Research Collection. Doctoral Thesis. ETH Library. Author(s): Dinkel, Martin. Publication Date: 2011
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1 Research Collection Doctoral Thesis Regulation of the NoCut Checkpoint and its Interplay with the Abscission Pathway Prevents Premature Fission of the Plasma Membrane in Saccharomyces Cerevisiae Author(s): Dinkel, Martin Publication Date: 2011 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 Regulation of the NoCut checkpoint and its interplay with the abscission pathway prevents premature fission of the plasma membrane in Saccharomyces cerevisiae A dissertation submitted to the ETH ZURICH For the degree of Doctor of Sciences ETH Presented by Martin Dinkel Dipl. Zool., University of Zurich, Switzerland Born Münsterlingen, Switzerland Accepted on the recommendation of Examiner: Prof. Dr. Yves Barral Co-examiner: Prof. Dr. Patrick Meraldi Co-examiner: Prof. Dr. Wolfgang Seufert
3 1 Abstract Abscission is the last step of cytokinesis and ultimately separates the two daughter cells. The faithful coordination of chromosome separation with plasma membrane resolution is therefore crucial for successful cell division. Studies in yeast and mammalian cells have shown that this coordination is regulated by the NoCut checkpoint. This checkpoint delays plasma membrane resolution until all chromosomes have been separated away from the division plane, in order to prevent DNA damage in yeast or tetraploidy in mammalian cells. However, how abscission is inhibited has been unknown. In my thesis, using Saccharomyces cerevisiae as a model organism, we further characterize the proteins Cyk4, Cyk5, and Cyk6, the Rho-GTPase Rho2 and the Rho-GEF Tus1 as members of genetic pathway triggering abscission. Further, we show that Cyk5, Tus1 and Rho2 are the main targets of NoCut to prevent premature plasma membrane resolution. Cyk5 helps to recruit Tus1 to the bud neck, in a myosin-ii dependent manner. Upon NoCut activation, Tus1 and its co-factor Cyk5 are displaced from the cleavage site. This displacement depends on the activation of Aurora B/Ipl1 and the anilin related proteins Boi1 and Boi2. The resulting abscission arrest can be bypassed by expressing a dominant active allele of Rho2. Together, these data defines a Boi1/Boi2/Cyk5/Tus1/Rho2 network that coordinates chromosome segregation with plasma membrane resolution. Interestingly, Boi1 and Boi2 also help recruit Tus1 to the cleavage site after checkpoint satisfaction. Thus, Boi1 and Boi2 have dual roles as checkpoint and abscission factors. In this study, we also provide insight into NoCut regulation. We show that the Nim1-related protein kinase Hsl1 and its co-factor, the arginine N- methyltransferase Hsl7, are checkpoint proteins. We also demonstrate that the conserved RAM pathway, specifically the kinase Cbk1, regulates NoCut function. Finally, we show that Boi2 is activated by the kinases Cbk1, Cdc5, Hsl1 and Ipl1. 7
4 This multi-step regulation modulates Boi2 activity in NoCut, independently of its subcellular localization. Together, our data show that NoCut is a highly regulated network that coordinates abscission with actomyosin ring contraction and chromosome segregation. 8
5 2 Zusammenfassung Die Zelltrennung ist der letzte Schritt der Zytokinese und separiert Tochterzellen endgültig von einander. Eine stringente Koordination zwischen Separierung der Chromosomen und Auflösung der gemeinsamen Plasmamembran ist entscheidend für eine erfolgreiche Zellteilung. Studien in Hefe und menschlichen Zellen haben gezeigt, dass dieses Zusammenspiel mit Hilfe des spezifischen Kontrollpunktes NoCut reguliert wird. Dieser Kontrollpunkt verzögert die Auflösung der gemeinsamen Plasmamembran bis alle Chromosomen aus der Zellteilungsebene entfernt wurden. Dadurch wird eine Schädigung der DNS oder die Entstehung eines mehrfachen Chromosomensatzes verhindert. Wie jedoch die Abtrennung der Zelle reguliert wird war bisher unbekannt. In meiner hier vorgelegten Arbeit beschreibe ich in der Bierhefe Saccharomyces cerevisiae, die Proteine Cyk4, Cyk5, und Cyk6, Rho-GTPase Rho2 und Rho-GEF Tus1, welche einen Abschnitt eines genetischen Pfades bilden, der zur Durchführung der Zellabtrennung notwendig ist. Im Weiteren beschreibe ich, dass Cyk5, Tus1 und Rho2 die Hauptziele des NoCut Kontrollpunktes sind um einen verfrühten Abbau der Plasmamembran zu verhindern. Dabei bestimmen Cyk5 zusammen mit Myosin-II die Positionierung von Tus1 an der Zellteilungsebene. Sobald der Kontrollpunkt NoCut aktiviert ist, wird Tus1 und dessen Interaktionspartner Cyk5 von der Teilungsebene entfernt. Dies geschieht infolge der Aktivierung der Kinase Aurora B/Ipl1 und der Anilin-ähnlichen Proteine Boi1 und Boi2. Der daraus resultierende Stopp im Zellzyklus kann mit dominant aktivierten Rho2 umgangen werden. Zusammen wird mit diesen Daten ein Netzwerk, bestehend aus Boi1/Boi2/Cyk5/Tus1/Rho2, definiert welches die Koordination zwischen der Segregation der Chromosomen und der Auflösung der Plasmamembran ermöglicht. Nach erfolgreichem Durchlaufen des NoCut Kontrollpunktes lokalisiert Tus1 mittels Boi1 und Boi2 zur Teilungsebene. Dadurch wirken Boi1 9
6 und Boi2 sowohl als Teil eines Kontrollpunktes als auch bei der nachfolgenden Abtrennung. Diese Studie gibt auch einen Einblick in die Regulierung von NoCut. Wir zeigen, dass die mit Nim1 verwandte Proteinkinase Hsl1 und dessen Partner Hsl7, eine Arginin N-Methyltransferase, Bestandteile des Kontrollpunktes sind. Weiter können wir aufzeigen, dass der konservierte RAM Pfad, und im besonderen die Kinase Cbk1, NoCut Funktionen regulieren. Schliesslich können wir eine Aktivierung von Boi2 durch die Kinasen Cbk1, Cdc5, Hsl1 und Ipl1 nachweisen. Diese Regulierung verändert die Boi2 Aktivität in mehreren Schritten, wobei die Lokalisierung von Boi2 innerhalb der Zelle unverändert bleibt. Zusammenfassend definieren unsere Daten NoCut als ein in hohem Grade reguliertes Netzwerk, welches die Abtrennung der Zelle mit der Kontraktion des Actomyosinrings sowie der Chromosomentrennung koordiniert. 10
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