Specific Hepatic Sphingolipids Relate to Insulin Resistance, Oxidative Stress, and Inflammation in Nonalcoholic Steatohepatitis
Insulin resistance and nonalcoholic fatty liver disease have been linked to several lipid metabolites in animals, but their role in humans remains unclear. This study examined the relationship of sphingolipids with hepatic and peripheral metabolism in 21 insulin-resistant obese patients without (NAF...
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| Vydané v: | Diabetes care Ročník 41; číslo 6; s. 1235 |
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| Hlavní autori: | , , , , , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | English |
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United States
01.06.2018
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| ISSN: | 1935-5548, 1935-5548 |
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| Abstract | Insulin resistance and nonalcoholic fatty liver disease have been linked to several lipid metabolites in animals, but their role in humans remains unclear. This study examined the relationship of sphingolipids with hepatic and peripheral metabolism in 21 insulin-resistant obese patients without (NAFL-) or with (NAFL+) nonalcoholic fatty liver and nonalcoholic steatohepatitis (NASH) and 7 healthy lean individuals undergoing tissue biopsies during bariatric or elective abdominal surgery.
Hyperinsulinemic-euglycemic clamps with d-[6,6-
H
]glucose were performed to quantify tissue-specific insulin sensitivity. Hepatic oxidative capacity, lipid peroxidation, and the phosphorylated-to-total c-Jun N-terminal kinase (pJNK-to-tJNK) ratio were measured to assess mitochondrial function, oxidative stress, and inflammatory activity.
Hepatic total ceramides were higher by 50% and 33% in NASH compared with NAFL+ and NAFL-, respectively. Only in NASH were hepatic dihydroceramides (16:0, 22:0, and 24:1) and lactosylceramides increased. Serum total ceramides and dihydroceramides (hepatic dihydroceramides 22:0 and 24:1) correlated negatively with whole-body but not with hepatic insulin sensitivity. Hepatic maximal respiration related positively to serum lactosylceramide subspecies, hepatic sphinganine, and lactosylceramide 14:0. Liver lipid peroxides (total ceramides, sphingomyelin 22:0) and the pJNK-to-tJNK ratio (ceramide 24:0; hexosylceramides 22:0, 24:0, and 24:1) all positively correlated with the respective hepatic sphingolipids.
Sphingolipid species are not only increased in insulin-resistant humans with NASH but also correlate with hepatic oxidative stress and inflammation, suggesting that these lipids may play a role during progression of simple steatosis to NASH in humans. |
|---|---|
| AbstractList | Insulin resistance and nonalcoholic fatty liver disease have been linked to several lipid metabolites in animals, but their role in humans remains unclear. This study examined the relationship of sphingolipids with hepatic and peripheral metabolism in 21 insulin-resistant obese patients without (NAFL-) or with (NAFL+) nonalcoholic fatty liver and nonalcoholic steatohepatitis (NASH) and 7 healthy lean individuals undergoing tissue biopsies during bariatric or elective abdominal surgery.OBJECTIVEInsulin resistance and nonalcoholic fatty liver disease have been linked to several lipid metabolites in animals, but their role in humans remains unclear. This study examined the relationship of sphingolipids with hepatic and peripheral metabolism in 21 insulin-resistant obese patients without (NAFL-) or with (NAFL+) nonalcoholic fatty liver and nonalcoholic steatohepatitis (NASH) and 7 healthy lean individuals undergoing tissue biopsies during bariatric or elective abdominal surgery.Hyperinsulinemic-euglycemic clamps with d-[6,6-2H2]glucose were performed to quantify tissue-specific insulin sensitivity. Hepatic oxidative capacity, lipid peroxidation, and the phosphorylated-to-total c-Jun N-terminal kinase (pJNK-to-tJNK) ratio were