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Light-at-night exposure affects brain development through pineal allopregnanolone-dependent mechanisms

  1. Shogo Haraguchi  Is a corresponding author
  2. Masaki Kamata
  3. Takuma Tokita
  4. Kei-ichiro Tashiro
  5. Miku Sato
  6. Mitsuki Nozaki
  7. Mayumi Okamoto-Katsuyama
  8. Isao Shimizu
  9. Guofeng Han
  10. Vishwajit Sur Chowdhury
  11. Xiao-Feng Lei
  12. Takuro Miyazaki
  13. Joo-ri Kim-Kaneyama
  14. Tomoya Nakamachi
  15. Kouhei Matsuda
  16. Hirokazu Ohtaki
  17. Toshinobu Tokumoto
  18. Tetsuya Tachibana
  19. Akira Miyazaki
  20. Kazuyoshi Tsutsui  Is a corresponding author
  1. Waseda University, Japan
  2. Kyushu University, Japan
  3. Showa University School of Medicine, Japan
  4. University of Toyama, Japan
  5. Shizuoka University, Japan
  6. Ehime University, Japan
Research Article
  • Cited 4
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Cite this article as: eLife 2019;8:e45306 doi: 10.7554/eLife.45306

Abstract

The molecular mechanisms by which environmental light conditions affect cerebellar development are incompletely understood. We showed that circadian disruption by light-at-night induced Purkinje cell death through pineal allopregnanolone (ALLO) activity during early life in chicks. Light-at-night caused the loss of diurnal variation of pineal ALLO synthesis during early life and led to cerebellar Purkinje cell death, which was suppressed by a daily injection of ALLO. The loss of diurnal variation of pineal ALLO synthesis induced not only reduction in pituitary adenylate cyclase-activating polypeptide (PACAP), a neuroprotective hormone, but also transcriptional repression of the cerebellar Adcyap1 gene that produces PACAP, with subsequent Purkinje cell death. Taken together, pineal ALLO mediated the effect of light on early cerebellar development in chicks.

Article and author information

Author details

  1. Shogo Haraguchi

    Department of Biology, Waseda University, Tokyo, Japan
    For correspondence
    shogo.haraguchi@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8731-3311
  2. Masaki Kamata

    Department of Biology, Waseda University, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.
  3. Takuma Tokita

    Department of Biology, Waseda University, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.
  4. Kei-ichiro Tashiro

    Department of Biology, Waseda University, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.
  5. Miku Sato

    Department of Biology, Waseda University, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.
  6. Mitsuki Nozaki

    Department of Biology, Waseda University, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.
  7. Mayumi Okamoto-Katsuyama

    Department of Applied Chemistry, School of Science and Engineering, Waseda University, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.
  8. Isao Shimizu

    Department of Applied Chemistry, School of Science and Engineering, Waseda University, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.
  9. Guofeng Han

    Laboratory of Stress Physiology and Metabolism, Graduate School of Bioresource and Bioenvironmental Science, Kyushu University, Fukuoka, Japan
    Competing interests
    The authors declare that no competing interests exist.
  10. Vishwajit Sur Chowdhury

    Laboratory of Stress Physiology and Metabolism, Graduate School of Bioresource and Bioenvironmental Science, Kyushu University, Fukuoka, Japan
    Competing interests
    The authors declare that no competing interests exist.
  11. Xiao-Feng Lei

    Department of Biochemistry, Showa University School of Medicine, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.
  12. Takuro Miyazaki

    Department of Biochemistry, Showa University School of Medicine, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.
  13. Joo-ri Kim-Kaneyama

    Department of Biochemistry, Showa University School of Medicine, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.
  14. Tomoya Nakamachi

    Laboratory of Regulatory Biology, Graduate School of Science and Engineering, University of Toyama, Toyama, Japan
    Competing interests
    The authors declare that no competing interests exist.
  15. Kouhei Matsuda

    Laboratory of Regulatory Biology, Graduate School of Science and Engineering, University of Toyama, Toyama, Japan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8253-5230
  16. Hirokazu Ohtaki

    Department of Anatomy, Showa University School of Medicine, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.
  17. Toshinobu Tokumoto

    Integrated Bioscience Section, Graduate School of Science and Technology, Shizuoka University, Shizuoka, Japan
    Competing interests
    The authors declare that no competing interests exist.
  18. Tetsuya Tachibana

    Department of Agrobiological Science, Faculty of Agriculture, Ehime University, Matsuyama, Japan
    Competing interests
    The authors declare that no competing interests exist.
  19. Akira Miyazaki

    Department of Biochemistry, Showa University School of Medicine, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.
  20. Kazuyoshi Tsutsui

    Department of Biology, Waseda University, Tokyo, Japan
    For correspondence
    k-tsutsui@waseda.jp
    Competing interests
    The authors declare that no competing interests exist.

Funding

Japan Society for the Promotion of Science (15K18571)

  • Shogo Haraguchi

Takeda Science Foundation

  • Shogo Haraguchi

Ichiro Kanehara Foundation for the Promotion of Medical Sciences and Medical Care

  • Shogo Haraguchi

Kao Corporation

  • Shogo Haraguchi

Naito Foundation

  • Shogo Haraguchi

Narishige Zoological Science Foundation

  • Shogo Haraguchi

Yamaguchi Endocrine Research Foundation

  • Shogo Haraguchi

Suntory Foundation for Life Sciences

  • Shogo Haraguchi

Japan Society for the Promotion of Science (22227002)

  • Kazuyoshi Tsutsui

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

Ethics

Animal experimentation: The experimental protocols (2011-A090, 2012-A003, 2013-A010, 2014-A063, 2015-A012, 29M050, 30M047) were in accordance with the Guide for the Care and Use of Laboratory Animals of Waseda University or Showa University, Japan.

Reviewing Editor

  1. Vatsala Thirumalai, National Centre for Biological Sciences, India

Publication history

  1. Received: January 18, 2019
  2. Accepted: September 29, 2019
  3. Accepted Manuscript published: September 30, 2019 (version 1)
  4. Version of Record published: November 12, 2019 (version 2)

Copyright

© 2019, Haraguchi 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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