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USP7 controls NGN3 stability and pancreatic endocrine lineage development

USP7 controls NGN3 stability and pancreatic endocrine lineage development
USP7 controls NGN3 stability and pancreatic endocrine lineage development

Understanding the factors and mechanisms involved in beta-cell development will guide therapeutic efforts to generate fully functional beta cells for diabetes. Neurogenin 3 (NGN3) is the key transcription factor that marks endocrine progenitors and drives beta-cell differentiation. Here we screen for binding partners of NGN3 and identify the deubiquitylating enzyme USP7 as a key regulator of NGN3 stability. Mechanistically, USP7 interacts with, deubiquitinates and stabilizes NGN3. In vivo, conditional knockout of Usp7 in the mouse embryonic pancreas causes a dramatic reduction in islet formation and hyperglycemia in adult mice, due to impaired NGN3-mediated endocrine specification during pancreatic development. Furthermore, pharmacological inhibition of USP7 during endocrine specification in human iPSC models of beta-cell differentiation decreases NGN3 expressing progenitor cell numbers and impairs beta cell differentiation. Thus, the USP7-NGN3 axis is an essential mechanism for driving endocrine development and beta-cell differentiation, which can be therapeutically exploited.

Adult, Animals, Humans, Mice, Basic Helix-Loop-Helix Transcription Factors/metabolism, Cell Differentiation, Islets of Langerhans/metabolism, Pancreas/metabolism, Transcription Factors/metabolism, Ubiquitin-Specific Peptidase 7/genetics
2041-1723
Manea, Teodora
b880590d-91b2-4f3c-a72a-6f3f6b480e79
Nelson, Jessica Kristine
7dc3f0c8-5a67-4467-a332-efd560a0630b
Garrone, Cristina Maria
b7f8cda5-f328-455a-a518-bbbc8d6a3c15
Hansson, Karin
b6cbfede-a5c3-4f74-9733-ec618b86ae2c
Evans, Ian
3eec7918-a789-4c47-aa19-8e014e4c23e9
Behrens, Axel
562a632f-5241-42aa-b554-d3c593f9b7ce
Sancho, Rocio
2ba8667c-1657-4c82-a847-fc257ee50bde
Manea, Teodora
b880590d-91b2-4f3c-a72a-6f3f6b480e79
Nelson, Jessica Kristine
7dc3f0c8-5a67-4467-a332-efd560a0630b
Garrone, Cristina Maria
b7f8cda5-f328-455a-a518-bbbc8d6a3c15
Hansson, Karin
b6cbfede-a5c3-4f74-9733-ec618b86ae2c
Evans, Ian
3eec7918-a789-4c47-aa19-8e014e4c23e9
Behrens, Axel
562a632f-5241-42aa-b554-d3c593f9b7ce
Sancho, Rocio
2ba8667c-1657-4c82-a847-fc257ee50bde

Manea, Teodora, Nelson, Jessica Kristine, Garrone, Cristina Maria, Hansson, Karin, Evans, Ian, Behrens, Axel and Sancho, Rocio (2023) USP7 controls NGN3 stability and pancreatic endocrine lineage development. Nature Communications, 14 (1), [2457]. (doi:10.1038/s41467-023-38146-9).

Record type: Article

Abstract

Understanding the factors and mechanisms involved in beta-cell development will guide therapeutic efforts to generate fully functional beta cells for diabetes. Neurogenin 3 (NGN3) is the key transcription factor that marks endocrine progenitors and drives beta-cell differentiation. Here we screen for binding partners of NGN3 and identify the deubiquitylating enzyme USP7 as a key regulator of NGN3 stability. Mechanistically, USP7 interacts with, deubiquitinates and stabilizes NGN3. In vivo, conditional knockout of Usp7 in the mouse embryonic pancreas causes a dramatic reduction in islet formation and hyperglycemia in adult mice, due to impaired NGN3-mediated endocrine specification during pancreatic development. Furthermore, pharmacological inhibition of USP7 during endocrine specification in human iPSC models of beta-cell differentiation decreases NGN3 expressing progenitor cell numbers and impairs beta cell differentiation. Thus, the USP7-NGN3 axis is an essential mechanism for driving endocrine development and beta-cell differentiation, which can be therapeutically exploited.

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s41467-023-38146-9 - Version of Record
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Accepted/In Press date: 18 April 2023
Published date: 28 April 2023
Keywords: Adult, Animals, Humans, Mice, Basic Helix-Loop-Helix Transcription Factors/metabolism, Cell Differentiation, Islets of Langerhans/metabolism, Pancreas/metabolism, Transcription Factors/metabolism, Ubiquitin-Specific Peptidase 7/genetics

Identifiers

Local EPrints ID: 505363
URI: http://eprints.soton.ac.uk/id/eprint/505363
ISSN: 2041-1723
PURE UUID: 37942330-ae9d-4e82-86d3-64122a6c01b6
ORCID for Jessica Kristine Nelson: ORCID iD orcid.org/0000-0003-2866-5170

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Date deposited: 07 Oct 2025 16:45
Last modified: 08 Oct 2025 02:17

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Contributors

Author: Teodora Manea
Author: Jessica Kristine Nelson ORCID iD
Author: Cristina Maria Garrone
Author: Karin Hansson
Author: Ian Evans
Author: Axel Behrens
Author: Rocio Sancho

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