaccines that do not bind human complement factor H. Infect Immun. 2012;80:2667–77. doi:10.1128/IAI.00103-12.
   PubMed Web of Science ®Google Scholar
• Beernink PT, Shaughnessy J, Pajon R, Braga EM, Ram S, Granoff DM. The effect of human factor H on immunogenicity of meningococcal native outer membrane vesicle vaccines with over-expressed factor H binding protein. PLoS Pathog. 2012;8:e1002688. doi:10.1371/journal.ppat.1002688.
   PubMed Web of Science ®Google Scholar
• Beernink PT, Ispasanie E, Lewis LA, Ram S, Moe GR, Granoff DM. A meningococcal native outer membrane vesicle vaccine with attenuated endotoxin and overexpressed Factor H binding protein elicits gonococcal bactericidal antibodies. J Infect Dis. 2019;219:1130–37. doi:10.1093/infdis/jiy609.
   PubMed Web of Science ®Google Scholar
• Beernink PT, Vianzon V, Lewis LA, Moe GR, Granoff DM. A meningococcal outer membrane vesicle vaccine with overexpressed mutant FHbp elicits higher protective antibody responses in infant rhesus macaques than a licensed serogroup B vaccine. mBio. 2019;10:e01231–19. doi:10.1128/mBio.01231-19.
   PubMed Web of Science ®Google Scholar
• Beernink PT, Shaughnessy J, Ram S, Granoff DM. Impaired immunogenicity of a meningococcal factor H-binding protein vaccine engineered to eliminate factor H binding. Clin Vaccine Immunol. 2010;17:1074–78. doi:10.1128/CVI.00103-10.
   PubMed Web of Science ®Google Scholar
• Rossi R, Granoff DM, Beernink PT. Meningococcal factor H-binding protein vaccines with decreased binding to human complement factor H have enhanced immunogenicity in human factor H transgenic mice. Vaccine. 2013;31:5451–57. doi:10.1016/j.vaccine.2013.08.099.
   PubMed Web of Science ®Google Scholar
• van der Veen S, Johnson S, Jongerius I, Malik T, Genovese A, Santini L, Staunton D, Ufret-Vincenty RL, Pickering MC, Lea SM, et al. Nonfunctional variant 3 factor H binding proteins as meningococcal vaccine candidates. Infect Immun. 2014;82:1157–63. doi:10.1128/IAI.01183-13.
   PubMed Web of Science ®Google Scholar
• Konar M, Rossi R, Walter H, Pajon R, Beernink PT. A mutant library approach to identify improved meningococcal Factor H binding protein vaccine antigens. PLoS One. 2015;10:e0128185. doi:10.1371/journal.pone.0128185.
   PubMed Web of Science ®Google Scholar
• Rossi R, Konar M, Beernink PT. Meningococcal Factor H binding protein vaccine antigens with increased thermal stability and decreased binding of human Factor H. Infect Immun. 2016;84:1735–42. doi:10.1128/IAI.01491-15.
   PubMed Web of Science ®Google Scholar
• Wang X, Cohn A, Comanducci M, Andrew L, Zhao X, MacNeil JR, Schmink S, Muzzi A, Bambini S, Rappuoli R, et al. Prevalence and genetic diversity of candidate vaccine antigens among invasive Neisseria meningitidis isolates in the United States. Vaccine. 2011;29:4739–44. doi:10.1016/j.vaccine.2011.04.092.
   PubMed Web of Science ®Google Scholar
• Murphy E, Andrew L, Lee KL, Dilts DA, Nunez L, Fink PS, Ambrose K, Borrow R, Findlow J, Taha M-K, 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;200:379–89. doi:10.1086/600141.
   PubMed Web of Science ®Google Scholar
• Beernink PT, Welsch JA, Bar-Lev M, Koeberling O, Comanducci M, Granoff DM. Fine antigenic specificity and cooperative bactericidal activity of monoclonal antibodies directed at the meningococcal vaccine candidate factor H-binding protein. Infect Immun. 2008;76:4232–40. doi:10.1128/IAI.00367-08.
   PubMed Web of Science ®Google Scholar
• Beernink PT, Giuntini S, Costa I, Lucas AH, Granoff DM. Functional analysis of the human antibody response to meningococcal Factor H binding protein. mBio. 2015;6:e00842–15. doi:10.1128/mBio.00842-15.
