Targeting a ceramide double bond improves insulin resistance and hepatic steatosis
Ceramides contribute to the lipotoxicity that underlies diabetes, hepatic steatosis, and heart disease. By genetically engineering mice, we deleted the enzyme dihydroceramide desaturase 1 (DES1), which normally inserts a conserved double bond into the backbone of ceramides and other predominant sphi...
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| Published in | Science (American Association for the Advancement of Science) Vol. 365; no. 6451; pp. 386 - 392 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
American Association for the Advancement of Science
26.07.2019
The American Association for the Advancement of Science |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Ceramides contribute to the lipotoxicity that underlies diabetes, hepatic steatosis, and heart disease. By genetically engineering mice, we deleted the enzyme dihydroceramide desaturase 1 (DES1), which normally inserts a conserved double bond into the backbone of ceramides and other predominant sphingolipids. Ablation of DES1 from whole animals or tissue-specific deletion in the liver and/or adipose tissue resolved hepatic steatosis and insulin resistance in mice caused by leptin deficiency or obesogenic diets. Mechanistic studies revealed ceramide actions that promoted lipid uptake and storage and impaired glucose utilization, none of which could be recapitulated by (dihydro)ceramides that lacked the critical double bond. These studies suggest that inhibition of DES1 may provide a means of treating hepatic steatosis and metabolic disorders. |
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| AbstractList | Ceramides contribute to the lipotoxicity that underlies diabetes, hepatic steatosis, and heart disease. By genetically engineering mice, we deleted the enzyme dihydroceramide desaturase 1 (DES1), which normally inserts a conserved double bond into the backbone of ceramides and other predominant sphingolipids. Ablation of DES1 from whole animals or tissue-specific deletion in the liver and/or adipose tissue resolved hepatic steatosis and insulin resistance in mice caused by leptin deficiency or obesogenic diets. Mechanistic studies revealed ceramide actions that promoted lipid uptake and storage and impaired glucose utilization, none of which could be recapitulated by (dihydro)ceramides that lacked the critical double bond. These studies suggest that inhibition of DES1 may provide a means of treating hepatic steatosis and metabolic disorders. Excess calorie intake can ultimately lead to a metabolic syndrome that interferes with fat or lipid metabolism. There are many different types of lipids, and it has been widely debated which are the true culprits underlying metabolic disorders. Chaurasia et al. report that ceramides are the major contributor to insulin resistance and fatty liver disease (see the Perspective by Kusminski and Scherer). This appears to be caused by the enzyme dihydroceramide desaturase 1 (DES1), which is normally involved in ceramide production by inserting a double bond into the backbone of the molecule. In mice fed a high-fat diet, deletion of DES1 improved glucose and lipid metabolism. Science , this issue p. 386 ; see also p. 319 Deletion of dihydroceramide desaturase 1 (DES1) resolves insulin resistance and fatty liver in mice. Ceramides contribute to the lipotoxicity that underlies diabetes, hepatic steatosis, and heart disease. By genetically engineering mice, we deleted the enzyme dihydroceramide desaturase 1 (DES1), which normally inserts a conserved double bond into the backbone of ceramides and other predominant sphingolipids. Ablation of DES1 from whole animals or tissue-specific deletion in the liver and/or adipose tissue resolved hepatic steatosis and insulin resistance in mice caused by leptin deficiency or obesogenic diets. Mechanistic studies revealed ceramide actions that promoted lipid uptake and storage and impaired glucose utilization, none of which could be recapitulated by (dihydro)ceramides that lacked the critical double bond. These studies suggest that inhibition of DES1 may provide a means of treating hepatic steatosis and metabolic disorders. Ceramides contribute to the lipotoxicity that underlies diabetes, hepatic steatosis, and heart disease. By genetically engineering mice, we deleted the enzyme dihydroceramide desaturase 1 (DES1), which normally inserts a conserved double bond into the backbone of ceramides and other predominant sphingolipids. Ablation of DES1 from whole animals or tissue-specific deletion in the liver and/or adipose tissue resolved hepatic steatosis and insulin resistance in mice caused by leptin deficiency or obesogenic diets. Mechanistic studies revealed ceramide actions that promoted lipid uptake and storage and impaired glucose utilization, none of which could be recapitulated by (dihydro)ceramides