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

The DOI matches its Crossref record; 31 of the 31 references it cites were found in a registry or an index.

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

Open access

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

Open this paper in CoChat — free account Open PDF

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.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1172/jci73742

Cites

31 of 31 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

IL-33, an Interleukin-1-like Cytokine that Signals via the IL-1 Receptor-Related Protein ST2 and Induces T Helper Type 2-Associated Cytokines
Schmitz, J., Owyang, A. M., Oldham, E. R., Song, Y., Murphy, E., McClanahan, T. K., Zurawski, G., Moshrefi, M., Qin, J., Li, X., et al. (2005) · Immunity · doi:10.1016/j.immuni.2005.09.015 · Cited by 3,773
Innate lymphoid cells — a proposal for uniform nomenclature
Spits, H., Artis, D., Colonna, M., Diefenbach, A., Disanto, J. D., Eberl, G., Koyasu, S., Locksley, R., McKenzie, A., Mebius, R., et al. (2013) · Nature reviews. Immunology · doi:10.1038/nri3365 · Cited by 2,380
Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity
Neill, D. R., Wong, S. H., Bellosi, A., Flynn, R. J., Daly, M. G., Langford, T. K. A., Bucks, C. M., Kane, C. M., Fallon, P. G., Pannell, R., et al. (2010) · Nature · doi:10.1038/nature08900 · Cited by 2,079
Innate production of TH2 cytokines by adipose tissue-associated c-Kit+Sca-1+ lymphoid cells
Moro, K., Yamada, T., Tanabe, M., Takeuchi, T., Ikawa, T., Kawamoto, H., Furusawa, J.-I., Ohtani, M., Fujii, H., & Koyasu, S. (2009) · Nature · doi:10.1038/nature08636 · Cited by 1,994
Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus
Monticelli, L. A., Sonnenberg, G. F., Abt, M. C., Alenghat, T., Ziegler, C. G. K., Doering, T. A., Angelosanto, J., Laidlaw, B. J., Yang, C. Y., Sathaliyawala, T., et al. (2011) · Nature Immunology · doi:10.1038/ni.2131 · Cited by 1,327
Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus
Monticelli (2011) · PubMed · doi:10.1031/ni.2131 · Cited by 1,286
Disease-associated functions of IL-33: the new kid in the IL-1 family
Liew, F. Y., Pitman, N. I., & McInnes, I. B. (2010) · Nature reviews. Immunology · doi:10.1038/nri2692 · Cited by 1,020
Lung Natural Helper Cells Are a Critical Source of Th2 Cell-Type Cytokines in Protease Allergen-Induced Airway Inflammation
Halim, T. Y. F., Krauss, R., Sun, A. C., & Takei, F. (2012) · Immunity · doi:10.1016/j.immuni.2011.12.020 · Cited by 836
Innate lymphoid cells mediate influenza-induced airway hyper-reactivity independently of adaptive immunity
Chang, Y., Kim, H. Y., Albacker, L. A., Baumgarth, N., McKenzie, A. N. J., Smith, D. E., DeKruyff, R. H., & Umetsu, D. T. (2011) · Nature Immunology · doi:10.1038/ni.2045 · Cited by 797
Transcription factor RORα is critical for nuocyte development
Wong, S. H., Walker, J. A., Jolin, H. E., Drynan, L. F., Hams, E., Camelo, A., Barlow, J. L., Neill, D. R., Panova, V., Koch, U., et al. (2012) · Nature Immunology · doi:10.1038/ni.2208 · Cited by 577

