Transient inflammatory response mediated by interleukin-1β is required for proper regeneration in zebrafish fin fold

  1. Tomoya Hasegawa
  2. Christopher J Hall
  3. Philip S Crosier
  4. Gembu Abe
  5. Koichi Kawakami
  6. Akira Kudo
  7. Atsushi Kawakami  Is a corresponding author
  1. Tokyo Institute of Technology, Japan
  2. University of Auckland, New Zealand
  3. Graduate School of Life Sciences, Tohoku University, Japan
  4. National Institute of Genetics, Japan

Abstract

Cellular responses to injury are recognized to be crucial for complete tissue regeneration, but their underlying processes remain incompletely elucidated. We have previously reported that myeloid-defective zebrafish mutants display apoptosis of regenerative cells during fin fold regeneration. Here, we found that the apoptosis phenotype is induced by the prolonged expression of interleukin 1 beta (il1b). Myeloid cells have been considered to be the principal source of Il1b, but we show that epithelial cells express il1b in response to tissue injury and initiate the inflammatory response, and that its resolution by macrophages is necessary for the survival of regenerative cells. We further show that Il1b also plays an essential role in normal fin fold regeneration by regulating the expression of regeneration-induced genes. Our study reveals that proper levels of Il1b signaling and tissue inflammation, which are tuned¬ by macrophages, play a crucial role in tissue regeneration.

Article and author information

Author details

  1. Tomoya Hasegawa

    School of Bioscience and Biotechnology, Tokyo Institute of Technology, Yokohama, Japan
    Competing interests
    The authors declare that no competing interests exist.
  2. Christopher J Hall

    Department of Molecular Medicine and Pathology, School of Medical Sciences, University of Auckland, Auckland, New Zealand
    Competing interests
    The authors declare that no competing interests exist.
  3. Philip S Crosier

    Department of Molecular Medicine and Pathology, School of Medical Sciences, University of Auckland, Auckland, New Zealand
    Competing interests
    The authors declare that no competing interests exist.
  4. Gembu Abe

    Laboratory of Organ Morphogenesis, Department of Developmental Biology and Neurosciences, Graduate School of Life Sciences, Tohoku University, Sendai, Japan
    Competing interests
    The authors declare that no competing interests exist.
  5. Koichi Kawakami

    Division of Molecular and Developmental Biology, National Institute of Genetics, Mishima, Japan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9993-1435
  6. Akira Kudo

    School of Bioscience and Biotechnology, Tokyo Institute of Technology, Yokohama, Japan
    Competing interests
    The authors declare that no competing interests exist.
  7. Atsushi Kawakami

    School of Bioscience and Biotechnology, Tokyo Institute of Technology, Yokohama, Japan
    For correspondence
    atkawaka@bio.titech.ac.jp
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9461-6372

Funding

Japan Society for the Promotion of Science (Grant-in-Aid for Scientific Research (C))

  • Atsushi Kawakami

Japan Agency for Medical Research and Development (National BioResource Project)

  • Koichi Kawakami

Royal Society of New Zealand (Marsden Fund)

  • Christopher J Hall

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Didier YR Stainier, Max Planck Institute for Heart and Lung Research, Germany

Ethics

Animal experimentation: This study was performed in strict accordance with the recommendations in the Act on Welfare and Management of Animals in Japan and the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All of the animals were handled according to the Animal Research Guidelines at Tokyo Institute of Technology. The protocol was approved by the Committee on the Ethics of Animal Experiments of the Tokyo Institute of Technology. All surgery was performed under tricaine (3-aminobenzoic acid ethyl ester) anesthesia, and every effort was made to minimize suffering.

Version history

  1. Received: October 26, 2016
  2. Accepted: February 13, 2017
  3. Accepted Manuscript published: February 23, 2017 (version 1)
  4. Version of Record published: March 21, 2017 (version 2)

Copyright

© 2017, Hasegawa 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. Tomoya Hasegawa
  2. Christopher J Hall
  3. Philip S Crosier
  4. Gembu Abe
  5. Koichi Kawakami
  6. Akira Kudo
  7. Atsushi Kawakami
(2017)
Transient inflammatory response mediated by interleukin-1β is required for proper regeneration in zebrafish fin fold
eLife 6:e22716.
https://doi.org/10.7554/eLife.22716

Share this article

https://doi.org/10.7554/eLife.22716

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