Pancreatic β cell interleukin-22 receptor subunit alpha 1 deficiency impairs β cell function in type 2 diabetes via cytochrome b5 reductase 3

Summary: Impaired β cell function is a hallmark of type 2 diabetes (T2D), but the underlying cellular signaling machineries that regulate β cell function remain unknown. Here, we identify that the interleukin-22 receptor subunit alpha 1 (IL-22RA1), known as a co-receptor for IL-22, is downregulated...

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Main Authors: Fan Yu, Shuting Xie, Tongyu Wang, Yeping Huang, Hong Zhang, Danfeng Peng, Yifan Feng, Yumei Yang, Zheyu Zhang, Yunxia Zhu, Zhuoxian Meng, Rong Zhang, Xiaomu Li, Hao Yin, Jie Xu, Cheng Hu
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Language:English
Published: Elsevier 2024-12-01
Series:Cell Reports
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Online Access:http://www.sciencedirect.com/science/article/pii/S2211124724014086
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author Fan Yu
Shuting Xie
Tongyu Wang
Yeping Huang
Hong Zhang
Danfeng Peng
Yifan Feng
Yumei Yang
Zheyu Zhang
Yunxia Zhu
Zhuoxian Meng
Rong Zhang
Xiaomu Li
Hao Yin
Jie Xu
Cheng Hu
author_facet Fan Yu
Shuting Xie
Tongyu Wang
Yeping Huang
Hong Zhang
Danfeng Peng
Yifan Feng
Yumei Yang
Zheyu Zhang
Yunxia Zhu
Zhuoxian Meng
Rong Zhang
Xiaomu Li
Hao Yin
Jie Xu
Cheng Hu
author_sort Fan Yu
collection DOAJ
description Summary: Impaired β cell function is a hallmark of type 2 diabetes (T2D), but the underlying cellular signaling machineries that regulate β cell function remain unknown. Here, we identify that the interleukin-22 receptor subunit alpha 1 (IL-22RA1), known as a co-receptor for IL-22, is downregulated in human and mouse T2D β cells. Mice with β cell Il22ra1 knockout (Il22ra1βKO) exhibit defective insulin secretion and impaired glucose tolerance after being fed a high-fat diet (HFD) or an HFD/low dose of streptozotocin (STZ). Mechanistically, β cell IL-22RA1 deficiency inhibits cytochrome b5 reductase 3 (CYB5R3) expression via the IL-22RA1/signal transducer and activator of the transcription 3 (STAT3)/c-Jun axis, thereby impairing mitochondrial function and reducing β cell identity. Overexpression of CYB5R3 reinstates mitochondrial function, β cell identity, and insulin secretion in Il22ra1βKO mice. Moreover, the pharmacological activation of CYB5R3 with tetrahydroindenoindole restores insulin secretion in Il22ra1βKO mice, IL-22RA1-knockdown human islets, and Min6 cells. In conclusion, these findings suggest an important role of IL-22RA1 in preserving β cell function in T2D, which offers a potential therapeutic target for treating diabetes.
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spelling doaj-art-b621618e862344b8b062771bb13e98f52024-12-15T06:15:25ZengElsevierCell Reports2211-12472024-12-014312115057Pancreatic β cell interleukin-22 receptor subunit alpha 1 deficiency impairs β cell function in type 2 diabetes via cytochrome b5 reductase 3Fan Yu0Shuting Xie1Tongyu Wang2Yeping Huang3Hong Zhang4Danfeng Peng5Yifan Feng6Yumei Yang7Zheyu Zhang8Yunxia Zhu9Zhuoxian Meng10Rong Zhang11Xiaomu Li12Hao Yin13Jie Xu14Cheng Hu15Shanghai Diabetes Institute, Department of Endocrinology and Metabolism, Shanghai Key Laboratory of Diabetes Mellitus, Shanghai Clinical Centre for Diabetes, Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai 200233, ChinaShanghai Diabetes Institute, Department of Endocrinology and Metabolism, Shanghai Key Laboratory of Diabetes Mellitus, Shanghai Clinical Centre for Diabetes, Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai 200233, ChinaShanghai Diabetes Institute, Department of Endocrinology and Metabolism, Shanghai Key Laboratory of Diabetes Mellitus, Shanghai Clinical Centre for Diabetes, Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai 200233, ChinaShanghai Diabetes Institute, Department of Endocrinology and Metabolism, Shanghai Key Laboratory of Diabetes Mellitus, Shanghai Clinical Centre for Diabetes, Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai 200233, ChinaShanghai Diabetes Institute, Department of Endocrinology and Metabolism, Shanghai Key Laboratory of Diabetes Mellitus, Shanghai Clinical Centre for Diabetes, Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai 200233, ChinaShanghai Diabetes Institute, Department of Endocrinology and Metabolism, Shanghai Key Laboratory of Diabetes Mellitus, Shanghai Clinical Centre for Diabetes, Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai 200233, ChinaOrgan Transplant Center, Shanghai