SIRT5 inhibits peroxisomal ACOX1 to prevent oxidative damage and is downregulated in liver cancer

Peroxisomes account for ~35% of total H 2 O 2 generation in mammalian tissues. Peroxisomal ACOX1 (acyl‐CoA oxidase 1) is the first and rate‐limiting enzyme in fatty acid β‐oxidation and a major producer of H 2 O 2 . ACOX1 dysfunction is linked to peroxisomal disorders and hepatocarcinogenesis. Here,...

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Veröffentlicht in:	EMBO reports Jg. 19; H. 5
Hauptverfasser:	Chen, Xiu‐Fei, Tian, Meng‐Xin, Sun, Ren‐Qiang, Zhang, Meng‐Li, Zhou, Li‐Sha, Jin, Lei, Chen, Lei‐Lei, Zhou, Wen‐Jie, Duan, Kun‐Long, Chen, Yu‐Jia, Gao, Chao, Cheng, Zhou‐Li, Wang, Fang, Zhang, Jin‐Ye, Sun, Yi‐Ping, Yu, Hong‐Xiu, Zhao, Yu‐Zheng, Yang, Yi, Liu, Wei‐Ren, Shi, Ying‐Hong, Xiong, Yue, Guan, Kun‐Liang, Ye, Dan
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	London Nature Publishing Group UK 01.05.2018 Springer Nature B.V John Wiley and Sons Inc
Schlagworte:	ACOX1 Acyl-CoA Oxidase - antagonists & inhibitors Acyl-CoA Oxidase - genetics Acyl-CoA Oxidase - metabolism Animals Carcinoma, Hepatocellular - metabolism Clonal deletion Damage prevention Deoxyribonucleic acid Dimers DNA DNA Damage Down-Regulation EMBO03 EMBO29 EMBO31 Female Gene Knockdown Techniques HEK293 Cells HeLa Cells Hep G2 Cells Hepatocellular carcinoma Homeostasis Humans Hydrogen Peroxide Liver Liver cancer Liver Neoplasms - metabolism Male Metabolism Mice Mice, Knockout Middle Aged Oxidation Oxidation-Reduction Oxidative Stress Peroxisomes Peroxisomes - chemistry Prognosis Reactive oxygen species SIRT5 Sirtuins - genetics Sirtuins - metabolism succinylation SIRT5 liver cancer succinylation ACOX1 oxidative stress
ISSN:	1469-221X, 1469-3178, 1469-3178
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Abstract	Peroxisomes account for ~35% of total H 2 O 2 generation in mammalian tissues. Peroxisomal ACOX1 (acyl‐CoA oxidase 1) is the first and rate‐limiting enzyme in fatty acid β‐oxidation and a major producer of H 2 O 2 . ACOX1 dysfunction is linked to peroxisomal disorders and hepatocarcinogenesis. Here, we show that the deacetylase sirtuin 5 (SIRT5) is present in peroxisomes and that ACOX1 is a physiological substrate of SIRT5. Mechanistically, SIRT5‐mediated desuccinylation inhibits ACOX1 activity by suppressing its active dimer formation in both cultured cells and mouse livers. Deletion of SIRT5 increases H 2 O 2 production and oxidative DNA damage, which can be alleviated by ACOX1 knockdown. We show that SIRT5 downregulation is associated with increased succinylation and activity of ACOX1 and oxidative DNA damage response in hepatocellular carcinoma (HCC). Our study reveals a novel role of SIRT5 in inhibiting peroxisome‐induced oxidative stress, in liver protection, and in suppressing HCC development. Synopsis This study reveals a role for SIRT5 in regulating peroxisomal H 2 O 2 and ROS homeostasis and indicates its potential function in liver protection and hepatocellular carcinoma suppression. SIRT5 is localized in peroxisomes where it controls H 2 O 2 metabolism. SIRT5‐mediated desuccinylation inhibits ACOX1 activity by suppressing its active dimer formation. SIRT5 downregulation increases ACOX1 activity and oxidative DNA damage response in HCC. Graphical Abstract This study reveals a role for SIRT5 in regulating peroxisomal H 2 O 2 and ROS homeostasis and indicates its potential function in liver protection and hepatocellular carcinoma suppression.
