Circular RNA ACTN4 promotes intrahepatic cholangiocarcinoma progression by recruiting YBX1 to initiate FZD7 transcription
Intrahepatic cholangiocarcinoma (ICC) is a primary liver cancer with high aggressiveness and extremely poor prognosis. The role of circular RNAs (circRNAs) in ICC carcinogenesis and progression remains to be determined. CircRNA microarray was performed to screen significantly upregulated circRNAs in...
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| Published in | Journal of Hepatology Vol. 76; no. 1; pp. 135 - 147 |
|---|---|
| Main Authors | , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Netherlands
Elsevier B.V
01.01.2022
Elsevier BV Elsevier Science Ltd |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Intrahepatic cholangiocarcinoma (ICC) is a primary liver cancer with high aggressiveness and extremely poor prognosis. The role of circular RNAs (circRNAs) in ICC carcinogenesis and progression remains to be determined.
CircRNA microarray was performed to screen significantly upregulated circRNAs in paired ICC and non-tumor tissues. Colony formation, transwell, and xenograft models were used to examine the role of circRNAs in ICC proliferation and metastasis. RNA pulldown, mass spectrometry, chromatin immunoprecipitation, RNA-binding protein immunoprecipitation, chromatin isolation by RNA purification, electrophoretic mobility shift assay, and luciferase reporter assays were used to explore the molecular sponge role of the circRNA (via miRNA binding), and the interaction between circRNA and RNA-binding proteins.
Hsa_circ_0050898, which originated from exon 1 to exon 20 of the ACTN4 gene (named circACTN4), was significantly upregulated in ICC. High circACTN4 expression was associated with enhanced tumor proliferation and metastasis in vitro and in vivo, as well as a worse prognosis following ICC resection. In addition, circACTN4 upregulated Yes-associated protein 1 (YAP1) expression by sponging miR-424-5p. More importantly, circACTN4 also recruited Y-box binding protein 1 (YBX1) to stimulate Frizzled-7 (FZD7) transcription. Furthermore, circACTN4 overexpression in ICC cells enhanced the interaction between YAP1 and β-catenin, which are the core components of the Hippo and Wnt signaling pathways, respectively.
CircACTN4 was upregulated in ICC and promoted ICC proliferation and metastasis by acting as a molecular sponge of miR-424-5p, as well as by interacting with YBX1 to transcriptionally activate FZD7. These results suggest that circACTN4 is a potential prognostic marker and therapeutic target for ICC.
Intrahepatic cholangiocarcinoma is a primary liver cancer associated with aggressiveness and extremely poor prognosis. It is essential for therapeutic development that we uncover relevant pathogenic pathways. Herein, we showed that a circular RNA (circACTN4) was highly expressed in intrahepatic cholangiocarcinoma and was positively associated with tumor growth and metastasis through key developmental signaling pathways. Thus, circACTN4 could be a prognostic biomarker and therapeutic target for intrahepatic cholangiocarcinoma.
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•CircACTN4 was upregulated in ICC and is associated with a worse prognosis.•CircACTN4 promoted ICC growth and metastasis in vitro and in vivo.•CircACTN4 recruited YBX1 to initiate FZD7 transcription.•CircACTN4 acted as sponge of miR-424-5p to upregulate YAP1.•CircACTN4 enhanced the interaction between the Wnt/β-catenin and Hippo/YAP pathways. |
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| AbstractList | Intrahepatic cholangiocarcinoma (ICC) is a primary liver cancer with high aggressiveness and extremely poor prognosis. The role of circular RNAs (circRNAs) in ICC carcinogenesis and progression remains to be determined.
CircRNA microarray was performed to screen significantly upregulated circRNAs in paired ICC and non-tumor tissues. Colony formation, transwell, and xenograft models were used to examine the role of circRNAs in ICC proliferation and metastasis. RNA pulldown, mass spectrometry, chromatin immunoprecipitation, RNA-binding protein immunoprecipitation, chromatin isolation by RNA purification, electrophoretic mobility shift assay, and luciferase reporter assays were used to explore the molecular sponge role of the circRNA (via miRNA binding), and the interaction between circRNA and RNA-binding proteins.
