Skip to main content

Advertisement

Log in

Regulatory network of miRNA on its target: coordination between transcriptional and post-transcriptional regulation of gene expression

  • Review
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

MicroRNAs (miRNAs) are a class of endogenous small noncoding RNAs that participate in a majority of biological processes via regulating target gene expression. The post-transcriptional repression through miRNA seed region binding to 3′ UTR of target mRNA is considered as the canonical mode of miRNA-mediated gene regulation. However, emerging evidence suggests that other regulatory modes exist beyond the canonical mechanism. In particular, the function of intranuclear miRNA in gene transcriptional regulation is gradually revealed, with evidence showing their contribution to gene silencing or activating. Therefore, miRNA-mediated regulation of gene transcription not only expands our understanding of the molecular mechanism underlying miRNA regulatory function, but also provides new evidence to explain its ability in the sophisticated regulation of many bioprocesses. In this review, mechanisms of miRNA-mediated gene transcriptional and post-transcriptional regulation are summarized, and the synergistic effects among these actions which form a regulatory network of a miRNA on its target are particularly elaborated. With these discussions, we aim to emphasize the importance of miRNA regulatory network on target gene regulation and further highlight the potential application of the network mode in the achievement of a more effective and stable modulation of the target gene expression.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

AGO:

Argonaute proteins

ASO:

Antisense oligonucleotides

CYP2E1:

Cytochrome P450 (CYP) 2E1

DGCR8:

DiGeorge syndrome chromosomal [or critical] region 8

DOX:

Doxorubicin

HCV:

Hepatitis C virus

IPO8:

Importin 8

miRISC:

MicroRNA-induced silencing complex

miRNA:

MicroRNA

nt:

Nucleotides

NPC:

Nuclear pore complex

snoRNA:

Small nucleolar RNA

SMARCE1:

SWI/SNF-related matrix-associated actin-dependent regulator of chromatin subfamily E member 1

PTGS:

Post-transcriptional gene silencing

pre-miRNAs:

Precursor miRNAs

P-body:

Processing body

Pol II:

Polymerase II

RNAi:

RNA silencing

TRBP:

Transactivation-responsive RNA-binding protein

TGS:

Transcriptional gene silencing

TGA:

Transcriptional gene activating

trnc6a:

Trinucleotide repeat-containing gene 6A

UTR:

Untranslated region

XPO5:

Exportin-5

References

  1. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116(2):281–297

    Article  CAS  PubMed  Google Scholar 

  2. Lee Y, Kim M, Han J, Yeom KH, Lee S, Baek SH, Kim VN (2004) MicroRNA genes are transcribed by RNA polymerase II. EMBO J 23(20):4051–4060. https://doi.org/10.1038/sj.emboj.7600385

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Lee Y, Ahn C, Han J, Choi H, Kim J, Yim J, Lee J, Provost P, Radmark O, Kim S, Kim VN (2003) The nuclear RNase III Drosha initiates microRNA processing. Nature 425(6956):415–419. https://doi.org/10.1038/nature01957

    Article  CAS  PubMed  Google Scholar 

  4. Carmell MA, Hannon GJ (2004) RNase III enzymes and the initiation of gene silencing. Nat Struct Mol Biol 11(3):214–218. https://doi.org/10.1038/nsmb729

    Article  CAS  PubMed  Google Scholar 

  5. Gregory RI, Yan KP, Amuthan G, Chendrimada T, Doratotaj B, Cooch N, Shiekhattar R (2004) The microprocessor complex mediates the genesis of microRNAs. Nature 432(7014):235–240. https://doi.org/10.1038/nature03120

    Article  CAS  PubMed  Google Scholar 

  6. Yi R, Qin Y, Macara IG, Cullen BR (2003) Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev 17(24):3011–3016. https://doi.org/10.1101/gad.1158803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Lund E, Guttinger S, Calado A, Dahlberg JE, Kutay U (2004) Nuclear export of microRNA precursors. Science 303(5654):95–98. https://doi.org/10.1126/science.1090599

    Article  CAS  PubMed  Google Scholar 

  8. Katahira J, Yoneda Y (2011) Nucleocytoplasmic transport of microRNAs and related small RNAs. Traffic 12(11):1468–1474. https://doi.org/10.1111/j.1600-0854.2011.01211.x

    Article  CAS  PubMed  Google Scholar 

  9. Bernstein E, Caudy AA, Hammond SM, Hannon GJ (2001) Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409(6818):363–366. https://doi.org/10.1038/35053110

    Article  CAS  PubMed  Google Scholar 

  10. Khvorova A, Reynolds A, Jayasena SD (2003) Functional siRNAs and miRNAs exhibit strand bias. Cell 115(2):209–216

    Article  CAS  PubMed  Google Scholar 

  11. Chendrimada TP, Gregory RI, Kumaraswamy E, Norman J, Cooch N, Nishikura K, Shiekhattar R (2005) TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing. Nature 436(7051):740–744. https://doi.org/10.1038/nature03868

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Ameres SL, Zamore PD (2013) Diversifying microRNA sequence and function. Nat Rev Mol Cell Biol 14(8):475–488. https://doi.org/10.1038/nrm3611

    Article  CAS  PubMed  Google Scholar 

  13. Lewis BP, Shih IH, Jones-Rhoades MW, Bartel DP, Burge CB (2003) Prediction of mammalian microRNA targets. Cell 115(7):787–798

    Article  CAS  PubMed  Google Scholar 

  14. Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136(2):215–233. https://doi.org/10.1016/j.cell.2009.01.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. van den Berg A, Mols J, Han J (2008) RISC-target interaction: cleavage and translational suppression. Biochim Biophys Acta 1779(11):668–677. https://doi.org/10.1016/j.bbagrm.2008.07.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Kim DH, Saetrom P, Snove O Jr, Rossi JJ (2008) MicroRNA-directed transcriptional gene silencing in mammalian cells. Proc Natl Acad Sci USA 105(42):16230–16235. https://doi.org/10.1073/pnas.0808830105

    Article  PubMed  PubMed Central  Google Scholar 

  17. Tan Y, Zhang B, Wu T, Skogerbo G, Zhu X, Guo X, He S, Chen R (2009) Transcriptional inhibiton of Hoxd4 expression by miRNA-10a in human breast cancer cells. BMC Mol Biol 10:12. https://doi.org/10.1186/1471-2199-10-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Younger ST, Corey DR (2011) Transcriptional gene silencing in mammalian cells by miRNA mimics that target gene promoters. Nucleic Acids Res 39(13):5682–5691. https://doi.org/10.1093/nar/gkr155

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Adilakshmi T, Sudol I, Tapinos N (2012) Combinatorial action of miRNAs regulates transcriptional and post-transcriptional gene silencing following in vivo PNS injury. PLoS One 7(7):e39674. https://doi.org/10.1371/journal.pone.0039674

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Benhamed M, Herbig U, Ye T, Dejean A, Bischof O (2012) Senescence is an endogenous trigger for microRNA-directed transcriptional gene silencing in human cells. Nat Cell Biol 14(3):266–275. https://doi.org/10.1038/ncb2443

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Zardo G, Ciolfi A, Vian L, Starnes LM, Billi M, Racanicchi S, Maresca C, Fazi F, Travaglini L, Noguera N, Mancini M, Nanni M, Cimino G, Lo-Coco F, Grignani F, Nervi C (2012) Polycombs and microRNA-223 regulate human granulopoiesis by transcriptional control of target gene expression. Blood 119(17):4034–4046. https://doi.org/10.1182/blood-2011-08-371344

    Article  CAS  PubMed  Google Scholar 

  22. Roberts TC (2014) The MicroRNA biology of the mammalian nucleus. Mol Ther Nucleic Acids 3:e188. https://doi.org/10.1038/mtna.2014.40

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Miao L, Yao H, Li C, Pu M, Yao X, Yang H, Qi X, Ren J, Wang Y (2016) A dual inhibition: microRNA-552 suppresses both transcription and translation of cytochrome P450 2E1. Biochim Biophys Acta 1859(4):650–662. https://doi.org/10.1016/j.bbagrm.2016.02.016

    Article  CAS  PubMed  Google Scholar 

  24. Friedman RC, Farh KK, Burge CB, Bartel DP (2009) Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19(1):92–105. https://doi.org/10.1101/gr.082701.108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Seok H, Ham J, Jang ES, Chi SW (2016) MicroRNA target recognition: insights from transcriptome-wide non-canonical interactions. Mol Cells 39(5):375–381. https://doi.org/10.14348/molcells.2016.0013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Pu M, Li C, Qi X, Chen J, Wang Y, Gao L, Miao L, Ren J (2017) MiR-1254 suppresses HO-1 expression through seed region-dependent silencing and non-seed interaction with TFAP2A transcript to attenuate NSCLC growth. PLoS Genet 13(7):e1006896. https://doi.org/10.1371/journal.pgen.1006896

