Transcriptional Dynamics of Hepatic Sinusoid‐Associated Cells After Liver Injury
Background and Aims Hepatic sinusoidal cells are known actors in the fibrogenic response to injury. Activated hepatic stellate cells (HSCs), liver sinusoidal endothelial cells, and Kupffer cells are responsible for sinusoidal capillarization and perisinusoidal matrix deposition, impairing vascular e...
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Published in | Hepatology (Baltimore, Md.) Vol. 72; no. 6; pp. 2119 - 2133 |
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Main Authors | , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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01.12.2020
John Wiley and Sons Inc |
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Abstract | Background and Aims
Hepatic sinusoidal cells are known actors in the fibrogenic response to injury. Activated hepatic stellate cells (HSCs), liver sinusoidal endothelial cells, and Kupffer cells are responsible for sinusoidal capillarization and perisinusoidal matrix deposition, impairing vascular exchange and heightening the risk of advanced fibrosis. While the overall pathogenesis is well understood, functional relations between cellular transitions during fibrogenesis are only beginning to be resolved. At single‐cell resolution, we here explored the heterogeneity of individual cell types and dissected their transitions and crosstalk during fibrogenesis.
Approach and Results
We applied single‐cell transcriptomics to map the heterogeneity of sinusoid‐associated cells in healthy and injured livers and reconstructed the single‐lineage HSC trajectory from pericyte to myofibroblast. Stratifying each sinusoidal cell population by activation state, we projected shifts in sinusoidal communication upon injury. Weighted gene correlation network analysis of the HSC trajectory led to the identification of core genes whose expression proved highly predictive of advanced fibrosis in patients with nonalcoholic steatohepatitis (NASH). Among the core members of the injury‐repressed gene module, we identified plasmalemma vesicle–associated protein (PLVAP) as a protein amply expressed by mouse and human HSCs. PLVAP expression was suppressed in activated HSCs upon injury and may hence define hitherto unknown roles for HSCs in the regulation of microcirculatory exchange and its breakdown in chronic liver disease.
Conclusions
Our study offers a single‐cell resolved account of drug‐induced injury of the mammalian liver and identifies key genes that may serve important roles in sinusoidal integrity and as markers of advanced fibrosis in human NASH. |
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AbstractList | Background and Aims
Hepatic sinusoidal cells are known actors in the fibrogenic response to injury. Activated hepatic stellate cells (HSCs), liver sinusoidal endothelial cells, and Kupffer cells are responsible for sinusoidal capillarization and perisinusoidal matrix deposition, impairing vascular exchange and heightening the risk of advanced fibrosis. While the overall pathogenesis is well understood, functional relations between cellular transitions during fibrogenesis are only beginning to be resolved. At single‐cell resolution, we here explored the heterogeneity of individual cell types and dissected their transitions and crosstalk during fibrogenesis.
Approach and Results
We applied single‐cell transcriptomics to map the heterogeneity of sinusoid‐associated cells in healthy and injured livers and reconstructed the single‐lineage HSC trajectory from pericyte to myofibroblast. Stratifying each sinusoidal cell population by activation state, we projected shifts in sinusoidal communication upon injury. Weighted gene correlation network analysis of the HSC trajectory led to the identification of core genes whose expression proved highly predictive of advanced fibrosis in patients with nonalcoholic steatohepatitis (NASH). Among the core members of the injury‐repressed gene module, we identified plasmalemma vesicle–associated protein (PLVAP) as a protein amply expressed by mouse and human HSCs. PLVAP expression was suppressed in activated HSCs upon injury and may hence define hitherto unknown roles for HSCs in the regulation of microcirculatory exchange and its breakdown in chronic liver disease.
