BMB Reports

Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
권호 표지
DOI QR코드

DOI QR Code

MicroRNA-directed cleavage of targets: mechanism and experimental approaches

  • Park, June Hyun (Department of Agricultural Biotechnology, Seoul National University) ;
  • Shin, Chanseok (Department of Agricultural Biotechnology, Seoul National University)
  • Received : 2014.05.20
  • Published : 2014.08.31
Download PDF
⟨ Previous Next ⟩

Abstract

MicroRNAs (miRNAs) are a large family of post-transcriptional regulators, which are 21-24 nt in length and play a role in a wide variety of biological processes in eukaryotes. The past few years have seen rapid progress in our understanding of miRNA biogenesis and the mechanism of action, which commonly entails a combination of target degradation and translational repression. The target degradation mediated by Argonaute-catalyzed endonucleolytic cleavage exerts a significant repressive effect on target mRNA expression, particularly during rapid developmental transitions. This review outlines the current understanding of the mechanistic aspects of this important process and discusses several different experimental approaches to identify miRNA cleavage targets.

Keywords

References

  1. Lee, Y., Kim, M., Han, J., Yeom, K. H., Lee, S., Baek, S. H. and Kim, V. N. (2004) MicroRNA genes are transcribed by RNA polymerase II. EMBO J. 23, 4051-4060. https://doi.org/10.1038/sj.emboj.7600385
  2. Lee, Y., Ahn, C., Han, J., Choi, H., Kim, J., Yim, J., Lee, J., Provost, P., Radmark, O., Kim, S. and Kim, V. N. (2003) The nuclear RNase III Drosha initiates microRNA processing. Nature 425, 415-419. https://doi.org/10.1038/nature01957
  3. Krol, J., Loedige, I. and Filipowicz, W. (2010) The widespread regulation of microRNA biogenesis, function and decay. Nat. Rev. Genet. 11, 597-610.
  4. Voinnet, O. (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136, 669-687. https://doi.org/10.1016/j.cell.2009.01.046
  5. Shin, C. (2008) Cleavage of the star strand facilitates assembly of some microRNAs into Ago2-containing silencing complexes in mammals. Mol. Cells 26, 308-313.
  6. Huntzinger, E. and Izaurralde, E. (2011) Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat. Rev. Genet. 12, 99-110. https://doi.org/10.1038/nrg2936
  7. Subtelny, A. O., Eichhorn, S. W., Chen, G. R., Sive, H. and Bartel, D. P. (2014) Poly(A)-tail profiling reveals an embryonic switch in translational control. Nature 508, 66-71. https://doi.org/10.1038/nature13007
  8. Bazzini, A. A., Lee, M. T. and Giraldez, A. J. (2012) Ribosome Profiling Shows That miR-430 Reduces Translation Before Causing mRNA Decay in Zebrafish. Science 336, 233-237. https://doi.org/10.1126/science.1215704
  9. Bohmert, K., Camus, I., Bellini, C., Bouchez, D., Caboche, M. and Benning, C. (1998) AGO1 defines a novel locus of Arabidopsis controlling leaf development. EMBO J. 17, 170-180. https://doi.org/10.1093/emboj/17.1.170
  10. Ender, C. and Meister, G. (2010) Argonaute proteins at a glance. J. Cell Sci. 123, 1819-1823. https://doi.org/10.1242/jcs.055210
  11. Cerutti, L., Mian, N. and Bateman, A. (2000) Domains in gene silencing and cell differentiation proteins: the novel PAZ domain and redefinition of the Piwi domain. Trends. Biochem. Sci. 25, 481-482. https://doi.org/10.1016/S0968-0004(00)01641-8
