Research Collection. Doctoral Thesis. ETH Library. Author(s): Kälin, Roland. Publication Date: 2005
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1 Research Collection Doctoral Thesis Studies on vertebrate vascular development: The role of apelin signaling in angiogenesis and molecular characterzation of lymphangiogenesis in Xenopus Author(s): Kälin, Roland Publication Date: 2005 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 Doctoral Thesis ETH No Studies on vertebrate vascular development: Tbe role of apelin signaling in angiogenesis and molecular cbaracterization oflympbangiogenesis in Xenopus A dissertation submitted to the SWISS FEDERAL INSTITUTE OF TECHNOLOGY ZURlCH for the degree of Doctor ofnatural Seiences presented by ROLAND KÄLIN Diploma of'biochemistry, Universität Basel bom citizen ofeinsiedeln, Schwyz accepted on the recommendation of Prof. Dr. Andre Brändli, examiner Prof. Dr. Dario Neri, co-examiner 2005
3 Summary Summary Over the last years, amphibians have become a convenient model system for studies on vascular deve1opment. In Xenopus, the heart starts to beat two days after fertilization assuring blood circulation and further growth. Thus, the circulatory system constitutes the first functional organ and its organization resembles the embryonie structure ofthe human vascular system. Moreover its development involves similar molecular and cellular processes as the increasingly complex vasculature ofhigher vertebrates. The central objective ofthis thesis was to dissect the role ofthe 0 protein-coupled receptor AP] and its ligand apelin in vasculature development. Towards this aim novel molecular markers for the development of the Xenopus embryonie vasculature were identified and characterized. In the course of this work, I discovered that the Xenopus embryo represents an attractive vertebrate model for studies on the development and function of the lymphatic vascular system. In a first study, I identified and characterized Xenopus cdnas encoding two genes, VEGFRI and PECAMI, which are important for vertebrate vascular development. VEGFRI is a member of the VEOF receptor tyrosine kinase family required for vascular development in the mouse and the adhesion moleeule PECAMI is extensively used as a standard molecular marker for the vasculature in mammals and in human pathology. Key studies in Xenopus demonstrate that VEGFRI is expressed in the early vasculature during specification of the angioblast Iineage, while PECAMI expression is confined to the endothelial cells during vascular maturation. These findings establish novel markers ofvascular development for the Xenopus model system, In addition, I developed microangiography as a tool to visualize the functional vasculature ofxenopus tadpoles. Microangiography offers the advantage of visualizing the entire patent vasculature. Furthermore, this technique permits studies on blood vessel structure and function in the Iiving tadpole. The G protein-coupled receptor Msr has been a popular molecular marker for vascular development inxenopus. However, the function ofmsr in embryonie vascular development is unknown. Msr is the Xenopus orthologue ofthe mammalian OPCR APJ. In the second study of this thesis, Ireport that APJ/Msr and its ligand apelin regulate angiogenic sprouting in the Xenopus embryo, Comparison ofgene expression in Xenopus and mouse revealed that apelin expression occurs in elose vicinity ofapj-expressing cells. Apelin expression is however restricted to regions of angiogenesis. Loss-of-function of either gene in Xenopus specifically 5
