Regulation of miRNA content. Part 2. Degradation of miRNAs

Authors

DOI:

https://doi.org/10.22141/2224-0551.16.5.2021.239719

Keywords:

microRNA, microRNA degradation, exoribonucleases, RNA-degrading exosome, polynucleotide phosphorylase, review

Abstract

The scientific review presents the process of regulation of microRNA content — microRNA degradation. To write the article, information was searched using databases Scopus, Web of Science, MedLine, PubMed, Google Scholar, EMBASE, Global Health, The Cochrane Library, CyberLeninka. The article presents the characteristics of the most important process of RNA metabolism — degradation of 3'→5' RNA. Degradation of microRNA is inherent in organisms of all kingdoms of life and is involved in the regulation of RNA representation, elimination of dysfunctional or incorrectly constructed RNA molecules and processing of RNA precursors. Exoribonucleases that affect the stability of mature forms of miRNA are presented. It is emphasized that XRN exoribonucleases degrade various RNA substrates during total RNA degradation and are involved in specific processes such as nonsense-mediated degradation, gene silencing, rRNA maturation, and transcription termination. It is shown that exoribonuclease XRN2 plays a crucial role in the termination of transcription during viral infection, namely it has cytoplasmic antiviral activity against hepatitis C virus. The role of RNA-degrading exosome in microRNA degradation is presented. RNA-degrading exosome is a ubiquitous complex and 3'-5'-endo- and exoribonucleases of eukaryotes, which interacts with several processing cofactors and degrades almost all classes of cytoplasmic RNA. The article reflects the function of evolutionarily conserved phosphorolytic 3'-5'-exoribonuclease — polynucleotide phosphorylase. The role of exoribonuclease 1, which is an evolutio­narily conserved 3'-5'-exoribonuclease of the DEDDh family, is involved in the final processing of 5.8S rRNA, replication-dependent histone mRNA, siRNA, and miRNA. Eri1 exoribonuclease has been shown to regulate global microRNA homeostasis in lymphocytes and to participate in NK cell development and antiviral response. Thus, one of the mechanisms of regulation of miRNA content is the most important process of RNA metabolism, which is inherent in organisms of all kingdoms of life, namely the degradation of miRNAs.

Downloads

Download data is not yet available.

References

Bail S, Swerdel M, Liu H, et al. Differential regulation of microRNA stability. RNA. 2010 May;16(5):1032-9. doi:10.1261/rna.1851510.

Black JJ, Johnson AW. Genetics animates structure: leveraging genetic interactions to study the dynamics of ribosome biogenesis. Curr Genet. 2021 Apr 12. doi:10.1007/s00294-021-01187-y.

Cai Y, Yu X, Hu S, Yu J. A brief review on the mechanisms of miRNA regulation. Genomics Proteomics Bioinformatics. 2009 Dec;7(4):147-54. doi:10.1016/S1672-0229(08)60044-3.

Chang JH, Xiang S, Tong L. 5'-3' exoribonucleases. In: Nicholson AW, editor. Ribonucleases. Vol 26. Heidelberg: Springer; 2011. 167-192 pp.

Chatterjee S, Grosshans H. Active turnover modulates mature microRNA activity in Caenorhabditis elegans. Nature. 2009 Sep 24;461(7263):546-9. doi:10.1038/nature08349.

Cheng Y, Patel DJ. Crystallographic structure of the nuclease domain of 3'hExo, a DEDDh family member, bound to rAMP. J Mol Biol. 2004 Oct 15;343(2):305-12. doi: 10.1016/j.jmb.2004.08.055.

Das SK, Sokhi UK, Bhutia SK, et al. Human polynucleotide phosphorylase selectively and preferentially degrades microRNA-221 in human melanoma cells. Proc Natl Acad Sci U S A. 2010 Jun 29;107(26):11948-53. doi:10.1073/pnas.0914143107.

Delan-Forino C, Schneider C, Tollervey D. Transcriptome-wide analysis of alternative routes for RNA substrates into the exosome complex. PLoS Genet. 2017 Mar 29;13(3):e1006699. doi:10.1371/journal.pgen.1006699.