Hsa_circ_0050898, which originated from exon 1 to exon 20 of the ACTN4 gene (named circACTN4), was significantly upregulated in ICC. High circACTN4 expression was associated with enhanced tumor proliferation and metastasis in vitro and in vivo, as well as a worse prognosis following ICC resection. In addition, circACTN4 upregulated Yes-associated protein 1 (YAP1) expression by sponging miR-424-5p. More importantly, circACTN4 also recruited Y-box binding protein 1 (YBX1) to stimulate Frizzled-7 (FZD7) transcription. Furthermore, circACTN4 overexpression in ICC cells enhanced the interaction between YAP1 and β-catenin, which are the core components of the Hippo and Wnt signaling pathways, respectively.
CircACTN4 was upregulated in ICC and promoted ICC proliferation and metastasis by acting as a molecular sponge of miR-424-5p, as well as by interacting with YBX1 to transcriptionally activate FZD7. These results suggest that circACTN4 is a potential prognostic marker and therapeutic target for ICC.
Intrahepatic cholangiocarcinoma is a primary liver cancer associated with aggressiveness and extremely poor prognosis. It is essential for therapeutic development that we uncover relevant pathogenic pathways. Herein, we showed that a circular RNA (circACTN4) was highly expressed in intrahepatic cholangiocarcinoma and was positively associated with tumor growth and metastasis through key developmental signaling pathways. Thus, circACTN4 could be a prognostic biomarker and therapeutic target for intrahepatic cholangiocarcinoma.
[Display omitted]
•CircACTN4 was upregulated in ICC and is associated with a worse prognosis.•CircACTN4 promoted ICC growth and metastasis in vitro and in vivo.•CircACTN4 recruited YBX1 to initiate FZD7 transcription.•CircACTN4 acted as sponge of miR-424-5p to upregulate YAP1.•CircACTN4 enhanced the interaction between the Wnt/β-catenin and Hippo/YAP pathways. Background & Aims: Intrahepatic cholangiocarcinoma (ICC) is a primary liver cancer with high aggressiveness and extremely poor prognosis. The role of circular RNAs (circRNAs) in ICC carcinogenesis and progression remains to be determined. Methods: CircRNA microarray was performed to screen significantly upregulated circRNAs in paired ICC and non-tumor tissues. Colony formation, transwell, and xenograft models were used to examine the role of circRNAs in ICC proliferation and metastasis. RNA pulldown, mass spectrometry, chromatin immunoprecipitation, RNA-binding protein immunoprecipitation, chromatin isolation by RNA purification, electrophoretic mobility shift assay, and luciferase reporter assays were used to explore the molecular sponge role of the circRNA (via miRNA binding), and the interaction between circRNA and RNA-binding proteins. Results: Hsa_circ_0050898, which originated from exon 1 to exon 20 of the ACTN4 gene (named circACTN4), was significantly upregulated in ICC. High circACTN4 expression was associated with enhanced tumor proliferation and metastasis in vitro and in vivo, as well as a worse prognosis following ICC resection. In addition, circACTN4 upregulated Yes-associated protein 1 (YAP1) expression by sponging miR-424-5p. More importantly, circACTN4 also recruited Y-box binding protein 1 (YBX1) to stimulate Frizzled-7 (FZD7) transcription. Furthermore, circACTN4 overexpression in ICC cells enhanced the interaction between YAP1 and β-catenin, which are the core components of the Hippo and Wnt signaling pathways, respectively. Conclusions: CircACTN4 was upregulated in ICC and promoted ICC proliferation and metastasis by acting as a molecular sponge of miR-424-5p, as well as by interacting with YBX1 to transcriptionally activate FZD7. These results suggest that circACTN4 is a potential prognostic marker and therapeutic target for ICC. Intrahepatic cholangiocarcinoma (ICC) is a primary liver cancer with high aggressiveness and extremely poor prognosis. The role of circular RNAs (circRNAs) in ICC carcinogenesis