Comparative Role of Immunoglobulin A in Protective Immunity against the Bordetellae

ABSTRACT The genus Bordetella includes a group of closely related mammalian pathogens that cause a variety of respiratory diseases in a long list of animals (B. bronchiseptica) and whooping cough in humans (B. pertussis and B. parapertussis). While past research has examined how these pathogens are eliminated from the lower respiratory tract, the host factors that control and/or clear the bordetellae from the upper respiratory tract remain unclear. We hypothesized that immunoglobulin A (IgA), the predominant mucosal antibody isotype, would have a protective role against these mucosal pathogens. IgA−/− mice were indistinguishable from wild-type mice in their control and clearance of B. pertussis or B. parapertussis, suggesting that IgA is not crucial to immunity to these organisms. However, naïve and convalescent IgA−/− mice were defective in reducing the numbers of B. bronchiseptica in the upper respiratory tract compared to wild-type controls. Passively transferred serum from convalescent IgA−/− mice was not as effective as serum from convalescent wild-type mice in clearing this pathogen from the tracheae of naive recipient mice. IgA induced by B. bronchiseptica infection predominantly recognized lipopolysaccharide-containing O-antigen, and antibodies against O-antigen were important to bacterial clearance from the trachea. Since an IgA response contributes to the control of B. bronchiseptica infection of the upper respiratory tract, immunization strategies aimed at inducing B. bronchiseptica-specific IgA may be beneficial to preventing the spread of this bacterium among domestic animal populations.

[1]  F. Mooi,et al.  Immunoglobulin A-Mediated Protection against Bordetella pertussis Infection , 2001, Infection and Immunity.

[2]  J. Orenstein,et al.  Killing of Streptococcus pneumoniae by capsular polysaccharide-specific polymeric IgA, complement, and phagocytes. , 1999, The Journal of clinical investigation.

[3]  D. Dombrowicz,et al.  Heterogeneity of Expression of IgA Receptors by Human, Mouse, and Rat Eosinophils1 , 2005, The Journal of Immunology.

[4]  M. van Egmond,et al.  The Fc receptor for IgA (FcalphaRI, CD89). , 2004, Immunology letters.

[5]  G. Pier,et al.  Polyclonal and monoclonal antibody therapy for experimental Pseudomonas aeruginosa pneumonia , 1986, Infection and immunity.

[6]  Jeff F. Miller,et al.  Comparative Phenotypic Analysis of the Bordetella parapertussis Isolate Chosen for Genomic Sequencing , 2002, Infection and Immunity.

[7]  J. Miller,et al.  BvgAS-mediated signal transduction: analysis of phase-locked regulatory mutants of Bordetella bronchiseptica in a rabbit model , 1994, Infection and immunity.

[8]  F. Mooi,et al.  Reemergence of pertussis in the highly vaccinated population of the Netherlands: observations on surveillance data. , 2000, Emerging infectious diseases.

[9]  R. Monteiro,et al.  IgA Fc receptors. , 2003, Annual review of immunology.

[10]  J. Cherry,et al.  Determination of serum antibody to Bordetella pertussis adenylate cyclase toxin in vaccinated and unvaccinated children and in children and adults with pertussis. , 2004, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[11]  E. Cox,et al.  The IgA system: a comparison of structure and function in different species. , 2006, Veterinary research.

[12]  A. Bradley,et al.  Targeted deletion of the IgA constant region in mice leads to IgA deficiency with alterations in expression of other Ig isotypes. , 1999, Journal of immunology.

[13]  R. Heyderman,et al.  Influence of age and carriage status on salivary IgA to Neisseria meningitidis , 2005, Epidemiology and Infection.

[14]  R. Schneerson,et al.  Hypothesis for vaccine development: protective immunity to enteric diseases caused by nontyphoidal salmonellae and shigellae may be conferred by serum IgG antibodies to the O-specific polysaccharide of their lipopolysaccharides. , 1992, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[15]  B. Finlay,et al.  Clearance of Citrobacter rodentium Requires B Cells but Not Secretory Immunoglobulin A (IgA) or IgM Antibodies , 2004, Infection and Immunity.

[16]  A. Melegaro,et al.  The current burden of pneumococcal disease in England and Wales. , 2006, The Journal of infection.

[17]  D. Metzger,et al.  An Important Role for Polymeric Ig Receptor-Mediated Transport of IgA in Protection against Streptococcus pneumoniae Nasopharyngeal Carriage1 , 2004, The Journal of Immunology.

[18]  D. Relman,et al.  Recognition of a bacterial adhesin by an integrin: Macrophage CR3 (α M β 2, CD11b CD18 ) binds filamentous hemagglutinin of Bordetella pertussis , 1990, Cell.

