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2016 | 63 | 4 | 773-783
Article title

How short RNAs impact the human ribonuclease Dicer activity: putative regulatory feedback-loops and other RNA-mediated mechanisms controlling microRNA processing

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EN
Abstracts
EN
Ribonuclease Dicer plays a pivotal role in RNA interference pathways by processing long double-stranded RNAs and single-stranded hairpin RNA precursors into small interfering RNAs (siRNAs) and microRNAs (miRNAs), respectively. While details of Dicer regulation by a variety of proteins are being elucidated, less is known about non-protein factors, e.g. RNA molecules, that may influence this enzyme's activity. Therefore, we decided to investigate the question of whether the RNA molecules can function not only as Dicer substrates but also as its regulators. Our previous in vitro studies indicated that the activity of human Dicer can be influenced by short RNA molecules that either bind to Dicer or interact with its substrates, or both. Those studies were carried out with commercial Dicer preparations. Nevertheless, such preparations are usually not homogeneous enough to carry out more detailed RNA-binding studies. Therefore, we have established our own system for the production of human Dicer in insect cells. In this manuscript, we characterize the RNA-binding and RNA-cleavage properties of the obtained preparation. We demonstrate that Dicer can efficiently bind single-stranded RNAs that are longer than ~20-nucleotides. Consequently, we revisit possible scenarios of Dicer regulation by single-stranded RNA species ranging from ~10- to ~60-nucleotides, in the context of their binding to this enzyme. Finally, we show that siRNA/miRNA-sized RNAs may affect miRNA production either by binding to Dicer or by participating in regulatory feedback-loops. Altogether, our studies suggest a broad regulatory role of short RNAs in Dicer functioning.
Publisher

Year
Volume
63
Issue
4
Pages
773-783
Physical description
Dates
published
2016
received
2016-06-01
revised
2016-06-27
accepted
2016-06-30
(unknown)
2016-10-13
Contributors
  • Institute of Bioorganic Chemistry, Polish Academy of Sciences, Poznań, Poland
  • Intercollegiate Faculty of Biotechnology of the University of Gdansk and Medical University of Gdańsk, Gdansk, Poland
  • Institute of Bioorganic Chemistry, Polish Academy of Sciences, Poznań, Poland
  • Institute of Bioorganic Chemistry, Polish Academy of Sciences, Poznań, Poland
  • Intercollegiate Faculty of Biotechnology of the University of Gdansk and Medical University of Gdańsk, Gdansk, Poland
  • Intercollegiate Faculty of Biotechnology of the University of Gdansk and Medical University of Gdańsk, Gdansk, Poland
  • Institute of Bioorganic Chemistry, Polish Academy of Sciences, Poznań, Poland; Institute of Computing Science, Poznan University of Technology, Poznań, Poland
  • Institute of Bioorganic Chemistry, Polish Academy of Sciences, Poznań, Poland
References
  • Andersson MG, Haasnoot PC, Xu N, Berenjian S, Berkhout B, Akusjarvi G (2005) Suppression of RNA interference by adenovirus virus-associated RNA. J Virol 79: 9556-9565. https://doi.org/10.1128/JVI.79.15.9556-9565.2005.
  • Bellaousov S, Reuter JS, Seetin MG, Mathews DH (2013) RNAstructure: web servers for RNA secondary structure prediction and analysis. Nucleic Acids Res 41: W471-W474. https://doi.org/10.1093/nar/gkt290.
  • Belter A, Rolle K, Piwecka M, Fedoruk-Wyszomirska A, Naskret-Barciszewska MZ, Barciszewski J (2016) Inhibition of miR-21 in glioma cells using catalytic nucleic acids. Sci Rep 6: 24516. https://doi.org/10.1038/srep24516.
  • Bennasser Y, Jeang KT (2006) HIV-1 Tat interaction with Dicer: requirement for RNA. Retrovirology 3: 95. https://doi.org/10.1186/1742-4690-3-95.
  • Berkhout B, Haasnoot J (2006) The interplay between virus infection and the cellular RNA interference machinery. FEBS Lett 580: 2896-2902. https://doi.org/10.1016/j.febslet.2006.02.070.