AbstractList	Peroxisomes account for ~35% of total H2O2 generation in mammalian tissues. Peroxisomal ACOX1 (acyl‐CoA oxidase 1) is the first and rate‐limiting enzyme in fatty acid β‐oxidation and a major producer of H2O2. ACOX1 dysfunction is linked to peroxisomal disorders and hepatocarcinogenesis. Here, we show that the deacetylase sirtuin 5 (SIRT5) is present in peroxisomes and that ACOX1 is a physiological substrate of SIRT5. Mechanistically, SIRT5‐mediated desuccinylation inhibits ACOX1 activity by suppressing its active dimer formation in both cultured cells and mouse livers. Deletion of SIRT5 increases H2O2 production and oxidative DNA damage, which can be alleviated by ACOX1 knockdown. We show that SIRT5 downregulation is associated with increased succinylation and activity of ACOX1 and oxidative DNA damage response in hepatocellular carcinoma (HCC). Our study reveals a novel role of SIRT5 in inhibiting peroxisome‐induced oxidative stress, in liver protection, and in suppressing HCC development. Peroxisomes account for ~35% of total H 2 O 2 generation in mammalian tissues. Peroxisomal ACOX1 (acyl‐CoA oxidase 1) is the first and rate‐limiting enzyme in fatty acid β‐oxidation and a major producer of H 2 O 2 . ACOX1 dysfunction is linked to peroxisomal disorders and hepatocarcinogenesis. Here, we show that the deacetylase sirtuin 5 (SIRT5) is present in peroxisomes and that ACOX1 is a physiological substrate of SIRT5. Mechanistically, SIRT5‐mediated desuccinylation inhibits ACOX1 activity by suppressing its active dimer formation in both cultured cells and mouse livers. Deletion of SIRT5 increases H 2 O 2 production and oxidative DNA damage, which can be alleviated by ACOX1 knockdown. We show that SIRT5 downregulation is associated with increased succinylation and activity of ACOX1 and oxidative DNA damage response in hepatocellular carcinoma (HCC). Our study reveals a novel role of SIRT5 in inhibiting peroxisome‐induced oxidative stress, in liver protection, and in suppressing HCC development. Synopsis This study reveals a role for SIRT5 in regulating peroxisomal H 2 O 2 and ROS homeostasis and indicates its potential function in liver protection and hepatocellular carcinoma suppression. SIRT5 is localized in peroxisomes where it controls H 2 O 2 metabolism. SIRT5‐mediated desuccinylation inhibits ACOX1 activity by suppressing its active dimer formation. SIRT5 downregulation increases ACOX1 activity and oxidative DNA damage response in HCC. Graphical Abstract This study reveals a role for SIRT5 in regulating peroxisomal H 2 O 2 and ROS homeostasis and indicates its potential function in liver protection and hepatocellular carcinoma suppression. Peroxisomes account for ~35% of total H2O2 generation in mammalian tissues. Peroxisomal ACOX1 (acyl-CoA oxidase 1) is the first and rate-limiting enzyme in fatty acid β-oxidation and a major producer of H2O2 ACOX1 dysfunction is linked to peroxisomal disorders and hepatocarcinogenesis. Here, we show that the deacetylase sirtuin 5 (SIRT5) is present in peroxisomes and that ACOX1 is a physiological substrate of SIRT5. Mechanistically, SIRT5-mediated desuccinylation inhibits ACOX1 activity by suppressing its active dimer formation in both cultured cells and mouse livers. Deletion of SIRT5 increases H2O2 production and oxidative DNA damage, which can be alleviated by ACOX1 knockdown. We show that SIRT5 downregulation is associated with increased succinylation and activity of ACOX1 and oxidative DNA damage response in hepatocellular carcinoma (HCC). Our study reveals a novel role of SIRT5 in inhibiting peroxisome-induced oxidative stress, in liver protection, and