Research Collection. Mechanisms of neural crest development. Doctoral Thesis. ETH Library. Author(s): Hagedorn, Lilian. Publication Date: 2000
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1 Research Collection Doctoral Thesis Mechanisms of neural crest development Author(s): Hagedorn, Lilian Publication Date: 2000 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 MECHANISMS OF NEURAL CREST DEVELOPMENT A dissertation submitted to the EIDGENOESSISCHE TECHNISCHE HOCHSCHULE (ETH) ZüRICH for the degree of Doctor of Natural Sciences presented by Lilian Hagedorn Diplom- Chemikerin Ruprecht-Karls-Universität Heidelberg, Germany Born October 3, 1968 in Heidelberg, Germany Citizen of Germany Accepted on the recommendation of Prof. Dr. Ueli Suter, examiner Prof. Dr. Martin Schwab, co-examiner Dr. Lukas Sommer, co-examiner April 2000
3 Summary 1. SUMMARY The various cell types 01' the vertebrate peripheral nervous system (PNS) are generared from a migratory population of multipotent embryonie stem cells, the so-called neural crest (NC). A central issue of developmental biology is to understand how an initially multipotent cell becomes fate restricted and gives rise to a variety of distinct cell types at different locations (Edlund and Jessell, 1999). Transplantation and lineage-tracing experirnents in vivo combined with the results of clonal analyses in vitro suggest that neural crest cells gradually undergo restrictions in their developmental potential during migration and at sites 01' differentiation (reviewed in Anderson et al., 1997; Le Douarin, 1986; Le Douarin and ZilJer, 1993). The molecular basis 01' fate restriction in neural crest development is believed to involve exposure to environmental signals (reviewed in Anderson et a1., 1997; Le Douarin and Ziller, 1993). However, the regulatory interactions between extracellular signals and intracellular programs that control determination and differentiation processes are only poor1y understood. In the first part 01' my thesis, I show that pro tein zero (PO) and peripheral myelin protein 22 (PMP22), both prominent components of peripheral myelin, are not only expressed in glial cells long before the onset of myelination but also mark a multipotent cell type in the early dorsal root ganglion (DRO). Comparab1e to neural crest stem cells (NCSC), this PO/PMP22-positive progenitor can be induced with extracellular growth faetors to give rise to neurons, glia, and smooth muscle-like cells, A sirnilar progenitor cell type can be generated frorn NCSC cultures in which the expression 01' PO and PMP22 precedes the appearance of overt glial and neuronal differentiation markers. Single cell analysis identifies this neural crest-derived cell as a multi potent progenitor of the PNS. Strikingly, the PO/PMP22-positive progenitor displays community effects when exposed to extracellular signals. While single PO/PMP22-positive progenitors can generate smooth muscle in responsc to factors 01' the TOFf:) family, progenitor communities interpret TOFf:) signaling differently anel produce autonornic neurons or undergo cell death, but will not generate smooth muscle-like cells. Interestingly, TOFf:) seems to act in a concentration dependent manner on cell communities in contrast to single cells: at low doses neurogenesis is induced, while apoptosis is promoted at high doses of TOFf3. These data are consistent with a model in which cellular assoeiation of postmigratory multipotent progenitors might be involved in the suppression of a non-neural fate in forming peripheral ganglia. Moreover, the expression of PO and PMP22 in multipotent postmigratory progenitors isolated from early DROs and from NCSC cultures reveals that these molecules are not markers for cornmitted neural crest-derived sublineages (Hagedorn, L., Suter, U., and Sommer, L. (1999). PO and PMP22 mark a multipotent 4
