Type 2 Diabetes and Congenital Hyperinsulinism Cause DNA Double-Strand Breaks and p53 Activity in β Cells
β cell failure in type 2 diabetes (T2D) is associated with hyperglycemia, but the mechanisms are not fully understood. Congenital hyperinsulinism caused by glucokinase mutations (GCK-CHI) is associated with β cell replication and apoptosis. Here, we show that genetic activation of β cell glucokinase...
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Published in | Cell metabolism Vol. 19; no. 1; pp. 109 - 121 |
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Main Authors | , , , , , , , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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Elsevier Inc
07.01.2014
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Abstract | β cell failure in type 2 diabetes (T2D) is associated with hyperglycemia, but the mechanisms are not fully understood. Congenital hyperinsulinism caused by glucokinase mutations (GCK-CHI) is associated with β cell replication and apoptosis. Here, we show that genetic activation of β cell glucokinase, initially triggering replication, causes apoptosis associated with DNA double-strand breaks and activation of the tumor suppressor p53. ATP-sensitive potassium channels (KATP channels) and calcineurin mediate this toxic effect. Toxicity of long-term glucokinase overactivity was confirmed by finding late-onset diabetes in older members of a GCK-CHI family. Glucagon-like peptide-1 (GLP-1) mimetic treatment or p53 deletion rescues β cells from glucokinase-induced death, but only GLP-1 analog rescues β cell function. DNA damage and p53 activity in T2D suggest shared mechanisms of β cell failure in hyperglycemia and CHI. Our results reveal membrane depolarization via KATP channels, calcineurin signaling, DNA breaks, and p53 as determinants of β cell glucotoxicity and suggest pharmacological approaches to enhance β cell survival in diabetes.
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•β cell DNA damage and p53 activity in type 2 diabetes and congenital hyperinsulinism•Hyperglycolysis causes DNA breaks and β cell death via KATP channel inactivation•A GLP-1 analog or p53 deletion prevents glucotoxic β cell death |
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AbstractList | β cell failure in type 2 diabetes (T2D) is associated with hyperglycemia, but the mechanisms are not fully understood. Congenital hyperinsulinism caused by glucokinase mutations (GCK-CHI) is associated with β cell replication and apoptosis. Here, we show that genetic activation of β cell glucokinase, initially triggering replication, causes apoptosis associated with DNA double-strand breaks and activation of the tumor suppressor p53. ATP-sensitive potassium channels (KATP channels) and calcineurin mediate this toxic effect. Toxicity of long-term glucokinase overactivity was confirmed by finding late-onset diabetes in older members of a GCK-CHI family. Glucagon-like peptide-1 (GLP-1) mimetic treatment or p53 deletion rescues β cells from glucokinase-induced death, but only GLP-1 analog rescues β cell function. DNA damage and p53 activity in T2D suggest shared mechanisms of β cell failure in hyperglycemia and CHI. Our results reveal membrane depolarization via KATP channels, calcineurin signaling, DNA breaks, and p53 as determinants of β cell glucotoxicity and suggest pharmacological approaches to enhance β cell survival in diabetes. Summary beta cell failure in type 2 diabetes (T2D) is associated with hyperglycemia, but the mechanisms are not fully understood. Congenital hyperinsulinism caused by glucokinase mutations (GCK-CHI) is associated with beta cell replication and apoptosis. Here, we show that genetic activation of beta cell glucokinase, initially triggering replication, causes apoptosis associated with DNA double-strand breaks and activation of the tumor suppressor p53. ATP-sensitive potassium channels (KATP channels) and calcineurin mediate this toxic effect. Toxicity of long-term glucokinase overactivity was confirmed by finding late-onset diabetes in older members of a GCK-CHI family. Glucagon-like peptide-1 (GLP-1) mimetic treatment or p53 deletion rescues beta cells from glucokinase-induced death, but only GLP-1 analog rescues beta cell function. DNA damage and p53 activity in T2D suggest shared mechanisms of