4 Summary bloeked outgrowth ofthe intersomitie vessels, while apelin gain-of-function lead to premature outgrowth ofintersomitie vessels. Furthermore, I demonstrate that apelin aets ehemotaetieally on primary human endothelial eells. Apelin expression was induced by VEGFA overexpression in the Xenopus embryo and both genes showed a synergistie effeet on vasculogenesis of the vitelline veins and angiogenie sprouting of the intersomitie vessels. Finally, analysis ofpathologieal tissue sampies indicated that apelin and AP] expression were upregulated in human brain tumor. Taken together, my studies define apelin-apj signaling as a novel, essential regulator ofangiogenesis with a possible role in tumor angiogenesis. Besides the arterial and venous vasculature, the lymphatic system represents a further important but much underappreciated component ofthe bodies vascular system. Mouse and human genetics have to date provided mueh towards our knowledge about the key molecular players regulating lymphatic development. In the final study presented here, I assessed whether the Xenopus embryo would represent an alternative experimental model for studies on vertebrate lymphangiogenesis. In a first step, I developed a novel method, which permits specifie fluoreseent labeling oflymphatic endothelial cells in vivo. Next, I identified Xenopus cdnas eneoding key regulators and markers of mammalian lymphatic development. Expression pattern analysis revealed that, similar to mammals, the Xenopus lymphatic system develops by sprouting from the posterior eardinal vein. Finally, I demonstrate that VEGFC loss-of-function specifically disrupts lymphangiogenesis in the Xenopus embryo. These findings indicate that lymphangiogenesis in Xenopus and mammals appears to be controlled by the same evolutionary conserved VEGFC-dependent signaling patbway. In summary, the present thesis describes novel methodology to visualize the blood and lymphatic vasculature in the living Xenopus tadpole. Several new vascular and lymphatic markers are eharaeterized, whieh will be invaluable tools in future studies. The diseovery of the apelin-apj signaling system as a novel essential regulator ofangiogenesis provides new perspeetives for therapeutic intervention in pathologieal angiogenesis. Finally, my work on lymphangiogenesis in the Xenopus embryo modellays the foundation for future studies on the development and function ofthe lymphatie vaseular system in vertebrates. 6
5 Zusammenfassung Zusammenfassung Im Verlaufe der letzten Jahre sind die Amphibien zu einem praktischen Studienmodell für die Blutgefässentwicklung geworden. Im Frosch Xenopus laevis beginnt das Herz bereits zwei Tage nach der Befruchtung zu schlagen. Die Blutzirkulation ermöglicht somit das weitere Wachstum des Froschembryos. Deshalb kann das Kreislaufsystem als das erste funktionierende Organ im frühen Embryo betrachtet werden. Sein Aufbau gleicht der embryonalen Struktur des menschlichen Blutgefässsystems. Im weiteren sind in dessen embryonalen Entwicklung dieselben molekularen und zellulären Mechanismen beteiligt, wie im immer komplexer werdenden Blutgefässsystem der höheren Wirbeltiere. Die Hauptziele meiner Doktorarbeit waren die Entschlüsselung der Rolle des G proteingekoppelten Rezeptors APJ und seines Liganden Apelin während der Blutgefässentwicklung, Auf dem Weg dazu wurden neue Blutgefässmarker identifiziert und charakterisiert. Im Verlaufe dieser Arbeit habe ich ebenfalls entdeckt, dass der Xenopus-Embryo ein attraktives Wirbeltiermodell für Studien über die Entwicklung und Funktion des Lymphsystems darstellt. In einer ersten Studie habe ich Xenopus-cDNAs, die für VEGFRI und PECAMI kodieren, identifiziert und charakterisiert. Beide Gene sind wichtig für die Entwicklung des Blutgefässsystems. VEGFR1 ist ein Rezeptor für den Blutgefässwachstumsfaktor VEGF und gehört zur Familie der Tyrosinkinaserezeptoren. An Mäusen wurde gezeigt, dass dieser Rezeptor für die Blutgefässentwicklung notwendig ist. PECAM I ist ein Adhäsionsmolekül von Blutgefässzellen und wird als molekularer Standardmarker für die Blutgefässe der Säugetiere und die humane Pathologie umfassend genutzt. Schlüsselexperimente im Xenopus demonstrieren, dass VEGFRI im friihen Blutgefässsystern während der Differenzierung der Angioblasten exprimiert ist, wogegen PECAMI ein Marker für die spätere Reifung der Blutgefässe ist. Diese Resultate etablieren neue Marker für die Blutgefässentwicklung im Xenopus