  12. Yan, K. S., Yan, S., Farooq, A., Han, A., Zeng, L. and Zhou, M. M. (2003) Structure and conserved RNA binding of the PAZ domain. Nature 426, 468-474. https://doi.org/10.1038/nature02129
  13. Lingel, A., Simon, B., Izaurralde, E. and Sattler, M. (2003) Structure and nucleic-acid binding of the Drosophila Argonaute 2 PAZ domain. Nature 426, 465-469. https://doi.org/10.1038/nature02123
  14. Song, J. J., Liu, J., Tolia, N. H., Schneiderman, J., Smith, S. K., Martienssen, R. A., Hannon, G. J. and Joshua-Tor, L. (2003) The crystal structure of the Argonaute2 PAZ domain reveals an RNA binding motif in RNAi effector complexes. Nat. Struct. Biol. 10, 1026-1032. https://doi.org/10.1038/nsb1016
  15. Wang, Y., Juranek, S., Li, H., Sheng, G., Wardle, G. S., Tuschl, T. and Patel, D. J. (2009) Nucleation, propagation and cleavage of target RNAs in Ago silencing complexes. Nature 461, 754-761. https://doi.org/10.1038/nature08434
  16. Song, J. J., Smith, S. K., Hannon, G. J. and Joshua-Tor, L. (2004) Crystal structure of Argonaute and its implications for RISC slicer activity. Science 305, 1434-1437. https://doi.org/10.1126/science.1102514
  17. Wang, Y., Sheng, G., Juranek, S., Tuschl, T. and Patel, D. J. (2008) Structure of the guide-strand-containing argonaute silencing complex. Nature 456, 209-213. https://doi.org/10.1038/nature07315
  18. Jinek, M. and Doudna, J. A. (2009) A three-dimensional view of the molecular machinery of RNA interference. Nature 457, 405-412. https://doi.org/10.1038/nature07755
  19. Frank, F., Sonenberg, N. and Nagar, B. (2010) Structural basis for 5'-nucleotide base-specific recognition of guide RNA by human AGO2. Nature 465, 818-822. https://doi.org/10.1038/nature09039
  20. Boland, A., Huntzinger, E., Schmidt, S., Izaurralde, E. and Weichenrieder, O. (2011) Crystal structure of the MID-PIWI lobe of a eukaryotic Argonaute protein. Proc. Natl. Acad. Sci. U. S. A. 108, 10466-10471. https://doi.org/10.1073/pnas.1103946108
  21. Nowotny, M., Gaidamakov, S. A., Crouch, R. J. and Yang, W. (2005) Crystal structures of RNase H bound to an RNA/DNA hybrid: substrate specificity and metal-dependent catalysis. Cell 121, 1005-1016. https://doi.org/10.1016/j.cell.2005.04.024
  22. Katayanagi, K., Miyagawa, M., Matsushima, M., Ishikawa, M., Kanaya, S., Ikehara, M., Matsuzaki, T. and Morikawa, K. (1990) Three-dimensional structure of ribonuclease H from E. coli. Nature 347, 306-309. https://doi.org/10.1038/347306a0
  23. Rivas, F. V., Tolia, N. H., Song, J. J., Aragon, J. P., Liu, J., Hannon, G. J. and Joshua-Tor, L. (2005) Purified Argonaute2 and an siRNA form recombinant human RISC. Nat. Struct. Mol. Biol. 12, 340-349. https://doi.org/10.1038/nsmb918
  24. Nakanishi, K., Weinberg, D. E., Bartel, D. P. and Patel, D. J. (2012) Structure of yeast Argonaute with guide RNA. Nature 486, 368-374. https://doi.org/10.1038/nature11211
  25. Schurmann, N., Trabuco, L. G., Bender, C., Russell, R. B. and Grimm, D. (2013) Molecular dissection of human Argonaute proteins by DNA shuffling. Nat. Struct. Mol. Biol. 20, 818-826. https://doi.org/10.1038/nsmb.2607