Conclusions
Our study offers a single‐cell resolved account of drug‐induced injury of the mammalian liver and identifies key genes that may serve important roles in sinusoidal integrity and as markers of advanced fibrosis in human NASH. BACKGROUND AND AIMSHepatic sinusoidal cells are known actors in the fibrogenic response to injury. Activated hepatic stellate cells (HSCs), liver sinusoidal endothelial cells, and Kupffer cells are responsible for sinusoidal capillarization and perisinusoidal matrix deposition, impairing vascular exchange and heightening the risk of advanced fibrosis. While the overall pathogenesis is well understood, functional relations between cellular transitions during fibrogenesis are only beginning to be resolved. At single-cell resolution, we here explored the heterogeneity of individual cell types and dissected their transitions and crosstalk during fibrogenesis. APPROACH AND RESULTSWe applied single-cell transcriptomics to map the heterogeneity of sinusoid-associated cells in healthy and injured livers and reconstructed the single-lineage HSC trajectory from pericyte to myofibroblast. Stratifying each sinusoidal cell population by activation state, we projected shifts in sinusoidal communication upon injury. Weighted gene correlation network analysis of the HSC trajectory led to the identification of core genes whose expression proved highly predictive of advanced fibrosis in patients with nonalcoholic steatohepatitis (NASH). Among the core members of the injury-repressed gene module, we identified plasmalemma vesicle-associated protein (PLVAP) as a protein amply expressed by mouse and human HSCs. PLVAP expression was suppressed in activated HSCs upon injury and may hence define hitherto unknown roles for HSCs in the regulation of microcirculatory exchange and its breakdown in chronic liver disease. CONCLUSIONSOur study offers a single-cell resolved account of drug-induced injury of the mammalian liver and identifies key genes that may serve important roles in sinusoidal integrity and as markers of advanced fibrosis in human NASH. Hepatic sinusoidal cells are known actors in the fibrogenic response to injury. Activated hepatic stellate cells (HSCs), liver sinusoidal endothelial cells, and Kupffer cells are responsible for sinusoidal capillarization and perisinusoidal matrix deposition, impairing vascular exchange and heightening the risk of advanced fibrosis. While the overall pathogenesis is well understood, functional relations between cellular transitions during fibrogenesis are only beginning to be resolved. At single-cell resolution, we here explored the heterogeneity of individual cell types and dissected their transitions and crosstalk during fibrogenesis. We applied single-cell transcriptomics to map the heterogeneity of sinusoid-associated cells in healthy and injured livers and reconstructed the single-lineage HSC trajectory from pericyte to myofibroblast. Stratifying each sinusoidal cell population by activation state, we projected shifts in sinusoidal communication upon injury. Weighted gene correlation network analysis of the HSC trajectory led to the identification of core genes whose expression proved highly predictive of advanced fibrosis in patients with nonalcoholic steatohepatitis (NASH). Among the core members of the injury-repressed gene module, we identified plasmalemma vesicle-associated protein (PLVAP) as a protein amply expressed by mouse and human HSCs. PLVAP expression was suppressed in activated HSCs upon injury and may hence define hitherto unknown roles for HSCs in the regulation of microcirculatory exchange and its breakdown in chronic liver disease. Our study offers a single-cell resolved account of drug-induced injury of the mammalian liver and identifies key genes that may serve important roles in sinusoidal integrity and as markers of advanced fibrosis in human NASH. |
Author | Sorensen, Grith L. Ravnskjaer, Kim Mandrup, Susanne Bendixen, Sofie M. Krag, Aleksander Natarajan, Kedar N. Scott, Emma A.H. Dimke, Henrik Hansen, Daniel Andersen, Thomas L. Schlosser, Anders Detlefsen, Sönke Moeller, Andreas F. Nielsen, Ronni Terkelsen, Mike K. |
AuthorAffiliation | 2 Center for Functional Genomics and Tissue Plasticity (ATLAS) University of Southern Denmark Odense M Denmark 5 Department of Pathology Odense University Hospital Odense C Denmark 6 Department of Gastroenterology and Hepatology Odense University Hospital Odense C Denmark 1 Department of Biochemistry and Molecular Biology University of Southern Denmark Odense M Denmark 7 Department of Nephrology Odense University Hospital Odense C Denmark 4 Department of Clinical Research University of Southern Denmark Odense C Denmark 3 Department of Molecular Medicine University of Southern Denmark Odense C Denmark 8 Danish Institute for Advanced Study University of Southern Denmark Odense M Denmark |
AuthorAffiliation_xml | – name: 2 Center for Functional Genomics and Tissue Plasticity (ATLAS) University of Southern Denmark Odense M Denmark – name: 4 Department of Clinical Research University of Southern Denmark Odense C Denmark – name: 5 Department of Pathology Odense University Hospital Odense C Denmark – name: 6 Department of Gastroenterology and Hepatology Odense University Hospital Odense C Denmark – name: 1 Department of Biochemistry and Molecular Biology University of Southern Denmark Odense M Denmark – name: 8 Danish Institute for Advanced Study University of Southern Denmark Odense M Denmark – name: 7 Department of Nephrology Odense University Hospital Odense C Denmark – name: 3 Department of Molecular Medicine University of Southern Denmark Odense C Denmark |
