Genome-wide RNAi screening approaches to generate an inventory of human ribosome biogenesis factors
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1 Research Collection Doctoral Thesis Genome-wide RNAi screening approaches to generate an inventory of human ribosome biogenesis factors Author(s): Badertscher, Lukas Publication Date: 2015 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. (22792) Genome-wide RNAi screening approaches to generate an inventory of human ribosome biogenesis factors A dissertation submitted to ETH ZURICH for the degree of Doctor of Sciences (Dr. sc. ETH Zurich) presented by Lukas Badertscher Master of Science in Molecular Biology, University of Basel Born June 24 th, 1984 Basel, Switzerland Accepted on the recommendation of Prof. Ulrike Kutay, examiner Prof. Witold Filipowicz, co-examiner Prof. Matthias Peter, co-examiner 2015
3 Summary Ribosome biogenesis is one of the most energy consuming and fundamental processes of the cell. The complexity of this tremendous cellular task is reflected by the fact that more than 200 non-ribosomal proteins, termed trans-acting factors, assist in the assembly of both ribosomal subunits in eukaryotes. The identity of these factors has mainly been derived from studies performed in yeast, yet, surprisingly little is known about ribosome synthesis in human cells despite its central role for cellular homeostasis. In this thesis, we used visual read-outs to follow the maturation routes of both pre-40s and pre-60s ribosomal particles in combination with RNAi, which enabled us to systematically identify factors that support the synthesis of ribosomes in human cells. In a first step, we investigated the contribution of about 500 candidate factors to ribosome production. Among others, these genes included ribosomal proteins and human homologs of yeast ribosome synthesis factors. We are able to demonstrate that core features of ribosome assembly are highly conserved between yeast and humans. However, certain interspecies adaptations were observed, for example a contribution of exportin 5 to 60S subunit export from the nucleus in human cells. In a second step, the screening approaches were consequently extended to a genomic scale, which not only allowed generating a first inventory of human ribosome biogenesis factors for both ribosomal subunits, but also highlighting analogies and differences between 40S and 60S maturation. Interestingly, the biogenesis of 40S subunits is highly sensitive to strong 60S maturation defects as indicated by the presence of RPL proteins in both hit lists. In contrast, depletion of RPS proteins and 40S biogenesis factors did not affect 60S biogenesis to similar extents, suggesting that an imbalance in 60S subunit production is sensed III
4 by cells to maintain subunit balance. Another identified cellular hub required for ribosome production is the ubiquitin-proteasome system. Impaired proteasome function affects early biogenesis steps of both subunits. Our data suggests a potential involvement of CUL4-RING E3 ubiquitin ligases in this process. Remarkably, we identified a novel vertebrate-specific ribosome synthesis factor, named RBIS, which acts downstream of rrna transcription and supports maturation of both ribosomal subunits, indicated by nucleoplasmic accumulation of pre-40s and pre-60s particles and a reduction of mature 18S and 28S rrna after its depletion. We provide evidence that RBIS is present on pre-ribosomal particles. Based on its striking resemblance to ribosomal proteins it is likely that this factor is capable of binding to the negatively charged rrna backbone. The importance of RBIS in production of ribosomes was further substantiated by its conserved function in numerous different human cell lineages. Moreover, our data revealed a central role of GLUL, the human glutamine synthetase, in ribosome synthesis. Interestingly, especially the efficient production of 40S subunits appeared to be hypersensitive not only to changes in extracellular glutamine levels, but also required intracellular glutamine synthesis. Numerous cancer cells are addicted to glutamine and this might be connected to the massive production of ribosomes in these cells. In conclusion, our screening approaches allowed generating a first overview of human ribosome synthesis factors for both ribosomal subunits on a genomic scale. Remarkably, several of the identified genes have been connected to human diseases, often associated with cancer susceptibility. This emphasizes the central role of ribosome synthesis in organismal homeostasis and it is likely that more disease-causing mutations in genes encoding for ribosome synthesis might be discovered. IV
