Loss of neurogenesis inHydraleads to compensatory regulation of neurogenic and neurotransmission genes in epithelial cells

Abstract

Hydra continuously differentiates a sophisticated nervous system made of mechanosensory cells (nematocytes) and sensory–motor and ganglionic neurons from interstitial stem cells. However, this dynamic adult neurogenesis is dispensable for morphogenesis. Indeed animals depleted of their interstitial stem cells and interstitial progenitors lose their active behaviours but maintain their developmental fitness, and regenerate and bud when force-fed. To characterize the impact of the loss of neurogenesis in Hydra, we first performed transcriptomic profiling at five positions along the body axis. We found neurogenic genes predominantly expressed along the central body column, which contains stem cells and progenitors, and neurotransmission genes predominantly expressed at the extremities, where the nervous system is dense. Next, we performed transcriptomics on animals depleted of their interstitial cells by hydroxyurea, colchicine or heat-shock treatment. By crossing these results with cell-type-specific transcriptomics, we identified epithelial genes up-regulated upon loss of neurogenesis: transcription factors (Dlx, Dlx1, DMBX1/Manacle, Ets1, Gli3, KLF11, LMX1A, ZNF436, Shox1), epitheliopeptides (Arminins, PW peptide), neurosignalling components (CAMK1D, DDCl2, Inx1), ligand-ion channel receptors (CHRNA1, NaC7), G-Protein Coupled Receptors and FMRFRL. Hence epitheliomuscular cells seemingly enhance their sensing ability when neurogenesis is compromised. This unsuspected plasticity might reflect the extended multifunctionality of epithelial-like cells in early eumetazoan evolution.

Trends in tissue repair and regeneration

“…Brigitte Galliot (Geneva University, Switzerland) showed that H. vulgaris epithelial cells adapt to the loss of neurogenesis by overexpressing genes with potential neurogenic, neurotransmission or reprogramming functions (Wenger et al, 2016). By contrast, some H. oligactis strains lack this property, and animals rapidly lose regenerative capacity and develop an ageing phenotype.…”

Introduction to ‘Homology and convergence in nervous system evolution’

“…A case in point is made by Galliot and co-workers [25] using Hydra, a genus of Cnidaria, that are characterized by a simple nerve net that interconnects sensory photoreceptors and touch-sensitive mechanosensory and sensory-motor neurons located in their body wall and tentacles. The latter neurons continuously differentiate from interstitial stem cells but perturbation of this mode of adult neurogenesis results in cell-type-specific alterations of gene expression.…”

“…The latter neurons continuously differentiate from interstitial stem cells but perturbation of this mode of adult neurogenesis results in cell-type-specific alterations of gene expression. Wenger et al [25] determine transcriptome data which reveal that epitheliomuscular cells switch on expression of genes encoding proteins involved in neurogenesis and neurotransmission typical for sensory neurons. The authors suggest that ancestral multi-functional epithelial cells in basal metazoans possessed proto-neuronal functions which progressively diversified into more specialized cells during evolution.…”

Can Digital Games Be a Way of Improving the Neuroplasticity in Stroke Damage? Can the Adult Brain Grow New Cells or Rewire Itself in Response to a New Experience?

“…Research indicates that neurogenesis may well continue to occur throughout the human life span, although it occurs less rapidly in adults [13]. Most of the new neurons that form in adults die almost immediately, but the evidence suggests that some cells that can integrate themselves into the existing web of neural connections [14].…”