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Hyperactivation of sympathetic nerves drives depletion of melanocyte stem cells

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Listed:
  • Bing Zhang

    (Harvard University and Harvard Stem Cell Institute)

  • Sai Ma

    (Harvard University and Harvard Stem Cell Institute
    Klarman Cell Observatory, Broad Institute of MIT and Harvard
    Massachusetts Institute of Technology)

  • Inbal Rachmin

    (Massachusetts General Hospital, Harvard Medical School)

  • Megan He

    (Harvard University and Harvard Stem Cell Institute
    Harvard University)

  • Pankaj Baral

    (Harvard Medical School)

  • Sekyu Choi

    (Harvard University and Harvard Stem Cell Institute)

  • William A. Gonçalves

    (Federal University of Minas Gerais)

  • Yulia Shwartz

    (Harvard University and Harvard Stem Cell Institute)

  • Eva M. Fast

    (Harvard University and Harvard Stem Cell Institute
    Stem Cell Program and Division of Hematology/Oncology, Boston Children’s Hospital and Dana-Farber Cancer Institute, Harvard Medical School)

  • Yiqun Su

    (Massachusetts General Hospital, Harvard Medical School)

  • Leonard I. Zon

    (Harvard University and Harvard Stem Cell Institute
    Stem Cell Program and Division of Hematology/Oncology, Boston Children’s Hospital and Dana-Farber Cancer Institute, Harvard Medical School
    Howard Hughes Medical Institute)

  • Aviv Regev

    (Klarman Cell Observatory, Broad Institute of MIT and Harvard
    Massachusetts Institute of Technology
    Howard Hughes Medical Institute)

  • Jason D. Buenrostro

    (Harvard University and Harvard Stem Cell Institute)

  • Thiago M. Cunha

    (Harvard Medical School
    University of São Paulo)

  • Isaac M. Chiu

    (Harvard Medical School)

  • David E. Fisher

    (Massachusetts General Hospital, Harvard Medical School)

  • Ya-Chieh Hsu

    (Harvard University and Harvard Stem Cell Institute)

Abstract

Empirical and anecdotal evidence has associated stress with accelerated hair greying (formation of unpigmented hairs)1,2, but so far there has been little scientific validation of this link. Here we report that, in mice, acute stress leads to hair greying through the fast depletion of melanocyte stem cells. Using a combination of adrenalectomy, denervation, chemogenetics3,4, cell ablation and knockout of the adrenergic receptor specifically in melanocyte stem cells, we find that the stress-induced loss of melanocyte stem cells is independent of immune attack or adrenal stress hormones. Instead, hair greying results from activation of the sympathetic nerves that innervate the melanocyte stem-cell niche. Under conditions of stress, the activation of these sympathetic nerves leads to burst release of the neurotransmitter noradrenaline (also known as norepinephrine). This causes quiescent melanocyte stem cells to proliferate rapidly, and is followed by their differentiation, migration and permanent depletion from the niche. Transient suppression of the proliferation of melanocyte stem cells prevents stress-induced hair greying. Our study demonstrates that neuronal activity that is induced by acute stress can drive a rapid and permanent loss of somatic stem cells, and illustrates an example in which the maintenance of somatic stem cells is directly influenced by the overall physiological state of the organism.

Suggested Citation

  • Bing Zhang & Sai Ma & Inbal Rachmin & Megan He & Pankaj Baral & Sekyu Choi & William A. Gonçalves & Yulia Shwartz & Eva M. Fast & Yiqun Su & Leonard I. Zon & Aviv Regev & Jason D. Buenrostro & Thiago , 2020. "Hyperactivation of sympathetic nerves drives depletion of melanocyte stem cells," Nature, Nature, vol. 577(7792), pages 676-681, January.
  • Handle: RePEc:nat:nature:v:577:y:2020:i:7792:d:10.1038_s41586-020-1935-3
    DOI: 10.1038/s41586-020-1935-3
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    Cited by:

    1. Malmendier, Ulrike M. & Borgschulte, Mark & Guenzel, Marius & Liu, Canyao, 2020. "CEO Stress, Aging, and Death," CEPR Discussion Papers 14933, C.E.P.R. Discussion Papers.
    2. Luye An & Dahihm Kim & Leanne R. Donahue & Menansili Abraham Mejooli & Chi-Yong Eom & Nozomi Nishimura & Andrew C. White, 2024. "Sexual dimorphism in melanocyte stem cell behavior reveals combinational therapeutic strategies for cutaneous repigmentation," Nature Communications, Nature, vol. 15(1), pages 1-18, December.

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