4.5 Article

Schwann cell precursors generate sympathoadrenal system during zebrafish development

Journal

JOURNAL OF NEUROSCIENCE RESEARCH
Volume 99, Issue 10, Pages 2540-2557

Publisher

WILEY
DOI: 10.1002/jnr.24909

Keywords

axons; chromaffin cells; GTX128374; motor neurons; neurogenesis; RRID; AB_162542; RRID; AB_303395; RRID; AB_2313713; RRID; AB_2716636; RRID; AB_2762830; RRID; AB_2762834; RRID; AB_2861427; RRID; AB_2887225; RRID; AB_10615776; RRID; SCR_003070; RRID; SCR_002798; RRID; SCR_007370; RRID; SCR_018163; sympathetic neurons; teleost fish

Categories

Funding

  1. Russian Science Foundation [19-15-00241]
  2. RFBR [19-29-04035]
  3. Paradifference Foundation
  4. Swedish Research Council
  5. Austrian Science Fund (FWF)
  6. Knut and Alice Wallenberg Foundation
  7. Cancer Fonden
  8. EMBO Young Investigator Program
  9. ERC Synergy grant (Kill-Or-Differentiat)
  10. Bertil Hallsten Research Foundation
  11. Russian Science Foundation [19-15-00241] Funding Source: Russian Science Foundation

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Using genetic tracing, it was discovered that a significant proportion of sympathetic neurons and most chromaffin cells in zebrafish originate from Schwann cell precursors during a specific embryonic development period. The conversion of SCPs into neurons and chromaffin cells is ErbB receptor dependent, and these cells migrate along spinal motor axons to reach appropriate target locations. This study highlights the evolutionary conservation of SCP-to-neuron and SCP-to-chromaffin cell transitions in fish and suggests the presence of multipotent SCPs in postnatal vertebrate tissues for regeneration of autonomic neurons and chromaffin cells.
The autonomic portion of the peripheral nervous system orchestrates tissue homeostasis through direct innervation of internal organs, and via release of adrenalin and noradrenalin into the blood flow. The developmental mechanisms behind the formation of autonomic neurons and chromaffin cells are not fully understood. Using genetic tracing, we discovered that a significant proportion of sympathetic neurons in zebrafish originates from Schwann cell precursors (SCPs) during a defined period of embryonic development. Moreover, SCPs give rise to the main portion of the chromaffin cells, as well as to a significant proportion of enteric and other autonomic neurons associated with internal organs. The conversion of SCPs into neuronal and chromaffin cells is ErbB receptor dependent, as the pharmacological inhibition of the ErbB pathway effectively perturbed this transition. Finally, using genetic ablations, we revealed that SCPs producing neurons and chromaffin cells migrate along spinal motor axons to reach appropriate target locations. This study reveals the evolutionary conservation of SCP-to-neuron and SCP-to-chromaffin cell transitions over significant growth periods in fish and highlights relevant cellular-genetic mechanisms. Based on this, we anticipate that multipotent SCPs might be present in postnatal vertebrate tissues, retaining the capacity to regenerate autonomic neurons and chromaffin cells.

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