Skip to main content
Top
Published in: General Thoracic and Cardiovascular Surgery 1/2024

16-07-2023 | Original Article

CircGFPT1 regulates the growth and apoptosis of esophageal squamous cell carcinoma through miR-142-5p/HAX1 axis

Authors: Zheng Feng, Tianyi Zhang, Shaoyi Cheng, Xunliang Yin, Yongan Zhou

Published in: General Thoracic and Cardiovascular Surgery | Issue 1/2024

Login to get access

Abstract

Background

Currently, multiple circular RNAs (circRNAs) have been verified to act as essential regulators in the progression of esophageal squamous cell carcinoma (ESCC). However, there is no study regarding the role of circGFPT1 in the progression of cancers including ESCC. We aimed to investigate the role of circGFPT1 in ESCC progression.

Methods

Quantitative real-time polymerase chain reaction (qRT-PCR) was utilized to measure the expression of circGFPT1, miR-142-5p and HS1-associated protein X-1 (HAX1). 3-(4,5-Dimethyl-2-thiazolyl)-2,5-diphenyl-2-H-tetrazolium bromide (MTT) and 5-ethynyl-2′-deoxyuridine (EdU) assays were employed to evaluate cell proliferation. Cell migration and invasion were detected by wound-healing and transwell assays. Flow cytometry analysis was conducted to assess cell apoptosis. The protein expression of E-cadherin, N-cadherin, Vimentin, C-caspase3, HAX1 and nuclear proliferation marker (Ki67) was analyzed by western blot or immunohistochemistry assay.

Results

CircGFPT1 was up-regulated in ESCC tissues and cells. Silencing of circGFPT1 repressed cell proliferation and induced cell apoptosis in ESCC cells. CircGFPT1 acted as a sponge of miR-142-5p. The effects of circGFPT1 knockdown on ESCC cell proliferation and apoptosis were reversed by miR-142-5p inhibition. HAX1 was confirmed to be a target gene of miR-142-5p. CircGFPT1 knockdown inhibited HAX1 expression by targeting miR-142-5p. Additionally, circGFPT1 knockdown hampered tumorigenesis in vivo.