Modellsystem. Um die funktionellen Blutgefässe im Frosch sichtbar zu machen, habe ich zusätzlich die Technik der Mikroangiographie an das Xenopus-Tiermodell angepasst. Die Mikroangiographie hat den Vorteil, dass sie die reifen Blutgefässe in ihrer Gesamtheit zeigt. Dazu erlaubt sie strukturelle und funktionelle Studien in der lebenden Kaulquappe. Der G protein-gekoppelte Rezeptor Msr wurde schon früher als molekularer Marker für die Entwicklung der Blutgefässsysteme im Xenopus genutzt. Die Funktion von Msr in der embryonalen Blutgefässentwicklung ist jedoch unbekannt. Msr ist das Xenopus-Gegenstück zum G protein-gekoppelten Rezeptor APJ, bekannt in Wirbeltieren. In der zweiten Studie 7
6 Zusammenfassung dieser Doktorarbeit berichte ich darüber, dass APJ/Msr und sein Ligand Apelin das Spriessen der Blutgefässe während der Angiogenese in Xenopus-Embryonen regulieren. Vergleiche der Genexpression in Maus und Xenopus enthüllten, dass Apelin in der Nähe von APJexprimierenden Zellen vorkommt. Apelinexpression ist jedoch auf Regionen laufender Angiogenese beschränkt. Funktionsverluststudien beider Gene blockierten im speziellen das Auswachsen von intersomitischen Blutgefässen, während Funktionsgewinnstudien zu verfrühtem Auswachsen dieser Gefässe zwischen den zukünftigen Rückenwirbeln führten. Im weiteren zeige ich, dass Apelin in der Zellkultur chemotaktisch aufhumane Blutgefässzellen wirkt. Durch die Überexpression von VEGF wurde im Xenopus-Embryo die Expression von Apelin induziert und beide Gene zusammen zeigten einen gesteigerten Effekt auf die Vaskulogenese der Venen des Dottersacks und das Spriessen der intersomitischen Gefässe in der Angiogenese. Schliesslich hat die Analyse von pathologischem Tumorgewebe gezeigt, dass die Apelin- und APJ-Expression in menschlichen Hirntumoren erhöht ist. Zusammengefasst definieren meine Studien Apelin und APJ als essentielle Regulatoren der Angiogenese mit einer möglichen Rolle in der Tumorangiogenese. Neben den arteriellen und venösen Blutgefässen sind die Lymphgefässe ein weiterer, jedoch ziemlich unbekannter, Teil des Gefässystems des Körpers. Bis heute haben vor allem genetische Studien in Maus und Mensch viel zu unserem Verständnis über die molekularen Schlüsselregulatoren in der Entwicklung der Lymphgefässe beigetragen. In der letzten vorgelegten Arbeit habe ich getestet, ob der Xenopus-Embryo ein alternatives Modelsystem für Studien über die Lymphangiogenese in Wirbeltieren darstellen könnte. In einem ersten Schritt habe ich eine neue Methode entwickelt, die es erlaubt, Lymphgefässzellen in vivo spezifisch fluoreszent zu markieren. Als nächstes habe ich Xenopus-cDNAs identifiziert, welche Schlüsselregulatoren und wichtige Marker für die Lymphgefässentwicklung in Säugetieren kodieren. Die Analyse ihrer Expressionsmuster hat aufgezeigt, dass das Lymphgefässsystem im Xenopus, ähnlich wie bei den Säugetieren, über Sprossung aus der posterioren Kardinalvene hervorgeht. Schlussendlich konnte ich in einer Funktionsverluststudie von VEGFC spezifisch die Lymphangiogenese im Xenopus-Embryo unterbrechen. Diese Resultate weisen darauf hin, dass Lymphangiogenese in Xenopus und in Säugetieren auf gleiche Weise, und zwar über den VEGFC-abhängigen Signalprozess, gesteuert wird. Zusammengefasst beschreibt die vorgelegte Dissertation neue Methoden um Blut- und Lymphgefässe in der lebenden Kaulquappe zu visualisieren. Mehrere neuartige Marker für das Blut- und das Lymphgefässsystem wurden charakterisiert, welche unverzichtbare Werkzeuge 8
7 Zusammenfassung für zukünftige Studien darstellen. Die Entdeckung des Apelin-APJ-Signalsystems als ein neuartiger Regulationsmechanismus für die Angiogenese eröffnet neue Möglichkeiten für therapeutische Interventionen, was die pathologische Angiogenese betrifft. Schliesslich legt meine Arbeit über die Entwicklung und Funktion der Lymphangiogenese im Xenopus-Embryo den Grundstein für zukünftige Studien über das Lymphgefässsystem der Wirbeltiere. 9
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