Drazkowska K, Tomecki R, Stodus K, Kowalska K, Czarnocki-Cieciura M, Dziembowski A. The RNA exosome complex central channel controls both exonuclease and endonuclease Dis3 activities in vivo and in vitro. Nucleic Acids Res. 2013 Apr 1;41(6):3845-58. doi:10.1093/nar/gkt060.

Evguenieva-Hackenberg E, Hou L, Glaeser S, Klug G. Structure and function of the archaeal exosome. Wiley Interdiscip Rev RNA. 2014 Sep-Oct;5(5):623-35. doi:10.1002/wrna.1234.

Evguenieva-Hackenberg E. The Archaeal Exosome. In: Jensen TH, editor. RNA Exosome. Advances in Experimental Medicine and Biology, vol 702. New York, NY: Springer; 2010. 29-38 pp. doi:10.1007/978-1-4419-7841-7_3.

Frazier MN, Pillon MC, Kocaman S, Gordon J, Stanley RE. Structural overview of macromolecular machines involved in ribosome biogenesis. Curr Opin Struct Biol. 2021 Apr;67:51-60. doi:10.1016/j.sbi.2020.09.003.

Frederick MI, Heinemann IU. Regulation of RNA stability at the 3' end. Biol Chem. 2020 Nov 27;402(4):425-431. doi:10.1515/hsz-2020-0325.

Grosshans H, Chatterjee S. MicroRNAses and the regulated degradation of mature animal miRNAs. Adv Exp Med Biol. 2010;700:140-55.

Jiang H, Bai L, Ji L, et al. Degradation of MicroRNA miR-466d-3p by Japanese Encephalitis Virus NS3 Facilitates Viral Replication and Interleukin-1β Expression. J Virol. 2020 Jul 16;94(15):e00294-20. doi:10.1128/JVI.00294-20.

Januszyk K, Lima CD. The eukaryotic RNA exosome. Curr Opin Struct Biol. 2014 Feb;24:132-40. doi:10.1016/j.sbi.2014.01.011.

Kilchert C. RNA Exosomes and Their Cofactors. Methods Mol Biol. 2020;2062:215-235. doi:10.1007/978-1-4939-9822-7_11.

Koyano K, Bahn JH, Xiao X. Extracellular microRNA 3' end modification across diverse body fluids. Epigenetics. 2020 Nov 2:1-16. doi:10.1080/15592294.2020.1834922.

Łabno A, Tomecki R, Dziembowski A. Cytoplasmic RNA decay pathways - Enzymes and mechanisms. Biochim Biophys Acta. 2016 Dec;1863(12):3125-3147. doi:10.1016/j.bbamcr.2016.09.023.

Lau B, Cheng J, Flemming D, et al. Structure of the Maturing 90S Pre-ribosome in Association with the RNA Exosome. Mol Cell. 2021 Jan 21;81(2):293-303.e4. doi:10.1016/j.molcel.2020.11.009.

Liu X, Haniff HS, Childs-Disney JL, et al. Targeted Degradation of the Oncogenic MicroRNA 17-92 Cluster by Structure-Targeting Ligands. J Am Chem Soc. 2020 Apr 15;142(15):6970-6982. doi:10.1021/jacs.9b13159.

Machlin ES, Sarnow P, Sagan SM. Masking the 5' terminal nucleotides of the hepatitis C virus genome by an unconventional microRNA-target RNA complex. Proc Natl Acad Sci U S A. 2011 Feb 22;108(8):3193-8. doi:10.1073/pnas.1012464108.

Miki TS, Großhans H. The multifunctional RNase XRN2. Biochem Soc Trans. 2013 Aug;41(4):825-30. doi:10.1042/BST20130001.

Morton DJ, Kuiper EG, Jones SK, Leung SW, Corbett AH, Fasken MB. The RNA exosome and RNA exosome-linked disease. RNA. 2018 Feb;24(2):127-142. doi:10.1261/rna.064626.117.