Conclusion

CircGFPT1 promoted ESCC cell growth and repressed apoptosis by up-regulating HAX1 through sponging miR-142-5p.
Appendix
Available only for authorised users
Literature
1.
go back to reference Murphy G, McCormack V, Abedi-Ardekani B, Arnold M, Camargo MC, Dar NA, et al. International cancer seminars: a focus on esophageal squamous cell carcinoma. Ann Oncol. 2017;28:2086–93.CrossRefPubMedPubMedCentral Murphy G, McCormack V, Abedi-Ardekani B, Arnold M, Camargo MC, Dar NA, et al. International cancer seminars: a focus on esophageal squamous cell carcinoma. Ann Oncol. 2017;28:2086–93.CrossRefPubMedPubMedCentral
2.
go back to reference Abnet CC, Arnold M, Wei WQ. Epidemiology of esophageal squamous cell carcinoma. Gastroenterology. 2018;154:360–73.CrossRefPubMed Abnet CC, Arnold M, Wei WQ. Epidemiology of esophageal squamous cell carcinoma. Gastroenterology. 2018;154:360–73.CrossRefPubMed
3.
go back to reference Reichenbach ZW, Murray MG, Saxena R, Farkas D, Karassik EG, Klochkova A, et al. Clinical and translational advances in esophageal squamous cell carcinoma. Adv Cancer Res. 2019;144:95–135.CrossRefPubMed Reichenbach ZW, Murray MG, Saxena R, Farkas D, Karassik EG, Klochkova A, et al. Clinical and translational advances in esophageal squamous cell carcinoma. Adv Cancer Res. 2019;144:95–135.CrossRefPubMed
4.
go back to reference Li C, Tian Y, Liang Y, Li Q. Circ_0008035 contributes to cell proliferation and inhibits apoptosis and ferroptosis in gastric cancer via miR-599/EIF4A1 axis. Cancer Cell Int. 2020;20:84.CrossRefPubMedPubMedCentral Li C, Tian Y, Liang Y, Li Q. Circ_0008035 contributes to cell proliferation and inhibits apoptosis and ferroptosis in gastric cancer via miR-599/EIF4A1 axis. Cancer Cell Int. 2020;20:84.CrossRefPubMedPubMedCentral
6.
go back to reference Zhong Z, Lv M, Chen J. Screening differential circular RNA expression profiles reveals the regulatory role of circTCF25-miR-103a-3p/miR-107-CDK6 pathway in bladder carcinoma. Sci Rep. 2016;6:30919.CrossRefPubMedPubMedCentral Zhong Z, Lv M, Chen J. Screening differential circular RNA expression profiles reveals the regulatory role of circTCF25-miR-103a-3p/miR-107-CDK6 pathway in bladder carcinoma. Sci Rep. 2016;6:30919.CrossRefPubMedPubMedCentral
7.
go back to reference Hansen TB, Jensen TI, Clausen BH, Bramsen JB, Finsen B, Damgaard CK, et al. Natural RNA circles function as efficient microRNA sponges. Nature. 2013;495:384–8.CrossRefPubMed Hansen TB, Jensen TI, Clausen BH, Bramsen JB, Finsen B, Damgaard CK, et al. Natural RNA circles function as efficient microRNA sponges. Nature. 2013;495:384–8.CrossRefPubMed
8.
go back to reference Ahmed I, Karedath T, Andrews SS, Al-Azwani IK, Mohamoud YA, Querleu D, et al. Altered expression pattern of circular RNAs in primary and metastatic sites of epithelial ovarian carcinoma. Oncotarget. 2016;7:36366–81.CrossRefPubMedPubMedCentral Ahmed I, Karedath T, Andrews SS, Al-Azwani IK, Mohamoud YA, Querleu D, et al. Altered expression pattern of circular RNAs in primary and metastatic sites of epithelial ovarian carcinoma. Oncotarget. 2016;7:36366–81.CrossRefPubMedPubMedCentral
9.
go back to reference Zhang Z, Li X, Xiong F, Ren Z, Han Y. Hsa_circ_0012563 promotes migration and invasion of esophageal squamous cell carcinoma by regulating XRCC1/EMT pathway. J Clin Lab Anal. 2020;34:e23308.CrossRefPubMedPubMedCentral Zhang Z, Li X, Xiong F, Ren Z, Han Y. Hsa_circ_0012563 promotes migration and invasion of esophageal squamous cell carcinoma by regulating XRCC1/EMT pathway. J Clin Lab Anal. 2020;34:e23308.CrossRefPubMedPubMedCentral
10.
go back to reference Zhang C, Lian H, Xie L, Yin N, Cui Y. LncRNA ELFN1-AS1 promotes esophageal cancer progression by up-regulating GFPT1 via sponging miR-183-3p. Biol Chem. 2020;401:1053–61.CrossRefPubMed Zhang C, Lian H, Xie L, Yin N, Cui Y. LncRNA ELFN1-AS1 promotes esophageal cancer progression by up-regulating GFPT1 via sponging miR-183-3p. Biol Chem. 2020;401:1053–61.CrossRefPubMed