beta cell failure in hyperglycemia and CHI. Our results reveal membrane depolarization via KATP channels, calcineurin signaling, DNA breaks, and p53 as determinants of beta cell glucotoxicity and suggest pharmacological approaches to enhance beta cell survival in diabetes. β cell failure in type 2 diabetes (T2D) is associated with hyperglycemia, but the mechanisms are not fully understood. Congenital hyperinsulinism caused by glucokinase mutations (GCK-CHI) is associated with β cell replication and apoptosis. Here, we show that genetic activation of β cell glucokinase, initially triggering replication, causes apoptosis associated with DNA double-strand breaks and activation of the tumor suppressor p53. ATP-sensitive potassium channels (KATP channels) and calcineurin mediate this toxic effect. Toxicity of long-term glucokinase overactivity was confirmed by finding late-onset diabetes in older members of a GCK-CHI family. Glucagon-like peptide-1 (GLP-1) mimetic treatment or p53 deletion rescues β cells from glucokinase-induced death, but only GLP-1 analog rescues β cell function. DNA damage and p53 activity in T2D suggest shared mechanisms of β cell failure in hyperglycemia and CHI. Our results reveal membrane depolarization via KATP channels, calcineurin signaling, DNA breaks, and p53 as determinants of β cell glucotoxicity and suggest pharmacological approaches to enhance β cell survival in diabetes. [Display omitted] •β cell DNA damage and p53 activity in type 2 diabetes and congenital hyperinsulinism•Hyperglycolysis causes DNA breaks and β cell death via KATP channel inactivation•A GLP-1 analog or p53 deletion prevents glucotoxic β cell death |
Author | Ziv, Oren Stanley, Charles Dadon, Daniela Glaser, Benjamin Stolovich-Rain, Miri Porat, Shay Philipson, Louis H. Furth-Lavi, Judith Granot, Zvi Tzipilevich, Elhanan Magnuson, Mark A. Dor, Yuval Ashcroft, Frances M. In’t Veld, Peter Kadosh, Tehila Herold, Kevan C. Tornovsky-Babeay, Sharona Schyr-Ben Haroush, Rachel Bhatti, Tricia R. Saada, Ann Hija, Ayat |
Author_xml | – sequence: 1 givenname: Sharona surname: Tornovsky-Babeay fullname: Tornovsky-Babeay, Sharona organization: Endocrinology and Metabolism Service, Department of Internal Medicine, Hadassah-Hebrew University Medical Center, Jerusalem 91120, Israel – sequence: 2 givenname: Daniela surname: Dadon fullname: Dadon, Daniela organization: Department of Developmental Biology and Cancer Research, The Institute for Medical Research Israel-Canada, The Hebrew University-Hadassah Medical School, Jerusalem 91120, Israel – sequence: 3 givenname: Oren surname: Ziv fullname: Ziv, Oren organization: Department of Developmental Biology and Cancer Research, The Institute for Medical Research Israel-Canada, The Hebrew University-Hadassah Medical School, Jerusalem 91120, Israel – sequence: 4 givenname: Elhanan surname: Tzipilevich fullname: Tzipilevich, Elhanan organization: Department of Developmental Biology and Cancer Research, The Institute for Medical Research Israel-Canada, The Hebrew University-Hadassah Medical School, Jerusalem 91120, Israel – sequence: 5 givenname: Tehila surname: Kadosh fullname: Kadosh, Tehila organization: Department of Developmental Biology and Cancer Research, The Institute for Medical Research Israel-Canada, The Hebrew University-Hadassah Medical School, Jerusalem 91120, Israel – sequence: 6 givenname: Rachel surname: Schyr-Ben Haroush fullname: Schyr-Ben Haroush, Rachel organization: Endocrinology and Metabolism Service, Department of Internal Medicine, Hadassah-Hebrew University Medical Center, Jerusalem 91120, Israel – sequence: 7 givenname: Ayat surname: Hija fullname: Hija, Ayat organization: Department of Developmental Biology and Cancer Research, The Institute for Medical Research Israel-Canada, The Hebrew University-Hadassah Medical School, Jerusalem 91120, Israel – sequence: 8 givenname: Miri surname: Stolovich-Rain fullname: Stolovich-Rain, Miri organization: Department of Developmental Biology and Cancer Research, The Institute for Medical Research Israel-Canada, The Hebrew University-Hadassah Medical School, Jerusalem 91120, Israel – sequence: 9 givenname: Judith surname: Furth-Lavi fullname: Furth-Lavi, Judith organization: Endocrinology and Metabolism Service, Department of Internal Medicine, Hadassah-Hebrew University Medical Center, Jerusalem 