Region-specific regulation of stem cell-driven regeneration in tapeworms

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...

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Main Authors: Tania Rozario, Edward B Quinn, Jianbin Wang, Richard E Davis, Phillip A Newmark
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2019-09-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/48958
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author Tania Rozario
Edward B Quinn
Jianbin Wang
Richard E Davis
Phillip A Newmark
author_facet Tania Rozario
Edward B Quinn
Jianbin Wang
Richard E Davis
Phillip A Newmark
author_sort Tania Rozario
collection DOAJ
description 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.
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spelling doaj.art-4e42654e7ffe452ebabe5752e4b98af02022-12-22T03:33:51ZengeLife Sciences Publications LtdeLife2050-084X2019-09-01810.7554/eLife.48958Region-specific regulation of stem cell-driven regeneration in tapewormsTania Rozario0https://orcid.org/0000-0002-9971-5211Edward B Quinn1Jianbin Wang2https://orcid.org/0000-0003-3155-894XRichard E Davis3Phillip A Newmark4https://orcid.org/0000-0003-0793-022XMorgridge Institute for Research, Madison, United StatesMorgridge Institute for Research, Madison, United StatesRNA Bioscience Initiative, Department of Biochemistry and Molecular Genetics, University of Colorado School of Medicine, Aurora, United StatesRNA Bioscience Initiative, Department of Biochemistry and Molecular Genetics, University of Colorado School of Medicine, Aurora, United StatesMorgridge Institute for Research, Madison, United States; Howard Hughes Medical Institute, Chevy Chase, United States; Department of Integrative Biology, University of Wisconsin–Madison, Madison, United StatesTapeworms 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.https://elifesciences.org/articles/48958tapewormHymenolepis diminutacestodeflatwormstem cells
spellingShingle Tania Rozario
Edward B Quinn
Jianbin Wang
Richard E Davis
Phillip A Newmark
Region-specific regulation of stem cell-driven regeneration in tapeworms
eLife
tapeworm
Hymenolepis diminuta
cestode
flatworm
stem cells
title Region-specific regulation of stem cell-driven regeneration in tapeworms
title_full Region-specific regulation of stem cell-driven regeneration in tapeworms
title_fullStr Region-specific regulation of stem cell-driven regeneration in tapeworms
title_full_unstemmed Region-specific regulation of stem cell-driven regeneration in tapeworms
title_short Region-specific regulation of stem cell-driven regeneration in tapeworms
title_sort region specific regulation of stem cell driven regeneration in tapeworms
topic tapeworm
Hymenolepis diminuta
cestode
flatworm
stem cells
url https://elifesciences.org/articles/48958
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AT edwardbquinn regionspecificregulationofstemcelldrivenregenerationintapeworms
AT jianbinwang regionspecificregulationofstemcelldrivenregenerationintapeworms
AT richardedavis regionspecificregulationofstemcelldrivenregenerationintapeworms
AT phillipanewmark regionspecificregulationofstemcelldrivenregenerationintapeworms