Flagged first, then by citations

Show all 31 references

Research works printed but not linked: 1

Grubman, 1994, Am J Physiol., 266, G1060

Sorted by citations

Interleukin-33 in health and disease
Liew, F. Y., Girard, J., & Turnquist, H. R. (2016) · Nature reviews. Immunology · doi:10.1038/nri.2016.95 · Cited by 1,178
Innate lymphoid cells: A new paradigm in immunology
Eberl, G., Colonna, M., Di Santo, J. P., & McKenzie, A. N. J. (2015) · Science · doi:10.1126/science.aaa6566 · Cited by 878
Cell Death and Cell Death Responses in Liver Disease: Mechanisms and Clinical Relevance
Luedde, T., Kaplowitz, N., & Schwabe, R. F. (2014) · Gastroenterology · doi:10.1053/j.gastro.2014.07.018 · Cited by 785
Inflammation and Liver Cancer: Molecular Mechanisms and Therapeutic Targets
Yang, Y. M., Kim, S., & Seki, E. (2019) · Seminars in Liver Disease · doi:10.1055/s-0038-1676806 · Cited by 462
Alarmins and immunity
Yang, D., Han, Z., & Oppenheim, J. J. (2017) · Immunological Reviews · doi:10.1111/imr.12577 · Cited by 424
Innate Lymphoid Cells in Inflammation and Immunity
McKenzie, A. N. J., Spits, H., & Eberl, G. (2014) · Immunity · doi:10.1016/j.immuni.2014.09.006 · Cited by 384
Recent advancement of molecular mechanisms of liver fibrosis
Seki, E., & Brenner, D. A. (2015) · Journal of Hepato-Biliary-Pancreatic Sciences · doi:10.1002/jhbp.245 · Cited by 302
Pathogenesis of biliary atresia: defining biology to understand clinical phenotypes
Asai, A., Miethke, A. G., & Bezerra, J. A. (2015) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2015.74 · Cited by 282
Self-citation
WNT signaling drives cholangiocarcinoma growth and can be pharmacologically inhibited.
Boulter, L., Guest, R., Kendall, T., Wilson, D., Wojtacha, D., Robson, A., Ridgway, R., Samuel, K., van Rooijen, N., Barry, S., et al. (2015) · Journal of Clinical Investigation · doi:10.1172/jci76452 · Cited by 261
YAP promotes proliferation, chemoresistance, and angiogenesis in human cholangiocarcinoma through TEAD transcription factors
Marti, P., Stein, C., Blumer, T., Abraham, Y., Dill, M. T., Pikiolek, M., Orsini, V., Jurisic, G., Megel, P., Makowska, Z., et al. (2015) · Hepatology · doi:10.1002/hep.27992 · Cited by 232
Tumour-derived PGD2 and NKp30-B7H6 engagement drives an immunosuppressive ILC2-MDSC axis
Trabanelli, S., Chevalier, M. F., Martínez-Usatorre, A., Gomez‐Cadena, A., Salomé, B., Lecciso, M., Salvestrini, V., Verdeil, G., Racle, J., Papayannidis, C., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-00678-2 · Cited by 234
IL-33/ST2 Axis in Organ Fibrosis
Kotsiou, O. S., Gourgoulianis, K. I., & Zarogiannis, S. G. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02432 · Cited by 234
IL-33-Dependent Group 2 Innate Lymphoid Cells Promote Cutaneous Wound Healing
Rak, G. D., Osborne, L. C., Siracusa, M. C., Kim, B., Wang, K., Bayat, A., Artis, D., & Volk, S. W. (2015) · Journal of Investigative Dermatology · doi:10.1038/jid.2015.406 · Cited by 235
Human innate lymphoid cells
Mjösberg, J., & Spits, H. (2016) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2016.09.009 · Cited by 223
IL33 Promotes Colon Cancer Cell Stemness via JNK Activation and Macrophage Recruitment
Fang, M., Li, Y., Huang, K., Qi, S., Zhang, J., Zgodziński, W., Majewski, M., Wallner, G. T., Góźdź, S. S., Macek, P., et al. (2017) · Cancer Research · doi:10.1158/0008-5472.can-16-1602 · Cited by 187
