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Differentiation signals induce APOBEC3A expression via GRHL3 in squamous epithelia and squamous cell carcinoma

Differentiation signals induce APOBEC3A expression via GRHL3 in squamous epithelia and squamous cell carcinoma
Differentiation signals induce APOBEC3A expression via GRHL3 in squamous epithelia and squamous cell carcinoma
Two APOBEC DNA cytosine deaminase enzymes, APOBEC3A and APOBEC3B, generate somatic mutations in cancer, thereby driving tumour development and drug resistance. Here, we used single-cell RNA sequencing to study APOBEC3A and APOBEC3B expression in healthy and malignant mucosal epithelia, validating key observations with immunohistochemistry, spatial transcriptomics and functional experiments. Whereas APOBEC3B is expressed in keratinocytes entering mitosis, we show that APOBEC3A expression is confined largely to terminally differentiating cells and requires grainyhead-like transcription factor 3 (GRHL3). Thus, in normal tissue, neither deaminase appears to be expressed at high levels during DNA replication, the cell-cycle stage associated with APOBEC-mediated mutagenesis. In contrast, in squamous cell carcinoma we find that, there is expansion of GRHL3expression and activity to a subset of cells undergoing DNA replication and concomitant extension of APOBEC3A expression to proliferating cells. These findings suggest that APOBEC3A may play a functional role during keratinocyte differentiation, and offer a mechanism for acquisition of APOBEC3A mutagenic activity in tumours.
0261-4189
Smith, Nicola
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Reddin, Ian
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Policelli, Paige
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Oh, Sunwoo
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Zainal, Nur
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Howes, Emma
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Jenkins, Benjamin
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Tracy, Ian
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Edmond, Mark
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Sharpe, Benjamin
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Amendra, Damian
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Zheng, Ke
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Egawa, Nagayasu
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Doorbar, John
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Rao, Anjali
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Mahadevan, Sangeetha
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Carpenter, Michael A.
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Harris, Reuben S.
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Ali, Simak
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Hanley, Christopher
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Buisson, Rémi
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King, Emma
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Thomas, Gareth J.
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Fenton, Tim R.
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Smith, Nicola
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Reddin, Ian
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Policelli, Paige
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Oh, Sunwoo
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Zainal, Nur
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Howes, Emma
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Jenkins, Benjamin
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Tracy, Ian
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Edmond, Mark
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Sharpe, Benjamin
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Amendra, Damian
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Zheng, Ke
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Egawa, Nagayasu
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Doorbar, John
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Rao, Anjali
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Mahadevan, Sangeetha
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Carpenter, Michael A.
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Harris, Reuben S.
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Ali, Simak
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Hanley, Christopher
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Buisson, Rémi
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King, Emma
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Thomas, Gareth J.
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Fenton, Tim R.
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Smith, Nicola, Reddin, Ian, Policelli, Paige, Oh, Sunwoo, Zainal, Nur, Howes, Emma, Jenkins, Benjamin, Tracy, Ian, Edmond, Mark, Sharpe, Benjamin, Amendra, Damian, Zheng, Ke, Egawa, Nagayasu, Doorbar, John, Rao, Anjali, Mahadevan, Sangeetha, Carpenter, Michael A., Harris, Reuben S., Ali, Simak, Hanley, Christopher, Buisson, Rémi, King, Emma, Thomas, Gareth J. and Fenton, Tim R. (2024) Differentiation signals induce APOBEC3A expression via GRHL3 in squamous epithelia and squamous cell carcinoma. The EMBO Journal. (doi:10.1038/s44318-024-00298-9).

Record type: Article

Abstract

Two APOBEC DNA cytosine deaminase enzymes, APOBEC3A and APOBEC3B, generate somatic mutations in cancer, thereby driving tumour development and drug resistance. Here, we used single-cell RNA sequencing to study APOBEC3A and APOBEC3B expression in healthy and malignant mucosal epithelia, validating key observations with immunohistochemistry, spatial transcriptomics and functional experiments. Whereas APOBEC3B is expressed in keratinocytes entering mitosis, we show that APOBEC3A expression is confined largely to terminally differentiating cells and requires grainyhead-like transcription factor 3 (GRHL3). Thus, in normal tissue, neither deaminase appears to be expressed at high levels during DNA replication, the cell-cycle stage associated with APOBEC-mediated mutagenesis. In contrast, in squamous cell carcinoma we find that, there is expansion of GRHL3expression and activity to a subset of cells undergoing DNA replication and concomitant extension of APOBEC3A expression to proliferating cells. These findings suggest that APOBEC3A may play a functional role during keratinocyte differentiation, and offer a mechanism for acquisition of APOBEC3A mutagenic activity in tumours.

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More information

Accepted/In Press date: 24 October 2024
e-pub ahead of print date: 15 November 2024

Identifiers

Local EPrints ID: 490178
URI: http://eprints.soton.ac.uk/id/eprint/490178
ISSN: 0261-4189
PURE UUID: 05c23ddf-10c6-460e-90e4-11d14020d853
ORCID for Ian Reddin: ORCID iD orcid.org/0000-0001-5478-7855
ORCID for Paige Policelli: ORCID iD orcid.org/0000-0002-8854-0081
ORCID for Ian Tracy: ORCID iD orcid.org/0000-0003-4624-672X
ORCID for Christopher Hanley: ORCID iD orcid.org/0000-0003-3816-7220
ORCID for Tim R. Fenton: ORCID iD orcid.org/0000-0002-4737-8233

Catalogue record

Date deposited: 16 May 2024 16:40
Last modified: 16 Nov 2024 03:03

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Contributors

Author: Nicola Smith
Author: Ian Reddin ORCID iD
Author: Paige Policelli ORCID iD
Author: Sunwoo Oh
Author: Nur Zainal
Author: Emma Howes
Author: Benjamin Jenkins
Author: Ian Tracy ORCID iD
Author: Mark Edmond
Author: Benjamin Sharpe
Author: Damian Amendra
Author: Ke Zheng
Author: Nagayasu Egawa
Author: John Doorbar
Author: Anjali Rao
Author: Sangeetha Mahadevan
Author: Michael A. Carpenter
Author: Reuben S. Harris
Author: Simak Ali
Author: Rémi Buisson
Author: Emma King
Author: Tim R. Fenton ORCID iD

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