Autotaxin-lysophosphatidic acid receptor signalling regulates hepatitis C virus replication
[Display omitted] Chronic hepatitis C is a global health problem with an estimated 170 million hepatitis C virus (HCV) infected individuals at risk of progressive liver disease and hepatocellular carcinoma (HCC). Autotaxin (ATX, gene name: ENPP2) is a phospholipase with diverse roles in the physiolo...
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| Veröffentlicht in: | Journal of hepatology Jg. 66; H. 5; S. 919 - 929 |
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| Hauptverfasser: | , , , , , , , , , , , , , , , |
| Format: | Journal Article |
| Sprache: | Englisch |
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Netherlands
Elsevier B.V
01.05.2017
Elsevier Science Ltd Elsevier |
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| ISSN: | 0168-8278, 1600-0641, 1600-0641 |
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| Abstract | [Display omitted]
Chronic hepatitis C is a global health problem with an estimated 170 million hepatitis C virus (HCV) infected individuals at risk of progressive liver disease and hepatocellular carcinoma (HCC). Autotaxin (ATX, gene name: ENPP2) is a phospholipase with diverse roles in the physiological and pathological processes including inflammation and oncogenesis. Clinical studies have reported increased ATX expression in chronic hepatitis C, however, the pathways regulating ATX and its role in the viral life cycle are not well understood.
In vitro hepatocyte and ex vivo liver culture systems along with chimeric humanized liver mice and HCC tissue enabled us to assess the interplay between ATX and the HCV life cycle.
HCV infection increased hepatocellular ATX RNA and protein expression. HCV infection stabilizes hypoxia inducible factors (HIFs) and we investigated a role for these transcription factors to regulate ATX. In vitro studies show that low oxygen increases hepatocellular ATX expression and transcriptome analysis showed a positive correlation between ATX mRNA levels and hypoxia gene score in HCC tumour tissue associated with HCV and other aetiologies. Importantly, inhibiting ATX-lysophosphatidic acid (LPA) signalling reduced HCV replication, demonstrating a positive role for this phospholipase in the viral life cycle. LPA activates phosphoinositide-3-kinase that stabilizes HIF-1α and inhibiting the HIF signalling pathway abrogates the pro-viral activity of LPA.
Our data support a model where HCV infection increases ATX expression which supports viral replication and HCC progression.
Chronic hepatitis C is a global health problem with infected individuals at risk of developing liver disease that can progress to hepatocellular carcinoma. Autotaxin generates the biologically active lipid lysophosphatidic acid that has been reported to play a tumorigenic role in a wide number of cancers. In this study we show that hepatitis C virus infection increases autotaxin expression via hypoxia inducible transcription factor and provides an environment in the liver that promotes fibrosis and liver injury. Importantly, we show a new role for lysophosphatidic acid in positively regulating hepatitis C virus replication. |
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| AbstractList | Graphical abstract Background & Aims Chronic hepatitis C is a global health problem with an estimated 170 million hepatitis C virus (HCV) infected individuals at risk of progressive liver disease and hepatocellular carcinoma (HCC). Autotaxin (ATX, gene name: ENPP2) is a phospholipase with diverse roles in the physiological and pathological processes including inflammation and oncogenesis. Clinical studies have reported increased ATX expression in chronic hepatitis C, however, the pathways regulating ATX and its role in the viral life cycle are not well understood. Methods In vitro hepatocyte and ex vivo liver culture systems along with chimeric humanized liver mice and HCC tissue enabled us to assess the interplay between ATX and the HCV life cycle. Results HCV infection increased hepatocellular ATX RNA and protein expression. HCV infection stabilizes hypoxia inducible factors (HIFs) and we investigated a role for these transcription factors to regulate ATX. In vitro studies show that low oxygen increases hepatocellular ATX expression and transcriptome analysis showed a positive correlation between ATX mRNA levels and hypoxia gene score in HCC tumour tissue associated with HCV and other aetiologies. Importantly, inhibiting ATX-lysophosphatidic acid (LPA) signalling reduced HCV replication, demonstrating a positive role for this phospholipase in the viral life cycle. LPA activates phosphoinositide-3-kinase that stabilizes HIF-1α and inhibiting the HIF signalling pathway abrogates the pro-viral activity of LPA. Conclusions Our data support a model where HCV infection increases ATX expression