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Erschienen in: Digestive Diseases and Sciences 6/2022

22.05.2021 | Original Article

Circular RNA circ_0006948 Promotes Esophageal Squamous Cell Carcinoma Progression by Regulating microRNA-3612/LASP1 Axis

Erschienen in: Digestive Diseases and Sciences | Ausgabe 6/2022

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Abstract

Background

Esophageal squamous cell carcinoma (ESCC) is the most prevalent malignancy worldwide. Circular RNAs (circRNAs) circ_0006948 is reported to be upregulated in ESCC cells.

Aims

This study is designed to explore the role and mechanism of circ_0006948 in ESCC progression.

Methods

Circ_0006948, linear FNDC3B, microRNA-3612 (miR-3612), and LIM and SH3 protein 1 (LASP1) levels were detected by real-time quantitative polymerase chain reaction (RT-qPCR). Cell viability, colony number, migration, invasion, and apoptosis were examined by Cell Counting Kit-8 (CCK-8), colony formation, transwell, and flow cytometry assays, severally. Glucose consumption, lactate production, and ATP level were measured by the corresponding kits. Protein levels of hexokinase 2 (HK2) and lactate dehydrogenase A (LDHA), and LASP1 were assessed by western blot assay. The cytoplasmic localization of circ_0006948 was identified by the subcellular fractionation assay. The binding relationship between miR-3612 and circ_0006948 or LASP1 was predicted by starBase or TargetScan and then verified by a dual-luciferase reporter assay. The biological role of circ_0006948 on ESCC tumor growth was examined by the xenograft tumor model in vivo.

Results

Circ_0006948 and LASP1 were increased, and miR-3612 was decreased in ESCC tissues and cells. Furthermore, circ_0006948 knockdown could suppress cell viability, colony number, migration, invasion, glycolysis, and boost apoptosis in ESCC cells. Mechanically, circ_0006948 could act as a sponge of miR-3612 to regulate LASP1 expression. In addition, circ_0006948 silencing inhibited ESCC tumor growth in vivo.

