Mini-Review Article

Non-Canonical Targets of MicroRNAs: Role in Transcriptional Regulation, Disease Pathogenesis and Potential for Therapeutic Targets

Author(s): Aishwarya Ray, Abhisek Sarkar, Sounak Banerjee and Kaushik Biswas*

Volume 13, Issue 2, 2024

Published on: 22 January, 2024

Page: [83 - 95] Pages: 13

DOI: 10.2174/0122115366278651240105071533

Price: $65

Open Access Journals Promotions 2
Abstract

MicroRNAs are a class of regulatory, non-coding small ribonucleic acid (RNA) molecules found in eukaryotes. Dysregulated expression of microRNAs can lead to downregulation or upregulation of their target gene. In general, microRNAs bind with the Argonaute protein and its interacting partners to form a silencing complex. This silencing complex binds with fully or partial complementary sequences in the 3’-UTR of their cognate target mRNAs and leads to degradation of the transcripts or translational inhibition, respectively. However, recent developments point towards the ability of these microRNAs to bind to the promoters, enhancers or coding sequences, leading to upregulation of their target genes. This review briefly summarizes the various non-canonical binding sites of microRNAs and their regulatory roles in various diseased conditions.

Keywords: microRNA, non-canonical targets, gene expression, promotor, enhancer, coding sequence, 5’-UTR.

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[1]
Iwasaki S, Kobayashi M, Yoda M, et al. Hsc70/Hsp90 chaperone machinery mediates ATP-dependent RISC loading of small RNA duplexes. Mol Cell 2010; 39(2): 292-9.
[http://dx.doi.org/10.1016/j.molcel.2010.05.015] [PMID: 20605501]
[2]
Kuzuoğlu-Öztürk D, Bhandari D, Huntzinger E, Fauser M, Helms S, Izaurralde E. mi RISC and the CCR 4- NOT complex silence mRNA targets independently of 43S ribosomal scanning. EMBO J 2016; 35(11): 1186-203.
[http://dx.doi.org/10.15252/embj.201592901] [PMID: 27009120]
[3]
Jonas S, Izaurralde E. Towards a molecular understanding of microRNA-mediated gene silencing. Nat Rev Genet 2015; 16(7): 421-33.
[http://dx.doi.org/10.1038/nrg3965] [PMID: 26077373]
[4]
Braun JE, Huntzinger E, Izaurralde E. A molecular link between miRISCs and deadenylases provides new insight into the mechanism of gene silencing by microRNAs. Cold Spring Harb Perspect Biol 2012; 4(12): a012328.
[http://dx.doi.org/10.1101/cshperspect.a012328] [PMID: 23209154]
[5]
Fabian MR, Sonenberg N. The mechanics of miRNA-mediated gene silencing: A look under the hood of miRISC. Nat Struct Mol Biol 2012; 19(6): 586-93.
[http://dx.doi.org/10.1038/nsmb.2296] [PMID: 22664986]
[6]
Hafner M, Katsantoni M, Köster T, et al. CLIP and complementary methods. Nat Rev Methods Primers 2021; 1(1): 20.
[http://dx.doi.org/10.1038/s43586-021-00018-1]
[7]
Eulalio A, Huntzinger E, Nishihara T, Rehwinkel J, Fauser M, Izaurralde E. Deadenylation is a widespread effect of miRNA regulation. RNA 2009; 15(1): 21-32.
[http://dx.doi.org/10.1261/rna.1399509] [PMID: 19029310]
[8]
Chen CYA, Zheng D, Xia Z, Shyu AB. Ago-TNRC6 triggers microRNA-mediated decay by promoting two deadenylation steps. Nat Struct Mol Biol 2009; 16(11): 1160-6.
[http://dx.doi.org/10.1038/nsmb.1709] [PMID: 19838187]
[9]
Fukao A, Mishima Y, Takizawa N, et al. MicroRNAs trigger dissociation of eIF4AI and eIF4AII from target mRNAs in humans. Mol Cell 2014; 56(1): 79-89.
