Circadian Homeostasis of Liver Metabolism Suppresses Hepatocarcinogenesis
Chronic jet lag induces spontaneous hepatocellular carcinoma (HCC) in wild-type mice following a mechanism very similar to that observed in obese humans. The process initiates with non-alcoholic fatty liver disease (NAFLD) that progresses to steatohepatitis and fibrosis before HCC detection. This pa...
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| Published in: | Cancer cell Vol. 30; no. 6; pp. 909 - 924 |
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| Main Authors: | , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
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United States
Elsevier Inc
12-12-2016
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| Abstract | Chronic jet lag induces spontaneous hepatocellular carcinoma (HCC) in wild-type mice following a mechanism very similar to that observed in obese humans. The process initiates with non-alcoholic fatty liver disease (NAFLD) that progresses to steatohepatitis and fibrosis before HCC detection. This pathophysiological pathway is driven by jet-lag-induced genome-wide gene deregulation and global liver metabolic dysfunction, with nuclear receptor-controlled cholesterol/bile acid and xenobiotic metabolism among the top deregulated pathways. Ablation of farnesoid X receptor dramatically increases enterohepatic bile acid levels and jet-lag-induced HCC, while loss of constitutive androstane receptor (CAR), a well-known liver tumor promoter that mediates toxic bile acid signaling, inhibits NAFLD-induced hepatocarcinogenesis. Circadian disruption activates CAR by promoting cholestasis, peripheral clock disruption, and sympathetic dysfunction.
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•Chronic circadian disruption induces NAFLD and spontaneous hepatocarcinogenesis•Circadian dysfunction promotes global gene deregulation and metabolic disruption•The nuclear receptor CAR drives NAFLD to NASH, fibrosis, and HCC progression•Circadian disruption activates CAR via sympathetic dysfunction and cholestasis
Kettner et al. show that experimental chronic jet lag induces persistent deregulation of liver gene expression and metabolism, culminating in the development of hepatocellular carcinoma. The bile acid receptor FXR and xenobiotic receptor CAR play an important role in this process. |
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| AbstractList | Chronic jet lag induces spontaneous hepatocellular carcinoma (HCC) in wild-type mice following a mechanism very similar to that observed in obese humans. The process initiates with non-alcoholic fatty liver disease (NAFLD) that progresses to steatohepatitis and fibrosis before HCC detection. This pathophysiological pathway is driven by jet-lag-induced genome-wide gene deregulation and global liver metabolic dysfunction, with nuclear receptor-controlled cholesterol/bile acid and xenobiotic metabolism among the top deregulated pathways. Ablation of farnesoid X receptor dramatically increases enterohepatic bile acid levels and jet-lag-induced HCC, while loss of constitutive androstane receptor (CAR), a well-known liver tumor promoter that mediates toxic bile acid signaling, inhibits NAFLD-induced hepatocarcinogenesis. Circadian disruption activates CAR by promoting cholestasis, peripheral clock disruption, and sympathetic dysfunction. Chronic jet lag induces spontaneous hepatocellular carcinoma (HCC) in wild-type mice following a mechanism very similar to that observed in obese humans. The process initiates with non-alcoholic fatty liver disease (NAFLD) that progresses to steatohepatitis and fibrosis before HCC detection. This pathophysiological pathway is driven by jet lag induced genome-wide gene deregulation and global liver metabolic dysfunction, with nuclear receptor-controlled cholesterol/bile acid and xenobiotic metabolism among the top deregulated pathways. Ablation of farnesoid X receptor (FXR) dramatically increases enterohepatic bile acid levels and jet lag-induced HCC, while loss of constitutive androstane receptor (CAR), a well-known liver tumor promoter that mediates toxic bile acid signaling, inhibits NAFLD-induced hepatocarcinogenesis. Circadian disruption activates CAR by promoting cholestasis, peripheral clock disruption, and sympathetic dysfunction. Kettner et al. show that experimental chronic jet lag induces persistent deregulation of liver gene expression and metabolism, culminating in the development of hepatocellular carcinoma. The bile acid receptor FXR and xenobiotic receptor CAR play an important role in this process. Chronic jet lag induces spontaneous hepatocellular carcinoma (HCC) in wild-type mice following a mechanism very similar to that observed in obese humans. The process initiates with non-alcoholic fatty liver disease (NAFLD) that progresses to steatohepatitis and fibrosis before HCC detection. This pathophysiological pathway is driven by jet-lag-induced genome-wide gene deregulation and global liver metabolic dysfunction, with nuclear receptor-controlled cholesterol/bile acid and xenobiotic metabolism among the top deregulated pathways. Ablation of farnesoid X receptor dramatically increases enterohepatic bile acid levels and jet-lag-induced HCC, while loss of constitutive androstane receptor (CAR), a well-known liver tumor promoter that mediates toxic bile acid signaling, inhibits NAFLD-induced hepatocarcinogenesis. Circadian disruption activates CAR by promoting cholestasis, peripheral clock disruption, and sympathetic dysfunction. [Display omitted] •Chronic circadian disruption induces NAFLD and spontaneous hepatocarcinogenesis•Circadian dysfunction promotes global gene deregulation and metabolic disruption•The nuclear receptor CAR drives NAFLD to NASH, fibrosis, and HCC progression•Circadian disruption activates CAR via sympathetic dysfunction and cholestasis Kettner et al. show that experimental chronic jet lag induces persistent deregulation of liver gene expression and metabolism, culminating in the development of hepatocellular carcinoma. The bile acid receptor FXR and xenobiotic receptor CAR play an important role in this process. |
