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Infection and Immunity, June 2005, p. 3618-3626, Vol. 73, No. 6
0019-9567/05/$08.00+0     doi:10.1128/IAI.73.6.3618-3626.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Bordetella bronchiseptica Adherence to Cilia Is Mediated by Multiple Adhesin Factors and Blocked by Surfactant Protein A

Jessica A. Edwards,1,2 Nathan A. Groathouse,3 and Scott Boitano1,2,4*

Department of Cell Biology and Anatomy,1 Arizona Respiratory Center,2 Department of Physiology, University of Arizona Health Sciences Center, Tucson, Arizona 85724,4 Department of Microbiology, Immunology and Pathology Colorado State University, Fort Collins, Colorado 80523-16823

Received 9 November 2004/ Returned for modification 15 December 2004/ Accepted 9 January 2005

In the virulent state (Bvg+), Bordetella bronchiseptica expresses adhesins and toxins that mediate adherence to the upper airway epithelium, an essential early step in pathogenesis. In this study, we used a rabbit tracheal epithelial cell binding assay to test how specific host or pathogen factors contribute to ciliary binding. The host antimicrobial agent surfactant protein A (SP-A) effectively reduced ciliary binding by Bvg+ B. bronchiseptica. To evaluate the relative contributions of bacterial adhesins and toxins to ciliary binding, we used mutant strains of B. bronchiseptica in the binding assay. When compared to Bvg+ or Bvg– phase-locked B. bronchiseptica strains, single-knockout strains lacking one of the known adhesins (filamentous hemagglutinin, pertactin, or fimbriae) displayed an intermediate ciliary binding capacity throughout the coincubation. A B. bronchiseptica strain deficient in adenylate cyclase-hemolysin toxin also displayed an intermediate level of adherence between Bvg+ and Bvg– strains and had the lowest ciliary affinity of any of the Bvg+ phase strains tested. A B. bronchiseptica strain that was missing dermonecrotic toxin also displayed intermediate binding; however, this strain displayed ciliary binding significantly higher than most of the adhesin knockouts tested. Taken together, these findings suggest that virulent-state B. bronchiseptica expresses multiple adhesins with overlapping contributions to ciliary adhesion and that host production of SP-A can provide innate immunity by blocking bacterial adherence to the ciliated epithelium.

* Corresponding author. Mailing address: Arizona Respiratory Center, Room 2338, AHSC Arizona Health Sciences Center, 1501 N. Campbell Avenue, Tucson, AZ 85724-5030. Phone: (520) 626-2105. Fax: (520) 626-6970. E-mail: sboitano{at}email.arizona.edu.

Editor: D. L. Burns

Infection and Immunity, June 2005, p. 3618-3626, Vol. 73, No. 6
0019-9567/05/$08.00+0     doi:10.1128/IAI.73.6.3618-3626.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.



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