[http://dx.doi.org/10.1016/j.molcel.2014.09.005] [PMID: 25280105]
[10]
de Rie D, Abugessaisa I, Alam T, et al. An integrated expression atlas of miRNAs and their promoters in human and mouse. Nat Biotechnol 2017; 35(9): 872-8.
[http://dx.doi.org/10.1038/nbt.3947] [PMID: 28829439]
[11]
He L, Hannon GJ. MicroRNAs: Small RNAs with a big role in gene regulation. Nat Rev Genet 2004; 5(7): 522-31.
[http://dx.doi.org/10.1038/nrg1379] [PMID: 15211354]
[12]
Hwang H-W, Mendell JT. MicroRNAs in cell proliferation, cell death, and tumorigenesis. Br J Cancer 2006; 94(6): 776-80.
[http://dx.doi.org/10.1038/sj.bjc.6603023] [PMID: 16495913]
[13]
Paul P, Chakraborty A, Sarkar D, et al. Interplay between miRNAs and human diseases. J Cell Physiol 2018; 233(3): 2007-18.
[http://dx.doi.org/10.1002/jcp.25854] [PMID: 28181241]
[14]
Natarajan SK, Smith MA, Wehrkamp CJ, Mohr AM, Mott JL. MicroRNA function in human diseases. Med Epigenet 2013; 1(1): 106-15.
[http://dx.doi.org/10.1159/000356447]
[15]
Croce CM. Causes and consequences of microRNA dysregulation in cancer. Nat Rev Genet 2009; 10(10): 704-14.
[http://dx.doi.org/10.1038/nrg2634] [PMID: 19763153]
[16]
Wang J, Chen J, Sen S. MicroRNA as biomarkers and diagnostics. J Cell Physiol 2016; 231(1): 25-30.
[http://dx.doi.org/10.1002/jcp.25056] [PMID: 26031493]
[17]
Zhang Y, Liu D, Chen X, et al. Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol Cell 2010; 39(1): 133-44.
[http://dx.doi.org/10.1016/j.molcel.2010.06.010] [PMID: 20603081]
[18]
Bayraktar R, Van Roosbroeck K, Calin GA. Cell-to-cell communication: MicroRNAs as hormones. Mol Oncol 2017; 11(12): 1673-86.
[http://dx.doi.org/10.1002/1878-0261.12144] [PMID: 29024380]
[19]
Halvorsen AR, Bjaanæs M, LeBlanc M, et al. A unique set of 6 circulating microRNAs for early detection of non-small cell lung cancer. Oncotarget 2016; 7(24): 37250-9.
[http://dx.doi.org/10.18632/oncotarget.9363] [PMID: 27191990]
[20]
Liu Y, Tang D, Zheng S, Su R, Tang Y. Serum microRNA-195 as a potential diagnostic biomarker for breast cancer: A systematic review and meta-analysis. Int J Clin Exp Pathol 2019; 12(11): 3982-91.
[PMID: 31933794]
[21]
Sabry D, El-Deek SEM, Maher M, et al. Role of miRNA-210, miRNA-21 and miRNA-126 as diagnostic biomarkers in colorectal carcinoma: Impact of HIF-1α-VEGF signaling pathway. Mol Cell Biochem 2019; 454(1-2): 177-89.
[http://dx.doi.org/10.1007/s11010-018-3462-1] [PMID: 30357530]
[22]
Matin F, Jeet V, Moya L, et al. A plasma biomarker panel of four MicroRNAs for the diagnosis of prostate cancer. Sci Rep 2018; 8(1): 6653.
[http://dx.doi.org/10.1038/s41598-018-24424-w] [PMID: 29703916]
[23]
Wu T, Chen Y, Du Y, et al. Circulating exosomal miR-92b-5p is a promising diagnostic biomarker of heart failure with reduced ejection fraction patients hospitalized for acute heart failure. J Thorac Dis 2018; 10(11): 6211-20.
[http://dx.doi.org/10.21037/jtd.2018.10.52] [PMID: 30622793]
[24]
Zhang L, Wu ZA. MicroRNA-378a-3p downregulation as a novel biomarker with poor clinical outcomes in cervical cancer. BES 2021; 34(3): 213-21.
