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A Live Cell Reporter of Human Adenovirus Chromatin Zurich Open Repository and Archive University of Zurich Main Library Strickhofstrasse 39 CH-8057 Zurich www.zora.uzh.ch Year: 2010 A live cell reporter of human adenovirus chromatin Püntener, Daniel Abstract: Die Untersuchung von Viren hat substanziell zur biologischen Revolution im letzten Jahrhun- dert beigetragen. Die Analyse von Virus-Wirt Interaktionen hat viele zelluläre Prinzipien offenbart wie zum Beispiel die Gesetzmässigkeiten von Genen und deren Spleissung. Ein oft benutztes Model- system sind Adenoviren. Dies, weil sie nur beschränkt krankmachend, einfach zu vermehren und gut charakterisiert sind. Trotzdem sind die zugrundeliegenden zellulären Mechanismen, welche eine Infektion ermöglichen, immer noch nicht gut verstanden. Insbesondere Prozesse die zum Abbau viraler Kapside während des Imports führen und wie Viren die Zelle verlassen, war bisher schwierig zu untersuchen. In dieser Arbeit haben wir das Chromatin eines humanen Adenovirus fluoreszent markiert, indem wir das Protein V gegen das fluoreszierende Fusionsprotein GFP-pV ausgetauscht haben, ohne dabei andere vi- rale Gene zu zerstören. Dieses Virus, genannt Ad2-GFP-pV, durchlief den vollen Replikationszyklus und erlaubte es uns daher, viralen Transport und Freisetzung von Viren am Ende des Zyklus zu untersuchen. Wir konnten zeigen, dass während des Eintritts des Kapsids in die Zellen das GFP-pV in zwei Schritten dissoziiert. Innerhalb von 30 Minuten wurden 65% vom GFP-pV ins Zytosol abgegeben und nach 90 Minuten das restliche Protein. Der zweite Schritt war dabei abhängig von einer Interaktion der Viren mit dem Zellkern. Im Weiteren ist es uns gelungen, zum ersten Mal die Dynamik der Virenfreisetzung am Ende des viralen Replikationszykluses zu bestimmen. Wir konnten zeigen, dass dieser Prozess anisotrop ist und in zwei Schritten geschieht. Einem Zerfall der Kernmembran folgt die Lyse der Plasmamembran. Zusammenfassend konnten wir zeigen, dass dieses neue Virus ermöglicht, den vollständigen Replikation- szyklus von Adenoviren zu untersuchen. Es hat das Potential, Echtzeituntersuchungen von Infektionen und deren Ausbreitung in Organismen zu machen oder als diagnostisches Virus in der Gentherapie einge- setzt zu werden. SUMMARY Virology has contributed substantially to the biological revolution in the last century. Studying virus-host-interactions has revealed many of the fundamental molecular mech- anisms such as the nature of genes and splicing. Adenoviruses have received intense attention in this regard as they are of low pathogenicity, easy to grow and rather well characterized. Still, biological mechanisms enabling adenovirus infections are not completely understood. In particular, processes that lead to disassembly of viral particles during entry as well as release of newly synthesized particles upon cell lysis at the end of the viral replication cycle have been difficult to address. Here we generated a novel human adenovirus with fluorescently tagged chromatin by replacing protein V by GFP-pV while keeping all the other viral genes intact. This virus, named Ad2-GFP-pV, completed the full replication cycle and therefore allowed us to study transport of incoming viral cores as well as viral egress from infected cells. We showed that the viral core component GFP-pV is released from Ad2-GFP- pV during entry and disassembly in two distinct steps. A fast one within 30 min where about 65% of GFP-pV is released and a slower up to 90 min pi leading to full dissociation of GFP-pV from viral particles. The full dissociation is dependent on an interaction of the incoming virus with the nucleus. Using this virus we were also able for the first time to visualize dynamics of viral egress upon cell lysis. We observed that this process is nonisotropic and occurs in two morphologically distinct steps, nuclear disintegration preceding lysis of the plasma membrane. Taken together we showed that this new virus is suitable to study the whole viral replication cycle and thus might prove useful for live analyses of viral infection and spreading in organisms, as well as for applications in gene therapy. Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-83950 Dissertation Published Version Originally published at: Püntener, Daniel. A live cell reporter of human adenovirus chromatin. 2010, University of Zurich, Faculty of Science. 