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An IRF1-IRF4 toggle-switch controls tolerogenic and immunogenic transcriptional programming in human Langerhans cells

An IRF1-IRF4 toggle-switch controls tolerogenic and immunogenic transcriptional programming in human Langerhans cells
An IRF1-IRF4 toggle-switch controls tolerogenic and immunogenic transcriptional programming in human Langerhans cells
Langerhans cells (LCs) reside in the epidermis as a dense network of immune system sentinels, coordinating both immunogenic and tolerogenic immune responses. To determine molecular switches directing induction of LC immune activation, we performed mathematical modelling of gene regulatory networks identified by single cell RNA sequencing of LCs exposed to TNF-alpha, a key pro-inflammatory signal produced by the skin. Our approach delineated three programmes of LC phenotypic activation (immunogenic, tolerogenic or ambivalent), and confirmed that TNF-alpha enhanced LC immunogenic programming. Through regulon analysis followed by mutual information modelling, we identified IRF1 as the key transcription factor for the regulation of immunogenicity in LCs. Application of a mathematical toggle switch model, coupling IRF1 with tolerance-inducing transcription factors, determined the key set of transcription factors regulating the switch between tolerance and immunogenicity, and correctly predicted LC behaviour in LCs derived from different body sites. Our findings provide a mechanistic explanation of how combinatorial interactions between different transcription factors can coordinate specific transcriptional programmes in human LCs, interpreting the microenvironmental context of the local tissue microenvironments.
Langerhans cells, Interferon Regulatory Factors, toggle Switch, Systems Immunology
1664-3224
Davies, James
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Vallejo, Andres F.
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Sirvent, Sofia
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Porter, Gemma
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Clayton, Kalum
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Qumbelo, Yamkela
ae54321e-ae7d-4556-bd6a-bea37d03d132
Stumpf, Patrick
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West, Jonathan
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Gray, Clive
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Chigorimbo-Murefu, Nyaradzo
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Macarthur, Benjamin
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Polak, Marta
e0ac5e1a-7074-4776-ba23-490bd4da612d
Davies, James
a93b4fc9-80a2-4620-ada6-c12f05c5ee38
Vallejo, Andres F.
27bc0b94-0c40-4fd1-9533-7e267d588c0a
Sirvent, Sofia
c8c68bc8-a5a7-456d-899d-6e48ccfac02f
Porter, Gemma
5f0c0ee9-ed05-41de-8552-8ad7390fc7a8
Clayton, Kalum
499fec32-9297-45bd-9207-5ba699734844
Qumbelo, Yamkela
ae54321e-ae7d-4556-bd6a-bea37d03d132
Stumpf, Patrick
3aa7f861-0629-4a6c-a7be-3afd99e11314
West, Jonathan
f1c2e060-16c3-44c0-af70-242a1c58b968
Gray, Clive
05f296b9-6b11-470e-9593-792afd41a994
Chigorimbo-Murefu, Nyaradzo
107529f5-1f5e-4e8c-b2e6-788b575f812a
Macarthur, Benjamin
2c0476e7-5d3e-4064-81bb-104e8e88bb6b
Polak, Marta
e0ac5e1a-7074-4776-ba23-490bd4da612d

Davies, James, Vallejo, Andres F., Sirvent, Sofia, Porter, Gemma, Clayton, Kalum, Qumbelo, Yamkela, Stumpf, Patrick, West, Jonathan, Gray, Clive, Chigorimbo-Murefu, Nyaradzo, Macarthur, Benjamin and Polak, Marta (2021) An IRF1-IRF4 toggle-switch controls tolerogenic and immunogenic transcriptional programming in human Langerhans cells. Frontiers in Immunology, 12, [665312]. (doi:10.3389/fimmu.2021.665312).

Record type: Article

Abstract

Langerhans cells (LCs) reside in the epidermis as a dense network of immune system sentinels, coordinating both immunogenic and tolerogenic immune responses. To determine molecular switches directing induction of LC immune activation, we performed mathematical modelling of gene regulatory networks identified by single cell RNA sequencing of LCs exposed to TNF-alpha, a key pro-inflammatory signal produced by the skin. Our approach delineated three programmes of LC phenotypic activation (immunogenic, tolerogenic or ambivalent), and confirmed that TNF-alpha enhanced LC immunogenic programming. Through regulon analysis followed by mutual information modelling, we identified IRF1 as the key transcription factor for the regulation of immunogenicity in LCs. Application of a mathematical toggle switch model, coupling IRF1 with tolerance-inducing transcription factors, determined the key set of transcription factors regulating the switch between tolerance and immunogenicity, and correctly predicted LC behaviour in LCs derived from different body sites. Our findings provide a mechanistic explanation of how combinatorial interactions between different transcription factors can coordinate specific transcriptional programmes in human LCs, interpreting the microenvironmental context of the local tissue microenvironments.

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Accepted/In Press date: 25 May 2021
Published date: 15 June 2021
Keywords: Langerhans cells, Interferon Regulatory Factors, toggle Switch, Systems Immunology

Identifiers

Local EPrints ID: 453508
URI: http://eprints.soton.ac.uk/id/eprint/453508
ISSN: 1664-3224
PURE UUID: 586a3ffd-8a3f-4474-9649-c2afdca522de
ORCID for Andres F. Vallejo: ORCID iD orcid.org/0000-0002-4688-0598
ORCID for Sofia Sirvent: ORCID iD orcid.org/0000-0003-0050-8579
ORCID for Gemma Porter: ORCID iD orcid.org/0000-0003-0681-6986
ORCID for Kalum Clayton: ORCID iD orcid.org/0000-0002-1143-3931
ORCID for Jonathan West: ORCID iD orcid.org/0000-0002-5709-6790
ORCID for Benjamin Macarthur: ORCID iD orcid.org/0000-0002-5396-9750

Catalogue record

Date deposited: 18 Jan 2022 18:05
Last modified: 17 Mar 2024 03:46

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Contributors

Author: James Davies
Author: Andres F. Vallejo ORCID iD
Author: Sofia Sirvent ORCID iD
Author: Gemma Porter ORCID iD
Author: Kalum Clayton ORCID iD
Author: Yamkela Qumbelo
Author: Patrick Stumpf
Author: Jonathan West ORCID iD
Author: Clive Gray
Author: Nyaradzo Chigorimbo-Murefu
Author: Marta Polak

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