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Single-cell, single-nucleus, and spatial transcriptomics characterization of the immunological landscape in the healthy and PSC human liver.

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Τίτλος: Single-cell, single-nucleus, and spatial transcriptomics characterization of the immunological landscape in the healthy and PSC human liver.
Συγγραφείς: Andrews TS; Ajmera Transplant Centre, Toronto General Research Institute, University Health Network, Toronto, ON, M5G 2C4, Canada; Department of Biochemistry, Schulich School of Medicine and Dentistry, University of Western Ontario, London, ON, N6A 5C1, Canada; Department of Computer Science, University of Western Ontario, London, ON, N6A 3K7, Canada. Electronic address: tandrew6@uwo.ca., Nakib D; Ajmera Transplant Centre, Toronto General Research Institute, University Health Network, Toronto, ON, M5G 2C4, Canada; Department of Immunology, University of Toronto, Toronto, ON, M5S 1A8, Canada. Electronic address: diana.nakib@mail.utoronto.ca., Perciani CT; Ajmera Transplant Centre, Toronto General Research Institute, University Health Network, Toronto, ON, M5G 2C4, Canada; Department of Immunology, University of Toronto, Toronto, ON, M5S 1A8, Canada; Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, ON, M5G 1L7, Canada., Ma XZ; Ajmera Transplant Centre, Toronto General Research Institute, University Health Network, Toronto, ON, M5G 2C4, Canada., Liu L; Ajmera Transplant Centre, Toronto General Research Institute, University Health Network, Toronto, ON, M5G 2C4, Canada; Department of Immunology, University of Toronto, Toronto, ON, M5S 1A8, Canada., Winter E; Ajmera Transplant Centre, Toronto General Research Institute, University Health Network, Toronto, ON, M5G 2C4, Canada., Camat D; Ajmera Transplant Centre, Toronto General Research Institute, University Health Network, Toronto, ON, M5G 2C4, Canada; Department of Immunology, University of Toronto, Toronto, ON, M5S 1A8, Canada., Chung SW; Ajmera Transplant Centre, Toronto General Research Institute, University Health Network, Toronto, ON, M5G 2C4, Canada; Department of Immunology, University of Toronto, Toronto, ON, M5S 1A8, Canada., Lumanto P; Ajmera Transplant Centre, Toronto General Research Institute, University Health Network, Toronto, ON, M5G 2C4, Canada; Department of Immunology, University of Toronto, Toronto, ON, M5S 1A8, Canada., Manuel J; Ajmera Transplant Centre, Toronto General Research Institute, University Health Network, Toronto, ON, M5G 2C4, Canada., Mangroo S; Division of Gastroenterology, Hepatology and Nutrition, The Hospital for Sick Children, Toronto, ON, M5G 1X8, Canada., Hansen B; Toronto Centre for Liver Disease, University Health Network, Toronto, ON, M5G 2C4, Canada; Institute of Health Policy, Management and Evaluation, University of Toronto, Toronto, ON, M5T 3M6, Canada., Arpinder B; Ajmera Transplant Centre, Toronto General Research Institute, University Health Network, Toronto, ON, M5G 2C4, Canada., Thoeni C; Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, ON, M5G 1L7, Canada., Sayed B; Ajmera Transplant Centre, Toronto General Research Institute, University Health Network, Toronto, ON, M5G 2C4, Canada., Feld J; Toronto Centre for Liver Disease, University Health Network, Toronto, ON, M5G 2C4, Canada., Gehring A; Department of Immunology, University of Toronto, Toronto, ON, M5S 1A8, Canada; Toronto Centre for Liver Disease, University Health Network, Toronto, ON, M5G 2C4, Canada., Gulamhusein A; Toronto Centre for Liver Disease, University Health Network, Toronto, ON, M5G 2C4, Canada., Hirschfield GM; Toronto Centre for Liver Disease, University Health Network, Toronto, ON, M5G 2C4, Canada., Ricciuto A; Division of Gastroenterology, Hepatology and Nutrition, The Hospital for Sick Children, Toronto, ON, M5G 1X8, Canada., Bader GD; The Donnelly Centre, University of Toronto, Toronto, ON, M5S 3E1, Canada. Electronic address: gary.bader@utoronto.ca., McGilvray ID; Ajmera Transplant Centre, Toronto General Research Institute, University Health Network, Toronto, ON, M5G 2C4, Canada. Electronic address: Ian.Mcgilvray@uhn.ca., MacParland S; Ajmera Transplant Centre, Toronto General Research Institute, University Health Network, Toronto, ON, M5G 2C4, Canada; Department of Immunology, University of Toronto, Toronto, ON, M5S 1A8, Canada; Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, ON, M5G 1L7, Canada. Electronic address: s.macparland@utoronto.ca.
