Interactions of Streptococcus suis with primary porcine respiratory cells co-infected with Bordetella bronchiseptica
Parasitology and Biology of Tropical Infectious Disease Pathogens
Final Report Abstract
Respiratory diseases are a major problem in pig breeding and fattening as they cause serious health issues for the animals and high economic losses for the pig industry. The pathogenesis of respiratory diseases is very complex because not only infectious agents, but also environmental factors are involved (“Porcine Respiratory Disease Complex”, PRDC). It is generally accepted that obligatory pathogenic agents (“keystone pathogens”), which are mainly viruses, pave the way for infection with secondary (opportunistic) bacterial pathogens by increasing bacterial attachment or colonization, disrupting the respiratory epithelial barrier, or modulating the host’s immune response. Streptococcus suis is a “pathobiont” in the porcine respiratory tract – on the one hand it is a frequent and innocuous colonizer of the upper porcine respiratory tract but on the other hand it can cause life-threatening disease once it has overcome the respiratory epithelial barrier. In a previous study (first funding period), we demonstrated that swine influenza virus (SIV) promotes infection with S. suis by impairment of the mucociliary defense mechanisms and facilitation of streptococcal adherence and colonization. Notably, the bacterial pathogen Bordetella bronchiseptica has similar detrimental effects on the ciliated respiratory epithelium as we have seen it for SIV. Several studies demonstrated that B. bronchiseptica can predispose to infection with other respiratory pathogens. Thus, in this project, we wanted to investigate whether B. bronchiseptica can also promote infection with S. suis and how in particular the pore-forming toxin suilysin (SLY) might contribute to these bacterial-bacterial-host cell interactions. In accordance with the previous studies, we used porcine precision-cut lung slices (PCLS) and air-liquid interface (ALI) cultures with primary porcine respiratory epithelial cells to study the pathogen-host interactions in more detail. Our major findings were that (I) B. bronchiseptica reduces the ciliary activity and disrupts the respiratory epithelial barrier, (II) B. bronchiseptica promotes infection with S. suis by enhancing the colonization capacity of S. suis and the cytotoxic effects of SLY, and that (III) B. bronchiseptica affects the host’s pro-inflammatory response. Additionally, we found that (IV) SLY plays an important role in expression of cyclooxygenase-2 (COX-2), an enzyme involved in immune activation and inflammation modulation, during infection of PCLS with S. suis. Thus, our findings demonstrate that the bacterial pathogen B. bronchiseptica is able to pave the way for S. suis infection, though the cytotoxicity of S. suis is strictly dependent on the presence of SLY. In addition, analysis of the host’s inflammatory response revealed insights into the complex interactions during bacterial co-infection of porcine respiratory epithelial cells.
Publications
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Bordetella bronchiseptica promotes adherence, colonization, and cytotoxicity of Streptococcus suis in a porcine precision-cut lung slice model. Virulence, 12(1), 84-95.
Vötsch, Désirée; Willenborg, Maren; Baumgärtner, Wolfgang; Rohde, Manfred & Valentin-Weigand, Peter
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“Coinfection of a porcine precision-cut lung slice model with Bordetella bronchiseptica and Streptococcus suis”; International Symposium on Zoonoses Research 2020
Vötsch, D.; Willenborg, M.; Baumgärtner, W.; Rohde, M. & Valentin-Weigand, P.
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Streptococcus suis Induces Expression of Cyclooxygenase-2 in Porcine Lung Tissue. Microorganisms, 9(2), 366.
Dresen, Muriel; Schenk, Josephine; Berhanu, Weldearegay Yenehiwot; Vötsch, Désirée; Baumgärtner, Wolfgang; Valentin-Weigand, Peter & Nerlich, Andreas
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“Coinfection of a porcine precision-cut lung slice model with Bordetella bronchiseptica and Streptococcus suis”; World Microbe Forum 2021
Vötsch, D.; Valentin-Weigand, P.; Willenborg, M.; Baumgärtner, W. & Rohde, M.
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“The role of the dermonecrotic toxin of Bordetella bronchiseptica in infection of porcine respiratory epithelial cells”; Junior Scientist Zoonoses Meeting 2021
Vötsch, D.; Baumgärtner, W.; Brockmeier, S. L. & Valentin-Weigand, P.
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„Co- Infektion von porzinen Präzisionslungenschnitten mit Bordetella bronchiseptica und Streptococcus suis“; Tagung der DVG-Fachgruppe Bakteriologie und Mykologie 2021
Vötsch, D.; Willenborg, M.; Baumgärtner, W.; Rohde, M. & Valentin-Weigand, P.
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„Streptococcus suis Induces Expression of Cyclooxygenase- 2 in Porcine Lung Tissue”; International Symposium on Zoonoses Research 2021
Dresen, M.; Schenk, J.; Weldearegay, B. Y.; Vötsch, D.; Baumgartner, W.; Valentin-Weigand, P. & Nerlich, A.
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„Porcine Respiratory Disease Complex – Bordetella bronchiseptica als Wegbereiter für Streptococcus suis”; Tagung der DVG-Fachgruppe Schweinekrankheiten 2022
Schaaf, D.; Willenborg, M.; Baumgärtner, W.; Rohde, M. & Valentin-Weigand, P.
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„Bordetella bronchiseptica paves the way for Streptococcus suis infection in a Porcine Precision-Cut Lung Slice Model”, 5th German Pneumococcal and Streptococcal Symposium 2023
Schaaf, D.; Willenborg, M.; Baumgärtner, W.; Rohde, M. & Valentin-Weigand, P.
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„Die Rolle des dermonekrotischen Toxins von Bordetella bronchiseptica in Monound Co-Infektionen des porzinen Respirationstraktes“; Tagung der DVG-Fachgruppe Bakteriologie und Mykologie 2023
Schaaf, D.; Weldearegay, B. Y.; Baumgärtner, W.; Brockmeier, S. L. & Valentin-Weigand, P.
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“Microbial interactions in the porcine respiratory tract”; United Microbiology Symposium Hannover 2024
Schaaf, D.
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„In vitro-Untersuchungen zu Erregern des ‚Porcine Respiratory Disease Complex‘“, 54. Tagung des Arbeitskreises Tiergarten 2024
Schaaf, D. & Spriewald, R.
