4.6

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2.2

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  • ISSN 1674-8301
  • CN 32-1810/R
Lan Ma, Haiyan Chu, Meilin Wang, Zhengdong Zhang. Biological functions and potential implications of circular RNAs[J]. The Journal of Biomedical Research, 2023, 37(2): 89-99. DOI: 10.7555/JBR.36.20220095
Citation: Lan Ma, Haiyan Chu, Meilin Wang, Zhengdong Zhang. Biological functions and potential implications of circular RNAs[J]. The Journal of Biomedical Research, 2023, 37(2): 89-99. DOI: 10.7555/JBR.36.20220095

Biological functions and potential implications of circular RNAs

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  • Corresponding author:

    Zhengdong Zhang, School of Public Health, Nanjing Medical University, 101 Longmian Avenue, Jiangning District, Nanjing, Jiangsu 211166, China. Tel: +86-25-86868423, E-mail: drzdzhang@njmu.edu.cn

  • Received Date: April 26, 2022
  • Revised Date: August 17, 2022
  • Accepted Date: August 29, 2022
  • Available Online: October 27, 2022
  • Circular RNAs (circRNAs) are characterized by a covalent closed-loop structure with an absence of both 5′ cap structure and 3′ polyadenylated tail. Numerous studies have found that circRNAs play an important role in various diseases and have a variety of biological regulatory mechanisms, including acting as microRNA sponges, interacting with proteins, modulating the expression of related genes and translating into peptides or proteins. CircRNAs have also been used as biomarkers for a number of diseases, which could improve clinical practice. This review summarizes the most recent advances in biogenesis and knowledge of the biological functions of circRNAs as well as the related bioinformatics databases. We specifically describe developments in understanding of circRNA functions in the field of environmental exposure-induced diseases. Finally, we focus on potential clinical implications of circRNAs to facilitate their clinical transformation into disease treatment.
  • CLC number: Q522, Document code: A

    The authors reported no conflict of interests.

  • [1]
    Sanger HL, Klotz G, Riesner D, et al. Viroids are single-stranded covalently closed circular RNA molecules existing as highly base-paired rod-like structures[J]. Proc Natl Acad Sci U S A, 1976, 73(11): 3852–3856. doi: 10.1073/pnas.73.11.3852
    [2]
    Capel B, Swain A, Nicolis S, et al. Circular transcripts of the testis-determining gene Sry in adult mouse testis[J]. Cell, 1993, 73(5): 1019–1030. doi: 10.1016/0092-8674(93)90279-Y
    [3]
    Szabo L, Salzman J. Detecting circular RNAs: bioinformatic and experimental challenges[J]. Nat Rev Genet, 2016, 17(11): 679–692. doi: 10.1038/nrg.2016.114
    [4]
    Huang J, Chen M, Xu K, et al. Microarray expression profile and functional analysis of circular RNAs in choroidal neovascularization[J]. J Biomed Res, 2019, 34(1): 67–74. doi: 10.7555/JBR.33.20190063
    [5]
    Fang Z, Jiang C, Li S. The potential regulatory roles of circular RNAs in tumor immunology and immunotherapy[J]. Front Immunol, 2021, 11: 617583. doi: 10.3389/fimmu.2020.617583
    [6]
    Kristensen LS, Jakobsen T, Hager H, et al. The emerging roles of circRNAs in cancer and oncology[J]. Nat Rev Clin Oncol, 2022, 19(3): 188–206. doi: 10.1038/s41571-021-00585-y
    [7]
    Mei X, Chen S. Circular RNAs in cardiovascular diseases[J]. Pharmacol Ther, 2022, 232: 107991. doi: 10.1016/j.pharmthera.2021.107991
    [8]
    Li F, Yang Q, He AT, et al. Circular RNAs in cancer: limitations in functional studies and diagnostic potential[J]. Semin Cancer Biol, 2021, 75: 49–61. doi: 10.1016/j.semcancer.2020.10.002
    [9]
    Hong W, Xue M, Jiang J, et al. Circular RNA circ-CPA4/ let-7 miRNA/PD-L1 axis regulates cell growth, stemness, drug resistance and immune evasion in non-small cell lung cancer (NSCLC)[J]. J Exp Clin Cancer Res, 2020, 39(1): 149. doi: 10.1186/s13046-020-01648-1
    [10]
    Xu J, Wan Z, Tang M, et al. N6-methyladenosine-modified CircRNA-SORE sustains sorafenib resistance in hepatocellular carcinoma by regulating β-catenin signaling[J]. Mol Cancer, 2020, 19(1): 163. doi: 10.1186/s12943-020-01281-8
