Functional characterization of novel human Cul3 E3 ubiquitin ligases in cell cycle regulation
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1 Research Collection Doctoral Thesis Functional characterization of novel human Cul3 E3 ubiquitin ligases in cell cycle regulation Author(s): Märki, Sarah A. Publication Date: 2010 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 N Functional Characterization of Novel Human Cul3 E3 Ubiquitin Ligases in Cell Cycle Regulation A dissertation submitted to ETH ZURICH For the degree of Doctor of Sciences Presented by Sarah Andrea Märki Master of Science, University of Basel Born 26 Aug 1983 Citizen of Schlieren ZH Accepted on the recommendation of Prof. Matthias Peter, examiner Prof. Daniel Gerlich, co examiner Prof. Patrick Meraldi, co examiner 2010
3 Summary 2 Summary During the cell cycle, cells grow, replicate their DNA and distribute their chromosomes to the two daughter cells. These processes are tightly regulated to ensure genomic stability and error free segregation of chromosomes. Cell cycle progression is controlled through timed protein expression, phosphorylation and ubiquitin dependent protein degradation. Within the ubiquitination pathway, substrate specificity is provided by E3 ubiquitin ligases (E3 ligases). Cullins are scaffolding proteins of a family of RING type E3 ligases. Human Cullin 3 (Cul3) assembles E3 ligase complexes with BTB domain containing substrate specific adaptor proteins. We have recently identified Cul3 E3 ligases as novel important regulators of mitosis. Specifically, we found that Cul3 E3 ligase containing the BTB Kelch adaptors KLHL9 and KLHL13 regulates localization of the chromosome passenger complex (CPC) and cytokinesis possibly by mediating ubiquitination of the mitotic kinase Aurora B. The aim of this study was to identify novel Cul3 E3 ligases which regulate the human cell cycle. We analyzed the cellular phenotypes caused by depletion of BTB adaptor proteins we had previously identified as stable interactors of Cul3. Following this approach we identified two new Cul3 E3 ligases which regulate progression through mitosis. The Cul3/KLHL21 E3 ligase is required for CPC translocation to the spindle midzone at anaphase onset, similar to the previously described Cul3/KLHL9/KLHL13 E3 ligase. Interestingly, our data suggests that the BTB Kelch adaptor KLHL21 is a specificity factor for Cul3 mediated ubiquitination of Aurora B at the spindle midzone and thereby ensures recruitment of the CPC and completion of cytokinesis. The Cul3/KLHL22 E3 ligase is required for chromosome alignment at the metaphase plate, possibly by regulating the removal of the mitotic kinase Plk1 from kinetochores. In addition to its role in mitosis, Cul3 has been proposed to regulate DNA replication possibly in a complex with the BTB adaptor proteins BTBD1 and BTBD2 and by mediating the degradation of DNA Topoisomerase 1 (TOP1). In this study we could confirm that Cul3 is required for normal progression through S phase. But, we could not observe a requirement of Cul3/BTBD1/BTBD2 E3 ligase or other Cul3 E3 ligases in proteasomedependent degradation of TOP1 DNA covalent complexes. The data obtained in this study emphasizes the importance of Cul3 E3 ligases as important regulators of mitosis and DNA replication. 4
4 Zusammenfassung 3 Zusammenfassung Während des Zellzyklus wird die genetische Information verdoppelt und auf zwei Tochterzellen verteilt. Die verschiedenen Phasen des Zellzyklus sind exakt aufeinander abgestimmt um genetische Stabilität und fehlerfreie Verteilung der Chromosomen auf die Tochterzellen zu garantieren. Kontrollmechanismen regulieren den korrekten Ablauf des Zellzyklus durch zeitlich abgestimmte Proteinexpression, Proteinphosphorylierung und Ubiquitin abhängigen Proteinabbau. E3 Ubiquitin Ligasen (E3 Ligasen) katalysieren den letzten Schritt der Ubiquitinierungsreaktion und vermitteln den Transfer von Ubiquitin auf Substratproteine. Sie sind daher verantwortlich für die Substratspezifität der Ubiquitinierungsreaktion. Cullin Proteine dienen als Gerüste von Cullin RING E3 Ligasen. Humanes Cullin 3 (Cul3) bildet zusammen mit Adaptor Proteinen, welche eine BTB Domäne enthalten, Cul3 E3 Ligase Komplexe. Wir haben kürzlich gezeigt, dass Cul3 für den normalen Ablauf der Mitose unentbehrlich ist. Cul3 in Komplexen mit den BTB Kelch Adaptoren KLHL9 und KLHL13 reguliert die Lokalisierung des Chromosomalen Passenger Complex (CPC) und die Zytokinese, wahrscheinlich durch Ubiquitinierung der mitotischen Kinase Aurora B. Das Ziel unserer Studie war es, neue Cul3 E3 Ligasen zu finden, welche den menschlichen Zellzyklus regulieren. Um dies zu erreichen haben wir die Expression von BTB Adaptor Proteinen, welche wir in früheren Studien als stabile Interaktoren von Cul3 identifiziert hatten, durch Verwendung von sirna unterbunden und den Phänotyp der so veränderten Zellen studiert. Mit diesem Ansatz haben wir zwei neue Cul3 E3 Ligasen gefunden, welche für die normale Zellteilung unentbehrlich sind. Die Cul3/KLHL21 E3 ligase reguliert die Lokalisierung des CPC zu Beginn der Anaphase, ähnlich wie die früher beschriebene Cul3/KLHL9/KLHL13 E3 Ligase. Unsere neuen Daten deuten darauf hin, dass KLHL21 ein Spezifitätsfaktor für die Ubiquitinierung von Aurora B durch Cul3 E3 Ligasen an der zentralen Spindel ist und dadurch die Rekrutierung des CPC zu den Mikrotubuli und die Zytokinese reguliert. Die Cul3/KLHL22 E3 Ligase ist unentbehrlich für die korrekte Anordnung von bipolar an die Spindelfasern angebundene Chromosomen in der Metaphase und unsere Daten suggerieren, dass Cul3/KLHL22 die mitotische Kinase Plk1 ubiquitiniert und dadurch die Bindung von Plk1 an Kinetochore reguliert. Es wurde gezeigt, dass Cul3, zusätzlich zur etablierten Funktion in der Mitose, auch die DNS Replikation (S Phase) reguliert. Resultate 5
5 Zusammenfassung früherer Studien haben angedeutet, dass Cul3 in einem Komplex mit den BTB Proteinen BTBD1 und BTBD2 den Abbau der DNS Topoisomerase 1 (TOP1) steuern könnte. Wir konnten nun bestätigen, dass Cul3 für eine normale S Phase unentbehrlich ist. Jedoch sehen wir keine Funktion der Cul3/BTBD1/BTBD2 E3 Ligase oder anderer Cul3 E3 Ligasen im Abbau von TOP1. Die Resultate unserer Studie stärken die Bedeutung von Cul3 E3 Ligasen als neue Regulatoren der Mitose und der S Phase. 6
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