Epithelial splicing regulatory protein 2–mediated alternative splicing reprograms hepatocytes in severe alcoholic hepatitis
Open accessAbstract
Severe alcoholic hepatitis (SAH) is a deadly liver disease without an effective medical therapy. Although SAH mortality is known to correlate with hepatic accumulation of immature liver cells, why this occurs and how it causes death are unclear. Here, we demonstrate that expression of epithelial splicing regulatory protein 2 (ESRP2), an RNA-splicing factor that maintains the nonproliferative, mature phenotype of adult hepatocytes, was suppressed in both human SAH and various mouse models of SAH in parallel with the severity of alcohol consumption and liver damage. Inflammatory cytokines released by excessive alcohol ingestion reprogrammed adult hepatocytes into proliferative, fetal-like cells by suppressing ESRP2. Sustained loss of ESRP2 permitted reemergence of a fetal RNA-splicing program that attenuates the Hippo signaling pathway and thus allows fetal transcriptional regulators to accumulate in adult liver. We further showed that depleting ESRP2 in mice exacerbated alcohol-induced steatohepatitis, enabling surviving hepatocytes to shed adult hepatocyte functions and become more regenerative, but threatening overall survival by populating the liver with functionally immature hepatocytes. Our findings revealed a mechanism that explains why liver failure develops in patients with the clinical syndrome of SAH, suggesting that recovery from SAH might be improved by limiting adult-to-fetal reprogramming in hepatocytes.
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Inflammatory cytokines such as tumor necrosis factor or IL1B are common drivers of hepatocyte dedifferentiation and dysfunction.
“inflammatory cytokines such as tumor necrosis factor or IL1B are well‐established common drivers of hepatocyte dedifferentiation and dysfunction (Del Campo et al, 2018; Hyun et al, 2020).”
From An extended transcription factor regulatory network controls hepatocyte identity (2023) · cites this paper as Hyun et al, 2020
The paper reports that TNF-α and IL-1β make hepatocytes fetal-like by suppressing the ESRP2-mediated adult splicing program (April 2020 issue, Figure 5 discussion). It also reports impaired ammonia detoxification in cytokine-reprogrammed hepatocytes (Figure 6 discussion). These findings support dedifferentiation and dysfunction, but the paper does not establish that the cytokines are well-established, common drivers of those outcomes across settings. (LLM, conf=0.86)
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Dysregulated RNA splicing induces regeneration failure in alcohol-associated liver diseasePreprint
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Equal opportunity offer for all hepatocytes
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- Authors
- Hyun, J., Sun, Z., Ahmadi, A. R., Bangru, S., Chembazhi, U. V., Du, K., Chen, T., Tsukamoto, H., Rusyn, I., Kalsotra, A., & Diehl, A. M.
- Affiliations
- Duke University (US)
- Johns Hopkins University (US)
- University of Illinois Urbana-Champaign (US)
- Duke University Health System (US)
- University of Southern California (US)
- Texas A&M University (US)
- Corresponding author
- Kalsotra, Auinash
- Diehl, Anna Mae
- ORCID
- Venue
- Journal of Clinical Investigation
- Published
- 2020-03-16
- Volume
- 130
- Issue
- 4
- Pages
- 2129-2145
- ISSN
- 0021-9738 (ISSN-L)
- 1558-8238
- PMC
- PMC7108908
- OpenAlex
- W3000151207
- Cited by
- 76
- References
- 81
- Citations by year
- 2026: 3 · 2025: 15 · 2024: 14 · 2023: 14 · 2022: 10 · 2021: 16 · 2020: 4
- FWCI
- 6.47
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Clinical Investigation (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- NIH (DK106633,AA010154,DK077794, HL126845, AA025017, T32-EB019944)
- Duke University (Florence McAlister Professorship of Medicine)
- Cancer Center at Illinois (Planning Grant Award)
- Duke Regeneration Next Initiative (postdoc fellowship)
- Topics
- Health Sciences › Medicine › Hepatology › Liver physiology and pathology
- Health Sciences › Medicine › Pathology and Forensic Medicine › Alcohol Consumption and Health Effects
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Keywords
- severe alcoholic hepatitis, ESRP2, alternative splicing, hepatocyte reprogramming, Hippo signaling pathway, steatohepatitis, liver failure, inflammatory cytokines, RNA splicing regulation, hepatocyte proliferation
- MeSH terms
- Animals, Cell Line, Cell Survival, Disease Models, Animal, Female, Hepatitis, Alcoholic, Humans, Male, Severity of Illness Index, Signal Transduction, RNA-Binding Proteins, Alternative Splicing, Mice, Knockout, Hepatocytes, Mice, Cellular Reprogramming
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