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Yes-Associated Protein Up-regulates Jagged-1 and Activates the NOTCH Pathway in Human Hepatocellular Carcinoma
Open accessAbstract
Background & aims Cancer cells often lose contact inhibition to undergo anchorage-independent proliferation and become resistant to apoptosis by inactivating the Hippo signaling pathway, resulting in activation of the transcriptional co-activator yes-associated protein (YAP). However, the oncogenic mechanisms of YAP activity are unclear.Methods By using cross-species analysis of expression data, the Notch ligand Jagged-1 (Jag-1) was identified as a downstream target of YAP in hepatocytes and hepatocellular carcinoma (HCC) cells. We analyzed the functions of YAP in HCC cells via overexpression and RNA silencing experiments. We used transgenic mice that overexpressed a constitutively activated form of YAP (YAP(S127A)), and measured protein levels in HCC, colorectal and pancreatic tumor samples from patients.Results Human HCC cell lines and mouse hepatocytes that overexpress YAP(S127A) up-regulated Jag-1, leading to activation of the Notch pathway and increased proliferation. Induction of Jag-1, activation of Notch, and cell proliferation required binding of YAP to its transcriptional partner TEA domain family member 4 (TEAD4); TEAD4 binding required the Mst1/2 but not β-catenin signaling. Levels of YAP correlated with Jag-1 expression and Notch signaling in human tumor samples and correlated with shorter survival times of patients with HCC or colorectal cancer.Conclusions The transcriptional regulator YAP up-regulates Jag-1 to activate Notch signaling in HCC cells and mouse hepatocytes. YAP-dependent activity of Jag-1 and Notch correlate in human HCC and colorectal tumor samples with patient survival times, suggesting the use of YAP and Notch inhibitors as therapeutics for gastrointestinal cancer. Transcript profiling: microarray information was deposited at the Gene Expression Omnibus database (http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?token=jxepvsumwosqkve&acc=GSE35004).
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“Despite the protective effects of IL-6, YAP-mediated Notch signaling activation contributed to tumor growth in human hepatocellular carcinoma and murine hepatocytes (Tschaharganeh et al., 2013”
From Targeting Interleukin-6 Signaling in Clinic (2019) · cites this paper as Tschaharganeh et al., 2013
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“Over the years, a number of inhibitors targeting YAP/TAZ-TEAD have been reported, including peptides such as super-TDU (173),437 and small molecules such as verteporfin (174) and MGH-CP1 (175).438–440”
From Recent advances in targeting the “undruggable” proteins: from drug discovery to clinical trials (2023) · cites this paper as [439]
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1 retracted
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“Mst1), occurs in 50 to 70% of HCCs.(3,5,11) Also, functional studies have revealed oncogenic properties for nuclear YAP.”
InfluentialTEAD mediates YAP-dependent gene induction and growth control
Zhao, B., Ye, X., Yu, J., Li, L., Li, W., Li, S., Yu, J., Lin, J. D., Wang, C.-Y., Chinnaiyan, A. M., et al. (2008) · Genes & Development · doi:10.1101/gad.1664408 · Cited by 2,498 · cited 1×
“YAP regulates target gene transcription in tumor and non-malignantly transformed cells through interaction with different transcription factors including TEAD family members.(18) Our results demonstrate that YAP-dependent expression of Jag-1 strictly depends on the presence of TEAD4, while other known binding partners…”
Elucidation of a universal size-control mechanism in Drosophila and mammals
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“To define the effector mechanisms mediating protumorigenic properties of YAP, expression profiles of human HuH-7 cells after YAP knockdown were compared with transcriptomic data of murine hepatocytes with inducible YAP expression (Figure 1A).(5) YAP-dependent expression of genes inversely regulated (including CTGF, CX…”
InfluentialLiu-Chittenden, Y., Huang, B., Shim, J. S., Chen, Q., Lee, S.-J., Anders, R. A., Liu, J. O., & Pan, D. (2012) · Genes & Development · doi:10.1101/gad.192856.112 · Cited by 1,452 · cited 1×
“Importantly, the increased luciferase activity of Jag-1 region 1 was inhibited in a dose-dependent manner when either YAP or TEAD4 plasmid transfection was paralleled by treatment with verteporfin, a drug, which disrupts the YAP-TEAD binding (Figure 4D).(19)”
The Hippo transducer TAZ confers cancer stem cell-related traits on breast cancer cells
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YAP1 increases organ size and expands undifferentiated progenitor cells
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“For this purpose, primary murine hepatocytes were isolated from 10 week old transgenic animals expressing YAP under negative control of the liver-specific LAP doxycycline transactivator domain.(8) Short-term administration of doxycycline and subsequent downregulation of YAP were followed by reduced expression of Jag-1…”
InfluentialThe Hippo pathway in organ size control, tissue regeneration and stem cell self-renewal
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“Inactivation of the Hippo pathway leads to the nuclear translocation of YAP and subsequent interaction with several transcription factors including TEAD and SMAD family members, Runx2, or p73.(2)”
Identification and validation of oncogenes in liver cancer using an integrative oncogenomic approach
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“Although transcription factors are believed to be non- 21 druggable due to large and stable protein/DNA surface interactions, crystal structure analysis of the YAP/TEAD4 complex demonstrated that the proteins are connected mainly via two short helices, one in the C-terminal domain of TEAD4 and one in the N-terminal re…”
InfluentialClassification and prediction of survival in hepatocellular carcinoma by gene expression profiling
Lee, J., Chu, I., Heo, J., Calvisi, D. F., Sun, Z., Roskams, T., Durnez, A., Demetris, A. J., & Thorgeirsson, S. S. (2004) · Hepatology · doi:10.1002/hep.20375 · Cited by 942
Self-citation
Research works printed but not linked: 1
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“A recent research also suggested that YAP1 promoted human hepatocellular carcinoma development and progression was through upregulating Jagged1 and activating the Notch pathway.(29) Moreover, several researches also revealed the target relationship between YAP1 and miR-497.”