measured to assess mitochondrial function, oxidative stress, and inflammatory activity.RESEARCH DESIGN AND METHODSHyperinsulinemic-euglycemic clamps with d-[6,6-2H2]glucose were performed to quantify tissue-specific insulin sensitivity. Hepatic oxidative capacity, lipid peroxidation, and the phosphorylated-to-total c-Jun N-terminal kinase (pJNK-to-tJNK) ratio were measured to assess mitochondrial function, oxidative stress, and inflammatory activity.Hepatic total ceramides were higher by 50% and 33% in NASH compared with NAFL+ and NAFL-, respectively. Only in NASH were hepatic dihydroceramides (16:0, 22:0, and 24:1) and lactosylceramides increased. Serum total ceramides and dihydroceramides (hepatic dihydroceramides 22:0 and 24:1) correlated negatively with whole-body but not with hepatic insulin sensitivity. Hepatic maximal respiration related positively to serum lactosylceramide subspecies, hepatic sphinganine, and lactosylceramide 14:0. Liver lipid peroxides (total ceramides, sphingomyelin 22:0) and the pJNK-to-tJNK ratio (ceramide 24:0; hexosylceramides 22:0, 24:0, and 24:1) all positively correlated with the respective hepatic sphingolipids.RESULTSHepatic total ceramides were higher by 50% and 33% in NASH compared with NAFL+ and NAFL-, respectively. Only in NASH were hepatic dihydroceramides (16:0, 22:0, and 24:1) and lactosylceramides increased. Serum total ceramides and dihydroceramides (hepatic dihydroceramides 22:0 and 24:1) correlated negatively with whole-body but not with hepatic insulin sensitivity. Hepatic maximal respiration related positively to serum lactosylceramide subspecies, hepatic sphinganine, and lactosylceramide 14:0. Liver lipid peroxides (total ceramides, sphingomyelin 22:0) and the pJNK-to-tJNK ratio (ceramide 24:0; hexosylceramides 22:0, 24:0, and 24:1) all positively correlated with the respective hepatic sphingolipids.Sphingolipid species are not only increased in insulin-resistant humans with NASH but also correlate with hepatic oxidative stress and inflammation, suggesting that these lipids may play a role during progression of simple steatosis to NASH in humans.CONCLUSIONSSphingolipid species are not only increased in insulin-resistant humans with NASH but also correlate with hepatic oxidative stress and inflammation, suggesting that these lipids may play a role during progression of simple steatosis to NASH in humans. Insulin resistance and nonalcoholic fatty liver disease have been linked to several lipid metabolites in animals, but their role in humans remains unclear. This study examined the relationship of sphingolipids with hepatic and peripheral metabolism in 21 insulin-resistant obese patients without (NAFL-) or with (NAFL+) nonalcoholic fatty liver and nonalcoholic steatohepatitis (NASH) and 7 healthy lean individuals undergoing tissue biopsies during bariatric or elective abdominal surgery. Hyperinsulinemic-euglycemic clamps with d-[6,6- H ]glucose were performed to quantify tissue-specific insulin sensitivity. Hepatic oxidative capacity, lipid peroxidation, and the phosphorylated-to-total c-Jun N-terminal kinase (pJNK-to-tJNK) ratio were measured to assess mitochondrial function, oxidative stress, and inflammatory activity. Hepatic total ceramides were higher by 50% and 33% in NASH compared with NAFL+ and NAFL-, respectively. Only in NASH were hepatic dihydroceramides (16:0, 22:0, and 24:1) and lactosylceramides increased. Serum total ceramides and dihydroceramides (hepatic dihydroceramides 22:0 and 24:1) correlated negatively with whole-body but not with hepatic insulin sensitivity. Hepatic maximal respiration related positively to serum lactosylceramide subspecies, hepatic sphinganine, and lactosylceramide 14:0. Liver lipid peroxides (total ceramides, sphingomyelin 22:0) and the pJNK-to-tJNK ratio (ceramide 24:0; hexosylceramides 22:0, 24:0, and 24:1) all positively correlated with the respective hepatic sphingolipids. Sphingolipid species are not only increased in insulin-resistant humans with NASH but also correlate with hepatic oxidative stress and inflammation, suggesting that these lipids may play a role during progression of simple steatosis to NASH in humans. |