and progression remains to be determined.BACKGROUND & AIMSIntrahepatic cholangiocarcinoma (ICC) is a primary liver cancer with high aggressiveness and extremely poor prognosis. The role of circular RNAs (circRNAs) in ICC carcinogenesis and progression remains to be determined.CircRNA microarray was performed to screen significantly upregulated circRNAs in paired ICC and non-tumor tissues. Colony formation, transwell, and xenograft models were used to examine the role of circRNAs in ICC proliferation and metastasis. RNA pulldown, mass spectrometry, chromatin immunoprecipitation, RNA-binding protein immunoprecipitation, chromatin isolation by RNA purification, electrophoretic mobility shift assay, and luciferase reporter assays were used to explore the molecular sponge role of the circRNA (via miRNA binding), and the interaction between circRNA and RNA-binding proteins.METHODSCircRNA microarray was performed to screen significantly upregulated circRNAs in paired ICC and non-tumor tissues. Colony formation, transwell, and xenograft models were used to examine the role of circRNAs in ICC proliferation and metastasis. RNA pulldown, mass spectrometry, chromatin immunoprecipitation, RNA-binding protein immunoprecipitation, chromatin isolation by RNA purification, electrophoretic mobility shift assay, and luciferase reporter assays were used to explore the molecular sponge role of the circRNA (via miRNA binding), and the interaction between circRNA and RNA-binding proteins.Hsa_circ_0050898, which originated from exon 1 to exon 20 of the ACTN4 gene (named circACTN4), was significantly upregulated in ICC. High circACTN4 expression was associated with enhanced tumor proliferation and metastasis in vitro and in vivo, as well as a worse prognosis following ICC resection. In addition, circACTN4 upregulated Yes-associated protein 1 (YAP1) expression by sponging miR-424-5p. More importantly, circACTN4 also recruited Y-box binding protein 1 (YBX1) to stimulate Frizzled-7 (FZD7) transcription. Furthermore, circACTN4 overexpression in ICC cells enhanced the interaction between YAP1 and β-catenin, which are the core components of the Hippo and Wnt signaling pathways, respectively.RESULTSHsa_circ_0050898, which originated from exon 1 to exon 20 of the ACTN4 gene (named circACTN4), was significantly upregulated in ICC. High circACTN4 expression was associated with enhanced tumor proliferation and metastasis in vitro and in vivo, as well as a worse prognosis following ICC resection. In addition, circACTN4 upregulated Yes-associated protein 1 (YAP1) expression by sponging miR-424-5p. More importantly, circACTN4 also recruited Y-box binding protein 1 (YBX1) to stimulate Frizzled-7 (FZD7) transcription. Furthermore, circACTN4 overexpression in ICC cells enhanced the interaction between YAP1 and β-catenin, which are the core components of the Hippo and Wnt signaling pathways, respectively.CircACTN4 was upregulated in ICC and promoted ICC proliferation and metastasis by acting as a molecular sponge of miR-424-5p, as well as by interacting with YBX1 to transcriptionally activate FZD7. These results suggest that circACTN4 is a potential prognostic marker and therapeutic target for ICC.CONCLUSIONSCircACTN4 was upregulated in ICC and promoted ICC proliferation and metastasis by acting as a molecular sponge of miR-424-5p, as well as by interacting with YBX1 to transcriptionally activate FZD7. These results suggest that circACTN4 is a potential prognostic marker and therapeutic target for ICC.Intrahepatic cholangiocarcinoma is a primary liver cancer associated with aggressiveness and extremely poor prognosis. It is essential for therapeutic development that we uncover relevant pathogenic pathways. Herein, we showed that a circular RNA (circACTN4) was highly expressed in intrahepatic cholangiocarcinoma and was positively associated with tumor growth and metastasis through key developmental signaling pathways. Thus, circACTN4 