[19]  Paul B. Mann,et al.  Role of Antibodies in Immunity to Bordetella Infections , 2003, Infection and Immunity.

[20]  D. Relman,et al.  Recognition of a bacterial adhesion by an integrin: macrophage CR3 (alpha M beta 2, CD11b/CD18) binds filamentous hemagglutinin of Bordetella pertussis. , 1990, Cell.

[21]  D. Wolfe,et al.  Clearance of Bordetella parapertussis from the Lower Respiratory Tract Requires Humoral and Cellular Immunity , 2005, Infection and Immunity.

[22]  E. van Garderen,et al.  IgA and the IgA Fc receptor. , 2001, Trends in immunology.

[23]  A. A. Akhiani,et al.  IgA Antibodies Impair Resistance against Helicobacter pylori Infection: Studies on Immune Evasion in IL-10-Deficient Mice1 , 2005, The Journal of Immunology.

[24]  B. Barrell,et al.  Genetic Basis for Lipopolysaccharide O-Antigen Biosynthesis in Bordetellae , 1999, Infection and Immunity.

[25]  Paul B. Mann,et al.  Use of a Genetically Defined Double Mutant Strain of Bordetella bronchiseptica Lacking Adenylate Cyclase and Type III Secretion as a Live Vaccine , 2007, Infection and Immunity.

[26]  S. Halperin,et al.  Pertussis of adults and infants. , 2002, The Lancet. Infectious diseases.

[27]  M. Egmond,et al.  Chapter 2 The Fc receptor for IgA (FcαRI, CD89) , 2004 .

[28]  D. Skowronski,et al.  The changing age and seasonal profile of pertussis in Canada. , 2002, The Journal of infectious diseases.

[29]  D. Wolfe,et al.  Different mechanisms of vaccine-induced and infection-induced immunity to Bordetella bronchiseptica. , 2007, Microbes and infection.

[30]  Seema Mattoo,et al.  Molecular Pathogenesis, Epidemiology, and Clinical Manifestations of Respiratory Infections Due to Bordetella pertussis and Other Bordetella Subspecies , 2005, Clinical Microbiology Reviews.

[31]  P. Wright,et al.  Role of IgA versus IgG in the Control of Influenza Viral Infection in the Murine Respiratory Tract1 , 2004, The Journal of Immunology.

[32]  Mahavir Singh,et al.  Role of IgA in the defense against respiratory infections IgA deficient mice exhibited increased susceptibility to intranasal infection with Mycobacterium bovis BCG. , 2005, Vaccine.

[33]  D. Maskell,et al.  Molecular and functional analysis of the lipopolysaccharide biosynthesis locus wlb from Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica , 1998, Molecular microbiology.

[34]  D. Bemis,et al.  An improved system for studying the effect of Bordetella bronchiseptica on the ciliary activity of canine tracheal epithelial cells. , 1981, The Journal of infectious diseases.

[35]  M. L. Ciofi Degli Atti,et al.  Bordetella parapertussis Infection in Children: Epidemiology, Clinical Symptoms, and Molecular Characteristics of Isolates , 1998, Journal of Clinical Microbiology.

[36]  R. Goodnow Biology of Bordetella bronchiseptica , 1980, Microbiological reviews.

[37]  I. Mitov,et al.  Protective efficacy of IgA monoclonal antibodies to O and H antigens in a mouse model of intranasal challenge with Salmonella enterica serotype Enteritidis. , 2004, Microbes and infection.

[38]  N. Chanter,et al.  The pathogenesis of turbinate atrophy in pigs caused by Bordetella bronchiseptica. , 1988, Veterinary microbiology.

[39]  Jane W. Marsh,et al.  Antigenic shift and increased incidence of meningococcal disease. , 2006, The Journal of infectious diseases.

[40]  K. Switzer,et al.  Mucosal immunity to influenza without IgA: an IgA knockout mouse model. , 1999, Journal of immunology.

[41]  M. Massari,et al.  Resurgence of Pertussis in Europe , 2005, The Pediatric infectious disease journal.

[42]  L. Babiuk,et al.  Maternal Immunity Provides Protection against Pertussis in Newborn Piglets , 2006, Infection and Immunity.

[43]  Paul B. Mann,et al.  The Complex Mechanism of Antibody-Mediated Clearance of Bordetella from the Lungs Requires TLR41 , 2005, The Journal of Immunology.

[44]  D. Metzger,et al.  Mucosal B Cell Deficiency in IgA−/− Mice Abrogates the Development of Allergic Lung Inflammation1 , 2005, The Journal of Immunology.