RhoA function in spinal cord and cerebellar development
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1 Research Collection Doctoral Thesis RhoA function in spinal cord and cerebellar development Author(s): Herzog, Dominik Publication Date: 2009 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 RhoA function in spinal cord and cerebellar development A dissertation submitted to ETH ZURICH for the degree of Doctor of Science presented by Dominik Herzog Dipl. Biochem. Universität Potsdam, Germany Born April 11, 1979 in Hannover, Germany Citizen of Germany Accepted on the recommendation of Prof. Dr. Ueli Suter, examiner Prof. Dr. Lukas Sommer, co examiner Dr. João Bettencourt Relvas, co examiner October 2009
3 Summary II Summary Neural stem cells are first found after neural induction of the ectoderm in the neuroepithelium, but persist into adulthood in specialized niches. All cells present in the mature central nervous system are initially derived from the homogeneous pool of proliferating undifferentiated neuroepithelial cells (NEPs). Like other epithelial cells, NEPs are highly polarized, and their maintenance as well as their cell fate decisions and differentiation are strictly controlled by a variety of signalling networks. Small RhoGTPases are central intracellular signalling molecules that are known to regulate a huge range of cellular functions, including stem cell function, and the importance of two well known RhoGTPase family members, Cdc42 and Rac1, has already been shown in the development of the mouse nervous system. In the present work, I was interested in the roles of the small RhoGTPase RhoA in CNS development. Besides its function in the regulation of the cytoskeleton and stress fibre formation, RhoA is also involved in the regulation of cytokinesis, cell cycle progression, mitotic spindle positioning, and cell cell and cell extracellular matrix adhesion, making it an interesting candidate for study of its function in neural stem cell biology. I used the conditional ablation of RhoA in the mouse neuroepithelium to demonstrate the requirement for this signalling molecule in embryonic CNS development. RhoA function is critical for the proliferation and survival of neural stem cells in the developing spinal cord, and additionally I could show that RhoA is needed to ensure the maintenance of cell cell adhesion, likely by regulating mdia1, and thus to preserve the tissue integrity of the neuroepithelium. As the conditional ablation of RhoA in the neuroepithelium led to late embryonic lethality of mutant embryos, I also conditionally ablated RhoA later in neural development in radial glia cells, into which NEPs transform after the onset of neurogenesis. This resulted in postnatal lethality of mutant mice around P20, still allowing me to analyze early postnatal CNS development. Besides showing a similar involvement of RhoA in the proliferation of radial glia cells and in the maintenance of tissue integrity of the ventricular zone and cell cell adhesions in the spinal cord as well as in the cerebellar primordium, I can demonstrate a critical role of RhoA in postnatal cerebellar development. RhoA function is critical for the normal generation of cerebellar lobes and cortical layering, as well as for granule cell precursors to become postmitotic. This could have implications in the formation of 3
4 Summary medulloblastoma, the most common tumour in children. They are thought to originate from granule cells or its precursors and I observed the formation of hyperplasia in RhoA mutant cerebella with the presence of ectopic dividing granule cell precursors. 4
5 Zusammenfassung III Zusammenfassung Neurale Stammzellen bilden sich zuerst im Neuroepithel nach der neuralen Induktion des Mesoderms, bestehen jedoch in speziellen Nischen bis ins Erwachsenenalter im Gehirn fort. Alle Zellen des zentralen Nervensystems (ZNS) gehen auf das homogene Reservoir der proliferierenden undifferenzierten Neuroepithelzellen zurück. Wie auch andere Epithelzellen, so sind die Neuroepithelzellen hochgradig polarisiert. Die Erhaltung als neurale Stammzelle bzw. die Entscheidung zu differenzieren ist über verschiedenen Signalkaskaden genau reguliert. Kleine Rho GTPasen sind zentrale intrazelluläre Signalmoleküle, die dafür bekannt sind eine Vielzahl an zellulären Funktionen zu regulieren, so auch in Stammzellen. Es wurde bereits gezeigt, dass die zwei kleinen RhoGTPasen, Cdc42 and Rac1, einen entscheidenden Einfluss auf die Entwicklung des Nervensystems der Maus nehmen. Ziel der hier präsentierten Arbeit ist es den Einfluss der kleinen GTPase RhoA auf die Entwicklung des zentralen Nervensystems zu zeigen. Abgesehen von seiner Funktion bei der Regulierung des Zellskeletts und der Stressfasern, ist RhoA ebenso an der Regulierung der Zellteilung, des Zellzyklus, der Positionierung des Spindelapparates sowie an der Aufrechterhaltung der interzellulären Zelladhäsion und Zell Substrat Adhäsion beteiligt. Daher ist RhoA ein guter Kandidat, um seine Funktion in neuralen Stammzellen zu untersuchen. Ich zeige durch die konditionale Entfernung des RhoA Genes im Neuroepithel der Maus, daß dieses Signalmolekül wichtig für die normale Embryonalentwicklung des ZNS ist. RhoA sorgt für das Überleben und die Proliferation der neuralen Stammzellen im Rückenmark. Desweiteren wird RhoA für die Aufrechterhaltung der Integrität des Neuroepithels benötigt. RhoA reguliert mdia1, wodurch die Aufrechterhaltung der interzellulären Zelladhäsion gewährleistest wird. Da die konditionale Entfernung von RhoA im Neuroepithel dazu führt, dass die genetisch veränderten Embryonen spät in der Embryonalentwicklung sterben, habe ich das RhoA Gen auch später in der Embryogenese in radialen Gliazellen entfernt. Diese radialen Gliazellen entwickeln sich aus den Neuroepithelzellen nach dem Einsetzen der Neurogenese. Die Entfernung von RhoA in diesen Zellen hat es mir ermöglicht, frühe postnatale Entwicklungsstufen des ZNS zu untersuchen, da diese genetisch veränderten Mäuse erst nach circa 20 Tagen sterben. Desweiteren kann eine wichtige Funktion in der postnatalen Entwicklung des 5
6 Zusammenfassung Kleinhirnes gezeigt werden, zusätzlich zu den Funktionen, die RhoA im embryonalen Rückenmark und der Kleinhirnanlage in radialen Gliazellen hat., ist RhoA wichtig für deren Proliferation, ähnlich wie in den Neuroepithelzellen, und ebenso für die Gewebsintegrität der ventrikulären Zone und der Aufrechterhaltung der interzellulären Adhäsionen. In der postnatalen Entwicklung des Kleinhirns ist RhoA wichtig für die normale Faltung, den normalen Aufbau der Kleinhirnrinde und dafür, daß die Vorläufer der Körnerzellen den Zellzyklus verlassen können und aufhören zu proliferieren. Zusätzlich können im Kleinhirn der genetisch veränderten Mäuse Hyperplasien von Körnerzellvorläufern nachgewiesen werden. Dies könnte dementsprechende Auswirkungen auf die Entstehung von Medulloblastomen haben, da davon ausgegangen wird, dass sich diese aus Körnerzellen oder ihren Vorläufern entwickeln. Medulloblastome stellen bisher eine der häufigsten malignen Tumorerkrankung von Kindern dar. 6
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