IL-33 activates tumor stroma to promote intestinal polyposis
Maywald, R. L., Doerner, S. K., Pastorelli, L., Salvo, C. D., Benton, S. M., Dawson, E. P., Lanza, D. G., Berger, N. A., Markowitz, S. D., Lenz, H., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1422445112 · Cited by 159
IL‐33 facilitates oncogene‐induced cholangiocarcinoma in mice by an interleukin‐6‐sensitive mechanism
Yamada, D., Ilyas, S. I., Razumilava, N., Bronk, S. F., Davila, J. I., Champion, M. D., Borad, M. J., Bezerra, J. A., Chen, X., & Gores, G. J. (2015) · Hepatology · doi:10.1002/hep.27687 · Cited by 144
Self-citation
The reciprocal interaction between tumor cells and activated fibroblasts mediated by TNF-α/IL-33/ST2L signaling promotes gastric cancer metastasis
Zhou, Q., Wu, X., Wang, X., Yu, Z., Pan, T., Li, Z., Chang, X., Jin, Z., Li, J., Zhu, Z., et al. (2019) · Oncogene · doi:10.1038/s41388-019-1078-x · Cited by 135
Self-citation
Interleukin-13 Activates Distinct Cellular Pathways Leading to Ductular Reaction, Steatosis, and Fibrosis
Gieseck, R. L., Ramalingam, T. R., Hart, K. M., Vannella, K. M., Cantu, D. A., Lu, W.-Y., Ferreira-González, S., Forbes, S. J., Vallier, L., & Wynn, T. A. (2016) · Immunity · doi:10.1016/j.immuni.2016.06.009 · Cited by 132
NUAK2 is a critical YAP target in liver cancer
Yuan, W.-C., Pepe-Mooney, B. J., Galli, G. G., Dill, M. T., Huang, H., Hao, M., Wang, Y., Liang, H., Calogero, R., & Camargo, F. D. (2018) · Nature Communications · doi:10.1038/s41467-018-07394-5 · Cited by 129
Self-citation
IL-33 exacerbates liver sterile inflammation by amplifying neutrophil extracellular trap formation
Yazdani, H. O., Chen, H., Tohme, S. T., Tai, S., van der Windt, D. J., Loughran, P., Rosborough, B. R., Sud, V., Beer–Stolz, D., Turnquist, H. R., et al. (2017) · Journal of Hepatology · doi:10.1016/j.jhep.2017.09.010 · Cited by 131
The Pleiotropic Immunomodulatory Functions of IL-33 and Its Implications in Tumor Immunity
Afferni, C., Buccione, C., Andreone, S., Galdiero, M. R., Varricchi, G., Marone, G., Mattei, F., & Schiavoni, G. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02601 · Cited by 126
Primary Sclerosing Cholangitis as a Premalignant Biliary Tract Disease: Surveillance and Management
Ilyas, S. I., Eaton, J. E., & Gores, G. J. (2015) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2015.05.035 · Cited by 120
Self-citation
Why Innate Lymphoid Cells?
Kotas, M. E., & Locksley, R. M. (2018) · Immunity · doi:10.1016/j.immuni.2018.06.002 · Cited by 123
The Role of IL-33/ST2 Pathway in Tumorigenesis
Larsen, K. M., Minaya, M. K., Vaish, V., & Peña, M. M. O. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19092676 · Cited by 122
Interleukin-33 in tumorigenesis, tumor immune evasion, and cancer immunotherapy
Lu, B., Yang, M., & Wang, Q. (2016) · Journal of Molecular Medicine · doi:10.1007/s00109-016-1397-0 · Cited by 107
Functional and Structural Features of Cholangiocytes in Health and Disease
Maroni, L., Haibo, B., Ray, D., Zhou, T., Wan, Y., Meng, F., Marzioni, M., & Alpini, G. D. (2015) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2015.05.005 · Cited by 116
Emerging concepts and future challenges in innate lymphoid cell biology
Wojno, E. D. T., & Artis, D. (2016) · The Journal of Experimental Medicine · doi:10.1084/jem.20160525 · Cited by 108
