An autocrine signaling circuit in hepatic stellate cells underlies advanced fibrosis in nonalcoholic steatohepatitis
Open accessAbstract
Advanced hepatic fibrosis, driven by the activation of hepatic stellate cells (HSCs), affects millions worldwide and is the strongest predictor of mortality in nonalcoholic steatohepatitis (NASH); however, there are no approved antifibrotic therapies. To identify antifibrotic drug targets, we integrated progressive transcriptomic and morphological responses that accompany HSC activation in advanced disease using single-nucleus RNA sequencing and tissue clearing in a robust murine NASH model. In advanced fibrosis, we found that an autocrine HSC signaling circuit emerged that was composed of 68 receptor-ligand interactions conserved between murine and human NASH. These predicted interactions were supported by the parallel appearance of markedly increased direct stellate cell-cell contacts in murine NASH. As proof of principle, pharmacological inhibition of one such autocrine interaction, neurotrophic receptor tyrosine kinase 3–neurotrophin 3, inhibited human HSC activation in culture and reversed advanced murine NASH fibrosis. In summary, we uncovered a repertoire of antifibrotic drug targets underlying advanced fibrosis in vivo. The findings suggest a therapeutic paradigm in which stage-specific therapies could yield enhanced antifibrotic efficacy in patients with advanced hepatic fibrosis.
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Recent single-cell human liver studies have largely focused on chronic liver disease rather than ALF, with emphasis on non-parenchymal cell populations.
“Recent single-cell human liver studies have largely focused on chronic liver disease rather than ALF, with emphasis on non-parenchymal cell populations7–9”
From Multimodal decoding of human liver regeneration (2024) · cites this paper as [9]
Our single-nuclear RNA-seq in murine MASH models and MASH patients showed enrichment of myofibroblast pathways regulating ECM production and cell migration, including MMPs, TIMPs, and LOXLs.
“We recently used single nuclear RNA-seq in murine MASH models and patients with MASH to demonstrate enrichment of pathways in myofibroblasts that regulate extracellular matrix production and cell migration, including matrix metalloproteinase (MMPs), tissue inhibitors of metalloproteinases (TIMPs), and lysyl oxidases (LOXLs) (47-49), similar to earlier studies of mouse fibrosis and human cirrhosis”
From Found in translation—Fibrosis in metabolic dysfunction–associated steatohepatitis (MASH) (2023) · cites this paper as [48]
Our single-nucleus RNA-seq profiling of FAT-MASH macrophages showed no enrichment of ECM-related pathways, only induction of MMP2, MMP12, and MMP14 and decreased COL18A1.
“Our profiling of FAT-MASH macrophages using single nucleus RNA-seq showed no enrichment of ECM-related pathways, only induction of a few select matrix metalloproteinases (MMP2, matrix metalloproteinase 12 (MMP12), matrix metalloproteinase 14 (MMP14)) and decreased collagen type 18 alpha 1 (COL18A1) (48).”
From Found in translation—Fibrosis in metabolic dysfunction–associated steatohepatitis (MASH) (2023) · cites this paper as [48]
Detection of both quiescent and activated HSCs in mouse liver injury models by single-cell RNA-seq supports HSC activation as a driver of fibrosis across etiologies, including MASH.
“The detection of both quiescent and activated HSCs in mouse liver injury models using single cell RNA-seq reinforces HSC activation as a driver of fibrosis common across etiologies that includes MASH (46-50).”
From Found in translation—Fibrosis in metabolic dysfunction–associated steatohepatitis (MASH) (2023) · cites this paper as [48]
Although activated HSCs are the primary fibrogenic cells in MASH, single-cell methods have identified an expanded list of fibrogenic drivers expressed by activated HSCs that could be antifibrotic drug targets.
“Although activated HSCs are the primary fibrogenic cells in MASH, these methods have identified an expanded list of fibrogenic drivers expressed by activated HSCs that could represent antifibrotic drug targets (42, 48, 49, 125).”
From Found in translation—Fibrosis in metabolic dysfunction–associated steatohepatitis (MASH) (2023) · cites this paper as [48]
Differential ligand-receptor signaling pairs suggest that disease drivers and signaling events may change as disease advances, so advanced fibrotic stages may respond to different pharmacotherapies than earlier stages.
“These different communication networks are reflected in the differential expression of ligand-receptor signaling pairs, suggesting that the repertoire of disease drivers – and therefore the underlying signaling events – may change as the disease advances, such that advanced fibrotic stages may respond to different pharmacotherapies than earlier stages (48, 49).”
From Found in translation—Fibrosis in metabolic dysfunction–associated steatohepatitis (MASH) (2023) · cites this paper as [48]
Applying informatic tools and databases uncovered an altered cell-cell communication network in MASH based on differential ligand and receptor expression across cell types.
“Applying recent developments in informatic tools and databases (130, 131) has uncovered an altered cell-cell communication network in MASH based on the differential expression of ligands and receptors in different cell types (48, 49).”
From Found in translation—Fibrosis in metabolic dysfunction–associated steatohepatitis (MASH) (2023) · cites this paper as [48]
FAT-MASH mice exhibit transcriptomic similarities to human MASH patients.