91120, Israel – sequence: 10 givenname: Zvi surname: Granot fullname: Granot, Zvi organization: Department of Developmental Biology and Cancer Research, The Institute for Medical Research Israel-Canada, The Hebrew University-Hadassah Medical School, Jerusalem 91120, Israel – sequence: 11 givenname: Shay surname: Porat fullname: Porat, Shay organization: Department of Developmental Biology and Cancer Research, The Institute for Medical Research Israel-Canada, The Hebrew University-Hadassah Medical School, Jerusalem 91120, Israel – sequence: 12 givenname: Louis H. surname: Philipson fullname: Philipson, Louis H. organization: Department of Medicine, The University of Chicago, Chicago, IL 60637, USA – sequence: 13 givenname: Kevan C. surname: Herold fullname: Herold, Kevan C. organization: Departments of Immunobiology and Internal Medicine, Yale University School of Medicine, New Haven, CT 06511, USA – sequence: 14 givenname: Tricia R. surname: Bhatti fullname: Bhatti, Tricia R. organization: Division of Endocrinology and Diabetes, The Children’s Hospital of Philadelphia, Philadelphia, PA 19104, USA – sequence: 15 givenname: Charles surname: Stanley fullname: Stanley, Charles organization: Division of Endocrinology and Diabetes, The Children’s Hospital of Philadelphia, Philadelphia, PA 19104, USA – sequence: 16 givenname: Frances M. surname: Ashcroft fullname: Ashcroft, Frances M. organization: Department of Physiology, Anatomy & Genetics, Oxford University, Oxford OX1 3QX, UK – sequence: 17 givenname: Peter surname: In’t Veld fullname: In’t Veld, Peter organization: Diabetes Research Center, Brussels Free University, Laarbeeklaan 103, B1090 Brussels, Belgium – sequence: 18 givenname: Ann surname: Saada fullname: Saada, Ann organization: Monique and Jacques Roboh Department of Genetic Research and the Department of Genetics and Metabolic Diseases, Hadassah-Hebrew University Medical Center, Jerusalem 91120, Israel – sequence: 19 givenname: Mark A. surname: Magnuson fullname: Magnuson, Mark A. organization: Center for Stem Cell Biology and Department of Molecular Physiology and Biophysics, Vanderbilt University School of Medicine, Nashville, TN 37232, USA – sequence: 20 givenname: Benjamin surname: Glaser fullname: Glaser, Benjamin email: beng@cc.huji.ac.il organization: Endocrinology and Metabolism Service, Department of Internal Medicine, Hadassah-Hebrew University Medical Center, Jerusalem 91120, Israel – sequence: 21 givenname: Yuval surname: Dor fullname: Dor, Yuval email: yuvald@ekmd.huji.ac.il organization: Department of Developmental Biology and Cancer Research, The Institute for Medical Research Israel-Canada, The Hebrew University-Hadassah Medical School, Jerusalem 91120, Israel |
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Snippet | β cell failure in type 2 diabetes (T2D) is associated with hyperglycemia, but the mechanisms are not fully understood. Congenital hyperinsulinism caused by... β cell failure in type 2 diabetes (T2D) is associated with hyperglycemia, but the mechanisms are not fully understood. Congenital hyperinsulinism caused by... Summary beta cell failure in type 2 diabetes (T2D) is associated with hyperglycemia, but the mechanisms are not fully understood. Congenital hyperinsulinism... |
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SubjectTerms | Animals Biomarkers - metabolism Calcineurin - metabolism Cell Death - drug effects Cell Proliferation - drug effects Congenital Hyperinsulinism - complications Congenital Hyperinsulinism - enzymology Congenital Hyperinsulinism - pathology Diabetes Mellitus, Type 2 - complications Diabetes Mellitus, Type 2 - enzymology Diabetes Mellitus, Type 2 - pathology Disease Models, Animal DNA Breaks, Double-Stranded - drug effects Enzyme Activation - drug effects Enzyme Induction - drug effects Fasting - metabolism Glucagon-Like Peptide 1 - pharmacology Glucokinase - biosynthesis Glucose - toxicity Humans Insulin-Secreting Cells - drug effects Insulin-Secreting Cells - enzymology Insulin-Secreting Cells - metabolism Insulin-Secreting Cells - pathology Membrane Potentials - drug effects Mice Transgenes Tumor Suppressor Protein p53 - metabolism |
Title | Type 2 Diabetes and Congenital Hyperinsulinism Cause DNA Double-Strand Breaks and p53 Activity in β Cells |
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