Virulence factors and host defenses contributing to Salmonella Typhimurium enterocolitis
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- Franka Schumacher
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1 Diss. ETH No Virulence factors and host defenses contributing to Salmonella Typhimurium enterocolitis A dissertation submitted to the ETH Zurich for the degree of Doctor of Sciences presented by Rina Carmen Käppeli Dipl. Natw. ETH Born August 15th 1979 Citizen of Hornussen (AG) Accepted on the recommendation of Prof. Dr. Wolf-Dietrich Hardt (examiner) Prof. Dr. Annette Oxenius (co-examiner) Prof. Dr. Dirk Bumann (co-examiner) Zurich 2010
2 Summary Gastrointestinal infections caused by Salmonella enterica subspecies I serovar Typhimurium (S. Typhimurium) are worldwide a major health problem. S. Typhimurium causes a self-limiting gut infection in humans and cattle, and bacteria do usually not disseminate beyond the lamina propria and gut associated lymphoid tissues. In contrast, susceptible mice infected with S. Typhimurium come down with a systemic disease but generally do not develop intestinal inflammation due to colonization resistance. Colonization resistance describes the failure of most pathogenic bacteria to colonize the normal murine gut due to the abundant presence of commensal bacteria, called the microbiota, resulting in the inability to cause enteric disease. Work in our laboratory first established that oral pretreatment of mice with a single dose of streptomycin not only leads to efficient S. Typhimurium colonization but also to the development of colitis (Barthel et al., 2003). The emerging inflammation is restricted to the large intestine (mainly cecum and colon are affected). This inflammation displays several criteria of an acute inflammation, which resembles the human infection. Using streptomycinpretreated mice as model for Salmonella colitis allows the analysis of both, host factors (mouse) and the pathogen (S. Typhimurium). In the first part of the thesis, we investigated the role of the S. Typhimurium effector proteins SpvB and SpvC in the induction of inflammation. It has been known that most clinical S. Typhimurium strains harbor spvb and spvc. However, their exact role in the inflammation process remained unclear. We were able to show that spvbc deletion mutants of a type III secretion system 1 (TTSS-1) negative background are attenuated in host cell inflammation 3 days post infection. Furthermore, SpvB was essential for efficient lamina propria colonization. S. Typhimurium lacking TTSS-1 needs to transit the epithelium in a dendritic cell-dependent manner and thereby re-localizes from CD11c + to CD11c - cells. We were able to show that this translocation depends partially on functional SpvB and SpvC. Hence, SpvB and SpvC play an important role in the TTSS-1 independent establishment of cecal inflammation by probably mediating the CD11c + to CD11c - cell translocation in the host. In the second part of the thesis, we studied bacteria, which might play a role in providing colonization resistance to the host. We were able to show that mice which have high intrinsic 9
3 E. coli densities in the gut microbiota, were more susceptible to S. enterica infection without streptomycin-pretreatment of mice. Moreover, the higher the intrinsic Lactobacilli titers were, the better a closely related Lactobacillus reuteri RR strain was able to colonize. These data suggest that closely related species increase the chance for colonization of incoming species. This might allow identifying highly susceptible individuals. In the third part of the thesis, we investigated the role of a newly found antimicrobial peptide called RegIIIβ. It is well known, that the inflamed gut offers altered conditions to the microbiota including a diverse nutrient supply or antimicrobial compounds released by the inflamed tissue which may be detrimental for the microbiota but not for the pathogen. We could show that RegIIIβ is upregulated in an inflamed gut and kills selectively various commensal bacterial species but not S. Typhimurium. Moreover, mice fed with daily RegIIIβ doses showed prolonged S. Typhimurium colonization. Thus it is tempting to speculate that upregulation of RegIIIβ results in killing of the microbiota and that this might allow S. Typhimurium to colonize the gut lumen efficiently. In conclusion, the presented work provides new insights into the host-pathogen interactions in the murine model of Salmonella diarrhea at the level of the pathogen virulence factors, the microbial gut ecosystem and the mucosal immune responses. However, the efficient infection of hosts by Salmonella spp. is a highly complex process, which needs further investigation to fully understand all the ongoing steps and underlying mechanisms. 10