[PMID: 33766217]
[25]
Hara N, Kikuchi M, Miyashita A, et al. Serum microRNA miR-501-3p as a potential biomarker related to the progression of Alzheimer’s disease. Acta Neuropathol Commun 2017; 5(1): 10.
[http://dx.doi.org/10.1186/s40478-017-0414-z] [PMID: 28137310]
[26]
Uhlmann S, Mannsperger H, Zhang JD, et al. Global microRNA level regulation of EGFR‐driven cell‐cycle protein network in breast cancer. Mol Syst Biol 2012; 8(1): 570.
[http://dx.doi.org/10.1038/msb.2011.100] [PMID: 22333974]
[27]
Gu S, Jin L, Zhang F, Sarnow P, Kay MA. Biological basis for restriction of microRNA targets to the 3′ untranslated region in mammalian mRNAs. Nat Struct Mol Biol 2009; 16(2): 144-50.
[http://dx.doi.org/10.1038/nsmb.1552] [PMID: 19182800]
[28]
Ha M, Kim VN. Regulation of microRNA biogenesis. Nat Rev Mol Cell Biol 2014; 15(8): 509-24.
[http://dx.doi.org/10.1038/nrm3838] [PMID: 25027649]
[29]
Plotnikova O, Baranova A, Skoblov M. Comprehensive analysis of human microRNA-mRNA interactome. Front Genet 2019; 10: 933.
[http://dx.doi.org/10.3389/fgene.2019.00933] [PMID: 31649721]
[30]
Nguyen TA, Jo MH, Choi YG, et al. Functional anatomy of the human microprocessor. Cell 2015; 161(6): 1374-87.
[http://dx.doi.org/10.1016/j.cell.2015.05.010] [PMID: 26027739]
[31]
Partin AC, Ngo TD, Herrell E, Jeong BC, Hon G, Nam Y. Publisher Correction: Heme enables proper positioning of Drosha and DGCR8 on primary microRNAs. Nat Commun 2018; 9(1): 3852.
[http://dx.doi.org/10.1038/s41467-018-06426-4] [PMID: 30228298]
[32]
Helwak A, Kudla G, Dudnakova T, Tollervey D. Mapping the human miRNA interactome by CLASH reveals frequent noncanonical binding. Cell 2013; 153(3): 654-65.
[http://dx.doi.org/10.1016/j.cell.2013.03.043] [PMID: 23622248]
[33]
Moore MJ, Scheel TKH, Luna JM, et al. miRNA-target chimeras reveal miRNA 3′-end pairing as a major determinant of Argonaute target specificity. Nat Commun 2015; 6(1): 8864.
[http://dx.doi.org/10.1038/ncomms9864] [PMID: 26602609]
[34]
Denli AM, Tops BBJ, Plasterk RHA, Ketting RF, Hannon GJ. Processing of primary microRNAs by the microprocessor complex. Nature 2004; 432(7014): 231-5.
[http://dx.doi.org/10.1038/nature03049] [PMID: 15531879]
[35]
Zeng Y, Yi R, Cullen BR. Recognition and cleavage of primary microRNA precursors by the nuclear processing enzyme Drosha. EMBO J 2005; 24(1): 138-48.
[http://dx.doi.org/10.1038/sj.emboj.7600491] [PMID: 15565168]
[36]
Okada C, Yamashita E, Lee SJ, et al. A high-resolution structure of the pre-microRNA nuclear export machinery. Science 2009; 326(5957): 1275-9.
[http://dx.doi.org/10.1126/science.1178705] [PMID: 19965479]
[37]
Zhang H, Kolb FA, Jaskiewicz L, Westhof E, Filipowicz W. Single processing center models for human Dicer and bacterial RNase III. Cell 2004; 118(1): 57-68.
[http://dx.doi.org/10.1016/j.cell.2004.06.017] [PMID: 15242644]
[38]
Lai EC. Micro RNAs are complementary to 3′ UTR sequence motifs that mediate negative post-transcriptional regulation. Nat Genet 2002; 30(4): 363-4.
[http://dx.doi.org/10.1038/ng865] [PMID: 11896390]
[39]
Doench JG, Sharp PA. Specificity of microRNA target selection in translational repression. Genes Dev 2004; 18(5): 504-11.