Immune cells in liver regeneration
Li, N., & Hua, J. (2017) · Oncotarget · doi:10.18632/oncotarget.12275 · Cited by 104
Exogenous IL-33 Restores Dendritic Cell Activation and Maturation in Established Cancer
Dominguez, D., Ye, C., Geng, Z., Chen, S., Fan, J., Qin, L., Long, A., Wang, L., Zhang, Z., Zhang, Y., et al. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1501399 · Cited by 101
Innate Immunity and Pathogenesis of Biliary Atresia
Ortiz‐Perez, A., Donnelly, B., Temple, H., Tiao, G. M., Bansal, R., & Mohanty, S. K. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00329 · Cited by 102
Biliary organoids uncover delayed epithelial development and barrier function in biliary atresia
Amarachintha, S. P., Mourya, R., Ayabe, H., Yang, L., Luo, Z., Li, X., Thanekar, U., Shivakumar, P., & Bezerra, J. A. (2022) · Hepatology · doi:10.1002/hep.32107 · Cited by 98
Self-citation
Inflammation and immunity in liver homeostasis and disease: a nexus of hepatocytes, nonparenchymal cells and immune cells
(2025) · doi:10.1038/s41423-025-01313-7 · Cited by 97
The Pro-tumorigenic IL-33 Involved in Antitumor Immunity: A Yin and Yang Cytokine
Fournié, J., & Poupot, M. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02506 · Cited by 99
Cholangiocarcinoma 2026: status quo, unmet needs and priorities
Bañales, J. M., Rodrigues, P. M., Affò, S., Andersen, J. B., Aspichueta, P., Boulter, L., Bridgewater, J. A., Calvisi, D. F., Cárdenas, A., Cardinale, V., et al. (2025) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-025-01153-w · Cited by 112
Self-citation
A Hippo and Fibroblast Growth Factor Receptor Autocrine Pathway in Cholangiocarcinoma
Ilyas, S. I., Yamada, D., Hirsova, P., Bronk, S. F., Werneburg, N. W., Krishnan, A., Salim, W., Zhang, L. N., Trushina, E. V., Truty, M. J., et al. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.698472 · Cited by 94
Self-citation
Tissue microenvironment dictates the fate and tumor-suppressive function of type 3 ILCs
Nussbaum, K., Burkhard, S., Ohs, I., Mair, F., Klose, C. S. N., Arnold, S. J., Diefenbach, A., Tugues, S., & Becher, B. (2017) · The Journal of Experimental Medicine · doi:10.1084/jem.20162031 · Cited by 98
Biliary Atresia in Children
Antala, S., & Taylor, S. A. (2022) · Clinics in Liver Disease · doi:10.1016/j.cld.2022.03.001 · Cited by 93
Emerging concepts in biliary repair and fibrosis
Fabris, L., Spirlı̀, C., Cadamuro, M., Fiorotto, R., & Strazzabosco, M. (2017) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00452.2016 · Cited by 94
Biliary epithelial injury-induced regenerative response by IL-33 promotes cholangiocarcinogenesis from peribiliary glands
Nakagawa, H., Suzuki, N., Hirata, Y., Hikiba, Y., Hayakawa, Y., Kinoshita, H., Ihara, S., Uchino, K., Nishikawa, Y., Ijichi, H., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1619416114 · Cited by 91
New dog and new tricks: evolving roles for IL-33 in type 2 immunity
Lott, J. M., Sumpter, T. L., & Turnquist, H. R. (2015) · Journal of Leukocyte Biology · doi:10.1189/jlb.3ri1214-595r · Cited by 90
Update on Pathogenesis of Opisthorchiasis and Cholangiocarcinoma
Sripa, B., Tangkawattana, S., & Brindley, P. J. (2018) · Advances in Parasitology/Advances in parasitology · doi:10.1016/bs.apar.2018.10.001 · Cited by 90
Impact of microenvironment and stem-like plasticity in cholangiocarcinoma: Molecular networks and biological concepts