4 Zusammenfassung Gastrointestinale Erkrankungen, welche durch Salmonella enterica subspecies I serovar Typhimurium (S. Typhimurium) hervorgerufen werden, stellen ein weltweites Gesundheitsproblem dar. S. Typhimurium führt meistens zu selbstlimitierenden Infektionen in Menschen und Tieren, da die Bakterien sich normalerweise nicht weiter als bis zur Lamina propria und den Lymphgeweben des Darmes verbreiten. Im Gegensatz dazu zeigen empfindliche Mäuse, welche mit S. Typhimurium infiziert werden eine systemische Erkrankung, welche aber, wegen der Kolonisierung-Resistenz, selten zur Darmentzündung führt. Mit Kolonisierungs-Resistenz wird das Scheitern der Besiedelung des gewöhnlichen Mausdarms durch die meisten pathogenen Bakterien beschrieben, die eine enterische Erkrankung hervorrufen können. Diese Resistenz kommt durch die hohe Anzahl an kommensalen Bakterien, den Mikrobiota, zustande. Unser Labor etablierte eine Methode, in der eine einzelne orale Gabe von Streptomycin nicht nur zu einer effizienten S. Typhimurium Kolonisierung sondern auch der Entwicklung einer Colitis führt. Die resultierende Entzündung beschränkt sich auf den Dickdarm (vor allem Blinddarm und Kolon sind betroffen). Diese Entzündung im Mausdarm zeigt viele Faktoren einer akuten Entzündung welche im Menschen vorkommt. Das Streptomycin Mausmodell also Modell für eine Salmonellen Colitis erlaubt die Analyse von Faktoren des Wirtes ( der Maus) wie auch des Pathogens (S. Typhimurium). Im ersten Teil der Arbeit wurde die Rolle der S. Typhimurium Effektorproteine SpvB und SpvC in der Entzündungsreaktion untersucht. Es ist bekannt, dass die meisten S. Typhimurium Stämme die Gene spvb und spvc besitzen; ihre genaue Funktion ist aber unklar. Wir konnten zeigen, dass spvbc Deletionsmutanten welche sich in einem Typ III Sekretionssystem 1 (TTSS-1) negativen Hintergrund befanden am Tag 3 nach Infektion eine abgeschwächte Entzündung hervorrufen. Weiter haben wir festgestellt, dass SpvB für eine effektive Lamina propria Kolonisierung essentiell ist. S. Typhimurium welcher das TTSS-1 fehlt, ist bei der Durchquerung des Epitheliums auf Dendritische Zellen angewiesen und wechselt dabei von CD11c + in CD11c - Zellen. Wir konnten zeigen, dass diese Translokation teilweise von funktionellen spvb und spvc Genen abhängt. Demzufolge kann gefolgert werden, dass SpvB und SpvC eine wichtige Rolle im Etablieren einer TTSS-1 unabhängigen 11
5 Entzündung spielen, wahrscheinlich durch die Vermittlung der Zell Translokation von CD11c + in CD11c - Zellen des Wirtes. Im zweiten Teil der vorliegenden Arbeit, wurden Bakterien untersucht, welche wahrscheinlich eine Rolle in der Vermittlung der Kolonisierungsresistenz des Wirtes spielen. Wir konnten zeigen, dass Mäuse, welche hohe intrinsische E. coli Dichten in der Darm- Mikrobiota aufwiesen, anfälliger auf S. enterica Infektionen ohne Streptomycin Vorbehandlung der Mäuse waren. Des Weiteren korrelierten hohe intrinsische Laktobazillen Titer mit einer guten Kolonisierung des verwandten Stammes Lactobacillus reuteri RR. Diese Daten deuten darauf hin, dass nah verwandte Spezies die Chancen der Kolonisierung einer neuen Art erhöhen. Dies erlaubt unter Umständen die Identifizierung von stark gefährdeten Individuen. Im dritten Teil der These haben wir die Rolle eines neugefundenen antimikrobiellen Peptides namens RegIIIβ untersucht. Es ist bereits bekannt, dass der entzündete Darm die Mikrobiota vor veränderte Bedingungen stellt. So kann es beispielsweise zu einem veränderten Nahrungsangebot oder aber zu antimikrobiellen Stoffen kommen, welche vom entzündeten Gewebe sekretiert werden und für die Mikrobiota tödlich sein können, nicht aber für das Pathogen. Wir konnten zeigen, dass RegIIIβ in einem entzündeten Darm auf reguliert ist und selektiv diverse kommensalen Bakterien tötet, nicht aber S. Typhimurium. Außerdem zeigen Mäuse welche mit täglichen RegIIIβ Dosen gefüttert werden verlängerte S. Typhimurium Kolonisierung im Darm. Daraus folgern wir, dass das Hochregulieren von RegIIIβ einen Teil der Mikrobiota tötet und dadurch S. Typhimurium erlaubt effizient den Darm zu kolonisieren. Zusammenfassend lässt sich feststellen, dass die vorgelegte Arbeit neue Erkenntnisse in der Wirt-Pathogen Interaktion im Mausmodell für Salmonellosen auf der Ebene der Virulenzfaktoren des Pathogens, des mikrobiellen Darmökosystems und der mukosalen Immunantwort aufzeigt. Die effiziente Infektion eines Wirtes durch Salmonellen ist aber ein hoch komplexer Prozess, welcher weiterer Untersuchungen bedarf, um die ablaufenden Prozesse und die zugrunde liegenden Mechanismen ganz verstehen zu können. 12
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