[http://dx.doi.org/10.1101/gad.1184404] [PMID: 15014042]
[40]
Filipowicz W, Bhattacharyya SN, Sonenberg N. Mechanisms of post-transcriptional regulation by microRNAs: Are the answers in sight? Nat Rev Genet 2008; 9(2): 102-14.
[http://dx.doi.org/10.1038/nrg2290] [PMID: 18197166]
[41]
Bartel DP. MicroRNAs: Target recognition and regulatory functions. Cell 2009; 136(2): 215-33.
[http://dx.doi.org/10.1016/j.cell.2009.01.002] [PMID: 19167326]
[42]
Yang X, Du WW, Li H, et al. Both mature miR-17-5p and passenger strand miR-17-3p target TIMP3 and induce prostate tumor growth and invasion. Nucleic Acids Res 2013; 41(21): 9688-704.
[http://dx.doi.org/10.1093/nar/gkt680] [PMID: 23990326]
[43]
Shan SW, Fang L, Shatseva T, et al. Mature MiR-17-5p and passenger miR-17-3p induce hepatocellular carcinoma by targeting PTEN, GalNT7, and vimentin in different signal pathways. J Cell Sci 2013; 126(Pt 6): jcs.122895.
[http://dx.doi.org/10.1242/jcs.122895] [PMID: 23418359]
[44]
Yamada Y, Koshizuka K, Hanazawa T, et al. Passenger strand of miR-145-3p acts as a tumor-suppressor by targeting MYO1B in head and neck squamous cell carcinoma. Int J Oncol 2018; 52(1): 166-78.
[PMID: 29115582]
[45]
Yao P, Wu J, Lindner D, Fox PL. Interplay between miR-574-3p and hnRNP L regulates VEGFA mRNA translation and tumorigenesis. Nucleic Acids Res 2017; 45(13): 7950-64.
[http://dx.doi.org/10.1093/nar/gkx440] [PMID: 28520992]
[46]
Wu J, Venkata Subbaiah KC, Jiang F, et al. MicroRNA‐574 regulates FAM210A expression and influences pathological cardiac remodeling. EMBO Mol Med 2021; 13(2): e12710.
[http://dx.doi.org/10.15252/emmm.202012710] [PMID: 33369227]
[47]
Yuan K, Xie K, Fox J, et al. Decreased levels of miR-224 and the passenger strand of miR-221 increase MBD2, suppressing maspin and promoting colorectal tumor growth and metastasis in mice. Gastroenterology 2013; 145(4): 853-864.e9.
[http://dx.doi.org/10.1053/j.gastro.2013.06.008] [PMID: 23770133]
[48]
Cheloufi S, Dos Santos CO, Chong MMW, Hannon GJ. A dicer-independent miRNA biogenesis pathway that requires Ago catalysis. Nature 2010; 465(7298): 584-9.
[http://dx.doi.org/10.1038/nature09092] [PMID: 20424607]
[49]
Yang JS, Maurin T, Robine N, et al. Conserved vertebrate mir-451 provides a platform for Dicer-independent, Ago2-mediated microRNA biogenesis. Proc Natl Acad Sci 2010; 107(34): 15163-8.
[http://dx.doi.org/10.1073/pnas.1006432107] [PMID: 20699384]
[50]
Yoda M, Cifuentes D, Izumi N, et al. Poly(A)-specific ribonuclease mediates 3′-end trimming of Argonaute2-cleaved precursor microRNAs. Cell Rep 2013; 5(3): 715-26.
[http://dx.doi.org/10.1016/j.celrep.2013.09.029] [PMID: 24209750]
[51]
Frank F, Sonenberg N, Nagar B. Structural basis for 5′-nucleotide base-specific recognition of guide RNA by human AGO2. Nature 2010; 465(7299): 818-22.
[http://dx.doi.org/10.1038/nature09039] [PMID: 20505670]
[52]
Yi T, Arthanari H, Akabayov B, et al. eIF1A augments Ago2-mediated Dicer-independent miRNA biogenesis and RNA interference. Nat Commun 2015; 6(1): 7194.
[http://dx.doi.org/10.1038/ncomms8194] [PMID: 26018492]
[53]
Ruby JG, Jan CH, Bartel DP. Intronic microRNA precursors that bypass Drosha processing. Nature 2007; 448(7149): 83-6.
[http://dx.doi.org/10.1038/nature05983] [PMID: 17589500]
[54]
Okamura K, Hagen JW, Duan H, Tyler DM, Lai EC. The mirtron pathway generates microRNA-class regulatory RNAs in Drosophila. Cell 2007; 130(1): 89-100.
[http://dx.doi.org/10.1016/j.cell.2007.06.028] [PMID: 17599402]
[55]
Ender C, Krek A, Friedländer MR, et al. A human snoRNA with microRNA-like functions. Mol Cell 2008; 32(4): 519-28.
[http://dx.doi.org/10.1016/j.molcel.2008.10.017] [PMID: 19026782]
[56]
Xie M, Li M, Vilborg A, et al. Mammalian 5′-capped microRNA precursors that generate a single microRNA. Cell 2013; 155(7): 1568-80.
[http://dx.doi.org/10.1016/j.cell.2013.11.027] [PMID: 24360278]
[57]
Wang X. Composition of seed sequence is a major determinant of microRNA targeting patterns. Bioinformatics 2014; 30(10): 1377-83.
[http://dx.doi.org/10.1093/bioinformatics/btu045] [PMID: 24470575]
[58]
Akhtar MM, Micolucci L, Islam MS, Olivieri F, Procopio AD. A practical guide to miRNA target prediction. Methods Mol Biol 2019; 1970: 1-13.
[http://dx.doi.org/10.1007/978-1-4939-9207-2_1] [PMID: 30963484]
[59]
Lekprasert P, Mayhew M, Ohler U. Assessing the utility of thermodynamic features for microRNA target prediction under relaxed seed and no conservation requirements. PLoS One 2011; 6(6): e20622.
[http://dx.doi.org/10.1371/journal.pone.0020622] [PMID: 21674004]
[60]
Riolo G, Cantara S, Marzocchi C, Ricci C. miRNA targets: From prediction tools to experimental validation. Methods Protoc 2020; 4(1): 1.
[http://dx.doi.org/10.3390/mps4010001] [PMID: 33374478]
[61]
Kobayashi H, Tomari Y. RISC assembly: Coordination between small RNAs and Argonaute proteins. Biochim Biophys Acta Gene Regul Mech 2016; 1859(1): 71-81.
[http://dx.doi.org/10.1016/j.bbagrm.2015.08.007] [PMID: 26303205]
[62]
Marín RM, Vaníček J. Efficient use of accessibility in microRNA target prediction. Nucleic Acids Res 2011; 39(1): 19-29.
[http://dx.doi.org/10.1093/nar/gkq768] [PMID: 20805242]
[63]
Bertolazzi G, Benos PV, Tumminello M, Coronnello C. An improvement of ComiR algorithm for microRNA target prediction by exploiting coding region sequences of mRNAs. BMC Bioinformatics 2020; 21(S8): 201.
[http://dx.doi.org/10.1186/s12859-020-3519-5] [PMID: 32938407]
[64]
Steinkraus BR, Toegel M, Fulga TA. Tiny giants of gene regulation: Experimental strategies for microRNA functional studies. Wiley Interdiscip Rev Dev Biol 2016; 5(3): 311-62.
[http://dx.doi.org/10.1002/wdev.223] [PMID: 26950183]
[65]
Ule J, Jensen K, Mele A, Darnell RB. CLIP: A method for identifying protein-RNA interaction sites in living cells. Methods 2005; 37(4): 376-86.
[http://dx.doi.org/10.1016/j.ymeth.2005.07.018] [PMID: 16314267]
[66]
Toscano-Garibay JD, Aquino-Jarquin G. Transcriptional regulation mechanism mediated by miRNA-DNA•DNA triplex structure stabilized by Argonaute. Biochim Biophys Acta Gene Regul Mech 2014; 1839(11): 1079-83.
[http://dx.doi.org/10.1016/j.bbagrm.2014.07.016] [PMID: 25086339]
[67]
Paugh SW, Coss DR, Bao J, et al. MicroRNAs form triplexes with double stranded DNA at sequence-specific binding sites; a eukaryotic mechanism via which micrornas could directly alter gene expression. PLOS Comput Biol 2016; 12(2): e1004744.
