RNA editing deficiency models differential immunogenicity of pancreatic α- and β-cells

Objective: A longstanding question in type 1 diabetes (T1D) research pertains to the selective loss of β-cells whilst neighboring islet α-cells remain unharmed. We examined molecular mechanisms that may underly this differential vulnerability, by investigating the role of RNA editing, a cellular pro...

Full description

Saved in:
Bibliographic Details
Main Authors: Shani Peleg, Liza Zamashanski, Jonathan Belin, Roy Novoselsky, Roni Cohen-Fultheim, Udi Ehud Knebel, Benjamin Glaser, Shalev Itzkovitz, Klaus H. Kaestner, Alvin C. Powers, Erez Y. Levanon, Agnes Klochendler, Yuval Dor
Format: Article
Language:English
Published: Elsevier 2025-08-01
Series:Molecular Metabolism
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2212877825000900
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849744426028498944
author Shani Peleg
Liza Zamashanski
Jonathan Belin
Roy Novoselsky
Roni Cohen-Fultheim
Udi Ehud Knebel
Benjamin Glaser
Shalev Itzkovitz
Klaus H. Kaestner
Alvin C. Powers
Erez Y. Levanon
Agnes Klochendler
Yuval Dor
author_facet Shani Peleg
Liza Zamashanski
Jonathan Belin
Roy Novoselsky
Roni Cohen-Fultheim
Udi Ehud Knebel
Benjamin Glaser
Shalev Itzkovitz
Klaus H. Kaestner
Alvin C. Powers
Erez Y. Levanon
Agnes Klochendler
Yuval Dor
author_sort Shani Peleg
collection DOAJ
description Objective: A longstanding question in type 1 diabetes (T1D) research pertains to the selective loss of β-cells whilst neighboring islet α-cells remain unharmed. We examined molecular mechanisms that may underly this differential vulnerability, by investigating the role of RNA editing, a cellular process that prevents double-stranded RNA (dsRNA)-mediated interferon response, in mouse α- and β-cells. Methods: The enzyme responsible for RNA editing, Adar, was selectively deleted in vivo in mouse β-cells, α-cells, or in both cell types. Subsequent analyses were performed to investigate the impact of deficient RNA editing in α- or β-cells on the interferon response, islet inflammation, cell viability and metabolic outcomes. Results: Mosaic disruption of the Adar gene in mouse β-cells triggers a massive interferon response, islet inflammation and mutant β-cell destruction. Surprisingly, wild type β-cells are also eliminated, whereas neighboring α-cells are unaffected. α-cell Adar deletion leads to only a slight elevation in interferon signature and does not elicit inflammation nor a metabolic phenotype. Concomitant deletion of Adar in α- and β-cells leads to elimination of both cell populations, suggesting that in contrast to β-cells, α-cell death requires both cell autonomous deficiency in RNA editing and exogenous cytokines. Conclusions: We demonstrate differential sensitivity of mouse α- and β-cells to deficient RNA editing. The resistance of α-cells to RNA editing deficiency and to cytokines mirrors their persistence in T1D, and constitutes a molecularly defined model of differential islet cell vulnerability.
format Article
id doaj-art-b39b6cd886c7477b94079fd0f4811d41
institution DOAJ
issn 2212-8778
language English
publishDate 2025-08-01
publisher Elsevier
record_format Article
series Molecular Metabolism
spelling doaj-art-b39b6cd886c7477b94079fd0f4811d412025-08-20T03:17:24ZengElsevierMolecular Metabolism2212-87782025-08-019810218310.1016/j.molmet.2025.102183RNA editing deficiency models differential immunogenicity of pancreatic α- and β-cellsShani Peleg0Liza Zamashanski1Jonathan Belin2Roy Novoselsky3Roni Cohen-Fultheim4Udi Ehud Knebel5Benjamin Glaser6Shalev Itzkovitz7Klaus H. Kaestner8Alvin C. Powers9Erez Y. Levanon10Agnes Klochendler11Yuval Dor12Department of Developmental Biology and Cancer Research, Institute for Medical Research Israel-Canada, Faculty of Medicine, The Hebrew University of Jerusalem, Jerusalem, IsraelDepartment of Developmental Biology and Cancer Research, Institute for Medical Research Israel-Canada, Faculty of Medicine, The Hebrew University of Jerusalem, Jerusalem, IsraelDepartment of Developmental Biology and Cancer Research, Institute for Medical Research Israel-Canada, Faculty of Medicine, The Hebrew University of Jerusalem, Jerusalem, IsraelDepartment of Molecular Cell Biology, Weizmann Institute of Science, Rehovot, IsraelThe Mina and Everard Goodman Faculty of Life Sciences, Bar-Ilan University, Ramat Gan, 5290002, Israel; Institute of Nanotechnology and Advanced Materials, Bar-Ilan University, Ramat Gan, IsraelDepartment of Developmental Biology and Cancer Research, Institute for Medical Research Israel-Canada, Faculty of Medicine, The Hebrew University of Jerusalem, Jerusalem, IsraelDepartment of Endocrinology and Metabolism, Hadassah Medical Center and Faculty of Medicine, Hebrew University of Jerusalem, IsraelDepartment of Molecular Cell Biology, Weizmann Institute of Science, Rehovot, IsraelDepartment of Genetics and Institute for Diabetes, Obesity, and Metabolism, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USADivision of