Origins of neurogenesis, a cnidarian view

Abstract

New perspectives on the origin of neurogenesis emerged with the identification of genes encoding post-synaptic proteins as well as many "neurogenic" regulators as the NK, Six, Pax, bHLH proteins in the Demosponge genome, a species that might differentiate sensory cells but no neurons. However, poriferans seem to miss some key regulators of the neurogenic circuitry as the Hox/paraHox and Otx-like gene families. Moreover as a general feature, many gene families encoding evolutionarily-conserved signaling proteins and transcription factors were submitted to a wave of gene duplication in the last common eumetazoan ancestor, after Porifera divergence. In contrast gene duplications in the last common bilaterian ancestor, Urbilateria, are limited, except for the bHLH Atonal-class. Hence Cnidaria share with Bilateria a large number of genetic tools. The expression and functional analyses currently available suggest a neurogenic function for numerous orthologs in developing or adult cnidarians where neurogenesis takes place continuously. As an example, in the Hydra polyp, the Clytia medusa and the Acropora coral, the Gsx/cnox2/Anthox-2 ParaHox gene likely supports neurogenesis. Also neurons and nematocytes (mechanosensory cells) share in hydrozoans a common stem cell and several regulatory genes indicating that they can be considered as sister cells. Performed in anthozoan and medusozoan species, these studies should tell us more about the way(s) evolution hazards achieved the transition from epithelial to neuronal cell fate, and about the robustness of the genetic circuitry that allowed neuromuscular transmission to arise and be maintained across evolution.

Retinoic acid signaling and neuronal differentiation

“…For example, the primitive acoelomorph flatworm, Symsagittifera roscoffensis (aka the mint sauce worm), which is considered to represent the earliest extant bilaterian organism, lacks a nerve cord, but possesses neurite bundles that span the A-P axis of the body [76]. Prior to the emergence of more complex bilaterians, nerve ''cords'', ''nets'', and ''rings'' already existed in cnidarians [77,78] It is important to note that the presence of an apparent RAR or RXR in a particular species does not conclusively show that the receptor will bind to RA and regulate gene expression in an RA-dependent manner. For example, Reishia clavigera and Nucella lapillus RARs and RXRs heterodimerize as do their vertebrate counterparts, but tcRAR and nlRAR appear not to be responsive to RA [87,93].…”

Neuroglobins, Pivotal Proteins Associated with Emerging Neural Systems and Precursors of Metazoan Globin Diversity

“…They contain a single-use dart specialized for killing prey. Nematogenesis (the generation of nematocytes) in Cnidaria is used as a model for non-bilaterian neurogenesis (26,48), as these neural cells are continuously generated throughout larval and adult life.…”

The Hydra model: disclosing an apoptosis-driven generator of Wnt-based regeneration

“…At the other extremity, a basal disc (also named foot) secretes a mucous that helps the animal to attach to the substrate ( Figure 1A). Despite this simple anatomy, Hydra is already equipped to elaborate complex behaviors based on neuromuscular transmission 7 . Its two tissue layers contain a dozen cell types that correspond to the basic cell types shared by eumetazoans: typical epithelial cells that also differentiate myofibrils, gland cells that secrete digestive enzymes (also named 'pancreatic cells'), mucous cells, sensory-motor neurons and interneurons named ganglion cells 8 .…”