| Author | Finegold, Milton J. Moore, David D. Lee, Choogon Kettner, Nicole M. Voicu, Horatio Sreekumar, Arun Coarfa, Cristian Putluri, Nagireddy Fu, Loning Katchy, Chinenye A. |
| AuthorAffiliation | 2 Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, TX 77030, USA 1 Department of Pediatrics/U.S. Department of Agriculture/Agricultural Research Service/Children's Nutrition Research Center, Baylor College of Medicine, Houston, TX 77030, USA 3 Dan L. Duncan Cancer Center, Baylor College of Medicine, Houston, TX 77030, USA 5 Program in Neuroscience, Florida State University, College of Medicine, Tallahassee, FL 32306, USA 4 Department of Pathology, Baylor College of Medicine, Houston, TX 77030, USA |
| AuthorAffiliation_xml | – name: 1 Department of Pediatrics/U.S. Department of Agriculture/Agricultural Research Service/Children's Nutrition Research Center, Baylor College of Medicine, Houston, TX 77030, USA – name: 3 Dan L. Duncan Cancer Center, Baylor College of Medicine, Houston, TX 77030, USA – name: 2 Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, TX 77030, USA – name: 5 Program in Neuroscience, Florida State University, College of Medicine, Tallahassee, FL 32306, USA – name: 4 Department of Pathology, Baylor College of Medicine, Houston, TX 77030, USA |
| Author_xml | – sequence: 1 givenname: Nicole M. surname: Kettner fullname: Kettner, Nicole M. organization: Department of Pediatrics/U.S. Department of Agriculture/Agricultural Research Service/Children's Nutrition Research Center, Baylor College of Medicine, Houston, TX 77030, USA – sequence: 2 givenname: Horatio surname: Voicu fullname: Voicu, Horatio organization: Dan L. Duncan Cancer Center, Baylor College of Medicine, Houston, TX 77030, USA – sequence: 3 givenname: Milton J. surname: Finegold fullname: Finegold, Milton J. organization: Dan L. Duncan Cancer Center, Baylor College of Medicine, Houston, TX 77030, USA – sequence: 4 givenname: Cristian surname: Coarfa fullname: Coarfa, Cristian organization: Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, TX 77030, USA – sequence: 5 givenname: Arun surname: Sreekumar fullname: Sreekumar, Arun organization: Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, TX 77030, USA – sequence: 6 givenname: Nagireddy surname: Putluri fullname: Putluri, Nagireddy organization: Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, TX 77030, USA – sequence: 7 givenname: Chinenye A. surname: Katchy fullname: Katchy, Chinenye A. organization: Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, TX 77030, USA – sequence: 8 givenname: Choogon surname: Lee fullname: Lee, Choogon organization: Program in Neuroscience, Florida State University, College of Medicine, Tallahassee, FL 32306, USA – sequence: 9 givenname: David D. surname: Moore fullname: Moore, David D. email: moore@bcm.edu organization: Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, TX 77030, USA – sequence: 10 givenname: Loning surname: Fu fullname: Fu, Loning email: loningf@bcm.edu organization: Department of Pediatrics/U.S. Department of Agriculture/Agricultural Research Service/Children's Nutrition Research Center, Baylor College of Medicine, Houston, TX 77030, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/27889186$$D View this record in MEDLINE/PubMed |
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| Keywords | social jet lag non-alcoholic fatty liver disease cholestasis farnesoid X receptor (FXR) fibrosis sympathetic dysfunction hepatocarcinogenesis chronic circadian disruption non-alcoholic steatohepatitis constitutive androstane receptor (CAR) |
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| Snippet | Chronic jet lag induces spontaneous hepatocellular carcinoma (HCC) in wild-type mice following a mechanism very similar to that observed in obese humans. The... |
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| SubjectTerms | Animals Carcinoma, Hepatocellular - genetics Carcinoma, Hepatocellular - metabolism cholestasis chronic circadian disruption Circadian Clocks constitutive androstane receptor (CAR) Disease Models, Animal farnesoid X receptor (FXR) fibrosis Gene Expression Regulation Genetic Predisposition to Disease hepatocarcinogenesis Homeostasis Humans Liver - metabolism Liver Cirrhosis - genetics Liver Cirrhosis - metabolism Liver Neoplasms - genetics Liver Neoplasms - metabolism Metabolome Mice non-alcoholic fatty liver disease Non-alcoholic Fatty Liver Disease - complications Non-alcoholic Fatty Liver Disease - genetics Non-alcoholic Fatty Liver Disease - metabolism non-alcoholic steatohepatitis Receptors, Cytoplasmic and Nuclear - genetics Receptors, Cytoplasmic and Nuclear - metabolism social jet lag sympathetic dysfunction |
| Title | Circadian Homeostasis of Liver Metabolism Suppresses Hepatocarcinogenesis |
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