    [11]
    Zhang Y, Zhang X, Chen T, et al. Circular intronic long noncoding RNAs[J]. Mol Cell, 2013, 51(6): 792–806. doi: 10.1016/j.molcel.2013.08.017
    [12]
    Zhang X, Wang H, Zhang Y, et al. Complementary sequence-mediated exon circularization[J]. Cell, 2014, 159(1): 134–147. doi: 10.1016/j.cell.2014.09.001
    [13]
    Li Z, Huang C, Bao C, et al. Exon-intron circular RNAs regulate transcription in the nucleus[J]. Nat Struct Mol Biol, 2015, 22(3): 256–264. doi: 10.1038/nsmb.2959
    [14]
    Guarnerio J, Bezzi M, Jeong JC, et al. Oncogenic role of fusion-circRNAs derived from cancer-associated chromosomal translocations[J]. Cell, 2016, 165(2): 289–302. doi: 10.1016/j.cell.2016.03.020
    [15]
    Vo JN, Cieslik M, Zhang Y, et al. The landscape of circular RNA in cancer[J]. Cell, 2019, 176(4): 869–881.e13. doi: 10.1016/j.cell.2018.12.021
    [16]
    Jeck WR, Sorrentino JA, Wang K, et al. Circular RNAs are abundant, conserved, and associated with ALU repeats[J]. RNA, 2013, 19(2): 141–157. doi: 10.1261/rna.035667.112
    [17]
    Ashwal-Fluss R, Meyer M, Pamudurti NR, et al. circRNA biogenesis competes with pre-mRNA splicing[J]. Mol Cell, 2014, 56(1): 55–66. doi: 10.1016/j.molcel.2014.08.019
    [18]
    Liang D, Wilusz JE. Short intronic repeat sequences facilitate circular RNA production[J]. Genes Dev, 2014, 28(20): 2233–2247. doi: 10.1101/gad.251926.114
    [19]
    Zhang X, Dong R, Zhang Y, et al. Diverse alternative back-splicing and alternative splicing landscape of circular RNAs[J]. Genome Res, 2016, 26(9): 1277–1287. doi: 10.1101/gr.202895.115
    [20]
    Conn SJ, Pillman KA, Toubia J, et al. The RNA binding protein quaking regulates formation of circRNAs[J]. Cell, 2015, 160(6): 1125–1134. doi: 10.1016/j.cell.2015.02.014
    [21]
    Errichelli L, Dini Modigliani S, Laneve P, et al. FUS affects circular RNA expression in murine embryonic stem cell-derived motor neurons[J]. Nat Commun, 2017, 8: 14741. doi: 10.1038/ncomms14741
    [22]
    Stagsted LVW, O'Leary ET, Ebbesen KK, et al. The RNA-binding protein SFPQ preserves long-intron splicing and regulates circRNA biogenesis in mammals[J]. Elife, 2021, 10: e63088. doi: 10.7554/eLife.63088
    [23]
    Ivanov A, Memczak S, Wyler E, et al. Analysis of intron sequences reveals hallmarks of circular RNA biogenesis in animals[J]. Cell Rep, 2015, 10(2): 170–177. doi: 10.1016/j.celrep.2014.12.019
    [24]
    Eisenberg E, Levanon EY. A-to-I RNA editing-immune protector and transcriptome diversifier[J]. Nat Rev Genet, 2018, 19(8): 473–490. doi: 10.1038/s41576-018-0006-1
    [25]
    Aktaş T, Avşar Ilık İ, Maticzka D, et al. DHX9 suppresses RNA processing defects originating from the Alu invasion of the human genome[J]. Nature, 2017, 544(7648): 115–119. doi: 10.1038/nature21715
    [26]
    Zheng X, Huang M, Xing L, et al. The circRNA circSEPT9 mediated by E2F1 and EIF4A3 facilitates the carcinogenesis and development of triple-negative breast cancer[J]. Mol Cancer, 2020, 19(1): 73. doi: 10.1186/s12943-020-01183-9
    [27]
    Tang Z, Li X, Zhao J, et al. TRCirc: a resource for transcriptional regulation information of circRNAs[J]. Brief Bioinform, 2019, 20(6): 2327–2333. doi: 10.1093/bib/bby083
    [28]
    Wang J, Zhang Y, Song H, et al. The circular RNA circSPARC enhances the migration and proliferation of colorectal cancer by regulating the JAK/STAT pathway[J]. Mol Cancer, 2021, 20(1): 81. doi: 10.1186/s12943-021-01375-x
    [29]
    Jiang T, Wang H, Liu L, et al. CircIL4R activates the PI3K/AKT signaling pathway via the miR-761/TRIM29/PHLPP1 axis and promotes proliferation and metastasis in colorectal cancer[J]. Mol Cancer, 2021, 20(1): 167. doi: 10.1186/s12943-021-01474-9
    [30]
    Zhong Y, Du Y, Yang X, et al. Circular RNAs function as ceRNAs to regulate and control human cancer progression[J]. Mol Cancer, 2018, 17(1): 79. doi: 10.1186/s12943-018-0827-8
    [31]
    Kristensen LS, Andersen MS, Stagsted LVW, et al. The biogenesis, biology and characterization of circular RNAs[J]. Nat Rev Genet, 2019, 20(11): 675–691. doi: 10.1038/s41576-019-0158-7
    [32]
    Memczak S, Jens M, Elefsinioti A, et al. Circular RNAs are a large class of animal RNAs with regulatory potency[J]. Nature, 2013, 495(7441): 333–338. doi: 10.1038/nature11928
