A14 - Arendt

The vertebrate neural crest is a population of migratory multipotent cells that are specified at the lateral border of the neural plate, detach from the tip of the closing neural tube and invade different parts of the body, where they follow different paths of differentiation. Neural crest-derived cells include sympathetic and parasympathetic neurons of the peripheral nervous systems. Likewise, the vertebrate sensory placodes form along and laterally adjacent to the neural plate border and give rise to peripheral sensory neurons, subsets of which also show migratory behaviour. The spatial and temporal cues and the gene regulatory networks controlling neural crest migration and multipotency as well as the subsequent differentiation of the different types of peripheral neurons are subject to intense study, including several groups in the SFB488.

In the pioneer study proposed here, we investigate specification, cell lineage, possible migratory behaviour, differentiation and molecular identity of cell types developing from the lateral neuroectoderm in a marine annelid, the polychaete Platynereis dumerilii. Several lines of evidence indicate that the polychaete lateral neuroectodermal cells are evolutionarily related to neural crest- and placode-derived cell types in the vertebrates: (a) The overall tissue architecture of the annelid neuroectoderm bears striking resemblance to that of the vertebrate neural plate and infolding neural tube; (b) The lateral portion and border of the annelid neuroectoderm expresses vertebrate neural plate border markers (Msx, Dll and Pax3/7) and (c) preliminary evidence indicates that this region of the Platynereis larva gives rise to sensory cells of the peripheral nervous system that, by specific gene expression, correspond to sensory cells that develop from placodes and neural crest in the vertebrates. We aim here at obtaining a complete inventory and characterisation of Platynereis lateral neuroectodermal cell types, including cell lineage, expression profile and axonal outgrowth, for a large-scale comparative analysis of neuroectoderm border cell types in annelids and vertebrates. Also, we propose to elucidate the regulatory network specifying theses cells, to unravel conserved and derived aspects of placode and neural crest specification and to elucidate the evolutionary origin of these highly characteristic vertebrate features.

Experimentally, we will determine the ‘molecular fingerprint’, i.e. the unique aspects of the expression profile, for all cells descendant from the lateral annelid neuroectoderm by a technique newly developed in our lab and so far unique to our animal model, Wholemount In Silico Expression Profiling (WMISEP). This will be complemented by 4D in vivo recordings of Platynereis neurodevelopment to track cellular lineages through larval stages and to identify possible migratory events. We will also characterise axonal projections of identified neuron types using GFP labelling. Next, we will investigate the effect of morpholino oligonucleotide-mediated knockdown of Msx, Dll and Pax3/7 and of other candidate key transcription factors on the expression profile of single cells, taking advantage of WMISEP. Overall effects on gene expression will be assessed by qPCR, microarray and/or second generation sequencing, performed on batches of injected larvae.

Ziel des Projekts ist eine erste molekulare Charakterisierung der Entwicklung von peripheren Neuronen im Nervensystem des Meeresringelwurms Platynereis dumerilii (Annelida). Wie bei Wirbeltieren entwickeln sich die peripheren Neuronen bei Platynereis am Rand der Neuralanlage, und unsere vorläufige Studien haben gezeigt, dass dieser Randbereich bei Platynereis dieselbe hochspezifische Kombination von Transkriptionsfaktoren exprimiert. Unsere Studie wird neue Erkenntnisse über die Evolution der Neuralleistenzellen und der sensorischen Plakoden der Wirbeltiere liefern.

Own project-related publications

Arendt, D., Denes, A. S., Jekely, G., and Tessmar-Raible, K. (2008) The evolution of nervous system centralization. Philos Trans R Soc Lond B Biol Sci 363: 1523-1528

Denes, A. S., Jekely, G., Steinmetz, P. R., Raible, F., Snyman, H., Prud'homme, B., Ferrier, D. E., Balavoine, G., and Arendt, D. (2007) Molecular architecture of annelid nerve cord supports common origin of nervous system centralization in bilateria. Cell 129: 277-288

Jekely, G., and Arendt, D. (2007) Cellular resolution expression profiling using confocal detection of NBT/BCIP precipitate by reflection microscopy. Biotechniques 42: 751-755

Arendt, D., Tessmar-Raible, K., Snyman, H., Dorresteijn, A. W., and Wittbrodt, J. (2004) Ciliary Photoreceptors with a Vertebrate-Type Opsin in an Invertebrate Brain. Science 306: 869-871

Tessmar-Raible, K., Raible, F., Christodoulou, F., Guy, K., Rembold, M., Hausen, H., and Arendt, D. (2007) Conserved sensory-neurosecretory cell types in annelid and fish forebrain: insights into hypothalamus evolution. Cell 129: 1389-1400

Davidson, E. H. (2006) The Regulatory Genome (Burlington, MA: Academic Press (Elsevier)).

Pavlopoulos, A., and Averof, M. (2005) Establishing genetic transformation for comparative developmental studies in the crustacean Parhyale hawaiensis. Proc Natl Acad Sci U S A 102: 7888-7893

Tessmar-Raible, K., and Arendt, D. (2004) New animal models for evolution and development. Genome Biol 6: 303

Arendt, D., Tessmar-Raible, K., Snyman, H., Dorresteijn, A. W., and Wittbrodt, J. (2004) Ciliary Photoreceptors with a Vertebrate-Type Opsin in an Invertebrate Brain. Science 306: 869-871

Detlef Arendt

Institut für Zoologie
Universität Heidelberg

Im Neuenheimer Feld 230
69120 Heidelberg

Phone:  06221-387624
Fax:      06221-387166
email:    arendt(at)embl.de