2 A Live Cell Reporter of Human Adenovirus Chromatin Dissertation zur Erlangung der naturwissenschaftlichen Doktorwürde (Dr. sc. nat.) vorgelegt der Mathematisch-naturwissenschaftlichen Fakultät der Universität Zürich von Daniel Püntener von Erstfeld UR Promotionskomitee: Prof. Dr. Urs F. Greber (Vorsitz, Leitung der Dissertation) Prof. Dr. Michael O. Hottiger Prof. Dr. Ulrike Kutay Zürich, 2010 TABLE OF CONTENTS Summary 4 Zusammenfassung 5 Introduction 6 1. What we can learn from viruses 6 1.1 Insights into cellular mechanisms through viral studies 5 1.2 Viruses as pathogens 6 1.3 Viruses as oncogenic agents 7 1.4 Viruses as tools in gene therapy 8 2. Adenoviruses 9 2.1 Adenoviridae 9 2.2 Adenovirus structure and composition 9 3. Viral chromatin 11 3.1 Current model of adenovirus chromatin 11 3.2 Cellular chromatin in viral infections 12 4. Adenovirus life-cycle 14 4.1 Endocytosis and transport to the nucleus 14 4.2 Adenovirus DNA import 15 4.3 Adenovirus replication 18 4.4 Cell lysis and egress 20 5. References 22 Review 25 DNA-tumor virus entry – from plasma membrane to the nucleus 26 Puntener, D. & U.F. Greber. Semin Cell Dev Biol 2009 Results, Manuscript 61 Fluorescent DNA-core dynamics in entry and egress reveals 62 nonisotropic hatching of viruses from infected cell nuclei Daniel Puntener, Martin F. Engelke, Nicola Imelli, Zsolt Ruzsics, Karin Boucke, Corinne Wilhelm and Urs F. Greber. Manuscript submitted to PLoS Pathogens. Conclusions and Final Remarks 120 Acknowledgements 125 Abbreviations 127 Curriculum Vitae 129 3 SUMMARY Virology has contributed substantially to the biological revolution in the last century. Studying virus-host-interactions has revealed many of the fundamental molecular mechanisms such as the nature of genes and splicing. Adenoviruses have received intense attention in this regard as they are of low pathogenicity, easy to grow and rather well characterized. Still, biological mechanisms enabling adenovirus infections are not completely understood. In particular, processes that lead to disassembly of viral particles during entry as well as release of newly synthesized particles upon cell lysis at the end of the viral replication cycle have been difficult to address. Here we generated a novel human adenovirus with fluorescently tagged chromatin by replacing protein V by GFP-pV while keeping all the other viral genes intact. This virus, named Ad2-GFP-pV, completed the full replication cycle and therefore allowed us to study transport of incoming viral cores as well as viral egress from infected cells. We showed that the viral core component GFP-pV is released from Ad2-GFP-pV during entry and disassembly in two distinct steps. A fast one within 30 min where about 65% of GFP-pV is released and a slower up to 90 min pi leading to full dissociation of GFP-pV from viral particles. The full dissociation is dependent on an interaction of the incoming virus with the nucleus. Using this virus we were also able for the first time to visualize dynamics of viral egress upon cell lysis. We observed that this process is nonisotropic and occurs in two morphologically distinct steps, nuclear disintegration preceding lysis of the plasma membrane. Taken together we showed that this new virus is suitable to study the whole viral replication cycle and thus might prove useful for live analyses of viral infection and spreading in organisms, as well as for applications in gene therapy. 4 ZUSAMMENFASSUNG Die Untersuchung von Viren hat substanziell zur biologischen Revolution im letzten Jahrhundert beigetragen. Die Analyse von Virus-Wirt Interaktionen hat viele zelluläre Prinzipien offenbart wie zum Beispiel die Gesetzmässigkeiten von Genen und deren Spleissung. Ein oft benutztes Modelsystem sind Adenoviren. Dies, weil sie nur beschränkt krankmachend, einfach zu vermehren und gut charakterisiert sind. Trotzdem sind die zugrundeliegenden zellulären Mechanismen, welche eine Infektion ermöglichen, immer noch nicht gut verstanden. Insbesondere Prozesse die zum Abbau viraler Kapside während des Imports führen und wie Viren die Zelle verlassen, war bisher schwierig zu untersuchen. In dieser Arbeit haben wir das Chromatin eines humanen Adenovirus fluoreszent markiert, indem wir das Protein V gegen das fluoreszierende Fusionsprotein GFP-pV ausgetauscht haben, ohne dabei andere virale Gene zu zerstören. Dieses Virus, genannt Ad2-GFP-pV, durchlief den vollen Replikationszyklus und erlaubte es uns daher, viralen Transport und Freisetzung von Viren am Ende des Zyklus zu untersuchen. Wir konnten zeigen, dass während des Eintritts des Kapsids in die Zellen das GFP-pV in zwei Schritten dissoziiert. Innerhalb von 30 Minuten wurden 65% vom GFP-pV ins Zytosol abgegeben und nach 90 Minuten das restliche Protein. Der zweite Schritt war dabei abhängig von einer Interaktion der Viren mit dem Zellkern. Im Weiteren ist es uns gelungen, zum ersten Mal die Dynamik der Virenfreisetzung am Ende des viralen Replikationszykluses zu bestimmen. Wir konnten zeigen, dass dieser Prozess anisotrop ist und in zwei Schritten geschieht. Einem Zerfall der Kernmembran folgt die Lyse der Plasmamembran. Zusammenfassend konnten wir
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