Raggi, C., Invernizzi, P., & Andersen, J. B. (2014) · Journal of Hepatology · doi:10.1016/j.jhep.2014.09.007 · Cited by 87
The Role of IL-33-Dependent Inflammation in the Tumor Microenvironment
Wasmer, M.-H., & Krebs, P. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00682 · Cited by 84
Animal models of cholangiocarcinoma
Loeuillard, E. J., Fischbach, S. R., Gores, G. J., & Ilyas, S. I. (2018) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2018.03.026 · Cited by 84
Self-citation
Group 2 innate lymphoid cells in disease
Halim, T. Y. F. (2015) · International Immunology · doi:10.1093/intimm/dxv050 · Cited by 81
Immunometabolism: A novel perspective of liver cancer microenvironment and its influence on tumor progression
Zhang, Q., Lou, Y., Bai, X., & Liang, T. (2018) · World Journal of Gastroenterology · doi:10.3748/wjg.v24.i31.3500 · Cited by 81
TREM-2 plays a protective role in cholestasis by acting as a negative regulator of inflammation
Labiano, I., Agirre-Lizaso, A., Olaizola, P., Echebarria, A., Huici-Izagirre, M., Olaizola, I., Esparza-Baquer, A., Sharif, O., Hijona, E., Milkiewicz, P., et al. (2022) · Journal of Hepatology · doi:10.1016/j.jhep.2022.05.044 · Cited by 78
Cholangiocytes in the pathogenesis of primary sclerosing cholangitis and development of cholangiocarcinoma
Chung, B. K., Karlsen, T. H., & Folseraas, T. (2017) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2017.08.020 · Cited by 76
Type 2 Innate Lymphoid Cells Impede IL-33–Mediated Tumor Suppression
Long, A., Dominguez, D., Qin, L., Chen, S., Fan, J., Zhang, M., Fang, D., Zhang, Y., Kuzel, T. M., & Zhang, B. (2018) · The Journal of Immunology · doi:10.4049/jimmunol.1800173 · Cited by 74
Liver fibrosis in biliary atresia
Shen, W.-J., Chen, G., Wang, M., & Zheng, S. (2018) · World Journal of Pediatrics · doi:10.1007/s12519-018-0203-1 · Cited by 75
Programmed knockout mutation of liver fluke granulin attenuates virulence of infection-induced hepatobiliary morbidity
Arunsan, P., Ittiprasert, W., Smout, M. J., Cochran, C. J., Mann, V. H., Chaiyadet, S., Karinshak, S. E., Sripa, B., Young, N. D., Sotillo, J., et al. (2019) · eLife · doi:10.7554/elife.41463 · Cited by 77
Macrophages and cancer stem cells: a malevolent alliance
Allavena, P., Digifico, E., & Belgiovine, C. (2021) · Molecular Medicine · doi:10.1186/s10020-021-00383-3 · Cited by 76
Helper-like Innate Lymphoid Cells in Humans and Mice
Guia, S., & Narni-Mancinelli, É. (2020) · Trends in Immunology · doi:10.1016/j.it.2020.03.002 · Cited by 76
Macrophage and Innate Lymphoid Cell Interplay in the Genesis of Fibrosis
Hams, E., Bermingham, R., & Fallon, P. G. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00597 · Cited by 70
Nucleotide-binding oligomerization domain 1 acts in concert with the cholecystokinin receptor agonist, cerulein, to induce IL-33-dependent chronic pancreatitis
Watanabe, T., Sadakane, Y., Yagama, N., Sakurai, T., Ezoe, H., Kudo, M., Chiba, T., & Strober, W. (2016) · Mucosal Immunology · doi:10.1038/mi.2015.144 · Cited by 68
Interleukin‐1 Family Cytokines in Liver Diseases
Tsutsui, H., Cai, X., & Hayashi, S. (2015) · Mediators of Inflammation · doi:10.1155/2015/630265 · Cited by 63
Dual roles of yes-associated protein (YAP) in colorectal cancer