    [33]
    Piwecka M, Glažar P, Hernandez-Miranda LR, et al. Loss of a mammalian circular RNA locus causes miRNA deregulation and affects brain function[J]. Science, 2017, 357(6357): eaam8526. doi: 10.1126/science.aam8526
    [34]
    Yao W, Li Y, Han L, et al. The CDR1as/miR-7/TGFBR2 axis modulates EMT in silica-induced pulmonary fibrosis[J]. Toxicol Sci, 2018, 166(2): 465–478. doi: 10.1093/toxsci/kfy221
    [35]
    Wang J, Zhu M, Song J, et al. The circular RNA circTXNRD1 promoted ambient particulate matter-induced inflammation in human bronchial epithelial cells by regulating miR-892a/COX-2 axis[J]. Chemosphere, 2022, 286: 131614. doi: 10.1016/j.chemosphere.2021.131614
    [36]
    Li M, Hua Q, Shao Y, et al. Circular RNA circBbs9 promotes PM2.5-induced lung inflammation in mice via NLRP3 inflammasome activation[J]. Environ Int, 2020, 143: 105976. doi: 10.1016/j.envint.2020.105976
    [37]
    Zhou M, Li L, Chen B, et al. Circ-SHPRH suppresses cadmium-induced transformation of human bronchial epithelial cells by regulating QKI expression via miR-224–5p[J]. Ecotoxicol Environ Saf, 2021, 220: 112378. doi: 10.1016/j.ecoenv.2021.112378
    [38]
    Dai X, Chen C, Yang Q, et al. Exosomal circRNA_100284 from arsenite-transformed cells, via microRNA-217 regulation of EZH2, is involved in the malignant transformation of human hepatic cells by accelerating the cell cycle and promoting cell proliferation[J]. Cell Death Dis, 2018, 9(5): 454. doi: 10.1038/s41419-018-0485-1
    [39]
    Huang A, Zheng H, Wu Z, et al. Circular RNA-protein interactions: functions, mechanisms, and identification[J]. Theranostics, 2020, 10(8): 3503–3517. doi: 10.7150/thno.42174
    [40]
    Zang J, Lu D, Xu A. The interaction of circRNAs and RNA binding proteins: an important part of circRNA maintenance and function[J]. J Neurosci Res, 2020, 98(1): 87–97. doi: 10.1002/jnr.24356
    [41]
    Wang Z, Lei X. Prediction of RBP binding sites on circRNAs using an LSTM-based deep sequence learning architecture[J]. Brief Bioinform, 2021, 22(6): bbab342. doi: 10.1093/bib/bbab342
    [42]
    Du WW, Yang W, Li X, et al. A circular RNA circ-DNMT1 enhances breast cancer progression by activating autophagy[J]. Oncogene, 2018, 37(44): 5829–5842. doi: 10.1038/s41388-018-0369-y
    [43]
    Abdelmohsen K, Panda AC, Munk R, et al. Identification of HuR target circular RNAs uncovers suppression of PABPN1 translation by CircPABPN1[J]. RNA Biol, 2017, 14(3): 361–369. doi: 10.1080/15476286.2017.1279788
    [44]
    Du WW, Yang W, Liu E, et al. Foxo3 circular RNA retards cell cycle progression via forming ternary complexes with p21 and CDK2[J]. Nucleic Acids Res, 2016, 44(6): 2846–2858. doi: 10.1093/nar/gkw027
    [45]
    Du WW, Yang W, Chen Y, et al. Foxo3 circular RNA promotes cardiac senescence by modulating multiple factors associated with stress and senescence responses[J]. Eur Heart J, 2017, 38(18): 1402–1412. doi: 10.1093/eurheartj/ehw001
    [46]
    Chen R, Chen X, Xia L, et al. N6-methyladenosine modification of circNSUN2 facilitates cytoplasmic export and stabilizes HMGA2 to promote colorectal liver metastasis[J]. Nat Commun, 2019, 10(1): 4695. doi: 10.1038/s41467-019-12651-2
    [47]
    Jia Y, Li X, Nan A, et al. Circular RNA 406961 interacts with ILF2 to regulate PM2.5-induced inflammatory responses in human bronchial epithelial cells via activation of STAT3/JNK pathways[J]. Environ Int, 2020, 141: 105755. doi: 10.1016/j.envint.2020.105755
    [48]
    Zhou Z, Jiang R, Yang X, et al. circRNA mediates silica-induced macrophage activation via HECTD1/ZC3H12A-dependent ubiquitination[J]. Theranostics, 2018, 8(2): 575–592. doi: 10.7150/thno.21648
    [49]
    Bolisetty MT, Graveley BR. Circuitous route to transcription regulation[J]. Mol Cell, 2013, 51(6): 705–706. doi: 10.1016/j.molcel.2013.09.012
    [50]
    Ma N, Pan J, Wen Y, et al. RETRACTED: circTulp4 functions in Alzheimer's disease pathogenesis by regulating its parental gene, Tulp4[J]. Mol Ther, 2021, 29(6): 2167–2181. doi: 10.1016/j.ymthe.2021.02.008
    [51]