  26. Faehnle, C. R., Elkayam, E., Haase, A. D., Hannon, G. J. and Joshua-Tor, L. (2013) The making of a slicer: activation of human Argonaute-1. Cell Reports 3, 1901-1909. https://doi.org/10.1016/j.celrep.2013.05.033
  27. Hauptmann, J., Dueck, A., Harlander, S., Pfaff, J., Merkl, R. and Meister, G. (2013) Turning catalytically inactive human Argonaute proteins into active slicer enzymes. Nat. Struct. Mol. Biol. 20, 814-817. https://doi.org/10.1038/nsmb.2577
  28. Jones-Rhoades, M. W., Bartel, D. P. and Bartel, B. (2006) MicroRNAs and their regulatory roles in plants. Annu. Rev. Plant. Biol. 57, 19-53. https://doi.org/10.1146/annurev.arplant.57.032905.105218
  29. Rhoades, M. W., Reinhart, B. J., Lim, L. P., Burge, C. B., Bartel, B. and Bartel, D. P. (2002) Prediction of plant microRNA targets. Cell 110, 513-520. https://doi.org/10.1016/S0092-8674(02)00863-2
  30. Schwab, R., Palatnik, J. F., Riester, M., Schommer, C., Schmid, M. and Weigel, D. (2005) Specific effects of MicroRNAs on the plant transcriptome. Dev. Cell 8, 517-527. https://doi.org/10.1016/j.devcel.2005.01.018
  31. Llave, C., Xie, Z., Kasschau, K. D. and Carrington, J. C. (2002) Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 297, 2053-2056. https://doi.org/10.1126/science.1076311
  32. Tuschl, T., Zamore, P. D., Lehmann, R., Bartel, D. P. and Sharp, P. A. (1999) Targeted mRNA degradation by double- stranded RNA in vitro. Genes Dev. 13, 3191-3197. https://doi.org/10.1101/gad.13.24.3191
  33. Addo-Quaye, C., Eshoo, T. W., Bartel, D. P. and Axtell, M. J. (2008) Endogenous siRNA and miRNA targets identified by sequencing of the Arabidopsis degradome. Curr. Biol. 18, 758-762. https://doi.org/10.1016/j.cub.2008.04.042
  34. German, M. A., Pillay, M., Jeong, D. H., Hetawal, A., Luo, S., Janardhanan, P., Kannan, V., Rymarquis, L. A., Nobuta, K., German, R., De Paoli, E., Lu, C., Schroth, G., Meyers, B. C. and Green, P. J. (2008) Global identification of microRNA-target RNA pairs by parallel analysis of RNA ends. Nat. Biotechnol. 26, 941-946. https://doi.org/10.1038/nbt1417
  35. Gregory, B. D., O'Malley, R. C., Lister, R., Urich, M. A., Tonti-Filippini, J., Chen, H., Millar, A. H. and Ecker, J. R. (2008) A link between RNA metabolism and silencing affecting Arabidopsis development. Dev. Cell 14, 854-866. https://doi.org/10.1016/j.devcel.2008.04.005
  36. Li, Y. F., Zheng, Y., Addo-Quaye, C., Zhang, L., Saini, A., Jagadeeswaran, G., Axtell, M. J., Zhang, W. X. and Sunkar, R. (2010) Transcriptome-wide identification of microRNA targets in rice. Plant J. 62, 742-759. https://doi.org/10.1111/j.1365-313X.2010.04187.x
  37. Karlova, R., van Haarst, J. C., Maliepaard, C., van de Geest, H., Bovy, A. G., Lammers, M., Angenent, G. C. and de Maagd, R. A. (2013) Identification of microRNA targets in tomato fruit development using high-throughput sequencing and degradome analysis. J. Exp. Bot. 64, 1863-1878. https://doi.org/10.1093/jxb/ert049
  38. Pantaleo, V., Szittya, G., Moxon, S., Miozzi, L., Moulton, V., Dalmay, T. and Burgyan, J. (2010) Identification of grapevine microRNAs and their targets using high-throughput sequencing and degradome analysis. Plant J. 62, 960-976.