Πηγή: Journal of hepatology [J Hepatol] 2024 May; Vol. 80 (5), pp. 730-743. Date of Electronic Publication: 2024 Jan 08.
Τύπος έκδοσης: Journal Article; Research Support, Non-U.S. Gov't
Γλώσσα: English
Στοιχεία περιοδικού: Publisher: Elsevier Country of Publication: Netherlands NLM ID: 8503886 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1600-0641 (Electronic) Linking ISSN: 01688278 NLM ISO Abbreviation: J Hepatol Subsets: MEDLINE
Imprint Name(s): Publication: 2001- : Amsterdam : Elsevier
Original Publication: Copehnagen : Munksgaard International Publishers, [c1984-
Ιατρικοί όροι (MeSH): Cholangitis, Sclerosing*, Cicatrix/metabolism ; Cicatrix/pathology ; Liver/pathology ; Liver Cirrhosis/pathology ; Cytokines/metabolism ; Inflammation/metabolism ; Humans ; Ecosystem ; Gene Expression Profiling
Περίληψη: Background & Aims: Primary sclerosing cholangitis (PSC) is an immune-mediated cholestatic liver disease for which there is an unmet need to understand the cellular composition of the affected liver and how it underlies disease pathogenesis. We aimed to generate a comprehensive atlas of the PSC liver using multi-omic modalities and protein-based functional validation.
Methods: We employed single-cell and single-nucleus RNA sequencing (47,156 cells and 23,000 nuclei) and spatial transcriptomics (one sample by 10x Visium and five samples with Nanostring GeoMx DSP) to profile the cellular ecosystem in 10 PSC livers. Transcriptomic profiles were compared to 24 neurologically deceased donor livers (107,542 cells) and spatial transcriptomics controls, as well as 18,240 cells and 20,202 nuclei from three PBC livers. Flow cytometry was performed to validate PSC-specific differences in immune cell phenotype and function.
Results: PSC explants with parenchymal cirrhosis and prominent periductal fibrosis contained a population of cholangiocyte-like hepatocytes that were surrounded by diverse immune cell populations. PSC-associated biliary, mesenchymal, and endothelial populations expressed chemokine and cytokine transcripts involved in immune cell recruitment. Additionally, expanded CD4+ T cells and recruited myeloid populations in the PSC liver expressed the corresponding receptors to these chemokines and cytokines, suggesting potential recruitment. Tissue-resident macrophages, by contrast, were reduced in number and exhibited a dysfunctional and downregulated inflammatory response to lipopolysaccharide and interferon-γ stimulation.
Conclusions: We present a comprehensive atlas of the PSC liver and demonstrate an exhaustion-like phenotype of myeloid cells and markers of chronic cytokine expression in late-stage PSC lesions. This atlas expands our understanding of the cellular complexity of PSC and has potential to guide the development of novel treatments.
Impact and Implications: Primary sclerosing cholangitis (PSC) is a rare liver disease characterized by chronic inflammation and irreparable damage to the bile ducts, which eventually results in liver failure. Due to a limited understanding of the underlying pathogenesis of disease, treatment options are limited. To address this, we sequenced healthy and diseased livers to compare the activity, interactions, and localization of immune and non-immune cells. This revealed that hepatocytes lining PSC scar regions co-express cholangiocyte markers, whereas immune cells infiltrate the scar lesions. Of these cells, macrophages, which typically contribute to tissue repair, were enriched in immunoregulatory genes and demonstrated a lack of responsiveness to stimulation. These cells may be involved in maintaining hepatic inflammation and could be a target for novel therapies.
(Copyright © 2024 The Author(s). Published by Elsevier B.V. All rights reserved.)
