Clathrin- and caveolin-1- independent endocytosis of Simian Virus 40
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1 Diss. ETH No Clathrin- and caveolin-1- independent endocytosis of Simian Virus 40 A dissertation submitted to the Swiss Federal Institute of Technology Zürich for the degree of Doctor of Natural Sciences Eva-Maria Damm Diplom Humanbiologin, Philipps-Universität Marburg born on October 4th, 1976 citizen of Germany accepted on the recommendation of Prof. Dr. Ari Helenius, examiner Prof. Dr. Ulrike Kutay, co-examiner Prof. Dr. Urs Greber, co-examiner 2005
2 viii Summary Summary Endocytosis is an essential cellular process that allows the regulated uptake of nutrients and macromolecules, the transduction of signals, the maintenance of cellular homeostasis, and the defense against microorganisms. Depending on the cell type and the cargo, endocytosis can take many different forms. Many animal viruses and other pathogens make use of the cells endocytic machinery in order to enter and infect their host cells. One of these viruses is Simian Virus 40 (SV40), a double-stranded DNA virus belonging to the papova virus family. During its infectious entry, SV40 associates with plasma membrane caveolae, by which it is internalized by its host cell in a clathrin-independent, but caveolin-1- and dynamin2-dependent uptake process. Caveolar vesicles deliver their cargo to caveosomes, which are ph-neutral, lipid raft- and caveolin-1-enriched organelles. In caveosomes, virus particles are sorted into tubular carrier vesicles that are transported along microtubules to the smooth endoplasmic reticulum. Following the entry of SV40 in embryonic fibroblast cells derived from caveolin-1 knockout mice, it was found that the virus entered by an alternative tyrosine kinase- and lipid raftdependent endocytic pathway, that supported infection. The pathway differed from the caveolar pathway in that it was rapid and dynamin2-independent. SV40 was internalized into tight fitting endocytic vesicles, which delivered their cargo to intermediate organelles that resembled caveosomes but lacked caveolin-1. From these organelles, SV40-containing vesicles were transported along microtubules to the smooth endoplasmic reticulum. In wildtype mouse embryonic fibroblasts the virus apparently used the same dynamin2- independent uptake pathway with a major fraction of viruses internalized independently of caveolin-1. Both pathways merged at the level of caveosomes. In addition to SV40, also other caveolar ligands were found to be taken up into cells that lack caveolae, presumably by the same mechanism.
3 Summary ix In fusion experiments between caveolin-1-containing and caveolin-1-lacking cells, it was found that caveosomes and their caveolin-1 negative counterparts fused to form one organelle that accumulated ligands of the caveolar/raft pathway (SV40) and supported SV40 infection. The results showed that the caveolar and the lipid-raft pathway can coexist and complement each other. They are variants of a common endocytic mechanism.
4 x Zusammenfassung Zusammenfassung Endozytose ist ein essentieller zellulärer Prozess, der die kontrollierte Aufnahme von Nährstoffen und Makromolekülen, die Übermittlung von Signalen, die Aufrechterhaltung der zellulären Homöostase und die Abwehr von Mikroorganismen erlaubt. Je nach Zelltyp und Cargo können verschiedene endozytotische Prozesse aktiviert werden. Viren und andere Pathogene machen sich die Endozytosemaschinerie ihrer Wirtszelle zunutze, um diese befallen und infizieren zu können. Eines dieser Viren ist Simian Virus 40 (SV40), ein doppelsträngiges DNA Virus der Papova Virusfamilie. Um in die Wirtszelle eindringen zu können, assoziiert SV40 mit Caveolae an der Plasmamembran, mit deren Hilfe es in die Zelle aufgenommen wird. Dieser Aufnahmeschritt ist unabhängig von Clathrin, aber benötigt Caveolin-1 und Dynamin2. Das Cargo wird über die caveolären Vesikel zu ph-neutralen, Lipid Raft- und Caveolin-1- angereicherten Organellen, den Caveosomen, transportiert. Von dort werden die Viruspartikel in tubuläre Transportvesikel sortiert und entlang Mikrotubuli zum glatten Endoplasmatischen Retikulum transportiert. In der vorliegenden Arbeit wurde der Endozytoseweg von SV40 in embryonalen Fibroblasten analysiert, die aus Caveolin-1 Knockout Mäusen entnommen waren. Die Studie zeigte, dass das Virus mit Hilfe eines alternativen Tyrosinkinase- und Lipid Raft-abhängigen Endozytoseweges aufgenommen wurde, der eine Infektion begünstigte. Dieser Endozytoseweg unterschied sich von der Caveolae-vermittelten Endozytose durch schnellere Aufnahme und Dynamin2-Unabhängigkeit. SV40 wurde über eng membranumschlossene Vesikel internalisiert, die das Cargo zu intermediären Organellen transportierten. Diese waren den Caveosomen sehr ähnlich, enthielten jedoch kein Caveolin-1. Von diesen Organellen ausgehend wurden SV40-enthaltende Vesikel entlang Mikrotubuli zum glatten Endoplasmatischen Retikulum transportiert. In Wildtyp-Fibroblasten benutzte das Virus den gleichen Dynamin2-unabhängigen Endozytoseweg, und ein Grossteil der Viren internalisierte unabhängig von Caveolin-1. Beide Wege trafen in Caveosomen aufeinander. Zusätzlich zu
5 Zusammenfassung xi SV40 wurden auch andere Caveolae-Liganden ermittelt, die in Zellen ohne Caveolae internalisieren konnten. Es ist anzunehmen, dass dies über den gleichen obengenannten Mechanismus geschah. Fusionsexperimente zwischen Caveolin-1-haltigen und Caveolin-1-negativen Zellen zeigten, dass Caveosomen und ihre Caveolin-1-negativen Gegenstücke zu demselben Organell fusionierten. Dieses Organell konnte Liganden des Caveolae/Lipid Raft Endozytoseweges (SV40) aufnehmen und SV40-Infektion begünstigen. Diese Experimente zeigten, dass Caveolae- und Lipid Raft-Endozytosewege koexistieren und sich gegenseitig komplementieren können. Beide sind Varianten eines gemeinsamen endozytotischen Mechanismus.
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