The atypical kinase hrio1 is a trans- acting factor in cytoplasmic maturation of the 40S ribosomal subunit

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1 DISS. ETH NO The atypical kinase hrio1 is a trans- acting factor in cytoplasmic maturation of the 40S ribosomal subunit A dissertation submitted to ETH Zurich for the degree of Doctor of Sciences presented by BARBARA WIDMANN Master of Science ETH, ETH Zurich, Switzerland born citizen of Germany accepted on the recommendation of Prof. Ulrike Kutay, examiner Prof. Vikram Panse, co- examiner 2010

2 Summary Summary Ribosomes are huge ribonucleoprotein complexes, which are responsible for cellular protein production. Therefore, it is crucial to the cell to reliably build ribosomes. The biogenesis of the two ribosomal subunits, 40S and 60S, is a highly complex process which requires more than 170 auxiliary factors like kinases, GTPases, helicases, nucleases, chaperones and rrna modifying enzymes. In this thesis we set out to characterize the human kinase Rio1 the yeast homolog of which has been implicated in late steps of 40S biogenesis. hrio1 co- sedimented with 40S- sized particles on sucrose gradients together with several core components of 40S precursors, like henp1, hltv1, hrio2, hnob1 and hdim2. Immunoprecipitation assays and TAP experiments revealed that hrio1 is associated with pre- 40S particles. Although hrio1 is a component of 40S precursors, it is not required for assembly of the pre- 40S particle, since depletion of hrio1 did not significantly alter the composition of the particle. RNAi depletion experiments showed that hrio1 acts as a trans- acting factor in 40S biogenesis, as cytoplasmic maturation of the small ribosomal subunit is stalled in the absence of hrio1. hrio1 depletion caused the 40S trans- acting factors henp1, hltv1, hrio2, hnob1 and hdim2 to accumulate on cytoplasmic pre- 40S particles. Furthermore, the stalled 40S precursors are immature in terms of rrna content, as the last rrna precursor of the small ribosomal subunit, 18S- E pre- rrna, accumulated in the cytoplasm after hrio1 knockdown. Rescue experiments using wildtype or kinase- dead hrio1 revealed, that the kinase activity of hrio1 is dispensable for recycling of henp1, hltv1 and hrio2 from the 40S precursor. However, cytoplasmic release of hdim2 and hnob1 greatly depends on the kinase activity of hrio1. Moreover, overexpression of kinase- dead hrio1 has a strong dominant negative effect on hdim2 and hnob1 and traps these two 40S trans- acting factors on cytoplasmic pre- 40S. To elucidate the molecular function of hrio1 we set out to identify the substrate of hrio1 kinase. We show that hrio1 is active as a kinase as shown by its ability 1

3 Summary to autophosphorylate and to phosphorylate candidate substrates in vitro. Attempts to identify the physiological substrates suggested that hrps3 or hdim2 might be phosphorylated by hrio1. In summary, we could show that the kinase hrio1 functions as a trans- acting factor during the cytoplasmic steps in 40S maturation. 2

4 Zusammenfassung Zusammenfassung Ribosomen sind grosse Komplexe bestehend aus Ribonukleinsäuren und Proteinen, die für die zelluläre Proteinproduktion verantwortlich sind. Daher ist es äusserst wichtig für die Zelle, zuverlässig Ribosomen herzustellen. Die Biogenese der zwei ribosomalen Untereinheiten, 40S und 60S, ist ein sehr komplexer Prozess, der über 170 Helferproteine benötigt, wie zum Beispiel Kinasen, GTPasen, Helikasen, Nukleasen, Chaperone, sowie Enzyme, die die rrns modifizieren. In dieser Arbeit haben wir damit begonnen, die Kinase hrio1 im Menschen, deren Homolog in Hefe mit den späten Reifungsprozessen der 40S Untereinheit in Verbindung gebracht wurde, zu charakterisieren. hrio1 sedimentierte auf Saccharose- Gradienten mit Partikeln der Grösse 40S zusammen mit Hauptbestandteilen von 40S Vorläuferpartikeln wie henp1, hltv1, hrio2, hnob1 und hdim2. Immunopräzipitationsexperimente und TAP Aufreinigungen bestätigten, dass hrio1 mit prä- 40S Partikeln assoziiert ist. Obwohl hrio1 ein Bestandteil von 40S Vorläuferpartikeln ist, wird es nicht für das Zusammensetzen der prä- 40S Partikel benötigt, da die Depletion von hrio1 die Zusammensetzung dieser Partikel nicht signifikant änderte. Depletionsexperimente mit Hilfe von RNAi zeigten, dass hrio1 als 40S Biogenesefaktor in trans fungiert, da beim Fehlen von hrio1 die Reifung der kleinen ribosomalen Untereinheit im Zytoplasma blockiert wird. Depletion von hrio1 verursachte die Anreicherung der 40S Biogenesefaktoren henp1, hltv1, hrio2, hnob1 and hdim2 an zytoplasmatischen prä- 40S Partikeln. Des Weiteren sind diese 40S Vorläuferpartikel auch unreif bezüglich der rrns, da sich die letzte Vorstufe der rrns der kleinen ribosomalen Untereinheit, die 18S- E prä- rrns, im Zytoplasma anreicherte. Überexpression des Wildtyps oder einer inaktiven Mutante von hrio1 in Zellen, in denen hrio1 zuvor mittels RNAi runterreguliert wurde, liessen erkennen, dass die Kinaseaktivität von hrio1 für das Recycling von henp1, hltv1 und hrio2 3

5 Zusammenfassung entbehrlich ist, wohingegen hdim2 und hnob1 nur in Gegenwart von aktivem hrio1 von den prä- ribosomalen Partikeln abgelöst werden können. Zudem hat die inaktive Mutante von hrio1 einen starken dominant- negativen Effekt auf hdim2 und hnob1 und führt dazu, dass hnob1 und hdim2 an zytoplasmatischen prä- 40S Partikeln verbleiben. Um die molekulare Funktion von hrio1 herauszufinden, haben wir begonnen, das Substrat von hrio1 zu identifizieren. Wir zeigen hier, dass hrio1 als Kinase aktiv ist, da hrio1 sowohl sich selbst als auch Substratkandidaten in vitro phosphorylieren kann. Verschiedene Anläufe, das physiologische Substrat von hrio1 zu identifizieren, führten zu der Vermutung, dass hrps3 oder hdim2 von hrio1 phosphoryliert werden könnten. Zusammengefasst konnten wir zeigen, dass die Kinase hrio1 bei der Fertigstellung von 40S ribosomalen Untereinheiten im Zytoplasma als Biogenesefaktor mitwirkt. 4

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