The Bordetella pertussis type III secretion system tip complex protein Bsp22 is not a protective antigen and fails to elicit serum antibody responses during infection of humans and mice
Language English Country United States Media print-electronic
Document type Journal Article, Research Support, Non-U.S. Gov't
PubMed
23690400
PubMed Central
PMC3719584
DOI
10.1128/iai.00353-13
PII: IAI.00353-13
Knihovny.cz E-resources
- MeSH
- Antigens, Bacterial immunology MeSH
- Bacterial Proteins immunology MeSH
- Bordetella pertussis immunology MeSH
- Enzyme-Linked Immunosorbent Assay MeSH
- Bordetella Infections immunology MeSH
- Humans MeSH
- Mice, Inbred BALB C MeSH
- Mice MeSH
- Whooping Cough immunology MeSH
- Antibodies, Bacterial blood immunology MeSH
- Antibody Formation immunology MeSH
- Animals MeSH
- Check Tag
- Humans MeSH
- Mice MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Antigens, Bacterial MeSH
- Bacterial Proteins MeSH
- Antibodies, Bacterial MeSH
The type III secretion system (T3SS) of pathogenic bordetellae employs a self-associating tip complex protein Bsp22. This protein is immunogenic during infections by Bordetella bronchiseptica and could be used as a protective antigen to immunize mice against B. bronchiseptica challenge. Since low-passage clinical isolates of the human pathogen Bordetella pertussis produce a highly homologous Bsp22 protein (97% homology), we examined its vaccine and diagnostic potential. No Bsp22-specific antibodies were, however, detected in serum samples from 36 patients with clinically and serologically confirmed whooping cough disease (pertussis syndrome). Moreover, although the induction of Bsp22 secretion by the laboratory-adapted 18323 strain in the course of mice lung infection was observed, the B. pertussis 18323-infected mice did not mount any detectable serum antibody response against Bsp22. Furthermore, immunization with recombinant Bsp22 protein yielded induction of high Bsp22-specific serum antibody titers but did not protect mice against an intranasal challenge with B. pertussis 18323. Unlike for B. bronchiseptica, hence, the Bsp22 protein is nonimmunogenic, and/or the serum antibody response to it is suppressed, during B. pertussis infections of humans and mice.
Infect Immun. 2014 Jul;82(7):3088 PubMed
See more in PubMed
Cotter PA, Miller JF. 2000. Genetic analysis of the Bordetella infectious cycle. Immunopharmacology 48:253–255 PubMed
Mattoo S, Cherry JD. 2005. Molecular pathogenesis, epidemiology, and clinical manifestations of respiratory infections due to Bordetella pertussis and other Bordetella subspecies. Clin. Microbiol. Rev. 18:326–382 PubMed PMC
Crowcroft NS, Stein C, Duclos P, Birmingham M. 2003. How best to estimate the global burden of pertussis? Lancet Infect. Dis. 3:413–418 PubMed
Cherry JD. 2010. The present and future control of pertussis. Clin. Infect. Dis. 51:663–667 PubMed
Andrews R, Herceg A, Roberts C. 1997. Pertussis notifications in Australia, 1991 to 1997. Commun. Dis. Intell. 21:145–148 PubMed
de Melker HE, Schellekens JF, Neppelenbroek SE, Mooi FR, Rumke HC, Conyn-van Spaendonck MA. 2000. Reemergence of pertussis in the highly vaccinated population of the Netherlands: observations on surveillance data. Emerg. Infect. Dis. 6:348–357 PubMed PMC
Gzyl A, Augustynowicz E, van Loo I, Slusarczyk J. 2001. Temporal nucleotide changes in pertactin and pertussis toxin genes in Bordetella pertussis strains isolated from clinical cases in Poland. Vaccine 20:299–303 PubMed
