Dermal appendage-dependent patterning of zebrafish atoh1a+ Merkel cells
Touch system function requires precise interactions between specialized skin cells and somatosensory axons, as exemplified by the vertebrate mechanosensory Merkel cell-neurite complex. Development and patterning of Merkel cells and associated neurites during skin organogenesis remain poorly understo...
| Main Authors: | , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2023-01-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/85800 |
| _version_ | 1811170678599057408 |
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| author | Tanya L Brown Emma C Horton Evan W Craig Camille EA Goo Erik C Black Madeleine N Hewitt Nathaniel G Yee Everett T Fan David W Raible Jeffrey P Rasmussen |
| author_facet | Tanya L Brown Emma C Horton Evan W Craig Camille EA Goo Erik C Black Madeleine N Hewitt Nathaniel G Yee Everett T Fan David W Raible Jeffrey P Rasmussen |
| author_sort | Tanya L Brown |
| collection | DOAJ |
| description | Touch system function requires precise interactions between specialized skin cells and somatosensory axons, as exemplified by the vertebrate mechanosensory Merkel cell-neurite complex. Development and patterning of Merkel cells and associated neurites during skin organogenesis remain poorly understood, partly due to the in utero development of mammalian embryos. Here, we discover Merkel cells in the zebrafish epidermis and identify Atonal homolog 1a (Atoh1a) as a marker of zebrafish Merkel cells. We show that zebrafish Merkel cells derive from basal keratinocytes, express neurosecretory and mechanosensory machinery, extend actin-rich microvilli, and complex with somatosensory axons, all hallmarks of mammalian Merkel cells. Merkel cells populate all major adult skin compartments, with region-specific densities and distribution patterns. In vivo photoconversion reveals that Merkel cells undergo steady loss and replenishment during skin homeostasis. Merkel cells develop concomitant with dermal appendages along the trunk and loss of Ectodysplasin signaling, which prevents dermal appendage formation, reduces Merkel cell density by affecting cell differentiation. By contrast, altering dermal appendage morphology changes the distribution, but not density, of Merkel cells. Overall, our studies provide insights into touch system maturation during skin organogenesis and establish zebrafish as an experimentally accessible in vivo model for the study of Merkel cell biology. |
| first_indexed | 2024-04-10T17:00:35Z |
| format | Article |
| id | doaj.art-512962c3179e40978dacd297b1dd6b5f |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-10T17:00:35Z |
| publishDate | 2023-01-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-512962c3179e40978dacd297b1dd6b5f2023-02-06T14:31:35ZengeLife Sciences Publications LtdeLife2050-084X2023-01-011210.7554/eLife.85800Dermal appendage-dependent patterning of zebrafish atoh1a+ Merkel cellsTanya L Brown0https://orcid.org/0000-0001-9554-178XEmma C Horton1https://orcid.org/0000-0001-9730-7380Evan W Craig2Camille EA Goo3https://orcid.org/0000-0002-9118-4006Erik C Black4https://orcid.org/0000-0002-2333-8923Madeleine N Hewitt5https://orcid.org/0000-0002-4387-327XNathaniel G Yee6Everett T Fan7David W Raible8https://orcid.org/0000-0002-5342-5841Jeffrey P Rasmussen9https://orcid.org/0000-0001-6997-3773Department of Biology, University of Washington, Seattle, United StatesDepartment of Biology, University of Washington, Seattle, United StatesDepartment of Biology, University of Washington, Seattle, United StatesDepartment of Biology, University of Washington, Seattle, United StatesDepartment of Biology, University of Washington, Seattle, United States; Molecular and Cellular Biology Program, University of Washington, Seattle, United StatesMolecular and Cellular Biology Program, University of Washington, Seattle, United States; Department of Biological Structure, University of Washington, Seattle, United StatesDepartment of Biology, University of Washington, Seattle, United StatesDepartment of Biology, University of Washington, Seattle, United StatesDepartment of Biological Structure, University of Washington, Seattle, United States; Department of Otolaryngology - Head and Neck Surgery, University of Washington, Seattle, United States; Institute for Stem Cell and Regenerative Medicine, University of Washington, Seattle, United StatesDepartment of Biology, University of Washington, Seattle, United States; Institute for Stem Cell and Regenerative Medicine, University of Washington, Seattle, United StatesTouch system function requires precise interactions between specialized skin cells and somatosensory axons, as exemplified by the vertebrate mechanosensory Merkel cell-neurite complex. Development and patterning of Merkel cells and associated neurites during skin organogenesis remain poorly understood, partly due to the in utero development of mammalian embryos. Here, we discover Merkel cells in the zebrafish epidermis and identify Atonal homolog 1a (Atoh1a) as a marker of zebrafish Merkel cells. We show that zebrafish Merkel cells derive from basal keratinocytes, express neurosecretory and mechanosensory machinery, extend actin-rich microvilli, and complex with somatosensory axons, all hallmarks of mammalian Merkel cells. Merkel cells populate all major adult skin compartments, with region-specific densities and distribution patterns. In vivo photoconversion reveals that Merkel cells undergo steady loss and replenishment during skin homeostasis. Merkel cells develop concomitant with dermal appendages along the trunk and loss of Ectodysplasin signaling, which prevents dermal appendage formation, reduces Merkel cell density by affecting cell differentiation. By contrast, altering dermal appendage morphology changes the distribution, but not density, of Merkel cells. Overall, our studies provide insights into touch system maturation during skin organogenesis and establish zebrafish as an experimentally accessible in vivo model for the study of Merkel cell biology.https://elifesciences.org/articles/85800somatosensory neuronepidermisskintouchEctodysplasinFgf8 |
| spellingShingle | Tanya L Brown Emma C Horton Evan W Craig Camille EA Goo Erik C Black Madeleine N Hewitt Nathaniel G Yee Everett T Fan David W Raible Jeffrey P Rasmussen Dermal appendage-dependent patterning of zebrafish atoh1a+ Merkel cells eLife somatosensory neuron epidermis skin touch Ectodysplasin Fgf8 |
| title | Dermal appendage-dependent patterning of zebrafish atoh1a+ Merkel cells |
| title_full | Dermal appendage-dependent patterning of zebrafish atoh1a+ Merkel cells |
| title_fullStr | Dermal appendage-dependent patterning of zebrafish atoh1a+ Merkel cells |
| title_full_unstemmed | Dermal appendage-dependent patterning of zebrafish atoh1a+ Merkel cells |
| title_short | Dermal appendage-dependent patterning of zebrafish atoh1a+ Merkel cells |
| title_sort | dermal appendage dependent patterning of zebrafish atoh1a merkel cells |
| topic | somatosensory neuron epidermis skin touch Ectodysplasin Fgf8 |
| url | https://elifesciences.org/articles/85800 |
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