Investigating SipA-dependent Salmonella Typhimurium invasion in vitro
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1 Research Collection Doctoral Thesis Investigating SipA-dependent Salmonella Typhimurium invasion in vitro Author(s): Andritschke, Daniel Publication Date: 2015 Permanent Link: This page was generated automatically upon download from the ETH Zurich Research Collection. For more information please consult the Terms of use. ETH Library
2 Diss. ETH No Investigating SipA-dependent Salmonella Typhimurium invasion in vitro A thesis submitted to attain the degree of DOCTOR OF SCIENCES of ETH ZURICH (Dr. sc. ETH Zurich) presented by DANIEL ANDRITSCHKE M.Sc., Universität Zurich born January 3 rd 1987 Citizen of Germany Accepted on the recommendation of Prof. Dr. Wolf-Dietrich Hardt (examiner) Prof. Dr. Urs Greber (co-examiner) Prof. Dr. Jason Mercer (co-examiner) 2015
3 SUMMARY Salmonella enterica subspecies enterica serovar Typhimurium (S. Tm) is an enteroinvasive bacterial pathogen that represents a global health risk and one of the leading causes for human gastroenteritis. Infections occur via the oral route through ingestion of contaminated food or water. The invasion of gut epithelial cells plays a central role in the infection cycle of S. Tm. Common symptoms include diarrhea, nausea, vomiting and abdominal pain. Infections in healthy people are mostly self-limiting, but can be life-threatening for infants, elderly and immunocompromised patients. Because of the readily available tools available to genetically manipulate S. Tm, it has become a model organism for invasive bacteria. In order to improve therapies against Salmonella ssp. and other pathogenic bacterial pathogens, it is of high importance to gain detailed understanding of their infection processes. S. Tm has evolved sophisticated infection mechanisms. It employs two type three secretion systems (TTSS), TTSS-1 and TTSS-2, which inject a cocktail of effector proteins into host cells to induce internalization and establish a replicative niche, respectively. These bacterial effectors deregulate endogenous host cell mechanisms and S. Tm exploits them for its own advantage. Essential effectors required for internalization are SipA, SopE, SopE2 and SopB. They directly or indirectly induce actin polymerization leading to pronounced membrane ruffles at the site of infection. A number of interacting host cell factors are known for these effectors. However, comprehensive knowledge about molecular mechanisms is needed to fully understand the process of infection. In this work, we set out to decipher these ill-defined mechanisms. Using a combination of quantitative approaches like high-content RNAi screening, modelling and bioinformatics and qualitative cell biological methods, we investigated SipA-mediated Salmonella Typhimurium infection in an in vitro cell culture model. This type of invasion has been previously described to be morphologically distinct from wild type and SopE-mediated S. Tm infection processes and could potentially add important details to the understanding of SipA-driven molecular processes. 1
4 Chapter II describes the integration of a formerly performed genome wide sirna screen on S.Tm SipA (a strain lacking SopE, SopE2 and SopB, only driving invasion using SipA) into an analysis pipeline of the InfectX consortium aiming to explore the infectome of invasive bacteria and viruses. By reanalyzing this screen and functionally clustering hits we were able to pinpoint actin polymerization processes involved in this type of invasion. We found that, despite the morphological differences between SipA- and SopE-mediated invasion, similar parallel host cell mechanisms are involved. These differ in their degree of dependency from the SopE-type of S. Tm invasion. In contrast to S. Tm SopE, SipA-driven infection seems to employ the nucleation promoting factor WAVE2 to activate the same downstream actin nucleators to enter host cells. Additionally, it might use a second route of actin polymerization, exploiting proteins of the SPIRE family of actin nucleators. Because of the equally organized setup of our RNAi screening platform within the InfectX consortium, it was possible to tackle the profound problem of off-target effects in highcontent sirna screens of different pathogens. In collaboration with bioinformaticians in the consortium, we found mirna-like seed regions in our sets of sirnas that reproducibly changed infection phenotypes. Therefore, we attributed off-targets to this effect. Additionally, through another collaboration with modelers in the consortium it was possible to reconstruct single sirna phenotypes by predicting their potential to induce on- or off-target effects. This improved the interpretation of screening results. Our findings show that RNAi screens are great tools to uncover novel pathways and, in combination with different modelling approaches, can pave the way to better understand the interplay between host cells and pathogens. 2