which supports viral replication and HCC progression. [Display omitted] Chronic hepatitis C is a global health problem with an estimated 170 million hepatitis C virus (HCV) infected individuals at risk of progressive liver disease and hepatocellular carcinoma (HCC). Autotaxin (ATX, gene name: ENPP2) is a phospholipase with diverse roles in the physiological and pathological processes including inflammation and oncogenesis. Clinical studies have reported increased ATX expression in chronic hepatitis C, however, the pathways regulating ATX and its role in the viral life cycle are not well understood. In vitro hepatocyte and ex vivo liver culture systems along with chimeric humanized liver mice and HCC tissue enabled us to assess the interplay between ATX and the HCV life cycle. HCV infection increased hepatocellular ATX RNA and protein expression. HCV infection stabilizes hypoxia inducible factors (HIFs) and we investigated a role for these transcription factors to regulate ATX. In vitro studies show that low oxygen increases hepatocellular ATX expression and transcriptome analysis showed a positive correlation between ATX mRNA levels and hypoxia gene score in HCC tumour tissue associated with HCV and other aetiologies. Importantly, inhibiting ATX-lysophosphatidic acid (LPA) signalling reduced HCV replication, demonstrating a positive role for this phospholipase in the viral life cycle. LPA activates phosphoinositide-3-kinase that stabilizes HIF-1α and inhibiting the HIF signalling pathway abrogates the pro-viral activity of LPA. Our data support a model where HCV infection increases ATX expression which supports viral replication and HCC progression. Chronic hepatitis C is a global health problem with infected individuals at risk of developing liver disease that can progress to hepatocellular carcinoma. Autotaxin generates the biologically active lipid lysophosphatidic acid that has been reported to play a tumorigenic role in a wide number of cancers. In this study we show that hepatitis C virus infection increases autotaxin expression via hypoxia inducible transcription factor and provides an environment in the liver that promotes fibrosis and liver injury. Importantly, we show a new role for lysophosphatidic acid in positively regulating hepatitis C virus replication. Chronic hepatitis C is a global health problem with an estimated 170 million hepatitis C virus (HCV) infected individuals at risk of progressive liver disease and hepatocellular carcinoma (HCC). Autotaxin (ATX, gene name: ENPP2) is a phospholipase with diverse roles in the physiological and pathological processes including inflammation and oncogenesis. Clinical studies have reported increased ATX expression in chronic hepatitis C, however, the pathways regulating ATX and its role in the viral life cycle are not well understood. In vitro hepatocyte and ex vivo liver culture systems along with chimeric humanized liver mice and HCC tissue enabled us to assess the interplay between ATX and the HCV life cycle. HCV infection increased hepatocellular ATX RNA and protein expression. HCV infection stabilizes hypoxia inducible factors (HIFs) and we investigated a role for these transcription factors to regulate ATX. In vitro studies show that low oxygen increases hepatocellular ATX expression and transcriptome analysis showed a positive correlation between ATX mRNA levels and hypoxia gene score in HCC tumour tissue associated with HCV and other aetiologies. Importantly, inhibiting ATX-lysophosphatidic acid (LPA) signalling reduced HCV replication, demonstrating a positive role for this phospholipase in the viral life cycle. LPA activates phosphoinositide-3-kinase that stabilizes HIF-1α and inhibiting the HIF signalling pathway abrogates the pro-viral activity of LPA. Our data support a model where HCV infection increases ATX expression which supports viral replication and HCC progression. Chronic hepatitis C is a global health problem with infected individuals at risk of developing liver disease that can progress to hepatocellular carcinoma. Autotaxin generates the biologically active lipid lysophosphatidic acid that has been reported to play a tumorigenic role in a wide number of cancers. In this study we show that hepatitis C virus infection increases autotaxin expression via hypoxia inducible transcription factor and provides an environment in the liver that promotes fibrosis and liver injury. Importantly, we show a new role for lysophosphatidic acid in positively regulating hepatitis C virus replication. Chronic hepatitis C is a global health problem with an estimated 170 million hepatitis C virus (HCV) infected individuals at risk of progressive liver disease and hepatocellular carcinoma (HCC). Autotaxin (ATX, gene name: ENPP2) is a phospholipase with diverse roles in the physiological and pathological processes including inflammation and