Phosphatases counteracting Aurora B during mitotic exit
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1 Research Collection Doctoral Thesis Phosphatases counteracting Aurora B during mitotic exit Author(s): Wurzenberger, Claudia Katharina Publication Date: 2012 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 Nr Phosphatases counteracting Aurora B during mitotic exit a dissertation submitted to the ETH ZURICH for the degree of Doctor of Sciences presented by CLAUDIA KATHARINA WURZENBERGER M.Sc., Technical University Munich born May 15 th 1983 citizen of Germany accepted on the recommendation of Examiner: Prof. Dr. Patrick Meraldi Co-examiner: Prof. Dr. Daniel W. Gerlich Co-examiner: Prof. Dr. Michael Lampson 2012
3 ABSTRACT Abstract Progression through mitosis is tightly regulated to ensure that each daughter cell inherits one identical copy of each chromosome. The kinase Aurora B controls various steps of cell division, ranging from mitotic spindle assembly and correction of erroneous kinetochore-microtubule attachments to cleavage furrow ingression and abscission. To fulfill these diverse functions, Aurora B translocates from centromeres to the central spindle at anaphase onset. Consistently, the kinase phosphorylates different sets of substrates on chromosomes and kinetochores from prophase to metaphase, and on the central spindle and midbody during cytokinesis. Dephosphorylation of Aurora B sites on chromosomes and kinetochores in anaphase depends on kinase translocation and counteracting phosphatases, but the identity of these phosphatases is poorly defined. The aim of this PhD thesis is to identify phosphatases that counteract Aurora B during mitotic exit, and to characterize their function in chromosome segregation. Image-based RNA interference screening using a Fluorescence resonance energy transfer sensor for Aurora B substrate phosphorylation identified two regulatory subunits of protein phosphatase 1, Repo-Man and Sds22, to be required for timely dephosphorylation of Aurora B sites on chromatin. Depletion of Repo-Man or Sds22 induced inefficient and irregular chromosome segregation in anaphase, which correlated with increased levels of phosphorylated Dsn1, a microtubule-attachment factor, on kinetochores. This suggests Repo-Man and Sds22 are required to switch the kinetochore-microtubule interface from a state that promotes oscillatory movements and error correction in metaphase to stabilized attachments for linear force generation in anaphase. During late stages of cytokinesis, Aurora B prevents furrow regression and tetraploidization in the presence of unsegregated chromatin in the cleavage plane by assembling stable intercellular canals. In this thesis, I performed laser microsurgery on the chromosome bridge and introduced asbestos fibers as mechanical barriers to abscission to show that stabilization of intercellular canals depends on the continued presence of chromatin in the cleavage plane. The results presented here reveal new insights into the mechanisms that ensure faithful chromosome segregation during mitotic exit, after satisfaction of the spindle checkpoint. A detailed understanding of these pathways is crucial, as chromosome missegregation may lead to aneuploidy and chromosomal instability, two hallmarks of cancer cells. -9-
4 ZUSAMMENFASSUNG Zusammenfassung Der Ablauf der Zellteilung ist streng reguliert um sicherzustellen, dass jede Tochterzelle eine identische Kopie jedes Chromosoms erhält. Die Kinase Aurora B reguliert zahlreiche Schritte der Zellteilung vom Aufbau der mitotischen Spindel und der Korrektur fehlerhafter Anhaftungen der Mikrotubuli an Kinetochore bis hin zur Einschnürung einer Zellmembran zwischen den Tochterzellen und der Abszission. Um diese unterschiedlichen Funktionen zu erfüllen, transloziert Aurora B zu Beginn der Anaphase von Centromeren auf die Zentralspindel. Konsistent hierzu phosphoryliert Aurora B unterschiedliche Substrate auf Chromosomen und Kinetochoren von Prophase bis Metaphase, und auf der Zentralspindel und dem Mittelkörper während Zytokinese. Die Dephosphorylierung von Aurora B-Substraten auf Chromosomen und Kinetochoren erfordert die Relokalisation von Aurora B sowie Phosphatasen, welche der Kinase entgegenwirken. Die Identität dieser Phosphatasen ist jedoch weitgehend unerforscht. Das Ziel dieser Arbeit ist es, Phosphatasen, welche in späten Phasen der Zellteilung Aurora B entgegenwirken, zu identifizieren, und deren Funktion in der Segregation der Chromosomen zu charakterisieren. Mithilfe eines Mikroskopie-basierten RNA-Interferenz Screens, bei dem ein Fluoreszenz- Resonanz-Energie-Transfer-Sensor für die Phosphorylierung von Aurora B-Substraten verwendet wurde, konnten zwei Regulatoren von Protein Phosphatase 1, Repo-Man und Sds22, identifiziert werden, welche die rechtzeitige Dephosphorylierung von Aurora B- Substraten auf Chromatin vermitteln. Die Depletion von Repo-Man oder Sds22 führte zu ineffizienter und unregelmässiger Chromosomensegregation in Anaphase, was mit erhöhten Mengen an phosphoryliertem Dsn1, einem Faktor, der die Anhaftung von Mikrotubuli an Kinetochore reguliert, korrelierte. Diese Ergebnisse deuten darauf hin, dass Repo-Man und Sds22 die Schnittstelle zwischen Kinetochoren und Mikrotubuli von einem Status, der oszillierende Bewegungen und die Korrektur fehlerhafter Anhaftungen in Metaphase ermöglicht, hin zu stabilisierten Anhaftungen, welche lineare Chromosomensegregation in Anaphase unterstützen, verändern. In Zellen, in welchen missegregiertes Chromatin in der Teilungsebene zurückbleibt, bildet Aurora B in späten Phasen der Zytokinese stabile interzelluläre Kanäle aus und verhindert dadurch, dass sich die eingezogene Zellmembran zurückzieht und eine tetraploide Tochterzelle entsteht. Im Rahmen dieser Arbeit habe ich mithilfe von intrazellulärer -11-
5 ZUSAMMENFASSUNG Laser-Mikrochirurgie auf missegregiertem Chromatin und mithilfe von Asbestfasern, welche die Zytokinese mechanisch behindern, gezeigt, dass die Stabilität interzellulärer Kanäle die kontinuierliche Anwesenheit von Chromatin in der Teilungsebene erfordert. Die hier vorgestellten Ergebnisse liefern neue Erkenntnisse über die Mechanismen, welche die genaue Aufteilung der Chromosomen in späten Phasen der Zellteilung sicherstellen. Eine genaue Kenntnis dieser Mechanismen ist von grosser Bedeutung, da fehlerhafte Aufteilung von Chromosomen zu krebsähnlichen Zellen mit aneuploiden, instabilen Chromosomensätzen führen kann. -12-
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