Role of Neutrophils in Response to Bordetella pertussis Infection in Mice

ABSTRACT Pertussis is an acute respiratory disease caused by the bacterium Bordetella pertussis, for which humans are the only known reservoir. During infection, B. pertussis releases several toxins, including pertussis toxin (PT) and adenylate cyclase toxin (ACT), which have both been shown to play roles in promoting bacterial growth during early infection in a mouse model. Furthermore, in vitro and in vivo studies suggest that PT and ACT affect neutrophil chemotaxis and/or function, thereby altering the innate immune response. In this study we depleted animals of neutrophils to investigate whether neutrophils play a protective role during B. pertussis infection in mice. In addition, by infection with toxin-deficient strains, we investigated whether neutrophils are the main targets for PT and/or ACT activity in promoting bacterial growth. Surprisingly, we found no role for neutrophils during B. pertussis infection in naïve mice. However, in previously infected (immune) mice or in mice receiving immune serum, we observed a significant role for neutrophils during infection. Furthermore, in this immune mouse model our evidence indicates that neutrophils appear to be the main target cells for ACT, but not for PT.

[1]  N. Carbonetti,et al.  Pertussis Toxin Inhibits Early Chemokine Production To Delay Neutrophil Recruitment in Response to Bordetella pertussis Respiratory Tract Infection in Mice , 2008, Infection and Immunity.

[2]  M. Umemura,et al.  Interleukin‐17 as an Effector Molecule of Innate and Acquired Immunity against Infections , 2007, Microbiology and immunology.

[3]  N. Van Rooijen,et al.  Pertussis Toxin Targets Airway Macrophages To Promote Bordetella pertussis Infection of the Respiratory Tract , 2007, Infection and Immunity.

[4]  M. Marquis,et al.  CD8+ T Cells but Not Polymorphonuclear Leukocytes Are Required To Limit Chronic Oral Carriage of Candida albicans in Transgenic Mice Expressing Human Immunodeficiency Virus Type 1 , 2006, Infection and Immunity.

[5]  O. Bjørnstad,et al.  Pertussis toxin inhibits neutrophil recruitment to delay antibody-mediated clearance of Bordetella pertussis. , 2005, The Journal of clinical investigation.

[6]  A. Weiss,et al.  Influence of CR3 (CD11b/CD18) Expression on Phagocytosis of Bordetella pertussis by Human Neutrophils , 2005, Infection and Immunity.

[7]  A. Nelson,et al.  The Role of Innate Immune Responses in the Outcome of Interspecies Competition for Colonization of Mucosal Surfaces , 2005, PLoS pathogens.

[8]  M. Burdick,et al.  CXCR2 is critical for dsRNA-induced lung injury: relevance to viral lung infection , 2005, Journal of Inflammation.

[9]  N. Carbonetti,et al.  Pertussis Toxin and Adenylate Cyclase Toxin Provide a One-Two Punch for Establishment of Bordetella pertussis Infection of the Respiratory Tract , 2005, Infection and Immunity.

[10]  Aaron M Wendelboe,et al.  Duration of Immunity Against Pertussis After Natural Infection or Vaccination , 2005, The Pediatric infectious disease journal.

[11]  E. Dudley,et al.  Suppression of Serum Antibody Responses by Pertussis Toxin after Respiratory Tract Colonization by Bordetella pertussis and Identification of an Immunodominant Lipoprotein , 2004, Infection and Immunity.

[12]  M. Burdick,et al.  Depletion of CXCR2 Inhibits Tumor Growth and Angiogenesis in a Murine Model of Lung Cancer1 , 2004, The Journal of Immunology.

[13]  N. Carbonetti,et al.  Pertussis Toxin Plays an Early Role in Respiratory Tract Colonization by Bordetella pertussis , 2003, Infection and Immunity.

[14]  B. Connelly,et al.  Phagocytosis of Bordetella pertussis incubated with convalescent serum. , 2003, The Journal of infectious diseases.

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

[16]  J. Jensenius,et al.  EndoS and SpeB from Streptococcus pyogenes Inhibit Immunoglobulin-Mediated Opsonophagocytosis , 2002, Infection and Immunity.

[17]  J. Shellito,et al.  Requirement of Interleukin 17 Receptor Signaling for Lung Cxc Chemokine and Granulocyte Colony-Stimulating Factor Expression, Neutrophil Recruitment, and Host Defense , 2001, The Journal of experimental medicine.