  39. Jeong, D. H., Schmidt, S. A., Rymarquis, L. A., Park, S., Ganssmann, M., German, M. A., Accerbi, M., Zhai, J., Fahlgren, N., Fox, S. E., Garvin, D. F., Mockler, T. C., Carrington, J. C., Meyers, B. C. and Green, P. J. (2013) Parallel analysis of RNA ends enhances global investigation of microRNAs and target RNAs of Brachypodium distachyon. Genome Biol. 14, R145. https://doi.org/10.1186/gb-2013-14-12-r145
  40. Yekta, S., Shih, I. H. and Bartel, D. P. (2004) MicroRNA-directed cleavage of HOXB8 mRNA. Science 304, 594-596. https://doi.org/10.1126/science.1097434
  41. Shin, C., Nam, J. W., Farh, K. K., Chiang, H. R., Shkumatava, A. and Bartel, D. P. (2010) Expanding the microRNA targeting code: functional sites with centered pairing. Mol. Cell 38, 789-802. https://doi.org/10.1016/j.molcel.2010.06.005
  42. Karginov, F. V., Cheloufi, S., Chong, M. M., Stark, A., Smith, A. D. and Hannon, G. J. (2010) Diverse endonucleolytic cleavage sites in the mammalian transcriptome depend upon microRNAs, Drosha, and additional nucleases. Mol. Cell 38, 781-788. https://doi.org/10.1016/j.molcel.2010.06.001
  43. Park, J. H., Ahn, S., Kim, S., Lee, J., Nam, J. W. and Shin, C. (2013) Degradome sequencing reveals an endogenous microRNA target in C. elegans. FEBS Letters 587, 964-969. https://doi.org/10.1016/j.febslet.2013.02.029
  44. Moran, Y., Fredman, D., Praher, D., Li, X. Z., Wee, L. M., Rentzsch, F., Zamore, P. D., Technau, U. and Seitz, H. (2014) Cnidarian microRNAs frequently regulate targets by cleavage. Genome Res. 24, 651-663. https://doi.org/10.1101/gr.162503.113
  45. Moran, Y., Praher, D., Fredman, D. and Technau, U. (2013) The evolution of microRNA pathway protein components in Cnidaria. Mol. Biol. Evol. 30, 2541-2552. https://doi.org/10.1093/molbev/mst159
  46. Mercer, T. R., Dinger, M. E., Bracken, C. P., Kolle, G., Szubert, J. M., Korbie, D. J., Askarian-Amiri, M. E., Gardiner, B. B., Goodall, G. J., Grimmond, S. M. and Mattick, J. S. (2010) Regulated post-transcriptional RNA cleavage diversifies the eukaryotic transcriptome. Genome Res. 20, 1639-1650. https://doi.org/10.1101/gr.112128.110
  47. Brodersen, P., Sakvarelidze-Achard, L., Bruun-Rasmussen, M., Dunoyer, P., Yamamoto, Y. Y., Sieburth, L. and Voinnet, O. (2008) Widespread translational inhibition by plant miRNAs and siRNAs. Science 320, 1185-1190. https://doi.org/10.1126/science.1159151
  48. Iwakawa, H. and Tomari, Y. (2013) Molecular Insights into microRNA-Mediated Translational Repression in Plants. Mol. Cell 52, 591-601. https://doi.org/10.1016/j.molcel.2013.10.033
  49. Aukerman, M. J. and Sakai, H. (2003) Regulation of flowering time and floral organ identity by a MicroRNA and its APETALA2-like target genes. Plant Cell 15, 2730-2741. https://doi.org/10.1105/tpc.016238
  50. Bari, R., Datt Pant, B., Stitt, M. and Scheible, W. R. (2006) PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol. 141, 988-999. https://doi.org/10.1104/pp.106.079707
  51. Gandikota, M., Birkenbihl, R. P., Hohmann, S., Cardon, G. H., Saedler, H. and Huijser, P. (2007) The miRNA156/157 recognition element in the 3' UTR of the Arabidopsis SBP box gene SPL3 prevents early flowering by translational inhibition in seedlings. Plant J. 49, 683-693. https://doi.org/10.1111/j.1365-313X.2006.02983.x

