The cellular and molecular basis of cnidarian neurogenesis

Abstract

Neurogenesis initiates during early development and it continues through later developmental stages and in adult animals to enable expansion, remodeling, and homeostasis of the nervous system. The generation of nerve cells has been analyzed in detail in few bilaterian model organisms, leaving open many questions about the evolution of this process. As the sister group to bilaterians, cnidarians occupy an informative phylogenetic position to address the early evolution of cellular and molecular aspects of neurogenesis and to understand common principles of neural development. Here we review studies in several cnidarian model systems that have revealed significant similarities and interesting differences compared to neurogenesis in bilaterian species, and between different cnidarian taxa. Cnidarian neurogenesis is currently best understood in the sea anemone Nematostella vectensis, where it includes epithelial neural progenitor cells that express transcription factors of the soxB and atonal families. Notch signaling regulates the number of these neural progenitor cells, achaete-scute and dmrt genes are required for their further development and Wnt and BMP signaling appear to be involved in the patterning of the nervous system. In contrast to many vertebrates and Drosophila, cnidarians have a high capacity to generate neurons throughout their lifetime and during regeneration. Utilizing this feature of cnidarian biology will likely allow gaining new insights into the similarities and differences of embryonic and regenerative neurogenesis. The use of different cnidarian model systems and their expanding experimental toolkits will thus continue to provide a better understanding of evolutionary and developmental aspects of nervous system formation. © 2016 The Authors. WIREs Developmental Biology published by Wiley Periodicals, Inc. How to cite this article:WIREs Dev Biol 2017, 6:e257. doi: 10.1002/wdev.257 INTRODUCTIONC nidarians are an early offshoot in the evolution of animals, having separated from the lineage that led to the emergence of bilaterians more than 600 million years ago. 1 Their importance for understanding the evolution of nervous systems has long been recognized, based both on their phylogenetic position as an outgroup to bilaterians (Figure 1) and on the structure of their nervous system, which is predominantly organized as nerve nets. The cnidarians comprise two major clades, the anthozoans and the medusozoans (Figure 1), 2,3 which separated before 550 million years ago and thus not long after the cnidarian lineage separated from all other animals. 4 Two distinct body forms can be found in cnidarians: sessile polyps, which are tube-shaped animals with a single terminal body opening (called the mouth) surrounded by prey-catching tentacles; This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.and free-s...

Functional studies on the role of Notch signaling in Hydractinia development

“…Hence, the role of Notch in tentacle morphogenesis and nematogenesis seems to be conserved in cnidarians, but its function in neural development requires further research across the phylum. In particular, a role for Notch in de novo adult and embryonic neurogenesis in hydrozoans has yet to be assessed (Rentzsch et al, 2016). Furthermore, genetic approaches have not been utilized in hydrozoan Notch studies.…”

Characterization ofNvLWamide-likeneurons reveals stereotypy inNematostellanerve net development

“…jellyfish, corals, anemones, Hydra, etc.) represent the sister taxon to the bilaterians, and their nervous systems are comprised of a nerve net wherein neurites emanating from neural soma scattered throughout the body form a "net" encompassing the organism (Dunn et al, 2008;Hejnol et al, 2009;Rentzsch et al, 2016a). The phylogenetic position of cnidarians in relationship to bilaterians together with the fact that they have a nerve net, puts this group in a unique position to inform and potentially test hypotheses about the origin and evolution of bilaterian centralized nervous systems.…”

The genome of the jellyfish Clytia hemisphaerica and the evolution of the cnidarian life-cycle

“…We propose that, in Clytia, expression of conserved TFs in the medusa is associated with diverse cell types, notably with the neural and neurosensory functions of a complex nervous system, with continuous expression of certain transcription factors in post-mitotic neurons being necessary to maintain neuronal identity [34]. Members of the Sox, PRDL and Achaete scute (bHLH subfamily) orthology groups, commonly associated with neurogenesis [35,36] are detectable across all life cycle stages in Clytia, so our results are unlikely simply due to a higher production of nerve cells in the medusa.…”