Structural and methodological studies on protein RNA interactions
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1 Research Collection Doctoral Thesis Structural and methodological studies on protein RNA interactions Author(s): Theler, Dominik Emanuel 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. ETH No Structural and Methodological Studies on Protein RNA Interactions A dissertation submitted to ETH ZURICH for the degree of Doctor of Sciences presented by Dominik Emanuel Theler Dipl. Natw. ETH born August 21 st, 1981 citizen of Ausserberg, VS accepted on the recommendation of Prof. Dr. Frédéric Allain, examiner Prof. Dr. Ulrike Kutay, co-examiner Prof. Dr. Oliver Zerbe, co-examiner 2013
3 Abstract An ever increasing number of processes regulating gene expression acting at the post transcriptional level have been described. These processes allow cells to adapt to their environment and some of them allow them to increase the complexity of their proteome. Misregulations of these processes contribute to human diseases. Correcting such errors or using therapeutics based on these mechanisms can provide an avenue for treatment. Proteins besides several classes of non coding ribonucleic acid (RNA) molecules are key players in these processes. The study of interactions of proteins with RNA at the molecular level can provide valuable insights into the functions of these processes. RNA binding motif protein 4 (RBM4) is a protein involved in several of these post transcriptional processes such as alternative splicing, translational control and the mirna pathway. The binding preferences of its RNA recognition motif domain (RRM) domains were assayed by nuclear magnetic resonance (NMR) titrations. These titrations revealed that RRM1 of RBM4 is capable not only of interacting with single stranded RNA but also with stem structures. The affinity of RRM1 to its single stranded recognition sequence is greatly enhanced, if this sequence is present in the loop of a stemloop structure. This property would hint at an additional layer of regulation of this protein in vivo depending on the secondary structure of the target sequence. A preliminary NMR structure of this complex is presented revealing molecular details of the interaction with the single stranded loop as well as the stem. Recent studies indicate that numerous proteins bind to RNA, despite them lacking a known RNA binding domain. This indicates that known domains either possess this unattributed capability or the existence of novel domains within these proteins carrying out this function. One such novel domain is the yeast two hybrid homology domain (YTH) domain of which a preliminary structure is presented as well as NMR titrations with systematic evolution of ligands by exponential enrichment (SELEX) derived RNA revealing the binding interface of this novel RNA binding domain. The loose definition of the SELEX sequences did not allow to find a binding sequence and measurement conditions to solve the first protein RNA complex of such a domain by NMR. The binding preference of the domain was then further investigated by NMR titrations using oligonucleotides being degenerate at certain positions to allow independent investigation of another position. A binding sequence was obtained by this approach, which allowed to obtain a preliminary complex structure of the YTH domain in complex with RNA. To elucidate the binding preference of a RNA binding protein it would be useful to be able to apply this approach without prior knowledge of the binding preferences. Such a modified version is discussed and first results obtained presented. Methylation of adenosine at the N6 position is considered to be the most abundant messenger RNA modification besides the canonical cap structure. Impairment of methylase function leads to apoptosis in human cells or inability of organisms to reproduce. The demethylase has been described to be a risk gene for obesity. Recent studies characterized by high throughput i
4 sequencing thousands of methylation sites in the human and mouse transcriptome and identified two YTH domain containing proteins as binding preferentially to the methylated form of a RNA rather than the unmethylated one. The methylation consensus sequence resembles the binding sequence obtained by NMR. A methyl group attached to the adenosine, corresponding to the one, which gets methylated in the consensus, in the complex structure obtained with the NMR derived sequence would point towards the hydrophobic core of the YTH domain. NMR titrations revealed a drastic increase of affinity of the YTH domain, when the methyl group is present. A structure of the domain in complex with a RNA containing N6 methyladenosine was solved and revealed a similar mode of recognition for the methyl group as for methyl groups attached to lysines and arginines sidechains of histones recognized by their respective binding domains. Key residues for methyl recognition are conserved among all members of the YTH domain hinting that recognition of N6 methylated adenosines is a general property of this domain. Structure determination of RNA protein complexes by NMR greatly benefits from the use of labeled RNAs. Small RNAs with appropriate labeling are labour intensive to obtain by chemical synthesis, since the precursor phosphoramidites are not commercially available with 15 N/ 13 C labeling. An efficient method used on a preparative scale is presented to produce small labeled RNAs by cleavage of a larger precursor RNA obtained by in vitro transcription. The method relies on the use of a bacterial RNAse involved in bacterial defence against viral infection and is shown to have no sequence requirements for the small RNA. The work presented in this thesis expands the structural knowledge of protein RNA interactions as well as the presented methods should benefit further studies of protein RNA complexes. ii