could be a prognostic biomarker and therapeutic target for intrahepatic cholangiocarcinoma.LAY SUMMARYIntrahepatic cholangiocarcinoma is a primary liver cancer associated with aggressiveness and extremely poor prognosis. It is essential for therapeutic development that we uncover relevant pathogenic pathways. Herein, we showed that a circular RNA (circACTN4) was highly expressed in intrahepatic cholangiocarcinoma and was positively associated with tumor growth and metastasis through key developmental signaling pathways. Thus, circACTN4 could be a prognostic biomarker and therapeutic target for intrahepatic cholangiocarcinoma. Intrahepatic cholangiocarcinoma (ICC) is a primary liver cancer with high aggressiveness and extremely poor prognosis. The role of circular RNAs (circRNAs) in ICC carcinogenesis and progression remains to be determined. CircRNA microarray was performed to screen significantly upregulated circRNAs in paired ICC and non-tumor tissues. Colony formation, transwell, and xenograft models were used to examine the role of circRNAs in ICC proliferation and metastasis. RNA pulldown, mass spectrometry, chromatin immunoprecipitation, RNA-binding protein immunoprecipitation, chromatin isolation by RNA purification, electrophoretic mobility shift assay, and luciferase reporter assays were used to explore the molecular sponge role of the circRNA (via miRNA binding), and the interaction between circRNA and RNA-binding proteins. Hsa_circ_0050898, which originated from exon 1 to exon 20 of the ACTN4 gene (named circACTN4), was significantly upregulated in ICC. High circACTN4 expression was associated with enhanced tumor proliferation and metastasis in vitro and in vivo, as well as a worse prognosis following ICC resection. In addition, circACTN4 upregulated Yes-associated protein 1 (YAP1) expression by sponging miR-424-5p. More importantly, circACTN4 also recruited Y-box binding protein 1 (YBX1) to stimulate Frizzled-7 (FZD7) transcription. Furthermore, circACTN4 overexpression in ICC cells enhanced the interaction between YAP1 and β-catenin, which are the core components of the Hippo and Wnt signaling pathways, respectively. CircACTN4 was upregulated in ICC and promoted ICC proliferation and metastasis by acting as a molecular sponge of miR-424-5p, as well as by interacting with YBX1 to transcriptionally activate FZD7. These results suggest that circACTN4 is a potential prognostic marker and therapeutic target for ICC. Intrahepatic cholangiocarcinoma is a primary liver cancer associated with aggressiveness and extremely poor prognosis. It is essential for therapeutic development that we uncover relevant pathogenic pathways. Herein, we showed that a circular RNA (circACTN4) was highly expressed in intrahepatic cholangiocarcinoma and was positively associated with tumor growth and metastasis through key developmental signaling pathways. Thus, circACTN4 could be a prognostic biomarker and therapeutic target for intrahepatic cholangiocarcinoma. |
| Author | Li, Zheng Wang, Kui Li, Fengwei Yang, Tian Li, Jun Shen, Feng Cheng, Zhangjun Xia, Yong Shen, Hao Chen, Qinjunjie Zou, Yiran Wang, Haibo Liang, Leilei |
| Author_xml | – sequence: 1 givenname: Qinjunjie orcidid: 0000-0001-5910-5091 surname: Chen fullname: Chen, Qinjunjie organization: Department of Hepatic Surgery IV, the Eastern Hepatobiliary Surgery Hospital, Naval Medical University, Shanghai, China – sequence: 2 givenname: Haibo surname: Wang fullname: Wang, Haibo organization: Department of Hepatic Surgery IV, the Eastern Hepatobiliary Surgery Hospital, Naval Medical University, Shanghai, China – sequence: 3 givenname: Zheng orcidid: 0000-0001-8373-391X surname: Li fullname: Li, Zheng organization: Department of Hepatic Surgery IV, the Eastern Hepatobiliary Surgery Hospital, Naval Medical University, Shanghai, China – sequence: 4 givenname: Fengwei surname: Li fullname: Li, Fengwei organization: Department of Hepatic