Identification of a regeneration-organizing cell in the Xenopus tail

Unlike mammals, tadpoles have a high regenerative potential. To characterize this regenerative response, we performed single-cell RNA sequencing after tail amputation. By comparing naturally occurring regeneration-competent and -incompetent tadpoles, we identified a previously unrecognized cell type...

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Bibliographic Details
Published in:Science (American Association for the Advancement of Science) 2019-05, Vol.364 (6441), p.653-658
Main Authors: Aztekin, C, Hiscock, T W, Marioni, J C, Gurdon, J B, Simons, B D, Jullien, J
Format: Article
Language:English
Subjects:
Ablation
Amphibians
Amputation
Animals
Appendages
Cells (biology)
Embryos
Epidermal Cells - physiology
Epidermis
Epidermis - physiology
Gene sequencing
Grafts
Ligands
mRNA
Physical Disabilities
Progenitor cells
Re-Epithelialization - genetics
Re-Epithelialization - physiology
Regeneration
Relocation
Ribonucleic acid
RNA
Sequence Analysis, RNA - methods
Signaling
Single-Cell Analysis - methods
Tail - physiology
Tails
Transcription
Transcriptome
Transplantation
Vertebrates
Wounds
Xenopus laevis
Xenopus laevis - genetics
Xenopus laevis - physiology
Xenopus Proteins - genetics
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Summary:Unlike mammals, tadpoles have a high regenerative potential. To characterize this regenerative response, we performed single-cell RNA sequencing after tail amputation. By comparing naturally occurring regeneration-competent and -incompetent tadpoles, we identified a previously unrecognized cell type, which we term the regeneration-organizing cell (ROC). ROCs are present in the epidermis during normal tail development and specifically relocalize to the amputation plane of regeneration-competent tadpoles, forming the wound epidermis. Genetic ablation or manual removal of ROCs blocks regeneration, whereas transplantation of ROC-containing grafts induces ectopic outgrowths in early embryos. Transcriptional profiling revealed that ROCs secrete ligands associated with key regenerative pathways, signaling to progenitors to reconstitute lost tissue. These findings reveal the cellular mechanism through which ROCs form the wound epidermis and ensure successful regeneration.
ISSN:0036-8075
1095-9203
1095-9203
DOI:10.1126/science.aav9996