Ou, C., Sun, Z., Li, S., Li, G., Li, X., & Ma, J. (2017) · Oncotarget · doi:10.18632/oncotarget.20155 · Cited by 62
IL-33 facilitates proliferation of colorectal cancer dependent on COX2/PGE2
Li, Y., Shi, J., Qi, S., Zhang, J., Peng, D., Chen, Z., Wang, G., Wang, Z., & Wang, L. (2018) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-018-0839-7 · Cited by 62
Helminth infection–induced malignancy
Brindley, P. J., & Loukas, A. C. (2017) · PLoS Pathogens · doi:10.1371/journal.ppat.1006393 · Cited by 62
Interleukin‐8: A critical chemokine in biliary atresia
Dong, R., & Zheng, S. (2015) · Journal of Gastroenterology and Hepatology · doi:10.1111/jgh.12900 · Cited by 57
IL-33 Signaling Protects from Murine Oxazolone Colitis by Supporting Intestinal Epithelial Function
Waddell, A., Vallance, J. E., Moore, P. D., Hummel, A. T., Wu, D. X.-Y., Shanmukhappa, S. K., Fei, L., Washington, M. K., Minar, P., Coburn, L. A., et al. (2015) · Inflammatory Bowel Diseases · doi:10.1097/mib.0000000000000532 · Cited by 57
Characterisation of the immune-related transcriptome in resected biliary tract cancers
Ghidini, M., Cascione, L., Carotenuto, P., Lampis, A., Trevisani, F., Previdi, M. C., Hahne, J. C., Said‐Huntingford, I., Raj, M., Zerbi, A., et al. (2017) · European Journal of Cancer · doi:10.1016/j.ejca.2017.09.005 · Cited by 57
Platelet-derived Growth Factor Primes Cancer-associated Fibroblasts for Apoptosis
Ilyas, S. I., Mertens, J. C., Bronk, S. F., Hirsova, P., Dai, H., Roberts, L. R., Kaufmann, S. H., & Gores, G. J. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.563064 · Cited by 56
Self-citation
Human intrahepatic ILC2 are IL-13positive amphiregulinpositive and their frequency correlates with model of end stage liver disease score
Jeffery, H. C., McDowell, P., Lutz, P. L., Wawman, R. E., Roberts, S., Bagnall, C., Birtwistle, J., Adams, D., & Oo, Y. H. (2017) · PLoS ONE · doi:10.1371/journal.pone.0188649 · Cited by 57
Innate immunity is a key factor for the resolution of inflammation in asthma
Barnig, C., & Levy, B. D. (2015) · European Respiratory Review · doi:10.1183/09059180.00012514 · Cited by 56
Therapeutic targets for cholestatic liver injury
Woolbright, B. L., & Jaeschke, H. (2015) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728222.2016.1103735 · Cited by 54
The potential role of IL-33/ST2 signaling in fibrotic diseases
Gao, Q., Li, Y., & Li, M. (2015) · Journal of Leukocyte Biology · doi:10.1189/jlb.3ru0115-012r · Cited by 50
The MNK1/2–eIF4E Axis Supports Immune Suppression and Metastasis in Postpartum Breast Cancer
Guo, Q., Bartish, M., Gonçalves, C., Huang, F., Smith-Voudouris, J., Krisna, S. S., Preston, S. E. J., Émond, A., Li, V. Z., Duerr, C. U., et al. (2021) · Cancer Research · doi:10.1158/0008-5472.can-20-3143 · Cited by 46
Friend or Foe? The Ambiguous Role of Innate Lymphoid Cells in Cancer Development
Mattner, J., & Wirtz, S. J. (2016) · Trends in Immunology · doi:10.1016/j.it.2016.10.004 · Cited by 47
Innate lymphoid cells and cancer: Role in tumor progression and inhibition
Yuan, X., Rasul, F., Nashan, B., & Sun, C. (2021) · European Journal of Immunology · doi:10.1002/eji.202049033 · Cited by 48
Interleukin-13 (IL-13)—A Pleiotropic Cytokine Involved in Wound Healing and Fibrosis
Roeb, E. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241612884 · Cited by 45