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Grimson A, Farh KK, Johnston WK, Garrett-Engele P, Lim LP, Bartel DP (2007) MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol Cell 27(1):91–105. https://doi.org/10.1016/j.molcel.2007.06.017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Gibbings DJ, Ciaudo C, Erhardt M, Voinnet O (2009) Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat Cell Biol 11(9):1143–1149. https://doi.org/10.1038/ncb1929

    Article  CAS  PubMed  Google Scholar 

  29. Sripada L, Tomar D, Prajapati P, Singh R, Singh AK, Singh R (2012) Systematic analysis of small RNAs associated with human mitochondria by deep sequencing: detailed analysis of mitochondrial associated miRNA. PLoS One 7(9):e44873. https://doi.org/10.1371/journal.pone.0044873

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Zhang X, Zuo X, Yang B, Li Z, Xue Y, Zhou Y, Huang J, Zhao X, Zhou J, Yan Y, Zhang H, Guo P, Sun H, Guo L, Zhang Y, Fu XD (2014) MicroRNA directly enhances mitochondrial translation during muscle differentiation. Cell 158(3):607–619. https://doi.org/10.1016/j.cell.2014.05.047

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Leung AKL (2015) The whereabouts of microRNA actions: cytoplasm and beyond. Trends Cell Biol 25(10):601–610. https://doi.org/10.1016/j.tcb.2015.07.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Meister G, Landthaler M, Patkaniowska A, Dorsett Y, Teng G, Tuschl T (2004) Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol Cell 15(2):185–197. https://doi.org/10.1016/j.molcel.2004.07.007

    Article  CAS  PubMed  Google Scholar 

  33. Hwang HW, Wentzel EA, Mendell JT (2007) A hexanucleotide element directs microRNA nuclear import. Science 315(5808):97–100. https://doi.org/10.1126/science.1136235

    Article  CAS  PubMed  Google Scholar 

  34. Gagnon KT, Li L, Chu Y, Janowski BA, Corey DR (2014) RNAi factors are present and active in human cell nuclei. Cell Rep 6(1):211–221. https://doi.org/10.1016/j.celrep.2013.12.013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Daneholt B (1997) A look at messenger RNP moving through the nuclear pore. Cell 88(5):585–588

    Article  CAS  PubMed  Google Scholar 

  36. Wei Y, Li L, Wang D, Zhang CY, Zen K (2014) Importin 8 regulates the transport of mature microRNAs into the cell nucleus. J Biol Chem 289(15):10270–10275. https://doi.org/10.1074/jbc.C113.541417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Jeffries CD, Fried HM, Perkins DO (2011) Nuclear and cytoplasmic localization of neural stem cell microRNAs. RNA 17(4):675–686. https://doi.org/10.1261/rna.2006511

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Brameier M, Herwig A, Reinhardt R, Walter L, Gruber J (2011) Human box C/D snoRNAs with miRNA like functions: expanding the range of regulatory RNAs. Nucleic Acids Res 39(2):675–686. https://doi.org/10.1093/nar/gkq776

    Article  CAS  PubMed  Google Scholar 

  39. Politz JC, Hogan EM, Pederson T (2009) MicroRNAs with a nucleolar location. RNA 15(9):1705–1715. https://doi.org/10.1261/rna.1470409

    Article  CAS  PubMed  Google Scholar 

  40. Pitchiaya S, Heinicke LA, Park JI, Cameron EL, Walter NG (2017) Resolving subcellular miRNA trafficking and turnover at single-molecule resolution. Cell Rep 19(3):630–642. https://doi.org/10.1016/j.celrep.2017.03.075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Xiao M, Li J, Li W, Wang Y, Wu F, Xi Y, Zhang L, Ding C, Luo H, Li Y, Peng L, Zhao L, Peng S, Xiao Y, Dong S, Cao J, Yu W (2017) MicroRNAs activate gene transcription epigenetically as an enhancer trigger. RNA Biol 14(10):1326–1334. https://doi.org/10.1080/15476286.2015.1112487