  • Bernstein E, Caudy AA, Hammond SM, Hannon GJ (2001) Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409: 363-366. https://doi.org/10.1038/35053110.
  • Calin GA, Croce CM (2006) MicroRNA signatures in human cancers. Nat Rev Cancer 6: 857-866. https://doi.org/10.1038/nrc1997.
  • Chakravarthy S, Sternberg SH, Kellenberger CA, Doudna JA (2010) Substrate-specific kinetics of Dicer-catalyzed RNA processing. J Mol Biol 404: 392-402. https://doi.org/10.1016/j.jmb.2010.09.030.
  • Daniels SM, Melendez-Pena CE, Scarborough RJ, Daher A, Christensen HS, El Far M, Purcell DF, Laine S, Gatignol A (2009) Characterization of the TRBP domain required for dicer interaction and function in RNA interference. BMC Mol Biol 10: 38. https://doi.org/10.1186/1471-2199-10-38.
  • Doberstein K, Bretz NP, Schirmer U, Fiegl H, Blaheta R, Breunig C, Muller-Holzner E, Reimer D, Zeimet AG, Altevogt P (2014) miR-21-3p is a positive regulator of L1CAM in several human carcinomas. Cancer Lett 354: 455-466. https://doi.org/10.1016/j.canlet.2014.08.020.
  • Dutkiewicz M, Ojdowska A, Kuczynski J, Lindig V, Zeichhardt H, Kurreck J, Ciesiolka J (2015) Targeting highly structured RNA by cooperative action of siRNAs and helper antisense oligomers in living cells. PLoS One 10: e0136395. https://doi.org/10.1371/journal.pone.0136395.
  • Esquela-Kerscher A, Slack FJ (2006) Oncomirs - microRNAs with a role in cancer. Nat Rev Cancer 6: 259-269. https://doi.org/10.1038/nrc1840.
  • Feng Y, Zhang X, Graves P, Zeng Y (2012) A comprehensive analysis of precursor microRNA cleavage by human Dicer. RNA 18: 2083-2092. https://doi.org/10.1261/rna.033688.112.
  • Figlerowicz M, Alejska M, Kurzynska-Kokorniak A (2003) Genetic variability: the key problem in the prevention and therapy of RNA-based virus infections. Med Res Rev 23: 488-518. https://doi.org/10.1002/med.10045.
  • Friedman RC, Farh KK, Burge CB, Bartel DP (2009) Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19: 92-105. https://doi.org/10.1101/gr.082701.108.
  • Gorska A, Swiatkowska A, Dutkiewicz M, Ciesiolka J (2013) Modulation of p53 expression using antisense oligonucleotides complementary to the 5'-terminal region of p53 mRNA in vitro and in the living cells. PLoS One 8: e78863. https://doi.org/10.1371/journal.pone.0078863.
  • Gregory RI, Chendrimada TP, Cooch N, Shiekhattar R (2005) Human RISC couples microRNA biogenesis and posttranscriptional gene silencing. Cell 123: 631-640. https://doi.org/10.1016/j.cell.2005.10.022.
  • Gu S, Jin L, Zhang Y, Huang Y, Zhang F, Valdmanis PN, Kay MA (2012) The loop position of shRNAs and pre-miRNAs is critical for the accuracy of dicer processing in vivo. Cell 151: 900-911. https://doi.org/10.1016/j.cell.2012.09.042.
  • Haasnoot J, Berkhout B (2006) RNA interference: its use as antiviral therapy. Handb Exp Pharmacol: 117-150.
  • Hebert SS, De Strooper B (2009) Alterations of the microRNA network cause neurodegenerative disease. Trends Neurosci 32: 199-206. https://doi.org/10.1016/j.tins.2008.12.003.
  • Jackowiak P, Figlerowicz M, Kurzynska-Kokorniak A, Figlerowicz M (2011a) Mechanisms involved in the development of chronic hepatitis C as potential targets of antiviral therapy. Curr Pharm Biotechnol 12: 1774-1780.
  • Jackowiak P, Kowala-Piaskowska A, Figlerowicz M, Alejska M, Malinowska N (2012) Evolution of hepatitis C virus hypervariable region 1 in chronically infected children. Virus Res 167: 380-384. https://doi.org/10.1016/j.virusres.2012.05.005.
