{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,15]],"date-time":"2026-05-15T14:13:29Z","timestamp":1778854409236,"version":"3.51.4"},"reference-count":84,"publisher":"MDPI AG","issue":"7","license":[{"start":{"date-parts":[[2021,7,18]],"date-time":"2021-07-18T00:00:00Z","timestamp":1626566400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000024","name":"Canadian Institutes of Health Research","doi-asserted-by":"publisher","award":["MOP-130273"],"award-info":[{"award-number":["MOP-130273"]}],"id":[{"id":"10.13039\/501100000024","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000024","name":"Canadian Institutes of Health Research","doi-asserted-by":"publisher","award":["GSD-16701"],"award-info":[{"award-number":["GSD-16701"]}],"id":[{"id":"10.13039\/501100000024","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>Neisseria meningitidis causes a devastating invasive disease but is also a normal colonizer of the human nasopharynx. Due to the rapid progression of disease, the best tool to protect individuals against meningococcal infections is immunization. Clinical experience with polysaccharide conjugate vaccines has revealed that an ideal meningococcal vaccine must prevent both invasive disease and nasal colonization, which confers herd immunity. However, not all meningococcal vaccines are equal in their ability to prevent nasal colonization, for unknown reasons. Herein, we describe recent efforts to utilize humanized mouse models to understand the impact of different meningococcal vaccines on nasal colonization. These mice are susceptible to nasal colonization, and they become immune following live nasal infection or immunization with matched capsule-conjugate or protein-based vaccines, replicating findings from human work. We bring together insights regarding meningococcal colonization and immunity from clinical work with findings using humanized mouse models, providing new perspective into the different determinants of mucosal versus systemic immunity. Then, we use this as a framework to help focus future studies toward understanding key mechanistic aspects left unresolved, including the bacterial factors required for colonization and immune evasion, determinants of nasal mucosal protection, and characteristics of an ideal meningococcal vaccine.<\/jats:p>","DOI":"10.3390\/pathogens10070906","type":"journal-article","created":{"date-parts":[[2021,7,18]],"date-time":"2021-07-18T21:18:52Z","timestamp":1626643132000},"page":"906","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":6,"title":["Exploring the Ability of Meningococcal Vaccines to Elicit Mucosal Immunity: Insights from Humans and Mice"],"prefix":"10.3390","volume":"10","author":[{"given":"Elissa G.","family":"Currie","sequence":"first","affiliation":[{"name":"Department of Molecular Genetics, Temerty Faculty of Medicine, University of Toronto, Toronto, ON M5S 1A8, Canada"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1477-3616","authenticated-orcid":false,"given":"Scott D.","family":"Gray-Owen","sequence":"additional","affiliation":[{"name":"Department of Molecular Genetics, Temerty Faculty of Medicine, University of Toronto, Toronto, ON M5S 1A8, Canada"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2021,7,18]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1118","DOI":"10.1080\/21645515.2018.1454570","article-title":"Impact of meningococcal vaccination on carriage and disease transmission: A review of the literature","volume":"14","author":"Balmer","year":"2018","journal-title":"Hum. Vaccines Immunother."},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Campbell, H., Parikh, S.R., Borrow, R., Kaczmarski, E., Ramsay, M.E., and Ladhani, S.N. (2016). Presentation with gastrointestinal symptoms and high case fatality associated with group W meningococcal disease (MenW) in teenagers, England, July 2015 to January 2016. Eurosurveillance, 21.","DOI":"10.2807\/1560-7917.ES.2016.21.12.30175"},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Stinson, C., Burman, C., Presa, J., and Abalos, M. (2020). Atypical presentation of invasive meningococcal disease caused by serogroup W meningococci. Epidemiol. Infect., 148.","DOI":"10.1017\/S0950268819002152"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1146","DOI":"10.1080\/21645515.2018.1451810","article-title":"Progress toward the global control of Neisseria meningitidis: 21st century vaccines, current guidelines, and challenges for future vaccine development","volume":"14","author":"Dretler","year":"2018","journal-title":"Hum. Vaccines Immunother."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"B3","DOI":"10.1016\/j.vaccine.2011.12.062","article-title":"Meningococcal disease: Clinical presentation and sequelae","volume":"30","author":"Pace","year":"2011","journal-title":"Vaccine"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"421","DOI":"10.1007\/s40121-018-0213-2","article-title":"Systematic Review of invasive meningococcal disease: Sequelae and quality of life impact on patients and their caregivers","volume":"7","author":"Olbrich","year":"2018","journal-title":"Infect. Dis. Ther."