    Article  PubMed  Google Scholar 

  42. Gonzalez S, Pisano DG, Serrano M (2008) Mechanistic principles of chromatin remodeling guided by siRNAs and miRNAs. Cell Cycle 7(16):2601–2608. https://doi.org/10.4161/cc.7.16.6541

    Article  CAS  PubMed  Google Scholar 

  43. Younger ST, Corey DR (2011) Transcriptional regulation by miRNA mimics that target sequences downstream of gene termini. Mol BioSyst 7(8):2383–2388. https://doi.org/10.1039/c1mb05090g

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Catalanotto C, Cogoni C, Zardo G (2016) MicroRNA in control of gene expression: an overview of nuclear functions. Int J Mol Sci 17(10):1712. https://doi.org/10.3390/ijms17101712

    Article  CAS  PubMed Central  Google Scholar 

  45. Leucci E, Patella F, Waage J, Holmstrom K, Lindow M, Porse B, Kauppinen S, Lund AH (2013) microRNA-9 targets the long non-coding RNA MALAT1 for degradation in the nucleus. Sci Rep 3:2535. https://doi.org/10.1038/srep02535

    Article  PubMed  PubMed Central  Google Scholar 

  46. Tang R, Li L, Zhu D, Hou D, Cao T, Gu H, Zhang J, Chen J, Zhang CY, Zen K (2012) Mouse miRNA-709 directly regulates miRNA-15a/16-1 biogenesis at the posttranscriptional level in the nucleus: evidence for a microRNA hierarchy system. Cell Res 22(3):504–515. https://doi.org/10.1038/cr.2011.137

    Article  CAS  PubMed  Google Scholar 

  47. Place RF, Li LC, Pookot D, Noonan EJ, Dahiya R (2008) MicroRNA-373 induces expression of genes with complementary promoter sequences. Proc Natl Acad Sci USA 105(5):1608–1613. https://doi.org/10.1073/pnas.0707594105

    Article  PubMed  PubMed Central  Google Scholar 

  48. Huang V, Place RF, Portnoy V, Wang J, Qi Z, Jia Z, Yu A, Shuman M, Yu J, Li LC (2012) Upregulation of Cyclin B1 by miRNA and its implications in cancer. Nucleic Acids Res 40(4):1695–1707. https://doi.org/10.1093/nar/gkr934

    Article  CAS  PubMed  Google Scholar 

  49. Williams T, Fried M (1986) A mouse locus at which transcription from both DNA strands produces mRNAs complementary at their 3′ ends. Nature 322(6076):275–279. https://doi.org/10.1038/322275a0

    Article  CAS  PubMed  Google Scholar 

  50. Katayama S, Tomaru Y, Kasukawa T, Waki K, Nakanishi M, Nakamura M, Nishida H, Yap CC, Suzuki M, Kawai J, Suzuki H, Carninci P, Hayashizaki Y, Wells C, Frith M, Ravasi T, Pang KC, Hallinan J, Mattick J, Hume DA, Lipovich L, Batalov S, Engstrom PG, Mizuno Y, Faghihi MA, Sandelin A, Chalk AM, Mottagui-Tabar S, Liang Z, Lenhard B, Wahlestedt C, Group RGER, Genome Science G, Consortium F (2005) Antisense transcription in the mammalian transcriptome. Science 309(5740):1564–1566. https://doi.org/10.1126/science.1112009