5 Zusammenfassung Die Ribosomenbiogenese ist einer der am meisten Energie verbrauchenden und fundamentalen Prozesse der Zelle. Die Komplexität dieser gewaltigen zellulären Aufgabe wird durch die Tatsache reflektiert, dass in Eukaryoten mehr als 200 nicht-ribosomale Proteine, bezeichnet als trans-wirkende Faktoren, beim Aufbau der beiden ribosomalen Untereinheiten helfen. Die Identität dieser Faktoren stammt hauptsächlich aus Studien, welche in Hefe durchgeführt wurden, jedoch ist überraschenderweise wenig bekannt über die Ribosomensynthese in menschlichen Zellen - trotz ihrer zentralen Rolle für die zelluläre Homöostase. In dieser Arbeit haben wir visuelle Marker in Kombination mit RNAi verwendet, um die Reifungswege beider, prä-40s und prä-60s, ribosomalen Partikel zu verfolgen, was uns ermöglichte, systematisch Faktoren zu identifizieren, die die Synthese von Ribosomen in menschlichen Zellen unterstützen. In einem ersten Schritt untersuchten wir den Beitrag von etwa 500 Kandidatenfaktoren für die Ribosomenproduktion. Diese Gene beinhalteten unter anderem ribosomale Proteine und humane Homologe der Hefe Ribosomensynthesefaktoren. Wir sind in der Lage zu zeigen, dass Kernmerkmale des Ribosomenanfertigung stark zwischen Hefe und Menschen konserviert sind. Jedoch wurden gewisse artspezifische Anpassungen beobachtet, so zum Beispiel ein Beitrag von Exportin 5 zum Export der 60S-Untereinheit aus dem Zellkern in humanen Zellen. In einem zweiten Schritt wurden die Screening-Ansätze infolgedessen auf eine genomische Stufe ausgeweitet, was nicht nur erlaubte das erste Inventar von menschlichen Ribosomenbiogenesefaktoren für beide ribosomale Untereinheiten herzustellen, sondern auch die Übereinstimmungen und Unterschiede zwischen 40S und 60S Reifung beleuchtete. Interessanterweise ist die Biogenese der 40S Untereinheiten sehr empfindlich gegenüber starken 60S Reifungsdefekten, was V
6 durch die Anwesenheit von RPL Proteinen in beiden Trefferlisten angezeigt wird. Im Gegensatz dazu hatte eine Depletion von RPS Proteinen und 40S Biogenesefaktoren keinen Einfluss auf 60S Biogenese in ähnlichem Ausmass, was andeutet, dass ein Ungleichgewicht in der Produktion der 60S-Untereinheit von Zellen erfasst wird, um das Gleichgewicht zwischen den Untereinheiten zu erhalten. Ein weiterer identifizierter zellulärer Knotenpunkt, der für die Ribosomenproduktion benötigt wird, ist das Ubiquitin-Proteasom-System. Eine gestörte Proteasomfunktion beeinflusst frühe Biogenese Schritte beider Untereinheiten. Unsere Daten deuten auf eine mögliche Beteiligung von CUL4- RING E3 Ubiquitin Ligasen in diesem Prozess hin. Bemerkenswert ist, dass wir einen neuen, Vertebraten spezifischen Ribobosomensynthesefaktor, genannt RBIS identifiziert haben, der nach der rrna Transkription wirkt und die Reifung beider ribosomalen Untereinheiten unterstützt, angedeutet durch nukleoplasmatische Anhäufung von prä-40s und prä-60s Partikeln, und einer Reduktion von reifer 18S und 28S rrna nach dessen Depletion. Wir erbringen den Nachweis, dass RBIS auf prä-ribosomalen Partikeln vorhanden ist. Basierend auf seiner verblüffenden Ähnlichkeit mit ribosomalen Proteinen ist es wahrscheinlich, dass dieser Faktor fähig ist, an das negativ geladene rrna Rückgrat zu binden. Die Wichtigkeit von RBIS in der Produktion von Ribosomen wurde durch seine konservierte Funktion in zahlreichen verschiedenen menschlichen Zelllinien zusätzlich untermauert. Darüber hinaus, haben unsere Daten eine zentrale Rolle für GLUL, der menschlichen Glutaminsynthetase, in der Ribosomensynthese enthüllt. Interessanterweise erschien insbesondere die effiziente Produktion von 40S- Untereinheiten überempfindlich nicht nur auf Veränderungen des extrazellulären Glutaminpegels, sondern benötigte auch intrazelluläre Glutaminsynthese. VI
7 Zahlreiche Krebszellen sind abhängig von Glutamin und dies könnte verbunden sein mit der massiven Produktion von Ribosomen in diesen Zellen. Zusammengefasst erlaubten unsere Screening Ansätze das Erzeugen eines ersten Überblicks über menschliche Ribosomensynthesefaktoren für beide ribosomale Untereinheiten auf einer genomischen Stufe. Bemerkenswerterweise wurden mehrere der identifizierten Gene mit menschlichen Krankheiten in Verbindung gebracht, oftmals assoziiert mit Krebsanfälligkeit. Dies betont die zentrale Rolle der Ribosomensynthese für die Homöostase des ganzen Organismus und es ist wahrscheinlich, dass noch mehr krankheitsverursachende Mutationen in Genen, die für Ribosomensynthesefaktoren kodieren, entdeckt werden könnten. VII
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