4 Summary neural crest-derived cell type that displays community effects 111 response to TGF-ß factors. Development 126, ). In the second part of my thesis, I show that the expression of the Ets domain transcription factor Erm distinguishes satellite glia from Schwarm cells beginning early in rat PNS development. In developing dorsal root ganglia (DRG), Erm is present both in presumptive satellite glia and in neurons. In centrast. Erm is not detectable at any developmental stage in Schwalm cells in peripheral nerves, In addition, Erm is downregulated in DRG-derived glia adopting Schwann cell traits in culture. Thus, Erm is the first described transcription factor expressed in satellite glia but not in Schwann cells. In culture, the Neuregulin1 (NRG1) isoform GGF2 maintains Erm expression in presumptive satellite cells and reinduces Erm expression in DRG-derived glia but not in Schwann cells from sciatic nerve. These data demonstrate that there are intrinsic differences between these glial subtypes in their response to NRG1 signaling. In neural crest cultures, Erm-positive progenitor cells give rise to two distinct glial subtypes: Ermpositive, Oct-ö-negative satellite glia in response to GGF2, and Erm-negative, Oct-öpositive Schwann cells in the presence of serum and the adenylate cyclase activator forskolin. Thus, Erm-positive neural crest-derived progenitor cells and presumptive satellite glia are able to acquire Schwalm cell features. Given the in vivo expression of Erm in peripheral ganglia, this suggests that ganglionic Erm-positive cells may be precursors of Schwarm cells (Hagedorn, L, Paratore, C., Brugnoli, G., Baert, J.-L, Mercader, N., Suter, U., and Sommer, L (2000). The Ets domain transcription factor Erm distinguishes satellite glia from Schwann cells ancl is regulated in satellite cells by neuregulin signaling. Developmental Biology, 219, 44-58). 5
5 Zusammenfassung 2. ZUSAMMENFASSUNG In Wirbeltieren stammen die verschiedenen Zell typen des peripheren Nervensystems (PNS) - Gliazellen und Neuronen - von einer Population multipotenter Vorläuferzellen. den sogenannten Neuralleistenstammzellen, ab. Wie aus einer anfänglich multipotenten Vorläuferzelle eine Vielzahl unterschiedlichster Zellarten an verschiedensten Stellen im Körper entstehen kann, ist heute eine der Kernfragen der modernen Entwicklungsbiologie. Aus Daten von Transplantations- und Markierungsexperimenten in vivo und klonalen Analysen in vitro läßt sich schließen, daß die neuralen Stammzellen wahrscheinlich sukzessive ihr Potenzial auf ihrer Wanderung zu den Zielorganen oder in den Zielorganen selbst verlieren. Es wird angenommen, daß dabei auch Faktoren eme Rolle spielen, die von Geweben oder Zellen aus der näheren Umgebung der sich entwickelnden Vorläuferzellen abgegeben werden. Es ist allerdings nicht genau geklärt, wie diese extrazellulären Faktoren zellintrinsische Programme zur Zelldifferenzierung beeinflussen. Im ersten Teil dieser Arbeit konnte ich zeigen, daß PO und PMP22, beides wichtige Strukturproteine des peripheren Myelins, bereits lange vor Beginn der Myelinisierung von Gliazellen im peripheren Nervensystem exprirniert werden. Darüberhinaus wurde in den frühen Spinalganglien ein neuer, multipotenter Vorläuferzelltyp identifiziert, der sich durch die Expression von PO und PMP22 deutlich von den ebenfalls multipotenten Neuralleistenstammzellen unterscheidet. Durch Zugabe von extrazellulären Wachstumsfaktoren können diese PO/PMP22 positiven Vorläuferzellen zu Gliazellen, Neuronen oder glatten Muske1zellen ausdifferenziert werden. Eine ganz ähnliche Vorläuferzelle kann auch de novo aus Primärkulturen neuraler Stammzellen generiert werden. Auch in diesen Vorläuferzellen werden PO und PMP22 bereits sehr früh, vor anderen glialen oder neuronalen Differenzierungsmarkern. exprimiert. Einzeln und räumlich voneinander isoliert sind diese Zellen multipotent und reagieren auf die Zugabe instruktiver, extrazellulärer Wachstumsfaktoren. Im Verband allerdings scheint das Potenzial der de novo generierten PO/PMP22-positiven Vorläuferzellen reduziert, sie reagieren anders auf die Wachstumsfaktoren als die Einzelzellen: ein Phänomen, das man als "community effect" bezeichnet. Während PO/PMP22-doppelpositive Einzelzellen nach Zugabe von Wachstumsfaktoren aus der TGFß Familie zu glatter Muskulatur ausdifferenzieren, interpretiert der Zellverband das TGFß - Signal völlig neu und differenziert zu autonomen Neuronen oder stirbt. Im Gegensatz zu Einzelzellen scheint TGFß auf den Zellverband dosis abhängig zu wirken: bei niedrigen TGFß Konzentrationen werden hauptsächlich Neuronen produziert, wohingegen hohe TGFß Konzentrationen Zelltod auslösen. Aus a11 diesen Daten läßt sieh ein Modell für die frühe 6
