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Infection and Immunity, March 2008, p. 1257-1266, Vol. 76, No. 3
0019-9567/08/$08.00+0     doi:10.1128/IAI.00836-07
Copyright © 2008, American Society for Microbiology. All Rights Reserved.

Bordetella pertussis Expresses a Functional Type III Secretion System That Subverts Protective Innate and Adaptive Immune Responses{triangledown}

Neil K. Fennelly,1 Federico Sisti,2 Sarah C. Higgins,1 Pádraig J. Ross,1 Han van der Heide,3 Frits R. Mooi,3 Aoife Boyd,4,{dagger} and Kingston H. G. Mills1*,{dagger}

Immune Regulation Research Group, School of Biochemistry and Immunology, Trinity College, Dublin, Ireland,1 Instituto de Bioquimica y Biologia Molecular, Universidad Nacional de La Plata, La Plata, Argentina,2 Laboratory for Infectious Diseases and Screening, RIVM, Bilthoven, The Netherlands,3 Department of Microbiology, National University of Ireland Galway, Ireland4

Received 18 June 2007/ Returned for modification 9 August 2007/ Accepted 2 January 2008

Certain bacteria use a type III secretion system (TTSS) to deliver effector proteins that interfere with cell function into host cells. While transcription of genes encoding TTSS components has been demonstrated, studies to date have failed to identify TTSS effector proteins in Bordetella pertussis. Here we present the first evidence of a functionally active TTSS in B. pertussis. Three known TTSS effectors, Bsp22, BopN, and BopD, were identified as TTSS substrates in B. pertussis 12743. We found expression of Bsp22 in a significant proportion of clinical isolates but not in common laboratory-adapted strains of B. pertussis. We generated a TTSS mutant of B. pertussis 12743 and showed that it induced significantly lower respiratory tract colonization in mice than the wild-type bacteria. Respiratory infection of mice with the mutant bacteria induced significantly greater innate proinflammatory cytokine production in the lungs soon after challenge, and this correlated with significantly higher antigen-specific interleukin-17, gamma interferon, and immunoglobulin G responses later in infection. Our findings suggest that the TTSS subverts innate and adaptive immune responses during infection of the lungs and may be a functionally important virulence factor for B. pertussis infection of humans.

* Corresponding author. Mailing address: Immune Regulation Research Group, School of Biochemistry and Immunology, Trinity College, Dublin 2, Ireland. Phone: (353) 1 8963573. Fax: (353) 1 6772086. E-mail: kingston.mills{at}tcd.ie

{triangledown} Published ahead of print on 14 January 2008.

Editor: J. B. Bliska

{dagger} A.B. and K.H.G.M. contributed equally to this study.

Infection and Immunity, March 2008, p. 1257-1266, Vol. 76, No. 3
0019-9567/08/$08.00+0     doi:10.1128/IAI.00836-07
Copyright © 2008, American Society for Microbiology. All Rights Reserved.



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