    Article  PubMed  Google Scholar 

  51. Carninci P, Kasukawa T, Katayama S, Gough J, Frith MC, Maeda N, Oyama R, Ravasi T, Lenhard B, Wells C, Kodzius R, Shimokawa K, Bajic VB, Brenner SE, Batalov S, Forrest AR, Zavolan M, Davis MJ, Wilming LG, Aidinis V, Allen JE, Ambesi-Impiombato A, Apweiler R, Aturaliya RN, Bailey TL, Bansal M, Baxter L, Beisel KW, Bersano T, Bono H, Chalk AM, Chiu KP, Choudhary V, Christoffels A, Clutterbuck DR, Crowe ML, Dalla E, Dalrymple BP, de Bono B, Della Gatta G, di Bernardo D, Down T, Engstrom P, Fagiolini M, Faulkner G, Fletcher CF, Fukushima T, Furuno M, Futaki S, Gariboldi M, Georgii-Hemming P, Gingeras TR, Gojobori T, Green RE, Gustincich S, Harbers M, Hayashi Y, Hensch TK, Hirokawa N, Hill D, Huminiecki L, Iacono M, Ikeo K, Iwama A, Ishikawa T, Jakt M, Kanapin A, Katoh M, Kawasawa Y, Kelso J, Kitamura H, Kitano H, Kollias G, Krishnan SP, Kruger A, Kummerfeld SK, Kurochkin IV, Lareau LF, Lazarevic D, Lipovich L, Liu J, Liuni S, McWilliam S, Madan Babu M, Madera M, Marchionni L, Matsuda H, Matsuzawa S, Miki H, Mignone F, Miyake S, Morris K, Mottagui-Tabar S, Mulder N, Nakano N, Nakauchi H, Ng P, Nilsson R, Nishiguchi S, Nishikawa S, Nori F, Ohara O, Okazaki Y, Orlando V, Pang KC, Pavan WJ, Pavesi G, Pesole G, Petrovsky N, Piazza S, Reed J, Reid JF, Ring BZ, Ringwald M, Rost B, Ruan Y, Salzberg SL, Sandelin A, Schneider C, Schonbach C, Sekiguchi K, Semple CA, Seno S, Sessa L, Sheng Y, Shibata Y, Shimada H, Shimada K, Silva D, Sinclair B, Sperling S, Stupka E, Sugiura K, Sultana R, Takenaka Y, Taki K, Tammoja K, Tan SL, Tang S, Taylor MS, Tegner J, Teichmann SA, Ueda HR, van Nimwegen E, Verardo R, Wei CL, Yagi K, Yamanishi H, Zabarovsky E, Zhu S, Zimmer A, Hide W, Bult C, Grimmond SM, Teasdale RD, Liu ET, Brusic V, Quackenbush J, Wahlestedt C, Mattick JS, Hume DA, Kai C, Sasaki D, Tomaru Y, Fukuda S, Kanamori-Katayama M, Suzuki M, Aoki J, Arakawa T, Iida J, Imamura K, Itoh M, Kato T, Kawaji H, Kawagashira N, Kawashima T, Kojima M, Kondo S, Konno H, Nakano K, Ninomiya N, Nishio T, Okada M, Plessy C, Shibata K, Shiraki T, Suzuki S, Tagami M, Waki K, Watahiki A, Okamura-Oho Y, Suzuki H, Kawai J, Hayashizaki Y, Consortium F, Group RGER, Genome Science G (2005) The transcriptional landscape of the mammalian genome. Science 309(5740):1559–1563. https://doi.org/10.1126/science.1112014

    Article  CAS  PubMed  Google Scholar 

  52. Schwartz JC, Younger ST, Nguyen NB, Hardy DB, Monia BP, Corey DR, Janowski BA (2008) Antisense transcripts are targets for activating small RNAs. Nat Struct Mol Biol 15(8):842–848. https://doi.org/10.1038/nsmb.1444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Morris KV, Santoso S, Turner AM, Pastori C, Hawkins PG (2008) Bidirectional transcription directs both transcriptional gene activation and suppression in human cells. PLoS Genet 4(11):e1000258. https://doi.org/10.1371/journal.pgen.1000258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Modarresi F, Faghihi MA, Lopez-Toledano MA, Fatemi RP, Magistri M, Brothers SP, van der Brug MP, Wahlestedt C (2012) Inhibition of natural antisense transcripts in vivo results in gene-specific transcriptional upregulation. Nat Biotechnol 30(5):453–459. https://doi.org/10.1038/nbt.2158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Matsui M, Chu Y, Zhang H, Gagnon KT, Shaikh S, Kuchimanchi S, Manoharan M, Corey DR, Janowski BA (2013) Promoter RNA links transcriptional regulation of inflammatory pathway genes. Nucleic Acids Res 41(22):10086–10109. https://doi.org/10.1093/nar/gkt777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Liu M, Roth A, Yu M, Morris R, Bersani F, Rivera MN, Lu J, Shioda T, Vasudevan S, Ramaswamy S, Maheswaran S, Diederichs S, Haber DA (2013) The IGF2 intronic miR-483 selectively enhances transcription from IGF2 fetal promoters and enhances tumorigenesis. Genes Dev 27(23):2543–2548. https://doi.org/10.1101/gad.224170.113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Huang S, Wu S, Ding J, Lin J, Wei L, Gu J, He X (2010) MicroRNA-181a modulates gene expression of zinc finger family members by directly targeting their coding regions. Nucleic Acids Res 38(20):7211–7218. https://doi.org/10.1093/nar/gkq564

