Hyperactivation of sympathetic nerves drives depletion of melanocyte stem cells

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 M. Cunha, Isaac M. Chiu, David E. Fisher and Ya-Chieh Hsu ()
Additional contact information
Bing Zhang: Harvard University and Harvard Stem Cell Institute
Sai Ma: Harvard University and Harvard Stem Cell Institute
Inbal Rachmin: Massachusetts General Hospital, Harvard Medical School
Megan He: Harvard University and Harvard Stem Cell Institute
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
Yiqun Su: Massachusetts General Hospital, Harvard Medical School
Leonard I. Zon: Harvard University and Harvard Stem Cell Institute
Aviv Regev: Klarman Cell Observatory, Broad Institute of MIT and Harvard
Jason D. Buenrostro: Harvard University and Harvard Stem Cell Institute
Thiago M. Cunha: Harvard Medical School
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

Nature, 2020, vol. 577, issue 7792, 676-681

Abstract: 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.

Date: 2020
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DOI: 10.1038/s41586-020-1935-3

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