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1829","DOI":"10.1016\/S0140-6736(02)08679-8","article-title":"Carriage of serogroup C meningococci 1 year after meningococcal C conjugate polysaccharide vaccination","volume":"359","author":"Maiden","year":"2002","journal-title":"Lancet"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"737","DOI":"10.1086\/527401","article-title":"Impact of meningococcal serogroup C conjugate vaccines on carriage and herd immunity","volume":"197","author":"Maiden","year":"2008","journal-title":"J. Infect. Dis."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1136\/bmj.326.7385.365","article-title":"Herd immunity from meningococcal serogroup C conjugate vaccination in England: Database analysis","volume":"326","author":"Ramsay","year":"2003","journal-title":"Br. Med. J."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"757","DOI":"10.1016\/S1473-3099(12)70168-8","article-title":"Serogroup A meningococcal conjugate vaccination in Burkina Faso: Analysis of national surveillance data","volume":"12","author":"Novak","year":"2012","journal-title":"Lancet Infect. Dis."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Collard, J.-M., Issaka, B., Zaneidou, M., Hugonnet, S., Nicolas, P., Taha, M.-K., Greenwood, B., and Jusot, J.-F. (2013). Epidemiological changes in meningococcal meningitis in Niger from 2008 to 2011 and the impact of vaccination. BMC Infect. Dis., 13.","DOI":"10.1186\/1471-2334-13-576"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"354","DOI":"10.1093\/cid\/cis892","article-title":"Impact of the serogroup A meningococcal conjugate vaccine, MenAfriVac, on carriage and herd immunity","volume":"56","author":"Kristiansen","year":"2012","journal-title":"Clin. Infect. Dis."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"663","DOI":"10.1186\/s12879-014-0663-4","article-title":"Persistent low carriage of serogroup A Neisseria meningitidis two years after mass vaccination with the meningococcal conjugate vaccine, MenAfriVac","volume":"14","author":"Kristiansen","year":"2014","journal-title":"BMC Infect. Dis."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1098","DOI":"10.1080\/21645515.2017.1378841","article-title":"Successful African introduction of a new Group A meningococcal conjugate vaccine: Future challenges and next steps","volume":"14","author":"LaForce","year":"2018","journal-title":"Hum. Vaccines Immunother."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1080\/14760584.2017.1258308","article-title":"The Global Meningococcal Initiative: Global epidemiology, the impact of vaccines on meningococcal disease and the importance of herd protection","volume":"16","author":"Borrow","year":"2017","journal-title":"Expert Rev. Vaccines"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"911","DOI":"10.1093\/cid\/cir007","article-title":"\u201cHerd Immunity\u201d: A Rough Guide","volume":"52","author":"Fine","year":"2011","journal-title":"Clin. Infect. Dis."},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Johswich, K.O., McCaw, S.E., Islam, E., Sintsova, A., Gu, A., Shively, J.E., and Gray-Owen, S.D. (2013). In vivo adaptation and persistence of Neisseria meningitidis within the nasopharyngeal mucosa. PLoS Pathog., 9.","DOI":"10.1371\/journal.ppat.1003509"},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Johswich, K.O., and Gray-Owen, S.D. (2019). Modeling Neisseria meningitidis Infection in Mice: Methods and Logistical Considerations for Nasal Colonization and Invasive Disease, Humana Press Inc.","DOI":"10.1007\/978-1-4939-9202-7_11"},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Gu, A., Zhang, Z., Zhang, N., Tsark, W., and Shively, J.E. (2010). Generation of human CEACAM1 transgenic mice and binding of Neisseria Opa protein to their neutrophils. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0010067"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"354","DOI":"10.1128\/IAI.02495-14","article-title":"Sterilizing Immunity Elicited by Neisseria meningitidis carriage shows broader protection than predicted by serum antibody cross-reactivity in CEACAM1-humanized mice","volume":"83","author":"Johswich","year":"2015","journal-title":"Infect. Immun."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1590","DOI":"10.1093\/infdis\/jix162","article-title":"Discordant effects of licensed meningococcal serogroup B vaccination on invasive disease and nasal colonization in a humanized mouse model","volume":"215","author":"Buckwalter","year":"2017","journal-title":"J. Infect. Dis."