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Melton C, Judson RL, Blelloch R (2010) Opposing microRNA families regulate self-renewal in mouse embryonic stem cells. Nature 463(7281):621–626. https://doi.org/10.1038/nature08725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Qin W, Shi Y, Zhao B, Yao C, Jin L, Ma J, Jin Y (2010) miR-24 regulates apoptosis by targeting the open reading frame (ORF) region of FAF1 in cancer cells. PLoS One 5(2):e9429. https://doi.org/10.1371/journal.pone.0009429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. He XH, Zhu W, Yuan P, Jiang S, Li D, Zhang HW, Liu MF (2016) miR-155 downregulates ErbB2 and suppresses ErbB2-induced malignant transformation of breast epithelial cells. Oncogene 35(46):6015–6025. https://doi.org/10.1038/onc.2016.132

    Article  CAS  PubMed  Google Scholar 

  61. Panda AC, Sahu I, Kulkarni SD, Martindale JL, Abdelmohsen K, Vindu A, Joseph J, Gorospe M, Seshadri V (2014) miR-196b-mediated translation regulation of mouse insulin2 via the 5′UTR. PLoS One 9(7):e101084. https://doi.org/10.1371/journal.pone.0101084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Wang S, Pan Y, Zhang R, Xu T, Wu W, Zhang R, Wang C, Huang H, Calin CA, Yang H, Claret FX (2016) Hsa-miR-24-3p increases nasopharyngeal carcinoma radiosensitivity by targeting both the 3′ UTR and 5′ UTR of Jab1/CSN5. Oncogene 35(47):6096–6108. https://doi.org/10.1038/onc.2016.147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Grey F, Tirabassi R, Meyers H, Wu G, McWeeney S, Hook L, Nelson JA (2010) A viral microRNA down-regulates multiple cell cycle genes through mRNA 5′ UTRs. PLoS Pathog 6(6):e1000967. https://doi.org/10.1371/journal.ppat.1000967

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Shimakami T, Yamane D, Jangra RK, Kempf BJ, Spaniel C, Barton DJ, Lemon SM (2012) Stabilization of hepatitis C virus RNA by an Ago2-miR-122 complex. Proc Natl Acad Sci USA 109(3):941–946. https://doi.org/10.1073/pnas.1112263109

    Article  PubMed  PubMed Central  Google Scholar 

  65. Orom UA, Nielsen FC, Lund AH (2008) MicroRNA-10a binds the 5′ UTR of ribosomal protein mRNAs and enhances their translation. Mol Cell 30(4):460–471. https://doi.org/10.1016/j.molcel.2008.05.001

    Article  CAS  PubMed  Google Scholar 

  66. Ackerman WE, Buhimschi IA, Brubaker D, Maxwell S, Rood KM, Chance MR, Jing H, Mesiano S, Buhimschi CS (2018) Integrated microRNA and mRNA network analysis of the human myometrial transcriptome in the transition from quiescence to labor. Biol Reprod 98(6):834–845. https://doi.org/10.1093/biolre/ioy040

    Article  PubMed  PubMed Central  Google Scholar 

  67. M’Baya-Moutoula E, Louvet L, Molinie R, Guerrera IC, Cerutti C, Fourdinier O, Nourry V, Gutierrez L, Morliere P, Mesnard F, Massy ZA, Metzinger-Le Meuth V, Metzinger L (2018) A multi-omics analysis of the regulatory changes induced by miR-223 in a monocyte/macrophage cell line. Biochim Biophys Acta 1864(8):2664–2678. https://doi.org/10.1016/j.bbadis.2018.05.010

    Article  CAS  Google Scholar 

  68. Vella MC, Choi EY, Lin SY, Reinert K, Slack FJ (2004) The C. elegans microRNA let-7 binds to imperfect let-7 complementary sites from the lin-41 3′ UTR. Genes Dev 18(2):132–137. https://doi.org/10.1101/gad.1165404

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Yekta S, Shih IH, Bartel DP (2004) MicroRNA-directed cleavage of HOXB8 mRNA. Science 304(5670):594–596. https://doi.org/10.1126/science.1097434

