H19 lncRNA Promotes Skeletal Muscle Insulin Sensitivity in Part by Targeting AMPK
Skeletal muscle plays a pivotal role in regulating systemic glucose homeostasis in part through the conserved cellular energy sensor AMPK. AMPK activation increases glucose uptake, lipid oxidation, and mitochondrial biogenesis, leading to enhanced muscle insulin sensitivity and whole-body energy met...
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| Published in | Diabetes (New York, N.Y.) Vol. 67; no. 11; pp. 2183 - 2198 |
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| Main Authors | , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
American Diabetes Association
01.11.2018
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| Abstract | Skeletal muscle plays a pivotal role in regulating systemic glucose homeostasis in part through the conserved cellular energy sensor AMPK. AMPK activation increases glucose uptake, lipid oxidation, and mitochondrial biogenesis, leading to enhanced muscle insulin sensitivity and whole-body energy metabolism. Here we show that the muscle-enriched H19 long noncoding RNA (lncRNA) acts to enhance muscle insulin sensitivity, at least in part, by activating AMPK. We identify the atypical dual-specificity phosphatase DUSP27/DUPD1 as a potentially important downstream effector of H19. We show that DUSP27, which is highly expressed in muscle with previously unknown physiological function, interacts with and activates AMPK in muscle cells. Consistent with decreased H19 expression in the muscle of insulin-resistant human subjects and rodents, mice with genetic H19 ablation exhibit muscle insulin resistance. Furthermore, a high-fat diet downregulates muscle H19 via both posttranscriptional and epigenetic mechanisms. Our results uncover an evolutionarily conserved, highly expressed lncRNA as an important regulator of muscle insulin sensitivity. |
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| AbstractList | Skeletal muscle plays a pivotal role in regulating systemic glucose homeostasis in part through the conserved cellular energy sensor AMPK. AMPK activation increases glucose uptake, lipid oxidation, and mitochondrial biogenesis, leading to enhanced muscle insulin sensitivity and whole-body energy metabolism. Here we show that the muscle-enriched H19 long noncoding RNA (lncRNA) acts to enhance muscle insulin sensitivity, at least in part, by activating AMPK. We identify the atypical dual-specificity phosphatase DUSP27/DUPD1 as a potentially important downstream effector of H19. We show that DUSP27, which is highly expressed in muscle with previously unknown physiological function, interacts with and activates AMPK in muscle cells. Consistent with decreased H19 expression in the muscle of insulin-resistant human subjects and rodents, mice with genetic H19 ablation exhibit muscle insulin resistance. Furthermore, a high-fat diet downregulates muscle H19 via both posttranscriptional and epigenetic mechanisms. Our results uncover an evolutionarily conserved, highly expressed lncRNA as an important regulator of muscle insulin sensitivity. Skeletal muscle plays a pivotal role in regulating systemic glucose homeostasis in part through the conserved cellular energy sensor AMPK. AMPK activation increases glucose uptake, lipid oxidation, and mitochondrial biogenesis, leading to enhanced muscle insulin sensitivity and whole-body energy metabolism. Here we show that the muscle-enriched H19 long noncoding RNA (lncRNA) acts to enhance muscle insulin sensitivity, at least in part, by activating AMPK. We identify the atypical dual-specificity phosphatase DUSP27/DUPD1 as a potentially important downstream effector of H19. We show that DUSP27, which is highly expressed in muscle with previously unknown physiological function, interacts with and activates AMPK in muscle cells. Consistent with decreased H19 expression in the muscle of insulin-resistant human subjects and rodents, mice with genetic H19 ablation exhibit muscle insulin resistance. Furthermore, a high-fat diet downregulates muscle H19 via both posttranscriptional and epigenetic mechanisms. Our results uncover an evolutionarily conserved, highly expressed lncRNA as an important regulator of muscle insulin sensitivity.Skeletal muscle plays a pivotal role in regulating systemic glucose homeostasis in part through the conserved cellular energy sensor AMPK. AMPK activation increases glucose uptake, lipid oxidation, and mitochondrial biogenesis, leading to enhanced muscle insulin sensitivity and whole-body energy metabolism. Here we show that the muscle-enriched H19 long noncoding RNA (lncRNA) acts to enhance muscle insulin