oncogenesis. Clinical studies have reported increased ATX expression in chronic hepatitis C, however, the pathways regulating ATX and its role in the viral life cycle are not well understood.BACKGROUND & AIMSChronic hepatitis C is a global health problem with an estimated 170 million hepatitis C virus (HCV) infected individuals at risk of progressive liver disease and hepatocellular carcinoma (HCC). Autotaxin (ATX, gene name: ENPP2) is a phospholipase with diverse roles in the physiological and pathological processes including inflammation and oncogenesis. Clinical studies have reported increased ATX expression in chronic hepatitis C, however, the pathways regulating ATX and its role in the viral life cycle are not well understood.In vitro hepatocyte and ex vivo liver culture systems along with chimeric humanized liver mice and HCC tissue enabled us to assess the interplay between ATX and the HCV life cycle.METHODSIn vitro hepatocyte and ex vivo liver culture systems along with chimeric humanized liver mice and HCC tissue enabled us to assess the interplay between ATX and the HCV life cycle.HCV infection increased hepatocellular ATX RNA and protein expression. HCV infection stabilizes hypoxia inducible factors (HIFs) and we investigated a role for these transcription factors to regulate ATX. In vitro studies show that low oxygen increases hepatocellular ATX expression and transcriptome analysis showed a positive correlation between ATX mRNA levels and hypoxia gene score in HCC tumour tissue associated with HCV and other aetiologies. Importantly, inhibiting ATX-lysophosphatidic acid (LPA) signalling reduced HCV replication, demonstrating a positive role for this phospholipase in the viral life cycle. LPA activates phosphoinositide-3-kinase that stabilizes HIF-1α and inhibiting the HIF signalling pathway abrogates the pro-viral activity of LPA.RESULTSHCV infection increased hepatocellular ATX RNA and protein expression. HCV infection stabilizes hypoxia inducible factors (HIFs) and we investigated a role for these transcription factors to regulate ATX. In vitro studies show that low oxygen increases hepatocellular ATX expression and transcriptome analysis showed a positive correlation between ATX mRNA levels and hypoxia gene score in HCC tumour tissue associated with HCV and other aetiologies. Importantly, inhibiting ATX-lysophosphatidic acid (LPA) signalling reduced HCV replication, demonstrating a positive role for this phospholipase in the viral life cycle. LPA activates phosphoinositide-3-kinase that stabilizes HIF-1α and inhibiting the HIF signalling pathway abrogates the pro-viral activity of LPA.Our data support a model where HCV infection increases ATX expression which supports viral replication and HCC progression.CONCLUSIONSOur data support a model where HCV infection increases ATX expression which supports viral replication and HCC progression.Chronic hepatitis C is a global health problem with infected individuals at risk of developing liver disease that can progress to hepatocellular carcinoma. Autotaxin generates the biologically active lipid lysophosphatidic acid that has been reported to play a tumorigenic role in a wide number of cancers. In this study we show that hepatitis C virus infection increases autotaxin expression via hypoxia inducible transcription factor and provides an environment in the liver that promotes fibrosis and liver injury. Importantly, we show a new role for lysophosphatidic acid in positively regulating hepatitis C virus replication.LAY SUMMARYChronic hepatitis C is a global health problem with infected individuals at risk of developing liver disease that can progress to hepatocellular carcinoma. Autotaxin generates the biologically active lipid lysophosphatidic acid that has been reported to play a tumorigenic role in a wide number of cancers. In this study we show that hepatitis C virus infection increases autotaxin expression via hypoxia inducible transcription factor and provides an environment in the liver that promotes fibrosis and liver injury. Importantly, we show a new role for lysophosphatidic acid in positively regulating hepatitis C virus replication. |
| Author | McKeating, Jane A. Wilson, Garrick K. Ashcroft, Margaret Ciaccia, Maria Balfe, Peter Reynolds, Gary M. Humphreys, Isla S. Wakelam, Michael J.O. Baumert, Thomas F. Zhang, Qifeng Rudge, Simon A. Hu, Ke Mailly, Laurent Bhattacharya, Bishnupriya Farquhar, Michelle J. Roessler, Stephanie |