Wounds that heal and wounds that don’t − The role of the IL-33/ST2 pathway in tissue repair and tumorigenesis
Millar, N. L., O’Donnell, C., McInnes, I. B., & Brint, E. K. (2016) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2016.08.007 · Cited by 45
Regulation of Type 2 Immunity in Myocardial Infarction
Xu, J.-Y., Xiong, Y., Lu, X., & Yang, Y. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00062 · Cited by 42
IL33 and Mast Cells—The Key Regulators of Immune Responses in Gastrointestinal Cancers?
Eissmann, M. F., Büchert, M., & Ernst, M. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01389 · Cited by 45
Interleukin-33 and ST2 Signaling in Tumor Microenvironment
Hong, J., Kim, S., & Lin, P. C. (2018) · Journal of Interferon & Cytokine Research · doi:10.1089/jir.2018.0044 · Cited by 43
A Phase I/IIa Trial of Intravenous Immunoglobulin Following Portoenterostomy in Biliary Atresia
Mack, C. L., Spino, C., Alonso, E. M., Bezerra, J. A., Moore, J., Goodhue, C. J., Ng, V. L., Karpen, S. J., Venkat, V. L., Loomes, K. M., et al. (2019) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0000000000002256 · Cited by 40
Self-citation
The Janus Face of IL-33 Signaling in Tumor Development and Immune Escape
Choi, M.-R., Sosman, J. A., & Zhang, B. (2021) · Cancers · doi:10.3390/cancers13133281 · Cited by 40
Innate Lymphoid Cells in Tumor Immunity
van Beek, J. J. P., Martens, A. W. J., Bakdash, G., & de Vries, I. J. M. (2016) · Biomedicines · doi:10.3390/biomedicines4010007 · Cited by 40
Tissue-resident NK cells and other innate lymphoid cells
Zhou, J., Tian, Z., & Peng, H. C. (2019) · Advances in immunology · doi:10.1016/bs.ai.2019.11.002 · Cited by 37
The Yin and Yang of Innate Lymphoid Cells in Cancer
Carrega, P., Campana, S., Bonaccorsi, I., & Ferlazzo, G. (2016) · Immunology Letters · doi:10.1016/j.imlet.2016.06.003 · Cited by 36
Portal Fibrosis and the Ductular Reaction: Pathophysiological Role in the Progression of Liver Disease and Translational Opportunities
Gupta, V., Sehrawat, T. S., Pinzani, M., & Strazzabosco, M. (2024) · Gastroenterology · doi:10.1053/j.gastro.2024.07.044 · Cited by 36
Ly6cLo non-classical monocytes promote resolution of rhesus rotavirus-mediated perinatal hepatic inflammation
Alkhani, A., Levy, C. S., Tsui, M., Rosenberg, K., Polovina, K., Mattis, A. N., Mack, M., Dyken, S. J. V., Wang, B., Maher, J. J., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-64158-2 · Cited by 31
Crosstalk between macrophages and innate lymphoid cells (ILCs) in diseases
Yin, G., Zhao, C., & Pei, W. (2022) · International Immunopharmacology · doi:10.1016/j.intimp.2022.108937 · Cited by 33
Hide and seek: Plasticity of innate lymphoid cells in cancer
Bald, T., Wagner, M., Gao, Y., Koyasu, S., & Smyth, M. J. (2019) · Seminars in Immunology · doi:10.1016/j.smim.2019.04.001 · Cited by 34
Crosstalk between Innate Lymphoid Cells and Other Immune Cells in the Tumor Microenvironment
Flores‐Borja, F., Irshad, S., Gordon, P., Wong, F., Sheriff, I., Tutt, A. N. J., & Ng, T. (2016) · Journal of Immunology Research · doi:10.1155/2016/7803091 · Cited by 33
The pro- and anti-tumor role of ILC2s
Trabanelli, S., Chevalier, M. F., Derré, L., & Jandus, C. (2019) · Seminars in Immunology · doi:10.1016/j.smim.2019.04.004 · Cited by 31
IL33 activates CD8+T and NK cells through MyD88 pathway to suppress the lung cancer cell growth in mice