11.
go back to reference Yang C, Peng P, Li L, Shao M, Zhao J, Wang L, et al. High expression of GFAT1 predicts poor prognosis in patients with pancreatic cancer. Sci Rep. 2016;6:39044.CrossRefPubMedPubMedCentral Yang C, Peng P, Li L, Shao M, Zhao J, Wang L, et al. High expression of GFAT1 predicts poor prognosis in patients with pancreatic cancer. Sci Rep. 2016;6:39044.CrossRefPubMedPubMedCentral
12.
go back to reference Li D, Guan M, Cao X, Zha ZQ, Zhang P, Xiang H, et al. GFPT1 promotes the proliferation of cervical cancer via regulating the ubiquitination and degradation of PTEN. Carcinogenesis. 2022;43:969–79.CrossRefPubMed Li D, Guan M, Cao X, Zha ZQ, Zhang P, Xiang H, et al. GFPT1 promotes the proliferation of cervical cancer via regulating the ubiquitination and degradation of PTEN. Carcinogenesis. 2022;43:969–79.CrossRefPubMed
13.
go back to reference Hu X, Wu D, He X, Zhao H, He Z, Lin J, et al. circGSK3β promotes metastasis in esophageal squamous cell carcinoma by augmenting β-catenin signaling. Mol Cancer. 2019;18:160.CrossRefPubMedPubMedCentral Hu X, Wu D, He X, Zhao H, He Z, Lin J, et al. circGSK3β promotes metastasis in esophageal squamous cell carcinoma by augmenting β-catenin signaling. Mol Cancer. 2019;18:160.CrossRefPubMedPubMedCentral
14.
go back to reference Acunzo M, Romano G, Wernicke D, Croce CM. MicroRNA and cancer—a brief overview. Adv Biol Regul. 2015;57:1–9.CrossRefPubMed Acunzo M, Romano G, Wernicke D, Croce CM. MicroRNA and cancer—a brief overview. Adv Biol Regul. 2015;57:1–9.CrossRefPubMed
16.
go back to reference Labbe M, Hoey C, Ray J, Potiron V, Supiot S, Liu SK, et al. microRNAs identified in prostate cancer: Correlative studies on response to ionizing radiation. Mol Cancer. 2020;19:63.CrossRefPubMedPubMedCentral Labbe M, Hoey C, Ray J, Potiron V, Supiot S, Liu SK, et al. microRNAs identified in prostate cancer: Correlative studies on response to ionizing radiation. Mol Cancer. 2020;19:63.CrossRefPubMedPubMedCentral
17.
go back to reference Yu J, Chen S, Niu Y, Liu M, Zhang J, Yang Z, et al. Functional significance and therapeutic potential of miRNA-20b-5p in esophageal squamous cell carcinoma. Mol Ther Nucl Acids. 2020;21:315–31.CrossRef Yu J, Chen S, Niu Y, Liu M, Zhang J, Yang Z, et al. Functional significance and therapeutic potential of miRNA-20b-5p in esophageal squamous cell carcinoma. Mol Ther Nucl Acids. 2020;21:315–31.CrossRef
18.
go back to reference Wang Z, Liu Z, Fang X, Yang H. MiR-142-5p suppresses tumorigenesis by targeting PIK3CA in non-small cell lung cancer. Cell Physiol Biochem. 2017;43:2505–15.CrossRefPubMed Wang Z, Liu Z, Fang X, Yang H. MiR-142-5p suppresses tumorigenesis by targeting PIK3CA in non-small cell lung cancer. Cell Physiol Biochem. 2017;43:2505–15.CrossRefPubMed
19.
go back to reference Yao R, Xu L, Wei B, Qian Z, Wang J, Hui H, et al. miR-142-5p regulates pancreatic cancer cell proliferation and apoptosis by regulation of RAP1A. Pathol Res Pract. 2019;215:152416.CrossRefPubMed Yao R, Xu L, Wei B, Qian Z, Wang J, Hui H, et al. miR-142-5p regulates pancreatic cancer cell proliferation and apoptosis by regulation of RAP1A. Pathol Res Pract. 2019;215:152416.CrossRefPubMed
20.
go back to reference Yan J, Yang B, Lin S, Xing R, Lu Y. Downregulation of miR-142-5p promotes tumor metastasis through directly regulating CYR61 expression in gastric cancer. Gastric Cancer. 2019;22:302–13.CrossRefPubMed Yan J, Yang B, Lin S, Xing R, Lu Y. Downregulation of miR-142-5p promotes tumor metastasis through directly regulating CYR61 expression in gastric cancer. Gastric Cancer. 2019;22:302–13.CrossRefPubMed
21.