Cited by

  1. Targeting Glial Mitochondrial Function for Protection from Cerebral Ischemia: Relevance, Mechanisms, and the Role of MicroRNAs vol.2016, 2016, https://doi.org/10.1155/2016/6032306
  2. MiR-106b promotes migration and invasion through enhancing EMT via downregulation of Smad 7 in Kazakh’s esophageal squamous cell carcinoma vol.37, pp.11, 2016, https://doi.org/10.1007/s13277-016-5338-x
  3. Role of microRNAs in obesity and obesity-related diseases vol.12, pp.1, 2017, https://doi.org/10.1186/s12263-017-0577-z
  4. MicroRNA and Pathogenesis of Enterovirus Infection vol.8, pp.1, 2016, https://doi.org/10.3390/v8010011
  5. MicroRNAs as biomarkers for early breast cancer diagnosis, prognosis and therapy prediction vol.172, 2017, https://doi.org/10.1016/j.pharmthera.2016.11.012
  6. MiR-203 Participates in Human Placental Angiogenesis by Inhibiting VEGFA and VEGFR2 Expression 2017, https://doi.org/10.1177/1933719117725817
  7. MicroRNA-421 inhibits breast cancer metastasis by targeting metastasis associated 1 vol.83, 2016, https://doi.org/10.1016/j.biopha.2016.08.058
  8. miRNA-133a attenuates lipid accumulation via TR4-CD36 pathway in macrophages vol.127, 2016, https://doi.org/10.1016/j.biochi.2016.04.012
  9. Comparative transcriptome investigation of global gene expression changes caused by miR156 overexpression in Medicago sativa vol.17, pp.1, 2016, https://doi.org/10.1186/s12864-016-3014-6
  10. The dynamics of a feed-forward loop depends on the regulator type in its indirect pathway vol.60, pp.2, 2015, https://doi.org/10.1134/S0006350915020062
  11. A Comprehensive Meta-Analysis of MicroRNAs for Predicting Colorectal Cancer vol.95, pp.9, 2016, https://doi.org/10.1097/MD.0000000000002738
  12. MicroRNA and Transcription Factor: Key Players in Plant Regulatory Network vol.8, 2017, https://doi.org/10.3389/fpls.2017.00565
  13. Circulating hsa-miR-30e-5p, hsa-miR-92a-3p, and hsa-miR-223-3p may be novel biomarkers in systemic lupus erythematosus vol.88, pp.4, 2016, https://doi.org/10.1111/tan.12874
  14. Micro-RNA-1 is decreased by hypoxia and contributes to the development of pulmonary vascular remodeling via regulation of sphingosine kinase 1 vol.314, pp.3, 2018, https://doi.org/10.1152/ajplung.00057.2017
  15. miRNAs as Biomarkers for Diagnosis and Assessment of Prognosis of Coronary Artery Disease vol.08, pp.01, 2018, https://doi.org/10.4236/ojim.2018.81007
  16. The Interplay between the RNA Decay and Translation Machinery in Eukaryotes vol.10, pp.5, 2018, https://doi.org/10.1101/cshperspect.a032839
  17. MiR-320 regulates cardiomyocyte apoptosis induced by ischemia–reperfusion injury by targeting AKIP1 vol.23, pp.1, 2018, https://doi.org/10.1186/s11658-018-0105-1
  18. Transcriptomic analyses of rice (Oryza sativa) genes and non-coding RNAs under nitrogen starvation using multiple omics technologies vol.19, pp.1, 2018, https://doi.org/10.1186/s12864-018-4897-1
  19. Transcriptome analysis of microRNA156 overexpression alfalfa roots under drought stress vol.8, pp.1, 2018, https://doi.org/10.1038/s41598-018-27088-8
  20. Impact of miR-192 and miR-194 on cyst enlargement through EMT in autosomal dominant polycystic kidney disease vol.33, pp.2, 2019, https://doi.org/10.1096/fj.201800563RR