Multipotent peripheral glial cells generate neuroendocrine cells of the adrenal medulla

Alessandro Furlan, Vyacheslav Dyachuk, Maria Eleni Kastriti, Laura Calvo-Enrique, Hind Abdo, Saida Hadjab, Tatiana Chontorotzea, Natalia Akkuratova, Dmitry Usoskin, Dmitry Kamenev, Julian Petersen, Kazunori Sunadome, Fatima Memic, Ulrika Marklund, Kaj Fried, Piotr Topilko, Francois Lallemend, Peter V. Kharchenko, Patrik Ernfors, Igor Adameyko

Research output

48 Citations (Scopus)

Abstract

Adrenaline is a fundamental circulating hormone for bodily responses to internal and external stressors. Chromaffin cells of the adrenal medulla (AM) represent the main neuroendocrine adrenergic component and are believed to differentiate from neural crest cells. We demonstrate that large numbers of chromaffin cells arise from peripheral glial stem cells, termed Schwann cell precursors (SCPs). SCPs migrate along the visceral motor nerve to the vicinity of the forming adrenal gland, where they detach from the nerve and form postsynaptic neuroendocrine chromaffin cells. An intricate molecular logic drives two sequential phases of gene expression, one unique for a distinct transient cellular state and another for cell type specification. Subsequently, these programs down-regulate SCP-gene and up-regulate chromaffin cell–gene networks. The AM forms through limited cell expansion and requires the recruitment of numerous SCPs. Thus, peripheral nerves serve as a stem cell niche for neuroendocrine system development.

Original languageEnglish
Article number46
JournalScience
Volume357
Issue number6346
DOIs
Publication statusPublished - 7 Jul 2017

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Neuroendocrine Cells
Adrenal Medulla
Schwann Cells
Neuroglia
Chromaffin Cells
Stem Cell Niche
Neurosecretory Systems
Neural Crest
Adrenal Glands
Peripheral Nerves
Adrenergic Agents
Epinephrine
Up-Regulation
Down-Regulation
Hormones
Gene Expression
Genes

Scopus subject areas

  • General

Cite this

Furlan, A., Dyachuk, V., Kastriti, M. E., Calvo-Enrique, L., Abdo, H., Hadjab, S., ... Adameyko, I. (2017). Multipotent peripheral glial cells generate neuroendocrine cells of the adrenal medulla. Science, 357(6346), [46]. https://doi.org/10.1126/science.aal3753
Furlan, Alessandro ; Dyachuk, Vyacheslav ; Kastriti, Maria Eleni ; Calvo-Enrique, Laura ; Abdo, Hind ; Hadjab, Saida ; Chontorotzea, Tatiana ; Akkuratova, Natalia ; Usoskin, Dmitry ; Kamenev, Dmitry ; Petersen, Julian ; Sunadome, Kazunori ; Memic, Fatima ; Marklund, Ulrika ; Fried, Kaj ; Topilko, Piotr ; Lallemend, Francois ; Kharchenko, Peter V. ; Ernfors, Patrik ; Adameyko, Igor. / Multipotent peripheral glial cells generate neuroendocrine cells of the adrenal medulla. In: Science. 2017 ; Vol. 357, No. 6346.
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abstract = "Adrenaline is a fundamental circulating hormone for bodily responses to internal and external stressors. Chromaffin cells of the adrenal medulla (AM) represent the main neuroendocrine adrenergic component and are believed to differentiate from neural crest cells. We demonstrate that large numbers of chromaffin cells arise from peripheral glial stem cells, termed Schwann cell precursors (SCPs). SCPs migrate along the visceral motor nerve to the vicinity of the forming adrenal gland, where they detach from the nerve and form postsynaptic neuroendocrine chromaffin cells. An intricate molecular logic drives two sequential phases of gene expression, one unique for a distinct transient cellular state and another for cell type specification. Subsequently, these programs down-regulate SCP-gene and up-regulate chromaffin cell–gene networks. The AM forms through limited cell expansion and requires the recruitment of numerous SCPs. Thus, peripheral nerves serve as a stem cell niche for neuroendocrine system development.",
author = "Alessandro Furlan and Vyacheslav Dyachuk and Kastriti, {Maria Eleni} and Laura Calvo-Enrique and Hind Abdo and Saida Hadjab and Tatiana Chontorotzea and Natalia Akkuratova and Dmitry Usoskin and Dmitry Kamenev and Julian Petersen and Kazunori Sunadome and Fatima Memic and Ulrika Marklund and Kaj Fried and Piotr Topilko and Francois Lallemend and Kharchenko, {Peter V.} and Patrik Ernfors and Igor Adameyko",
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Furlan, A, Dyachuk, V, Kastriti, ME, Calvo-Enrique, L, Abdo, H, Hadjab, S, Chontorotzea, T, Akkuratova, N, Usoskin, D, Kamenev, D, Petersen, J, Sunadome, K, Memic, F, Marklund, U, Fried, K, Topilko, P, Lallemend, F, Kharchenko, PV, Ernfors, P & Adameyko, I 2017, 'Multipotent peripheral glial cells generate neuroendocrine cells of the adrenal medulla', Science, vol. 357, no. 6346, 46. https://doi.org/10.1126/science.aal3753