    Chen N, Zhao G, Yan X, et al. A novel FLI1 exonic circular RNA promotes metastasis in breast cancer by coordinately regulating TET1 and DNMT1[J]. Genome Biol, 2018, 19(1): 218. doi: 10.1186/s13059-018-1594-y
    [52]
    Gong X, Tian M, Cao N, et al. Circular RNA circEsyt2 regulates vascular smooth muscle cell remodeling via splicing regulation[J]. J Clin Invest, 2021, 131(24): e147031. doi: 10.1172/JCI147031
    [53]
    Wu N, Yuan Z, Du KY, et al. Translation of yes-associated protein (YAP) was antagonized by its circular RNA via suppressing the assembly of the translation initiation machinery[J]. Cell Death Differ, 2019, 26(12): 2758–2773. doi: 10.1038/s41418-019-0337-2
    [54]
    Pamudurti NR, Bartok O, Jens M, et al. Translation of CircRNAs[J]. Mol Cell, 2017, 66(1): 9–21.e7. doi: 10.1016/j.molcel.2017.02.021
    [55]
    Wang Y, Wu C, Du Y, et al. Expanding uncapped translation and emerging function of circular RNA in carcinomas and noncarcinomas[J]. Mol Cancer, 2022, 21(1): 13. doi: 10.1186/s12943-021-01484-7
    [56]
    Legnini I, Di Timoteo G, Rossi F, et al. Circ-ZNF609 is a circular RNA that can be translated and functions in myogenesis[J]. Mol Cell, 2017, 66(1): 22–37.e9. doi: 10.1016/j.molcel.2017.02.017
    [57]
    Zhang M, Zhao K, Xu X, et al. A peptide encoded by circular form of LINC-PINT suppresses oncogenic transcriptional elongation in glioblastoma[J]. Nat Commun, 2018, 9(1): 4475. doi: 10.1038/s41467-018-06862-2
    [58]
    Zhang M, Huang N, Yang X, et al. A novel protein encoded by the circular form of the SHPRH gene suppresses glioma tumorigenesis[J]. Oncogene, 2018, 37(13): 1805–1814. doi: 10.1038/s41388-017-0019-9
    [59]
    Meyer KD, Patil DP, Zhou J, et al. 5' UTR m6 A promotes cap-independent translation[J]. Cell, 2015, 163(4): 999–1010. doi: 10.1016/j.cell.2015.10.012
    [60]
    Yang Y, Fan X, Mao M, et al. Extensive translation of circular RNAs driven by N6-methyladenosine[J]. Cell Res, 2017, 27(5): 626–641. doi: 10.1038/cr.2017.31
    [61]
    Zhou J, Wan J, Gao X, et al. Dynamic m6A mRNA methylation directs translational control of heat shock response[J]. Nature, 2015, 526(7574): 591–594. doi: 10.1038/nature15377
    [62]
    Abe N, Matsumoto K, Nishihara M, et al. Rolling circle translation of circular RNA in living human cells[J]. Sci Rep, 2015, 5: 16435. doi: 10.1038/srep16435
    [63]
    Liu Y, Li Z, Zhang M, et al. Rolling-translated EGFR variants sustain EGFR signaling and promote glioblastoma tumorigenicity[J]. Neuro Oncol, 2021, 23(5): 743–756. doi: 10.1093/neuonc/noaa279
    [64]
    Glažar P, Papavasileiou P, Rajewsky N. circBase: a database for circular RNAs[J]. RNA, 2014, 20(11): 1666–1670. doi: 10.1261/rna.043687.113
    [65]
    Liu M, Wang Q, Shen J, et al. Circbank: a comprehensive database for circRNA with standard nomenclature[J]. RNA Biol, 2019, 16(7): 899–905. doi: 10.1080/15476286.2019.1600395
    [66]
    Dong R, Ma X, Li G, et al. CIRCpedia v2: an updated database for comprehensive circular RNA annotation and expression comparison[J]. Genomics Proteomics Bioinformatics, 2018, 16(4): 226–233. doi: 10.1016/j.gpb.2018.08.001
    [67]
    Xie F, Liu S, Wang J, et al. deepBase v3.0: expression atlas and interactive analysis of ncRNAs from thousands of deep-sequencing data[J]. Nucleic Acids Res, 2021, 49(D1): D877–D883. doi: 10.1093/nar/gkaa1039
    [68]
    Dudekula DB, Panda AC, Grammatikakis I, et al. CircInteractome: a web tool for exploring circular RNAs and their interacting proteins and microRNAs[J]. RNA Biol, 2016, 13(1): 34–42. doi: 10.1080/15476286.2015.1128065
    [69]
    Chen Y, Yao L, Tang Y, et al. CircNet 2.0: an updated database for exploring circular RNA regulatory networks in cancers[J]. Nucleic Acids Res, 2022, 50(D1): D93–D101. doi: 10.1093/nar/gkab1036
    [70]
    Wu W, Ji P, Zhao F. CircAtlas: an integrated resource of one million highly accurate circular RNAs from 1070 vertebrate transcriptomes[J]. Genome Biol, 2020, 21(1): 101. doi: 10.1186/s13059-020-02018-y
    [71]
    Li JH, Liu S, Zhou H, et al. starBase v2.0: decoding miRNA-ceRNA, miRNA-ncRNA and protein-RNA interaction networks from large-scale CLIP-Seq data[J]. Nucleic Acids Res, 2014, 42(Database issue): D92–D97. doi: 10.1093/nar/gkt1248.
