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Review

Circular RNAs as Novel Biomarkers with Regulatory Potency in Human Diseases

Article: FSO314 | Received 02 Apr 2018, Accepted 08 May 2018, Published online: 23 May 2018

References

  • Sanger HL, Klotz G, Riesner D, Gross HJ, Kleinschmidt AK. Viroids are single-stranded covalently closed circular RNA molecules existing as highly base-paired rod-like structures. Proc. Natl Acad. Sci. USA 73(11), 3852–3856 (1976).
  • Nigro JM, Cho KR, Fearon ER et al. Scrambled exons. Cell 64(3), 607–613 (1991).
  • Wang PL, Bao Y, Yee MC et al. Circular RNA is expressed across the eukaryotic tree of life. PLoS ONE 9(6), e90859 (2014).
  • Jeck WR, Sorrentino JA, Wang K et al. Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA 19(2), 141–157 (2013).
  • Li Z, Huang C, Bao C et al. exon–intron circular RNAs regulate transcription in the nucleus. Nat. Struct. Mol. Biol. 22(3), 256–264 (2015).
  • Zhang Y, Zhang XO, Chen T et al. Circular intronic long noncoding RNAs. Mol. Cell 51(6), 792–806 (2013).
  • Starke S, Jost I, Rossbach O et al. Exon circularization requires canonical splice signals. Cell Rep. 10(1), 103–111 (2015).
  • Xu T, Wu J, Han P, Zhao Z, Song X. Circular RNA expression profiles and features in human tissues: a study using RNA-seq data. BMC Genomics 18(Suppl. 6), 680 (2017).
  • Rybak-Wolf A, Stottmeister C, Glazar P et al. Circular RNAs in the mammalian brain are highly abundant, conserved, and dynamically expressed. Mol. Cell 58(5), 870–885 (2015).
  • Memczak S, Jens M, Elefsinioti A et al. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 495(7441), 333–338 (2013).
  • Hansen TB, Jensen TI, Clausen BH et al. Natural RNA circles function as efficient microRNA sponges. Nature 495(7441), 384–388 (2013).
  • Fan X, Weng X, Zhao Y, Chen W, Gan T, Xu D. Circular RNAs in cardiovascular disease: an overview. Biomed. Res. Int. 2017, 5135781 (2017).
  • Zhao Z, Li X, Jian D, Hao P, Rao L, Li M. Hsa_circ_0054633 in peripheral blood can be used as a diagnostic biomarker of pre-diabetes and type 2 diabetes mellitus. Acta Diabetol. 54(3), 237–245 (2017).
  • Li LJ, Huang Q, Pan HF, Ye DQ. Circular RNAs and systemic lupus erythematosus. Exp. Cell Res. 346(2), 248–254 (2016).
  • Idda ML, Munk R, Abdelmohsen K, Gorospe M. Noncoding RNAs in Alzheimer's disease. Wiley Interdiscip. Rev. RNA 9(2), doi:10.1002/wrna.1463 (2018) ( Epub ahead of print).
  • Han YN, Xia SQ, Zhang YY, Zheng JH, Li W. Circular RNAs: a novel type of biomarker and genetic tools in cancer. Oncotarget 8(38), 64551–64563 (2017).
  • Salzman J, Chen RE, Olsen MN, Wang PL, Brown PO. Cell-type specific features of circular RNA expression. PLoS Genet. 9(9), e1003777 (2013).
  • Memczak S, Papavasileiou P, Peters O, Rajewsky N. Identification and characterization of circular RNAs As a new class of putative biomarkers in human blood. PLoS ONE 10(10), e0141214 (2015).
  • Pan RY, Liu P, Zhou HT et al. Circular RNAs promote TRPM3 expression by inhibiting hsa-miR-130a-3p in coronary artery disease patients. Oncotarget 8(36), 60280–60290 (2017).
  • Bahn JH, Zhang Q, Li F et al. The landscape of microRNA, Piwi-interacting RNA, and circular RNA in human saliva. Clin. Chem. 61(1), 221–230 (2015).
  • Westholm JO, Miura P, Olson S et al. Genome-wide analysis of drosophila circular RNAs reveals their structural and sequence properties and age-dependent neural accumulation. Cell Rep. 9(5), 1966–1980 (2014).
