Region-specific regulation of stem cell-driven regeneration in tapeworms
Abstract
Tapeworms grow at rates rivaling the fastest-growing metazoan tissues. To propagate they shed large parts of their body; to replace these lost tissues they regenerate proglottids (segments) as part of normal homeostasis. Their remarkable growth and regeneration are fueled by adult somatic stem cells that have yet to be characterized molecularly. Using the rat intestinal tapeworm, Hymenolepis diminuta, we find that regenerative potential is regionally limited to the neck, where head-dependent extrinsic signals create a permissive microenvironment for stem cell-driven regeneration. Using transcriptomic analyses and RNA interference, we characterize and functionally validate regulators of tapeworm growth and regeneration. We find no evidence that stem cells are restricted to the regeneration-competent neck. Instead, lethally irradiated tapeworms can be rescued when cells from either regeneration-competent or regeneration-incompetent regions are transplanted into the neck. Together, the head and neck tissues provide extrinsic cues that regulate stem cells, enabling region-specific regeneration in this parasite.
Data availability
Sequencing data have been deposited in DDB/ENA/Genbank under accession codes GHNR01000000, PRJNA546290, PRJNA546293.
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Hymenolepis diminuta transcriptomeBioProject, PRJNA546290.
Article and author information
Author details
Funding
National Institute of Allergy and Infectious Diseases (R21AI119960)
- Phillip A Newmark
Howard Hughes Medical Institute
- Phillip A Newmark
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Animal experimentation: Rodent care was in accordance with protocols approved by the Institutional Animal Care and Use Committee (IACUC) of the University of Wisconsin-Madison (M005573).
Reviewing Editor
- Yukiko M Yamashita, University of Michigan, United States
Publication history
- Received: June 1, 2019
- Accepted: September 10, 2019
- Accepted Manuscript published: September 24, 2019 (version 1)
- Version of Record published: October 30, 2019 (version 2)
Copyright
© 2019, Rozario et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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