Research Collection. The role of type I interferon signaling on T cells during acute viral infections. Doctoral Thesis.
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1 Research Collection Doctoral Thesis The role of type I interferon signaling on T cells during acute viral infections Author(s): Crouse, Joshua Mark Publication Date: 2014 Permanent Link: Rights / License: In Copyright - Non-Commercial Use Permitted 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 The role of type I interferon signaling on T cells during acute viral infections A thesis submitted to attain the degree of DOCTOR OF SCIENCES OF ETH ZURICH (DR. SC. ETH ZURICH) presented by JOSHUA MARK CROUSE MSc ETH, ETH Zurich born on citizen of USA accepted on the recommendation of Prof. Dr. Annette Oxenius (examiner) Prof. Dr. Antonio Lanzavecchia (co-examiner) Prof. Dr. Dietmar Zehn (co-examiner) 2014
3 1.1 Summary The proper activation and establishment of a T cell response is important for the clearance of intracellular pathogens, such as viruses. Activation of T cells requires the coordinated effort of multiple signals. Of great importance for the full activation and proper expansion of T cells are the signal three cytokines. These secreted cytokines, such as IL-12 and type I interferons (IFN) can signal directly on activated T cells to ensure appropriate development of an effector T cell response. Viral infections often trigger robust type I IFN production, which plays a key role in the establishment of an innate anti-viral state as well as serving as a signal three cytokine. This thesis describes the role of type I IFN signaling directly on T cells during an acute infection associated with high levels of type I IFNs. In a first part, the role of type I IFN signaling on T cell differentiation was examined and an important role for type I IFNs in the differentiation of effector T cells was delineated. T cells lacking the ability to sense type I IFNs (IFNAR -/- ) fail to differentiate into short lived effector cells (SLEC) but retain the ability to differentiate into memory precursor effector cells and to form a fully functional memory cell population. Mechanistically direct type I IFN signaling on T cells was shown to drive the upregulation of the fate determining transcription factor T-bet, thereby revealing a connection between type I IFN signaling and the regulation of T cell differentiation. In a second part, we demonstrate that the curtailed expansion of IFNAR -/- T cells following an infection associated with high levels of type I IFNs is in part due to natural killer (NK) cell mediated killing of T cells lacking the ability to sense type I IFNs. We show that the inability of T cells to sense type I IFNs results in increased expression of NK cell activating ligands, with a dominant role of activating ligands for natural cytotoxicity triggering receptor 1 (NCR1). Recognition of IFNAR -/- T cells by NCR1 leads to perforin mediated killing of these T cells. These findings expand on our current knowledge of NK cell function and demonstrate a possible immunoregulatory role for NK cells. Importantly, these findings reveal an important role of type I IFNs in the protection of early activated T cells, demonstrating the multifaceted role of type I IFNs during viral infections where they are involved in both the initial innate response and in establishing a proper T cell response. 2
4 1.2 Zusammenfassung Die vollständige Aktivierung und Erzeugung einer T-Zell Antwort ist wichtig für die Bekämpfung von intrazellulären Pathogenen wie Viren. Die effiziente Aktivierung von T- Zellen erfordert den koordinierten Einsatz dreier Signale. Von grosser Bedeutung für die vollständige Aktivierung und Vermehrung von T-Zellen sind Zytokine, die das dritte Signal ausmachen. Diese sekretierten Zytokine, wie IL-12 und Typ I Interferone (IFN), können direkt auf aktivierte T-Zellen wirken, um die Ausbildung einer vollständigen Effektor T-Zell Antwort sicher zu stellen. Viele virale Infektionen induzieren eine starke Typ I IFN Antwort, welche eine wichtige Rolle spielen bei der Etablierung eines angeborenen antiviralen Zustands und auch als Signal drei Zytokin wirken. Diese Dissertation beschreibt die Rolle von Typ I IFN und deren direkte Wirkung auf T-Zellen während einer akuten Virusinfektion, die durch einen hohen Spiegel von Typ I IFN charakterisiert ist. Im ersten Teil dieser Arbeit untersuchen wir die Rolle von Typ I IFN Signalen und deren Auswirkung auf die T-Zell Differenzierung und zeigen damit die zentrale Rolle von Typ I IFN für die Differenzierung von Effektor T-Zellen. Wir zeigen, dass T-Zellen welche Typ I IFN nicht wahrnehmen können (IFNAR -/- ), die Fähigkeit verlieren in kurzlebige Effektor Zellen (SLEC) zu differenzieren, nicht aber die Fähigkeit in Gedächtnis Vorläufer Effektor Zellen (MPEC) zu differenzieren und eine voll funktionale Gedächtnis T-Zell Population zu bilden. Mechanistisch zeigen wir, dass direkte Typ I IFN Signale auf T-Zellen die Hochregulierung des schicksalsbestimmenden Transkriptionsfaktors T-bet induzieren kann. Dabei stellen wir eine Verbindung zwischen Typ I IFN Signalen und der Steuerung der T-Zell Differenzierung dar. Im zweiten Teil dieser Arbeit zeigen wir, dass die eingeschränkte Vermehrung von IFNAR -/- T-Zellen nach einer Virusinfektion, die mit einem hohen Spiegel von Typ I IFN assoziiert ist, zum Teil direkt durch Natürliche Killer Zellen (NK)-vermittelte Eliminierung von T-Zellen gesteuert ist, die Typ I IFN nicht wahrnehmen können. Zusätzlich zeigen wir, dass die Unfähigkeit von T-Zellen Typ I IFN zu erkennen, zu einer erhöhten Expression von NK-Zell aktivierenden Liganden führt. Unsere Arbeit weist auf eine dominante Rolle der NK-Zellaktivierenden Liganden (NCR1 Liganden) in diesem Prozess hin. Die Erkennung von IFNAR - /- T-Zellen durch NCR1 führt zur Perforin-vermittelten Eliminierung dieser T-Zellen. Unsere Ergebnisse erweitern die aktuellen Kenntnisse der NK-Zell-Funktion und deuten auf eine mögliche immunregulatorische Rolle von NK-Zellen hin. Wichtig ist, dass diese Ergebnisse eine bedeutende Rolle von Typ I IFN im Schutz von aktivierten T-Zellen zeigen. Zusammen 3
5 beweisen die Resultate die vielfältige Rolle von Typ I IFN während einer Virusinfektion, wo Typ I IFN nicht nur zu Beginn der angeborenen Antwort wichtig ist, sondern auch bei der Entwicklung einer effektiven T-Zellantwort. 4
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