  • Zhao T, Wang L, Li S, Xu M, Guan X, Zhou B. Characterization of conserved circular RNA in polyploid Gossypium species and their ancestors. FEBS Lett. 591(21), 3660–3669 (2017).
  • Dong R, Ma XK. Increased complexity of circRNA expression during species evolution. 14(8), 1064–1074 (2017).
  • Werfel S, Nothjunge S, Schwarzmayr T, Strom TM, Meitinger T, Engelhardt S. Characterization of circular RNAs in human, mouse and rat hearts. J. Mol. Cell. Cardiol. 98, 103–107 (2016).
  • Stoll L, Sobel J, Rodriguez-Trejo A et al. Circular RNAs as novel regulators of beta-cell functions in normal and disease conditions. Mol. Metab. 9, 69–83 (2018).
  • Wan L, Zhang L, Fan K, Cheng ZX, Sun QC, Wang JJ. Circular RNA-ITCH suppresses lung cancer proliferation via inhibiting the Wnt/beta-catenin pathway. BioMed Res. Int. 2016, 1579490 (2016).
  • Abdelmohsen K, Panda AC, Munk R et al. Identification of HuR target circular RNAs uncovers suppression of PABPN1 translation by CircPABPN1. RNA Biol. 14(3), 361–369 (2017).
  • Yang Y, Gao X, Zhang M et al. Novel role of FBXW7 circular RNA in repressing glioma tumorigenesis. J. Natl Cancer Inst. 110(3), doi:10.1093/jnci/djx166 (2018) ( Epub ahead of print).
  • Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 136(2), 215–233 (2009).
  • Guo JU, Agarwal V, Guo H, Bartel DP. Expanded identification and characterization of mammalian circular RNAs. Genome Biol. 15(7), 409 (2014).
  • Zheng Q, Bao C, Guo W et al. Circular RNA profiling reveals an abundant circHIPK3 that regulates cell growth by sponging multiple miRNAs. Nat. Commun. 7, 11215 (2016).
  • Chen G, Shi Y, Liu M, Sun J. circHIPK3 regulates cell proliferation and migration by sponging miR-124 and regulating AQP3 expression in hepatocellular carcinoma. Cell Death Dis. 9(2), 175 (2018).
  • Shan K, Liu C, Liu BH et al. Circular noncoding RNA HIPK3 mediates retinal vascular dysfunction in diabetes mellitus. Circulation 136(17), 1629–1642 (2017).
  • Huang C, Shan G. What happens at or after transcription: insights into circRNA biogenesis and function. Transcription 6(4), 61–64 (2015).
  • Li F, Zhang L, Li W et al. Circular RNA ITCH has inhibitory effect on ESCC by suppressing the Wnt/beta-catenin pathway. Oncotarget 6(8), 6001–6013 (2015).
  • Huang G, Zhu H, Shi Y, Wu W, Cai H, Chen X. cir-ITCH plays an inhibitory role in colorectal cancer by regulating the Wnt/beta-catenin pathway. PLoS ONE 10(6), e0131225 (2015).
  • Du WW, Yang W, Liu E, Yang Z, Dhaliwal P, Yang BB. Foxo3 circular RNA retards cell cycle progression via forming ternary complexes with p21 and CDK2. Nucleic Acids Res. 44(6), 2846–2858 (2016).
  • Holdt LM, Stahringer A, Sass K et al. Circular non-coding RNA ANRIL modulates ribosomal RNA maturation and atherosclerosis in humans. Nat. Commun. 7, 12429 (2016).
  • Glisovic T, Bachorik JL, Yong J, Dreyfuss G. RNA-binding proteins and post-transcriptional gene regulation. FEBS Lett. 582(14), 1977–1986 (2008).
  • Chen CY, Sarnow P. Initiation of protein synthesis by the eukaryotic translational apparatus on circular RNAs. Science 268(5209), 415–417 (1995).
  • Legnini I, Di Timoteo G, Rossi F et al. Circ-ZNF609 is a circular RNA that can be translated and functions in myogenesis. Mol. Cell 66(1), 22.e29–37.e29 (2017).
  • Zhang M, Huang N, Yang X et al. A novel protein encoded by the circular form of the SHPRH gene suppresses glioma tumorigenesis. Oncogene 37, 1805–1814 (2018).
