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Zebrafish cutaneous injury models reveal that Langerhans cells engulf axonal debris in adult epidermis

Somatosensory neurons extend enormous peripheral axons to the skin, where they detect diverse environmental stimuli. Somatosensory peripheral axons are easily damaged due to their small caliber and superficial location. Axonal damage results in Wallerian degeneration, creating vast quantities of cel...

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Autores principales: Peterman, Eric, Quitevis, Elgene J. A., Black, Erik C., Horton, Emma C., Aelmore, Rune L., White, Ethan, Sagasti, Alvaro, Rasmussen, Jeffrey P.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Company of Biologists Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10110399/
https://www.ncbi.nlm.nih.gov/pubmed/36876992
http://dx.doi.org/10.1242/dmm.049911
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author Peterman, Eric
Quitevis, Elgene J. A.
Black, Erik C.
Horton, Emma C.
Aelmore, Rune L.
White, Ethan
Sagasti, Alvaro
Rasmussen, Jeffrey P.
author_facet Peterman, Eric
Quitevis, Elgene J. A.
Black, Erik C.
Horton, Emma C.
Aelmore, Rune L.
White, Ethan
Sagasti, Alvaro
Rasmussen, Jeffrey P.
author_sort Peterman, Eric
collection PubMed
description Somatosensory neurons extend enormous peripheral axons to the skin, where they detect diverse environmental stimuli. Somatosensory peripheral axons are easily damaged due to their small caliber and superficial location. Axonal damage results in Wallerian degeneration, creating vast quantities of cellular debris that phagocytes must remove to maintain organ homeostasis. The cellular mechanisms that ensure efficient clearance of axon debris from stratified adult skin are unknown. Here, we established zebrafish scales as a tractable model to study axon degeneration in the adult epidermis. Using this system, we demonstrated that skin-resident immune cells known as Langerhans cells engulf the majority of axon debris. In contrast to immature skin, adult keratinocytes did not significantly contribute to debris removal, even in animals lacking Langerhans cells. Our study establishes a powerful new model for studying Wallerian degeneration and identifies a new function for Langerhans cells in maintenance of adult skin homeostasis following injury. These findings have important implications for pathologies that trigger somatosensory axon degeneration.
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spelling pubmed-101103992023-04-18 Zebrafish cutaneous injury models reveal that Langerhans cells engulf axonal debris in adult epidermis Peterman, Eric Quitevis, Elgene J. A. Black, Erik C. Horton, Emma C. Aelmore, Rune L. White, Ethan Sagasti, Alvaro Rasmussen, Jeffrey P. Dis Model Mech Research Article Somatosensory neurons extend enormous peripheral axons to the skin, where they detect diverse environmental stimuli. Somatosensory peripheral axons are easily damaged due to their small caliber and superficial location. Axonal damage results in Wallerian degeneration, creating vast quantities of cellular debris that phagocytes must remove to maintain organ homeostasis. The cellular mechanisms that ensure efficient clearance of axon debris from stratified adult skin are unknown. Here, we established zebrafish scales as a tractable model to study axon degeneration in the adult epidermis. Using this system, we demonstrated that skin-resident immune cells known as Langerhans cells engulf the majority of axon debris. In contrast to immature skin, adult keratinocytes did not significantly contribute to debris removal, even in animals lacking Langerhans cells. Our study establishes a powerful new model for studying Wallerian degeneration and identifies a new function for Langerhans cells in maintenance of adult skin homeostasis following injury. These findings have important implications for pathologies that trigger somatosensory axon degeneration. The Company of Biologists Ltd 2023-04-03 /pmc/articles/PMC10110399/ /pubmed/36876992 http://dx.doi.org/10.1242/dmm.049911 Text en © 2023. Published by The Company of Biologists Ltd https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Article
Peterman, Eric
Quitevis, Elgene J. A.
Black, Erik C.
Horton, Emma C.
Aelmore, Rune L.
White, Ethan
Sagasti, Alvaro
Rasmussen, Jeffrey P.
Zebrafish cutaneous injury models reveal that Langerhans cells engulf axonal debris in adult epidermis
title Zebrafish cutaneous injury models reveal that Langerhans cells engulf axonal debris in adult epidermis
title_full Zebrafish cutaneous injury models reveal that Langerhans cells engulf axonal debris in adult epidermis
title_fullStr Zebrafish cutaneous injury models reveal that Langerhans cells engulf axonal debris in adult epidermis
title_full_unstemmed Zebrafish cutaneous injury models reveal that Langerhans cells engulf axonal debris in adult epidermis
title_short Zebrafish cutaneous injury models reveal that Langerhans cells engulf axonal debris in adult epidermis
title_sort zebrafish cutaneous injury models reveal that langerhans cells engulf axonal debris in adult epidermis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10110399/
https://www.ncbi.nlm.nih.gov/pubmed/36876992
http://dx.doi.org/10.1242/dmm.049911
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