In-vitro and in-vivo analysis of the production of the Bordetella type three secretion system effector A in Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica

Microbes and Infection

Volumn 15, Issue 5, 2013, Pages 399-408

  Hegerle, Nicolas ^a,b   Rayat, Lamya ^a,b   Dore, Grégory ^a,b   Zidane, Nora ^a,b   Bedouelle, Hugues ^a,b   Guiso, Nicole ^a,b  

^a INSTITUT PASTEUR   (France)

^b CNRS URA3012   (France)

Author keywords

Bordetella; BteA; Vaccination

Indexed keywords

BORDETELLA VIRULENCE FACTOR;

ARTICLE; BORDETELLA BRONCHISEPTICA; BORDETELLA PARAPERTUSSIS; BORDETELLA PERTUSSIS; CELL MIGRATION; CONTROLLED STUDY; GENE INSERTION SEQUENCE; GENOTYPE; HEALTH CARE POLICY; HUMORAL IMMUNITY; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR WEIGHT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PURIFICATION; TYPE III SECRETION SYSTEM; TYPE THREE SECRETION SYSTEM EFFECTOR A;

ANIMALS; BACTERIAL TOXINS; BORDETELLA BRONCHISEPTICA; BORDETELLA INFECTIONS; BORDETELLA PARAPERTUSSIS; BORDETELLA PERTUSSIS; DISEASE MODELS, ANIMAL; DNA, BACTERIAL; FEMALE; FRANCE; HUMANS; MICE; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, DNA; VIRULENCE FACTORS;

BORDETELLA; BORDETELLA BRONCHISEPTICA; BORDETELLA PARAPERTUSSIS; BORDETELLA PERTUSSIS;

EID: 84876878973     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2013.02.006     Document Type: Article

References (47)