Contributed Indexing: Keywords: Liver; Myeloid Dysfunction; Primary Sclerosing Cholangitis; Single Cell RNA sequencing; Spatial Transcriptomics
Substance Nomenclature: 0 (Cytokines)
Entry Date(s): Date Created: 20240110 Date Completed: 20240422 Latest Revision: 20250815
Update Code: 20260130
DOI: 10.1016/j.jhep.2023.12.023
PMID: 38199298
Βάση Δεδομένων: MEDLINE
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  Data: Single-cell, single-nucleus, and spatial transcriptomics characterization of the immunological landscape in the healthy and PSC human liver.
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  Data: <searchLink fieldCode="AU" term="%22Andrews+TS%22">Andrews TS</searchLink>; Ajmera Transplant Centre, Toronto General Research Institute, University Health Network, Toronto, ON, M5G 2C4, Canada; Department of Biochemistry, Schulich School of Medicine and Dentistry, University of Western Ontario, London, ON, N6A 5C1, Canada; Department of Computer Science, University of Western Ontario, London, ON, N6A 3K7, Canada. Electronic address: tandrew6@uwo.ca.<br /><searchLink fieldCode="AU" term="%22Nakib+D%22">Nakib D</searchLink>; Ajmera Transplant Centre, Toronto General Research Institute, University Health Network, Toronto, ON, M5G 2C4, Canada; Department of Immunology, University of Toronto, Toronto, ON, M5S 1A8, Canada. Electronic address: diana.nakib@mail.utoronto.ca.<br /><searchLink fieldCode="AU" term="%22Perciani+CT%22">Perciani CT</searchLink>; Ajmera Transplant Centre, Toronto General Research Institute, University Health Network, Toronto, ON, M5G 2C4, Canada; Department of Immunology, University of Toronto, Toronto, ON, M5S 1A8, Canada; Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, ON, M5G 1L7, Canada.<br /><searchLink fieldCode="AU" term="%22Ma+XZ%22">Ma XZ</searchLink>; Ajmera Transplant Centre, Toronto General Research Institute, University Health Network, Toronto, ON, M5G 2C4, Canada.<br /><searchLink fieldCode="AU" term="%22Liu+L%22">Liu L</searchLink>; Ajmera Transplant Centre, Toronto General Research Institute, University Health Network, Toronto, ON, M5G 2C4, Canada; Department of Immunology, University of Toronto, Toronto, ON, M5S 1A8, Canada.<br /><searchLink fieldCode="AU" term="%22Winter+E%22">Winter E</searchLink>; Ajmera Transplant Centre, Toronto General Research Institute, University Health Network, Toronto, ON, M5G 2C4, Canada.<br /><searchLink fieldCode="AU" term="%22Camat+D%22">Camat D</searchLink>; Ajmera Transplant Centre, Toronto General Research Institute, University Health Network, Toronto, ON, M5G 2C4, Canada; Department of Immunology, University of Toronto, Toronto, ON, M5S 1A8, Canada.<br /><searchLink fieldCode="AU" term="%22Chung+SW%22">Chung SW</searchLink>; Ajmera Transplant Centre, Toronto General Research Institute, University Health Network, Toronto, ON, M5G 2C4, Canada; Department of Immunology, University of Toronto, Toronto, ON, M5S 1A8, Canada.<br /><searchLink fieldCode="AU" term="%22Lumanto+P%22">Lumanto P</searchLink>; Ajmera Transplant Centre, Toronto General Research Institute, University Health Network, Toronto, ON, M5G 2C4, Canada; Department of Immunology, University of Toronto, Toronto, ON, M5S 1A8, Canada.