that lacked the critical double bond. These studies suggest that inhibition of DES1 may provide a means of treating hepatic steatosis and metabolic disorders.Ceramides contribute to the lipotoxicity that underlies diabetes, hepatic steatosis, and heart disease. By genetically engineering mice, we deleted the enzyme dihydroceramide desaturase 1 (DES1), which normally inserts a conserved double bond into the backbone of ceramides and other predominant sphingolipids. Ablation of DES1 from whole animals or tissue-specific deletion in the liver and/or adipose tissue resolved hepatic steatosis and insulin resistance in mice caused by leptin deficiency or obesogenic diets. Mechanistic studies revealed ceramide actions that promoted lipid uptake and storage and impaired glucose utilization, none of which could be recapitulated by (dihydro)ceramides that lacked the critical double bond. These studies suggest that inhibition of DES1 may provide a means of treating hepatic steatosis and metabolic disorders. Ceramides in focusExcess calorie intake can ultimately lead to a metabolic syndrome that interferes with fat or lipid metabolism. There are many different types of lipids, and it has been widely debated which are the true culprits underlying metabolic disorders. Chaurasia et al. report that ceramides are the major contributor to insulin resistance and fatty liver disease (see the Perspective by Kusminski and Scherer). This appears to be caused by the enzyme dihydroceramide desaturase 1 (DES1), which is normally involved in ceramide production by inserting a double bond into the backbone of the molecule. In mice fed a high-fat diet, deletion of DES1 improved glucose and lipid metabolism.Science, this issue p. 386; see also p. 319Ceramides contribute to the lipotoxicity that underlies diabetes, hepatic steatosis, and heart disease. By genetically engineering mice, we deleted the enzyme dihydroceramide desaturase 1 (DES1), which normally inserts a conserved double bond into the backbone of ceramides and other predominant sphingolipids. Ablation of DES1 from whole animals or tissue-specific deletion in the liver and/or adipose tissue resolved hepatic steatosis and insulin resistance in mice caused by leptin deficiency or obesogenic diets. Mechanistic studies revealed ceramide actions that promoted lipid uptake and storage and impaired glucose utilization, none of which could be recapitulated by (dihydro)ceramides that lacked the critical double bond. These studies suggest that inhibition of DES1 may provide a means of treating hepatic steatosis and metabolic disorders. |
| Author | Howard, Andrew D. Sumida, Doris Hissako Kaddai, Vincent Tippetts, Trevor S. Chen, Ying Maschek, J. Alan Previs, Stephen F. Wu, Margaret Chaurasia, Bhagirath Qian, Ying Rutter, Jared Pearson, Mackenzie Erion, Mark D. Satapati, Santhosh Zhou, Heather McLaren, David G. Shen, Xiaolan Nunes, Christian N. Summers, Scott A. Monibas, Rafael Mayoral Sweeney, C. Rufus Poss, Annelise Liu, Jinqi Petrov, Aleksandr Lancaster, Graeme Iain Yao, Jun Wang, Liping Pereira, Renato Felipe Wang, Liangsu Kelley, David E. Cox, James E. Li, Ying Wilkerson, Joseph L. Holland, William L. Siddique, Monowarul Mobin |
| AuthorAffiliation | 3 School of Dentistry, São Paulo State University (UNESP), Araçatuba 16015, Brazil 6 Faculty of Science, University of Brunei Darussalam, Gadong 1410, Brunei Darussalam 2 Merck Research Laboratories, Merck, Kenilworth, NJ 07033, USA 5 Baker IDI Heart and Diabetes Institute, Melbourne, Victoria 3004, Australia 4 Department of Biochemistry and the Diabetes and Metabolism Research Center, University of Utah, Salt Lake City, UT 84112, USA 8 Howard Hughes Medical Institute, Salt Lake City, UT 84112, USA 1 Department of Nutrition and Integrative Physiology and the Diabetes and Metabolism Research Center, University of Utah, Salt Lake City, UT 84112, USA 7 Sciex, Framingham, MA 01701, USA |
| AuthorAffiliation_xml | – name: 8 Howard Hughes Medical Institute, Salt Lake City, UT 84112, USA – name: 4 Department of Biochemistry and the Diabetes and Metabolism Research Center, University of Utah, Salt Lake City, UT 84112, USA – name: 5 Baker IDI Heart and Diabetes Institute, Melbourne, Victoria 3004, Australia – name: 1 Department of Nutrition and Integrative Physiology and the Diabetes and Metabolism Research Center, University of Utah, Salt Lake City, UT 84112, USA – name: 6 Faculty of Science, University of Brunei Darussalam, Gadong 1410, Brunei Darussalam – name: 2 Merck Research Laboratories, Merck, Kenilworth, NJ 07033, USA – name: 3 School of Dentistry, São Paulo State University (UNESP), Araçatuba 16015, Brazil – name: 7 Sciex, Framingham, MA 01701, USA |