6 Zusammenfassung Entwicklung der Spinalganglien aus multipotenten neuralen Stammzellen ableiten, das erklärt, wie die Bildung nicht - neuraler Gewebe in den sich formenden Zellverbänden der späteren peripheren Ganglien durch "community effects" verhindert wird. Darüberhinaus zeigt die Expression von PO und PMP22 in den oben beschriebenen, multipotenten Vorläuferzelltypen, daß diese Proteine nicht wie früher angenommen Marker für bestimmte Zellinien des peripheren Nervensystems sind. (Hagedorn, L., Suter, U., and Sommer, L. (1999). PO and PMP22 mark a multipotent neural crest-derived cell type that displays community effects in response to TGF-ß factors. Development 126, ). Im zweiten Teil meiner Arbeit konnte ich zeigen, daß sich Satellitenzellen von Schwalmsehen Zellen bereits sehr früh in der Entwicklung des peripheren Nervensystems der Ratte durch die Expression des Transkriptionsfaktors Erm unterscheiden. Während Erm zu keinem Zeitpunkt in Schwannschen Zellen entlang der peripheren Nerven nachgewiesen werden kann, exprimieren sowohl Neuronen als auch Gliazellen in den sich bildenden Spinalganglien diesen ETS Domain Transkriptionsfaktor. Darüberhinaus wird die Expression von Errn in Schwann Zell - ähnlichen Gliazellen, die man in Kultur aus Satellitenzellen generieren kann, herunterreguliert. Erm ist der erste Transkriptionsfaktor, für den gezeigt werden konnte, daß er von Satellitenzellen und nicht von Schwannschen Zellen exprimiert wird. In Kultur ist die Neuregulin 1 (NRG1) Isoform GGF2 in der Lage, die Expression von Erm in aus Spinalganglien isolierten Satellitenzellen aufrecht zu erhalten bzw, zu reinduzieren. In aus peripheren Nerven isolierten, Erm-negativen Schwarmsehen Zellen dagegen konnte die Expression von Erm nicht mit GGF2 induziert werden. Diese Daten zeigen, daß es zellintrinsische Unterschiede zwischen diesen beiden verschiedenen Glia-Subtypen geben muß. Aus Primärkulturen neuraler Stammzellen kann man ebenfalls zwei verschiedene Glia-Subtypen aus Erm-positiven Vorläuferzellen generieren: bei Zugabe von GGF2 Erm-positive, Oct-6-negative Satellitenzellen. bei Zugabe von Serum und Forskolin, einem Adenylat-zyklase-aktivator, Erm-negative, Oct 6-positive SChWa11l1Sche Zellen. Sowohl aus neuralen Stammzellen generierte Ermpositive Vorläuferzellen als auch Satellitenzellen sind also in der Lage, sich zu Schwarm Zell-ähnlichen Gliazellen zu entwickeln. Bedenkt man, daß Erm in vivo in den Spinalganglien exprimiert wird, könnte dies bedeuten, daß Erm-positive Zellen in den frühen Spinalganglien Vorläuferzellen für Schwarmsehe Zellen entlang der peripheren Nerven sind (Hagedorn, L., Paratore, C., Brugnoli, G., Baert, J.-L., Mercader, N., Suter, U., and Sommer, L. (2000). The Ets domain transcription factor Erm distinguishes satellite glia from Schwarm cells and is regulated in satellite cells by neuregulin signaling. Developmental Biology, 219, 44-58). 7
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Pincher-generated Nogo-A signalosomes mediate growth cone collapse and retrograde transport
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Research Collection. Novel modes of protein-rna recognition in post-transcriptional gene regulation studied by NMR spectroscopy.
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Cauchy-Riemann distributions and boundary values of analytic functions
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Ecology and genetics of Crithidia bombi (trypanosomatidae) field study and experimental approach
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Humanes Tenascin Expression in Weichteiltumoren und Nachweis im Serum von Tumorpatienten
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Research Collection. Organic Farming Policy Networks in Europe. Doctoral Thesis. ETH Library. Author(s): Moschitz, Heidrun. Publication Date: 2008
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Contribution to the development of optical sensors for anions
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