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"911","DOI":"10.1084\/jem.179.3.911","article-title":"Multiple gonococcal opacity proteins are expressed during experimental urethral infection in the male","volume":"179","author":"Jerse","year":"1994","journal-title":"J. Exp. Med."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Mustapha, M.M., Marsh, J.W., Shutt, K.A., Schlackman, J., Ezeonwuka, C., Farley, M.M., Stephens, D.S., Wang, X., Van Tyne, D., and Harrison, L.H. (2020). Transmission dynamics and microevolution of Neisseria meningitidis during carriage and invasive disease in high school students in Georgia and Maryland, 2006\u20132007. J. Infect. Dis.","DOI":"10.1093\/infdis\/jiaa674"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1080\/14760584.2019.1557520","article-title":"The Global Meningococcal Initiative meeting on prevention of meningococcal disease worldwide: Epidemiology, surveillance, hypervirulent strains, antibiotic resistance and high-risk populations","volume":"18","author":"Acevedo","year":"2019","journal-title":"Expert Rev. Vaccines"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1307","DOI":"10.1084\/jem.129.6.1307","article-title":"Human immunity to the meningococcus. I. The role of humoral antibodies","volume":"129","author":"Goldschneider","year":"1969","journal-title":"J. Exp. Med."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"4414","DOI":"10.1016\/j.vaccine.2015.07.019","article-title":"Serum bactericidal antibody assays\u2014The role of complement in infection and immunity","volume":"33","author":"McIntosh","year":"2015","journal-title":"Vaccine"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1327","DOI":"10.1084\/jem.129.6.1327","article-title":"Human immunity to the meningococcus. II. Development of natural immunity","volume":"129","author":"Goldschneider","year":"1969","journal-title":"J. Exp. Med."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"S58","DOI":"10.1016\/S0264-410X(01)00299-7","article-title":"Planning, registration, and implementation of an immunisation campaign against meningococcal serogroup C disease in the UK: A success story","volume":"20","author":"Miller","year":"2001","journal-title":"Vaccine"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"B112","DOI":"10.1016\/j.vaccine.2009.04.065","article-title":"Bactericidal antibody is the immunologic surrogate of protection against meningococcal disease","volume":"27","author":"Frasch","year":"2009","journal-title":"Vaccine"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"5093","DOI":"10.1016\/j.vaccine.2006.03.091","article-title":"Neisseria meningitidis group B correlates of protection and assay standardization\u2014International Meeting Report Emory University, Atlanta, Georgia, United States, 16\u201317 March 2005","volume":"24","author":"Borrow","year":"2006","journal-title":"Vaccine"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"853","DOI":"10.1016\/S1473-3099(10)70251-6","article-title":"Meningococcal carriage by age: A systematic review and meta-analysis","volume":"10","author":"Christensen","year":"2010","journal-title":"Lancet Infect. Dis."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1327","DOI":"10.1016\/S0264-410X(00)00333-9","article-title":"Development of natural immunity to Neisseria meningitidis","volume":"19","author":"Pollard","year":"2001","journal-title":"Vaccine"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1301","DOI":"10.1128\/IAI.70.3.1301-1309.2002","article-title":"Characterization of humoral and cellular immune responses elicited by meningococcal carriage","volume":"70","author":"Robinson","year":"2002","journal-title":"Infect. Immun."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"883","DOI":"10.1017\/S0950268805004097","article-title":"Influence of age and carriage status on salivary IgA to Neisseria meningitidis","volume":"133","author":"Horton","year":"2005","journal-title":"Epidemiol. Infect."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"4263","DOI":"10.4049\/jimmunol.171.8.4263","article-title":"Evidence for naturally acquired T cell-mediated mucosal immunity to Neisseria meningitidis","volume":"171","author":"Davenport","year":"2003","journal-title":"J. Immunol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"2231","DOI":"10.4049\/jimmunol.0802531","article-title":"Absence of Mucosal immunity in the human upper respiratory tract to the commensal bacteria Neisseria lactamica but not pathogenic Neisseria meningitidis during the peak age of nasopharyngeal carriage","volume":"182","author":"Vaughan","year":"2009","journal-title":"J. Immunol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"S3","DOI":"10.1016\/j.jadohealth.2016.04.012","article-title":"The global evolution of meningococcal epidemiology following the introduction of meningococcal vaccines","volume":"59","author":"Pelton","year":"2016","journal-title":"J. Adolesc. Health"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"308","DOI":"10.1038\/nrd3012","article-title":"Carbohydrate vaccines: Developing sweet solutions to sticky situations?","volume":"9","author":"Astronomo","year":"2010","journal-title":"Nat. Rev. Drug Discov."