Defects in mitophagy promote redox‐driven metabolic syndrome in the absence of TP53INP1

Abstract The metabolic syndrome covers metabolic abnormalities including obesity and type 2 diabetes (T2D). T2D is characterized by insulin resistance resulting from both environmental and genetic factors. A genome‐wide association study (GWAS) published in 2010 identified TP53INP1 as a new T2D susc...

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Main Authors: Marion Seillier, Laurent Pouyet, Prudence N'Guessan, Marie Nollet, Florence Capo, Fabienne Guillaumond, Laure Peyta, Jean‐François Dumas, Annie Varrault, Gyslaine Bertrand, Stéphanie Bonnafous, Albert Tran, Gargi Meur, Piero Marchetti, Magalie A Ravier, Stéphane Dalle, Philippe Gual, Dany Muller, Guy A Rutter, Stéphane Servais, Juan L Iovanna, Alice Carrier
Format: Article
Language:English
Published: Springer Nature 2015-03-01
Series:EMBO Molecular Medicine
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Online Access:https://doi.org/10.15252/emmm.201404318
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author Marion Seillier
Laurent Pouyet
Prudence N'Guessan
Marie Nollet
Florence Capo
Fabienne Guillaumond
Laure Peyta
Jean‐François Dumas
Annie Varrault
Gyslaine Bertrand
Stéphanie Bonnafous
Albert Tran
Gargi Meur
Piero Marchetti
Magalie A Ravier
Stéphane Dalle
Philippe Gual
Dany Muller
Guy A Rutter
Stéphane Servais
Juan L Iovanna
Alice Carrier
author_facet Marion Seillier
Laurent Pouyet
Prudence N'Guessan
Marie Nollet
Florence Capo
Fabienne Guillaumond
Laure Peyta
Jean‐François Dumas
Annie Varrault
Gyslaine Bertrand
Stéphanie Bonnafous
Albert Tran
Gargi Meur
Piero Marchetti
Magalie A Ravier
Stéphane Dalle
Philippe Gual
Dany Muller
Guy A Rutter
Stéphane Servais
Juan L Iovanna
Alice Carrier
author_sort Marion Seillier
collection DOAJ
description Abstract The metabolic syndrome covers metabolic abnormalities including obesity and type 2 diabetes (T2D). T2D is characterized by insulin resistance resulting from both environmental and genetic factors. A genome‐wide association study (GWAS) published in 2010 identified TP53INP1 as a new T2D susceptibility locus, but a pathological mechanism was not identified. In this work, we show that mice lacking TP53INP1 are prone to redox‐driven obesity and insulin resistance. Furthermore, we demonstrate that the reactive oxygen species increase in TP53INP1‐deficient cells results from accumulation of defective mitochondria associated with impaired PINK/PARKIN mitophagy. This chronic oxidative stress also favors accumulation of lipid droplets. Taken together, our data provide evidence that the GWAS‐identified TP53INP1 gene prevents metabolic syndrome, through a mechanism involving prevention of oxidative stress by mitochondrial homeostasis regulation. In conclusion, this study highlights TP53INP1 as a molecular regulator of redox‐driven metabolic syndrome and provides a new preclinical mouse model for metabolic syndrome clinical research.
