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Role of BET-Proteins in the Function of Rhadinoviral Orf73-Proteins Von

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Role of BET-Proteins in the Function of Rhadinoviral Orf73-Proteins Von Role of BET-Proteins in the Function of Rhadinoviral Orf73-Proteins Von der Naturwissenschaftlichen Fakultät der Gottfried Wilhelm Leibniz Universität Hannover zur Erlangung des Grades Doktor der Naturwissenschaften Dr. rer. nat. genehmigte Dissertation von Dipl.-Biochem. Daniel Pliquet geboren am 14.12.1977 in Pinneberg 2011 Referent: Prof. Dr. Thomas F. Schulz Institut für Virologie Medizinische Hochschule Hannover Koreferent: Prof. Dr. Edgar Maiss Institut für Pflanzenkrankheiten und Pflanzenschutz Gottfried Wilhelm Leibniz Universität Hannover Tag der Promotion: 17.11.2010 2 Zusammenfassung Das Kaposi Sarkom assoziierte Herpesvirus (KSHV) gehört zusammen mit dem murinen γ- Herpesvirus 68 (MHV68) zur Gattung der Rhadinoviren in der Ordnung Herpesvirales. Beide Viren persistieren im lymphatischen Gewebe und spielen eine Rolle bei der Entstehung lymphoproliferativer Erkrankungen. Eines der wichtigsten Latenzproteine ist im offenen Leserahmen (orf) 73 kodiert, bei KSHV wird das Protein auch als Latenz assoziiertes nukleäres Antigen 1 (LANA-1) bezeichnet. Beide orf73 Proteine werden in der Latenzphase exprimiert und erfüllen verschiedene wichtige Funktionen für das Virus. Eine dieser Funktionen ist die Interaktion mit zellulären BET Proteinen. In dieser Arbeit wurde die molekulare Natur dieser Interaktion und deren Auswirkungen untersucht. Es gelang uns, zwei zuvor in einem Peptid Interaktionsversuch identifizierte Bindungsstellen für BET Proteine innerhalb des MHV68 orf73 Proteins zu bestätigen. Die Bindungsstellen wurden auf verschiedene Weise mutiert, um den Einfluss der Bindungsstellen auf Funktionen des MHV68 orf73 Proteins zu untersuchen. Das Aminosäuremotiv KKLK in der C-terminalen BET Bindungsstelle ist notwendig für die Interaktion des MHV68 orf73 Proteins mit den BET Proteinen Brd2 und Brd4. Mutationen in diesem Motiv verursachen keine Veränderung bei der Bindung des MHV68 orf73 Proteins an mitotische Chromosomen, das schliesst eine Beteiligung von BET Proteinen bei der Anheftung der viralen Genome an Chromosomen während der Mitose aus. Aber die Mutation des Bindungsmotivs verringert die Fähigkeit des MHV68 orf73 Proteins, die Transkription von Cyclin Promotoren zu aktivieren. Die Interaktion mit den BET Proteinen Brd2 und Brd4 spielt also eine Rolle bei der Aktivierung von transkriptionellen Prozessen durch das MHV68 orf73 Protein, ist aber nicht an der Persistenz des viralen Genoms in der Zelle beteiligt. Das LANA-1 Protein von KSHV wurde in einem Yeast two Hybrid Interaktionsversuch mit einer Bibliothek von Peptidaptameren verwendet. Es konnten drei Peptidaptamere identifiziert werden, die mit dem C-terminalen Teil des LANA-1 Proteins von Aminosäure 1090 bis 1162 interagieren, der auch die Region mit der höchsten Sequenzähnlichkeit zum MHV68 orf73 Protein und die Bindungsstelle für die BET Proteine im MHV68 orf73 Protein beinhaltet. Die interagierenden Peptidaptamere inhibierten sowohl die von LANA-1 verursachte Aktivierung des Cyclin E Promotors als auch eines Promotors, der auf Serum ansprechende Sequenzen enthält. Eine generelle Inhibition der Transkription wurde ausgeschlossen, da die interagierenden Peptidaptamere zwei virale Promotoren nicht beeinflussten. Die Peptidaptamere veränderten die Aktivierung des LTR Promotor von HIV durch das TAT Protein, welche durch Brd4 vermittelt wird, nicht. Die Erkenntnisse dieser Arbeit betonen die wichtige Rolle der Interaktion von BET Proteinen mit orf73 Proteinen für deren Funktion während des viralen Lebenszyklus. 