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The evolution of the neural crest from an annelid perspective: conserved cell types and signaling pathways in Platynereis dumerilii

Lauri, Antonella

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The neural crest is indisputably one of the major vertebrate innovations. Neural crest arises at the neural plate border and is the source of many cell types, such as those of the peripheral nervous system (sensory, autonomic neurons and supporting cells), pigments and cartilage. This region of the neural plate also gives rise to Rohon Beard cells (RBc, primary sensory neurons) that differentiate from the same precursor cells of the neural crest (Rossi, Kaji, & Artinger, 2009), (Jacobson, 1981). Despite the recent proposal for neural crest-like cells in basal chordates (Jeffery, Strickler, & Yamamoto, 2004), and the postulation of the origin of neural crest from migrating Rohon Beard cells -like cells, the evolution of the neural crest remains obscure. The aim of my PhD was to shed light on the evolution of such a special cell population in bilaterians. Using classical whole mount in situs, Edu pulse experiments, live imaging and drug treatments I studied the development of the pax3/7+ lateral neuroectoderm of the marine worm Platynereis dumerilii. I used Platynereis because it is a protostome that retains ancestral features and it has been successfully used in previous studies to investigate cell type evolution. I investigated the lateral trunk region because it has been recently proposed that this domain corresponds topologically and molecularly to the dorsal neural tube, where the vertebrate neural crest originates (Denes et al., 2007) I found that the pax3/7+ territory is set very early in development and expresses Rohon Beard cells and neural crest specific genes, such as prdm1-a , msx, ap-2 and snail. Furthermore, I found that canonical Wnt signaling controls the patterning of the annelid lateral neuroectdoderm, as in vertebrates. Next, I analyzed the fate of the cells emerging from this lateral territory. I found that sensory differentiation genes are turned on in ngn+ precursor neurons in a temporal sequence, similar to the one occurring in the neural crest derived sensory neurons (Marmigère & Ernfors, 2007), (Lallemend & Ernfors, 2012). The annelid neurons that arise from the lateral pax3/7+ domain have molecular features of the Rohon Beard-like cells and visceral sensory neurons. I found that also putative supporting cells ensheathing the axons arise peripherally. Next, I asked whether the other typical cell types that are neural crest-derived in vertebrates are present in Platynereis. I found that MitF + melanoblasts , putative enteric neurons as well as collagenous skeleton are also present in Platynereis, but apparently do not arise from the lateral domain. The development, survival and axon-pathfinding of the neural crest derived-sensory neurons depends on the neurotrophic signaling (Davies, 1994), (Gershon, 1994), (Tessarollo, 1998), (Sieber-Blum, 1998),(Ernsberger, 2009) Furthermore, the evolution of the neural crest has been associated with the emergence of this pathway, considered for long time a vertebrate innovation (Wittbrodt, 2007). This prompted me to search for the neurotrophic molecules in Platynereis dumerilii. I found that all the molecules of the canonical neurotrophic signaling are present in the worm and show vertebrate-like molecular features. They are widely expressed in the nervous system, therefore they likely act during neuronal development. This finding refutes the belief that neurotrophic signaling is a chordate novelty: a hypothesis based on a lack of conservation in other protostomes such as Drosophila (Pulido, Campuzano, Koda, Modolell, & Barbacid, 1992)and Lymnea (Beck et al., 2003) . Collectively, these annelid data suggest that the formation of Rohon Beard-like sensory neurons, putative visceral sensory neurons and supporting cells were already a feature of the cells emerging from the lateral neuroectoderm (a neural plate-like territory) at the dawn of bilaterians. A gradual co-option of genetic modules acting in other tissues into the neural plate-like territory might have driven the evolution of bona fine neural crest.

Item Type: Dissertation
Supervisor: Arendt, Prof. Dr. Detlev
Date of thesis defense: 18 February 2013
Date Deposited: 11 Oct 2013 08:54
Date: 2013
Faculties / Institutes: Service facilities > Centre for Organismal Studies Heidelberg (COS)
Subjects: 000 Generalities, Science
570 Life sciences
590 Zoological sciences
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