[18]  T. Standiford,et al.  Chemokine-Dependent Neutrophil Recruitment in a Murine Model of Legionella Pneumonia: Potential Role of Neutrophils as Immunoregulatory Cells , 2001, Infection and Immunity.

[19]  E. Hewlett,et al.  Neutralizing Antibodies to Adenylate Cyclase Toxin Promote Phagocytosis of Bordetella pertussis by Human Neutrophils , 2000, Infection and Immunity.

[20]  M. Burdick,et al.  The CXC Chemokine Receptor 2, CXCR2, Is the Putative Receptor for ELR+ CXC Chemokine-Induced Angiogenic Activity1 , 2000, The Journal of Immunology.

[21]  T. Standiford,et al.  CXC Chemokine Receptor CXCR2 Is Essential for Protective Innate Host Response in Murine Pseudomonas aeruginosaPneumonia , 2000, Infection and Immunity.

[22]  M. Trautmann,et al.  Binding to and Opsonophagocytic Activity of O-Antigen-Specific Monoclonal Antibodies against Encapsulated and NonencapsulatedKlebsiella pneumoniae Serotype O1 Strains , 2000, Infection and Immunity.

[23]  A. Weiss,et al.  Bordetella pertussis Virulence Factors Affect Phagocytosis by Human Neutrophils , 2000, Infection and Immunity.

[24]  T. Standiford,et al.  Bacterial Clearance and Survival Are Dependent on CXC Chemokine Receptor-2 Ligands in a Murine Model of Pulmonary Nocardia asteroides Infection1 , 2000, The Journal of Immunology.

[25]  Eric T. Harvill,et al.  Pregenomic Comparative Analysis betweenBordetella bronchiseptica RB50 and Bordetella pertussis Tohama I in Murine Models of Respiratory Tract Infection , 1999, Infection and Immunity.

[26]  C. Jarstrand,et al.  Combined treatment with surfactant and specific immunoglobulin reduces bacterial proliferation in experimental neonatal group B streptococcal pneumonia. , 1999, American journal of respiratory and critical care medicine.

[27]  Jeff F. Miller,et al.  Probing the Function of Bordetella bronchiseptica Adenylate Cyclase Toxin by Manipulating Host Immunity , 1999, Infection and Immunity.

[28]  D. Burns,et al.  Role of gamma interferon in natural clearance of Bordetella pertussis infection , 1997, Infection and immunity.

[29]  E. Hewlett Pertussis: current concepts of pathogenesis and prevention. , 1997, The Pediatric infectious disease journal.

[30]  C. A. Janeway Immunobiology: The Immune System in Health and Disease , 1996 .

[31]  D. Morrison,et al.  Pertussis toxin-sensitive factor differentially regulates lipopolysaccharide-induced tumor necrosis factor-alpha and nitric oxide production in mouse peritoneal macrophages. , 1993, Journal of immunology.

[32]  W. Goldman,et al.  Effects of Bordetella pertussis infection on human respiratory epithelium in vivo and in vitro , 1991, Infection and immunity.

[33]  R. Daynes,et al.  Inhibition of lymphocyte and neutrophil chemotaxis by pertussis toxin. , 1985, Journal of immunology.

[34]  E. Hansen,et al.  Role of C5 and recruited neutrophils in early clearance of nontypable Haemophilus influenzae from murine lungs , 1985, Infection and immunity.

[35]  H. Hahn,et al.  Influence of different immunoglobulin G preparations on phagocytosis of Pseudomonas aeruginosa by polymorphonuclear granulocytes. , 1985, Zentralblatt fur Bakteriologie, Mikrobiologie, und Hygiene. Series A, Medical microbiology, infectious diseases, virology, parasitology.

[36]  E. Hewlett,et al.  Pertussis toxin and extracytoplasmic adenylate cyclase as virulence factors of Bordetella pertussis. , 1984, The Journal of infectious diseases.

[37]  M. Rheins,et al.  Scanning electron microscopy of mouse ciliated oviduct and tracheal epithelium infected in vitro with Bordetella pertussis. , 1983, Canadian journal of microbiology.

[38]  J. Eaton,et al.  Phagocyte impotence caused by an invasive bacterial adenylate cyclase. , 1982, Science.

[39]  J. Baseman,et al.  Pathogenesis of infection with Bordetella pertussis in hamster tracheal organ culture. , 1977, The Journal of infectious diseases.

[40]  E. Hewlett,et al.  Pertussis toxin from Bordetella pertussis blocks neutrophil migration and neutrophil-dependent edema in response to inflammation. , 1995, Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas.