Cited by 202IL-33, ST2, and ILC PathwaysPediatric Hepatobiliary Diseases and TreatmentsLiver Diseases and Immunity

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Biliary repair and carcinogenesis are mediated by IL-33–dependent cholangiocyte proliferation

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Li, Jun, Razumilava, Nataliya, Gores, Gregory J., Walters, Stephanie, Mizuochi, Tatsuki, Mourya, Reena, Bessho, Kazuhiko, Wang, Yui-Hsi, Glaser, Shannon S., Shivakumar, Pranavkumar, Bezerra, Jorge A.·2014·Journal of Clinical Investigation

DOI 10.1172/jci73742PMC PMC4071370

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Abstract

Injury to the biliary epithelium triggers inflammation and fibrosis, which can result in severe liver diseases and may progress to malignancy. Development of a type 1 immune response has been linked to biliary injury pathogenesis; however, a subset of patients with biliary atresia, the most common childhood cholangiopathy, exhibit increased levels of Th2-promoting cytokines. The relationship among different inflammatory drivers, epithelial repair, and carcinogenesis remains unclear. Here, we determined that the Th2-activating cytokine IL-33 is elevated in biliary atresia patient serum and in the livers and bile ducts of mice with experimental biliary atresia. Administration of IL-33 to WT mice markedly increased cholangiocyte proliferation and promoted sustained cell growth, resulting in dramatic and rapid enlargement of extrahepatic bile ducts. The IL-33-dependent proliferative response was mediated by an increase in the number of type 2 innate lymphoid cells (ILC2s), which released high levels of IL-13 that in turn promoted cholangiocyte hyperplasia. Induction of the IL-33/ILC2/IL-13 circuit in a murine biliary injury model promoted epithelial repair; however, induction of this circuit in mice with constitutive activation of AKT and YAP in bile ducts induced cholangiocarcinoma with liver metastases. These findings reveal that IL-33 mediates epithelial proliferation and suggest that activation of IL-33/ILC2/IL-13 may improve biliary repair and disruption of the circuit may block progression of carcinogenesis.

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Authors: Li, J., Razumilava, N., Gores, G. J., Walters, S., Mizuochi, T., Mourya, R., Bessho, K., Wang, Y.-H., Glaser, S. S., Shivakumar, P., & Bezerra, J. A.
Affiliations: Cincinnati Children's Hospital Medical Center (US)
Mayo Clinic (US)
Texas A&M Health Science Center (US)
Corresponding author: Bezerra, Jorge A.
ORCID: Li, Jun
Razumilava, Nataliya
Gores, Gregory J.
Mizuochi, Tatsuki
Mourya, Reena
Bessho, Kazuhiko
Glaser, Shannon S.
Shivakumar, Pranavkumar
Bezerra, Jorge A.
Venue: Journal of Clinical Investigation
Publisher: American Society for Clinical Investigation
Published: 2014-06-02
Volume: 124
Issue: 7
Pages: 3241-3251
ISSN: 0021-9738 (ISSN-L)
DOI: 10.1172/jci73742
PMC: PMC4071370
OpenAlex: W2031633372
Cited by: 202
References: 31
Citations by year: 2026: 6 · 2025: 10 · 2024: 9 · 2023: 6 · 2022: 13 · 2021: 16 · 2020: 19 · 2019: 23 · 2018: 27 · 2017: 20 · 2016: 17 · 2015: 29 · 2014: 7
FWCI: 11.11
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Journal of Clinical Investigation (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Cincinnati Children's Hospital Medical Center
National Institutes of Health (7r01dk083781-14, DK-83781, DK78392, DK59427)
Tufts University School of Medicine
Medical Research Council
National Institute of Diabetes and Digestive and Kidney Diseases (DK 83781, R01-DK083781, DK78392, R56DK059427, DK 59427, DK-789392, DK 64008, R01DK059427, R01DK054811, R01DK064008, R01DK076898, P30DK078392)
Topics: Life Sciences › Immunology and Microbiology › Immunology › IL-33, ST2, and ILC Pathways
Health Sciences › Medicine › Surgery › Pediatric Hepatobiliary Diseases and Treatments
Health Sciences › Medicine › Hepatology › Liver Diseases and Immunity
Keywords: IL-33, biliary atresia, cholangiocyte proliferation, ILC2, IL-13, biliary carcinogenesis, cholangiocarcinoma, YAP, Akt, Th2 immune response, biliary injury, liver fibrosis, liver metastasis
MeSH terms: Interleukin-33, Animals, Animals, Newborn, Biliary Atresia, Biliary Tract Neoplasms, Cell Line, Disease Models, Animal, Female, Humans, Interleukins, Male, Mice, Inbred BALB C, Bile Ducts, Extrahepatic, Cholangiocarcinoma, Mice, Knockout, Th2 Cells, Interleukin-13, Cell Line, Tumor, Cell Proliferation, Mice, Carcinogenesis

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Biliary repair and carcinogenesis are mediated by IL-33–dependent cholangiocyte proliferation

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