    [72]
    Chen X, Han P, Zhou T, et al. circRNADb: a comprehensive database for human circular RNAs with protein-coding annotations[J]. Sci Rep, 2016, 6: 34985. doi: 10.1038/srep34985
    [73]
    Huang W, Ling Y, Zhang S, et al. TransCirc: an interactive database for translatable circular RNAs based on multi-omics evidence[J]. Nucleic Acids Res, 2021, 49(D1): D236–D242. doi: 10.1093/nar/gkaa823
    [74]
    Li H, Xie M, Wang Y, et al. riboCIRC: a comprehensive database of translatable circRNAs[J]. Genome Biol, 2021, 22(1): 79. doi: 10.1186/s13059-021-02300-7
    [75]
    Feng J, Chen W, Dong X, et al. CSCD2: an integrated interactional database of cancer-specific circular RNAs[J]. Nucleic Acids Res, 2022, 50(D1): D1179–D1183. doi: 10.1093/nar/gkab830
    [76]
    Fan C, Lei X, Tie J, et al. CircR2Disease v2.0: an updated web server for experimentally validated circRNA-disease associations and its application[J]. Genomics Proteomics Bioinformatics, 2021, S1672-0229(21): 00246-1. doi: 10.1016/j.gpb.2021.10.002
    [77]
    Zhang W, Liu Y, Min Z, et al. circMine: a comprehensive database to integrate, analyze and visualize human disease-related circRNA transcriptome[J]. Nucleic Acids Res, 2022, 50(D1): D83–D92. doi: 10.1093/nar/gkab809
    [78]
    Ghosal S, Das S, Sen R, et al. Circ2Traits: a comprehensive database for circular RNA potentially associated with disease and traits[J]. Front Genet, 2013, 4: 283. doi: 10.3389/fgene.2013.00283
    [79]
    Lai H, Li Y, Zhang H, et al. exoRBase 2.0: an atlas of mRNA, lncRNA and circRNA in extracellular vesicles from human biofluids[J]. Nucleic Acids Res, 2022, 50(D1): D118–D128. doi: 10.1093/nar/gkab1085
    [80]
    Zhang P, Meng X, Chen H, et al. PlantCircNet: a database for plant circRNA-miRNA-mRNA regulatory networks[J]. Database, 2017, 2017: bax089. doi: 10.1093/database/bax089
    [81]
    Wang S, Zhang K, Tan S, et al. Circular RNAs in body fluids as cancer biomarkers: the new frontier of liquid biopsies[J]. Mol Cancer, 2021, 20(1): 13. doi: 10.1186/s12943-020-01298-z
    [82]
    Li D, Li Z, Yang Y, et al. Circular RNAs as biomarkers and therapeutic targets in environmental chemical exposure-related diseases[J]. Environ Res, 2020, 180: 108825. doi: 10.1016/j.envres.2019.108825
    [83]
    Misir S, Wu N, Yang BB. Specific expression and functions of circular RNAs[J]. Cell Death Differ, 2022, 29(3): 481–491. doi: 10.1038/s41418-022-00948-7
    [84]
    Wang Y, Liu J, Ma J, et al. Exosomal circRNAs: biogenesis, effect and application in human diseases[J]. Mol Cancer, 2019, 18(1): 116. doi: 10.1186/s12943-019-1041-z
    [85]
    Li J, Zhang G, Liu CG, et al. The potential role of exosomal circRNAs in the tumor microenvironment: insights into cancer diagnosis and therapy[J]. Theranostics, 2022, 12(1): 87–104. doi: 10.7150/thno.64096
    [86]
    Zhou H, He X, He Y, et al. Exosomal circRNAs: emerging players in tumor metastasis[J]. Front Cell Dev Biol, 2021, 9: 786224. doi: 10.3389/fcell.2021.786224
    [87]
    Yang Q, Li F, He AT, et al. Circular RNAs: expression, localization, and therapeutic potentials[J]. Mol Ther, 2021, 29(5): 1683–1702. doi: 10.1016/j.ymthe.2021.01.018
    [88]
    Fan Z, Xiao T, Luo H, et al. A study on the roles of long non-coding RNA and circular RNA in the pulmonary injuries induced by polystyrene microplastics[J]. Environ Int, 2022, 163: 107223. doi: 10.1016/j.envint.2022.107223
    [89]
    Fang S, Guo H, Cheng Y, et al. circHECTD1 promotes the silica-induced pulmonary endothelial-mesenchymal transition via HECTD1[J]. Cell Death Dis, 2018, 9(3): 396. doi: 10.1038/s41419-018-0432-1
    [90]
    Yang X, Wang J, Zhou Z, et al. Silica-induced initiation of circular ZC3H4 RNA/ZC3H4 pathway promotes the pulmonary macrophage activation[J]. FASEB J, 2018, 32(6): 3264–3277. doi: 10.1096/fj.201701118R
    [91]
    Cheng Z, Zhang Y, Wu S, et al. Peripheral blood circular RNA hsa_circ_0058493 as a potential novel biomarker for silicosis and idiopathic pulmonary fibrosis[J]. Ecotoxicol Environ Saf, 2022, 236: 113451. doi: 10.1016/j.ecoenv.2022.113451
    [92]
    Roy S, Kanda M, Nomura S, et al. Diagnostic efficacy of circular RNAs as noninvasive, liquid biopsy biomarkers for early detection of gastric cancer[J]. Mol Cancer, 2022, 21(1): 42. doi: 10.1186/s12943-022-01527-7
    [93]