in suppressing HCC development.Peroxisomes account for ~35% of total H2O2 generation in mammalian tissues. Peroxisomal ACOX1 (acyl-CoA oxidase 1) is the first and rate-limiting enzyme in fatty acid β-oxidation and a major producer of H2O2 ACOX1 dysfunction is linked to peroxisomal disorders and hepatocarcinogenesis. Here, we show that the deacetylase sirtuin 5 (SIRT5) is present in peroxisomes and that ACOX1 is a physiological substrate of SIRT5. Mechanistically, SIRT5-mediated desuccinylation inhibits ACOX1 activity by suppressing its active dimer formation in both cultured cells and mouse livers. Deletion of SIRT5 increases H2O2 production and oxidative DNA damage, which can be alleviated by ACOX1 knockdown. We show that SIRT5 downregulation is associated with increased succinylation and activity of ACOX1 and oxidative DNA damage response in hepatocellular carcinoma (HCC). Our study reveals a novel role of SIRT5 in inhibiting peroxisome-induced oxidative stress, in liver protection, and in suppressing HCC development. Peroxisomes account for ~35% of total H2O2 generation in mammalian tissues. Peroxisomal ACOX1 (acyl‐CoA oxidase 1) is the first and rate‐limiting enzyme in fatty acid β‐oxidation and a major producer of H2O2. ACOX1 dysfunction is linked to peroxisomal disorders and hepatocarcinogenesis. Here, we show that the deacetylase sirtuin 5 (SIRT5) is present in peroxisomes and that ACOX1 is a physiological substrate of SIRT5. Mechanistically, SIRT5‐mediated desuccinylation inhibits ACOX1 activity by suppressing its active dimer formation in both cultured cells and mouse livers. Deletion of SIRT5 increases H2O2 production and oxidative DNA damage, which can be alleviated by ACOX1 knockdown. We show that SIRT5 downregulation is associated with increased succinylation and activity of ACOX1 and oxidative DNA damage response in hepatocellular carcinoma (HCC). Our study reveals a novel role of SIRT5 in inhibiting peroxisome‐induced oxidative stress, in liver protection, and in suppressing HCC development. Synopsis This study reveals a role for SIRT5 in regulating peroxisomal H2O2 and ROS homeostasis and indicates its potential function in liver protection and hepatocellular carcinoma suppression. SIRT5 is localized in peroxisomes where it controls H2O2 metabolism. SIRT5‐mediated desuccinylation inhibits ACOX1 activity by suppressing its active dimer formation. SIRT5 downregulation increases ACOX1 activity and oxidative DNA damage response in HCC. This study reveals a role for SIRT5 in regulating peroxisomal H2O2 and ROS homeostasis and indicates its potential function in liver protection and hepatocellular carcinoma suppression. Peroxisomes account for ~35% of total H O generation in mammalian tissues. Peroxisomal ACOX1 (acyl-CoA oxidase 1) is the first and rate-limiting enzyme in fatty acid β-oxidation and a major producer of H O ACOX1 dysfunction is linked to peroxisomal disorders and hepatocarcinogenesis. Here, we show that the deacetylase sirtuin 5 (SIRT5) is present in peroxisomes and that ACOX1 is a physiological substrate of SIRT5. Mechanistically, SIRT5-mediated desuccinylation inhibits ACOX1 activity by suppressing its active dimer formation in both cultured cells and mouse livers. Deletion of SIRT5 increases H O production and oxidative DNA damage, which can be alleviated by knockdown. We show that SIRT5 downregulation is associated with increased succinylation and activity of ACOX1 and oxidative DNA damage response in hepatocellular carcinoma (HCC). Our study reveals a novel role of SIRT5 in inhibiting peroxisome-induced oxidative stress, in liver protection, and in suppressing HCC development.