<br /><searchLink fieldCode="AU" term="%22Manuel+J%22">Manuel J</searchLink>; Ajmera Transplant Centre, Toronto General Research Institute, University Health Network, Toronto, ON, M5G 2C4, Canada.<br /><searchLink fieldCode="AU" term="%22Mangroo+S%22">Mangroo S</searchLink>; Division of Gastroenterology, Hepatology and Nutrition, The Hospital for Sick Children, Toronto, ON, M5G 1X8, Canada.<br /><searchLink fieldCode="AU" term="%22Hansen+B%22">Hansen B</searchLink>; Toronto Centre for Liver Disease, University Health Network, Toronto, ON, M5G 2C4, Canada; Institute of Health Policy, Management and Evaluation, University of Toronto, Toronto, ON, M5T 3M6, Canada.<br /><searchLink fieldCode="AU" term="%22Arpinder+B%22">Arpinder B</searchLink>; Ajmera Transplant Centre, Toronto General Research Institute, University Health Network, Toronto, ON, M5G 2C4, Canada.<br /><searchLink fieldCode="AU" term="%22Thoeni+C%22">Thoeni C</searchLink>; Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, ON, M5G 1L7, Canada.<br /><searchLink fieldCode="AU" term="%22Sayed+B%22">Sayed B</searchLink>; Ajmera Transplant Centre, Toronto General Research Institute, University Health Network, Toronto, ON, M5G 2C4, Canada.<br /><searchLink fieldCode="AU" term="%22Feld+J%22">Feld J</searchLink>; Toronto Centre for Liver Disease, University Health Network, Toronto, ON, M5G 2C4, Canada.<br /><searchLink fieldCode="AU" term="%22Gehring+A%22">Gehring A</searchLink>; Department of Immunology, University of Toronto, Toronto, ON, M5S 1A8, Canada; Toronto Centre for Liver Disease, University Health Network, Toronto, ON, M5G 2C4, Canada.<br /><searchLink fieldCode="AU" term="%22Gulamhusein+A%22">Gulamhusein A</searchLink>; Toronto Centre for Liver Disease, University Health Network, Toronto, ON, M5G 2C4, Canada.<br /><searchLink fieldCode="AU" term="%22Hirschfield+GM%22">Hirschfield GM</searchLink>; Toronto Centre for Liver Disease, University Health Network, Toronto, ON, M5G 2C4, Canada.<br /><searchLink fieldCode="AU" term="%22Ricciuto+A%22">Ricciuto A</searchLink>; Division of Gastroenterology, Hepatology and Nutrition, The Hospital for Sick Children, Toronto, ON, M5G 1X8, Canada.<br /><searchLink fieldCode="AU" term="%22Bader+GD%22">Bader GD</searchLink>; The Donnelly Centre, University of Toronto, Toronto, ON, M5S 3E1, Canada. Electronic address: gary.bader@utoronto.ca.<br /><searchLink fieldCode="AU" term="%22McGilvray+ID%22">McGilvray ID</searchLink>; Ajmera Transplant Centre, Toronto General Research Institute, University Health Network, Toronto, ON, M5G 2C4, Canada. Electronic address: Ian.Mcgilvray@uhn.ca.<br /><searchLink fieldCode="AU" term="%22MacParland+S%22">MacParland S</searchLink>; Ajmera Transplant Centre, Toronto General Research Institute, University Health Network, Toronto, ON, M5G 2C4, Canada; Department of Immunology, University of Toronto, Toronto, ON, M5S 1A8, Canada; Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, ON, M5G 1L7, Canada. Electronic address: s.macparland@utoronto.ca.
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  Data: <searchLink fieldCode="JN" term="%228503886%22">Journal of hepatology</searchLink> [J Hepatol] 2024 May; Vol. 80 (5), pp. 730-743. <i>Date of Electronic Publication: </i>2024 Jan 08.
