Notochord-derived hedgehog is essential for tail regeneration in Xenopus tadpole

Yuka Taniguchi,Makoto Mochii,Kenji Watanabe

doi:10.1186/1471-213x-14-27

Abstract

BackgroundAppendage regeneration in amphibians is regulated by the combinatorial actions of signaling molecules. The requirement of molecules secreted from specific tissues is reflected by the observation that the whole process of regeneration can be inhibited if a certain tissue is removed from the amputated stump. Interestingly, urodeles and anurans show different tissue dependencies during tail regeneration. The spinal cord is essential for tail regeneration in urodele but not in anuran larva, whereas the notochord but not the spinal cord is essential for tail regeneration in anuran tadpoles. Sonic hedgehog is one of the signaling molecules responsible for such phenomenon in axolotl, as hedgehog signaling is essential for overall tail regeneration and sonic hedgehog is exclusively expressed in the spinal cord. In order to know whether hedgehog signaling is involved in the molecular mechanism underlying the inconsistent tissue dependency for tail regeneration between anurans and urodeles, we investigated expression of hedgehog signal-related genes in the regenerating tail of Xenopus tadpole and examined the effect of the hedgehog signal inhibitor, cyclopamine, on the tail regeneration.ResultsIn Xenopus, sonic hedgehog is expressed exclusively in the notochord but not in the spinal cord of the regenerate. Overall regeneration was severely impaired in cyclopamine-treated tadpoles. Notochord maturation in the regenerate, including cell alignment and vacuolation, and myofiber formation were inhibited. Proliferation of spinal cord cells in the neural ampulla and of mesenchymal cells was also impaired.ConclusionAs in the axolotl, hedgehog signaling is required for multiple steps in tail regeneration in the Xenopus tadpole, although the location of the Shh source is quite different between the two species. This difference in Shh localization is the likely basis for the differing tissue requirement for tail regeneration between urodeles and anurans.

Highlights

Appendage regeneration in amphibians is regulated by the combinatorial actions of signaling molecules
Reverse transcription-polymerase chain reaction (RT-PCR) showed that shh and bhh were expressed in the regenerating tail but cephalic/desert hedgehogs were not (Figure 1A)
In axolotl shh is exclusively expressed in the regenerating spinal cord during tail regeneration [13], whereas a previous study suggested that it is expressed in the regenerating notochord but not in the regenerating spinal cord in Xenopus larva [23]

Summary

Introduction

Appendage regeneration in amphibians is regulated by the combinatorial actions of signaling molecules. Urodeles and anurans show different tissue dependencies during tail regeneration. In order to know whether hedgehog signaling is involved in the molecular mechanism underlying the inconsistent tissue dependency for tail regeneration between anurans and urodeles, we investigated expression of hedgehog signal-related genes in the regenerating tail of Xenopus tadpole and examined the effect of the hedgehog signal inhibitor, cyclopamine, on the tail regeneration. Multiple signaling molecules have critical roles both in anuran and urodele tail regeneration. A significant role of FGFs and Wnts has been suggested by their expression patterns during tail regeneration in adult or larval salamander [14,15,16,17]. A considerable number of signaling mechanisms are thought to be shared between anurans and urodeles during tail regeneration

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Results

Conclusion