| Author_xml | – sequence: 1 givenname: Michelle J. surname: Farquhar fullname: Farquhar, Michelle J. organization: Viral Hepatitis Laboratory, Centre for Human Virology, University of Birmingham, UK – sequence: 2 givenname: Isla S. surname: Humphreys fullname: Humphreys, Isla S. organization: Viral Hepatitis Laboratory, Centre for Human Virology, University of Birmingham, UK – sequence: 3 givenname: Simon A. surname: Rudge fullname: Rudge, Simon A. organization: The Babraham Institute, Cambridge, UK – sequence: 4 givenname: Garrick K. surname: Wilson fullname: Wilson, Garrick K. organization: Viral Hepatitis Laboratory, Centre for Human Virology, University of Birmingham, UK – sequence: 5 givenname: Bishnupriya surname: Bhattacharya fullname: Bhattacharya, Bishnupriya organization: Viral Hepatitis Laboratory, Centre for Human Virology, University of Birmingham, UK – sequence: 6 givenname: Maria surname: Ciaccia fullname: Ciaccia, Maria organization: The Babraham Institute, Cambridge, UK – sequence: 7 givenname: Ke surname: Hu fullname: Hu, Ke organization: Viral Hepatitis Laboratory, Centre for Human Virology, University of Birmingham, UK – sequence: 8 givenname: Qifeng surname: Zhang fullname: Zhang, Qifeng organization: The Babraham Institute, Cambridge, UK – sequence: 9 givenname: Laurent surname: Mailly fullname: Mailly, Laurent organization: INSERM U1110, University of Strasbourg, 3 Rue Koeberlé, F-67000 Strasbourg, France – sequence: 10 givenname: Gary M. surname: Reynolds fullname: Reynolds, Gary M. organization: NIHR Liver Biomedical Research Unit, University of Birmingham, Birmingham, UK – sequence: 11 givenname: Margaret surname: Ashcroft fullname: Ashcroft, Margaret organization: Cambridge Biomedical Campus, University of Cambridge, Cambridge, UK – sequence: 12 givenname: Peter surname: Balfe fullname: Balfe, Peter organization: Viral Hepatitis Laboratory, Centre for Human Virology, University of Birmingham, UK – sequence: 13 givenname: Thomas F. surname: Baumert fullname: Baumert, Thomas F. organization: INSERM U1110, University of Strasbourg, 3 Rue Koeberlé, F-67000 Strasbourg, France – sequence: 14 givenname: Stephanie surname: Roessler fullname: Roessler, Stephanie organization: Institute of Pathology, University Hospital Heidelberg, Heidelberg, Germany – sequence: 15 givenname: Michael J.O. surname: Wakelam fullname: Wakelam, Michael J.O. organization: The Babraham Institute, Cambridge, UK – sequence: 16 givenname: Jane A. surname: McKeating fullname: McKeating, Jane A. email: jane.mckeating@ndm.ox.ac.uk organization: Viral Hepatitis Laboratory, Centre for Human Virology, University of Birmingham, UK |
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| Keywords | Hypoxia Lysophosphatidic acid Hepatitis C virus Lipid signalling Autotaxin Hypoxia-Inducible Factor 1, alpha subunit |
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article-title: Lysophosphatidic acid receptor LPAR6 supports the tumorigenicity of hepatocellular carcinoma publication-title: Cancer Res doi: 10.1158/0008-5472.CAN-14-1607 – volume: 9 start-page: 71 year: 2010 ident: 10.1016/j.jhep.2017.01.009_b0035 article-title: Autotaxin expression and its connection with the TNF-alpha-NF-kappaB axis in human hepatocellular carcinoma publication-title: Mol Cancer doi: 10.1186/1476-4598-9-71 – volume: 5 start-page: 1935 year: 2013 ident: 10.1016/j.jhep.2017.01.009_b0190 article-title: Development of lysophosphatidic acid pathway modulators as therapies for fibrosis publication-title: Future Med Chem doi: 10.4155/fmc.13.154 – volume: 148 start-page: 30 year: 2015 ident: 10.1016/j.jhep.2017.01.009_b0160 article-title: Gut-liver axis in alcoholic liver disease publication-title: Gastroenterology doi: 10.1053/j.gastro.2014.10.042 |
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Chronic hepatitis C is a global health problem with an estimated 170 million hepatitis C virus (HCV) infected individuals at risk of... Graphical abstract Chronic hepatitis C is a global health problem with an estimated 170 million hepatitis C virus (HCV) infected individuals at risk of progressive liver disease... Background & Aims Chronic hepatitis C is a global health problem with an estimated 170 million hepatitis C virus (HCV) infected individuals at risk of... |
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| SubjectTerms | Aerospace medicine Animals Autotaxin Cell Line Gastroenterology and Hepatology Gene expression Genes Hepacivirus - physiology Hepatitis Hepatitis C Hepatitis C virus Hepatitis C, Chronic - complications Hepatocellular carcinoma Human health and pathology Humans Hypoxia Hypoxia-Inducible Factor 1, alpha subunit Hypoxia-Inducible Factor 1, alpha Subunit - physiology Hépatology and Gastroenterology Life cycles Life Sciences Lipid signalling Liver diseases Liver Neoplasms - etiology Lysophosphatidic acid Mice Phospholipase Phosphoric Diester Hydrolases - genetics Phosphoric Diester Hydrolases - physiology Promoter Regions, Genetic Receptors, Lysophosphatidic Acid - physiology Replication RNA, Messenger - analysis Signal Transduction Transcription factors Tumorigenesis Tumors Virus Replication Viruses |
| Title | Autotaxin-lysophosphatidic acid receptor signalling regulates hepatitis C virus replication |
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