Diabetes, Endocrinology and Metabolism, Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, 37232, USA; Department of Molecular Physiology and Biophysics, Vanderbilt University School of Medicine, Nashville, TN, 37232, USA; VA Tennessee Valley Healthcare System, Nashville, TN, 37212, USAThe Mina and Everard Goodman Faculty of Life Sciences, Bar-Ilan University, Ramat Gan, 5290002, Israel; Institute of Nanotechnology and Advanced Materials, Bar-Ilan University, Ramat Gan, IsraelDepartment of Developmental Biology and Cancer Research, Institute for Medical Research Israel-Canada, Faculty of Medicine, The Hebrew University of Jerusalem, Jerusalem, Israel; Corresponding author.Department of Developmental Biology and Cancer Research, Institute for Medical Research Israel-Canada, Faculty of Medicine, The Hebrew University of Jerusalem, Jerusalem, Israel; Corresponding author.Objective: A longstanding question in type 1 diabetes (T1D) research pertains to the selective loss of β-cells whilst neighboring islet α-cells remain unharmed. We examined molecular mechanisms that may underly this differential vulnerability, by investigating the role of RNA editing, a cellular process that prevents double-stranded RNA (dsRNA)-mediated interferon response, in mouse α- and β-cells. Methods: The enzyme responsible for RNA editing, Adar, was selectively deleted in vivo in mouse β-cells, α-cells, or in both cell types. Subsequent analyses were performed to investigate the impact of deficient RNA editing in α- or β-cells on the interferon response, islet inflammation, cell viability and metabolic outcomes. Results: Mosaic disruption of the Adar gene in mouse β-cells triggers a massive interferon response, islet inflammation and mutant β-cell destruction. Surprisingly, wild type β-cells are also eliminated, whereas neighboring α-cells are unaffected. α-cell Adar deletion leads to only a slight elevation in interferon signature and does not elicit inflammation nor a metabolic phenotype. Concomitant deletion of Adar in α- and β-cells leads to elimination of both cell populations, suggesting that in contrast to β-cells, α-cell death requires both cell autonomous deficiency in RNA editing and exogenous cytokines. Conclusions: We demonstrate differential sensitivity of mouse α- and β-cells to deficient RNA editing. The resistance of α-cells to RNA editing deficiency and to cytokines mirrors their persistence in T1D, and constitutes a molecularly defined model of differential islet cell vulnerability.http://www.sciencedirect.com/science/article/pii/S2212877825000900RNA editingType 1 diabetesβ-cellsα-cellsIslet inflammationInterferon response
spellingShingle Shani Peleg
Liza Zamashanski
Jonathan Belin
Roy Novoselsky
Roni Cohen-Fultheim
Udi Ehud Knebel
Benjamin Glaser
Shalev Itzkovitz
Klaus H. Kaestner
Alvin C. Powers
Erez Y. Levanon
Agnes Klochendler
Yuval Dor
RNA editing deficiency models differential immunogenicity of pancreatic α- and β-cells
Molecular Metabolism
RNA editing
Type 1 diabetes
β-cells
α-cells
Islet inflammation
Interferon response
title RNA editing deficiency models differential immunogenicity of pancreatic α- and β-cells
title_full RNA editing deficiency models differential immunogenicity of pancreatic α- and β-cells
title_fullStr RNA editing deficiency models differential immunogenicity of pancreatic α- and β-cells
title_full_unstemmed RNA editing deficiency models differential immunogenicity of pancreatic α- and β-cells
title_short RNA editing deficiency models differential immunogenicity of pancreatic α- and β-cells
title_sort rna editing deficiency models differential immunogenicity of pancreatic α and β cells
topic RNA editing
Type 1 diabetes
β-cells
α-cells
Islet inflammation
Interferon response
url http://www.sciencedirect.com/science/article/pii/S2212877825000900
work_keys_str_mv AT shanipeleg rnaeditingdeficiencymodelsdifferentialimmunogenicityofpancreaticaandbcells
AT lizazamashanski rnaeditingdeficiencymodelsdifferentialimmunogenicityofpancreaticaandbcells
AT jonathanbelin rnaeditingdeficiencymodelsdifferentialimmunogenicityofpancreaticaandbcells
AT roynovoselsky rnaeditingdeficiencymodelsdifferentialimmunogenicityofpancreaticaandbcells
AT ronicohenfultheim rnaeditingdeficiencymodelsdifferentialimmunogenicityofpancreaticaandbcells
AT udiehudknebel rnaeditingdeficiencymodelsdifferentialimmunogenicityofpancreaticaandbcells
AT benjaminglaser rnaeditingdeficiencymodelsdifferentialimmunogenicityofpancreaticaandbcells
AT shalevitzkovitz rnaeditingdeficiencymodelsdifferentialimmunogenicityofpancreaticaandbcells
AT klaushkaestner rnaeditingdeficiencymodelsdifferentialimmunogenicityofpancreaticaandbcells
AT alvincpowers rnaeditingdeficiencymodelsdifferentialimmunogenicityofpancreaticaandbcells
AT erezylevanon rnaeditingdeficiencymodelsdifferentialimmunogenicityofpancreaticaandbcells
AT agnesklochendler rnaeditingdeficiencymodelsdifferentialimmunogenicityofpancreaticaandbcells
AT yuvaldor rnaeditingdeficiencymodelsdifferentialimmunogenicityofpancreaticaandbcells