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1073\/pnas.1819612116","article-title":"On the mechanisms of conjugate vaccines","volume":"116","author":"Rappuoli","year":"2019","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1073\/pnas.1816401115","article-title":"Polysaccharide structure dictates mechanism of adaptive immune response to glycoconjugate vaccines","volume":"116","author":"Sun","year":"2019","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1216","DOI":"10.1093\/cid\/ciu601","article-title":"A decade of herd protection after introduction of meningococcal serogroup C conjugate vaccination","volume":"59","author":"Bijlsma","year":"2014","journal-title":"Clin. Infect. Dis."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"B117","DOI":"10.1016\/j.vaccine.2009.04.066","article-title":"Relative importance of complement-mediated bactericidal and opsonic activity for protection against meningococcal disease","volume":"27","author":"Granoff","year":"2009","journal-title":"Vaccine"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"799","DOI":"10.1128\/CVI.00036-08","article-title":"Vaccine-induced opsonophagocytic immunity to Neisseria meningitidis group B","volume":"15","author":"Plested","year":"2008","journal-title":"Clin. Vaccine Immunol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"176","DOI":"10.1038\/mi.2014.55","article-title":"Antibody blocks acquisition of bacterial colonization through agglutination","volume":"8","author":"Roche","year":"2015","journal-title":"Mucosal Immunol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1038\/mi.2016.71","article-title":"Agglutination by anti-capsular polysaccharide antibody is associated with protection against experimental human pneumococcal carriage","volume":"10","author":"Mitsi","year":"2017","journal-title":"Mucosal Immunol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"103571","DOI":"10.1016\/j.micpath.2019.103571","article-title":"Global estimate of Neisseria meningitidis serogroups proportion in invasive meningococcal disease: A systematic review and meta-analysis","volume":"134","author":"Purmohamad","year":"2019","journal-title":"Microb. Pathog."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1393","DOI":"10.1080\/14760584.2016.1187068","article-title":"Fighting Neisseria meningitidis: Past and current vaccination strategies","volume":"15","author":"Piccini","year":"2016","journal-title":"Expert Rev. Vaccines"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"305","DOI":"10.1179\/2047773214Y.0000000162","article-title":"Bexsero\u00ae chronicle","volume":"108","author":"Vernikos","year":"2014","journal-title":"Pathog. Glob. Health"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"875","DOI":"10.1016\/j.vaccine.2015.11.057","article-title":"Clinical experience with the meningococcal B vaccine, Bexsero\u00ae: Prospects for reducing the burden of meningococcal serogroup B disease","volume":"34","author":"Watson","year":"2016","journal-title":"Vaccine"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1080\/14760584.2018.1483726","article-title":"From research to licensure and beyond: Clinical development of MenB-FHbp, a broadly protective meningococcal B vaccine","volume":"17","author":"Perez","year":"2018","journal-title":"Expert Rev. Vaccines"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"1816","DOI":"10.1126\/science.287.5459.1816","article-title":"Identification of vaccine candidates against serogroup B meningococcus by whole-genome sequencing","volume":"287","author":"Pizza","year":"2000","journal-title":"Science"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1007\/s40121-016-0107-0","article-title":"Meningococcal vaccinations","volume":"5","author":"Sullivan","year":"2016","journal-title":"Infect. Dis. Ther."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"19490","DOI":"10.1073\/pnas.1013758107","article-title":"Qualitative and quantitative assessment of meningococcal antigens to evaluate the potential strain coverage of protein-based vaccines","volume":"107","author":"Donnelly","year":"2010","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"124","DOI":"10.1016\/j.vaccine.2013.03.063","article-title":"Diversity of Canadian meningococcal serogroup B isolates and estimated coverage by an investigational meningococcal serogroup B vaccine (4CMenB)","volume":"32","author":"Bettinger","year":"2013","journal-title":"Vaccine"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"4968","DOI":"10.1016\/j.vaccine.2013.08.006","article-title":"Bactericidal antibody against a representative epidemiological meningococcal serogroup B panel confirms that MATS underestimates 4CMenB vaccine strain coverage","volume":"31","author":"Frosi","year":"2013","journal-title":"Vaccine"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"725","DOI":"10.1080\/21645515.2018.1537756","article-title":"Evaluation of strain coverage of the multicomponent meningococcal serogroup B vaccine (4CMenB) administered in infants according to different immunisation schedules","volume":"15","author":"Biolchi","year":"2019","journal-title":"Hum. Vaccines Immunother."