3 Summary The Kaposi sarcoma-associated herpesvirus (KSHV) belongs, together with murine γ-herpesvirus 68 (MHV68), to the genus of Rhadinoviruses within the order of Herpesvirales. Both viruses persist in lymphoid tissues and are involved in lymphoproliferative disease. A main factor for the latent infection is encoded in open reading frame (orf) 73, the protein is termed latency-associated nuclear antigen 1 (LANA-1) for KSHV. Both orf73 proteins are expressed during latency and fulfil several important functions in the viral life cycle. One of the conserved functions is the interaction with cellular BET proteins. In this thesis we investigated the molecular nature of the interaction of the MHV68 orf73 protein with the BET proteins Brd2 and Brd4 and the consequences of this interaction. We were able to verify two potential BET binding sites within the MHV68 orf73 protein, which were identified by an in vitro peptide interaction assay. These BET binding sites were mutated in several variants to adress the impact of the interaction with BET proteins on MHV68 orf73 functions. The motif of the amino acids (aa) KKLK in the C-terminal BET binding site mediated interaction with the two BET proteins Brd2 and Brd4. Mutation of this motif did not alter tethering of the MHV68 orf73 protein to mitotic chromosomes and therefore BET proteins are not involved in tethering of the MHV68 viral genome to chromosomes during mitosis. However, the mutation of BET binding sites impaired the induction of transcription from cyclin promotors by the MHV68 orf73. Therefore the interaction with the BET proteins Brd2 and/or Brd4 is involved in transcriptional activation processes of the MHV68 orf73, but not in viral genome maintenance. The KSHV LANA-1 protein was subject of a yeast two hybrid screen with a library of peptide aptamers. We identified three peptide aptamers, which bind to aa 1090-1162 of the LANA-1 protein, which encompasses the region with the highest sequence similarity to the MHV68 orf73 protein and the binding site for BET proteins. The interacting peptide aptamers were able to impair LANA-1 mediated activation of transcription from the cyclin E promotor and a serum reponse element containing promotor, in contrast to a not interacting peptide aptamer or the empty expression vector. This downregulation is not caused by a general inhibition of transcription, as the transcription from the long terminal repeat promotor (LTR) of HIV and the immediate early promotor of human cytomegalovirus (CMV) are not affected by the expression of any peptide aptamer. Also a general inhibition of the positive effect of Brd4 in the P-TEFb complex can be excluded, since the induction of the LTR promotor by the HIV transactivator of transcription (TAT) was not altered by any peptide aptamer. These findings indicate the importance of the interaction between BET proteins and the orf73 proteins for their regular function during the viral life cycle. 