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

  1. Tania Rozario  Is a corresponding author
  2. Edward B Quinn
  3. Jianbin Wang
  4. Richard E Davis
  5. Phillip A Newmark  Is a corresponding author
  1. Morgridge Institute for Research, United States
  2. University of Colorado School of Medicine, United States

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.

The following data sets were generated

Article and author information

Author details

  1. Tania Rozario

    Morgridge Institute for Research, Madison, United States
    For correspondence
    TRozario@morgridge.org
    Competing interests
    No competing interests declared.
  2. Edward B Quinn

    Morgridge Institute for Research, Madison, United States
    Competing interests
    No competing interests declared.
  3. Jianbin Wang

    Department of Biochemistry and Molecular Genetics, University of Colorado School of Medicine, Aurora, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3155-894X
  4. Richard E Davis

    Department of Biochemistry and Molecular Genetics, University of Colorado School of Medicine, Aurora, United States
    Competing interests
    No competing interests declared.
  5. Phillip A Newmark

    Morgridge Institute for Research, Madison, United States
    For correspondence
    pnewmark@morgridge.org
    Competing interests
    Phillip A Newmark, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0793-022X

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

  1. Yukiko M Yamashita, University of Michigan, United States

Publication history

  1. Received: June 1, 2019
  2. Accepted: September 10, 2019
  3. Accepted Manuscript published: September 24, 2019 (version 1)
  4. 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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  1. Tania Rozario
  2. Edward B Quinn
  3. Jianbin Wang
  4. Richard E Davis
  5. Phillip A Newmark
(2019)
Region-specific regulation of stem cell-driven regeneration in tapeworms
eLife 8:e48958.
https://doi.org/10.7554/eLife.48958

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