| Author | Gancheva, Sofia Roden, Michael Schlensak, Matthias Esposito, Irene Jelenik, Tomas Markgraf, Daniel Koliaki, Chrysi De Filippo, Elisabetta Jankowiak, Frank Apostolopoulou, Maria Scherer, Philipp E Gordillo, Ruth Herder, Christian |
| Author_xml | – sequence: 1 givenname: Maria surname: Apostolopoulou fullname: Apostolopoulou, Maria organization: German Center for Diabetes Research, München-Neuherberg, Germany – sequence: 2 givenname: Ruth surname: Gordillo fullname: Gordillo, Ruth organization: Touchstone Diabetes Center, Department of Internal Medicine, The University of Texas Southwestern Medical Center, Dallas, TX – sequence: 3 givenname: Chrysi surname: Koliaki fullname: Koliaki, Chrysi organization: German Center for Diabetes Research, München-Neuherberg, Germany – sequence: 4 givenname: Sofia surname: Gancheva fullname: Gancheva, Sofia organization: German Center for Diabetes Research, München-Neuherberg, Germany – sequence: 5 givenname: Tomas orcidid: 0000-0002-2061-1162 surname: Jelenik fullname: Jelenik, Tomas organization: German Center for Diabetes Research, München-Neuherberg, Germany – sequence: 6 givenname: Elisabetta surname: De Filippo fullname: De Filippo, Elisabetta organization: German Center for Diabetes Research, München-Neuherberg, Germany – sequence: 7 givenname: Christian orcidid: 0000-0002-2050-093X surname: Herder fullname: Herder, Christian organization: German Center for Diabetes Research, München-Neuherberg, Germany – sequence: 8 givenname: Daniel surname: Markgraf fullname: Markgraf, Daniel organization: German Center for Diabetes Research, München-Neuherberg, Germany – sequence: 9 givenname: Frank surname: Jankowiak fullname: Jankowiak, Frank organization: Institute of Pathology, Medical Faculty, Heinrich-Heine University, Düsseldorf, Germany – sequence: 10 givenname: Irene surname: Esposito fullname: Esposito, Irene organization: Institute of Pathology, Medical Faculty, Heinrich-Heine University, Düsseldorf, Germany – sequence: 11 givenname: Matthias surname: Schlensak fullname: Schlensak, Matthias organization: General Surgery Department, Schön Clinic, Düsseldorf, Germany – sequence: 12 givenname: Philipp E orcidid: 0000-0002-5336-1358 surname: Scherer fullname: Scherer, Philipp E organization: Touchstone Diabetes Center, Department of Internal Medicine, The University of Texas Southwestern Medical Center, Dallas, TX – sequence: 13 givenname: Michael orcidid: 0000-0001-8200-6382 surname: Roden fullname: Roden, Michael email: michael.roden@ddz.uni-duesseldorf.de organization: German Center for Diabetes Research, München-Neuherberg, Germany |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/29602794$$D View this record in MEDLINE/PubMed |
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| SubjectTerms | Adult Animals Disease Progression Female Glucose Clamp Technique Humans Inflammation - blood Inflammation - metabolism Inflammation - physiopathology Insulin Resistance - physiology Lipid Peroxidation - physiology Liver - chemistry Liver - metabolism Liver - pathology Male Middle Aged Non-alcoholic Fatty Liver Disease - blood Non-alcoholic Fatty Liver Disease - metabolism Non-alcoholic Fatty Liver Disease - physiopathology Obesity - blood Obesity - metabolism Obesity - physiopathology Obesity - surgery Oxidation-Reduction Oxidative Stress - physiology Prospective Studies Sphingolipids - analysis Sphingolipids - blood Sphingolipids - metabolism |
| Title | Specific Hepatic Sphingolipids Relate to Insulin Resistance, Oxidative Stress, and Inflammation in Nonalcoholic Steatohepatitis |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/29602794 https://www.proquest.com/docview/2020492551 |
| Volume | 41 |
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