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Submitted to the Combined Faculties for the Natural Sciences and For DISSERTATION submitted to the Combined Faculties for the Natural Sciences and for Mathematics of the Ruperto-Carola University of Heidelberg, Germany for the degree of Doctor of Natural Sciences presented by Dipl.-Biol. Sonja Matt born in Gronau (Westphalia) Oral Examination: Topic Polycomb Group Proteins in the freshwater polyp Hydra Referees: Prof. Dr. Gabriele Petersen PD Dr. Renate Voit I hereby confirm that the presented dissertation is my own work; and that, to the best of my knowledge and belief, all published or other sources of material consulted have been acknowledged in notes to the text or the bibliography. I confirm that this disser- tation has not been submitted for a comparable academic award to another department or university. I confirm that this dissertation has not been published and that I will not perform publication prior to completion of the examination procedure. I am aware of the regulations concerning the conferral of doctoral degrees. Heidelberg, Sonja Matt for my parents Seul l’inconnu épouvante les hommes. Mais, pour quiconque l’affronte, il n’est déjà plus l’inconnu. Antoine de Saint-Exupéry (Terre des Hommes, 1939) Only the unknown frightens men. But once a man has faced the unknown, that terror becomes the known. Antoine de Saint-Exupéry (Wind, Sand and Stars, 1939) Nur das Unbekannte ängstigt den Menschen. Sobald man ihm die Stirn bietet, ist es schon kein Unbekanntes mehr. Antoine de Saint-Exupéry (Wind, Sand und Sterne, 1939) ABSTRACT xi Abstract During the development of a multicellular organism, different cell types with specific functions have to be generated, although the cells contain the same genetic information. This is achieved by a cell type specific expression of genes. The gene expression pattern and the identity of the cell have to be maintained for several rounds of cell division. The growing field of epigenetics deals with the inheritance of traits, which are not determined in the underlying DNA sequence. The long-term maintenance of gene expression patterns, which can be described as a kind of a cellular memory, is counted among epigenetic mechanisms. Different epigenetic inheritance systems like chromatin remodeling exist. For instance, the chromatin structure can be altered by the histone modifying Polycomb Group (PcG) proteins. The PcG proteins are responsible for the inheritance of the repressed state. Many genes, which are controlling development, differentiation and the cell cycle, are regulated by PcG proteins. The proteins have been shown to act as large multipro- tein complexes, so-called Polycomb Repressive Complexes (PRCs). In the scope of this thesis, PcG and associated proteins have been characterized in the freshwater polyp Hydra. The PcG genes Scm and Pho/YY1 could be identified in the Hydra genome and have been cloned. Together with the already identified proteins of the PRC1 and PRC2 complexes, Hy- dra possesses a complete set of PcG proteins. A comparison with homologous proteins of other species could demonstrate that the functional domains of the Hydra PcG proteins are highly con- served. Interestingly, the genes of the PRC2 complex are exclusively expressed in one of the three cell lineages of Hydra. The genes are expressed in the so-called interstitial cell lineage. Studies with sexual polyps could show that the genes are also expressed in the gonads of the animals. The cell line specific expression of the genes in Hydra seems to separate interstitial cells from the epithelial cell lineages. The DNA binding protein HyYY1 has been of special interest in this study. It is a homolog of the Drosophila protein Pho and of the human transcription factor YY1. Pho can be found in a PcG complex termed PhoRC (Pleiohomeotic Repressive Complex) in combination with dSfmbt. This complex is responsible for the recruitment of the other PcG complexes to their target genes in the fruit fly. YY1 acts as a ’molecular adapter’ and links the PcG complexes to so-called Polycomb Response Elements (PREs). These cis-regulatory elements can be found close to target genes and are important for the recruitment of the PcG complexes. The Hydra protein has both a zinc fin- ger domain, which is responsible for the DNA binding, and a so-called REPO domain, which is necessary for the interaction with the PRCs. With the help of gel retardation assays, it could be demonstrated that HyYY1 can effectively interact with the DNA in a sequence-specific manner. The consensus sequence is equivalent to the CCAT-motif found in Drosophila and mammals. In the fruit fly, this sequence can be found within PREs. A polyclonal antibody against recombinantly expressed HyYY1 has been generated during this study - making immunohistochemical analyses and immunoprecipitations (IPs) possible. An in- dication of the interaction of HyYY1 with other PcG proteins could be provided by a Co-IP. How- ever, this preliminary result has to be verified. In addition, it should be kept in mind that the xii ABSTRACT recruitment of PcG complexes in Hydra is not necessarily dependent on Pho/YY1 and PRE sites. At least for mammals, other recruiting mechanisms are known. The existing antibodies against HyYY1 and otherHydra PcG proteins render chromatin-IPs to identify target genes possible. In a preliminary experiment, sequences of the Hydra genome could be precipitated. Next-generation sequencing technologies will enable large-scale ChIP-Seq exper- iments and the future identification of PcG target genes in Hydra. ZUSAMMENFASSUNG xiii Zusammenfassung Während der Entwicklung eines vielzelligen Organismus müssen unterschiedliche Zelltypen mit spezifischen Funktionen gebildet werden, obwohl alle Zellen dieselbe Erbinformation enthalten. Dies wird durch eine zelltypspezifische Expression von Genen erreicht. Das Genexpressionsmu- ster - und damit die Identität der Zelle, muss über viele Zellteilungen hinweg aufrecht erhalten werden. Das wachsende Feld der Epigenetik beschäftigt sich mit der Vererbung von Merkmalen, die nicht in der DNA-Sequenz festgelegt sind. Darunter fällt auch die langfristige Aufrechter- haltung von Genexpressionsmustern, welche auch als eine Art ’Zellgedächtnis’ bezeichnet wer- den kann. Es existieren verschiedene epigenetische Vererbungssysteme, wie beispielsweise der Chromatinumbau (’chromatin remodeling’). Die Chromatinstruktur kann unter anderem durch die Histon-modifizierenden Polycomb Group (PcG) Proteine derart verändert werden, dass die Transkription verhindert wird. PcG Proteine sind für die Vererbung des reprimierten Zustandes verantwortlich. Viele Gene, welche die Entwicklung, die Differenzierung und den Zellzyklus kontrollieren, werden durch PcG Proteine reguliert. Die Proteine agieren dabei als große Multi- proteinkomplexe, sogenannte Polycomb Repressive Complexes (PRCs). Im Rahmen dieser Arbeit wurden Polycomb Group (PcG) und assoziierte Proteine im Süßwas- serpolypen Hydra näher untersucht. Im Laufe dieser Arbeit konnten die PcG Gene Scm und Pho/YY1 im Hydra-Genom identifiziert und kloniert werden. Zusammen mit den in früheren Studien identifizierten PcG Proteine der PRC1 und PRC2 Komplexe besitzt Hydra damit einen vollständigen Satz an PcG Proteinen. Durch den Vergleich mit homologen Proteinen anderer Or- ganismen konnte gezeigt werden, dass vor allem die funktionellen Domänen der PcG Proteine in Hydra hoch konserviert sind. Interessanterweise werden die Gene des PRC2 Komplexes ausschließlich in einer der drei Zell- linien von Hydra exprimiert. Die Gene werden in der sogenannten interstitiellen Zelllinie expri- miert. Anhand von Studien an geschlechtlichen Polypen konnte außerdem gezeigt werden, dass die Gene in den Gonaden der Tiere exprimiert werden. Die zelllinienspezifische Expression der Gene in Hydra scheint eine Abgrenzung der interstitiellen Zellen von den beiden Epithelzelllinien darzustellen. Von besonderem Interesse war das DNA bindende Protein HyYY1, welches ein Homolog des Dro- sophila Proteins Pho und des humanen Transkriptionsfaktors YY1 ist. In der Fruchtfliege bildet Pho zusammen mit dSfmbt einen PcG Komplex namens PhoRC (Pleiohomeotic Repressive Com- plex), welcher für die Rekrutierung der anderen PcG Protein-komplexe zu den Zielgenen verant- wortlich ist. YY1 agiert als ein ’molekularer Adapter’ und verbindet die PcG Komplexe mit soge- nannten Polycomb Response Elements (PREs). Diese cis-regulatorischen Elemente werden in der Nähe von Zielgenen gefunden und sind für die Rekrutierung der PcG Proteine von Bedeutung. Das Hydra Protein besitzt sowohl vier Zinkfinger, welche für die DNS-Interaktion verantwortlich sind, als auch eine REPO-Domäne, welche für die Interaktion mit den PcG Komplexen notwen- dig ist. Anhand von Gelretardations-Analysen konnte gezeigt werden, dass HyYY1 tatsächlich sequenzspezifisch mit der DNS interagieren kann. Die Konsensussequenz entspricht dem CCAT- Motiv von Drosophila und Säugern. In der Fruchtfliege wird diese Sequenz in PREs gefunden. xiv ZUSAMMENFASSUNG Während dieser Arbeit wurde ein polyklonaler Antikörper gegen rekombinant exprimiertes HyYY1 hergestellt, welcher immunhistochemische Analysen und Methoden wie die Immunpräzipitation (IP) erlaubt. Durch eine Co-IP konnte ein anfänglicher Hinweis auf die Interaktion von HyYY1 mit anderen PcG Proteinen erbracht werden. Dieses vorläufige Ergebnis muss allerdings verifi- ziert werden. Desweiteren sollte bedacht werden, dass die Rekrutierung der PcG Komplexe in Hydra nicht zwangsläufig über Pho/YY1 und PREs erfolgen muss. Zumindest in Säugern wur- den weitere Mechanismen der Rekrutierung gefunden. Die vorhandenen Antikörper
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