[http://dx.doi.org/10.1371/journal.pcbi.1004744] [PMID: 26844769]
[68]
Liu H, Lei C, He Q, Pan Z, Xiao D, Tao Y. Nuclear functions of mammalian MicroRNAs in gene regulation, immunity and cancer. Mol Cancer 2018; 17(1): 64.
[http://dx.doi.org/10.1186/s12943-018-0765-5] [PMID: 29471827]
[69]
Portnoy V, Lin SHS, Li KH, et al. saRNA-guided Ago2 targets the RITA complex to promoters to stimulate transcription. Cell Res 2016; 26(3): 320-35.
[http://dx.doi.org/10.1038/cr.2016.22] [PMID: 26902284]
[70]
Place RF, Li LC, Pookot D, Noonan EJ, Dahiya R. MicroRNA-373 induces expression of genes with complementary promoter sequences. Proc Natl Acad Sci 2008; 105(5): 1608-13.
[http://dx.doi.org/10.1073/pnas.0707594105] [PMID: 18227514]
[71]
Zhang Y, Fan M, Zhang X, et al. Cellular microRNAs up-regulate transcription via interaction with promoter TATA-box motifs. RNA 2014; 20(12): 1878-89.
[http://dx.doi.org/10.1261/rna.045633.114] [PMID: 25336585]
[72]
Younger ST, Corey DR. Transcriptional gene silencing in mammalian cells by miRNA mimics that target gene promoters. Nucleic Acids Res 2011; 39(13): 5682-91.
[http://dx.doi.org/10.1093/nar/gkr155] [PMID: 21427083]
[73]
Majid S, Dar AA, Saini S, et al. MicroRNA‐205-directed transcriptional activation of tumor suppressor genes in prostate cancer. Cancer 2010; 116(24): 5637-49.
[http://dx.doi.org/10.1002/cncr.25488] [PMID: 20737563]
[74]
Li S, Wang C, Yu X, et al. miR-3619-5p inhibits prostate cancer cell growth by activating CDKN1A expression. Oncol Rep 2017; 37(1): 241-8.
[http://dx.doi.org/10.3892/or.2016.5250] [PMID: 27878260]
[75]
Qu H, Zheng L, Pu J, et al. miRNA-558 promotes tumorigenesis and aggressiveness of neuroblastoma cells through activating the transcription of heparanase. Hum Mol Genet 2015; 24(9): 2539-51.
[http://dx.doi.org/10.1093/hmg/ddv018] [PMID: 25616966]
[76]
Xiang X, Mei H, Zhao X, et al. miRNA-337-3p suppresses neuroblastoma progression by repressing the transcription of matrix metalloproteinase 14. Oncotarget 2015; 6(26): 22452-66.
[http://dx.doi.org/10.18632/oncotarget.4311] [PMID: 26084291]
[77]
Arnold PR, Wells AD, Li XC. Diversity and emerging roles of enhancer RNA in regulation of gene expression and cell fate. Front Cell Dev Biol 2020; 7: 377.
[http://dx.doi.org/10.3389/fcell.2019.00377] [PMID: 31993419]
[78]
Zhang T, Zhang Z, Dong Q, Xiong J, Zhu B. Histone H3K27 acetylation is dispensable for enhancer activity in mouse embryonic stem cells. Genome Biol 2020; 21(1): 45.
[http://dx.doi.org/10.1186/s13059-020-01957-w] [PMID: 32085783]
[79]
Stavast C, Erkeland S. The non-canonical aspects of MicroRNAs: Many roads to gene regulation. Cells 2019; 8(11): 1465.
[http://dx.doi.org/10.3390/cells8111465] [PMID: 31752361]
[80]
Xiao M, Li J, Li W, et al. MicroRNAs activate gene transcription epigenetically as an enhancer trigger. RNA Biol 2017; 14(10): 1326-34.
[http://dx.doi.org/10.1080/15476286.2015.1112487] [PMID: 26853707]
[81]
Xiong D, Wang Y, You M. Tumor intrinsic immunity related proteins may be novel tumor suppressors in some types of cancer. Sci Rep 2019; 9(1): 10918.