| Author_xml | – sequence: 1 givenname: Bhagirath surname: Chaurasia fullname: Chaurasia, Bhagirath – sequence: 2 givenname: Trevor S. surname: Tippetts fullname: Tippetts, Trevor S. – sequence: 3 givenname: Rafael Mayoral surname: Monibas fullname: Monibas, Rafael Mayoral – sequence: 4 givenname: Jinqi surname: Liu fullname: Liu, Jinqi – sequence: 5 givenname: Ying surname: Li fullname: Li, Ying – sequence: 6 givenname: Liping surname: Wang fullname: Wang, Liping – sequence: 7 givenname: Joseph L. surname: Wilkerson fullname: Wilkerson, Joseph L. – sequence: 8 givenname: C. Rufus surname: Sweeney fullname: Sweeney, C. Rufus – sequence: 9 givenname: Renato Felipe surname: Pereira fullname: Pereira, Renato Felipe – sequence: 10 givenname: Doris Hissako surname: Sumida fullname: Sumida, Doris Hissako – sequence: 11 givenname: J. Alan surname: Maschek fullname: Maschek, J. Alan – sequence: 12 givenname: James E. surname: Cox fullname: Cox, James E. – sequence: 13 givenname: Vincent surname: Kaddai fullname: Kaddai, Vincent – sequence: 14 givenname: Graeme Iain surname: Lancaster fullname: Lancaster, Graeme Iain – sequence: 15 givenname: Monowarul Mobin surname: Siddique fullname: Siddique, Monowarul Mobin – sequence: 16 givenname: Annelise surname: Poss fullname: Poss, Annelise – sequence: 17 givenname: Mackenzie surname: Pearson fullname: Pearson, Mackenzie – sequence: 18 givenname: Santhosh surname: Satapati fullname: Satapati, Santhosh – sequence: 19 givenname: Heather surname: Zhou fullname: Zhou, Heather – sequence: 20 givenname: David G. surname: McLaren fullname: McLaren, David G. – sequence: 21 givenname: Stephen F. surname: Previs fullname: Previs, Stephen F. – sequence: 22 givenname: Ying surname: Chen fullname: Chen, Ying – sequence: 23 givenname: Ying surname: Qian fullname: Qian, Ying – sequence: 24 givenname: Aleksandr surname: Petrov fullname: Petrov, Aleksandr – sequence: 25 givenname: Margaret surname: Wu fullname: Wu, Margaret – sequence: 26 givenname: Xiaolan surname: Shen fullname: Shen, Xiaolan – sequence: 27 givenname: Jun surname: Yao fullname: Yao, Jun – sequence: 28 givenname: Christian N. surname: Nunes fullname: Nunes, Christian N. – sequence: 29 givenname: Andrew D. surname: Howard fullname: Howard, Andrew D. – sequence: 30 givenname: Liangsu surname: Wang fullname: Wang, Liangsu – sequence: 31 givenname: Mark D. surname: Erion fullname: Erion, Mark D. – sequence: 32 givenname: Jared surname: Rutter fullname: Rutter, Jared – sequence: 33 givenname: William L. surname: Holland fullname: Holland, William L. – sequence: 34 givenname: David E. surname: Kelley fullname: Kelley, David E. – sequence: 35 givenname: Scott A. surname: Summers fullname: Summers, Scott A. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31273070$$D View this record in MEDLINE/PubMed |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Present address: Morphic Therapeutic, Waltham, MA 02451, USA. These authors contributed equally to this work. Present address: Bristol Myers Squibb, Princeton, NJ 08648, USA. Author contributions: S.A.S., J.L., D.E.K., and B.C. conceived of the project, designed the experiments, and wrote the manuscript. B.C., T.S.T., R.M.M., J.L., Y.L., L.W., J.L.W., A.Po., C.R.S., R.F.P., V.K., G.I.L., M.M.S., S.S., H.Z., D.G.M., S.F.P., Y.C., Y.Q., A.Pe., M.W., X.S., J.Y., C.N.N., A.D.H.,L.W., M.D.E., D.H.S., J.R., and W.L.H. performed experiments and analyzed data. J.A.M., J.E.C., M.P. aided in lipid quantification. Present address: Johnson and Johnson, Spring House, PA 19477, USA. |
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| Snippet | Ceramides contribute to the lipotoxicity that underlies diabetes, hepatic steatosis, and heart disease. By genetically engineering mice, we deleted the enzyme... Excess calorie intake can ultimately lead to a metabolic syndrome that interferes with fat or lipid metabolism. There are many different types of lipids, and... Ceramides in focusExcess calorie intake can ultimately lead to a metabolic syndrome that interferes with fat or lipid metabolism. There are many different... |
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| SubjectTerms | Ablation Adipose tissue Animals Backbone Cardiovascular diseases Ceramide Ceramides - chemistry Ceramides - genetics Ceramides - metabolism Coronary artery disease Desaturase Diabetes mellitus Diet Diet, High-Fat - adverse effects Disease resistance Disorders Enzymes Fat metabolism Fatty liver Fatty Liver - genetics Fatty Liver - metabolism Gene Deletion Genetic engineering Glucose Glucose metabolism Heart diseases High fat diet Inserts Insulin Insulin resistance Insulin Resistance - genetics Leptin Leptin - deficiency Lipid metabolism Lipids Liver Liver diseases Membrane Proteins - genetics Metabolic disorders Metabolic syndrome Metabolism Mice Mice, Mutant Strains Nutrient deficiency Oxidoreductases - genetics Sphingolipids Sphingolipids - chemistry Sphingolipids - metabolism Steatosis |
| Title | Targeting a ceramide double bond improves insulin resistance and hepatic steatosis |
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