Nagarajan VK, Jones CI, Newbury SF, Green PJ. XRN 5'→3' exoribonucleases: structure, mechanisms and functions. Biochim Biophys Acta. 2013 Jun-Jul;1829(6-7):590-603. doi:10.1016/j.bbagrm.2013.03.005.

Nejad C, Pillman KA, Siddle KJ, et al. miR-222 isoforms are differentially regulated by type-I interferon. RNA. 2018 Mar;24(3):332-341. doi:10.1261/rna.064550.117.

Porrua O, Libri D. RNA quality control in the nucleus: the Angels' share of RNA. Biochim Biophys Acta. 2013 Jun-Jul;1829(6-7):604-11. doi:10.1016/j.bbagrm.2013.02.012.

Proudfoot NJ. Ending the message: poly(A) signals then and now. Genes Dev. 2011 Sep 1;25(17):1770-82. doi:10.1101/gad.17268411.

Sarkar D, Fisher PB. Polynucleotide phosphorylase: an evolutionary conserved gene with an expanding repertoire of functions. Pharmacol Ther. 2006 Oct;112(1):243-63. doi:10.1016/j.pharmthera.2006.04.003.

Sedano CD, Sarnow P. Hepatitis C virus subverts liver-specific miR-122 to protect the viral genome from exoribonuclease Xrn2. Cell Host Microbe. 2014 Aug 13;16(2):257-264. doi:10.1016/j.chom.2014.07.006.

Sedano CD, Sarnow P. Interaction of host cell microRNAs with the HCV RNA genome during infection of liver cells. Semin Liver Dis. 2015 Feb;35(1):75-80. doi:10.1055/s-0034-1397351.

Sikorska N, Zuber H, Gobert A, Lange H, Gagliardi D. RNA degradation by the plant RNA exosome involves both phosphorolytic and hydrolytic activities. Nat Commun. 2017 Dec 18;8(1):2162. doi:10.1038/s41467-017-02066-2.

Sokhi UK, Bacolod MD, Dasgupta S, et al. Identification of genes potentially regulated by human polynucleotide phosphorylase (hPNPase old-35) using melanoma as a model. PLoS One. 2013 Oct 15;8(10):e76284. doi:10.1371/journal.pone.0076284.

Thomas MF, Abdul-Wajid S, Panduro M, et al. Eri1 regulates microRNA homeostasis and mouse lymphocyte development and antiviral function. Blood. 2012 Jul 5;120(1):130-42. doi:10.1182/blood-2011-11-394072.

Thomas MF, L'Etoile ND, Ansel KM. Eri1: a conserved enzyme at the crossroads of multiple RNA-processing pathways. Trends Genet. 2014 Jul;30(7):298-307. doi:10.1016/j.tig.2014.05.003.

Towler BP, Jones CI, Viegas SC, et al. The 3'-5' exoribonuclease Dis3 regulates the expression of specific microRNAs in Drosophila wing imaginal discs. RNA Biol. 2015;12(7):728-41. doi:10.1080/15476286.2015.1040978.

Zangari J, Ilie M, Rouaud F, et al. Rapid decay of engulfed extracellular miRNA by XRN1 exonuclease promotes transient epithelial-mesenchymal transition. Nucleic Acids Res. 2017 Apr 20;45(7):4131-4141. doi:10.1093/nar/gkw1284.

Zhao S, Liu MF. Mechanisms of microRNA-mediated gene regulation. Sci China C Life Sci. 2009 Dec;52(12):1111-6. doi:10.1007/s11427-009-0152-y.

Published

2022-01-05

How to Cite

Abaturov, A., & Babуch V. (2022). Regulation of miRNA content. Part 2. Degradation of miRNAs. CHILD`S HEALTH, 16(5), 384–390. https://doi.org/10.22141/2224-0551.16.5.2021.239719

Issue

Section

Theoretical Medicine

Most read articles by the same author(s)

1 2 3 4 5 6 7 8 > >>