Research Collection. Doctoral Thesis. ETH Library. Author(s): Bänziger-Tobler, Nadja Erika. Publication Date: 2008
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1 Research Collection Doctoral Thesis Identification and targeting of novel receptors and signaling mediators involved in lymphatic vessel formation and function in vitro and in vivo Author(s): Bänziger-Tobler, Nadja Erika Publication Date: 2008 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 Identification and Targeting of Novel Receptors and Signaling Mediators Involved in Lymphatic Vessel Formation and Function in vitro and in vivo. A dissertation submitted to the Swiss Federal Institute of Technology Zurich for the degree of Doctor of Sciences ETH Zürich presented by Nadja Erika Bänziger-Tobler Dipl. Mikrobiol. University of Zurich, Zurich born August 13, 1979 Citizen of Rehetobel (AR) and Urnäsch (AR) Accepted on the recommendation of Prof. Dr. Michael Detmar, examiner Prof. Dr. Dario Neri, co-examiner 2008
3 1 Summary 6
4 1.1 Summary Lymphatic vessel activation plays an important role during the inflammatory response and in cancer progression. Lymphangiogenesis is regulated by several different factors which work together in a complex way. However, the underlying molecular mechanisms and the relative importance of each factor in physiological and pathological lymphangiogenesis are still poorly understood. A deeper knowledge of the importance of receptors and signaling pathways during the process of lymphatic vessel formation and function would further support the understanding of pathological conditions such as chronic inflammation and cancer metastasis and likely accelerate anti-lymphangiogenic drug development. Therefore, the aim of this thesis was to assign receptors and signaling molecules to lymphatic vessel formation and function. For this purpose, different approaches have been taken. In a first step, we aimed to identify novel lymphangiogenic factors. Using comparative transcriptional profiling studies of cultured lymphatic endothelial cells (LEC) versus blood vascular endothelial cells (BVEC), we found that among a number of other genes - growth hormone receptor was expressed at higher levels in LEC than in BVEC. This finding was confirmed by quantitative real-time RT-PCR and by Western blot analyses. In vitro, growth hormone promoted several processes needed for the formation of new vessels. Analysis of lymphatic vessels in healthy skin of bovine growth hormone transgenic mice revealed no alterations. However, transgenic delivery of growth hormone accelerated lymphatic vessel ingrowth into the granulation tissue of full-thickness skin wounds, and intradermal delivery of growth hormone resulted in enlargement and enhanced proliferation of cutaneous lymphatic vessels in wildtype mice. With this study we could assign a new, pro-lymphangiogenic, function to growth hormone and its receptor. 7
5 The second approach taken was based on forward chemical genetics screening using a library of 1,280 small molecules with defined target specificities on Xenopus laevis tadpoles, in a collaboration with Prof. A. Braendli and R. Kaelin. In combination with whole-mount in situ hybridization, this approach allowed us to identify 34 compounds interfering with embryonic lymphatic and/or blood vessel formation in vivo. 25 out of these 34 compounds were also tested on LEC and BVEC proliferation and tube formation in vitro, which revealed a number of molecules directly interfering with endothelial cell function. Several molecules targeting well-known receptors involved in lymphangiogenesis, such as VEGF-receptors, were identified. Additionally, a number of compounds were found that target receptors/signaling mediators which were so far unknown to play a role in lymphangiogenesis. These included adenosine A1 receptors, voltage gated calcium channels and Src-family kinases. As a proofof-concept, the anti-(lymph)angiogenic property of a small molecule adenosine A1 receptor antagonist was further confirmed in a mouse VEGF-A-induced (lymph)angiogenesis model. With this approach, we were able to assign and characterize novel receptors and signaling mediators that are involved in lymphatic vessel formation and function. A Src-family kinase (Lck) inhibitor (abbreviated name: 7Cp) was further investigated and was found to inhibit LEC adhesion, haptotaxis and migration in vitro. Because Lck was described to be exclusively expressed by T-cells, RT-PCR and Western blot analysis were used to identify the Src-family kinases which are present in LEC in vitro. Furthermore, the potential therapeutic potential of 7Cp was characterized during pathological inflammation-based lymphangiogenesis in vivo. With this approach, we identified novel signaling mediators involved in LEC function in vitro and pathological lymphangiogenesis in vivo and confirmed the anti-inflammatory properties of 7Cp. 8