“It is worth noting that the FAT-MASH mice exhibit transcriptomic similarities to human MASH patients (48), and their microbiome changes also resemble human MASH pathology (197).”
From Found in translation—Fibrosis in metabolic dysfunction–associated steatohepatitis (MASH) (2023) · cites this paper as [48]
Several robust platforms using machine or deep learning have been established to quantify the amount of scar and structural features of extracellular matrix that may reflect progression or regression.
“To improve the quantitative measurement of fibrosis in liver biopsies, several robust platforms have been established that leverage machine or deep learning to precisely quantify not only the amount of scar, but also structural features of the extracellular matrix that may reflect progression or regression (48, 258, 290, 291).”
From Found in translation—Fibrosis in metabolic dysfunction–associated steatohepatitis (MASH) (2023) · cites this paper as [48]
Identification of HSC subpopulations that are the main fibrosis drivers will lead to more targeted, safer therapies.
“3) Identification of HSC subpopulations that are the main fibrosis drivers will lead to more targeted, safer therapies (42, 48).”
From Found in translation—Fibrosis in metabolic dysfunction–associated steatohepatitis (MASH) (2023) · cites this paper as [48]
In advanced human or rodent liver fibrosis, HSCs interact directly with neighbouring HSCs through autocrine pathways that amplify fibrogenesis.
“In advanced (human or rodent) hepatic fibrosis, HSC directly interacts with surrounding HSCs, driven by autocrine pathways that amplify fibrogenesis.112”
From An integrated view of anti-inflammatory and antifibrotic targets for the treatment of NASH (2023) · cites this paper as [112]
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The pivotal role of dysregulated autophagy in the progression of non-alcoholic fatty liver disease
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Temporal tissue dynamics from a spatial snapshot
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Self-citationEmerging mechanisms of non-alcoholic steatohepatitis and novel drug therapies
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Smart Microneedle Arrays Integrating Cell‐Free Therapy and Nanocatalysis to Treat Liver Fibrosis
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Self-citationHepatic Stellate Cells Functional Heterogeneity in Liver Cancer
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EphB2 Receptor Promotes Dermal Fibrosis in Systemic Sclerosis
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ZBED3 exacerbates hyperglycemia by promoting hepatic gluconeogenesis through CREB signaling
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Self-citationA Critical Role for the Mitochondrial Pyruvate Carrier in Hepatic Stellate Cell Activation
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Hepatic stellate cells: From bad reputation to mediators of liver homeostasis
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Towards a reference cell atlas of liver diversity over the human lifespan
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Effect of free fatty acids on TGF-β1 mediated fibrogenesis in hepatic stellate cells
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- Authors
- Wang, S., Li, K., Pickholz, E., Dobie, R., Matchett, K. P., Henderson, N. C., Carrico, C., Driver, I., Borch Jensen, M., Chen, L., Petitjean, M., Bhattacharya, D., Fiel, M. I., Liu, X., Kisseleva, T., Alon, U., Adler, M., Medzhitov, R., & Friedman, S. L.
- Affiliations
- Icahn School of Medicine at Mount Sinai (US)
- Centre for Inflammation Research (GB)
- Gordian Biotechnology, San Francisco, CA 94107, USA.
- PharmaNest Inc., Princeton, NJ 08540, USA.
- University of California San Diego (US)
- Weizmann Institute of Science (IL)
- Yale University (US)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Friedman, Scott L.
- ORCID
- Venue
- Science Translational Medicine
- Published
- 2023-01-04
- Volume
- 15
- Issue
- 677
- Pages
- eadd3949-eadd3949
- ISSN
- 1946-6234 (ISSN-L)
- 1946-6242
- PMC
- PMC10686705
- OpenAlex
- W4313544888
- Cited by
- 176
- References
- 31
- Citations by year
- 2026: 43 · 2025: 51 · 2024: 40 · 2023: 41 · 2020: 1
- FWCI
- 29.29
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Science Translational Medicine (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- American Gastroenterological Association
- Wellcome Trust (219542/Z/19/Z)
- Cancer Research UK (A27145, 27145, C19767/A27145)
- National Institutes of Health (DK120515, UL1TR004419)
- National Institute on Alcohol Abuse and Alcoholism (U01AA029019, R01AA028550, P50AA011999)
- National Cancer Institute (P30CA196521)
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK111866, R01DK056621, R01DK128289, R01DK136016, P30DK120515, R01DK101737, R01DK099205)
- National Center for Advancing Translational Sciences
- Topics
- Health Sciences › Medicine › Hepatology › Liver physiology and pathology
- Health Sciences › Medicine › Epidemiology › Liver Disease Diagnosis and Treatment
- Health Sciences › Medicine › Hepatology › Liver Diseases and Immunity
- Keywords
- hepatic stellate cells, nonalcoholic steatohepatitis, liver fibrosis, autocrine signaling, ligand-receptor interactions, NTRK3, neurotrophin-3, stellate cell activation, single-nucleus RNA sequencing, tissue clearing
- MeSH terms
- Animals, Fibrosis, Humans, Liver, Liver Cirrhosis, Autocrine Communication, Mice, Hepatic Stellate Cells, Non-alcoholic Fatty Liver Disease
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