4 Schlagwörter: Herpesviren, BET-Proteine, Zellzyklus Keywords: Herpesvirus, BET-Proteins, Cellcycle 5 Table of content: Zusammenfassung 3 Summary 4 1. Introduction 10 1.1. The family of Herpesviridae 10 1.2. The subfamily of γγγ-Herpesviridae 12 1.2.1. Kaposi’s sarcoma-associated herpesvirus (KSHV) 12 History of KSHV 12 Epidemiology of KSHV 13 Transmission of KSHV 14 KSHV and neoplastic disorders 15 KSHV lifecycle 17 Immune evasion by KSHV 20 1.2.2. Murine gammaherpesvirus 68 (MHV68) 25 1.3. Replication of Rhadinoviruses 28 1.4. Cell cycle and its alteration by Rhadinoviruses 33 1.4.1. Cell cycle regulation 34 Cyclins and cyclin dependent kinases (CDK) 34 The retinoblastoma protein (Rb) and progression to S phase 35 1.4.2. Cell cycle modification by Rhadinoviruses 37 Viral Cyclin 37 Latency-associated nuclear antigen 1 (LANA-1) 38 LANA-2/vIRF-3 38 Lytic proteins 39 1.5. Orf73 encoded proteins of Rhadinoviruses 40 1.5.1. Latency-associated nuclear antigen 1 of KSHV 40 1.5.2. The orf73 protein of MHV68 47 1.6. Bromodomain and extraterminal domain containing (BET) proteins 48 Bromodomain 49 Extraterminal (ET) domain 49 1.6.1. BET proteins in yeast and drosophila 50 Yeast Bdf-1 and Bdf-2 proteins 50 Drosophila female sterile homoetic (fsh) protein 51 1.6.2. Mammalian BET-proteins 51 6 Brd3/OrfX 52 Brd6/BrdT 52 Brd2/RING3 53 Brd4/HUNK/MCAP 55 1.7. Objectives 58 2. Materials and Methods 59 2.1. Reagents 59 2.1.1. Antibodies 59 2.2. Vectors and Primers 61 2.2.1. Eukaryotic expression vectors 61 2.2.2. Prokaryotic expression vectors 66 2.2.3. Reporter vectors 68 2.2.4. Primers 70 2.2.5. Recombinant baculovirus 71 2.3. Cell culture methods for eukaryotic cells 71 2.3.1. Supplies used for propagation 71 2.3.2. Eukaryotic cell lines 71 2.3.3. Cell culture conditions 72 2.3.4. Cryopreservation of eukaryotic cells 72 2.3.5. Baculovirus expression system 73 2.3.6. Transient transfection of plasmid DNA 73 2.4. Cell culture methods for prokaryotic cells 74 2.4.1. Medium used for propagation 74 2.4.2. Bacterial strains 74 2.4.3. Cryopreservation of prokaryotic cells 75 2.4.4. Preparation of competent cells and transformation 75 2.5. Molecular biology methods 76 2.5.1. Isolation of plasmid DNA 76 2.5.2. Enzymatic modification of DNA 76 2.5.3. PCR amplification of DNA 76 2.5.4. Electrophoresis and extraction of DNA in agarose gels 77 2.5.5. DNA sequencing 78 2.6. Biochemical and cell biology methods 78 2.6.1. Preparation of cell lysates 78 7 2.6.2. SDS polyacrylamide gel electrophoresis (PAGE) and Coomassie staining 79 2.6.3. Immunoblotting 80 2.6.4. Luciferase reporter assay 82 2.6.5. βββ-galactosidase assay 83 2.6.6. Immunofluorescence microscopy 84 2.6.7. Purification of His tagged proteins 86 2.6.8. Interaction assays with GST fusion proteins (GST pulldowns) 88 2.6.9. Coimmunoprecipitation 89 2.6.10. Nuclear fractionation assay 90 3. Results 92 3.1. Functional consequences of the interaction between cellular BET proteins and the MHV68 orf73 protein 92 3.1.1. Identification of binding sites for BET proteins within the MHV68 orf73 protein and charcterization of their interaction patterns 92 The aa 228-231 of MHV68 Orf73 interact with Brd2 93 The interaction between the MHV68 orf73 protein and the Brd4S protein depends on aa 20-23 and aa 228-231 of MHV68 orf73 94 Endogenous Brd4 binding to the MHV68 orf73 protein is mediated by aa 228-231 of MHV68 orf73 95 Mutation of the C-terminal BET protein binding site does not reduce the oligomerization capability of the MHV68 orf73 protein 97 Interaction of the MHV68 orf73 protein with Rb is not affected by mutation of the BET protein binding sites 98 3.1.2.
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