Distinct mechanisms underlie oral vs aboral regeneration in the cnidarian Hydractinia echinata.

Brian Bradshaw,Kerry Thompson,Uri Frank

doi:10.7554/elife.05506

Abstract

Cnidarians possess remarkable powers of regeneration, but the cellular and molecular mechanisms underlying this capability are unclear. Studying the hydrozoan Hydractinia echinata we show that a burst of stem cell proliferation occurs following decapitation, forming a blastema at the oral pole within 24 hr. This process is necessary for head regeneration. Knocking down Piwi1, Vasa, Pl10 or Ncol1 expressed by blastema cells inhibited regeneration but not blastema formation. EdU pulse-chase experiments and in vivo tracking of individual transgenic Piwi1(+) stem cells showed that the cellular source for blastema formation is migration of stem cells from a remote area. Surprisingly, no blastema developed at the aboral pole after stolon removal. Instead, polyps transformed into stolons and then budded polyps. Hence, distinct mechanisms act to regenerate different body parts in Hydractinia. This model, where stem cell behavior can be monitored in vivo at single cell resolution, offers new insights for regenerative biology.

Highlights

Cnidarians are renowned for their remarkable ability to regenerate any missing body part
We show that Hydractinia echinata, which is a common colony-forming cnidarian in the European North Atlantic (Figure 1), provides a powerful model system to study the cellular and molecular basis of animal regeneration
We found that knockdown of Piwi1, Vasa, Pl10, or Ncol1 had no visible effect on cell proliferation (Figure 4G)

Summary

Introduction

Cnidarians are renowned for their remarkable ability to regenerate any missing body part. By contrast, proliferation of pluripotent stem cells (called neoblasts) and formation of a mass of undifferentiated cells (called blastema) are required for head, tail, and pharynx regeneration (Reddien and Sanchez Alvarado, 2004; Baguna , 2012; Reddien, 2013; Adler et al, 2014). Urodele amphibians are the only vertebrate tetrapods that can regenerate amputated limbs as adults. They are similar to planarians in their requirement for cell proliferation and blastema formation to complete regeneration, but the cellular source for urodele regeneration is different. Amphibian blastema cells are lineage restricted rather than being pluripotent (Kragl et al, 2009)

Methods

Results

Conclusion