    Zheng R, Zhang K, Tan S, et al. Exosomal circLPAR1 functions in colorectal cancer diagnosis and tumorigenesis through suppressing BRD4 via METTL3-eIF3h interaction[J]. Mol Cancer, 2022, 21(1): 49. doi: 10.1186/s12943-021-01471-y
    [94]
    Li J, Li Z, Jiang P, et al. Circular RNA IARS (circ-IARS) secreted by pancreatic cancer cells and located within exosomes regulates endothelial monolayer permeability to promote tumor metastasis[J]. J Exp Clin Cancer Res, 2018, 37(1): 177. doi: 10.1186/s13046-018-0822-3
    [95]
    Li J, Hu ZQ, Yu SY, et al. CircRPN2 Inhibits Aerobic Glycolysis and Metastasis in Hepatocellular Carcinoma[J]. Cancer Res, 2022, 82(6): 1055–1069. doi: 10.1158/0008-5472.CAN-21-1259
    [96]
    Liang G, Ling Y, Mehrpour M, et al. Autophagy-associated circRNA circCDYL augments autophagy and promotes breast cancer progression[J]. Mol Cancer, 2020, 19(1): 65. doi: 10.1186/s12943-020-01152-2
    [97]
    He AT, Liu J, Li F, et al. Targeting circular RNAs as a therapeutic approach: current strategies and challenges[J]. Signal Transduct Target Ther, 2021, 6(1): 185. doi: 10.1038/s41392-021-00569-5
    [98]
    Lavenniah A, Luu TDA, Li YP, et al. Engineered circular RNA sponges act as miRNA inhibitors to attenuate pressure overload-induced cardiac hypertrophy[J]. Mol Ther, 2020, 28(6): 1506–1517. doi: 10.1016/j.ymthe.2020.04.006
    [99]
    Du A, Li S, Zhou Y, et al. M6A-mediated upregulation of circMDK promotes tumorigenesis and acts as a nanotherapeutic target in hepatocellular carcinoma[J]. Mol Cancer, 2022, 21(1): 109. doi: 10.1186/s12943-022-01575-z
    [100]
    Zhao Q, Liu J, Deng H, et al. Targeting Mitochondria-Located circRNA SCAR Alleviates NASH via Reducing mROS Output[J]. Cell, 2020, 183(1): 76–93.e22. doi: 10.1016/j.cell.2020.08.009
    [101]
    Yang L, Han B, Zhang Z, et al. Extracellular vesicle-mediated delivery of circular RNA SCMH1 promotes functional recovery in rodent and nonhuman primate ischemic stroke models[J]. Circulation, 2020, 142(6): 556–574. doi: 10.1161/CIRCULATIONAHA.120.045765
    [102]
    Zhang D, Ni N, Wang Y, et al. CircRNA-vgll3 promotes osteogenic differentiation of adipose-derived mesenchymal stem cells via modulating miRNA-dependent integrin α5 expression[J]. Cell Death Differ, 2021, 28(1): 283–302. doi: 10.1038/s41418-020-0600-6
    [103]
    Hu K, Liu X, Li Y, et al. Exosomes mediated transfer of circ_UBE2D2 enhances the resistance of breast cancer to tamoxifen by binding to MiR-200a-3p[J]. Med Sci Monit, 2020, 26: e922253. doi: 10.12659/MSM.922253
    [104]
    Qu L, Yi Z, Shen Y, et al. Circular RNA vaccines against SARS-CoV-2 and emerging variants[J]. Cell, 2022, 185(10): 1728–1744.e16. doi: 10.1016/j.cell.2022.03.044
    [105]
    Gu J, Su C, Huang F, et al. Past, present and future: the relationship between circular RNA and immunity[J]. Front Immunol, 2022, 13: 894707. doi: 10.3389/fimmu.2022.894707
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    Periodical cited type(45)

    1. Hou W, Guan F, Chen W, et al. Breastfeeding, genetic susceptibility, and the risk of asthma and allergic diseases in children and adolescents: a retrospective national population-based cohort study. BMC Public Health, 2024, 24(1): 3056. DOI:10.1186/s12889-024-20501-0
    2. Nandi S, Varotariya K, Luhana S, et al. GWAS for identification of genomic regions and candidate genes in vegetable crops. Funct Integr Genomics, 2024, 24(6): 203. DOI:10.1007/s10142-024-01477-x
    3. Sung HL, Lin WY. Causal effects of cardiovascular health on five epigenetic clocks. Clin Epigenetics, 2024, 16(1): 134. DOI:10.1186/s13148-024-01752-5
    4. Kang HY, Choe EK. Clinical Strategies in Gene Screening Counseling for the Healthy General Population. Korean J Fam Med, 2024, 45(2): 61-68. DOI:10.4082/kjfm.23.0254
    5. Lee SB, Choi JE, Hong KW, et al. Genetic Variants Linked to Myocardial Infarction in Individuals with Non-Alcoholic Fatty Liver Disease and Their Potential Interaction with Dietary Patterns. Nutrients, 2024, 16(5): 602. DOI:10.3390/nu16050602
    6. Zhang S, Jiang Z, Zeng P. Incorporating genetic similarity of auxiliary samples into eGene identification under the transfer learning framework. J Transl Med, 2024, 22(1): 258. DOI:10.1186/s12967-024-05053-6
    7. Seo H, Park JH, Hwang JT, et al. Epigenetic Profiling of Type 2 Diabetes Mellitus: An Epigenome-Wide Association Study of DNA Methylation in the Korean Genome and Epidemiology Study. Genes (Basel), 2023, 14(12): 2207. DOI:10.3390/genes14122207
    8. Han J, Zhang L, Yan R, et al. CoNet: Efficient Network Regression for Survival Analysis in Transcriptome-Wide Association Studies-With Applications to Studies of Breast Cancer. Genes (Basel), 2023, 14(3): 586. DOI:10.3390/genes14030586
    9. Padilla-Martinez F, Szczerbiński Ł, Citko A, et al. Testing the Utility of Polygenic Risk Scores for Type 2 Diabetes and Obesity in Predicting Metabolic Changes in a Prediabetic Population: An Observational Study. Int J Mol Sci, 2022, 23(24): 16081. DOI:10.3390/ijms232416081
    10. Muneeb M, Feng S, Henschel A. Transfer learning for genotype-phenotype prediction using deep learning models. BMC Bioinformatics, 2022, 23(1): 511. DOI:10.1186/s12859-022-05036-8
    11. Qiao J, Shao Z, Wu Y, et al. Detecting associated genes for complex traits shared across East Asian and European populations under the framework of composite null hypothesis testing. J Transl Med, 2022, 20(1): 424. DOI:10.1186/s12967-022-03637-8
    12. Shao Z, Wang T, Qiao J, et al. A comprehensive comparison of multilocus association methods with summary statistics in genome-wide association studies. BMC Bioinformatics, 2022, 23(1): 359. DOI:10.1186/s12859-022-04897-3
    13. Roh H. A genome-wide association study of the occurrence of genetic variations in Edwardsiella piscicida, Vibrio harveyi, and Streptococcus parauberis under stressed environments. J Fish Dis, 2022, 45(9): 1373-1388. DOI:10.1111/jfd.13668
    14. Zhang M, Qiao J, Zhang S, et al. Exploring the association between birthweight and breast cancer using summary statistics from a perspective of genetic correlation, mediation, and causality. J Transl Med, 2022, 20(1): 227. DOI:10.1186/s12967-022-03435-2
    15. Yamamoto A, Shibuya T. More practical differentially private publication of key statistics in GWAS. Bioinform Adv, 2021, 1(1): vbab004. DOI:10.1093/bioadv/vbab004
    16. Mkize N, Maiwashe A, Dzama K, et al. Suitability of GWAS as a Tool to Discover SNPs Associated with Tick Resistance in Cattle: A Review. Pathogens, 2021, 10(12): 1604. DOI:10.3390/pathogens10121604
    17. Lu H, Qiao J, Shao Z, et al. A comprehensive gene-centric pleiotropic association analysis for 14 psychiatric disorders with GWAS summary statistics. BMC Med, 2021, 19(1): 314. DOI:10.1186/s12916-021-02186-z
    18. Monnot S, Desaint H, Mary-Huard T, et al. Deciphering the Genetic Architecture of Plant Virus Resistance by GWAS, State of the Art and Potential Advances. Cells, 2021, 10(11): 3080. DOI:10.3390/cells10113080
    19. Lu H, Wei Y, Jiang Z, et al. Integrative eQTL-weighted hierarchical Cox models for SNP-set based time-to-event association studies. J Transl Med, 2021, 19(1): 418. DOI:10.1186/s12967-021-03090-z
    20. Gao Y, Zhang J, Zhao H, et al. Instrumental Heterogeneity in Sex-Specific Two-Sample Mendelian Randomization: Empirical Results From the Relationship Between Anthropometric Traits and Breast/Prostate Cancer. Front Genet, 2021, 12: 651332. DOI:10.3389/fgene.2021.651332
    21. Petersen KS, Kris-Etherton PM, McCabe GP, et al. Perspective: Planning and Conducting Statistical Analyses for Human Nutrition Randomized Controlled Trials: Ensuring Data Quality and Integrity. Adv Nutr, 2021, 12(5): 1610-1624. DOI:10.1093/advances/nmab045
    22. Muneeb M, Henschel A. Eye-color and Type-2 diabetes phenotype prediction from genotype data using deep learning methods. BMC Bioinformatics, 2021, 22(1): 198. DOI:10.1186/s12859-021-04077-9
    23. O'Rielly DD, Rahman P. Genetic Epidemiology of Complex Phenotypes. Methods Mol Biol, 2021, 2249: 335-367. DOI:10.1007/978-1-0716-1138-8_19
    24. Scossa F, Fernie AR. Ancestral sequence reconstruction - An underused approach to understand the evolution of gene function in plants?. Comput Struct Biotechnol J, 2021, 19: 1579-1594. DOI:10.1016/j.csbj.2021.03.008
    25. Lu H, Zhang J, Jiang Z, et al. Detection of Genetic Overlap Between Rheumatoid Arthritis and Systemic Lupus Erythematosus Using GWAS Summary Statistics. Front Genet, 2021, 12: 656545. DOI:10.3389/fgene.2021.656545