He Q, Makinen J, Berbers G, Mooi FR, Viljanen MK, Arvilommi H, Mertsola J. 2003. Bordetella pertussis protein pertactin induces type-specific antibodies: one possible explanation for the emergence of antigenic variants? J. Infect. Dis. 187:1200–1205 PubMed
Hellenbrand W, Beier D, Jensen E, Littmann M, Meyer C, Oppermann H, Wirsing von Konig CH, Reiter S. 2009. The epidemiology of pertussis in Germany: past and present. BMC Infect. Dis. 9:22.10.1186/1471-2334-9-22 PubMed DOI PMC
King AJ, Berbers G, van Oirschot HF, Hoogerhout P, Knipping K, Mooi FR. 2001. Role of the polymorphic region 1 of the Bordetella pertussis protein pertactin in immunity. Microbiology 147:2885–2895 PubMed
Raguckas SE, VandenBussche HL, Jacobs C, Klepser ME. 2007. Pertussis resurgence: diagnosis, treatment, prevention, and beyond. Pharmacotherapy 27:41–52 PubMed
Tanaka M, Vitek CR, Pascual FB, Bisgard KM, Tate JE, Murphy TV. 2003. Trends in pertussis among infants in the United States, 1980–1999. JAMA 290:2968–2975 PubMed
Witt MA, Katz PH, Witt DJ. 2012. Unexpectedly limited durability of immunity following acellular pertussis vaccination in preadolescents in a North American outbreak. Clin. Infect. Dis. 54:1730–1735 PubMed
Clark TA, Messonnier NE, Hadler SC. 2012. Pertussis control: time for something new? Trends Microbiol. 20:211–213 PubMed
Poolman JT, Hallander H, Halperin SA. 2012. Pertussis vaccines: where to now? Expert Rev. Vaccines 10:1497–1500 PubMed
Fennelly NK, Sisti F, Higgins SC, Ross PJ, van der Heide H, Mooi FR, Boyd A, Mills KH. 2008. Bordetella pertussis expresses a functional type III secretion system that subverts protective innate and adaptive immune responses. Infect. Immun. 76:1257–1266 PubMed PMC
Coburn B, Sekirov I, Finlay BB. 2007. Type III secretion systems and disease. Clin. Microbiol. Rev. 20:535–549 PubMed PMC
Galan JE, Wolf-Watz H. 2006. Protein delivery into eukaryotic cells by type III secretion machines. Nature 444:567–573 PubMed
Ghosh P. 2004. Process of protein transport by the type III secretion system. Microbiol. Mol. Biol. Rev. 68:771–795 PubMed PMC
Shrivastava R, Miller JF. 2009. Virulence factor secretion and translocation by Bordetella species. Curr. Opin. Microbiol. 12:88–93 PubMed PMC
Kozak NA, Mattoo S, Foreman-Wykert AK, Whitelegge JP, Miller JF. 2005. Interactions between partner switcher orthologs BtrW and BtrV regulate type III secretion in Bordetella. J. Bacteriol. 187:5665–5676 PubMed PMC
Mattoo S, Yuk MH, Huang LL, Miller JF. 2004. Regulation of type III secretion in Bordetella. Mol. Microbiol. 52:1201–1214 PubMed
Yuk MH, Harvill ET, Cotter PA, Miller JF. 2000. Modulation of host immune responses, induction of apoptosis and inhibition of NF-κB activation by the Bordetella type III secretion system. Mol. Microbiol. 35:991–1004 PubMed
Yuk MH, Harvill ET, Miller JF. 1998. The BvgAS virulence control system regulates type III secretion in Bordetella bronchiseptica. Mol. Microbiol. 28:945–959 PubMed
Han HJ, Kuwae A, Abe A, Arakawa Y, Kamachi K. 2011. Differential expression of type III effector BteA protein due to IS481 insertion in Bordetella pertussis. PLoS One 6:e17797.10.1371/journal.pone.0017797 PubMed DOI PMC