Conclusion

Circ_0006948 boosted ESCC progression partly by regulating the miR-3612/LASP1 axis, providing an underlying therapeutic target for the ESCC treatment.
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Literatur
1.
Zurück zum Zitat Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68:394–424.CrossRef Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68:394–424.CrossRef
2.
Zurück zum Zitat Lagergren J, Smyth E, Cunningham D, Lagergren P. Oesophageal cancer. Lancet. 2017;390:2383–2396.CrossRef Lagergren J, Smyth E, Cunningham D, Lagergren P. Oesophageal cancer. Lancet. 2017;390:2383–2396.CrossRef
3.
Zurück zum Zitat Codipilly DC, Qin Y, Dawsey SM et al. Screening for esophageal squamous cell carcinoma: recent advances. Gastrointest Endosc. 2018;88:413–426.CrossRef Codipilly DC, Qin Y, Dawsey SM et al. Screening for esophageal squamous cell carcinoma: recent advances. Gastrointest Endosc. 2018;88:413–426.CrossRef
4.
Zurück zum Zitat Chen YH, Li SH, Chiu YC et al. Comparative study of esophageal stent and feeding gastrostomy/jejunostomy for tracheoesophageal fistula caused by esophageal squamous cell carcinoma. PLoS ONE 2012;7:e42766.CrossRef Chen YH, Li SH, Chiu YC et al. Comparative study of esophageal stent and feeding gastrostomy/jejunostomy for tracheoesophageal fistula caused by esophageal squamous cell carcinoma. PLoS ONE 2012;7:e42766.CrossRef
5.
Zurück zum Zitat Kagami H, Akutsu T, Maegawa S, Hosokawa H, Nacher JC. Determining associations between human diseases and non-coding RNAS with critical roles in network control. Sci Rep. 2015;5:14577.CrossRef Kagami H, Akutsu T, Maegawa S, Hosokawa H, Nacher JC. Determining associations between human diseases and non-coding RNAS with critical roles in network control. Sci Rep. 2015;5:14577.CrossRef
6.
Zurück zum Zitat Wilusz JE. A 360° view of circular RNAs: from biogenesis to functions. Wiley Interdiscip Rev RNA. 2018;9:e1478.CrossRef Wilusz JE. A 360° view of circular RNAs: from biogenesis to functions. Wiley Interdiscip Rev RNA. 2018;9:e1478.CrossRef
7.
Zurück zum Zitat Holdt LM, Kohlmaier A, Teupser D. Molecular roles and function of circular RNAs in eukaryotic cells. Cell Mol Life Sci. 2018;75:1071–1098.CrossRef Holdt LM, Kohlmaier A, Teupser D. Molecular roles and function of circular RNAs in eukaryotic cells. Cell Mol Life Sci. 2018;75:1071–1098.CrossRef
8.
Zurück zum Zitat Memczak S, Jens M, Elefsinioti A et al. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature. 2013;495:333–338.CrossRef Memczak S, Jens M, Elefsinioti A et al. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature. 2013;495:333–338.CrossRef
9.
Zurück zum Zitat Ng WL, Mohd Mohidin TB, Shukla K. Functional role of circular RNAs in cancer development and progression. RNA Biol. 2018;15:995–1005.PubMedPubMedCentral Ng WL, Mohd Mohidin TB, Shukla K. Functional role of circular RNAs in cancer development and progression. RNA Biol. 2018;15:995–1005.PubMedPubMedCentral
10.
Zurück zum Zitat Solé C, Lawrie CH. Circular RNAs and cancer: opportunities and challenges. Adv Clin Chem. 2020;99:87–146.CrossRef Solé C, Lawrie CH. Circular RNAs and cancer: opportunities and challenges. Adv Clin Chem. 2020;99:87–146.CrossRef
11.
Zurück zum Zitat Shi N, Shan B, Gu B, Song Y. Circular RNA circ-PRKCI functions as a competitive endogenous RNA to regulate AKT3 expression by sponging miR-3680-3p in esophageal squamous cell carcinoma. J Cell Biochem. 2019;120:10021–10030.CrossRef Shi N, Shan B, Gu B, Song Y. Circular RNA circ-PRKCI functions as a competitive endogenous RNA to regulate AKT3 expression by sponging miR-3680-3p in esophageal squamous cell carcinoma. J Cell Biochem. 2019;120:10021–10030.CrossRef
