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Convergent evolution of monocyte differentiation in adult skin instructs Langerhans cell identity

Convergent evolution of monocyte differentiation in adult skin instructs Langerhans cell identity
Convergent evolution of monocyte differentiation in adult skin instructs Langerhans cell identity

Langerhans cells (LCs) are distinct among phagocytes, functioning both as embryo-derived, tissue-resident macrophages in skin innervation and repair and as migrating professional antigen-presenting cells, a function classically assigned to dendritic cells (DCs). Here, we demonstrate that both intrinsic and extrinsic factors imprint this dual identity. Using ablation of embryo-derived LCs in the murine adult skin and tracking differentiation of incoming monocyte-derived replacements, we found intrinsic intraepidermal heterogeneity. We observed that ontogenically distinct monocytes give rise to LCs. Within the epidermis, Jagged-dependent activation of Notch signaling, likely within the hair follicle niche, provided an initial site of LC commitment before metabolic adaptation and survival of monocyte-derived LCs. In the human skin, embryo-derived LCs in newborns retained transcriptional evidence of their macrophage origin, but this was superseded by DC-like immune modules after postnatal expansion. Thus, adaptation to adult skin niches replicates conditioning of LC at birth, permitting repair of the embryo-derived LC network.

2470-9468
Appios, Anna
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Davies, James
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Sirvent, Sofia
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Henderson, Stephen
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Trzebanski, Sébastien
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Schroth, Johannes
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Law, Morven L.
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Carvalho, Inês Boal
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Pinto, Marlene Magalhaes
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Carvalho, Cyril
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Kan, Howard Yuan Hao
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Lovlekar, Shreya
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Major, Christina
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Vallejo, Andres
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Hall, Nigel J.
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Ardern-Jones, Michael
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Liu, Zhaoyuan
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Ginhoux, Florent
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Henson, Sian M.
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Gentek, Rebecca
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Emmerson, Elaine
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Jung, Steffen
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Polak, Marta E.
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Bennett, Clare L.
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Appios, Anna
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Davies, James
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Sirvent, Sofia
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Henderson, Stephen
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Trzebanski, Sébastien
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Schroth, Johannes
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Law, Morven L.
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Carvalho, Inês Boal
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Pinto, Marlene Magalhaes
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Carvalho, Cyril
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Kan, Howard Yuan Hao
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Lovlekar, Shreya
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Major, Christina
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Vallejo, Andres
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Hall, Nigel J.
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Ardern-Jones, Michael
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Liu, Zhaoyuan
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Ginhoux, Florent
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Henson, Sian M.
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Gentek, Rebecca
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Emmerson, Elaine
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Jung, Steffen
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Polak, Marta E.
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Bennett, Clare L.
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Appios, Anna, Davies, James, Sirvent, Sofia, Henderson, Stephen, Trzebanski, Sébastien, Schroth, Johannes, Law, Morven L., Carvalho, Inês Boal, Pinto, Marlene Magalhaes, Carvalho, Cyril, Kan, Howard Yuan Hao, Lovlekar, Shreya, Major, Christina, Vallejo, Andres, Hall, Nigel J., Ardern-Jones, Michael, Liu, Zhaoyuan, Ginhoux, Florent, Henson, Sian M., Gentek, Rebecca, Emmerson, Elaine, Jung, Steffen, Polak, Marta E. and Bennett, Clare L. (2024) Convergent evolution of monocyte differentiation in adult skin instructs Langerhans cell identity. Science immunology, 9 (99), [eadp0344]. (doi:10.1126/sciimmunol.adp0344).

Record type: Article

Abstract

Langerhans cells (LCs) are distinct among phagocytes, functioning both as embryo-derived, tissue-resident macrophages in skin innervation and repair and as migrating professional antigen-presenting cells, a function classically assigned to dendritic cells (DCs). Here, we demonstrate that both intrinsic and extrinsic factors imprint this dual identity. Using ablation of embryo-derived LCs in the murine adult skin and tracking differentiation of incoming monocyte-derived replacements, we found intrinsic intraepidermal heterogeneity. We observed that ontogenically distinct monocytes give rise to LCs. Within the epidermis, Jagged-dependent activation of Notch signaling, likely within the hair follicle niche, provided an initial site of LC commitment before metabolic adaptation and survival of monocyte-derived LCs. In the human skin, embryo-derived LCs in newborns retained transcriptional evidence of their macrophage origin, but this was superseded by DC-like immune modules after postnatal expansion. Thus, adaptation to adult skin niches replicates conditioning of LC at birth, permitting repair of the embryo-derived LC network.

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Accepted/In Press date: 14 August 2024
e-pub ahead of print date: 6 September 2024
Additional Information: For the purpose of open access, the author has applied a CC-BY public copyright license to any author-accepted manuscript version arising from this submission.

Identifiers

Local EPrints ID: 495219
URI: http://eprints.soton.ac.uk/id/eprint/495219
ISSN: 2470-9468
PURE UUID: 9c073403-4826-462a-a0b5-6f9246dcf534
ORCID for Sofia Sirvent: ORCID iD orcid.org/0000-0003-0050-8579
ORCID for Andres Vallejo: ORCID iD orcid.org/0000-0002-4688-0598
ORCID for Nigel J. Hall: ORCID iD orcid.org/0000-0001-8570-9374
ORCID for Michael Ardern-Jones: ORCID iD orcid.org/0000-0003-1466-2016

Catalogue record

Date deposited: 01 Nov 2024 18:04
Last modified: 02 Nov 2024 02:54

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Contributors

Author: Anna Appios
Author: James Davies
Author: Sofia Sirvent ORCID iD
Author: Stephen Henderson
Author: Sébastien Trzebanski
Author: Johannes Schroth
Author: Morven L. Law
Author: Inês Boal Carvalho
Author: Marlene Magalhaes Pinto
Author: Cyril Carvalho
Author: Howard Yuan Hao Kan
Author: Shreya Lovlekar
Author: Christina Major
Author: Andres Vallejo ORCID iD
Author: Nigel J. Hall ORCID iD
Author: Zhaoyuan Liu
Author: Florent Ginhoux
Author: Sian M. Henson
Author: Rebecca Gentek
Author: Elaine Emmerson
Author: Steffen Jung
Author: Marta E. Polak
Author: Clare L. Bennett

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