Research Collection. Studies in epigenetics: investigating recruitement, modulation and dysfunction. Doctoral Thesis. ETH Library
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1 Research Collection Doctoral Thesis Studies in epigenetics: investigating recruitement, modulation and dysfunction Author(s): Sievers, Cem Publication Date: 2013 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.-No. ETH Studies in epigenetics: investigating recruitment, modulation and dysfunction A dissertation submitted to ETH ZURICH for the degree of Doctor of Sciences presented by CEM SIEVERS Diplom-Biotechnologe, Technische Universität Braunschweig citizen of Germany and Turkey accepted on the recommendation of Prof. Dr. Renato Paro Prof. Dr. Niko Beerenwinkel Prof. Dr. Manfred Claassen 2013
3 Abstract Polycomb group (PcG) proteins are involved in the maintenance of cell typespecific gene expression and, thereby, play a major role in the formation of cell type diversity observed in animals and plants. PcG-mediated gene regulation requires the formation of multimeric protein complexes, which localize to specific sites at chromatin where they catalyze particular histone modifications. These modifications in turn are thought to block gene expression by interfering with transcriptional elongation or causing compaction of the chromatin fiber. The mechanism of recruitment is only partially understood, as most PcG proteins do not bind DNA directly. However, recent work suggests an involvement of non-coding RNAs (ncrnas) in this process. The putative RNA helicase MOV10, previously linked to the microrna (mirna) pathway, was suggested to facilitate interactions between ncrnas and PcG proteins. To study MOV10 function in more detail, we performed MOV10 PAR-CLIP experiments, to globally identify MOV10-bound RNAs. To identify high-confidence RNA-MOV10 interaction sites, we developed the wavcluster algorithm. Our analysis revealed that most MOV10 binding sites are located in 3 UTRs suggesting a predominant involvement in the mirna pathway, whereas a role in PcG-mediated transcriptional control could not be confirmed. Modulation of the epigenomic landscape requires sensing of environmental cues. In this work, we studied the function of the environment sensitive molecular chaperone Hsp90 in the nucleus. Genome-wide binding profiles of Hsp90, previously implicated in epigenetic mechanisms, revealed preferential binding to promoters. Further characterization of Hsp90 at promoters identified a functional link to the process of RNA polymerase (pol) II pausing, established via the pausing factor NELF-E. The involvement of Hsp90 in RNA pol II pausing may constitute another interface to epigenetic gene regulation. The dysfunction of the PcG system is associated with different diseases including cancer. The knockdown of the PcG protein Polyhomeotic (Ph) leads to reproducible formation of highly proliferative tumors in Drosophila. To analyze if Ph impairment also leads to genome instability during tumorigenesis, we performed genome sequencing of a tumor and searched for tumor-specific structural variations (SVs). On this account, we developed the Deterministic Structural Variation Detection algorithm, which allows for the identification of a broad range of SVs. The analysis did not reveal any tumor-specific SVs, suggesting that, in this tumor model, tumor progression can occur in absence of genome instability and genetic mutations. Hence, epigenetic lesions appear to be sufficient to drive tumorigenesis in Drosophila.
4 Kurzfassung Polycomb Gruppen (PcG) Proteine sind notwendig für die Aufrechterhaltung zelltypspezifischer Genexpression und spielen somit eine grundlegende Rolle in der Schaffung von Zelltypdiversität in Tieren und Pflanzen. PcG-vermittelte Genregulation bedingt die Bildung multimerischer Proteinkomplexe, welche bestimmte Bereiche im Chromatin binden und dort spezifische Histonmodifikationen katalysieren. Diese Modifikationen wiederum reprimieren die Genexpression in dem sie vermutlich die transkriptionelle Elongation verhindern oder das Chromatin kondensieren. Der Mechanismus der Rekrutierung an spezifische Zielgene ist nicht vollständig aufgeklärt, da bespielsweise die meisten PcG Proteine nicht die Fähigkeit besitzen, direkt an die DNA zu binden. Allerdings deuten neue Ergebnisse darauf hin, dass nicht kodierende RNAs (ncrnas) eine funktionale Rolle spielen. Die mutmaßliche RNA Helikase MOV10, bisher als Bestandteil des mirna Prozesses beschrieben, scheint Wechselwirkungen zwischen ncrna und PcG Proteinen zu ermöglichen. Zum besseren Verständnis der MOV10 Funktion haben wir MOV10 PAR-CLIP Experiment durchgeführt, um alle MOV10 gebundenen RNAs zu identifizieren. Um hoch konfidente MOV10-RNA Bindungsstellen zu erfassen, haben wir den wavcluster Algorithmus entwickelt. Die Analyse ergab, dass die meisten MOV10 Bindungsstellen in 3 UTRs liegen, was für eine primäre Rolle des Proteins im mirna Mechanimus spricht, während eine Rolle in PcG-vermittelter Genrepression nicht bestätigt werden konnte. Die Wahrnehmung externer Umweltzustände führt zur Modulation epigenetischer Zustände. In unserer Studie untersuchten wir die Funktion des umweltsensitiven molekularen Chaperones Hsp90 im Zellkern. Genomweite Bindungsprofile von Hsp90, dessen Beteiligung an epigenetischen Mechanismen bereits gezeigt wurde, wies eine bevorzugte Bindung an Promotoren auf. Die weitere Charakterisierung des Promotorgebundenen Hsp90 ergab einen funktionellen Zusammenhang mit dem sogenannten RNA Polymerase II (Pol II) Pausing, durch den Pausingfaktor NELF-E. Die Beteiligung von Hsp90 an RNA Pol II Pausing kann eine weitere Schnittstelle zwischen Hsp90 und der epigenetischen Genregulation darstellen. Fehlfunktionen des PcG Systems werden mit verschiedenen Krankheiten, einschließ Krebs, in Verbindung gebracht. Der Verlust des PcG Proteins Polyhomeotic (Ph) führt zur reproduzierbaren Entstehung von hoch proliferativen Tumoren in Drosophila. Um zu Untersuchen, ob eine Einschränkung der Ph Funktion zu einer Genominstabilität während der Tumorigenese führt, haben wir das Genom eines Tumors sequenziert und nach tumorspezifischen strukturellen Variationen (SV) gesucht. Zu diesem
5 6 Zweck haben wir den Deterministic Structural Variation Detection Algorithmus entwickelt, welcher die Identifikation eines breiten Spektrums an SVs zulässt. Die Analyse ergab keine tumorspezifischen SVs, was darauf hindeutet, dass in diesem Tumormodel Tumorprogression auch in Abwesenheit von Genominstabilität und genetischen Mutationen stattfinden kann. Demzufolge sind epigenetische Läsionen offenbar ausreichend, um in Drosophila Tumorigenese zu verursachen.
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