  • Li CY, Ma L, Yu B. Circular RNA hsa_circ_0003575 regulates oxLDL induced vascular endothelial cells proliferation and angiogenesis. Biomed. Pharmacother. 95, 1514–1519 (2017).
  • Li X, Zhao Z, Jian D, Li W, Tang H, Li M. Hsa-circRNA11783–2 in peripheral blood is correlated with coronary artery disease and Type 2 diabetes mellitus. Diab. Vasc. Dis. Res. 14(6), 510–515 (2017).
  • Wang K, Gan TY, Li N et al. Circular RNA mediates cardiomyocyte death via miRNA-dependent upregulation of MTP18 expression. Cell Death Differ. 24(6), 1111–1120 (2017).
  • Salgado-Somoza A, Zhang L, Vausort M, Devaux Y. The circular RNA MICRA for risk stratification after myocardial infarction. Int. J. Cardiol. Heart Vasc. 17, 33–36 (2017).
  • Wu N, Jin L, Cai J. Profiling and bioinformatics analyses reveal differential circular RNA expression in hypertensive patients. Clin. Exp. Hypertens. 39(5), 454–459 (2017).
  • Tang CM, Zhang M, Huang L et al. CircRNA_000203 enhances the expression of fibrosis-associated genes by derepressing targets of miR-26b-5p, Col1a2 and CTGF, in cardiac fibroblasts. Sci. Rep. 7, 40342 (2017).
  • Zhou B, Yu JW. A novel identified circular RNA, circRNA_010567, promotes myocardial fibrosis via suppressing miR-141 by targeting TGF-beta1. Biochem. Biophys. Res. Commun. 487(4), 769–775 (2017).
  • Wang K, Long B, Liu F et al. A circular RNA protects the heart from pathological hypertrophy and heart failure by targeting miR-223. Eur. Heart J. 37(33), 2602–2611 (2016).
  • Zhang SJ, Chen X, Li CP et al. Identification and characterization of circular RNAs as a new class of putative biomarkers in diabetes retinopathy. Invest. Ophthalmol. Vis. Sci. 58(14), 6500–6509 (2017).
  • Ouyang Q, Wu J, Jiang Z et al. Microarray expression profile of circular RNAs in peripheral blood mononuclear cells from rheumatoid arthritis patients. Cell. Physiol. Biochem. 42(2), 651–659 (2017).
  • Luan J, Jiao C, Kong W et al. circHLA-C plays an important role in lupus nephritis by sponging miR-150. Mol. Ther. Nucleic Acids 10, 245–253 (2018).
  • Hu DY, Pan CY, Yu JM. The relationship between coronary artery disease and abnormal glucose regulation in China: the China Heart Survey. Eur. Heart J. 27(21), 2573–2579 (2006).
  • Tondera D, Czauderna F, Paulick K, Schwarzer R, Kaufmann J, Santel A. The mitochondrial protein MTP18 contributes to mitochondrial fission in mammalian cells. J. Cell Sci. 118(Pt 14), 3049–3059 (2005).
  • Cheng X, Joe B. Circular RNAs in rat models of cardiovascular and renal diseases. Physiol. Genomics 49(9), 484–490 (2017).
  • Czubryt MP. Common threads in cardiac fibrosis, infarct scar formation, and wound healing. Fibrogenesis & Tissue Repair 5(1), 19 (2012).
  • Murtaza I, Wang HX, Feng X et al. Down-regulation of catalase and oxidative modification of protein kinase CK2 lead to the failure of apoptosis repressor with caspase recruitment domain to inhibit cardiomyocyte hypertrophy. J. Biol. Chem. 283(10), 5996–6004 (2008).
  • Chen J, Cui L, Yuan J, Zhang Y, Sang H. Circular RNA WDR77 target FGF-2 to regulate vascular smooth muscle cells proliferation and migration by sponging miR-124. Biochem. Biophys. Res. Commun. 494(1–2), 126–132 (2017).
  • Gu Y, Ke G, Wang L, Zhou E, Zhu K, Wei Y. Altered expression profile of circular RNAs in the serum of patients with diabetic retinopathy revealed by microarray. Ophthalmic Res. 58(3), 176–184 (2017).