Author	Chen, Xiu‐Fei Xiong, Yue Zhou, Li‐Sha Zhang, Jin‐Ye Gao, Chao Cheng, Zhou‐Li Wang, Fang Liu, Wei‐Ren Zhao, Yu‐Zheng Ye, Dan Duan, Kun‐Long Zhou, Wen‐Jie Sun, Yi‐Ping Yu, Hong‐Xiu Guan, Kun‐Liang Zhang, Meng‐Li Chen, Yu‐Jia Chen, Lei‐Lei Shi, Ying‐Hong Sun, Ren‐Qiang Jin, Lei Tian, Meng‐Xin Yang, Yi
AuthorAffiliation	2 Key Laboratory of Metabolism and Molecular Medicine, Ministry of Education Department of Biochemistry and Molecular Biology School of Basic Medical Sciences Fudan University Shanghai China 7 Lineberger Comprehensive Cancer Center Department of Biochemistry and Biophysics University of North Carolina at Chapel Hill Chapel Hill NC USA 3 State Key Laboratory of Genetic Engineering Collaborative Innovation Center of Genetics and Development School of Life Sciences Fudan University Shanghai China 8 Department of Pharmacology and Moores Cancer Center University of California San Diego La Jolla CA USA 6 School of Pharmacy East China University of Science and Technology Shanghai China 4 Department of Liver Surgery Liver Cancer Institute Zhongshan Hospital Fudan University Shanghai China 5 Key Laboratory of Carcinogenesis and Cancer Invasion of Ministry of Education Shanghai China 1 Molecular and Cell Biology Lab Institute of Biomedical Sciences Shanghai Medical College Shanghai China 9 Department of
AuthorAffiliation_xml	– name: 7 Lineberger Comprehensive Cancer Center Department of Biochemistry and Biophysics University of North Carolina at Chapel Hill Chapel Hill NC USA – name: 8 Department of Pharmacology and Moores Cancer Center University of California San Diego La Jolla CA USA – name: 2 Key Laboratory of Metabolism and Molecular Medicine, Ministry of Education Department of Biochemistry and Molecular Biology School of Basic Medical Sciences Fudan University Shanghai China – name: 1 Molecular and Cell Biology Lab Institute of Biomedical Sciences Shanghai Medical College Shanghai China – name: 9 Department of General Surgery Huashan Hospital Fudan University Shanghai China – name: 6 School of Pharmacy East China University of Science and Technology Shanghai China – name: 4 Department of Liver Surgery Liver Cancer Institute Zhongshan Hospital Fudan University Shanghai China – name: 3 State Key Laboratory of Genetic Engineering Collaborative Innovation Center of Genetics and Development School of Life Sciences Fudan University Shanghai China – name: 5 Key Laboratory of Carcinogenesis and Cancer Invasion of Ministry of Education Shanghai China
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Department of Biochemistry and Molecular Biology, School of Basic Medical Sciences, Fudan University, State Key Laboratory of Genetic Engineering, Collaborative Innovation Center of Genetics and Development, School of Life Sciences, Fudan University, Department of General Surgery, Huashan Hospital, Fudan University
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Snippet	Peroxisomes account for ~35% of total H 2 O 2 generation in mammalian tissues. Peroxisomal ACOX1 (acyl‐CoA oxidase 1) is the first and rate‐limiting enzyme in... Peroxisomes account for ~35% of total H2O2 generation in mammalian tissues. Peroxisomal ACOX1 (acyl‐CoA oxidase 1) is the first and rate‐limiting enzyme in... Peroxisomes account for ~35% of total H O generation in mammalian tissues. Peroxisomal ACOX1 (acyl-CoA oxidase 1) is the first and rate-limiting enzyme in... Peroxisomes account for ~35% of total H2O2 generation in mammalian tissues. Peroxisomal ACOX1 (acyl-CoA oxidase 1) is the first and rate-limiting enzyme in...
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SubjectTerms	ACOX1 Acyl-CoA Oxidase - antagonists & inhibitors Acyl-CoA Oxidase - genetics Acyl-CoA Oxidase - metabolism Animals Carcinoma, Hepatocellular - metabolism Clonal deletion Damage prevention Deoxyribonucleic acid Dimers DNA DNA Damage Down-Regulation EMBO03 EMBO29 EMBO31 Female Gene Knockdown Techniques HEK293 Cells HeLa Cells Hep G2 Cells Hepatocellular carcinoma Homeostasis Humans Hydrogen Peroxide Liver Liver cancer Liver Neoplasms - metabolism Male Metabolism Mice Mice, Knockout Middle Aged Oxidation Oxidation-Reduction Oxidative Stress Peroxisomes Peroxisomes - chemistry Prognosis Reactive oxygen species SIRT5 Sirtuins - genetics Sirtuins - metabolism succinylation
Title	SIRT5 inhibits peroxisomal ACOX1 to prevent oxidative damage and is downregulated in liver cancer
URI	https://link.springer.com/article/10.15252/embr.201745124 https://onlinelibrary.wiley.com/doi/abs/10.15252%2Fembr.201745124 https://www.ncbi.nlm.nih.gov/pubmed/29491006 https://www.proquest.com/docview/2034202054 https://www.proquest.com/docview/2009568062 https://pubmed.ncbi.nlm.nih.gov/PMC5934778
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