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“This finding was consistent with the results of several previous studies [11, 22, 26-28], which further confirmed the viewpoint that enhanced YAP expression might be a common event in the carcinogenesis of CRC.”
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Yap Expression Is Closely Related to Tumor Angiogenesis and Poor Prognosis in Hepatoblastoma
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“nosis in multiple cancer types, such as hepatocellular carcinoma [9,10], breast cancer”
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Self-citationHNF4α and CDX2 Regulate Intestinal YAP1 Promoter Activity
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“There are several studies focused on the YAP1-Notch positive feedback loop in cancers (14,18,21,23,43).”
BackgroundInfluentialNanomaterials in modulating tumor-associated macrophages and enhancing immunotherapy
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CRKL Enhances YAP Signaling through Binding and JNK/JUN Pathway Activation in Liver Cancer
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MDM 2– MOF –H4K16ac axis contributes to tumorigenesis induced by Notch
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BackgroundExpression characteristics of the yes-associated protein in breast cancer: A meta-analysis
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“115-117 Also, inactivating calcium channel by PV_mito significantly inhibits EMT and HCC invasion.”
BackgroundEpigenetic activation of JAG1 by AID contributes to metastasis of hepatocellular carcinoma
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“The currently known mechanisms of the NOTCH pathway provide potential targets for therapeutic agents that can inhibit NOTCH activity (24 – 29).”
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Self-citationYAP induziert chromosomale Instabilität in Leberkrebspatienten
Weiler, S. (2018) · Der Pathologe · doi:10.1007/s00292-018-0494-y · Cited by 3
Experimental Models to Define the Genetic Predisposition to Liver Cancer
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“It exerts its tumor-supporting properties by up-regulating Jag-1 expression and activating the Notch pathway(28).”
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Nichtautonome Effekte des Onkogens YAP in der Hepatokarzinogenese
Marquard, S., Thomann, S., Weiler, S., Sticht, C., Gretz, N., Schirmacher, P., & Breuhahn, K. (2017) · Der Pathologe · doi:10.1007/s00292-017-0361-2 · Cited by 2
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Selective targeting of KRAS-driven lung tumorigenesis via unresolved ER stress
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“Other cancer-related pathways, such as Notch signaling, were also influenced by verteporfin, which is consistent with previous reports (Figure 4C) (25).”
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Metadata
- Authors
- Tschaharganeh, D. F., Chen, X., Latzko, P., Malz, M., Gaida, M. M., Felix, K., Ladu, S., Singer, S., Pinna, F., Gretz, N., Sticht, C., Tomasi, M. L., Delogu, S., Evert, M., Fan, B., Ribback, S., Jiang, L., Brozzetti, S., Bergmann, F., Dombrowski, F., Schirmacher, P., Calvisi, D. F., & Breuhahn, K.
- Affiliations
- University Hospital Heidelberg (DE)
- University of California, San Francisco (US)
- University of Chieti-Pescara (IT)
- Medizinische Fakultät Mannheim (DE)
- University of Southern California (US)
- Universität Greifswald (DE)
- Sapienza University of Rome (IT)
- Corresponding author
- Breuhahn, Kai
- ORCID
- Venue
- Gastroenterology
- Publisher
- Elsevier BV
- Published
- 2013-06
- Volume
- 144
- Issue
- 7
- Pages
- 1530-1542.e12
- ISSN
- 0016-5085 (ISSN-L)
- PMC
- PMC3665638
- OpenAlex
- W2060323466
- Cited by
- 326
- References
- 47
- Citations by year
- 2026: 8 · 2025: 16 · 2024: 16 · 2023: 19 · 2022: 26 · 2021: 29 · 2020: 35 · 2019: 26 · 2018: 26 · 2017: 25 · 2016: 28 · 2015: 35 · 2014: 28 · 2013: 8
- FWCI
- 19.34
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Gastroenterology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- IRIS Research product catalog (Sapienza University of Rome) (submittedVersion)
- Funders
- National Institutes of Health
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Hippo pathway signaling and YAP/TAZ
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer-related molecular mechanisms research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- YAP, Jagged1, Notch signaling, hepatocellular carcinoma, TEAD4, MST1/2, Hippo signaling pathway, colorectal cancer, pancreatic cancer, cell proliferation, patient survival, transcriptional coactivator, therapeutic target
- MeSH terms
- Serrate-Jagged Proteins, Jagged-1 Protein, YAP-Signaling Proteins, TEA Domain Transcription Factors, Animals, Calcium-Binding Proteins, DNA-Binding Proteins, Carcinoma, Hepatocellular, Humans, Liver Neoplasms, Membrane Proteins, Muscle Proteins, Phosphoproteins, Transcription Factors, Up-Regulation, Gene Expression Regulation, Neoplastic, Cell Cycle Proteins, Hepatocytes, Intercellular Signaling Peptides and Proteins, Cell Line, Tumor, Adaptor Proteins, Signal Transducing, Cell Proliferation, Mice, Receptors, Notch
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