  • Korn C, Augustin HG. Mechanisms of vessel pruning and regression. Dev. Cell 34(1), 5–17 (2015).
  • Campochiaro PA. Ocular neovascularization. J. Mol. Med. (Berl.) 91(3), 311–321 (2013).
  • Xu H, Guo S, Li W, Yu P. The circular RNA Cdr1as, via miR-7 and its targets, regulates insulin transcription and secretion in islet cells. Sci. Rep. 5, 12453 (2015).
  • Stoll L, Sobel J, Rodriguez-Trejo A et al. Circular RNAs as novel regulators of beta-cell functions in normal and disease conditions. Mol. Metabol. 9, 69–83 (2018).
  • Zheng F, Yu X, Huang J, Dai Y. Circular RNA expression profiles of peripheral blood mononuclear cells in rheumatoid arthritis patients, based on microarray chip technology. Mol. Med. Rep. 16(6), 8029–8036 (2017).
  • Li H, Li K, Lai W et al. Comprehensive circular RNA profiles in plasma reveals that circular RNAs can be used as novel biomarkers for systemic lupus erythematosus. Clin. Chim. Acta 480, 17–25 (2018).
  • Zhou H, Hasni SA, Perez P et al. miR-150 promotes renal fibrosis in lupus nephritis by downregulating SOCS1. J. Am. Soc. Nephrol. 24(7), 1073–1087 (2013).
  • Luo YH, Zhu XZ, Huang KW et al. Emerging roles of circular RNA hsa_circ_0000064 in the proliferation and metastasis of lung cancer. Biomed. Pharmacother. 96, 892–898 (2017).
  • Yao JT, Zhao SH, Liu QP et al. Over-expression of CircRNA 10.876 in non-small cell lung cancer and its prognostic value. Pathol. Res. Pract. 213(5), 453–456 (2017).
  • Zhang S, Zeng X, Ding T et al. Microarray profile of circular RNAs identifies hsa_circ_0014130 as a new circular RNA biomarker in non-small cell lung cancer. Sci. Rep. 8(1), 2878 (2018).
  • Zhu X, Wang X, Wei S et al. hsa_circ_0013958: a circular RNA and potential novel biomarker for lung adenocarcinoma. FEBS J. 284(14), 2170–2182 (2017).
  • Wang X, Zhu X, Zhang H et al. Increased circular RNA hsa_circ_0012673 acts as a sponge of miR-22 to promote lung adenocarcinoma proliferation. Biochem. Biophys. Res. Commun. 496(4), 1069–1075 (2018).
  • Wang H, Xiao Y, Wu L, Ma D. Comprehensive circular RNA profiling reveals the regulatory role of the circRNA-000911/miR-449a pathway in breast carcinogenesis. Int. J. Oncol. 52(3), 743–754 (2018).
  • Liang HF, Zhang XZ, Liu BG, Jia GT, Li WL. Circular RNA circ-ABCB10 promotes breast cancer proliferation and progression through sponging miR-1271. Am. J. Cancer Res. 7(7), 1566–1576 (2017).
  • Tang YY, Zhao P, Zou TN et al. Circular RNA hsa_circ_0001982 promotes breast cancer cell carcinogenesis through decreasing miR-143. DNA Cell Biol. 36(11), 901–908 (2017).
  • He R, Liu P, Xie X et al. circGFRA1 and GFRA1 act as ceRNAs in triple negative breast cancer by regulating miR-34a. J. Exp. Clin. Cancer Res. 36(1), 145 (2017).
  • Xie Y, Shao Y, Sun W et al. Downregulated expression of hsa_circ_0074362 in gastric cancer and its potential diagnostic values. Biomarkers Med. 12(1), 11–20 (2018).
  • Li P, Chen S, Chen H et al. Using circular RNA as a novel type of biomarker in the screening of gastric cancer. Clin. Chim. Acta 444, 132–136 (2015).
  • Shao Y, Li J, Lu R et al. Global circular RNA expression profile of human gastric cancer and its clinical significance. Cancer Med. 6(6), 1173–1180 (2017).
  • Chen S, Li T, Zhao Q, Xiao B, Guo J. Using circular RNA hsa_circ_0000190 as a new biomarker in the diagnosis of gastric cancer. Clin. Chim. Acta 466, 167–171 (2017).