12.
Zurück zum Zitat Huang H, Wei L, Qin T, Yang N, Li Z, Xu Z. Circular RNA ciRS-7 triggers the migration and invasion of esophageal squamous cell carcinoma via miR-7/KLF4 and NF-κB signals. Cancer Biol Ther. 2019;20:73–80.CrossRef Huang H, Wei L, Qin T, Yang N, Li Z, Xu Z. Circular RNA ciRS-7 triggers the migration and invasion of esophageal squamous cell carcinoma via miR-7/KLF4 and NF-κB signals. Cancer Biol Ther. 2019;20:73–80.CrossRef
13.
Zurück zum Zitat Pan Z, Lin J, Wu D et al. Hsa_circ_0006948 enhances cancer progression and epithelial-mesenchymal transition through the miR-490-3p/HMGA2 axis in esophageal squamous cell carcinoma. Aging (Albany NY). 2019;11:11937–11954.CrossRef Pan Z, Lin J, Wu D et al. Hsa_circ_0006948 enhances cancer progression and epithelial-mesenchymal transition through the miR-490-3p/HMGA2 axis in esophageal squamous cell carcinoma. Aging (Albany NY). 2019;11:11937–11954.CrossRef
14.
Zurück zum Zitat Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004;116:281–297.CrossRef Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004;116:281–297.CrossRef
15.
Zurück zum Zitat Zhong X, Huang G, Ma Q et al. Identification of crucial miRNAs and genes in esophageal squamous cell carcinoma by miRNA-mRNA integrated analysis. Medicine (Baltimore) 2019;98:e16269.CrossRef Zhong X, Huang G, Ma Q et al. Identification of crucial miRNAs and genes in esophageal squamous cell carcinoma by miRNA-mRNA integrated analysis. Medicine (Baltimore) 2019;98:e16269.CrossRef
16.
Zurück zum Zitat Yan Z, Yang Q, Xue M, Wang S, Hong W. YY1-induced lncRNA ZFPM2-AS1 facilitates cell proliferation and invasion in small cell lung cancer via upregulating of TRAF4. Cancer Cell Int. 2020;20:108.CrossRef Yan Z, Yang Q, Xue M, Wang S, Hong W. YY1-induced lncRNA ZFPM2-AS1 facilitates cell proliferation and invasion in small cell lung cancer via upregulating of TRAF4. Cancer Cell Int. 2020;20:108.CrossRef
17.
Zurück zum Zitat Sun G, Wu C. ZFPM2-AS1 facilitates cell growth in esophageal squamous cell carcinoma via up-regulating TRAF4. Biosci Rep. 2020;40:BSR20194352.CrossRef Sun G, Wu C. ZFPM2-AS1 facilitates cell growth in esophageal squamous cell carcinoma via up-regulating TRAF4. Biosci Rep. 2020;40:BSR20194352.CrossRef
18.
Zurück zum Zitat Mihlan S, Reiß C, Thalheimer P et al. Nuclear import of LASP-1 is regulated by phosphorylation and dynamic protein-protein interactions. Oncogene. 2013;32:2107–2113.CrossRef Mihlan S, Reiß C, Thalheimer P et al. Nuclear import of LASP-1 is regulated by phosphorylation and dynamic protein-protein interactions. Oncogene. 2013;32:2107–2113.CrossRef
19.
Zurück zum Zitat Traenka C, Remke M, Korshunov A et al. Role of LIM and SH3 protein 1 (LASP1) in the metastatic dissemination of medulloblastoma. Cancer Res. 2010;70:8003–8014.CrossRef Traenka C, Remke M, Korshunov A et al. Role of LIM and SH3 protein 1 (LASP1) in the metastatic dissemination of medulloblastoma. Cancer Res. 2010;70:8003–8014.CrossRef
20.
Zurück zum Zitat Shen Q, Sun Y, Xu S. LINC01503/miR-342-3p facilitates malignancy in non-small-cell lung cancer cells via regulating LASP1. Respir Res. 2020;21:235.CrossRef Shen Q, Sun Y, Xu S. LINC01503/miR-342-3p facilitates malignancy in non-small-cell lung cancer cells via regulating LASP1. Respir Res. 2020;21:235.CrossRef
21.
Zurück zum Zitat Tilley AMC, Howard CM. The CXCR4-dependent LASP1-Ago2 interaction in triple-negative breast cancer. Cancers. 2020;12:2455.CrossRef Tilley AMC, Howard CM. The CXCR4-dependent LASP1-Ago2 interaction in triple-negative breast cancer. Cancers. 2020;12:2455.CrossRef
