Bordetella spp. block eosinophil recruitment to suppress the generation of early mucosal protection
Nicholas J. First,
Katelyn M. Parrish,
Amparo Martínez-Pérez,
África González-Fernández,
Sushma Bharrhan,
Matthew Woolard,
James B. McLachlan,
Rona S. Scott,
Jian Wang,
Monica C. Gestal
Affiliations
Nicholas J. First
Department of Microbiology and Immunology, Louisiana State University Health Sciences Center at Shreveport, Shreveport, LA 71106, USA
Katelyn M. Parrish
Department of Microbiology and Immunology, Louisiana State University Health Sciences Center at Shreveport, Shreveport, LA 71106, USA
Amparo Martínez-Pérez
CINBIO, Universidade de Vigo, Immunology Group, Instituto de Investigación Sanitaria Galicia Sur (IIS Galicia Sur), SERGAS-UVIGO, 36310 Vigo, Galicia, Spain
África González-Fernández
CINBIO, Universidade de Vigo, Immunology Group, Instituto de Investigación Sanitaria Galicia Sur (IIS Galicia Sur), SERGAS-UVIGO, 36310 Vigo, Galicia, Spain
Sushma Bharrhan
Department of Microbiology and Immunology, Louisiana State University Health Sciences Center at Shreveport, Shreveport, LA 71106, USA; Immunophenotyping Core, Center for Applied Immunology and Pathological Processes, Department of Microbiology and Immunology, Louisiana State University Health Sciences Center at Shreveport, Shreveport, LA 71106, USA
Matthew Woolard
Department of Microbiology and Immunology, Louisiana State University Health Sciences Center at Shreveport, Shreveport, LA 71106, USA; Immunophenotyping Core, Center for Applied Immunology and Pathological Processes, Department of Microbiology and Immunology, Louisiana State University Health Sciences Center at Shreveport, Shreveport, LA 71106, USA
James B. McLachlan
Department of Microbiology and Immunology, Tulane University School of Medicine, New Orleans, LA 70112, USA
Rona S. Scott
Department of Microbiology and Immunology, Louisiana State University Health Sciences Center at Shreveport, Shreveport, LA 71106, USA; Bioinformatics and Modeling Core, Center for Applied Immunology and Pathological Processes, Department of Microbiology and Immunology, Louisiana State University Health Sciences Center at Shreveport, Shreveport, LA 71106, USA
Jian Wang
Department of Microbiology and Immunology, Louisiana State University Health Sciences Center at Shreveport, Shreveport, LA 71106, USA; Bioinformatics and Modeling Core, Center for Applied Immunology and Pathological Processes, Department of Microbiology and Immunology, Louisiana State University Health Sciences Center at Shreveport, Shreveport, LA 71106, USA
Monica C. Gestal
Department of Microbiology and Immunology, Louisiana State University Health Sciences Center at Shreveport, Shreveport, LA 71106, USA; Corresponding author
Summary: Bordetella spp. are respiratory pathogens equipped with immune evasion mechanisms. We previously characterized a Bordetella bronchiseptica mutant (RB50ΔbtrS) that fails to suppress host responses, leading to rapid clearance and long-lasting immunity against reinfection. This work revealed eosinophils as an exclusive requirement for RB50ΔbtrS clearance. We also show that RB50ΔbtrS promotes eosinophil-mediated B/T cell recruitment and inducible bronchus-associated lymphoid tissue (iBALT) formation, with eosinophils being present throughout iBALT for Th17 and immunoglobulin A (IgA) responses. Finally, we provide evidence that XCL1 is critical for iBALT formation but not maintenance, proposing a novel role for eosinophils as facilitators of adaptive immunity against B. bronchiseptica. RB50ΔbtrS being incapable of suppressing eosinophil effector functions illuminates active, bacterial targeting of eosinophils to achieve successful persistence and reinfection. Overall, our discoveries contribute to understanding cellular mechanisms for use in future vaccines and therapies against Bordetella spp. and extension to other mucosal pathogens.
