Abstract
Objectives
Recent studies have revealed that circular RNA (circRNA) plays a pivotal role in cancer development. The study aimed to investigate the role of circ_0081146 in gastric cancer (GC).
Results
Circ_0081146 was upregulated in GC tissues and cells. Patients with high expression of circ_0081146 had a significantly reduced 5-year overall survival rate. Circ_0081146 knockdown restrained the growth, migration and invasion of GC cells in vitro as well as tumorigenesis in vivo. Circ_0081146 targeted miR-144 and HMGB1 was targeted by miR-144. Circ_0081146 was negatively correlated with miR-144 expression, while positively correlated with HMGB1 expression in GC tissues. Moreover, the inhibitory effect of circ_0081146 knockdown on the progression of GC cells were reversed by silencing miR-144 or HMGB1 overexpression. Mechanically, circ_0081146 increased HMGB1 expression by targeting miR-144.
Conclusion
Circ_0081146 functions as an oncogene in GC to promote cell growth, migration and invasion via modulating the miR-144/HMGB1 axis.
Similar content being viewed by others
References
Ambros V (2001) microRNAs: tiny regulators with great potential. Cell 107:823–826. https://doi.org/10.1016/s0092-8674(01)00616-x
Chan JJ, Tay Y (2018) Noncoding RNA:RNA regulatory networks in cancer. Int J Mol Sci 19:1310. https://doi.org/10.3390/ijms19051310
Chen Y, Li C, Tan C, Liu X (2016) Circular RNAs: a new frontier in the study of human diseases. J Med Genet 53:359–365. https://doi.org/10.1136/jmedgenet-2016-103758
Chen J et al (2017) Circular RNA profile identifies circPVT1 as a proliferative factor and prognostic marker in gastric cancer. Cancer Lett 388:208–219. https://doi.org/10.1016/j.canlet.2016.12.006
Dang Y et al (2017) Circular RNAs expression profiles in human gastric cancer. Sci Rep 7:9060. https://doi.org/10.1038/s41598-017-09076-6
D’Angelo B et al (2016) MicroRNAs: a puzzling tool in cancer diagnostics and therapy. Anticancer Res 3611:5571–5575. https://doi.org/10.21873/anticanres.11142
Ge S et al (2019) MiR-181a, a new regulator of TGF-β signaling, can promote cell migration and proliferation in gastric cancer. Invest New Drugs 375:923–934. https://doi.org/10.1007/s10637-018-0695-5
Gong J et al (2019) Integrated analysis of circular RNA-associated ceRNA network in cervical cancer: observational study. Medicine (Baltimore) 98:e16922. https://doi.org/10.1097/md.0000000000016922
He H, Wang X, Chen J, Sun L, Sun H, Xie K (2019) High-Mobility Group Box 1 (HMGB1) promotes angiogenesis and tumor migration by regulating hypoxia-inducible factor 1 (HIF-1alpha) expression via the phosphatidylinositol 3-Kinase (PI3K)/AKT signaling pathway in breast cancer cells. Med Sci Monit 25:2352–2360. https://doi.org/10.12659/msm.915690
Huang S et al (2019a) A novel circular RNA hsa_circ_0008035 contributes to gastric cancer tumorigenesis through targeting the miR-375/YBX1 axis. Am J Transl Res 11:2455–2462
Huang X et al (2019b) Circular RNA AKT3 upregulates PIK3R1 to enhance cisplatin resistance in gastric cancer via miR-198 suppression. Mol Cancer 18:71. https://doi.org/10.1186/s12943-019-0969-3
Jin W et al (2019) Downregulation miR-539 is associated with poor prognosis of gastric cancer patients and aggressive progression of gastric cancer cells. Cancer Biomark 262:183–191. https://doi.org/10.3233/CBM-190384
Karimi P, Islami F, Anandasabapathy S, Freedman ND, Kamangar F (2014) Gastric cancer: descriptive epidemiology, risk factors, screening, and prevention. Cancer Epidemiol Biomarkers Prev 23:700–713. https://doi.org/10.1158/1055-9965.epi-13-1057
Ke XS, Liu CM, Liu DP, Liang CC (2003) MicroRNAs: key participants in gene regulatory networks. Curr Opin Chem Biol 7:516–523. https://doi.org/10.1016/s1367-5931(03)00075-9
Ledford H (2013) Circular RNAs throw genetics for a loop. Nature 494:415. https://doi.org/10.1038/494415a
Li Y et al (2015) Circular RNA is enriched and stable in exosomes: a promising biomarker for cancer diagnosis. Cell Res 25:981–984. https://doi.org/10.1038/cr.2015.82
Li Y et al (2017) CircHIPK3 sponges miR-558 to suppress heparanase expression in bladder cancer cells. EMBO Rep 18:1646–1659. https://doi.org/10.15252/embr.201643581
Li P, Xu M, Cai H, Thapa N, He C, Song Z (2019) The effect of HMGB1 on the clinicopathological and prognostic features of cervical cancer. Biosci Rep. https://doi.org/10.1042/bsr20181016
Liu J et al (2015) MicroRNA-144 inhibits the metastasis of gastric cancer by targeting MET expression. J Exp Clin Cancer Res 34:35. https://doi.org/10.1186/s13046-015-0154-5