[http://dx.doi.org/10.1038/s41598-019-47382-3] [PMID: 31358815]
[82]
Tang F, Zhang Y, Huang QQ, et al. Genome-wide identification and analysis of enhancer-regulated microRNAs across 31 human cancers. Front Genet 2020; 11: 644.
[http://dx.doi.org/10.3389/fgene.2020.00644] [PMID: 32714372]
[83]
Weintraub AS, Li CH, Zamudio AV, et al. YY1 is a structural regulator of enhancer-promoter loops. Cell 2017; 171(7): 1573-1588.e28.
[http://dx.doi.org/10.1016/j.cell.2017.11.008] [PMID: 29224777]
[84]
Yun MR, Lim SM, Kim SK, et al. Enhancer remodeling and MicroRNA alterations are associated with acquired resistance to ALK inhibitors. Cancer Res 2018; 78(12): 3350-62.
[http://dx.doi.org/10.1158/0008-5472.CAN-17-3146] [PMID: 29669761]
[85]
Suzuki HI, Young RA, Sharp PA. Super-enhancer-mediated RNA processing revealed by integrative MicroRNA network analysis. Cell 2017; 168(6): 1000-1014.e15.
[http://dx.doi.org/10.1016/j.cell.2017.02.015] [PMID: 28283057]
[86]
Lin L, Gerth AJ, Peng SL. Active inhibition of plasma cell development in resting B cells by microphthalmia-associated transcription factor. J Exp Med 2004; 200(1): 115-22.
[http://dx.doi.org/10.1084/jem.20040612] [PMID: 15226356]
[87]
Porstner M, Winkelmann R, Daum P, et al. miR‐148a promotes plasma cell differentiation and targets the germinal center transcription factors Mitf and Bach2. Eur J Immunol 2015; 45(4): 1206-15.
[http://dx.doi.org/10.1002/eji.201444637] [PMID: 25678371]
[88]
Wang H, Flach H, Onizawa M, Wei L, McManus MT, Weiss A. Negative regulation of Hif1a expression and TH17 differentiation by the hypoxia-regulated microRNA miR-210. Nat Immunol 2014; 15(4): 393-401.
[http://dx.doi.org/10.1038/ni.2846] [PMID: 24608041]
[89]
Wang W, Kwon EJ, Tsai LH. MicroRNAs in learning, memory, and neurological diseases: Figure 1. Learn Mem 2012; 19(9): 359-68.
[http://dx.doi.org/10.1101/lm.026492.112] [PMID: 22904366]
[90]
Kuchen S, Resch W, Yamane A, et al. Regulation of microRNA expression and abundance during lymphopoiesis. Immunity 2010; 32(6): 828-39.
[http://dx.doi.org/10.1016/j.immuni.2010.05.009] [PMID: 20605486]
[91]
Iadevaia V, Caldarola S, Tino E, Amaldi F, Loreni F. All translation elongation factors and the e, f, and h subunits of translation initiation factor 3 are encoded by 5′-terminal oligopyrimidine (TOP) mRNAs. RNA 2008; 14(9): 1730-6.
[http://dx.doi.org/10.1261/rna.1037108] [PMID: 18658124]
[92]
Ørom UA, Nielsen FC, Lund AH. MicroRNA-10a binds the 5'UTR of ribosomal protein mRNAs and enhances their translation. Mol Cell 2008; 30(4): 460-71.
[http://dx.doi.org/10.1016/j.molcel.2008.05.001] [PMID: 18498749]
[93]
Lee I, Ajay SS, Yook JI, et al. New class of microRNA targets containing simultaneous 5′-UTR and 3′-UTR interaction sites. Genome Res 2009; 19(7): 1175-83.
[http://dx.doi.org/10.1101/gr.089367.108] [PMID: 19336450]
[94]
Zhang J, Zhou W, Liu Y, Liu T, Li C, Wang L. Oncogenic role of microRNA-532 5p in human colorectal cancer via targeting of the 5'UTR of RUNX3. Oncol Lett 2018; 15(5): 7215-20.
