DEP-1 is a brain insulin receptor phosphatase that prevents the simultaneous activation of counteracting metabolic pathways

Summary: A healthy metabolism relies on precise regulation of anabolic and catabolic pathways. While insulin deficiency impairs anabolism, insulin resistance in obesity causes metabolic dysfunction, especially via altered brain insulin receptor (IR) activity. Density-enhanced phosphatase 1 (DEP-1) n...

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Main Authors: Simran Chopra, Otsuware Linda-Josephine Kadiri, Jannis Ulke, Robert Hauffe, Wenke Jonas, Sahar Cheshmeh, Luisa Schmidt, Christopher A. Bishop, Selma Yagoub, Mareike Schell, Michaela Rath, Janine Krüger, Rachel N. Lippert, Marcus Krüger, Kai Kappert, André Kleinridders
Format: Article
Language:English
Published: Elsevier 2024-12-01
Series:Cell Reports
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Online Access:http://www.sciencedirect.com/science/article/pii/S2211124724013354
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author Simran Chopra
Otsuware Linda-Josephine Kadiri
Jannis Ulke
Robert Hauffe
Wenke Jonas
Sahar Cheshmeh
Luisa Schmidt
Christopher A. Bishop
Selma Yagoub
Mareike Schell
Michaela Rath
Janine Krüger
Rachel N. Lippert
Marcus Krüger
Kai Kappert
André Kleinridders
author_facet Simran Chopra
Otsuware Linda-Josephine Kadiri
Jannis Ulke
Robert Hauffe
Wenke Jonas
Sahar Cheshmeh
Luisa Schmidt
Christopher A. Bishop
Selma Yagoub
Mareike Schell
Michaela Rath
Janine Krüger
Rachel N. Lippert
Marcus Krüger
Kai Kappert
André Kleinridders
author_sort Simran Chopra
collection DOAJ
description Summary: A healthy metabolism relies on precise regulation of anabolic and catabolic pathways. While insulin deficiency impairs anabolism, insulin resistance in obesity causes metabolic dysfunction, especially via altered brain insulin receptor (IR) activity. Density-enhanced phosphatase 1 (DEP-1) negatively modulates the IR in peripheral tissues. Our study shows that DEP-1 is an insulin-regulated gene, dysregulated in obesity, and uncovers its role in brain insulin signaling, impacting both anabolic and catabolic pathways. Neuro-2a cells lacking DEP-1 demonstrated heightened IR phosphorylation upon acute insulin stimulation. This coincided with simultaneous AMP-activated protein kinase (AMPK) activation, which governs catabolic pathways, due to increased phospholipase C-gamma 1 signaling. These opposing pathways in male DEP-1 forebrain-specific knockout mice resulted in elevated lipolysis in white adipose tissue and fat oxidation in brown adipose tissue, with enhanced sympathetic activation and β-adrenergic receptor expression. In conclusion, DEP-1 deficiency causes the simultaneous activation of IR and AMPK signaling in the brain, with enhanced sympathetic activity in adipose tissues.
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spelling doaj-art-64bbfe6718224c24ba3e8e674c800a6a2025-08-20T01:52:42ZengElsevierCell Reports2211-12472024-12-01431211498410.1016/j.celrep.2024.114984DEP-1 is a brain insulin receptor phosphatase that prevents the simultaneous activation of counteracting metabolic pathwaysSimran Chopra0Otsuware Linda-Josephine Kadiri1Jannis Ulke2Robert Hauffe3Wenke Jonas4Sahar Cheshmeh5Luisa Schmidt6Christopher A. Bishop7Selma Yagoub8Mareike Schell9Michaela Rath10Janine Krüger11Rachel N. Lippert12Marcus Krüger13Kai Kappert14André Kleinridders15Department of Molecular and Experimental Nutritional Medicine, Institute of Nutritional Science, University of Potsdam, Arthur-Scheunert-Allee 114–116, 14558 Nuthetal, GermanyDepartment of Molecular and Experimental Nutritional Medicine, Institute of Nutritional Science, University of Potsdam, Arthur-Scheunert-Allee 114–116, 14558 Nuthetal, GermanyInstitute of Diagnostic Laboratory Medicine, Clinical Chemistry and Pathobiochemistry, Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, Augustenburger Platz 1, 13353 Berlin, Germany; Cardiovascular-Metabolic-Renal (CMR) Research Center, Charité – Universitätsmedizin Berlin, Hessische Straße 3–4, 10115 Berlin, GermanyDepartment of Molecular and Experimental Nutritional Medicine, Institute of Nutritional Science, University of Potsdam, Arthur-Scheunert-Allee 114–116, 14558 Nuthetal, GermanyDepartment of Experimental Diabetology, German Institute of Human Nutrition Potsdam-Rehbrücke (DIfE), 14558 Nuthetal, Germany; German Center for Diabetes Research (DZD), 85764 München-Neuherberg, GermanyDepartment of Molecular and Experimental Nutritional Medicine, Institute of Nutritional Science, University of Potsdam, Arthur-Scheunert-Allee 114–116, 14558 Nuthetal, GermanyInstitute for Genetics, Cologne Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases (CECAD), Cologne, GermanyDepartment Physiology of Energy Metabolism, German Institute of Human Nutrition Potsdam-Rehbrücke (DIfE), 14558 Nuthetal, GermanyDepartment of Neurocircuit, Development and Function, German Institute of Human Nutrition Potsdam-Rehbrücke (DIfE), 14558 Nuthetal, GermanyDepartment of Molecular and Experimental Nutritional Medicine, Institute of Nutritional Science, University of Potsdam, Arthur-Scheunert-Allee 114–116, 14558 Nuthetal, GermanyDepartment of Molecular and Experimental Nutritional Medicine, Institute of Nutritional Science, University of Potsdam, Arthur-Scheunert-Allee 114–116, 14558 Nuthetal, GermanyInstitute of Diagnostic Laboratory Medicine, Clinical Chemistry and Pathobiochemistry, Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, Augustenburger Platz 1, 13353 Berlin, Germany; Cardiovascular-Metabolic-Renal (CMR) Research Center, Charité – Universitätsmedizin Berlin, Hessische Straße 3–4, 10115 Berlin, GermanyGerman Center for Diabetes Research (DZD), 85764 München-Neuherberg, Germany; Department of Neurocircuit, Development and Function, German Institute of Human Nutrition Potsdam-Rehbrücke (DIfE), 14558 Nuthetal, Germany; NeuroCure Cluster of Excellence, Charité – Universitätsmedizin Berlin, 10117 Berlin, GermanyInstitute for Genetics, Cologne Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases (CECAD), Cologne, Germany; Center for Molecular Medicine (CMMC), University of Cologne, 50931 Cologne, GermanyInstitute of Diagnostic Laboratory Medicine, Clinical Chemistry and Pathobiochemistry, Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, Augustenburger Platz 1, 13353 Berlin, Germany; Cardiovascular-Metabolic-Renal (CMR) Research Center, Charité – Universitätsmedizin Berlin, Hessische Straße 3–4, 10115 Berlin, GermanyDepartment of Molecular and Experimental Nutritional Medicine, Institute of Nutritional Science, University of Potsdam, Arthur-Scheunert-Allee 114–116, 14558 Nuthetal, Germany; Corresponding authorSummary: A healthy metabolism relies on precise regulation of anabolic and catabolic pathways. While insulin deficiency impairs anabolism, insulin resistance in obesity causes metabolic dysfunction, especially via altered brain insulin receptor (IR) activity. Density-enhanced phosphatase 1 (DEP-1) negatively modulates the IR in peripheral tissues. Our study shows that DEP-1 is an insulin-regulated gene, dysregulated in obesity, and uncovers its role in brain insulin signaling, impacting both anabolic and catabolic pathways. Neuro-2a cells lacking DEP-1 demonstrated heightened IR phosphorylation upon acute insulin stimulation. This coincided with simultaneous AMP-activated protein kinase (AMPK) activation, which governs catabolic pathways, due to increased phospholipase C-gamma 1 signaling. These opposing pathways in male DEP-1 forebrain-specific knockout mice resulted in elevated lipolysis in white adipose tissue and fat oxidation in brown adipose tissue, with enhanced sympathetic activation and β-adrenergic receptor expression. In conclusion, DEP-1 deficiency causes the simultaneous activation of IR and AMPK signaling in the brain, with enhanced sympathetic activity in adipose tissues.http://www.sciencedirect.com/science/article/pii/S2211124724013354CP: NeuroscienceCP: Metabolism
spellingShingle Simran Chopra
Otsuware Linda-Josephine Kadiri
Jannis Ulke
Robert Hauffe
Wenke Jonas
Sahar Cheshmeh
Luisa Schmidt
Christopher A. Bishop
Selma Yagoub
Mareike Schell
Michaela Rath
Janine Krüger
Rachel N. Lippert
Marcus Krüger
Kai Kappert
André Kleinridders
DEP-1 is a brain insulin receptor phosphatase that prevents the simultaneous activation of counteracting metabolic pathways
Cell Reports
CP: Neuroscience
CP: Metabolism
title DEP-1 is a brain insulin receptor phosphatase that prevents the simultaneous activation of counteracting metabolic pathways
title_full DEP-1 is a brain insulin receptor phosphatase that prevents the simultaneous activation of counteracting metabolic pathways
title_fullStr DEP-1 is a brain insulin receptor phosphatase that prevents the simultaneous activation of counteracting metabolic pathways
title_full_unstemmed DEP-1 is a brain insulin receptor phosphatase that prevents the simultaneous activation of counteracting metabolic pathways
title_short DEP-1 is a brain insulin receptor phosphatase that prevents the simultaneous activation of counteracting metabolic pathways
title_sort dep 1 is a brain insulin receptor phosphatase that prevents the simultaneous activation of counteracting metabolic pathways
topic CP: Neuroscience
CP: Metabolism
url http://www.sciencedirect.com/science/article/pii/S2211124724013354
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