5 ZUSAMMENFASSUNG Salmonella Typhimurium (S. Tm) ist ein enteroinvasives, bakterielles Pathogen dass ein globales Gesundheitsrisiko darstellt und zu den Hauptverursachern für Gastroenteritis zählt. Infektionen erfolgen durch Schlucken von kontaminiertem Wasser oder Nahrung. Die Invasion von Darmepithelzellen spielt eine zentrale Role im Infektionszyklus von S. Tm. Zu den allgemein auftretenden Symptomen zählen Durchfall, Übelkeit, Erbrechen und Bauchschmerzen. Infektionen in gesunden Patienten sind meist selbst limitierend. In sehr jungen, alten und immunsupprimierten Menschen können diese jedoch lebensbedrohlich werden. Aufgrund der verfügbaren Möglichkeiten S. Tm genetisch zu verändern, hat es sich zu einem Modellorganismus für invasive Bakterien entwickelt. Um Therapien gegen Salmonellen ssp. und andere pathogene Bakterien zu verbessern ist es wichtig detailliertes Verständnis des Infektionsprozesses zu erlangen. Salmonella Typhimurium benutzt ausgeklügelte Infektionsmechanismen. Mit Hilfe von zwei Typ 3 Sekretionssystemen (TTSS), TTSS-1 und TTSS-2, die ein Gemisch an Effektorproteinen in Wirtszellen injizieren, wird die Aufnahme von S. Tm induziert und eine Nische zur Replikation zur gebildet. Diese bakteriellen Effektoren deregulieren endogene Wirtszellmechanismen. SipA, SopE, SopE2 und SopB sind essentielle Effektorproteine für die Aufnahme in Wirtszellen. Diese Proteine induzieren, direkt oder indirekt, die Polymerisation von Aktin, welche zu ausgeprägten Membranausstülpungen um Infektionsstellen führt. Einige Interaktionen dieser Effektoren mit Wirtszellen sind bereits bekannt. Um den ganzen Prozess vollkommen zu verstehen ist jedoch mehr Wissen über die molekularen Mechanismen nötig. In dieser Arbeit versuchen wir die nicht ausreichend bekannten Mechanismen zu entschlüsseln. Wir untersuchen SipA-abhängige S. Tm Invasion mit einer Kombination aus Modellierung-, Bioinformatik-, Zellbiologie- und Screening-Experimenten in einem in vitro Zellkulturmodel. Kürzlich wurde gezeigt, dass SipA-Invasion sich morphologisch von Wildtyp und SopE-Invasion unterscheidet. Wir können aus unseren Versuchen Schlüsse daraus ziehen wie SipA-abhängige molekulare Prozesse ablaufen. In Abschnitt II wird die Integration des Datensatzes eines früheren Genom-weiten sirna Experimentes an S. Tm SipA in einen Analysekanal des InfectX Konsortiums beschrieben. Dieses 3
6 Konsortium wurde initiiert um das Infektom von invasiven Bakterien und Viren zu entschlüsseln. Durch die Reanalyse des Screen und unter Verwendung einer funktioneller Häufungsanalyse der Ergebnisse ist es uns gelungen, Prozesse der Aktinpolymerisation zu finden die im Infektionsprozess involviert sind. Trotz der morphologischen Unterschiede zwischen SipA und SopE-vermittelter Invasion spielen vergleichbare Mechanismen in beiden Invasionsformen eine Rolle. Der Unterschied zwischen den Invasionformen besteht hier im Wesentlichen im Grad der Beteiligung der Wirtsproteine. SipA-induzierte Invasion hängt stark vom Nukleations-treibenden Faktor WAVE2 ab. Dieser wiederrum aktiviert die gleichen Aktin Nukleatoren die auch in SopE-abhängiger Invasion gebraucht werden. Zusätzlich wird vermutlich noch eine zweite Route, die SPIRE Proteine beinhaltet, genutzt um Aktin zu polymerisieren. Aufgrund des vergleichbaren Aufbaus der RNAi Screening Plattformen im InfectX Konsortium war es möglich das ausgeprägte Problem von Off-Target-Effekten in diesen Experimenten zu untersuchen. In Kollaboration mit Bioinformatikern des Konsortiums haben wir micrornaähnliche "Seed"-Regionen in unserer sirna Sammlung gefunden. Diese beeinflussen unsere Phänotypen reproduzierbar und nachhaltig. Durch eine weitere Kollaboration im Konsortium war es möglich Phänotypen einzelner sirna zu rekonstruieren. Dies wurde durch Modelvoraussagen ihrer "On-" und "Off-Target" Effekte erreicht und verbesserte die Interpretation von Screening Resultaten merklich. Unsere Ergebnisse zeigen dass RNAi Screens sehr gute Werkzeuge darstellen um bisher unbekannte Signalwege aufzudecken und, in Kombination mit verschiedenen Modellansätzen, zukünftig den Weg zu einem besseren Verständnis des Zusammenspiels zwischen Wirtszellen und Pathogenen zu ebnen. 4
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