5 Zusammenfassung Eine stetig steigende Anzahl von zellulären Prozessen sind beschrieben worden, welche die Genexpression auf post transkriptioneller Stufe regulieren. Diese Prozesse ermöglichen es Zellen sich ihrer Umwelt anzupassen und einige dieser erlauben die Erhöhung der Komplexität ihres Proteoms. Fehlregulierung dieser Prozesse trägt zur Enstehung menschlischer Krankheiten bei. Die Behebung solcher Fehler oder Therapeutika basierend auf diesen Mechanismen könnten eine Möglichkeit zur Behandlung darstellen. Neben Proteinen nehmen auch nicht kodierende RNAs eine Schlüsselrolle in diesen Prozessen ein. Das Studium der molekularen Interaktionen von Proteinen und RNA kann zu wertvollen Einsichten in die Funktion solcher Prozesse führen. RBM4 ist ein Protein involviert in mehreren solchen posttranskriptionellen Prozessen wie alternativem Spleissen, Translationskontrolle und dem mirna System. Die Bindungspräferenzen seiner RRM Domänen wurden mittels NMR Titrationen studiert. Diese Titrationen zeigten, dass RRM1 of RBM4 nicht nur fähig ist einzelsträngige RNA zu binden sondern auch mit RNA, die Teil einer Haarnadelstruktur ist. Die Affinität von RRM1 gegenüber seiner einzelsträngigen Erkennungssequenz ist stark erhöht, wenn diese im Kontext einer Haarnadelstrucktur vorkommt. Diese Eigenschaft deutet auf eine zusätzliche Regulationsebene für dieses Protein in vivo hin, welche auf RNA Sekundärstruktur basiert. Eine preliminäre NMR Struktur dieses Komplexes wird vorgestellt, welche molekulare Details der Interaktion des Proteins mit dem einzelsträngigen wie auch dem doppelsträngigen Teil der RNA zeigt. Kürzlich veröffentlichte Studien zeigen, dass zahlreiche Proteine RNA binden, obwohl sie keine bekannte RNA bindende Domäne besitzen. Dies deutet darauf hin, dass entweder bekannte Domänen diese unbeschriebene Fähigkeit haben oder das unbekannte Domänen in diesen Proteinen existieren, welche diese Funktion übernehmen. Eine solche neuartige Domäne ist die YTH Domäne, von welcher eine präliminäre Struktur präsentiert wie auch NMR Titrationsdaten mit SELEX selektierter RNA, welche die Bindungsoberfläche dieser neuen RNA bindenden Domäne beschreiben. Die SELEX Sequenzen sind loose definiert und erlaubten es nicht eine Bindungssequenz und Messbedingungen zu finden, welche die Strukturaufklärung des ersten Protein RNA Komplexes dieser Domäne mittels NMR erlaubt hätten. Die Bindungspräferenz der Domäne wurde mittels NMR Titrationen weiter untersucht mittels Benutzung von Oligonukleotiden mit zufällig synthetisierten Positionen, welche es erlauben eine andere Position unabängig zu untersuchen. Diese Experimente erlaubten uns eine Sequenz zu finden mit welcher eine präliminäre Komplexstruktur der YTH Domäne mit RNA aufgeklärt werden konnte. Weiter wird eine Modfikation des Verfahrens diskutiert, welche keine vorgängiges Wissen über die Bindungssequenz vorrausetzen sollte, und erste Resultate präsentiert. Methylierung von Adenosinen an der N6 Position gilt als die häufigste Modifikation von Boten RNA neben der kanonischen Kappenstruktur. Die Beeinträchtigung der Methylasefunktion führt zu Apoptose in menschlichen Zellen oder der Unfähigkeit von Organismen sich fortzupflanzen. Das Demethylierungsenzym gilt as Risikofaktor für Fettleibigkeit. Kürzlich iii
6 durchgeführte Studien charakterisierten mittels Hochdurchsatz Sequenzierung tausende von Methylierungstellen im Transkriptom von Mensch- und Mäusezellen und identifizierten zwei YTH Domänen beinhaltende Proteine, welche präferentiell die methylierte Form einer gegebenen RNA binden. Die Methylierungskonsensussequenz ähnelt der Bindungsequenz, welche mittels NMR ermittelt wurde. Eine Methylgruppe an das Adenosine angehängt, welches korrespondiert zu demjenigen, welches in der Konsensussequenz methyliert wäre, würde Kontakte mit dem hydrophobischen Kern der Domäne machen, wenn die preliminäre Struktur betrachtet wird. NMR Titrationen zeigten eine stark erhöhte Affinität der YTH Domäne, wenn die RNA eine solche Methylgruppe enthielt. Eine Struktur der Domäne mit einer RNA, welche ein solches N6 methyliertes Adenosine enthält konnte gelöst werden und zeigte, dass die Methylgruppe ähnlich erkannt wird wie methylierte Arginin- und Lysineseitenketten von Histonen durch andere Proteindomänen. Schlüsselaminosäuren sind konserviert unter den Mitgliedern der YTH Domäne. Dies deutet darauf hin, dass die Erkennung von N6 methylierten Adenosinen eine generelle Eigenschaft dieser Domäne ist. Die Strukturbestimmung von RNA Protein Komplexen mittels NMR profitiert massiv vom Gebrauch von markierten RNAs. Kleine RNAs mit der gewünschten Markierung sind nur aufwändig erhältlich mittels chemischer Synthese, da die Phosphoramidite kommerziell nicht mit 15 N/ 13 C Markierung erhältlich sind. Eine effiziente Methode angewandt auf einer präparativen Skala wird präsentiert zur Herstellung solcher kleiner markierter RNA mittels Spaltung einer grösseren RNA, welche durch in vitro Transkription hergestellt wurde. Diese Methhode basiert auf dem Gebrauch einer bakteriellen RNAse, welche der Abwehr viraler Infektionen dient und keine Sequenzanforderungen an die kleine RNA stellt. Die in dieser Dissertation präsentierte Arbeit trägt zum Wissen über Protein RNA Interaktionen bei. Die Methoden sollten von Nutzen sein für weitere Untersuchungen von Protein RNA Komplexen mittels NMR. iv
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