    26. McGuire D, Jiang Y, Liu M, et al. Model-based assessment of replicability for genome-wide association meta-analysis. Nat Commun, 2021, 12(1): 1964. DOI:10.1038/s41467-021-21226-z
    27. Dennis JK, Sealock JM, Straub P, et al. Clinical laboratory test-wide association scan of polygenic scores identifies biomarkers of complex disease. Genome Med, 2021, 13(1): 6. DOI:10.1186/s13073-020-00820-8
    28. Ramanan VK, Wang X, Przybelski SA, et al. Variants in PPP2R2B and IGF2BP3 are associated with higher tau deposition. Brain Commun, 2020, 2(2): fcaa159. DOI:10.1093/braincomms/fcaa159
    29. Chen H, Wang T, Yang J, et al. Improved Detection of Potentially Pleiotropic Genes in Coronary Artery Disease and Chronic Kidney Disease Using GWAS Summary Statistics. Front Genet, 2020, 11: 592461. DOI:10.3389/fgene.2020.592461
    30. Xiao L, Yuan Z, Jin S, et al. Multiple-Tissue Integrative Transcriptome-Wide Association Studies Discovered New Genes Associated With Amyotrophic Lateral Sclerosis. Front Genet, 2020, 11: 587243. DOI:10.3389/fgene.2020.587243
    31. Jin T, Youn J, Kim AN, et al. Interactions of Habitual Coffee Consumption by Genetic Polymorphisms with the Risk of Prediabetes and Type 2 Diabetes Combined. Nutrients, 2020, 12(8): 2228. DOI:10.3390/nu12082228
    32. Kuo TT, Jiang X, Tang H, et al. iDASH secure genome analysis competition 2018: blockchain genomic data access logging, homomorphic encryption on GWAS, and DNA segment searching. BMC Med Genomics, 2020, 13(Suppl 7): 98. DOI:10.1186/s12920-020-0715-0
    33. Padilla-Martínez F, Collin F, Kwasniewski M, et al. Systematic Review of Polygenic Risk Scores for Type 1 and Type 2 Diabetes. Int J Mol Sci, 2020, 21(5): 1703. DOI:10.3390/ijms21051703
    34. Lan T, Yang B, Zhang X, et al. Statistical Methods and Software for Substance Use and Dependence Genetic Research. Curr Genomics, 2019, 20(3): 172-183. DOI:10.2174/1389202920666190617094930
    35. Gaudillo J, Rodriguez JJR, Nazareno A, et al. Machine learning approach to single nucleotide polymorphism-based asthma prediction. PLoS One, 2019, 14(12): e0225574. DOI:10.1371/journal.pone.0225574
    36. Romagnoni A, Jégou S, Van Steen K, et al. Comparative performances of machine learning methods for classifying Crohn Disease patients using genome-wide genotyping data. Sci Rep, 2019, 9(1): 10351. DOI:10.1038/s41598-019-46649-z
    37. Himmerich H, Bentley J, Kan C, et al. Genetic risk factors for eating disorders: an update and insights into pathophysiology. Ther Adv Psychopharmacol, 2019, 9: 2045125318814734. DOI:10.1177/2045125318814734
    38. Sanyal N, Lo MT, Kauppi K, et al. GWASinlps: non-local prior based iterative SNP selection tool for genome-wide association studies. Bioinformatics, 2019, 35(1): 1-11. DOI:10.1093/bioinformatics/bty472
    39. Brinster R, Köttgen A, Tayo BO, et al. Control procedures and estimators of the false discovery rate and their application in low-dimensional settings: an empirical investigation. BMC Bioinformatics, 2018, 19(1): 78. DOI:10.1186/s12859-018-2081-x
    40. Zeng P, Wang T, Huang S. Cis-SNPs Set Testing and PrediXcan Analysis for Gene Expression Data using Linear Mixed Models. Sci Rep, 2017, 7(1): 15237. DOI:10.1038/s41598-017-15055-8
    41. Zeng P, Zhou X, Huang S. Prediction of gene expression with cis-SNPs using mixed models and regularization methods. BMC Genomics, 2017, 18(1): 368. DOI:10.1186/s12864-017-3759-6
    42. Läll K, Mägi R, Morris A, et al. Personalized risk prediction for type 2 diabetes: the potential of genetic risk scores. Genet Med, 2017, 19(3): 322-329. DOI:10.1038/gim.2016.103
    43. Umehara H, Numata S, Tajima A, et al. Calcium Signaling Pathway Is Associated with the Long-Term Clinical Response to Selective Serotonin Reuptake Inhibitors (SSRI) and SSRI with Antipsychotics in Patients with Obsessive-Compulsive Disorder. PLoS One, 2016, 11(6): e0157232. DOI:10.1371/journal.pone.0157232
    44. Zhang Q, Zhao Y, Zhang R, et al. A Comparative Study of Five Association Tests Based on CpG Set for Epigenome-Wide Association Studies. PLoS One, 2016, 11(6): e0156895. DOI:10.1371/journal.pone.0156895
    45. Gasc C, Peyretaillade E, Peyret P. Sequence capture by hybridization to explore modern and ancient genomic diversity in model and nonmodel organisms. Nucleic Acids Res, 2016, 44(10): 4504-18. DOI:10.1093/nar/gkw309

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