Transcriptional profiling of pediatric cholestatic livers identifies three distinct macrophage populations.

<h4>Background & aims</h4>Limited understanding of the role for specific macrophage subsets in the pathogenesis of cholestatic liver injury is a barrier to advancing medical therapy. Macrophages have previously been implicated in both the mal-adaptive and protective responses in obst...

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Main Authors: Sarah A Taylor, Shang-Yang Chen, Gaurav Gadhvi, Liang Feng, Kyle D Gromer, Hiam Abdala-Valencia, Kiwon Nam, Salina T Dominguez, Anna B Montgomery, Paul A Reyfman, Lorena Ostilla, Joshua B Wechsler, Carla M Cuda, Richard M Green, Harris Perlman, Deborah R Winter
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2021-01-01
Series:PLoS ONE
Online Access:https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0244743&type=printable
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author Sarah A Taylor
Shang-Yang Chen
Gaurav Gadhvi
Liang Feng
Kyle D Gromer
Hiam Abdala-Valencia
Kiwon Nam
Salina T Dominguez
Anna B Montgomery
Paul A Reyfman
Lorena Ostilla
Joshua B Wechsler
Carla M Cuda
Richard M Green
Harris Perlman
Deborah R Winter
author_facet Sarah A Taylor
Shang-Yang Chen
Gaurav Gadhvi
Liang Feng
Kyle D Gromer
Hiam Abdala-Valencia
Kiwon Nam
Salina T Dominguez
Anna B Montgomery
Paul A Reyfman
Lorena Ostilla
Joshua B Wechsler
Carla M Cuda
Richard M Green
Harris Perlman
Deborah R Winter
author_sort Sarah A Taylor
collection DOAJ
description <h4>Background & aims</h4>Limited understanding of the role for specific macrophage subsets in the pathogenesis of cholestatic liver injury is a barrier to advancing medical therapy. Macrophages have previously been implicated in both the mal-adaptive and protective responses in obstructive cholestasis. Recently two macrophage subsets were identified in non-diseased human liver; however, no studies to date fully define the heterogeneous macrophage subsets during the pathogenesis of cholestasis. Here, we aim to further characterize the transcriptional profile of macrophages in pediatric cholestatic liver disease.<h4>Methods</h4>We isolated live hepatic immune cells from patients with biliary atresia (BA), Alagille syndrome (ALGS), and non-cholestatic pediatric liver by fluorescence activated cell sorting. Through single-cell RNA sequencing analysis and immunofluorescence, we characterized cholestatic macrophages. We next compared the transcriptional profile of pediatric cholestatic and non-cholestatic macrophage populations to previously published data on normal adult hepatic macrophages.<h4>Results</h4>We identified 3 distinct macrophage populations across cholestatic liver samples and annotated them as lipid-associated macrophages, monocyte-like macrophages, and adaptive macrophages based on their transcriptional profile. Immunofluorescence of liver tissue using markers for each subset confirmed their presence across BA (n = 6) and ALGS (n = 6) patients. Cholestatic macrophages demonstrated reduced expression of immune regulatory genes as compared to normal hepatic macrophages and were distinct from macrophage populations defined in either healthy adult or pediatric non-cholestatic liver.<h4>Conclusions</h4>We are the first to perform single-cell RNA sequencing on human pediatric cholestatic liver and identified three macrophage subsets with distinct transcriptional signatures from healthy liver macrophages. Further analyses will identify similarities and differences in these macrophage sub-populations across etiologies of cholestatic liver disease. Taken together, these findings may allow for future development of targeted therapeutic strategies to reprogram macrophages to an immune regulatory phenotype and reduce cholestatic liver injury.
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spelling doaj-art-c015eb78f3cb4aa88de1330263a1b31d2025-08-20T02:41:14ZengPublic Library of Science (PLoS)PLoS ONE1932-62032021-01-01161e024474310.1371/journal.pone.0244743Transcriptional profiling of pediatric cholestatic livers identifies three distinct macrophage populations.Sarah A TaylorShang-Yang ChenGaurav GadhviLiang FengKyle D GromerHiam Abdala-ValenciaKiwon NamSalina T DominguezAnna B MontgomeryPaul A ReyfmanLorena OstillaJoshua B WechslerCarla M CudaRichard M GreenHarris PerlmanDeborah R Winter<h4>Background & aims</h4>Limited understanding of the role for specific macrophage subsets in the pathogenesis of cholestatic liver injury is a barrier to advancing medical therapy. Macrophages have previously been implicated in both the mal-adaptive and protective responses in obstructive cholestasis. Recently two macrophage subsets were identified in non-diseased human liver; however, no studies to date fully define the heterogeneous macrophage subsets during the pathogenesis of cholestasis. Here, we aim to further characterize the transcriptional profile of macrophages in pediatric cholestatic liver disease.<h4>Methods</h4>We isolated live hepatic immune cells from patients with biliary atresia (BA), Alagille syndrome (ALGS), and non-cholestatic pediatric liver by fluorescence activated cell sorting. Through single-cell RNA sequencing analysis and immunofluorescence, we characterized cholestatic macrophages. We next compared the transcriptional profile of pediatric cholestatic and non-cholestatic macrophage populations to previously published data on normal adult hepatic macrophages.<h4>Results</h4>We identified 3 distinct macrophage populations across cholestatic liver samples and annotated them as lipid-associated macrophages, monocyte-like macrophages, and adaptive macrophages based on their transcriptional profile. Immunofluorescence of liver tissue using markers for each subset confirmed their presence across BA (n = 6) and ALGS (n = 6) patients. Cholestatic macrophages demonstrated reduced expression of immune regulatory genes as compared to normal hepatic macrophages and were distinct from macrophage populations defined in either healthy adult or pediatric non-cholestatic liver.<h4>Conclusions</h4>We are the first to perform single-cell RNA sequencing on human pediatric cholestatic liver and identified three macrophage subsets with distinct transcriptional signatures from healthy liver macrophages. Further analyses will identify similarities and differences in these macrophage sub-populations across etiologies of cholestatic liver disease. Taken together, these findings may allow for future development of targeted therapeutic strategies to reprogram macrophages to an immune regulatory phenotype and reduce cholestatic liver injury.https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0244743&type=printable
spellingShingle Sarah A Taylor
Shang-Yang Chen
Gaurav Gadhvi
Liang Feng
Kyle D Gromer
Hiam Abdala-Valencia
Kiwon Nam
Salina T Dominguez
Anna B Montgomery
Paul A Reyfman
Lorena Ostilla
Joshua B Wechsler
Carla M Cuda
Richard M Green
Harris Perlman
Deborah R Winter
Transcriptional profiling of pediatric cholestatic livers identifies three distinct macrophage populations.
PLoS ONE
title Transcriptional profiling of pediatric cholestatic livers identifies three distinct macrophage populations.
title_full Transcriptional profiling of pediatric cholestatic livers identifies three distinct macrophage populations.
title_fullStr Transcriptional profiling of pediatric cholestatic livers identifies three distinct macrophage populations.
title_full_unstemmed Transcriptional profiling of pediatric cholestatic livers identifies three distinct macrophage populations.
title_short Transcriptional profiling of pediatric cholestatic livers identifies three distinct macrophage populations.
title_sort transcriptional profiling of pediatric cholestatic livers identifies three distinct macrophage populations
url https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0244743&type=printable
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