Gaillard ME, Bottero D, Castuma CE, Basile LA, Hozbor D. 2011. Laboratory adaptation of Bordetella pertussis is associated with the loss of type three secretion system functionality. Infect. Immun. 79:3677–3682 PubMed PMC
Skinner JA, Reissinger A, Shen H, Yuk MH. 2004. Bordetella type III secretion and adenylate cyclase toxin synergize to drive dendritic cells into a semimature state. J. Immunol. 173:1934–1940 PubMed
Medhekar B, Shrivastava R, Mattoo S, Gingery M, Miller JF. 2009. Bordetella Bsp22 forms a filamentous type III secretion system tip complex and is immunoprotective in vitro and in vivo. Mol. Microbiol. 71:492–504 PubMed PMC
Antoine R, Locht C. 1990. Roles of the disulfide bond and the carboxy-terminal region of the S1 subunit in the assembly and biosynthesis of pertussis toxin. Infect. Immun. 58:1518–1526 PubMed PMC
Stainer DW, Scholte MJ. 1970. A simple chemically defined medium for the production of phase I Bordetella pertussis. J. Gen. Microbiol. 63:211–220 PubMed
Khan F, He M, Taussig MJ. 2006. Double-hexahistidine tag with high-affinity binding for protein immobilization, purification, and detection on ni-nitrilotriacetic acid surfaces. Anal. Chem. 78:3072–3079 PubMed
Benada O, Pokorny V. 1990. Modification of the Polaron sputter-coater unit for glow-discharge activation of carbon support films. J. Electron Microsc. Technol. 16:235–239 PubMed
Ozcengiz E, Kilinc K, Buyuktanir O, Gunalp A. 2004. Rapid purification of pertussis toxin (PT) and filamentous hemagglutinin (FHA) by cation-exchange chromatography. Vaccine 22:1570–1575 PubMed
Karimova G, Fayolle C, Gmira S, Ullmann A, Leclerc C, Ladant D. 1998. Charge-dependent translocation of Bordetella pertussis adenylate cyclase toxin into eukaryotic cells: implication for the in vivo delivery of CD8(+) T cell epitopes into antigen-presenting cells. Proc. Natl. Acad. Sci. U. S. A. 95:12532–12537 PubMed PMC
Osicka R, Osickova A, Basar T, Guermonprez P, Rojas M, Leclerc C, Sebo P. 2000. Delivery of CD8+ T-cell epitopes into major histocompatibility complex class I antigen presentation pathway by Bordetella pertussis adenylate cyclase: delineation of cell invasive structures and permissive insertion sites. Infect. Immun. 68:247–256 PubMed PMC
Guiso N, Berbers G, Fry NK, He Q, Riffelmann M, Wirsing von Konig CH. 2011. What to do and what not to do in serological diagnosis of pertussis: recommendations from EU reference laboratories. Eur. J. Clin. Microbiol. Infect. Dis. 30:307–312 PubMed PMC
Betsou F, Sebo P, Guiso N. 1993. CyaC-mediated activation is important not only for toxic but also for protective activities of Bordetella pertussis adenylate cyclase-hemolysin. Infect. Immun. 61:3583–3589 PubMed PMC
Betsou F, Sebo P, Guiso N. 1995. The C-terminal domain is essential for protective activity of the Bordetella pertussis adenylate cyclase-hemolysin. Infect. Immun. 63:3309–3315 PubMed PMC
Carbonetti NH, Artamonova GV, Andreasen C, Dudley E, Mays RM, Worthington ZE. 2004. Suppression of serum antibody responses by pertussis toxin after respiratory tract colonization by Bordetella pertussis and identification of an immunodominant lipoprotein. Infect. Immun. 72:3350–3358 PubMed PMC
Mielcarek N, Debrie AS, Raze D, Bertout J, Rouanet C, Younes AB, Creusy C, Engle J, Goldman WE, Locht C. 2006. Live attenuated B. pertussis as a single-dose nasal vaccine against whooping cough. PLoS Pathog. 2:e65.10.1371/journal.ppat.0020065 PubMed DOI PMC
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