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Int. J. Mol. Sci. 2018, 19(9), 2602; https://doi.org/10.3390/ijms19092602

Respiratory Bordetella bronchiseptica Carriage is Associated with Broad Phenotypic Alterations of Peripheral CD4+CD25+ T Cells and Differentially Affects Immune Responses to Secondary Non-Infectious and Infectious Stimuli in Mice

1
Infection Immunology Group, Institute of Medical Microbiology, Infection Control and Prevention, Health Campus Immunology, Infectiology and Inflammation, Otto-von-Guericke University Magdeburg, 39120 Magdeburg, Germany
2
Immune Regulation Group, Helmholtz Centre for Infection Research, 38124 Braunschweig, Germany
3
Department of Vaccinology and Applied Microbiology, Helmholtz Centre for Infection Research, 38124 Braunschweig, Germany
4
Genome Analytics Group, Helmholtz Centre for Infection Research, 38124 Braunschweig, Germany
5
Experimental Pneumology, University Hospital for Pneumology, Health Campus Immunology, Infectiology and Inflammation, Otto-von-Guericke University Magdeburg, 39120 Magdeburg, Germany
These authors contributed equally.
These authors contributed equally.
§
Current address Department of Gastroenterology, Hepatology and Endocrinology, Hannover Medical School, Hannover, Germany
*
Author to whom correspondence should be addressed.
Received: 30 May 2018 / Revised: 3 August 2018 / Accepted: 28 August 2018 / Published: 1 September 2018
(This article belongs to the Special Issue Host-Microbe Interaction 2018)
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Abstract

The respiratory tract is constantly exposed to the environment and displays a favorable niche for colonizing microorganisms. However, the effects of respiratory bacterial carriage on the immune system and its implications for secondary responses remain largely unclear. We have employed respiratory carriage with Bordetella bronchiseptica as the underlying model to comprehensively address effects on subsequent immune responses. Carriage was associated with the stimulation of Bordetella-specific CD4+, CD8+, and CD4+CD25+Foxp3+ T cell responses, and broad transcriptional activation was observed in CD4+CD25+ T cells. Importantly, transfer of leukocytes from carriers to acutely B. bronchiseptica infected mice, resulted in a significantly increased bacterial burden in the recipient’s upper respiratory tract. In contrast, we found that respiratory B. bronchiseptica carriage resulted in a significant benefit for the host in systemic infection with Listeria monocytogenes. Adaptive responses to vaccination and influenza A virus infection, were unaffected by B. bronchiseptica carriage. These data showed that there were significant immune modulatory processes triggered by B. bronchiseptica carriage, that differentially affect subsequent immune responses. Therefore, our results demonstrated the complexity of immune regulation induced by respiratory bacterial carriage, which can be beneficial or detrimental to the host, depending on the pathogen and the considered compartment. View Full-Text
Keywords: respiratory microbial carriage; polymicrobial interactions; respiratory immune regulation; secondary infections; vaccination; regulatory T cells; influenza A virus; Bordetella bronchiseptica; Listeria monocytogenes respiratory microbial carriage; polymicrobial interactions; respiratory immune regulation; secondary infections; vaccination; regulatory T cells; influenza A virus; Bordetella bronchiseptica; Listeria monocytogenes
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Jeron, A.; Boehme, J.D.; Volckmar, J.; Gereke, M.; Yevsa, T.; Geffers, R.; Guzmán, C.A.; Schreiber, J.; Stegemann-Koniszewski, S.; Bruder, D. Respiratory Bordetella bronchiseptica Carriage is Associated with Broad Phenotypic Alterations of Peripheral CD4+CD25+ T Cells and Differentially Affects Immune Responses to Secondary Non-Infectious and Infectious Stimuli in Mice. Int. J. Mol. Sci. 2018, 19, 2602.

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