Multipotent peripheral glial cells generate neuroendocrine cells of the adrenal medulla. / Furlan, Alessandro; Dyachuk, Vyacheslav; Kastriti, Maria Eleni; Calvo-Enrique, Laura; Abdo, Hind; Hadjab, Saida; Chontorotzea, Tatiana; Akkuratova, Natalia; Usoskin, Dmitry; Kamenev, Dmitry; Petersen, Julian; Sunadome, Kazunori; Memic, Fatima; Marklund, Ulrika; Fried, Kaj; Topilko, Piotr; Lallemend, Francois; Kharchenko, Peter V.; Ernfors, Patrik; Adameyko, Igor.

In: Science, Vol. 357, No. 6346, 46, 07.07.2017.

Research output

TY - JOUR

T1 - Multipotent peripheral glial cells generate neuroendocrine cells of the adrenal medulla

AU - Furlan, Alessandro

AU - Dyachuk, Vyacheslav

AU - Kastriti, Maria Eleni

AU - Calvo-Enrique, Laura

AU - Abdo, Hind

AU - Hadjab, Saida

AU - Chontorotzea, Tatiana

AU - Akkuratova, Natalia

AU - Usoskin, Dmitry

AU - Kamenev, Dmitry

AU - Petersen, Julian

AU - Sunadome, Kazunori

AU - Memic, Fatima

AU - Marklund, Ulrika

AU - Fried, Kaj

AU - Topilko, Piotr

AU - Lallemend, Francois

AU - Kharchenko, Peter V.

AU - Ernfors, Patrik

AU - Adameyko, Igor

PY - 2017/7/7

Y1 - 2017/7/7

N2 - Adrenaline is a fundamental circulating hormone for bodily responses to internal and external stressors. Chromaffin cells of the adrenal medulla (AM) represent the main neuroendocrine adrenergic component and are believed to differentiate from neural crest cells. We demonstrate that large numbers of chromaffin cells arise from peripheral glial stem cells, termed Schwann cell precursors (SCPs). SCPs migrate along the visceral motor nerve to the vicinity of the forming adrenal gland, where they detach from the nerve and form postsynaptic neuroendocrine chromaffin cells. An intricate molecular logic drives two sequential phases of gene expression, one unique for a distinct transient cellular state and another for cell type specification. Subsequently, these programs down-regulate SCP-gene and up-regulate chromaffin cell–gene networks. The AM forms through limited cell expansion and requires the recruitment of numerous SCPs. Thus, peripheral nerves serve as a stem cell niche for neuroendocrine system development.

AB - Adrenaline is a fundamental circulating hormone for bodily responses to internal and external stressors. Chromaffin cells of the adrenal medulla (AM) represent the main neuroendocrine adrenergic component and are believed to differentiate from neural crest cells. We demonstrate that large numbers of chromaffin cells arise from peripheral glial stem cells, termed Schwann cell precursors (SCPs). SCPs migrate along the visceral motor nerve to the vicinity of the forming adrenal gland, where they detach from the nerve and form postsynaptic neuroendocrine chromaffin cells. An intricate molecular logic drives two sequential phases of gene expression, one unique for a distinct transient cellular state and another for cell type specification. Subsequently, these programs down-regulate SCP-gene and up-regulate chromaffin cell–gene networks. The AM forms through limited cell expansion and requires the recruitment of numerous SCPs. Thus, peripheral nerves serve as a stem cell niche for neuroendocrine system development.

UR - http://www.scopus.com/inward/record.url?scp=85024098378&partnerID=8YFLogxK

U2 - 10.1126/science.aal3753

DO - 10.1126/science.aal3753

M3 - Article

C2 - 28684471

AN - SCOPUS:85024098378

VL - 357

JO - Science

JF - Science

SN - 0036-8075

IS - 6346

M1 - 46

ER -

Furlan A, Dyachuk V, Kastriti ME, Calvo-Enrique L, Abdo H, Hadjab S et al. Multipotent peripheral glial cells generate neuroendocrine cells of the adrenal medulla. Science. 2017 Jul 7;357(6346). 46. https://doi.org/10.1126/science.aal3753