   PubMed Web of Science ®Google Scholar
• Giuntini S, Beernink PT, Reason DC, Granoff DM. Monoclonal antibodies to meningococcal factor H binding protein with overlapping epitopes and discordant functional activity. PLoS One. 2012;7:e34272. doi:10.1371/journal.pone.0034272.
   PubMed Web of Science ®Google Scholar
• Lo Passo C, Zippilli L, Angiolillo A, Costa I, Pernice I, Galbo R, Felici F, Beernink PT. Molecular characterization of two sub-family specific monoclonal antibodies to meningococcal Factor H binding protein. Heliyon. 2018;4:e00591. doi:10.1016/j.heliyon.2018.e00591.
   PubMed Web of Science ®Google Scholar
• Madico G, Welsch JA, Lewis LA, McNaughton A, Perlman DH, Costello CE, Ngampasutadol J, Vogel U, Granoff DM, Ram S. The meningococcal vaccine candidate GNA1870 binds the complement regulatory protein factor H and enhances serum resistance. J Immunol. 2006;177:501–10. doi:10.4049/jimmunol.177.1.501.
   PubMed Web of Science ®Google Scholar
• Vu DM, Shaughnessy J, Lewis LA, Ram S, Rice PA, Granoff DM. Enhanced bacteremia in human factor H transgenic rats infected by Neisseria meningitidis. Infect Immun. 2012;80:643–50. doi:10.1128/IAI.05604-11.
   PubMed Web of Science ®Google Scholar
• Welsch JA, Factor RS. H and neisserial pathogenesis. Vaccine. 2008;26(Suppl 8):I40–5. doi:10.1016/j.vaccine.2008.11.060.
   PubMedGoogle Scholar
• Giuntini S, Reason DC, Granoff DM. Complement-mediated bactericidal activity of anti-factor H binding protein monoclonal antibodies against the meningococcus relies upon blocking factor H binding. Infect Immun. 2011;79:3751–59. doi:10.1128/IAI.05182-11.
   PubMed Web of Science ®Google Scholar
• Giuntini S, Reason DC, Granoff DM. 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;80:187–94. doi:10.1128/IAI.05956-11.
   PubMed Web of Science ®Google Scholar
• Malito E, Faleri A, Lo Surdo P, Veggi D, Maruggi G, Grassi E, Cartocci E, Bertoldi I, Genovese A, Santini L, et al. Defining a protective epitope on factor H binding protein, a key meningococcal virulence factor and vaccine antigen. Proc Natl Acad Sci USA. 2013;110:3304–09. doi:10.1073/pnas.1222845110.
   PubMed Web of Science ®Google Scholar
• Welsch JA, Rossi R, Comanducci M, Granoff DM. Protective activity of monoclonal antibodies to genome-derived neisserial antigen 1870, a Neisseria meningitidis candidate vaccine. J Immunol. 2004;172:5606–15. doi:10.4049/jimmunol.172.9.5606.
   PubMed Web of Science ®Google Scholar
• Malito E, Lo Surdo P, Veggi D, Santini L, Stefek H, Brunelli B, Luzzi E, Bottomley MJ, Beernink PT, Scarselli M. Neisseria meningitidis factor H-binding protein bound to monoclonal antibody JAR5: implications for antibody synergy. Biochem J. 2016;473:4699–713. doi:10.1042/BCJ20160806.
   PubMed Web of Science ®Google Scholar
• Scarselli M, Cantini F, Santini L, Veggi D, Dragonetti S, Donati C, Savino S, Giuliani MM, Comanducci M, Di Marcello F, et al. Epitope mapping of a bactericidal monoclonal antibody against the factor H binding protein of Neisseria meningitidis. J Mol Biol. 2009;386:97–108. doi:10.1016/j.jmb.2008.12.005.
   PubMed Web of Science ®Google Scholar
• Beernink PT, LoPasso C, Angiolillo A, Felici F, Granoff D. A region of the N-terminal domain of meningococcal factor H-binding protein that elicits bactericidal antibody across antigenic variant groups. Mol Immunol. 2009;46:1647–53. doi:10.1016/j.molimm.2009.02.021.
   PubMed Web of Science ®Google Scholar
• Vu DM, Pajon R, Reason DC, Granoff DM. A broadly cross-reactive monoclonal antibody against an epitope on the N-terminus of meningococcal fHbp. Sci Rep. 2012;2:341. doi:10.1038/srep00386.