6 1.2 Zusammenfassung Die Aktivierung und Neubildung lymphatischer Gefässe (Lymphangiogenese) spielt eine zentrale Rolle während der entzündlichen Reaktion und der Krebs-Metastasierung. Lymphangiogenese wird durch verschiedenste Faktoren reguliert. Die zugrundeliegenden molekularen Mechanismen und die Wichtigkeit jedes einzelnen Faktors während physiologischer und pathologischer Lymphangiogenese sind jedoch bis heute noch schlecht verstanden. Ein vertieftes Wissen über den Einfluss verschiedenster Rezeptoren, Wachstumsfaktoren und Signaltransduktionswege für die Lymphangiogenese ist dringend nötig: nicht nur würde das Verständnis von Krankheiten wie chronischer Entzündung und Krebsmetastasierung verbessert, sondern vermutlich auch die Entwicklung neuer lymphgefässdeaktivierender Medikamente gefördert. Daher war es das Ziel dieser Arbeit Zellmembranrezeptoren und Signaltransduktionswege der Lymphgefäss-Aktivierung zuzuordnen. Dafür wurden verschiedene Strategien verfolgt. In einem ersten Schritt ging es um die Identifikation neuer Lymphgefäss-aktivierender Faktoren. Dafür haben wir die Genexpressionsprofile von Lymph- und Blutgefässendothelzellen verglichen. Dabei fanden wir, dass die lymphatischen Endothelzellen - mitnunter einer Vielzahl unterschiedlich exprimierter Gene - mehr Wachstumshormon-Rezeptor mrna enthielten als Blutgefäss-Endothelzellen. Dieses Resultat wurde durch reverse Transkriptase PCR bestätigt. Auch auf Proteinebene wurde mittels Immuno-Blot Analysen mehr Wachstumshormon-Rezeptor in lymphatischen Endothelzellen detektiert als in Blutgefäss-Endothelzellen. In Zellkulturversuchen konnten wir zeigen, dass das Wachstumshormon, der Ligand des Wachstumshormonrezeptors, verschiedene Schritte der Gefäss-Neubildung stimulierte. Bereits früher wurde gezeigt, dass das Wachstumshormon einen aktivierenden Effekt auf Blutgefässe hat. Wir haben deshalb Haut Wachstumshormon-überproduzierender Mäuse analysiert, jedoch keine Gefäss- Veränderungen im Vergleich zu wildtyp Mäusen gefunden. Wurde der Haut aber eine Wunde 9
7 zugefügt, führte die Überproduktion von Wachstumshormon zu einem verfrühten Einwachsen neuer Lymphgefässe in die verletzte Region. Als nächstes haben wir Wachtsumshormonabsonderndes Gel in die Haut von wildtyp Mäusen implantiert. Dies führte zur Vergrösserung der Lymphgefässe und zu vermehrter Lymphendothel-Zellteilung. Zusammengefasst konnten wir mit dieser Studie dem Wachstumshormon eine Lymphgefäss-aktivierende Funktion zuordnen. In einer zweiten Studie haben wir eine Bibliothek mit 1'280 chemischen Verbindungen mit eindeutiger Binde-Spezifität auf die Eigenschaft geprüft, die embryonale Gefäss-Entwicklung im Krallenfrosch (Xenopus laevis) zu blockieren (Kollaboration mit Prof. A. Brändli und R. Kälin). Mittels in situ Hybridisierungen konnten wir beweisen, dass 34 Verbindungen der Bibliothek die embryonale Lymph- und Blutgefässbildung vollständig oder teilweise hemmten. Anschliessend wurden 25 dieser 34 Verbindungen in Zellkultur untersucht, ob sie die Teilung und Röhrchen-Bildung von Blutgefäss- und Lymph-Endothelzellen hemmen. Tatsächlich behinderte ein Teil der Moleküle diese Funktionen, was zeigt, dass diese einen direkten hemmenden Effekt auf Endothelzellen haben. Einige dieser Verbindungen blockieren Rezeptoren, von denen bereits bekannt ist, dass sie eine Rolle in der Lymphangiogenese spielen. Andere Verbindungen blockieren Rezeptoren und Signaltransduktionswege, die bis anhin nicht bekannt waren für ihre Rolle während der Lymphangiogenese, wie zum Beispiel die Adenosin A1 Rezeptoren, L-Typ Kalziumkanäle oder die Familie der Src-Kinasen. Der anti-lymphangiogene Effekt eines Adenosin A1 Rezeptor-Antagonisten wurde in einem Mausmodell verifiziert. Mit dieser Studie konnten wir zum ersten Mal zeigen, dass sich der Krallenfrosch als Tiermodell für Analysen in grossem Umfang eignet. Des weiteren konnten wir verschiedenen Rezeptoren und Signal-Mediatoren eine Rolle während der Lymphangiogenese zuordnen. Im Mausmodell konnten wir zeigen, dass Adenosin A1 Rezeptoren tatsächlich eine Rolle während der Lymphangiogenese spielen. 10
8 Ein Inhibitor einer Kinase der Src-Familie (Lck, abgekürzter Name des Moleküls: 7Cp) wurde detaillierter untersucht. Wir fanden, dass 7Cp die Adhäsion, Haptotaxis und Migration kultivierter Lymphendothelzellen blockiert. Lck wurde jedoch bis jetzt fast ausschliesslich in T-Zellen detektiert. Daher war es notwendig zu erforschen, ob Lymphendothelzellen in Kultur Lck exprimieren oder ob 7Cp mit einem anderen Protein kreuzreagiert. Daher untersuchten wir in einem nächsten Schritt, welche Kinasen der Src-Familie in lymphatischen Endothelzellen in vitro präsent sind. Der potentielle therapeutische Effekt von 7Cp wurde in einem Mausmodell für Lymphangiogenese während einer chronischen Ohrenentzündung untersucht. Damit konnten wir zeigen, dass die Familie der Src-kinasen in die Lymphangiogenese involviert ist und dass 7Cp anti-entzündliche Eigenschaften aufweist. 11
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