[http://dx.doi.org/10.3892/ol.2018.8217] [PMID: 29849790]
[95]
Liu M, Roth A, Yu M, et al. The IGF2 intronic miR-483 selectively enhances transcription from IGF2 fetal promoters and enhances tumorigenesis. Genes Dev 2013; 27(23): 2543-8.
[http://dx.doi.org/10.1101/gad.224170.113] [PMID: 24298054]
[96]
Chang J, Nicolas E, Marks D, et al. miR-122, a mammalian liver-specific microRNA, is processed from hcr mRNA and may downregulate the high affinity cationic amino acid transporter CAT-1. RNA Biol 2004; 1(2): 106-13.
[http://dx.doi.org/10.4161/rna.1.2.1066] [PMID: 17179747]
[97]
Jopling CL, Yi M, Lancaster AM, Lemon SM, Sarnow P. Modulation of hepatitis C virus RNA abundance by a liver-specific MicroRNA. Science 2005; 309(5740): 1577-81.
[http://dx.doi.org/10.1126/science.1113329] [PMID: 16141076]
[98]
Hausser J, Syed AP, Bilen B, Zavolan M. Analysis of CDS-located miRNA target sites suggests that they can effectively inhibit translation. Genome Res 2013; 23(4): 604-15.
[http://dx.doi.org/10.1101/gr.139758.112] [PMID: 23335364]
[99]
Kozar I, Philippidou D, Margue C, Gay LA, Renne R, Kreis S. Crosslinking ligation and sequencing of hybrids (qCLASH) reveals an unpredicted mirna targetome in melanoma cells. Cancers 2021; 13(5): 1096.
[http://dx.doi.org/10.3390/cancers13051096] [PMID: 33806450]
[100]
Tay Y, Zhang J, Thomson AM, Lim B, Rigoutsos I. MicroRNAs to Nanog, Oct4 and Sox2 coding regions modulate embryonic stem cell differentiation. Nature 2008; 455(7216): 1124-8.
[http://dx.doi.org/10.1038/nature07299] [PMID: 18806776]
[101]
Elcheva I, Goswami S, Noubissi FK, Spiegelman VS. CRD-BP protects the coding region of betaTrCP1 mRNA from miR-183-mediated degradation. Mol Cell 2009; 35(2): 240-6.
[http://dx.doi.org/10.1016/j.molcel.2009.06.007] [PMID: 19647520]
[102]
Friedrich M, Vaxevanis CK, Biehl K, Mueller A, Seliger B. Targeting the coding sequence: opposing roles in regulating classical and non-classical MHC class I molecules by miR-16 and miR-744. J Immunother Cancer 2020; 8(1): e000396.
[http://dx.doi.org/10.1136/jitc-2019-000396] [PMID: 32571994]
[103]
Xun Y, Tang Y, Hu L, et al. Purification and identification of miRNA target sites in genome using DNA affinity precipitation. Front Genet 2019; 10: 778.
[http://dx.doi.org/10.3389/fgene.2019.00778] [PMID: 31572429]
[104]
Meng Y, Shao C, Ma X, Wang H. Introns targeted by plant microRNAs: A possible novel mechanism of gene regulation. Rice 2013; 6(1): 8.
[http://dx.doi.org/10.1186/1939-8433-6-8] [PMID: 24280590]
[105]
Li S, Xu Z, Sheng J. tRNA-derived small RNA: A novel regulatory small non-coding RNA. Genes 2018; 9(5): 246.
[http://dx.doi.org/10.3390/genes9050246] [PMID: 29748504]
[106]
Gagnon KT, Li L, Chu Y, Janowski BA, Corey DR. RNAi factors are present and active in human cell nuclei. Cell Rep 2014; 6(1): 211-21.
[http://dx.doi.org/10.1016/j.celrep.2013.12.013] [PMID: 24388755]
[107]
Bansal P, Christopher AF, Kaur R, Kaur G, Kaur A, Gupta V. MicroRNA therapeutics: Discovering novel targets and developing specific therapy. Perspect Clin Res 2016; 7(2): 68-74.
[http://dx.doi.org/10.4103/2229-3485.179431] [PMID: 27141472]

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