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  Data: <i>Publisher: </i><searchLink fieldCode="PB" term="%22Elsevier%22">Elsevier </searchLink><i>Country of Publication: </i>Netherlands <i>NLM ID: </i>8503886 <i>Publication Model: </i>Print-Electronic <i>Cited Medium: </i>Internet <i>ISSN: </i>1600-0641 (Electronic) <i>Linking ISSN: </i><searchLink fieldCode="IS" term="%2201688278%22">01688278 </searchLink><i>NLM ISO Abbreviation: </i>J Hepatol <i>Subsets: </i>MEDLINE
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  Data: <searchLink fieldCode="MM" term="%22Cholangitis%2C+Sclerosing%22">Cholangitis, Sclerosing*</searchLink><br /><searchLink fieldCode="MH" term="%22Cicatrix%22">Cicatrix</searchLink>/<searchLink fieldCode="MH" term="%22Cicatrix+metabolism%22">metabolism</searchLink> ; <searchLink fieldCode="MH" term="%22Cicatrix%22">Cicatrix</searchLink>/<searchLink fieldCode="MH" term="%22Cicatrix+pathology%22">pathology</searchLink> ; <searchLink fieldCode="MH" term="%22Liver%22">Liver</searchLink>/<searchLink fieldCode="MH" term="%22Liver+pathology%22">pathology</searchLink> ; <searchLink fieldCode="MH" term="%22Liver+Cirrhosis%22">Liver Cirrhosis</searchLink>/<searchLink fieldCode="MH" term="%22Liver+Cirrhosis+pathology%22">pathology</searchLink> ; <searchLink fieldCode="MH" term="%22Cytokines%22">Cytokines</searchLink>/<searchLink fieldCode="MH" term="%22Cytokines+metabolism%22">metabolism</searchLink> ; <searchLink fieldCode="MH" term="%22Inflammation%22">Inflammation</searchLink>/<searchLink fieldCode="MH" term="%22Inflammation+metabolism%22">metabolism</searchLink> ; <searchLink fieldCode="MH" term="%22Humans%22">Humans</searchLink> ; <searchLink fieldCode="MH" term="%22Ecosystem%22">Ecosystem</searchLink> ; <searchLink fieldCode="MH" term="%22Gene+Expression+Profiling%22">Gene Expression Profiling</searchLink>
– Name: Abstract
  Label: Abstract
  Group: Ab
  Data: Background & Aims: Primary sclerosing cholangitis (PSC) is an immune-mediated cholestatic liver disease for which there is an unmet need to understand the cellular composition of the affected liver and how it underlies disease pathogenesis. We aimed to generate a comprehensive atlas of the PSC liver using multi-omic modalities and protein-based functional validation.<br />Methods: We employed single-cell and single-nucleus RNA sequencing (47,156 cells and 23,000 nuclei) and spatial transcriptomics (one sample by 10x Visium and five samples with Nanostring GeoMx DSP) to profile the cellular ecosystem in 10 PSC livers. Transcriptomic profiles were compared to 24 neurologically deceased donor livers (107,542 cells) and spatial transcriptomics controls, as well as 18,240 cells and 20,202 nuclei from three PBC livers. Flow cytometry was performed to validate PSC-specific differences in immune cell phenotype and function.<br />Results: PSC explants with parenchymal cirrhosis and prominent periductal fibrosis contained a population of cholangiocyte-like hepatocytes that were surrounded by diverse immune cell populations. PSC-associated biliary, mesenchymal, and endothelial populations expressed chemokine and cytokine transcripts involved in immune cell recruitment. Additionally, expanded CD4<superscript>+</superscript> T cells and recruited myeloid populations in the PSC liver expressed the corresponding receptors to these chemokines and cytokines, suggesting potential recruitment. Tissue-resident macrophages, by contrast, were reduced in number and exhibited a dysfunctional and downregulated inflammatory response to lipopolysaccharide and interferon-γ stimulation.<br />Conclusions: We present a comprehensive atlas of the PSC liver and demonstrate an exhaustion-like phenotype of myeloid cells and markers of chronic cytokine expression in late-stage PSC lesions. This atlas expands our understanding of the cellular complexity of PSC and has potential to guide the development of novel treatments.<br />Impact and Implications: Primary sclerosing cholangitis (PSC) is a rare liver disease characterized by chronic inflammation and irreparable damage to the bile ducts, which eventually results in liver failure. Due to a limited understanding of the underlying pathogenesis of disease, treatment options are limited. To address this, we sequenced healthy and diseased livers to compare the activity, interactions, and localization of immune and non-immune cells. This revealed that hepatocytes lining PSC scar regions co-express cholangiocyte markers, whereas immune cells infiltrate the scar lesions. Of these cells, macrophages, which typically contribute to tissue repair, were enriched in immunoregulatory genes and demonstrated a lack of responsiveness to stimulation. These cells may be involved in maintaining hepatic inflammation and could be a target for novel therapies.<br /> (Copyright © 2024 The Author(s). Published by Elsevier B.V. All rights reserved.)
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  Data: <i>Keywords: </i>Liver; Myeloid Dysfunction; Primary Sclerosing Cholangitis; Single Cell RNA sequencing; Spatial Transcriptomics
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        Type: general
      – SubjectFull: Cicatrix pathology
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