    Article  CAS  PubMed  Google Scholar 

  70. Brennecke J, Stark A, Russell RB, Cohen SM (2005) Principles of microRNA-target recognition. PLoS Biol 3(3):e85. https://doi.org/10.1371/journal.pbio.0030085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Chi SW, Zang JB, Mele A, Darnell RB (2009) Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature 460(7254):479–486. https://doi.org/10.1038/nature08170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Chi SW, Hannon GJ, Darnell RB (2012) An alternative mode of microRNA target recognition. Nat Struct Mol Biol 19(3):321–327. https://doi.org/10.1038/nsmb.2230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Wang C, Chen Q, Li S, Li S, Zhao Z, Gao H, Wang X, Li B, Zhang W, Yuan Y, Ming L, He H, Tao B, Zhong J (2017) Dual inhibition of PCDH9 expression by miR-215-5p up-regulation in gliomas. Oncotarget 8(6):10287–10297. https://doi.org/10.18632/oncotarget.14396

    Article  PubMed  Google Scholar 

  74. Bracken CP, Scott HS, Goodall GJ (2016) A network-biology perspective of microRNA function and dysfunction in cancer. Nat Rev Genet 17(12):719–732. https://doi.org/10.1038/nrg.2016.134

    Article  CAS  PubMed  Google Scholar 

  75. Zhao Y, Qi X, Chen J, Wei W, Yu C, Yan H, Pu M, Li Y, Miao L, Li C, Ren J (2017) The miR-491-3p/Sp3/ABCB1 axis attenuates multidrug resistance of hepatocellular carcinoma. Cancer Lett 408:102–111. https://doi.org/10.1016/j.canlet.2017.08.027

    Article  CAS  PubMed  Google Scholar 

  76. Sokolova V, Fiorino A, Zoni E, Crippa E, Reid JF, Gariboldi M, Pierotti MA (2015) The effects of miR-20a on p21: two mechanisms blocking growth arrest in TGF-beta-responsive colon carcinoma. J Cell Physiol 230(12):3105–3114. https://doi.org/10.1002/jcp.25051

    Article  CAS  PubMed  Google Scholar 

  77. Zhao Y, Chen J, Wei W, Qi X, Li C, Ren J (2018) The dual-inhibitory effect of miR-338-5p on the multidrug resistance and cell growth of hepatocellular carcinoma. Signal Transduct Target Ther 3:3. https://doi.org/10.1038/s41392-017-0003-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Lee I, Ajay SS, Yook JI, Kim HS, Hong SH, Kim NH, Dhanasekaran SM, Chinnaiyan AM, Athey BD (2009) New class of microRNA targets containing simultaneous 5′-UTR and 3′-UTR interaction sites. Genome Res 19(7):1175–1183. https://doi.org/10.1101/gr.089367.108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Lin CW, Chang YL, Chang YC, Lin JC, Chen CC, Pan SH, Wu CT, Chen HY, Yang SC, Hong TM, Yang PC (2013) MicroRNA-135b promotes lung cancer metastasis by regulating multiple targets in the Hippo pathway and LZTS1. Nat Commun 4:1877. https://doi.org/10.1038/ncomms2876

    Article  CAS  PubMed  Google Scholar 

  80. Zongaro S, Hukema R, D’Antoni S, Davidovic L, Barbry P, Catania MV, Willemsen R, Mari B, Bardoni B (2013) The 3′ UTR of FMR1 mRNA is a target of miR-101, miR-129-5p and miR-221: implications for the molecular pathology of FXTAS at the synapse. Hum Mol Genet 22(10):1971–1982. https://doi.org/10.1093/hmg/ddt044

    Article  CAS  PubMed  Google Scholar 

  81. Lai X, Wolkenhauer O, Vera J (2016) Understanding microRNA-mediated gene regulatory networks through mathematical modelling. Nucleic Acids Res 44(13):6019–6035. https://doi.org/10.1093/nar/gkw550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

No funding was received.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jin Ren.

Ethics declarations

Conflict of interest

The authors have declared that no competing interest exists.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pu, M., Chen, J., Tao, Z. et al. Regulatory network of miRNA on its target: coordination between transcriptional and post-transcriptional regulation of gene expression. Cell. Mol. Life Sci. 76, 441–451 (2019). https://doi.org/10.1007/s00018-018-2940-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-018-2940-7

Keywords

Navigation