The cellular basis of mechanosensory Merkel-cell innervation during development

Touch sensation is initiated by mechanosensory neurons that innervate distinct skin structures; however, little is known about how these neurons are patterned during mammalian skin development. We explored the cellular basis of touch-receptor patterning in mouse touch domes, which contain mechanosen...

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Main Authors: Blair A Jenkins, Natalia M Fontecilla, Catherine P Lu, Elaine Fuchs, Ellen A Lumpkin
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2019-02-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/42633
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spelling doaj-051b6fdca8a342a99ca32296d241d42a2021-05-05T17:25:49ZengeLife Sciences Publications LtdeLife2050-084X2019-02-01810.7554/eLife.42633The cellular basis of mechanosensory Merkel-cell innervation during developmentBlair A Jenkins0https://orcid.org/0000-0003-0226-5021Natalia M Fontecilla1Catherine P Lu2Elaine Fuchs3https://orcid.org/0000-0002-0978-5137Ellen A Lumpkin4https://orcid.org/0000-0002-1166-3374Department of Physiology and Cellular Biophysics, Columbia University, New York, United States; Department of Dermatology, Columbia University, New York, United StatesDepartment of Physiology and Cellular Biophysics, Columbia University, New York, United StatesRobin Neustein Laboratory of Mammalian Development and Cell Biology, Howard Hughes Medical Institute, The Rockefeller University, New York, United StatesRobin Neustein Laboratory of Mammalian Development and Cell Biology, Howard Hughes Medical Institute, The Rockefeller University, New York, United StatesDepartment of Physiology and Cellular Biophysics, Columbia University, New York, United StatesTouch sensation is initiated by mechanosensory neurons that innervate distinct skin structures; however, little is known about how these neurons are patterned during mammalian skin development. We explored the cellular basis of touch-receptor patterning in mouse touch domes, which contain mechanosensory Merkel cell-neurite complexes and abut primary hair follicles. At embryonic stage 16.5 (E16.5), touch domes emerge as patches of Merkel cells and keratinocytes clustered with a previously unsuspected population of Bmp4-expressing dermal cells. Epidermal Noggin overexpression at E14.5 disrupted touch-dome formation but not hair-follicle specification, demonstrating a temporally distinct requirement for BMP signaling in placode-derived structures. Surprisingly, two neuronal populations preferentially targeted touch domes during development but only one persisted in mature touch domes. Finally, Keratin-17-expressing keratinocytes but not Merkel cells were necessary to establish innervation patterns during development. These findings identify key cell types and signaling pathways required for targeting Merkel-cell afferents to discrete mechanosensory compartments.https://elifesciences.org/articles/42633touchskinsomatosensory neuronmechanoreceptordorsal root ganglionhair follicle
collection DOAJ
language English
format Article
sources DOAJ
author Blair A Jenkins
Natalia M Fontecilla
Catherine P Lu
Elaine Fuchs
Ellen A Lumpkin
spellingShingle Blair A Jenkins
Natalia M Fontecilla
Catherine P Lu
Elaine Fuchs
Ellen A Lumpkin
The cellular basis of mechanosensory Merkel-cell innervation during development
eLife
touch
skin
somatosensory neuron
mechanoreceptor
dorsal root ganglion
hair follicle
author_facet Blair A Jenkins
Natalia M Fontecilla
Catherine P Lu
Elaine Fuchs
Ellen A Lumpkin
author_sort Blair A Jenkins
title The cellular basis of mechanosensory Merkel-cell innervation during development
title_short The cellular basis of mechanosensory Merkel-cell innervation during development
title_full The cellular basis of mechanosensory Merkel-cell innervation during development
title_fullStr The cellular basis of mechanosensory Merkel-cell innervation during development
title_full_unstemmed The cellular basis of mechanosensory Merkel-cell innervation during development
title_sort cellular basis of mechanosensory merkel-cell innervation during development
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2019-02-01
description Touch sensation is initiated by mechanosensory neurons that innervate distinct skin structures; however, little is known about how these neurons are patterned during mammalian skin development. We explored the cellular basis of touch-receptor patterning in mouse touch domes, which contain mechanosensory Merkel cell-neurite complexes and abut primary hair follicles. At embryonic stage 16.5 (E16.5), touch domes emerge as patches of Merkel cells and keratinocytes clustered with a previously unsuspected population of Bmp4-expressing dermal cells. Epidermal Noggin overexpression at E14.5 disrupted touch-dome formation but not hair-follicle specification, demonstrating a temporally distinct requirement for BMP signaling in placode-derived structures. Surprisingly, two neuronal populations preferentially targeted touch domes during development but only one persisted in mature touch domes. Finally, Keratin-17-expressing keratinocytes but not Merkel cells were necessary to establish innervation patterns during development. These findings identify key cell types and signaling pathways required for targeting Merkel-cell afferents to discrete mechanosensory compartments.
topic touch
skin
somatosensory neuron
mechanoreceptor
dorsal root ganglion
hair follicle
url https://elifesciences.org/articles/42633
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