Surgery IV, the Eastern Hepatobiliary Surgery Hospital, Naval Medical University, Shanghai, China – sequence: 5 givenname: Leilei surname: Liang fullname: Liang, Leilei organization: Department of Gynecological Oncology, Chinese Academy of Medical Sciences Cancer Institute and Hospital: Cancer Hospital Chinese Academy of Medical Sciences, Beijing, China – sequence: 6 givenname: Yiran orcidid: 0000-0002-5956-3575 surname: Zou fullname: Zou, Yiran organization: Department of Hepatic Surgery IV, the Eastern Hepatobiliary Surgery Hospital, Naval Medical University, Shanghai, China – sequence: 7 givenname: Hao surname: Shen fullname: Shen, Hao organization: Department of Hepatobiliary Surgery, the Eastern Hepatobiliary Surgery Hospital, Naval Medical University, Shanghai, China – sequence: 8 givenname: Jun surname: Li fullname: Li, Jun organization: Department of Hepatic Surgery IV, the Eastern Hepatobiliary Surgery Hospital, Naval Medical University, Shanghai, China – sequence: 9 givenname: Yong surname: Xia fullname: Xia, Yong organization: Department of Hepatic Surgery IV, the Eastern Hepatobiliary Surgery Hospital, Naval Medical University, Shanghai, China – sequence: 10 givenname: Zhangjun surname: Cheng fullname: Cheng, Zhangjun organization: Hepato-Pancreato-Biliary Center, Zhongda Hospital, School of Medicine, Southeast University, Nanjing, China – sequence: 11 givenname: Tian surname: Yang fullname: Yang, Tian organization: Department of Hepatobiliary Surgery, the Eastern Hepatobiliary Surgery Hospital, Naval Medical University, Shanghai, China – sequence: 12 givenname: Kui surname: Wang fullname: Wang, Kui organization: Department of Hepatic Surgery II, the Eastern Hepatobiliary Surgery Hospital, Naval Medical University, Shanghai, China – sequence: 13 givenname: Feng orcidid: 0000-0002-8904-9745 surname: Shen fullname: Shen, Feng email: shenfengehbh@sina.com organization: Department of Hepatic Surgery IV, the Eastern Hepatobiliary Surgery Hospital, Naval Medical University, Shanghai, China |
| BackLink | https://cir.nii.ac.jp/crid/1871991017772007168$$DView record in CiNii https://www.ncbi.nlm.nih.gov/pubmed/34509526$$D View this record in MEDLINE/PubMed |
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| Keywords | YAP1 Wnt circACTN4 FZD7 Hippo Intrahepatic cholangiocarcinoma |
| Language | English |
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| Snippet | Intrahepatic cholangiocarcinoma (ICC) is a primary liver cancer with high aggressiveness and extremely poor prognosis. The role of circular RNAs (circRNAs) in... Background & Aims: Intrahepatic cholangiocarcinoma (ICC) is a primary liver cancer with high aggressiveness and extremely poor prognosis. The role of circular... |
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| SubjectTerms | Actinin Actinin - adverse effects Aged Carcinogenesis Carcinogenesis - genetics Cholangiocarcinoma Cholangiocarcinoma - etiology Cholangiocarcinoma - genetics Chromatin circACTN4 Circular RNA Disease Progression DNA microarrays Electrophoretic mobility Female Frizzled protein Frizzled Receptors Frizzled Receptors - drug effects Frizzled Receptors - metabolism FZD7 Hippo Humans Immunoprecipitation Intrahepatic cholangiocarcinoma Liver cancer Male Mass spectroscopy Metastases Metastasis Middle Aged miRNA Prognosis Proportional Hazards Models Protein purification Proteins Ribonucleic acid RNA RNA, Circular RNA, Circular - adverse effects RNA-binding protein Statistics, Nonparametric Therapeutic targets Transcription Tumors Wnt Wnt protein Wnt Signaling Pathway Wnt Signaling Pathway - drug effects Xenografts Y-Box-Binding Protein 1 Y-Box-Binding Protein 1 - adverse effects Y-Box-Binding Protein 1 - drug effects YAP1 Yes-associated protein β-Catenin |
| Title | Circular RNA ACTN4 promotes intrahepatic cholangiocarcinoma progression by recruiting YBX1 to initiate FZD7 transcription |
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