Changzheng Hospital, Second Affiliated Hospital of Naval Medical University, Shanghai 200003, ChinaDepartment of Endocrinology and Metabolism, Zhongshan Hospital Affiliated to Fudan University, Shanghai 200032, ChinaDepartment of Pathology and Pathophysiology and Department of Cardiology of the Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang 310009, ChinaKey Laboratory of Human Functional Genomics of Jiangsu Province, Nanjing Medical University, Nanjing, Jiangsu 211166, ChinaDepartment of Pathology and Pathophysiology and Department of Cardiology of the Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang 310009, ChinaShanghai Diabetes Institute, Department of Endocrinology and Metabolism, Shanghai Key Laboratory of Diabetes Mellitus, Shanghai Clinical Centre for Diabetes, Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai 200233, ChinaDepartment of Endocrinology and Metabolism, Zhongshan Hospital Affiliated to Fudan University, Shanghai 200032, China; Corresponding authorOrgan Transplant Center, Shanghai Changzheng Hospital, Second Affiliated Hospital of Naval Medical University, Shanghai 200003, China; Corresponding authorShanghai Diabetes Institute, Department of Endocrinology and Metabolism, Shanghai Key Laboratory of Diabetes Mellitus, Shanghai Clinical Centre for Diabetes, Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai 200233, China; Corresponding authorShanghai Diabetes Institute, Department of Endocrinology and Metabolism, Shanghai Key Laboratory of Diabetes Mellitus, Shanghai Clinical Centre for Diabetes, Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai 200233, China; Institute for Metabolic Disease, Fengxian Central Hospital Affiliated to Southern Medical University, Shanghai 201499, China; Corresponding authorSummary: Impaired β cell function is a hallmark of type 2 diabetes (T2D), but the underlying cellular signaling machineries that regulate β cell function remain unknown. Here, we identify that the interleukin-22 receptor subunit alpha 1 (IL-22RA1), known as a co-receptor for IL-22, is downregulated in human and mouse T2D β cells. Mice with β cell Il22ra1 knockout (Il22ra1βKO) exhibit defective insulin secretion and impaired glucose tolerance after being fed a high-fat diet (HFD) or an HFD/low dose of streptozotocin (STZ). Mechanistically, β cell IL-22RA1 deficiency inhibits cytochrome b5 reductase 3 (CYB5R3) expression via the IL-22RA1/signal transducer and activator of the transcription 3 (STAT3)/c-Jun axis, thereby impairing mitochondrial function and reducing β cell identity. Overexpression of CYB5R3 reinstates mitochondrial function, β cell identity, and insulin secretion in Il22ra1βKO mice. Moreover, the pharmacological activation of CYB5R3 with tetrahydroindenoindole restores insulin secretion in Il22ra1βKO mice, IL-22RA1-knockdown human islets, and Min6 cells. In conclusion, these findings suggest an important role of IL-22RA1 in preserving β cell function in T2D, which offers a potential therapeutic target for treating diabetes.http://www.sciencedirect.com/science/article/pii/S2211124724014086CP: Metabolism
spellingShingle Fan Yu
Shuting Xie
Tongyu Wang
Yeping Huang
Hong Zhang
Danfeng Peng
Yifan Feng
Yumei Yang
Zheyu Zhang
Yunxia Zhu
Zhuoxian Meng
Rong Zhang
Xiaomu Li
Hao Yin
Jie Xu
Cheng Hu
Pancreatic β cell interleukin-22 receptor subunit alpha 1 deficiency impairs β cell function in type 2 diabetes via cytochrome b5 reductase 3
Cell Reports
CP: Metabolism
title Pancreatic β cell interleukin-22 receptor subunit alpha 1 deficiency impairs β cell function in type 2 diabetes via cytochrome b5 reductase 3
title_full Pancreatic β cell interleukin-22 receptor subunit alpha 1 deficiency impairs β cell function in type 2 diabetes via cytochrome b5 reductase 3
title_fullStr Pancreatic β cell interleukin-22 receptor subunit alpha 1 deficiency impairs β cell function in type 2 diabetes via cytochrome b5 reductase 3
title_full_unstemmed Pancreatic β cell interleukin-22 receptor subunit alpha 1 deficiency impairs β cell function in type 2 diabetes via cytochrome b5 reductase 3
title_short Pancreatic β cell interleukin-22 receptor subunit alpha 1 deficiency impairs β cell function in type 2 diabetes via cytochrome b5 reductase 3
title_sort pancreatic β cell interleukin 22 receptor subunit alpha 1 deficiency impairs β cell function in type 2 diabetes via cytochrome b5 reductase 3
topic CP: Metabolism
url http://www.sciencedirect.com/science/article/pii/S2211124724014086
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