go back to reference Li X, Chen W, Jin Y, Xue R, Su J, Mu Z, et al. miR-142-5p enhances cisplatin-induced apoptosis in ovarian cancer cells by targeting multiple anti-apoptotic genes. Biochem Pharmacol. 2019;161:98–112.CrossRefPubMed Li X, Chen W, Jin Y, Xue R, Su J, Mu Z, et al. miR-142-5p enhances cisplatin-induced apoptosis in ovarian cancer cells by targeting multiple anti-apoptotic genes. Biochem Pharmacol. 2019;161:98–112.CrossRefPubMed
22.
go back to reference Xiao S, Liu N, Yang X, Ji G, Li M. Polygalacin D suppresses esophageal squamous cell carcinoma growth and metastasis through regulating miR-142-5p/Nrf2 axis. Free Radic Biol Med. 2021;164:58–75.CrossRefPubMed Xiao S, Liu N, Yang X, Ji G, Li M. Polygalacin D suppresses esophageal squamous cell carcinoma growth and metastasis through regulating miR-142-5p/Nrf2 axis. Free Radic Biol Med. 2021;164:58–75.CrossRefPubMed
23.
go back to reference Liang Z, Zhong Y, Meng L, Chen Y, Liu Y, Wu A, et al. HAX1 enhances the survival and metastasis of non-small cell lung cancer through the AKT/mTOR and MDM2/p53 signaling pathway. Thorac Cancer. 2020;11:3155–67.CrossRefPubMedPubMedCentral Liang Z, Zhong Y, Meng L, Chen Y, Liu Y, Wu A, et al. HAX1 enhances the survival and metastasis of non-small cell lung cancer through the AKT/mTOR and MDM2/p53 signaling pathway. Thorac Cancer. 2020;11:3155–67.CrossRefPubMedPubMedCentral
24.
go back to reference Yan J, Ma C, Cheng J, Li Z, Liu C. HAX-1 inhibits apoptosis in prostate cancer through the suppression of caspase-9 activation. Oncol Rep. 2015;34:2776–81.CrossRefPubMed Yan J, Ma C, Cheng J, Li Z, Liu C. HAX-1 inhibits apoptosis in prostate cancer through the suppression of caspase-9 activation. Oncol Rep. 2015;34:2776–81.CrossRefPubMed
25.
go back to reference Luo X, Li Z, Li X, Wang G, Liu W, Dong S, et al. hSav1 interacts with HAX1 and attenuates its anti-apoptotic effects in MCF-7 breast cancer cells. Int J Mol Med. 2011;28:349–55.PubMed Luo X, Li Z, Li X, Wang G, Liu W, Dong S, et al. hSav1 interacts with HAX1 and attenuates its anti-apoptotic effects in MCF-7 breast cancer cells. Int J Mol Med. 2011;28:349–55.PubMed
26.
go back to reference Huang D-W, Huang M, Lin X-S, Huang Q. CD155 expression and its correlation with clinicopathologic characteristics, angiogenesis, and prognosis in human cholangiocarcinoma. Onco Targets Ther. 2017;10:3817–25.CrossRefPubMedPubMedCentral Huang D-W, Huang M, Lin X-S, Huang Q. CD155 expression and its correlation with clinicopathologic characteristics, angiogenesis, and prognosis in human cholangiocarcinoma. Onco Targets Ther. 2017;10:3817–25.CrossRefPubMedPubMedCentral
27.
go back to reference Chen BJ, Byrne FL, Takenaka K, Modesitt SC, Olzomer EM, Mills JD, et al. Analysis of the circular RNA transcriptome in endometrial cancer. Oncotarget. 2018;9:5786–96.CrossRefPubMed Chen BJ, Byrne FL, Takenaka K, Modesitt SC, Olzomer EM, Mills JD, et al. Analysis of the circular RNA transcriptome in endometrial cancer. Oncotarget. 2018;9:5786–96.CrossRefPubMed
28.
go back to reference Zhang M, Huang N, Yang X, Luo J, Yan S, Xiao F, et al. A novel protein encoded by the circular form of the SHPRH gene suppresses glioma tumorigenesis. Oncogene. 2018;37:1805–14.CrossRefPubMed Zhang M, Huang N, Yang X, Luo J, Yan S, Xiao F, et al. A novel protein encoded by the circular form of the SHPRH gene suppresses glioma tumorigenesis. Oncogene. 2018;37:1805–14.CrossRefPubMed
29.
go back to reference Verduci L, Strano S, Yarden Y, Blandino G. The circRNA-microRNA code: emerging implications for cancer diagnosis and treatment. Mol Oncol. 2019;13:669–80.CrossRefPubMedPubMedCentral Verduci L, Strano S, Yarden Y, Blandino G. The circRNA-microRNA code: emerging implications for cancer diagnosis and treatment. Mol Oncol. 2019;13:669–80.CrossRefPubMedPubMedCentral
30.
31.