1. Pertussis vaccines: WHO position paper-recommendations. Vaccine 2011, 29:2355-2356.
2. Mattoo S., Cherry J.D. Molecular pathogenesis, epidemiology, and clinical manifestations of respiratory infections due to Bordetella pertussis and other Bordetella subspecies. Clin. Microbiol. Rev. 2005, 18:326-382.
3. Diavatopoulos D.A., Cummings C.A., Schouls L.M., Brinig M.M., Relman D.A., Mooi F.R. Bordetella pertussis, the causative agent of whooping cough, evolved from a distinct, human-associated lineage of B. bronchiseptica. PLoS Pathog. 2005, 1:e45.
4. Parkhill J., Sebaihia M., Preston A., Murphy L.D., Thomson N., Harris D.E., Holden M.T., Churcher C.M., Bentley S.D., Mungall K.L., Cerdeno-Tarraga A.M., Temple L., James K., Harris B., Quail M.A., Achtman M., Atkin R., Baker S., Basham D., Bason N., Cherevach I., Chillingworth T., Collins M., Cronin A., Davis P., Doggett J., Feltwell T., Goble A., Hamlin N., Hauser H., Holroyd S., Jagels K., Leather S., Moule S., Norberczak H., O'Neil S., Ormond D., Price C., Rabbinowitsch E., Rutter S., Sanders M., Saunders D., Seeger K., Sharp S., Simmonds M., Skelton J., Squares R., Squares S., Stevens K., Unwin L., Whitehead S., Barrell B.G., Maskell D.J. Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nat. Genet. 2003, 35:32-40.
5. Kallonen T., Grondahl-Yli-Hannuksela K., Elomaa A., Lutynska A., Fry N.K., Mertsola J., He Q. Differences in the genomic content of Bordetella pertussis isolates before and after introduction of pertussis vaccines in four European countries. Infect. Genet. Evol. 2011, 11:2034-2042.
6. Mooi F.R., He Q., Guiso N. Phylogeny, evolution and epidemiology of Bordetellae. Bordetella: Molecular Microbiology 2007, 17-45. Horizon Bioscience. F.C. Locht (Ed.).
7. Guiso N. Bordetella pertussis and pertussis vaccines. Clin. Infect. Dis. 2009, 49:1565-1569.
8. Barkoff A.M., Mertsola J., Guillot S., Guiso N., Berbers G., He Q. Appearance of Bordetella pertussis strains not expressing vaccine antigen pertactin in Finland. Clin. Vaccine Immunol. 2012, 19:1703-1704.
9. Bouchez V., Brun D., Cantinelli T., Dore G., Njamkepo E., Guiso N. First report and detailed characterization of B. pertussis isolates not expressing pertussis toxin or pertactin. Vaccine 2009, 27:6034-6041.
10. Hegerle N., Paris A.S., Brun D., Dore G., Njamkepo E., Guillot S., Guiso N. Evolution of French Bordetella pertussis and Bordetella parapertussis isolates: increase of Bordetellae not expressing pertactin. Clin. Microbiol. Infect. 2012, 18:E340-E346.
11. Otsuka N., Han H.J., Toyoizumi-Ajisaka H., Nakamura Y., Arakawa Y., Shibayama K., Kamachi K. Prevalence and genetic characterization of pertactin-deficient Bordetella pertussis in Japan. PLoS One 2012, 7:e31985.
12. Han H.J., Kuwae A., Abe A., Arakawa Y., Kamachi K. Differential expression of type III effector BteA protein due to IS481 insertion in Bordetella pertussis. PLoS One 2011, 6:e17797.
13. Panina E.M., Mattoo S., Griffith N., Kozak N.A., Yuk M.H., Miller J.F. A genome-wide screen identifies a Bordetella type III secretion effector and candidate effectors in other species. Mol. Microbiol. 2005, 58:267-279.
14. Mattoo S., Yuk M.H., Huang L.L., Miller J.F. Regulation of type III secretion in Bordetella. Mol. Microbiol. 2004, 52:1201-1214.
15. Fennelly N.K., Sisti F., Higgins S.C., Ross P.J., van der Heide H., Mooi F.R., Boyd A., Mills K.H. Bordetella pertussis expresses a functional type III secretion system that subverts protective innate and adaptive immune responses. Infect. Immun. 2008, 76:1257-1266.
16. Kuwae A., Matsuzawa T., Ishikawa N., Abe H., Nonaka T., Fukuda H., Imajoh-Ohmi S., Abe A. BopC is a novel type III effector secreted by Bordetella bronchiseptica and has a critical role in type III-dependent necrotic cell death. J. Biol. Chem. 2006, 281:6589-6600.
17. Weber C., Boursaux-Eude C., Coralie G., Caro V., Guiso N. Polymorphism of Bordetella pertussis isolates circulating for the last 10 years in France, where a single effective whole-cell vaccine has been used for more than 30 years. J. Clin. Microbiol. 2001, 39:4396-4403.
18. Bouchez V., Caro V., Levillain E., Guigon G., Guiso N. Genomic content of Bordetella pertussis clinical isolates circulating in areas of intensive children vaccination. PLoS One 2008, 3:e2437.
19. Le Blay K., Gueirard P., Guiso N., Chaby R. Antigenic polymorphism of the lipopolysaccharides from human and animal isolates of Bordetella bronchiseptica. Microbiology 1997, 143:1433-1441.
20. Pradel E., Guiso N., Menozzi F.D., Locht C. Bordetella pertussis TonB, a Bvg-independent virulence determinant. Infect. Immun. 2000, 68:1919-1927.
21. Betsou F., Sebo P., Guiso N. CyaC-mediated activation is important not only for toxic but also for protective activities of Bordetella pertussis adenylate cyclase-hemolysin. Infect. Immun. 1993, 61:3583-3589.
22. Fry N.K., Neal S., Harrison T.G., Miller E., Matthews R., George R.C. Genotypic variation in the Bordetella pertussis virulence factors pertactin and pertussis toxin in historical and recent clinical isolates in the United Kingdom. Infect. Immun. 2001, 69:5520-5528.