Xu, L., Zheng, Y., Wang, J., Xu, Y., Xie, Y., & Yang, Z. (2020) · Biotechnology Letters · doi:10.1007/s10529-020-02815-2 · Cited by 30
IL-33 induces type-2-cytokine phenotype but exacerbates cardiac remodeling post-myocardial infarction with eosinophil recruitment, worsened systolic dysfunction, and ventricular wall rupture
Ghali, R., Habeichi, N. J., Kaplan, A., Tannous, C., Abidi, E., Bekdash, A., Farhat, R., Itani, H. A., Jurjus, A. R., Booz, G. W., et al. (2020) · Clinical Science · doi:10.1042/cs20200402 · Cited by 30
Ductular Reactions in Liver Injury, Regeneration, and Disease Progression—An Overview
Mavila, N., Eshwaraiah, M. S., & Kennedy, J. (2024) · Cells · doi:10.3390/cells13070579 · Cited by 33
Integrative single-cell and spatial transcriptomic analyses identify a pathogenic cholangiocyte niche and TNFRSF12A as therapeutic target for biliary atresia
Xiao, M.-H., Ma, D., Wu, S., Huang, Z., Liang, P., Chen, H., Zhong, Z., Li, W., Wang, F., Tang, Y., et al. (2024) · Hepatology · doi:10.1097/hep.0000000000001064 · Cited by 33
Autoimmunity as an Etiological Factor of Cancer: The Transformative Potential of Chronic Type 2 Inflammation
Li, C. M., & Chen, Z. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.664305 · Cited by 29
Role of Immune Cells in Biliary Repair
Lan, T., Qian, S., Tang, C., & Gao, J. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.866040 · Cited by 31
Fibroinflammatory Liver Injuries as Preneoplastic Condition in Cholangiopathies
Cannito, S., Milani, C., Cappon, A., Parola, M., Strazzabosco, M., & Cadamuro, M. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19123875 · Cited by 26
Peribiliary Glands as the Cellular Origin of Biliary Tract Cancer
Nakagawa, H., Hayata, Y., Yamada, T., Kawamura, S., Suzuki, N., & Koike, K. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19061745 · Cited by 27
Biliary stents for active materials and surface modification: Recent advances and future perspectives
Li, Y., Yuan, K., Deng, C., Tang, H., Wang, J., Dai, X., Zhang, B., Sun, Z., Ren, G., Zhang, H., et al. (2024) · Bioactive Materials · doi:10.1016/j.bioactmat.2024.08.031 · Cited by 25
Molecular Mechanisms Driving Cholangiocarcinoma Invasiveness: An Overview
Brivio, S., Cadamuro, M., Fabris, L., & Strazzabosco, M. (2017) · Gene Expression · doi:10.3727/105221617x15088670121925 · Cited by 26
Correlation of Interleukin-33/ST2 Receptor and Liver Fibrosis Progression in Biliary Atresia Patients
Liu, J., Yang, Y., Zheng, C., Chen, G., Shen, Z. Z., Zheng, S., & Dong, R. (2019) · Frontiers in Pediatrics · doi:10.3389/fped.2019.00403 · Cited by 24
High level of interleukin-33 in cancer cells and cancer-associated fibroblasts correlates with good prognosis and suppressed migration in cholangiocarcinoma
Yangngam, S., Thongchot, S., Pongpaibul, A., Vaeteewoottacharn, K., Pinlaor, S., Thuwajit, P., Okada, S., & Thuwajit, C. (2020) · Journal of Cancer · doi:10.7150/jca.48327 · Cited by 24
Group 2 Innate Lymphoid Cells: A Double-Edged Sword in Cancer?
Maggi, E., Veneziani, I., Moretta, L., Cosmi, L., & Annunziato, F. (2020) · Cancers · doi:10.3390/cancers12113452 · Cited by 24

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

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

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

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks