Hair follicle epidermal stem cells define a niche for tactile sensation

  1. Chun-Chun Cheng
  2. Ko Tsutsui
  3. Toru Taguchi
  4. Noriko Sanzen
  5. Asako Nakagawa
  6. Kisa Kakiguchi
  7. Shigenobu Yonemura
  8. Chiharu Tanegashima
  9. Sean D Keeley
  10. Hiroshi Kiyonari
  11. Yasuhide Furuta
  12. Yasuko Tomono
  13. Fiona M Watt
  14. Hironobu Fujiwara  Is a corresponding author
  1. RIKEN, Japan
  2. Nagoya University, Japan
  3. Shigei Medical Research Institute, Japan
  4. King's College London, United Kingdom

Abstract

The heterogeneity and compartmentalization of stem cells is a common principle in many epithelia, and is known to function in epithelial maintenance, but its other physiological roles remain elusive. Here we show transcriptional and anatomical contributions of compartmentalized epidermal stem cells (EpSCs) in tactile sensory unit formation in the mouse hair follicle (HF). EpSCs in the follicle upper-bulge, where mechanosensory lanceolate complexes (LCs) innervate, express a unique set of extracellular matrix (ECM) and neurogenesis-related genes. These EpSCs deposit an ECM protein called EGFL6 into the collar matrix, a novel ECM that tightly ensheathes LCs. EGFL6 is required for the proper patterning, touch responses, and av integrin-enrichment of LCs. By maintaining a quiescent original EpSC niche, the old bulge, EpSCs provide anatomically stable HF–LC interfaces, irrespective of the stage of follicle regeneration cycle. Thus, compartmentalized EpSCs provide a niche linking the HF and the nervous system throughout the hair cycle.

Data availability

Fastq files of RNA-seq data have been submitted to NCBI SRA, and these data can be accessed through the BioProject ID: PRJNA342736.All data generated or analysed during this study are included in the Source data files.

The following data sets were generated

Article and author information

Author details

  1. Chun-Chun Cheng

    Center for Biosystems Dynamics Research, RIKEN, Kobe, Japan
    Competing interests
    The authors declare that no competing interests exist.
  2. Ko Tsutsui

    Center for Biosystems Dynamics Research, RIKEN, Kobe, Japan
    Competing interests
    The authors declare that no competing interests exist.
  3. Toru Taguchi

    Research Institute of Environmental Medicine, Nagoya University, Nagoya, Japan
    Competing interests
    The authors declare that no competing interests exist.
  4. Noriko Sanzen

    Center for Biosystems Dynamics Research, RIKEN, Kobe, Japan
    Competing interests
    The authors declare that no competing interests exist.
  5. Asako Nakagawa

    Center for Biosystems Dynamics Research, RIKEN, Kobe, Japan
    Competing interests
    The authors declare that no competing interests exist.
  6. Kisa Kakiguchi

    Center for Biosystems Dynamics Research, RIKEN, Kobe, Japan
    Competing interests
    The authors declare that no competing interests exist.
  7. Shigenobu Yonemura

    Center for Biosystems Dynamics Research, RIKEN, Kobe, Japan
    Competing interests
    The authors declare that no competing interests exist.
  8. Chiharu Tanegashima

    Center for Biosystems Dynamics Research, RIKEN, Kobe, Japan
    Competing interests
    The authors declare that no competing interests exist.
  9. Sean D Keeley

    Center for Biosystems Dynamics Research, RIKEN, Kobe, Japan
    Competing interests
    The authors declare that no competing interests exist.
  10. Hiroshi Kiyonari

    Center for Biosystems Dynamics Research, RIKEN, Kobe, Japan
    Competing interests
    The authors declare that no competing interests exist.
  11. Yasuhide Furuta

    Center for Biosystems Dynamics Research, RIKEN, Kobe, Japan
    Competing interests
    The authors declare that no competing interests exist.
  12. Yasuko Tomono

    Division of Molecular and Cell Biology, Shigei Medical Research Institute, Okayama, Japan
    Competing interests
    The authors declare that no competing interests exist.
  13. Fiona M Watt

    Centre for Stem Cells and Regenerative Medicine, King's College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9151-5154
  14. Hironobu Fujiwara

    Center for Biosystems Dynamics Research, RIKEN, Kobe, Japan
    For correspondence
    hironobu.fujiwara@riken.jp
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0883-3384

Funding

RIKEN (Intramural grant)

  • Hironobu Fujiwara

Japan Society for the Promotion of Science (25122720)

  • Hironobu Fujiwara

Uehara Memorial Foundation

  • Hironobu Fujiwara

Takeda Science Foundation

  • Hironobu Fujiwara

Cosmetology Research Foundation

  • Hironobu Fujiwara

Medical Research Council

  • Fiona M Watt

Biotechnology and Biological Sciences Research Council

  • Fiona M Watt

Wellcome

  • Fiona M Watt

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

Ethics

Animal experimentation: All animal experiments were conducted and performed in accordance with approved Institutional Animal Care and Use Committee protocols (#A2012-03-12).

Reviewing Editor

  1. Valerie Horsley, Yale University, United States

Publication history

  1. Received: June 5, 2018
  2. Accepted: October 24, 2018
  3. Accepted Manuscript published: October 25, 2018 (version 1)
  4. Version of Record published: November 9, 2018 (version 2)

Copyright

© 2018, Cheng 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. Chun-Chun Cheng
  2. Ko Tsutsui
  3. Toru Taguchi
  4. Noriko Sanzen
  5. Asako Nakagawa
  6. Kisa Kakiguchi
  7. Shigenobu Yonemura
  8. Chiharu Tanegashima
  9. Sean D Keeley
  10. Hiroshi Kiyonari
  11. Yasuhide Furuta
  12. Yasuko Tomono
  13. Fiona M Watt
  14. Hironobu Fujiwara
(2018)
Hair follicle epidermal stem cells define a niche for tactile sensation
eLife 7:e38883.
https://doi.org/10.7554/eLife.38883

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