  • Sun H, Tang W, Rong D et al. Hsa_circ_0000520, a potential new circular RNA biomarker, is involved in gastric carcinoma. Cancer Biomark. 21(2), 299–306 (2018).
  • Li T, Shao Y, Fu L et al. Plasma circular RNA profiling of patients with gastric cancer and their droplet digital RT-PCR detection. J. Mol. Med. (Berl.) 96(1), 85–96 (2018).
  • Zhang Y, Liu H, Li W et al. CircRNA 10.269 is downregulated in gastric cancer and suppresses tumor cell growth by targeting miR-630. Aging 9(6), 1585–1594 (2017).
  • Zhang J, Wang G, Chu SJ et al. Loss of large tumor suppressor 1 promotes growth and metastasis of gastric cancer cells through upregulation of the YAP signaling. Oncotarget 7(13), 16180–16193 (2016).
  • Qin M, Liu G, Huo X et al. Hsa_circ_0001649: a circular RNA and potential novel biomarker for hepatocellular carcinoma. Cancer Biomark. 16(1), 161–169 (2016).
  • Shang X, Li G, Liu H et al. Comprehensive circular RNA profiling reveals that hsa_circ_0005075, a new circular RNA biomarker, is involved in hepatocellular crcinoma development. Medicine 95(22), e3811 (2016).
  • Yao Z, Luo J, Hu K et al. ZKSCAN1 gene and its related circular RNA (circZKSCAN1) both inhibit hepatocellular carcinoma cell growth, migration, and invasion but through different signaling pathways. Mol. Oncol. 11(4), 422–437 (2017).
  • Han D, Li J, Wang H et al. Circular RNA circMTO1 acts as the sponge of microRNA-9 to suppress hepatocellular carcinoma progression. Hepatology 66(4), 1151–1164 (2017).
  • Yu J, Xu QG, Wang ZG et al. Circular RNA cSMARCA5 inhibits growth and metastasis in hepatocellular carcinoma. J. Hepatol. doi:10.1016/j.jhep.2018.01.012 (2018) ( Epub ahead of print).
  • Zhu Q, Lu G, Luo Z et al. CircRNA circ_0067934 promotes tumor growth and metastasis in hepatocellular carcinoma through regulation of miR-1324/FZD5/Wnt/beta-catenin axis. Biochem. Biophys. Res. Commun. 497(2), 626–632 (2018).
  • Huang XY, Huang ZL, Xu YH et al. Comprehensive circular RNA profiling reveals the regulatory role of the circRNA-100338/miR-141–3p pathway in hepatitis B-related hepatocellular carcinoma. Sci. Rep. 7(1), 5428 (2017).
  • Zhuo F, Lin H, Chen Z, Huang Z, Hu J. The expression profile and clinical significance of circRNA0003906 in colorectal cancer. Onco Targets Ther. 10, 5187–5193 (2017).
  • Wang X, Zhang Y, Huang L et al. Decreased expression of hsa_circ_001988 in colorectal cancer and its clinical significances. Int. J. Clin. Exp. Pathol. 8(12), 16020–16025 (2015).
  • Zhang P, Zuo Z, Shang W et al. Identification of differentially expressed circular RNAs in human colorectal cancer. Tumour Biol. 39(3), 1010428317694546 (2017).
  • Guo JN, Li J, Zhu CL et al. Comprehensive profile of differentially expressed circular RNAs reveals that hsa_circ_0000069 is upregulated and promotes cell proliferation, migration, and invasion in colorectal cancer. OncoTargets Ther. 9, 7451–7458 (2016).
  • Zhang R, Xu J, Zhao J, Wang X. Silencing of hsa_circ_0007534 suppresses proliferation and induces apoptosis in colorectal cancer cells. Eur. Rev. Med. Pharm. Sci. 22(1), 118–126 (2018).
  • Zhang XL, Xu LL, Wang F. Hsa_circ_0020397 regulates colorectal cancer cell viability, apoptosis and invasion by promoting the expression of the miR-138 targets TERT and PD-L1. Cell Biol. Int. 41(9), 1056–1064 (2017).
  • 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. 6, 30919 (2016).
  • Zhong Z, Huang M, Lv M et al. Circular RNA MYLK as a competing endogenous RNA promotes bladder cancer progression through modulating VEGFA/VEGFR2 signaling pathway. Cancer Lett. 403, 305–317 (2017).
