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

Published in Philosophical transactions - Royal Society. Biological sciences. 2016, vol. 371, no. 1685, 20150040
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.
Keywords Hydra adult neurogenesisPlasticity of epithelial cellsInterstitial stem cellsRNA-seq transcriptomicsFlow cytometry cell sortingHydroxyureaBehaviourCellular biologyDevelopmental biologyEvolution
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Article (Published version) (2.6 MB) - public document Free access
Research group Groupe Galliot
Swiss National Science Foundation: 31003A_149630
Autre: Human Frontier Science Program HFSP grant RGP0016/2010
(ISO format)
WENGER, Yvan, BUZGARIU, Wanda Christa, GALLIOT, Brigitte. Loss of neurogenesis in Hydra leads to compensatory regulation of neurogenic and neurotransmission genes in epithelial cells. In: Philosophical transactions - Royal Society. Biological sciences, 2016, vol. 371, n° 1685, p. 20150040. doi: 10.1098/rstb.2015.0040 https://archive-ouverte.unige.ch/unige:77611

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Deposited on : 2015-11-24

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