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Infection and Immunity, June 2004, p. 3350-3358, Vol. 72, No. 6
0019-9567/04/$08.00+0     DOI: 10.1128/IAI.72.6.3350-3358.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

Suppression of Serum Antibody Responses by Pertussis Toxin after Respiratory Tract Colonization by Bordetella pertussis and Identification of an Immunodominant Lipoprotein

Nicholas H. Carbonetti,1* Galina V. Artamonova,1 Charlotte Andreasen,1 Edward Dudley,2 R. Michael Mays,1 and Zoe E. V. Worthington1

Department of Microbiology and Immunology,1 Center for Vaccine Development, University of Maryland Medical School, Baltimore, Maryland 212012

Received 1 December 2003/ Returned for modification 6 January 2004/ Accepted 13 February 2004

Pertussis toxin (PT), a virulence factor secreted by Bordetella pertussis, contributes to respiratory tract infection and disease caused by this pathogen. By comparing a wild-type (WT) B. pertussis strain to a mutant strain with an in-frame deletion of the ptx genes encoding PT ({Delta}PT), we recently found that the lack of PT confers a significant defect in respiratory tract colonization in mice after intranasal inoculation. In this study, we analyzed serum antibody responses in mice infected with the WT or {Delta}PT strain and found that infection with the {Delta}PT strain elicited greater responses to several B. pertussis antigens than did infection with the WT, despite the lower colonization level achieved by the {Delta}PT strain. The same enhanced antibody response was observed after infection with a strain expressing an enzymatically inactive PT; but this response was not observed after infection with B. pertussis mutant strains lacking filamentous hemagglutinin or adenylate cyclase toxin, nor when purified PT was administered with the {Delta}PT inoculum, indicating a specific role for PT activity in this immunosuppressive effect. In particular, there were consistent strong serum antibody responses to one or more low-molecular-weight antigens after infection with the {Delta}PT strain. These antigens were Bvg independent, membrane localized, and also expressed by the closely related pathogens Bordetella parapertussis and Bordetella bronchiseptica. Two-dimensional gel electrophoresis and mass spectrometry were used to identify one of the immunodominant low-molecular-weight antigens as a protein with significant sequence homology to peptidoglycan-associated lipoprotein in several other gram-negative bacterial species. However, a serum antibody response to this protein alone did not protect mice against respiratory tract infection by B. pertussis.

* Corresponding author. Mailing address: Department of Microbiology and Immunology, University of Maryland School of Medicine, 655 W. Baltimore St., BRB13-009, Baltimore, MD 21201. Phone: (410) 706-7677. Fax: (410) 706-2129. E-mail: ncarbone{at}umaryland.edu.

Editor: A. D. O'Brien

Infection and Immunity, June 2004, p. 3350-3358, Vol. 72, No. 6
0019-9567/04/$08.00+0     DOI: 10.1128/IAI.72.6.3350-3358.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Andreasen, C., Carbonetti, N. H. (2009). Role of Neutrophils in Response to Bordetella pertussis Infection in Mice. Infect. Immun. 77: 1182-1188 [Abstract] [Full Text]  
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