Author_xml | – sequence: 1 givenname: Mike K. orcidid: 0000-0002-5478-7895 surname: Terkelsen fullname: Terkelsen, Mike K. organization: University of Southern Denmark – sequence: 2 givenname: Sofie M. orcidid: 0000-0001-9510-941X surname: Bendixen fullname: Bendixen, Sofie M. organization: University of Southern Denmark – sequence: 3 givenname: Daniel surname: Hansen fullname: Hansen, Daniel organization: University of Southern Denmark – sequence: 4 givenname: Emma A.H. surname: Scott fullname: Scott, Emma A.H. organization: University of Southern Denmark – sequence: 5 givenname: Andreas F. orcidid: 0000-0002-4073-5568 surname: Moeller fullname: Moeller, Andreas F. organization: University of Southern Denmark – sequence: 6 givenname: Ronni surname: Nielsen fullname: Nielsen, Ronni organization: University of Southern Denmark – sequence: 7 givenname: Susanne orcidid: 0000-0002-0961-5787 surname: Mandrup fullname: Mandrup, Susanne organization: University of Southern Denmark – sequence: 8 givenname: Anders surname: Schlosser fullname: Schlosser, Anders organization: University of Southern Denmark – sequence: 9 givenname: Thomas L. orcidid: 0000-0002-6981-7276 surname: Andersen fullname: Andersen, Thomas L. organization: Odense University Hospital – sequence: 10 givenname: Grith L. orcidid: 0000-0002-5273-1097 surname: Sorensen fullname: Sorensen, Grith L. organization: University of Southern Denmark – sequence: 11 givenname: Aleksander orcidid: 0000-0002-9598-4932 surname: Krag fullname: Krag, Aleksander organization: Odense University Hospital – sequence: 12 givenname: Kedar N. orcidid: 0000-0002-9264-1280 surname: Natarajan fullname: Natarajan, Kedar N. organization: University of Southern Denmark – sequence: 13 givenname: Sönke orcidid: 0000-0002-9466-2333 surname: Detlefsen fullname: Detlefsen, Sönke organization: Odense University Hospital – sequence: 14 givenname: Henrik orcidid: 0000-0002-9170-2168 surname: Dimke fullname: Dimke, Henrik organization: Odense University Hospital – sequence: 15 givenname: Kim orcidid: 0000-0002-5322-3887 surname: Ravnskjaer fullname: Ravnskjaer, Kim email: ravnskjaer@bmb.sdu.dk organization: University of Southern Denmark |
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ContentType | Journal Article |
Copyright | 2020 The Authors. Hepatology published by Wiley Periodicals, Inc., on behalf of American Association for the Study of Liver Diseases. 2020. This article is published under http://creativecommons.org/licenses/by-nc/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Supported by the National Danish Research Foundation and the University of Southern Denmark (ATLAS; M.K.T., S.M.B., R.N., S.M., A.K., K.R.), the Villum Foundation (K.N.N.), the Danish Institute for Advanced Study (K.N.N.), the Fuhrmann Foundation (D.H.), the Villum Foundation (K.N.N.), the Danish Institute for Advanced Study (K.N.N.), the Independent Research Fund Denmark (H.D., K.R.), the European Commission's Marie Skłodowska‐Curie Action (K.R.), and the European Foundation for the Study of Diabetes (K.R.). These authors contributed equally to this work. Potential conflict of interest: Nothing to report. |
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Snippet | Background and Aims
Hepatic sinusoidal cells are known actors in the fibrogenic response to injury. Activated hepatic stellate cells (HSCs), liver sinusoidal... Hepatic sinusoidal cells are known actors in the fibrogenic response to injury. Activated hepatic stellate cells (HSCs), liver sinusoidal endothelial cells,... Background and AimsHepatic sinusoidal cells are known actors in the fibrogenic response to injury. Activated hepatic stellate cells (HSCs), liver sinusoidal... BACKGROUND AND AIMSHepatic sinusoidal cells are known actors in the fibrogenic response to injury. Activated hepatic stellate cells (HSCs), liver sinusoidal... |
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SubjectTerms | Animals Biopsy Capillaries - cytology Capillaries - pathology Carbon Tetrachloride - administration & dosage Carbon Tetrachloride - toxicity Cell activation Chemical and Drug Induced Liver Injury - etiology Chemical and Drug Induced Liver Injury - pathology Disease Models, Animal Endothelial cells Endothelial Cells - pathology Endothelium, Vascular - cytology Endothelium, Vascular - pathology Female Fibrosis Gene Regulatory Networks Genes Hepatic Veins - cytology Hepatic Veins - pathology Hepatocytes Hepatology Humans Kupffer cells Liver Liver - blood supply Liver - pathology Liver Cirrhosis - genetics Liver Cirrhosis - pathology Liver diseases Membrane Proteins - genetics Mice Mice, Transgenic Non-alcoholic Fatty Liver Disease - pathology Oligonucleotide Array Sequence Analysis Original Plasma membranes RNA-Seq Single-Cell Analysis Stellate cells Transcription |
Title | Transcriptional Dynamics of Hepatic Sinusoid‐Associated Cells After Liver Injury |
URI | https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fhep.31215 https://www.ncbi.nlm.nih.gov/pubmed/32145072 https://www.proquest.com/docview/2472247271 https://search.proquest.com/docview/2374341189 https://pubmed.ncbi.nlm.nih.gov/PMC7820956 |
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