23. Mooi F.R., van Loo I.H., van Gent M., He Q., Bart M.J., Heuvelman K.J., de Greeff S.C., Diavatopoulos D., Teunis P., Nagelkerke N., Mertsola J. Bordetella pertussis strains with increased toxin production associated with pertussis resurgence. Emerg. Infect. Dis. 2009, 15:1206-1213.
24. Khelef N., Sakamoto H., Guiso N. Both adenylate cyclase and hemolytic activities are required by Bordetella pertussis to initiate infection. Microb. Pathog. 1992, 12:227-235.
25. van Gent M., Bart M.J., van der Heide H.G., Heuvelman K.J., Mooi F.R. Small mutations in Bordetella pertussis are associated with selective sweeps. PLoS One 2012, 7:e46407.
26. Gueirard P., Weber C., Le Coustumier A., Guiso N. Human Bordetella bronchiseptica infection related to contact with infected animals: persistence of bacteria in host. J. Clin. Microbiol. 1995, 33:2002-2006.
27. Harvill E.T., Preston A., Cotter P.A., Allen A.G., Maskell D.J., Miller J.F. Multiple roles for Bordetella lipopolysaccharide molecules during respiratory tract infection. Infect. Immun. 2000, 68:6720-6728.
28. Khelef N., Bachelet C.M., Vargaftig B.B., Guiso N. Characterization of murine lung inflammation after infection with parental Bordetella pertussis and mutants deficient in adhesins or toxins. Infect. Immun. 1994, 62:2893-2900.
29. Kurushima J., Kuwae A., Abe A. The type III secreted protein BspR regulates the virulence genes in Bordetella bronchiseptica. PLoS One 2012, 7:e38925.
30. French C.T., Panina E.M., Yeh S.H., Griffith N., Arambula D.G., Miller J.F. The Bordetella type III secretion system effector BteA contains a conserved N-terminal motif that guides bacterial virulence factors to lipid rafts. Cell. Microbiol. 2009, 11:1735-1749.
31. Yuk M.H., Harvill E.T., Miller J.F. The BvgAS virulence control system regulates type III secretion in Bordetella bronchiseptica. Mol. Microbiol. 1998, 28:945-959.
32. Buboltz A.M., Nicholson T.L., Weyrich L.S., Harvill E.T. Role of the type III secretion system in a hypervirulent lineage of Bordetella bronchiseptica. Infect. Immun. 2009, 77:3969-3977.
33. Kozak N.A., Panina E.M., Miller J.F. Type III secretion in Bordetella supspecies. Bordetella Molecular Microbiology 2007, 119-139. Horizon Bioscience. F.C. Locht (Ed.).
34. Medhekar B., Shrivastava R., Mattoo S., Gingery M., Miller J.F. Bordetella Bsp22 forms a filamentous type III secretion system tip complex and is immunoprotective in-vitro and in-vivo. Mol. Microbiol. 2009, 71:492-504.
35. Yuk M.H., Harvill E.T., Cotter P.A., Miller J.F. Modulation of host immune responses, induction of apoptosis and inhibition of NF-kappaB activation by the Bordetella type III secretion system. Mol. Microbiol. 2000, 35:991-1004.
36. Gaillard M.E., Bottero D., Castuma C.E., Basile L.A., Hozbor D. Laboratory adaptation of Bordetella pertussis is associated with the loss of type three secretion system functionality. Infect. Immun. 2011, 79:3677-3682.
37. Caro V., Hot D., Guigon G., Hubans C., Arrive M., Soubigou G., Renauld-Mongenie G., Antoine R., Locht C., Lemoine Y., Guiso N. Temporal analysis of French Bordetella pertussis isolates by comparative whole-genome hybridization. Microbe. Infect. 2006, 8:2228-2235.
38. Kallonen T., He Q. Bordetella pertussis strain variation and evolution postvaccination. Expert Rev. Vaccines 2009, 8:863-875.
39. Njamkepo E., Cantinelli T., Guigon G., Guiso N. Genomic analysis and comparison of Bordetella pertussis isolates circulating in low and high vaccine coverage areas. Microbe. Infect. 2008, 10:1582-1586.
40. Liese J.G., Renner C., Stojanov S., Belohradsky B.H. Clinical and epidemiological picture of B pertussis and B parapertussis infections after introduction of acellular pertussis vaccines. Arch. Dis. Child. 2003, 88:684-687.
41. Bart M.J., van Gent M., van der Heide H.G., Boekhorst J., Hermans P., Parkhill J., Mooi F.R. Comparative genomics of prevaccination and modern Bordetella pertussis strains. BMC Genom. 2010, 11:627.
42. Gueirard P., Minoprio P., Guiso N. Intranasal inoculation of Bordetella bronchiseptica in mice induces long-lasting antibody and T-cell mediated immune responses. Scand. J. Immunol. 1996, 43:181-192.
43. Weyrich L.S., Rolin O.Y., Muse S.J., Park J., Spidale N., Kennett M.J., Hester S.E., Chen C., Dudley E.G., Harvill E.T. A type VI secretion system encoding locus is required for Bordetella bronchiseptica immunomodulation and persistence in-vivo. PLoS One 2012, 7:e45892.
44. Chenal-Francisque V., Caro V., Boursaux-Eude C., Guiso N. Genomic analysis of the adenylate cyclase-hemolysin C-terminal region of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Res. Microbiol. 2009, 160:330-336.
45. Henderson M.W., Inatsuka C.S., Sheets A.J., Williams C.L., Benaron D.J., Donato G.M., Gray M.C., Hewlett E.L., Cotter P.A. Contribution of Bordetella filamentous hemagglutinin and adenylate cyclase toxin to suppression and evasion of interleukin-17-mediated inflammation. Infect. Immun. 2012, 80:2061-2075.
46. Bouchez V., Brun D., Dore G., Njamkepo E., Guiso N. Bordetella parapertussis isolates not expressing pertactin circulating in France. Clin. Microbiol. Infect. 2011, 17:675-682.
47. Gueirard P., Guiso N. Virulence of Bordetella bronchiseptica: role of adenylate cyclase-hemolysin. Infect. Immun. 1993, 61:4072-4078.