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1186\/s12866-015-0469-6","article-title":"Characterization of invasive Neisseria meningitidis strains from Qu\u00e9bec, Canada, during a period of increased serogroup B disease, 2009-2013: Phenotyping and genotyping with special emphasis on the non-carbohydrate protein vaccine targets","volume":"15","author":"Law","year":"2015","journal-title":"BMC Microbiol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"427","DOI":"10.1016\/j.vaccine.2016.11.071","article-title":"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 meningo","volume":"35","author":"Read","year":"2017","journal-title":"Vaccine"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"4243","DOI":"10.1016\/j.vaccine.2019.06.021","article-title":"Impact of a mass vaccination campaign against Serogroup B meningococcal disease in the Saguenay-Lac-Saint-Jean region of Quebec four years after its launch","volume":"37","author":"Deceuninck","year":"2019","journal-title":"Vaccine"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"318","DOI":"10.1056\/NEJMoa1900236","article-title":"Meningococcal B vaccine and meningococcal carriage in adolescents in Australia","volume":"382","author":"Marshall","year":"2020","journal-title":"N. Engl. J. Med."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"e020988","DOI":"10.1136\/bmjopen-2017-020988","article-title":"B Part of It protocol: A cluster randomised controlled trial to assess the impact of 4CMenB vaccine on pharyngeal carriage of Neisseria meningitidis in adolescents","volume":"8","author":"Marshall","year":"2018","journal-title":"BMJ Open"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"B87","DOI":"10.1016\/j.vaccine.2012.01.033","article-title":"The new multicomponent vaccine against meningococcal serogroup B, 4CMenB: Immunological, functional and structural characterization of the antigens","volume":"30","author":"Serruto","year":"2012","journal-title":"Vaccine"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"501","DOI":"10.4049\/jimmunol.177.1.501","article-title":"The meningococcal vaccine candidate GNA1870 binds the complement regulatory protein factor H and enhances serum resistance","volume":"177","author":"Madico","year":"2006","journal-title":"J. Immunol."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"3751","DOI":"10.1128\/IAI.05182-11","article-title":"Complement-mediated bactericidal activity of anti-factor H binding protein monoclonal antibodies against the meningococcus relies upon blocking factor H binding","volume":"79","author":"Giuntini","year":"2011","journal-title":"Infect. Immun."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1128\/IAI.05956-11","article-title":"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","volume":"80","author":"Giuntini","year":"2012","journal-title":"Infect. Immun."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"452","DOI":"10.1128\/IAI.01267-15","article-title":"Impaired immunogenicity of meningococcal neisserial surface protein A in human complement factor H transgenic mice","volume":"84","author":"Lujan","year":"2015","journal-title":"Infect. Immun."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"3606","DOI":"10.4049\/jimmunol.1003470","article-title":"A meningococcal factor H binding protein mutant that eliminates factor H binding enhances protective antibody responses to vaccination","volume":"186","author":"Beernink","year":"2011","journal-title":"J. Immunol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"e88907","DOI":"10.1172\/jci.insight.88907","article-title":"Enhanced protective antibody to a mutant meningococcal factor H-binding protein with low-factor H binding","volume":"1","author":"Granoff","year":"2016","journal-title":"JCI Insight"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"e01231-19","DOI":"10.1128\/mBio.01231-19","article-title":"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","volume":"10","author":"Beernink","year":"2019","journal-title":"mBio"},{"key":"ref_70","doi-asserted-by":"crossref","unstructured":"Frandoloso, R., Martinez-Martinez, S., Calmettes, C., Fegan, J., Costa, E., Curran, D., Yu, R.H., Gutierrez-Martin, C.B., Rodriguez Ferri, E.F., and Moraes, T.F. (2014). Nonbinding site-directed mutants of transferrin binding protein B enhances their immunogenicity and protective capabilities. Infect. Immun.","DOI":"10.1128\/IAI.02572-14"},{"key":"ref_71","doi-asserted-by":"crossref","unstructured":"Szatanik, M., Hong, E., Ruckly, C., Ledroit, M., Giorgini, D., Jopek, K., Nicola, M.A., Deghmane, A.E., and Taha, M.K. (2011). Experimental meningococcal sepsis in congenic transgenic mice expressing human transferrin. