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The ETS-family transcription factor PU.1 is a critical regulator of the inhibitory Fcγ receptor IIB expression in humans

The ETS-family transcription factor PU.1 is a critical regulator of the inhibitory Fcγ receptor IIB expression in humans
The ETS-family transcription factor PU.1 is a critical regulator of the inhibitory Fcγ receptor IIB expression in humans
The inhibitory Fc gamma receptor IIB (FcγRIIB) is a critical determinant of humoral immunity. By providing feedback inhibition, through inhibitory signalling or competition for antibody Fc engagement, it counterbalances and contextualises cellular responses to signals emanating from co-ligated activating receptors, such as the B-cell receptor and activating FcγR. These activities collectively suppress the emergence of B- cell-mediated autoimmune disease and immune complex-mediated pathologies. However, FcγRIIB upregulation within the tumour microenvironment limits the efficacy of monoclonal antibody (mAb)-mediated immunotherapy of cancer.

While the functional significance of FcγRIIB is well established in mice, its physiological roles and the regulatory mechanisms governing its expression remain incompletely understood in humans. Here we characterise the molecular determinants of FcγRIIB expression in human immune models and primary cells. Our findings reveal that the ETS-family transcription factor PU.1 plays a crucial role in regulating basal and inducible FcγRIIB expression. Moreover, when co-expressed, PU.1 co-operates with the related ETS-family member SPIB to drive FcγRIIB expression. PU.1 binding to the proximal FcγRIIB promoter elicits transcription, at least in part, through recruitment of the CBP/p300 transcriptional co-activators. Interestingly, similar mechanisms are also observed at the proximal promoters of the activating FcγRI and FcγRIIA, suggesting that additional, potentially lineage specific, factors cooperate with PU.1 to drive the distinct expression patterns of these FcγR. These insights pave the way for future investigations aimed at understanding the molecular mechanisms responsible for cell lineage-specific FcγR expression and subsequently manipulating them for therapeutic purposes.
FCGR2B, Fcγ receptors, PU.1, gene regulation, immunotherapy
0022-1767
1937-1950
Carter, Matthew J.
3baac102-d80c-42ba-ab4d-ad339a48169e
Bogdanov, Yury D.
0c970999-e191-4f1b-90d9-7bf25a5d5b4b
Smith, Rosanna C.
1fe5586f-92e9-4658-bd55-cd3eaa176b66
Cox, Kerry L.
7305c27e-9cdc-4e37-b994-ac55d7d1dfd2
Frampton, Sarah
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Ferson, Lili
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Foxall, Russell B.
cfe3a818-a281-4bcb-8889-e1d0b591117c
Hussain, Khiyam
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Strefford, Jonathan C.
3782b392-f080-42bf-bdca-8aa5d6ca532f
Beers, Stephen A.
a02548be-3ffd-41ab-9db8-d6e8c3b499a2
Cragg, Mark S.
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Carter, Matthew J.
3baac102-d80c-42ba-ab4d-ad339a48169e
Bogdanov, Yury D.
0c970999-e191-4f1b-90d9-7bf25a5d5b4b
Smith, Rosanna C.
1fe5586f-92e9-4658-bd55-cd3eaa176b66
Cox, Kerry L.
7305c27e-9cdc-4e37-b994-ac55d7d1dfd2
Frampton, Sarah
171e7585-97cf-4039-9bb6-175b63cb2a4f
Ferson, Lili
1219d19b-b257-4450-9520-df526ec99a99
Foxall, Russell B.
cfe3a818-a281-4bcb-8889-e1d0b591117c
Hussain, Khiyam
9468f252-81d0-4251-b800-702433b610f8
Strefford, Jonathan C.
3782b392-f080-42bf-bdca-8aa5d6ca532f
Beers, Stephen A.
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Cragg, Mark S.
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Carter, Matthew J., Bogdanov, Yury D., Smith, Rosanna C., Cox, Kerry L., Frampton, Sarah, Ferson, Lili, Foxall, Russell B., Hussain, Khiyam, Strefford, Jonathan C., Beers, Stephen A. and Cragg, Mark S. (2025) The ETS-family transcription factor PU.1 is a critical regulator of the inhibitory Fcγ receptor IIB expression in humans. Journal of Immunology, 214 (8), 1937-1950, [vkaf109]. (doi:10.1093/jimmun/vkaf109).

Record type: Article

Abstract

The inhibitory Fc gamma receptor IIB (FcγRIIB) is a critical determinant of humoral immunity. By providing feedback inhibition, through inhibitory signalling or competition for antibody Fc engagement, it counterbalances and contextualises cellular responses to signals emanating from co-ligated activating receptors, such as the B-cell receptor and activating FcγR. These activities collectively suppress the emergence of B- cell-mediated autoimmune disease and immune complex-mediated pathologies. However, FcγRIIB upregulation within the tumour microenvironment limits the efficacy of monoclonal antibody (mAb)-mediated immunotherapy of cancer.

While the functional significance of FcγRIIB is well established in mice, its physiological roles and the regulatory mechanisms governing its expression remain incompletely understood in humans. Here we characterise the molecular determinants of FcγRIIB expression in human immune models and primary cells. Our findings reveal that the ETS-family transcription factor PU.1 plays a crucial role in regulating basal and inducible FcγRIIB expression. Moreover, when co-expressed, PU.1 co-operates with the related ETS-family member SPIB to drive FcγRIIB expression. PU.1 binding to the proximal FcγRIIB promoter elicits transcription, at least in part, through recruitment of the CBP/p300 transcriptional co-activators. Interestingly, similar mechanisms are also observed at the proximal promoters of the activating FcγRI and FcγRIIA, suggesting that additional, potentially lineage specific, factors cooperate with PU.1 to drive the distinct expression patterns of these FcγR. These insights pave the way for future investigations aimed at understanding the molecular mechanisms responsible for cell lineage-specific FcγR expression and subsequently manipulating them for therapeutic purposes.

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Accepted/In Press date: 10 April 2025
e-pub ahead of print date: 26 May 2025
Published date: August 2025
Keywords: FCGR2B, Fcγ receptors, PU.1, gene regulation, immunotherapy

Identifiers

Local EPrints ID: 503758
URI: http://eprints.soton.ac.uk/id/eprint/503758
ISSN: 0022-1767
PURE UUID: 743ed7bc-441f-4b77-902a-ba6670ec439e
ORCID for Yury D. Bogdanov: ORCID iD orcid.org/0000-0003-4667-5890
ORCID for Rosanna C. Smith: ORCID iD orcid.org/0000-0002-4058-1263
ORCID for Lili Ferson: ORCID iD orcid.org/0000-0002-4840-4384
ORCID for Jonathan C. Strefford: ORCID iD orcid.org/0000-0002-0972-2881
ORCID for Stephen A. Beers: ORCID iD orcid.org/0000-0002-3765-3342
ORCID for Mark S. Cragg: ORCID iD orcid.org/0000-0003-2077-089X

Catalogue record

Date deposited: 12 Aug 2025 17:04
Last modified: 01 Oct 2025 02:13

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Contributors

Author: Rosanna C. Smith ORCID iD
Author: Kerry L. Cox
Author: Sarah Frampton
Author: Lili Ferson ORCID iD
Author: Russell B. Foxall
Author: Khiyam Hussain
Author: Mark S. Cragg ORCID iD

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