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series EMBO Molecular Medicine
spelling doaj-art-a391b04c6a3242c3a64fb5dbffab34222025-08-20T03:43:26ZengSpringer NatureEMBO Molecular Medicine1757-46761757-46842015-03-017680281810.15252/emmm.201404318Defects in mitophagy promote redox‐driven metabolic syndrome in the absence of TP53INP1Marion Seillier0Laurent Pouyet1Prudence N'Guessan2Marie Nollet3Florence Capo4Fabienne Guillaumond5Laure Peyta6Jean‐François Dumas7Annie Varrault8Gyslaine Bertrand9Stéphanie Bonnafous10Albert Tran11Gargi Meur12Piero Marchetti13Magalie A Ravier14Stéphane Dalle15Philippe Gual16Dany Muller17Guy A Rutter18Stéphane Servais19Juan L Iovanna20Alice Carrier21Inserm, U1068, CRCMInserm, U1068, CRCMInserm, U1068, CRCMInserm, U1068, CRCMInserm, U1068, CRCMInserm, U1068, CRCMInserm, U1069, Nutrition, Croissance et Cancer (N2C)Inserm, U1069, Nutrition, Croissance et Cancer (N2C)CNRS, UMR5203, Inserm, U661, Universités de Montpellier 1 & 2, IGFCNRS, UMR5203, Inserm, U661, Universités de Montpellier 1 & 2, IGFInserm, U1065, C3M, Team 8 “Hepatic Complications in Obesity”Inserm, U1065, C3M, Team 8 “Hepatic Complications in Obesity”Cell Biology, Department of Medicine, Imperial CollegeIslet Cell Laboratory, University of Pisa – Cisanello HospitalCNRS, UMR5203, Inserm, U661, Universités de Montpellier 1 & 2, IGFCNRS, UMR5203, Inserm, U661, Universités de Montpellier 1 & 2, IGFInserm, U1065, C3M, Team 8 “Hepatic Complications in Obesity”CNRS, UMR5203, Inserm, U661, Universités de Montpellier 1 & 2, IGFCell Biology, Department of Medicine, Imperial CollegeInserm, U1069, Nutrition, Croissance et Cancer (N2C)Inserm, U1068, CRCMInserm, U1068, CRCMAbstract The metabolic syndrome covers metabolic abnormalities including obesity and type 2 diabetes (T2D). T2D is characterized by insulin resistance resulting from both environmental and genetic factors. A genome‐wide association study (GWAS) published in 2010 identified TP53INP1 as a new T2D susceptibility locus, but a pathological mechanism was not identified. In this work, we show that mice lacking TP53INP1 are prone to redox‐driven obesity and insulin resistance. Furthermore, we demonstrate that the reactive oxygen species increase in TP53INP1‐deficient cells results from accumulation of defective mitochondria associated with impaired PINK/PARKIN mitophagy. This chronic oxidative stress also favors accumulation of lipid droplets. Taken together, our data provide evidence that the GWAS‐identified TP53INP1 gene prevents metabolic syndrome, through a mechanism involving prevention of oxidative stress by mitochondrial homeostasis regulation. In conclusion, this study highlights TP53INP1 as a molecular regulator of redox‐driven metabolic syndrome and provides a new preclinical mouse model for metabolic syndrome clinical research.https://doi.org/10.15252/emmm.201404318autophagydiabetesmitochondriaobesityoxidative stress
spellingShingle Marion Seillier
Laurent Pouyet
Prudence N'Guessan
Marie Nollet
Florence Capo
Fabienne Guillaumond
Laure Peyta
Jean‐François Dumas
Annie Varrault
Gyslaine Bertrand
Stéphanie Bonnafous
Albert Tran
Gargi Meur
Piero Marchetti
Magalie A Ravier
Stéphane Dalle
Philippe Gual
Dany Muller
Guy A Rutter
Stéphane Servais
Juan L Iovanna
Alice Carrier
Defects in mitophagy promote redox‐driven metabolic syndrome in the absence of TP53INP1
EMBO Molecular Medicine
autophagy
diabetes
mitochondria
obesity
oxidative stress
title Defects in mitophagy promote redox‐driven metabolic syndrome in the absence of TP53INP1
title_full Defects in mitophagy promote redox‐driven metabolic syndrome in the absence of TP53INP1
title_fullStr Defects in mitophagy promote redox‐driven metabolic syndrome in the absence of TP53INP1
title_full_unstemmed Defects in mitophagy promote redox‐driven metabolic syndrome in the absence of TP53INP1
title_short Defects in mitophagy promote redox‐driven metabolic syndrome in the absence of TP53INP1
title_sort defects in mitophagy promote redox driven metabolic syndrome in the absence of tp53inp1
topic autophagy
diabetes
mitochondria
obesity
oxidative stress
url https://doi.org/10.15252/emmm.201404318
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