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0022210"},{"key":"ref_72","doi-asserted-by":"crossref","unstructured":"Eriksson, L., Stenmark, B., Deghmane, A.E., Thulin Hedberg, S., Sall, O., Fredlund, H., Molling, P., and Taha, M.K. (2020). Difference in virulence between Neisseria meningitidis serogroups W and Y in transgenic mice. BMC Microbiol., 20.","DOI":"10.1186\/s12866-020-01760-4"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"950","DOI":"10.3201\/eid1206.051297","article-title":"Social behavior and meningococcal carriage in British teenagers","volume":"12","author":"MacLennan","year":"2006","journal-title":"Emerg. Infect. Dis."},{"key":"ref_74","doi-asserted-by":"crossref","unstructured":"Woringer, M., Martiny, N., Porgho, S., Bicaba, B.W., Bar-Hen, A., and Mueller, J.E. (2018). Atmospheric dust, early cases, and localized meningitis epidemics in the african meningitis belt: An analysis using high spatial resolution data. Environ. Health Perspect., 126.","DOI":"10.1289\/EHP2752"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1016\/j.ijid.2008.05.1223","article-title":"Meningococcal meningitis in Mali: A long-term study of persistence and spread","volume":"13","author":"Philippon","year":"2009","journal-title":"Int. J. Infect. Dis."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1016\/S0378-1097(03)00252-0","article-title":"A model of meningococcal bacteremia after respiratory superinfection in influenza A virus-infected mice","volume":"222","author":"Alonso","year":"2003","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"4848","DOI":"10.1073\/pnas.0501254102","article-title":"CD4+ T cells mediate antibody-independent acquired immunity to pneumococcal colonization","volume":"102","author":"Malley","year":"2005","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_78","doi-asserted-by":"crossref","unstructured":"Lu, Y.-J., Gross, J., Bogaert, D., Finn, A., Bagrade, L., Zhang, Q., Kolls, J.K., Srivastava, A., Lundgren, A., and Forte, S. (2008). Interleukin-17A mediates acquired immunity to pneumococcal colonization. PLoS Pathog., 4.","DOI":"10.1371\/journal.ppat.1000159"},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"627","DOI":"10.1038\/mi.2014.95","article-title":"Protection against Streptococcus pneumoniae lung infection after nasopharyngeal colonization requires both humoral and cellular immune responses","volume":"8","author":"Wilson","year":"2015","journal-title":"Mucosal Immunol."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"358","DOI":"10.3389\/fimmu.2019.00358","article-title":"Mechanisms of naturally acquired immunity to Streptococcus pneumoniae","volume":"10","author":"Ercoli","year":"2019","journal-title":"Front. Immunol."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1080\/22221751.2018.1564630","article-title":"Immunization with whole cell but not acellular pertussis vaccines primes CD4 TRM cells that sustain protective immunity against nasal colonization with Bordetella pertussis","volume":"8","author":"Wilk","year":"2019","journal-title":"Emerg. Microbes Infect."},{"key":"ref_82","doi-asserted-by":"crossref","unstructured":"Chasaide, C.N., and Mills, K.H.G. (2020). Next-generation pertussis vaccines based on the induction of protective T cells in the rRespiratory tract. Vaccines, 8.","DOI":"10.3390\/vaccines8040621"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"1753","DOI":"10.1038\/s41385-018-0073-9","article-title":"IL-17-dependent SIgA-mediated protection against nasal Bordetella pertussis infection by live attenuated BPZE1 vaccine","volume":"11","author":"Solans","year":"2018","journal-title":"Mucosal Immunol."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"2187","DOI":"10.1128\/IAI.74.4.2187-2195.2006","article-title":"Antibody-independent, interleukin-17A-mediated, cross-serotype immunity to pneumococci in mice immunized intranasally with the cell wall polysaccharide","volume":"74","author":"Malley","year":"2006","journal-title":"Infect. Immun."}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/10\/7\/906\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T06:31:27Z","timestamp":1760164287000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/10\/7\/906"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,7,18]]},"references-count":84,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2021,7]]}},"alternative-id":["pathogens10070906"],"URL":"https:\/\/doi.org\/10.3390\/pathogens10070906","relation":{},"ISSN":["2076-0817"],"issn-type":[{"value":"2076-0817","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,7,18]]}}}