Regeneration of the digestive system in the crinoid Himerometra robustipinna occurs by transdifferentiation of neurosecretory-like cells

PLoS One. 2017 Jul 28;12(7):e0182001. doi: 10.1371/journal.pone.0182001. eCollection 2017.

Abstract

The structure and regeneration of the digestive system in the crinoid Himerometra robustipinna (Carpenter, 1881) were studied. The gut comprises a spiral tube forming radial lateral processes, which gives it a five-lobed shape. The digestive tube consists of three segments: esophagus, intestine, and rectum. The epithelia of these segments have different cell compositions. Regeneration of the gut after autotomy of the visceral mass progresses very rapidly. Within 6 h after autotomy, an aggregation consisting of amoebocytes, coelomic epithelial cells and juxtaligamental cells (neurosecretory neurons) forms on the inner surface of the skeletal calyx. At 12 h post-autotomy, transdifferentiation of the juxtaligamental cells starts. At 24 h post-autotomy these cells undergo a mesenchymal-epithelial-like transition, resulting in the formation of the luminal epithelium of the gut. Specialization of the intestinal epithelial cells begins on day 2 post-autotomy. At this stage animals acquire the mouth and anal opening. On day 4 post-autotomy the height of both the enterocytes and the visceral mass gradually increases. Proliferation does not play any noticeable role in gut regeneration. The immersion of animals in a 10-7 M solution of colchicine neither stopped formation of the lost structures nor caused accumulation of mitoses in tissues. Weakly EdU-labeled nuclei were observed in the gut only on day 2 post-autotomy and were not detected at later regeneration stages. Single mitotically dividing cells were recorded during the same period. It is concluded that juxtaligamental cells play a major role in gut regeneration in H. robustipinna. The main mechanisms of morphogenesis are cell migration and transdifferentiation.

MeSH terms

  • Animals
  • Cell Transdifferentiation* / drug effects
  • Colchicine / pharmacology
  • DNA / biosynthesis
  • Echinodermata / cytology*
  • Echinodermata / drug effects
  • Echinodermata / physiology*
  • Epithelium / drug effects
  • Epithelium / ultrastructure
  • Gastrointestinal Tract / drug effects
  • Gastrointestinal Tract / physiology*
  • Gastrointestinal Tract / ultrastructure
  • Imaging, Three-Dimensional
  • Mitosis / drug effects
  • Neurosecretory Systems / cytology*
  • Neurosecretory Systems / drug effects
  • Regeneration / drug effects
  • Regeneration / physiology*
  • Solutions

Substances

  • Solutions
  • DNA
  • Colchicine

Grants and funding

This work was supported by The Russian Foundation for Basic Research (grant № 17-04-01334), http://www.rfbr.ru/rffi/eng for IYD, and Asia Pacific Network for Global Change Research (grant CAF2015-RR13-NMY-Dautova), https://www.apn-gcr.org/ for IYD. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.