   PubMed Web of Science ®Google Scholar
• Lopez-Sagaseta J, Beernink PT, Bianchi F, Santini L, Frigimelica E, Lucas AH, Pizza M, Bottomley MJ. Crystal structure reveals vaccine elicited bactericidal human antibody targeting a conserved epitope on meningococcal fHbp. Nat Commun. 2018;9:528. doi:10.1038/s41467-018-02827-7.
   PubMed Web of Science ®Google Scholar
• Giuliani M, Bartolini E, Galli B, Santini L, Lo Surdo P, Buricchi F, Bruttini M, Benucci B, Pacchiani N, Alleri L, et al. Human protective response induced by meningococcus B vaccine is mediated by the synergy of multiple bactericidal epitopes. Sci Rep. 2018;8:3700. doi:10.1038/s41598-018-22057-7.
   PubMed Web of Science ®Google Scholar
• Peschiera I, Giuliani M, Giusti F, Melero R, Paccagnini E, Donnarumma D, Pansegrau W, Carazo JM, Sorzano CO, Scarselli M, Masignani V. Structural basis for cooperativity of human monoclonal antibodies to meningococcal factor H binding protein. Comms Bio. 2019;2:241. doi:10.1038/s42003-019-0493-4.
   PubMed Web of Science ®Google Scholar
• Duncan AR, Winter G. The binding site for C1q on IgG. Nature. 1988;332:738–40. doi:10.1038/332738a0.
   PubMed Web of Science ®Google Scholar
• Biagini M, Spinsanti M, De Angelis G, Tomei S, Ferlenghi I, Scarselli M, Rigat F, Messuti N, Biolchi A, Muzzi A, et al. Expression of factor H binding protein in meningococcal strains can vary at least 15-fold and is genetically determined. Proc Natl Acad Sci USA. 2016;113:2714–19. doi:10.1073/pnas.1521142113.
   PubMed Web of Science ®Google Scholar
• Welsch JA, Ram S, Koeberling O, Granoff DM. Complement-dependent synergistic bactericidal activity of antibodies against factor H-binding protein, a sparsely distributed meningococcal vaccine antigen. J Infect Dis. 2008;197:1053–61. doi:10.1086/528994.
   PubMed Web of Science ®Google Scholar
• Vu DM, Wong TT, Granoff DM. Cooperative serum bactericidal activity between human antibodies to meningococcal factor H binding protein and Neisserial heparin binding antigen. Vaccine. 2011;29:1968–73. doi:10.1016/j.vaccine.2010.12.075.
   PubMed Web of Science ®Google Scholar
• Welsch JA, Granoff D. Immunity to Neisseria meningitidis group B in adults despite lack of serum bactericidal antibody. Clin Vaccine Immunol. 2007;14:1596–602. doi:10.1128/CVI.00341-07.
   PubMed Web of Science ®Google Scholar
• Plested JS, Granoff DM. Vaccine-induced opsonophagocytic immunity to Neisseria meningitidis group B. Clin Vaccine Immunol. 2008;15:799–804. doi:10.1128/CVI.00036-08.
   PubMed Web of Science ®Google Scholar
• Plested JS, Welsch JA, Granoff DM. Ex vivo model of meningococcal bacteremia using human blood for measuring vaccine-induced serum passive protective activity. Clin Vaccine Immunol. 2009;16:785–91. doi:10.1128/CVI.00007-09.
   PubMed Web of Science ®Google Scholar
• Read RC, Dull P, Bai X, Nolan K, Findlow J, Bazaz R, Kleinschmidt A, McCarthy M, Wang H, Toneatto D, et al. A phase III observer-blind randomized, controlled study to evaluate the immune response and the correlation with nasopharyngeal carriage after immunization of university students with a quadrivalent meningococcal ACWY glycoconjugate or serogroup B meningococcal vaccine. Vaccine. 2017;35:427–34. doi:10.1016/j.vaccine.2016.11.071.
   PubMed Web of Science ®Google Scholar
• Saez-Llorens X, Beltran-Rodriguez J, Novoa Pizarro JM, Mensi I, Keshavan P, Toneatto D. Four-year antibody persistence and response to a booster dose of a pentavalent MenABCWY vaccine administered to healthy adolescents and young adults. Hum Vaccin Immunother. 2018;14:1161–74. doi:10.1080/21645515.2018.1457595.
   PubMed Web of Science ®Google Scholar