22.
Zurück zum Zitat Du YY, Zhao LM, Chen L et al. The tumor-suppressive function of miR-1 by targeting LASP1 and TAGLN2 in esophageal squamous cell carcinoma. J Gastroenterol Hepatol. 2016;31:384–393.CrossRef Du YY, Zhao LM, Chen L et al. The tumor-suppressive function of miR-1 by targeting LASP1 and TAGLN2 in esophageal squamous cell carcinoma. J Gastroenterol Hepatol. 2016;31:384–393.CrossRef
23.
Zurück zum Zitat Qu Y, Liu J. lncRNA MAFG-AS1 contributes to esophageal squamous-cell carcinoma progression via regulating miR143/LASP1. Onco Targets Ther. 2020;13:8359–8370.CrossRef Qu Y, Liu J. lncRNA MAFG-AS1 contributes to esophageal squamous-cell carcinoma progression via regulating miR143/LASP1. Onco Targets Ther. 2020;13:8359–8370.CrossRef
24.
Zurück zum Zitat Takeshita N, Mori M, Kano M et al. miR-203 inhibits the migration and invasion of esophageal squamous cell carcinoma by regulating LASP1. Int J Oncol. 2012;41:1653–1661.CrossRef Takeshita N, Mori M, Kano M et al. miR-203 inhibits the migration and invasion of esophageal squamous cell carcinoma by regulating LASP1. Int J Oncol. 2012;41:1653–1661.CrossRef
25.
Zurück zum Zitat He B, Yin B, Wang B et al. Overexpression of LASP1 is associated with proliferation, migration and invasion in esophageal squamous cell carcinoma. Oncol Rep. 2013;29:1115–1123.CrossRef He B, Yin B, Wang B et al. Overexpression of LASP1 is associated with proliferation, migration and invasion in esophageal squamous cell carcinoma. Oncol Rep. 2013;29:1115–1123.CrossRef
26.
Zurück zum Zitat Shi J, Ye J, Fei H et al. YWHAZ promotes ovarian cancer metastasis by modulating glycolysis. Oncol Rep. 2019;41:1101–1112.PubMed Shi J, Ye J, Fei H et al. YWHAZ promotes ovarian cancer metastasis by modulating glycolysis. Oncol Rep. 2019;41:1101–1112.PubMed
27.
Zurück zum Zitat Dai S, Peng Y, Zhu Y et al. Glycolysis promotes the progression of pancreatic cancer and reduces cancer cell sensitivity to gemcitabine. Biomed Pharmacother. 2020;121:109521.CrossRef Dai S, Peng Y, Zhu Y et al. Glycolysis promotes the progression of pancreatic cancer and reduces cancer cell sensitivity to gemcitabine. Biomed Pharmacother. 2020;121:109521.CrossRef
28.
Zurück zum Zitat Cui H, Gao Q, Zhang L, Han F, Wang L. Knockdown of FOXK1 suppresses liver cancer cell viability by inhibiting glycolysis. Life Sci. 2018;213:66–73.CrossRef Cui H, Gao Q, Zhang L, Han F, Wang L. Knockdown of FOXK1 suppresses liver cancer cell viability by inhibiting glycolysis. Life Sci. 2018;213:66–73.CrossRef
29.
Zurück zum Zitat Panda AC. Circular RNAs Act as miRNA Sponges. Adv Exp Med Biol. 2018;1087:67–79.CrossRef Panda AC. Circular RNAs Act as miRNA Sponges. Adv Exp Med Biol. 2018;1087:67–79.CrossRef
30.
Zurück zum Zitat Kristensen LS, Hansen TB, Venø MT, Kjems J. Circular RNAs in cancer: opportunities and challenges in the field. Oncogene. 2018;37:555–565.CrossRef Kristensen LS, Hansen TB, Venø MT, Kjems J. Circular RNAs in cancer: opportunities and challenges in the field. Oncogene. 2018;37:555–565.CrossRef
31.
Zurück zum Zitat Chen Q, Liu T, Bao Y et al. CircRNA cRAPGEF5 inhibits the growth and metastasis of renal cell carcinoma via the miR-27a-3p/TXNIP pathway. Cancer Lett. 2020;469:68–77.CrossRef Chen Q, Liu T, Bao Y et al. CircRNA cRAPGEF5 inhibits the growth and metastasis of renal cell carcinoma via the miR-27a-3p/TXNIP pathway. Cancer Lett. 2020;469:68–77.CrossRef
32.
