Pathogen attachment is a crucial early step in mucosal infections. This step is mediated by important virulence factors called adhesins. To exert these functions, adhesins are typically surface-exposed, although, surprisingly, some are also released into the extracellular milieu, the relevance of which has previously not been studied. To address the role of adhesin release in pathogenesis, we used Bordetella pertussis as a model, since its major adhesin, filamentous hemagglutinin (FHA), partitions between the bacterial surface and the extracellular milieu. FHA release depends on its maturation by the specific B. pertussis protease SphB1. We constructed SphB1-deficient mutants and found that they were strongly affected in their ability to colonize the mouse respiratory tract, although they adhered even better to host cells in vitro than their wild-type parent strain. The defect in colonization could be overcome by prior nasal instillation of purified FHA or by coinfection with FHA-releasing B. pertussis strains, but not with SphB1-producing FHA-deficient strains, ruling out a nonspecific effect of SphB1. These results indicate that the release of FHA is important for colonization, as it may facilitate the dispersal of bacteria from microcolonies and the binding to new sites in the respiratory tract.
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17 March 2003
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March 10 2003
Role of Adhesin Release for Mucosal Colonization by a Bacterial Pathogen
Loïc Coutte,
Loïc Coutte
1Institut National de la Sante et de la Recherche Medicale U447, Institut de Biologie de Lille, Institut Pasteur de Lille, 59019 Lille Cedex, France
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Sylvie Alonso,
Sylvie Alonso
1Institut National de la Sante et de la Recherche Medicale U447, Institut de Biologie de Lille, Institut Pasteur de Lille, 59019 Lille Cedex, France
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Nathalie Reveneau,
Nathalie Reveneau
1Institut National de la Sante et de la Recherche Medicale U447, Institut de Biologie de Lille, Institut Pasteur de Lille, 59019 Lille Cedex, France
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Eve Willery,
Eve Willery
1Institut National de la Sante et de la Recherche Medicale U447, Institut de Biologie de Lille, Institut Pasteur de Lille, 59019 Lille Cedex, France
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Brigitte Quatannens,
Brigitte Quatannens
2Centre National de la Recherche Scientifique UMR 8526, Institut de Biologie de Lille, Institut Pasteur de Lille, 59019 Lille Cedex, France
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Camille Locht,
Camille Locht
1Institut National de la Sante et de la Recherche Medicale U447, Institut de Biologie de Lille, Institut Pasteur de Lille, 59019 Lille Cedex, France
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Françoise Jacob-Dubuisson
Françoise Jacob-Dubuisson
1Institut National de la Sante et de la Recherche Medicale U447, Institut de Biologie de Lille, Institut Pasteur de Lille, 59019 Lille Cedex, France
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Loïc Coutte
1Institut National de la Sante et de la Recherche Medicale U447, Institut de Biologie de Lille, Institut Pasteur de Lille, 59019 Lille Cedex, France
Sylvie Alonso
1Institut National de la Sante et de la Recherche Medicale U447, Institut de Biologie de Lille, Institut Pasteur de Lille, 59019 Lille Cedex, France
Nathalie Reveneau
1Institut National de la Sante et de la Recherche Medicale U447, Institut de Biologie de Lille, Institut Pasteur de Lille, 59019 Lille Cedex, France
Eve Willery
1Institut National de la Sante et de la Recherche Medicale U447, Institut de Biologie de Lille, Institut Pasteur de Lille, 59019 Lille Cedex, France
Brigitte Quatannens
2Centre National de la Recherche Scientifique UMR 8526, Institut de Biologie de Lille, Institut Pasteur de Lille, 59019 Lille Cedex, France
Camille Locht
1Institut National de la Sante et de la Recherche Medicale U447, Institut de Biologie de Lille, Institut Pasteur de Lille, 59019 Lille Cedex, France
Françoise Jacob-Dubuisson
1Institut National de la Sante et de la Recherche Medicale U447, Institut de Biologie de Lille, Institut Pasteur de Lille, 59019 Lille Cedex, France
Address correspondence to F. Jacob-Dubuisson, INSERM U447, Institut de Biologie de Lille, Institut Pasteur de Lille, 1 rue Calmette, 59019 Lille Cedex, France. Phone: 33-320-87-11-55; Fax: 33-320-87-11-58; E-mail: [email protected]
L. Coutte and S. Alonso contributed equally to this work.
S. Alonso's present address is Microbiology and Immunology, 5173 Veterinary Medical Center, Cornell University, Ithaca, NY 14853.
*
Abbreviations used in this paper: BG, Bordet-Gengou; FHA, filamentous hemagglutinin; PTX, pertussis toxin, PBSG, PBS with 5% glycerol.
Received:
July 10 2002
Revision Received:
December 30 2002
Accepted:
January 21 2003
Online ISSN: 1540-9538
Print ISSN: 0022-1007
The Rockefeller University Press
2003
J Exp Med (2003) 197 (6): 735–742.
Article history
Received:
July 10 2002
Revision Received:
December 30 2002
Accepted:
January 21 2003
Citation
Loïc Coutte, Sylvie Alonso, Nathalie Reveneau, Eve Willery, Brigitte Quatannens, Camille Locht, Françoise Jacob-Dubuisson; Role of Adhesin Release for Mucosal Colonization by a Bacterial Pathogen . J Exp Med 17 March 2003; 197 (6): 735–742. doi: https://doi.org/10.1084/jem.20021153
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