  • Li B, Xie F, Zheng FX, Jiang GS, Zeng FQ, Xiao XY. Overexpression of CircRNA BCRC4 regulates cell apoptosis and MicroRNA-101/EZH2 signaling in bladder cancer. J. Huazhong Univ. Sci. Technolog. Med. Sci. 37(6), 886–890 (2017).
  • Yang C, Yuan W, Yang X et al. Circular RNA circ-ITCH inhibits bladder cancer progression by sponging miR-17/miR-224 and regulating p21, PTEN expression. Mol. Cancer 17(1), 19 (2018).
  • Li G, Yang H, Han K, Zhu D, Lun P, Zhao Y. A novel circular RNA, hsa_circ_0046701, promotes carcinogenesis by increasing the expression of miR-142–3p target ITGB8 in glioma. Biochem. Biophys. Res. Commun. 498(1), 254–261 (2018).
  • Aggarwal A, Lewison G, Idir S et al. The state of lung cancer research: a global analysis. J. Thorac. Oncol. 11(7), 1040–1050 (2016).
  • Subramanian J, Govindan R. Lung cancer in never smokers: a review. J. Clin. Oncol. 25(5), 561–570 (2007).
  • Zhao J, Li L, Wang Q, Han H, Zhan Q, Xu M. CircRNA expression profile in early-stage lung adenocarcinoma patients. Cell. Physiol. Biochem. 44(6), 2138–2146 (2017).
  • Chen W, Zheng R, Baade PD et al. Cancer statistics in China, 2015. CA Cancer J. Clin. 66(2), 115–132 (2016).
  • Yan N, Xu H, Zhang J et al. Circular RNA profile indicates circular RNA VRK1 is negatively related with breast cancer stem cells. Oncotarget 8(56), 95704–95718 (2017).
  • Liu R, Shi P, Nie Z et al. Mifepristone suppresses basal triple-negative breast cancer stem cells by down-regulating KLF5 expression. Theranostics 6(4), 533–544 (2016).
  • Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Cancer J. Clin. 65(2), 87–108 (2015).
  • Sui W, Shi Z, Xue W et al. Circular RNA and gene expression profiles in gastric cancer based on microarray chip technology. Oncol. Rep. 37(3), 1804–1814 (2017).
  • Dang Y, Ouyang X, Zhang F et al. Circular RNAs expression profiles in human gastric cancer. Sci. Rep. 7(1), 9060 (2017).
  • Zhang Y, Li J, Yu J et al. Circular RNAs signature predicts the early recurrence of stage III gastric cancer after radical surgery. Oncotarget 8(14), 22936–22943 (2017).
  • Zhang J, Liu H, Hou L et al. Circular RNA_LARP4 inhibits cell proliferation and invasion of gastric cancer by sponging miR-424–5p and regulating LATS1 expression. Mol. Cancer 16(1), 151 (2017).
  • Zhu RX, Seto WK, Lai CL, Yuen MF. Epidemiology of hepatocellular carcinoma in the Asia-Pacific region. Gut Liver 10(3), 332–339 (2016).
  • Pineau P, Tiollais P. [Hepatitis B vaccination: a major player in the control of primary liver cancer]. Pathol. Biol. (Paris) 58(6), 444–453 (2010).
  • Cui S, Qian Z, Chen Y, Li L, Li P, Ding H. Screening of up- and downregulation of circRNAs in HBV-related hepatocellular carcinoma by microarray. Oncol. Lett. 15(1), 423–432 (2018).
  • Chaffer CL, Weinberg RA. A perspective on cancer cell metastasis. Science 331(6024), 1559–1564 (2011).
  • Jiang W, Zhang X, Chu Q et al. The circular RNA profiles of colorectal tumor metastatic cells. Front. Genet. 9, 34 (2018).
  • Zeng Y, Xu Y, Shu R et al. Altered expression profiles of circular RNA in colorectal cancer tissues from patients with lung metastasis. Int. J. Mol. Med. 40(6), 1818–1828 (2017).
  • Song X, Zhang N, Han P et al. Circular RNA profile in gliomas revealed by identification tool UROBORUS. Nucleic Acids Res. 44(9), e87 (2016).