go back to reference Zheng Q, Bao C, Guo W, Li S, Chen J, Chen B, et al. Circular RNA profiling reveals an abundant circHIPK3 that regulates cell growth by sponging multiple miRNAs. Nat Commun. 2016;7:11215.CrossRefPubMedPubMedCentral Zheng Q, Bao C, Guo W, Li S, Chen J, Chen B, et al. Circular RNA profiling reveals an abundant circHIPK3 that regulates cell growth by sponging multiple miRNAs. Nat Commun. 2016;7:11215.CrossRefPubMedPubMedCentral
32.
go back to reference Zhu J, Zhou L, Wei B, Qian Z, Wang J, Hui H, et al. miR1425p inhibits pancreatic cancer cell migration and invasion by targeting PIK3CA. Mol Med Rep. 2020;22:2085–92.CrossRefPubMed Zhu J, Zhou L, Wei B, Qian Z, Wang J, Hui H, et al. miR1425p inhibits pancreatic cancer cell migration and invasion by targeting PIK3CA. Mol Med Rep. 2020;22:2085–92.CrossRefPubMed
33.
go back to reference Liu J, Jiang X, Zou A, Mai Z, Huang Z, Sun L, et al. circIGHG-induced epithelial-to-mesenchymal transition promotes oral squamous cell carcinoma progression via miR-142-5p/IGF2BP3 signaling. Cancer Res. 2021;81:344–55.CrossRefPubMed Liu J, Jiang X, Zou A, Mai Z, Huang Z, Sun L, et al. circIGHG-induced epithelial-to-mesenchymal transition promotes oral squamous cell carcinoma progression via miR-142-5p/IGF2BP3 signaling. Cancer Res. 2021;81:344–55.CrossRefPubMed
34.
go back to reference Zhang Q, Liu H, Zhang J, Shan L, Yibureyimu B, Nurlan A, et al. MiR-142-5p suppresses lung cancer cell metastasis by targeting yin yang 1 to regulate epithelial-mesenchymal transition. Cell Reprogram. 2020;22:328–36.CrossRefPubMed Zhang Q, Liu H, Zhang J, Shan L, Yibureyimu B, Nurlan A, et al. MiR-142-5p suppresses lung cancer cell metastasis by targeting yin yang 1 to regulate epithelial-mesenchymal transition. Cell Reprogram. 2020;22:328–36.CrossRefPubMed
35.
go back to reference Zha Z, Li J. MicroRNA125a5p regulates liver cancer cell growth, migration and invasion and EMT by targeting HAX1. Int J Mol Med. 2020;46:1849–61.PubMedPubMedCentral Zha Z, Li J. MicroRNA125a5p regulates liver cancer cell growth, migration and invasion and EMT by targeting HAX1. Int J Mol Med. 2020;46:1849–61.PubMedPubMedCentral
36.
go back to reference Li R, Zheng JZ, Huang X. Suppression of HAX-1 induced by miR-325 resensitizes bladder cancer cells to cisplatin-induced apoptosis. Eur Rev Med Pharmacol Sci. 2020;24:9303–14.PubMed Li R, Zheng JZ, Huang X. Suppression of HAX-1 induced by miR-325 resensitizes bladder cancer cells to cisplatin-induced apoptosis. Eur Rev Med Pharmacol Sci. 2020;24:9303–14.PubMed
37.
38.
go back to reference Li F, Shang Y, Shi F, Zhang L, Yan J, Sun Q, et al. Expression of integrin β6 and HAX-1 correlates with aggressive features and poor prognosis in esophageal squamous cell carcinoma. Cancer Manag Res. 2020;12:9599–608.CrossRefPubMedPubMedCentral Li F, Shang Y, Shi F, Zhang L, Yan J, Sun Q, et al. Expression of integrin β6 and HAX-1 correlates with aggressive features and poor prognosis in esophageal squamous cell carcinoma. Cancer Manag Res. 2020;12:9599–608.CrossRefPubMedPubMedCentral
39.
go back to reference Yu Z, Ni F, Chen Y, Zhang J, Cai J, Shi W. miR-125b suppresses cell proliferation and metastasis by targeting HAX-1 in esophageal squamous cell carcinoma. Pathol Res Pract. 2020;216:152792.CrossRefPubMed Yu Z, Ni F, Chen Y, Zhang J, Cai J, Shi W. miR-125b suppresses cell proliferation and metastasis by targeting HAX-1 in esophageal squamous cell carcinoma. Pathol Res Pract. 2020;216:152792.CrossRefPubMed
Metadata
Title
CircGFPT1 regulates the growth and apoptosis of esophageal squamous cell carcinoma through miR-142-5p/HAX1 axis
Authors
Zheng Feng
Tianyi Zhang
Shaoyi Cheng
Xunliang Yin
Yongan Zhou
Publication date
16-07-2023
Publisher
Springer Nature Singapore
Published in
General Thoracic and Cardiovascular Surgery / Issue 1/2024
Print ISSN: 1863-6705
Electronic ISSN: 1863-6713
DOI
https://doi.org/10.1007/s11748-023-01955-2

Other articles of this Issue 1/2024

General Thoracic and Cardiovascular Surgery 1/2024 Go to the issue