sensitivity, at least in part, by activating AMPK. We identify the atypical dual-specificity phosphatase DUSP27/DUPD1 as a potentially important downstream effector of H19. We show that DUSP27, which is highly expressed in muscle with previously unknown physiological function, interacts with and activates AMPK in muscle cells. Consistent with decreased H19 expression in the muscle of insulin-resistant human subjects and rodents, mice with genetic H19 ablation exhibit muscle insulin resistance. Furthermore, a high-fat diet downregulates muscle H19 via both posttranscriptional and epigenetic mechanisms. Our results uncover an evolutionarily conserved, highly expressed lncRNA as an important regulator of muscle insulin sensitivity. |
| Author | Li, Da Huang, Yingqun Geng, Tingting Jiang, Ying Xu, Yetao Taylor, Hugh S. Carmichael, Gordon G. Zhang, Na Wang, Zhangsheng Liu, Ya |
| Author_xml | – sequence: 1 givenname: Tingting surname: Geng fullname: Geng, Tingting organization: Department of Obstetrics, Gynecology, and Reproductive Sciences, Yale School of Medicine, New Haven, CT, Department of Endocrinology, First Affiliated Hospital of Xi’an Jiaotong University School of Medicine, Xi’an, Shaanxi, People’s Republic of China – sequence: 2 givenname: Ya surname: Liu fullname: Liu, Ya organization: Department of Obstetrics, Gynecology, and Reproductive Sciences, Yale School of Medicine, New Haven, CT, Department of Veterinary Medicine, College of Animal Science and Technology, Anhui Agricultural University, Hefei, Anhui, People’s Republic of China – sequence: 3 givenname: Yetao surname: Xu fullname: Xu, Yetao organization: Department of Obstetrics, Gynecology, and Reproductive Sciences, Yale School of Medicine, New Haven, CT, Department of Obstetrics and Gynecology, First Affiliated Hospital of Nanjing Medical University, Nanjing, Jiangsu, People’s Republic of China – sequence: 4 givenname: Ying surname: Jiang fullname: Jiang, Ying organization: Department of Obstetrics, Women’s Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, People’s Republic of China – sequence: 5 givenname: Na surname: Zhang fullname: Zhang, Na organization: Department of Genetics and Genome Sciences, University of Connecticut Health Center, Farmington, CT – sequence: 6 givenname: Zhangsheng surname: Wang fullname: Wang, Zhangsheng organization: Department of Obstetrics, Gynecology, and Reproductive Sciences, Yale School of Medicine, New Haven, CT, Department of Cardiology, Fifth People’s Hospital of Shanghai, Fudan University, Shanghai, People’s Republic of China – sequence: 7 givenname: Gordon G. surname: Carmichael fullname: Carmichael, Gordon G. organization: Department of Genetics and Genome Sciences, University of Connecticut Health Center, Farmington, CT – sequence: 8 givenname: Hugh S. surname: Taylor fullname: Taylor, Hugh S. organization: Department of Obstetrics, Gynecology, and Reproductive Sciences, Yale School of Medicine, New Haven, CT – sequence: 9 givenname: Da surname: Li fullname: Li, Da organization: Department of Obstetrics, Gynecology, and Reproductive Sciences, Yale School of Medicine, New Haven, CT, Center of Reproductive Medicine, Department of Obstetrics and Gynecology, Shengjing Hospital, China Medical University, Shenyang, Liaoning, People’s Republic of China – sequence: 10 givenname: Yingqun orcidid: 0000-0002-0663-8465 surname: Huang fullname: Huang, Yingqun organization: Department of Obstetrics, Gynecology, and Reproductive Sciences, Yale School of Medicine, New Haven, CT |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30201684$$D View this record in MEDLINE/PubMed |
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| Copyright | 2018 by the American Diabetes Association. Copyright American Diabetes Association Nov 1, 2018 2018 by the American Diabetes Association. 2018 |
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| SubjectTerms | Ablation Adenylate Kinase - metabolism Animals Body Composition - physiology Down-Regulation Energy metabolism Epigenetics Glucose Glucose Clamp Technique High fat diet Homeostasis Humans Insulin Insulin resistance Insulin Resistance - physiology Lipid peroxidation Metabolism Mice Mice, Knockout Mitochondria Muscle Fibers, Skeletal - metabolism Muscle, Skeletal - metabolism Oxidation Phosphoprotein Phosphatases - genetics Phosphoprotein Phosphatases - metabolism Post-transcription Ribonucleic acid RNA RNA, Long Noncoding - genetics RNA, Long Noncoding - metabolism Skeletal muscle Skeletal system |
| Title | H19 lncRNA Promotes Skeletal Muscle Insulin Sensitivity in Part by Targeting AMPK |
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