Maladaptive regeneration - the reawakening of developmental pathways in NASH and fibrosis
Open accessAbstract
With the rapid expansion of the obesity epidemic, nonalcoholic fatty liver disease is now the most common chronic liver disease, with almost 25% global prevalence. Nonalcoholic fatty liver disease ranges in severity from simple steatosis, a benign 'pre-disease' state, to the liver injury and inflammation that characterize nonalcoholic steatohepatitis (NASH), which in turn predisposes individuals to liver fibrosis. Fibrosis is the major determinant of clinical outcomes in patients with NASH and is associated with increased risks of cirrhosis and hepatocellular carcinoma. NASH has no approved therapies, and liver fibrosis shows poor response to existing pharmacotherapy, in part due to an incomplete understanding of the underlying pathophysiology. Patient and mouse data have shown that NASH is associated with the activation of developmental pathways: Notch, Hedgehog and Hippo-YAP-TAZ. Although these evolutionarily conserved fundamental signals are known to determine liver morphogenesis during development, new data have shown a coordinated and causal role for these pathways in the liver injury response, which becomes maladaptive during obesity-associated chronic liver disease. In this Review, we discuss the aetiology of this reactivation of developmental pathways and review the cell-autonomous and cell-non-autonomous mechanisms by which developmental pathways influence disease progression. Finally, we discuss the potential prognostic and therapeutic implications of these data for NASH and liver fibrosis.
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Many patients with chronic liver disease are at increased risk of developing HCC or cholangiocellular carcinoma.
“Many patients with chronic liver disease are at an increased risk of developing hepatocellular carcinoma (HCC) or cholangiocellular carcinoma.159,160”
From Distinct hepatocyte identities in liver homeostasis and regeneration (2023) · cites this paper as [160]
The Abstract (page unavailable) states that fibrosis in patients with NAFLD–NASH increases the risk of HCC, and “Future directions — NASH-driven HCC?” reports HCC in a small percentage of patients with NAFLD. This supports the HCC-risk portion, but the paper does not establish increased risk of cholangiocellular carcinoma or make the same risk claim for patients with chronic liver disease generally. The latter cancer appears only in a reference title. (LLM, conf=0.87)
Experimental — accuracy not yet measuredThe fibrotic wound healing response is tightly linked to zonal injury and changes in hepatocyte identity via reprogramming.
“Likewise, the fibrotic ‘wound healing’ response is tightly linked to zonal injury and changes in hepatocyte identity via reprogramming.155,159,160”
From Distinct hepatocyte identities in liver homeostasis and regeneration (2023) · cites this paper as [160]
The Conclusions (page unavailable) describe developmental pathways coordinating a wound-healing response to liver injury, and “Hepatocyte reprogramming in liver diseases” describes injury-induced changes in hepatocyte identity. The passages do not establish a tight link between the fibrotic response and zonal injury; the reprogramming section also frames a progression from dysregulated regeneration to fibrosis as a possibility. (LLM, conf=0.84)
Experimental — accuracy not yet measuredHCC is more frequent in patients with zone 3 injury, such as NASH or alcohol-related liver disease, while cholangiocellular carcinoma risk is dramatically increased in patients with persistent periportal injury.
“While HCC is more frequent in patients with zone 3 injury, such as NASH or alcohol-related liver disease,160 cholangiocellular carcinoma risk is dramatically increased in patients with persistent periportal injury, e.g. in those with primary sclerosing cholangitis.159”
From Distinct hepatocyte identities in liver homeostasis and regeneration (2023) · cites this paper as [160]
Citation 160 is attached to the HCC clause, not the subsequent cholangiocellular-carcinoma clause. In “Future directions — NASH-driven HCC?” (page unavailable), the review links NASH to HCC, but it does not establish that HCC is more frequent with zone 3 injury or address alcohol-related liver disease as another example. Searches for those terms found no supporting passage. (LLM, conf=0.85)
Experimental — accuracy not yet measuredCholesterol and other mediators contribute to changes in transcriptional programmes in steatotic hepatocytes, leading to upregulation of developmental pathways such as Notch and TAZ, which can directly activate pro-fibrotic cell-cell communication between hepatocytes and neighbouring cells.
“In parallel, cholesterol and other mediators contribute to changes in the transcriptional programmes in steatotic hepatocytes, leading to an upregulation of developmental pathways that are often seen in bipotential progenitor cells or ductular cells, such as Notch and TAZ, which can directly activate pro-fibrotic cell-cell communication between hepatocytes and neighbouring cells.[28], [29], [30]”
From Understanding the cellular interactome of non-alcoholic fatty liver disease (2022) · cites this paper as [28]
Upregulation of developmental pathways such as Notch, Hedgehog, and Hippo-YAP-TAZ can directly activate profibrotic cell-cell communication between hepatocytes and neighbouring cells.
“This is paralleled by upregulation of developmental pathways (e.g. Notch, Hedgehog, Hippo-YAP-TAZ) that are often expressed by bipotential progenitor cells or ductular cells, which can directly activate profibrotic cell-cell communication between hepatocytes and neighbouring cells.18”
From An integrated view of anti-inflammatory and antifibrotic targets for the treatment of NASH (2023) · cites this paper as [18]
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- Authors
- Zhu, C., Tabas, I., Schwabe, R. F., & Pajvani, U. B.
- Affiliations
- Memorial Sloan Kettering Cancer Center (US)
- Columbia University (US)
- Columbia University Irving Medical Center (US)
- Corresponding author
- Pajvani, Utpal B.
- Venue
- Nature Reviews Gastroenterology & Hepatology
- Published
- 2020-10-13
- Volume
- 18
- Issue
- 2
- Pages
- 131-142
- ISSN
- 1759-5045 (ISSN-L)
- 1759-5053
- PMC
- PMC7854502
- OpenAlex
- W3092623718
- Cited by
- 112
- References
- 178
- Citations by year
- 2026: 13 · 2025: 16 · 2024: 18 · 2023: 21 · 2022: 30 · 2021: 13 · 2020: 1
- FWCI
- 2.56
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature Reviews Gastroenterology & Hepatology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK103818, R01DK116620, R01DK119767)
- Topics
- Health Sciences › Medicine › Epidemiology › Liver Disease Diagnosis and Treatment
- Health Sciences › Medicine › Hepatology › Liver physiology and pathology
- Health Sciences › Medicine › Hepatology › Liver Diseases and Immunity
- Keywords
- nonalcoholic steatohepatitis, liver fibrosis, developmental pathways, Notch signaling, Hedgehog signaling, liver regeneration, liver morphogenesis, liver cirrhosis, hepatocellular carcinoma, prognostic factors, therapeutic target
- MeSH terms
- Hippo Signaling Pathway, YAP-Signaling Proteins, Transcriptional Coactivator with PDZ-Binding Motif Proteins, Animals, Hepatectomy, Carcinoma, Hepatocellular, Humans, Inflammation, Liver, Liver Cirrhosis, Liver Neoplasms, Liver Regeneration, Obesity, Transcription Factors, Signal Transduction, Trans-Activators, Protein Serine-Threonine Kinases, Disease Progression, Hepatocytes, Adaptor Proteins, Signal Transducing, Receptors, Notch, Hedgehog Proteins, Wnt Signaling Pathway, Cellular Reprogramming, Non-alcoholic Fatty Liver Disease
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