Roles of microRNA-29a in the antifibrotic effect of farnesoid X receptor in hepatic stellate cells
Open accessAbstract
Liver fibrosis is a chronic disorder that is characterized by an alteration of the balance between fibrogenesis and fibrinolysis, which results in accumulation of excessive amounts of extracellular matrix (ECM) and distortion of the normal liver architecture. The activation and transformation of quiescent hepatic stellate cells (HSCs) into myofibroblast-like cells constitute a major mechanism for the increased production of ECM in the liver. The nuclear receptor farnesoid X receptor (FXR) shows potent antifibrotic activity in HSCs and protects animals in rodent models of liver fibrosis. However, the detailed mechanism remains incompletely understood. In this study, we report that treatment with 3-[2-[2-chloro-4-[[3-(2,6-dichlorophenyl)-5-(1-methylethyl)-4-isoxazolyl]methoxy]phenyl]ethenyl]benzoic acid (GW4064), a synthetic FXR ligand, led to up-regulation of microRNA-29a (miR-29a) in HSCs isolated from wild-type mice, rats, and humans but not from FXR(-/-) mice. miR-29a seems to play an inhibitory role in the regulation of ECM production because of the following: 1) transfection of HSCs with miR-29a mimic resulted in drastic down-regulation of the mRNA expression of several genes that encode ECM proteins; and 2) miR-29a significantly inhibited the expression of a reporter expression plasmid that contains the 3'-untranslated region of the corresponding ECM genes. Our results suggest that miR-29a is a FXR target gene because miR-29a promoter activity was significantly increased by pharmacologic or genetic activation of FXR. Functional analysis of human miR-29a promoter identified an imperfect inverted repeat spaced by one nucleotide DNA motif, inverted repeat-1 (5'-AGGTCAcAGACCT-3'), as a likely FXR-responsive element that is involved in miR-29a regulation. Our study uncovers a new mechanism by which FXR negatively regulates the expression of ECM in HSCs.
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FXR activation downregulates extracellular matrix expression in hepatic stellate cells and fibrogenesis via increased miR-29a promoter activity, and inhibits endothelin-1, which would enhance pro-fibrogenic gene expression in hepatic stellate cells.
“Further consequences of FXR activation include the downregulation of ECM expression in HSCs and fibrogenesis via an increased mrR-29a promoter activity [66], and the inhibition of endothelin-1 (ET-1) [67], which would enhance pro-fibrogenic gene expression in HSCs.[68]”
From Nuclear receptors in liver fibrosis (2021) · cites this paper as [66]
FXR is expressed in HSCs where it functions as a transcription factor regulating the expression of Shp and microRNA-29a, and thereby reduces expression of pro-fibrotic genes including Acta2, Tgfb1, Col1a1, Col1a2, Timp1, and Timp2.
“FXR is expressed in HSCs where it functions as a transcription factor regulating the expression of the small heterodimer partner (Shp) gene and microRNA-29a, and thereby reduces the expression of pro-fibrotic genes, including Acta2 (encoding αSMA), transforming growth factor β1 (Tgfb1), collagen1a1 (Col1a1), Col1a2, tissue inhibitor of metalloprotease 1 (Timp1), and Timp233,34.”
From SUMOylation inhibitors synergize with FXR agonists in combating liver fibrosis (2020) · cites this paper as [34]
FXR activation leads to up-regulation of microRNA-29a in HSCs, which inhibits ECM production.
“Early studies indicated that FXR activation led to up-regulation of microRNA-29a in HSCs, which plays an inhibitory role in ECM production35.”
From Combined obeticholic acid and apoptosis inhibitor treatment alleviates liver fibrosis (2019) · cites this paper as [35]
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- Authors
- Li, J., Zhang, Y., Kuruba, R., Gao, X., Gandhi, C. R., Xie, W., & Li, S.
- Affiliations
- University of Pittsburgh (US)
- Venue
- Molecular Pharmacology
- Publisher
- Elsevier BV
- Published
- 2011-07
- Volume
- 80
- Issue
- 1
- Pages
- 191-200
- ISSN
- 0026-895X (ISSN-L)
- PMC
- PMC3127536
- OpenAlex
- W2154985027
- Cited by
- 78
- References
- 46
- Citations by year
- 2026: 3 · 2025: 1 · 2024: 1 · 2023: 3 · 2022: 4 · 2021: 8 · 2020: 2 · 2019: 7 · 2018: 3 · 2017: 5 · 2016: 8 · 2015: 8 · 2014: 8 · 2013: 10 · 2012: 5
- FWCI
- 5.07
- Type
- journal article
- Language
- en
- Update notices
- erratum (2012-08-01)
- Open access
- bronze
- doi.org
- Locations
- Molecular Pharmacology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- University of Pittsburgh
- National Institutes of Health
- National Heart, Lung, and Blood Institute (R01HL068688, HL68688, R01HL091828, HL091828-01)
- Topics
- Health Sciences › Medicine › Hepatology › Liver physiology and pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Health Sciences › Medicine › Epidemiology › Liver Disease Diagnosis and Treatment
- Keywords
- miR-29a, farnesoid X receptor, hepatic stellate cells, liver fibrosis, extracellular matrix synthesis, antifibrotic effect, GW4064, 3' untranslated region, myofibroblast activation
- MeSH terms
- Receptor, Farnesoid X-Activated, Animals, Base Sequence, Humans, Liver, Male, Mice, Inbred C57BL, Molecular Sequence Data, Blotting, Western, Polymerase Chain Reaction, Rats, Sprague-Dawley, Receptors, Cytoplasmic and Nuclear, MicroRNAs, Chromatin Immunoprecipitation, Mice, Rats
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