Liu S et al (2017) Prognostic significance of low miR-144 expression in gastric cancer. Cancer Biomark 204:547–552. https://doi.org/10.3233/CBM-170351
Liu H et al (2018) Circular RNA YAP1 inhibits the proliferation and invasion of gastric cancer cells by regulating the miR-367-5p/p27 (Kip1) axis. Mol Cancer 17:151. https://doi.org/10.1186/s12943-018-0902-1
Liu JL et al (2019) MiR-144 inhibits tumor growth and metastasis in osteosarcoma via dual-suppressing RhoA/ROCK1 signaling pathway. Mol Pharmacol 95:451–461. https://doi.org/10.1124/mol.118.114207
Lv DJ et al (2019) HMGB1 promotes prostate cancer development and metastasis by interacting with brahma-related gene 1 and activating the Akt signaling pathway. Theranostics 9:5166–5182. https://doi.org/10.7150/thno.33972
Miao Z et al (2019) The long noncoding RNA NORAD promotes the growth of gastric cancer cells by sponging miR-608. Gene 687:116–124. https://doi.org/10.1016/j.gene.2018.11.052
Ren K, Liu QQ, An ZF, Zhang DP, Chen XH (2017) MiR-144 functions as tumor suppressor by targeting PIM1 in gastric cancer. Eur Rev Med Pharmacol Sci 21:3028–3037
Shi L et al (2019) Long non-coding RNA ZNFX1-AS1 promotes the tumor progression and metastasis of colorectal cancer by acting as a competing endogenous RNA of miR-144 to regulate EZH2 expression. Cell Death Dis 10:150. https://doi.org/10.1038/s41419-019-1332-8
Suren D, Arda Gokay A, Sayiner A (2018) High Mobility Group Box 1 (HMGB1) expression in gastric adenocarcinomas. J Buon 23:422–427
Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A (2015) Global cancer statistics, 2012. CA Cancer J Clin 65:87–108. https://doi.org/10.3322/caac.21262
Tripathi A, Shrinet K, Kumar A (2019) HMGB1 protein as a novel target for cancer. Toxicol Rep 6:253–261. https://doi.org/10.1016/j.toxrep.2019.03.002
Vicens Q, Westhof E (2014) Biogenesis of circular RNAs. Cell 159:13–14. https://doi.org/10.1016/j.cell.2014.09.005
Wu J et al (2018) CircIRAK3 sponges miR-3607 to facilitate breast cancer metastasis. Cancer Lett 430:179–192. https://doi.org/10.1016/j.canlet.2018.05.033
Yang H, Wang H, Czura CJ, Tracey KJ (2005) The cytokine activity of HMGB1. J Leukoc Biol 78:1–8. https://doi.org/10.1189/jlb.1104648
Yang J et al (2019) Circular RNA hsa_circRNA_0007334 is predicted to promote MMP7 and COL1A1 expression by functioning as a miRNA sponge in pancreatic ductal adenocarcinoma. J Oncol 2019:7630894. https://doi.org/10.1155/2019/7630894
Yao Q, Gu A, Wang Z, Xue Y (2018) MicroRNA-144 functions as a tumor suppressor in gastric cancer by targeting cyclooxygenase-2. Exp Ther Med 15:3088–3095. https://doi.org/10.3892/etm.2018.5763
Zhang LY et al (2013) MicroRNA-144 promotes cell proliferation, migration and invasion in nasopharyngeal carcinoma through repression of PTEN. Carcinogenesis 34:454–463. https://doi.org/10.1093/carcin/bgs346
Zhang J, Kou YB, Zhu JS, Chen WX, Li S (2014) Knockdown of HMGB1 inhibits growth and invasion of gastric cancer cells through the NF-kappaB pathway in vitro and in vivo. Int J Oncol 44:1268–1276. https://doi.org/10.3892/ijo.2014.2285
Zhang QY, Wu LQ, Zhang T, Han YF, Lin X (2015) Autophagy-mediated HMGB1 release promotes gastric cancer cell survival via RAGE activation of extracellular signal-regulated kinases 1/2. Oncol Rep 33:1630–1638. https://doi.org/10.3892/or.2015.3782
Zhang J et al (2017) Circular RNA_LARP4 inhibits cell proliferation and invasion of gastric cancer by sponging miR-424-5p and regulating LATS1 expression. Mol Cancer 16:151. https://doi.org/10.1186/s12943-017-0719-3
Zhang J et al (2018) High mobility group box 1 promotes the epithelial-to-mesenchymal transition in prostate cancer PC3 cells via the RAGE/NF-kappaB signaling pathway. Int J Oncol 53:659–671. https://doi.org/10.3892/ijo.2018.4420
Zhang L, Song X, Chen X, Wang Q, Zheng X, Wu C, Jiang J (2019) Circular RNA CircCACTIN promotes gastric cancer progression by sponging MiR-331-3p and regulating TGFBR1 expression. Int J Biol Sci 15:1091–1103. https://doi.org/10.7150/ijbs.31533
Funding
This study was supported by Shanghai Pudong Commission of Health and Family Planning (No. PWRd2016-12); and Talents Training Program of Seventh People’s Hospital of Shanghai University of TCM (No. XX2019-07).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors have no conflict of interest to declare.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Xu, Q., Liao, B., Hu, S. et al. Circular RNA 0081146 facilitates the progression of gastric cancer by sponging miR-144 and up-regulating HMGB1. Biotechnol Lett 43, 767–779 (2021). https://doi.org/10.1007/s10529-020-03058-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10529-020-03058-x