Zurück zum Zitat Chen X, Yu J, Tian H et al. Circle RNA hsa_circRNA_100290 serves as a ceRNA for miR-378a to regulate oral squamous cell carcinoma cells growth via Glucose transporter-1 (GLUT1) and glycolysis. J Cell Physiol. 2019;234:19130–19140.CrossRef Chen X, Yu J, Tian H et al. Circle RNA hsa_circRNA_100290 serves as a ceRNA for miR-378a to regulate oral squamous cell carcinoma cells growth via Glucose transporter-1 (GLUT1) and glycolysis. J Cell Physiol. 2019;234:19130–19140.CrossRef
33.
Zurück zum Zitat Jia Y, Liu M, Wang S. CircRNA hsa_circRNA_0001776 inhibits proliferation and promotes apoptosis in endometrial cancer via downregulating LRIG2 by sponging miR-182. Cancer Cell Int. 2020;20:412.CrossRef Jia Y, Liu M, Wang S. CircRNA hsa_circRNA_0001776 inhibits proliferation and promotes apoptosis in endometrial cancer via downregulating LRIG2 by sponging miR-182. Cancer Cell Int. 2020;20:412.CrossRef
34.
Zurück zum Zitat Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science. 2009;324:1029–1033.CrossRef Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science. 2009;324:1029–1033.CrossRef
35.
Zurück zum Zitat Lunt SY, Vander Heiden MG. Aerobic glycolysis: meeting the metabolic requirements of cell proliferation. Annu Rev Cell Dev Biol. 2011;27:441–464.CrossRef Lunt SY, Vander Heiden MG. Aerobic glycolysis: meeting the metabolic requirements of cell proliferation. Annu Rev Cell Dev Biol. 2011;27:441–464.CrossRef
36.
Zurück zum Zitat de la Cruz-López KG, Castro-Muñoz LJ, Reyes-Hernández DO, García-Carrancá A, Manzo-Merino J. Lactate in the regulation of tumor microenvironment and therapeutic approaches. Front Oncol. 2019;9:1143.CrossRef de la Cruz-López KG, Castro-Muñoz LJ, Reyes-Hernández DO, García-Carrancá A, Manzo-Merino J. Lactate in the regulation of tumor microenvironment and therapeutic approaches. Front Oncol. 2019;9:1143.CrossRef
37.
Zurück zum Zitat Kulcheski FR, Christoff AP, Margis R. Circular RNAs are miRNA sponges and can be used as a new class of biomarker. J Biotechnol. 2016;238:42–51.CrossRef Kulcheski FR, Christoff AP, Margis R. Circular RNAs are miRNA sponges and can be used as a new class of biomarker. J Biotechnol. 2016;238:42–51.CrossRef
38.
Zurück zum Zitat Wang A, Dai H, Gong Y et al. ANLN-induced EZH2 upregulation promotes pancreatic cancer progression by mediating miR-218-5p/LASP1 signaling axis. J Exp Clin Cancer Res. 2019;38:347.CrossRef Wang A, Dai H, Gong Y et al. ANLN-induced EZH2 upregulation promotes pancreatic cancer progression by mediating miR-218-5p/LASP1 signaling axis. J Exp Clin Cancer Res. 2019;38:347.CrossRef
39.
Zurück zum Zitat Howard CM, Bearss N, Subramaniyan B et al. The CXCR4-LASP1-eIF4F axis promotes translation of oncogenic proteins in triple-negative breast cancer cells. Front Oncol. 2019;9:284.CrossRef Howard CM, Bearss N, Subramaniyan B et al. The CXCR4-LASP1-eIF4F axis promotes translation of oncogenic proteins in triple-negative breast cancer cells. Front Oncol. 2019;9:284.CrossRef
40.
Zurück zum Zitat Sui Y, Zhang X, Yang H, Wei W, Wang M. MicroRNA-133a acts as a tumour suppressor in breast cancer through targeting LASP1. Oncol Rep. 2018;39:473–482.PubMed Sui Y, Zhang X, Yang H, Wei W, Wang M. MicroRNA-133a acts as a tumour suppressor in breast cancer through targeting LASP1. Oncol Rep. 2018;39:473–482.PubMed
Metadaten
Titel
Circular RNA circ_0006948 Promotes Esophageal Squamous Cell Carcinoma Progression by Regulating microRNA-3612/LASP1 Axis
Publikationsdatum
22.05.2021
Erschienen in
Digestive Diseases and Sciences / Ausgabe 6/2022
Print ISSN: 0163-2116
Elektronische ISSN: 1573-2568
DOI
https://doi.org/10.1007/s10620-021-07057-4

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