  • Jackowiak P, Kuls K, Budzko L, Mania A, Figlerowicz M (2014) Phylogeny and molecular evolution of the hepatitis C virus. Infect Genet Evol 21: 67-82. https://doi.org/10.1016/j.meegid.2013.10.021.
  • Jackowiak P, Nowacka M, Strozycki PM, Figlerowicz M (2011b) RNA degradome - its biogenesis and functions. Nucleic Acids Res 39: 7361-7370. https://doi.org/10.1093/nar/gkr450.
  • Kini HK, Walton SP (2007) In vitro binding of single-stranded RNA by human Dicer. FEBS Lett 581: 5611-5616. https://doi.org/10.1016/j.febslet.2007.11.010.
  • Kurzynska-Kokorniak A, Jackowiak P, Figlerowicz M, Figlerowicz M. (2009) Human- and virus-encoded microRNAs as potential targets of antiviral therapy. Mini Rev Med Chem 9: 927-937.
  • Kurzynska-Kokorniak A, Koralewska N, Pokornowska M, Urbanowicz A, Tworak A, Mickiewicz A, Figlerowicz M (2015) The many faces of Dicer: the complexity of the mechanisms regulating Dicer gene expression and enzyme activities. Nucleic Acids Res 43: 4365-4380. https://doi.org/10.1093/nar/gkv328.
  • Kurzynska-Kokorniak A, Koralewska N, Tyczewska A, Twardowski T, Figlerowicz M (2013) A new short oligonucleotide-based strategy for the precursor-specific regulation of microRNA processing by Dicer. PLoS One 8: e77703. https://doi.org/10.1371/journal.pone.0077703.
  • Kurzynska-Kokorniak A, Pokornowska M, Koralewska N, Hoffmann W, Bienkowska-Szewczyk K, Figlerowicz M (2016) Revealing a new activity of the human Dicer DUF283 domain in vitro. Sci Rep 6: 23989. https://doi.org/10.1038/srep23989.
  • Lee Y, Hur I, Park SY, Kim YK, Suh MR, Kim VN (2006) The role of PACT in the RNA silencing pathway. EMBO J 25: 522-532. https://doi.org/10.1038/sj.emboj.7600942.
  • Lima WF, Murray H, Nichols JG, Wu H, Sun H, Prakash TP, Berdeja AR, Gaus HJ, Crooke ST (2009) Human Dicer binds short single-strand and double-strand RNA with high affinity and interacts with different regions of the nucleic acids. J Biol Chem 284: 2535-2548. https://doi.org/10.1074/jbc.M803748200.
  • Lu S, Cullen BR (2004) Adenovirus VA1 noncoding RNA can inhibit small interfering RNA and MicroRNA biogenesis. J Virol 78: 12868-12876. https://doi.org/10.1128/JVI.78.23.12868-12876.2004.
  • Ma E, MacRae IJ, Kirsch JF, Doudna JA (2008) Autoinhibition of human dicer by its internal helicase domain. J Mol Biol 380: 237-243.S0022-2836. https://doi.org/10.1016/j.jmb.2008.05.005.
  • Ma E, Zhou K, Kidwell MA, Doudna JA (2012) Coordinated activities of human dicer domains in regulatory RNA processing. J Mol Biol 422: 466-476. https://doi.org/10.1016/j.jmb.2012.06.009.
  • Ma JB, Ye K, Patel DJ (2004) Structural basis for overhang-specific small interfering RNA recognition by the PAZ domain. Nature 429: 318-322. https://doi.org/10.1038/nature02519.
  • Macrae IJ, Li F, Zhou K, Cande WZ, Doudna JA (2006a) Structure of Dicer and mechanistic implications for RNAi. Cold Spring Harb Symp Quant Biol 71: 73-80. https://doi.org/10.1101/sqb.2006.71.042.
  • MacRae IJ, Ma E, Zhou M, Robinson CV, Doudna JA (2008) In vitro reconstitution of the human RISC-loading complex. Proc Natl Acad Sci U S A 105: 512-517. https://doi.org/10.1073/pnas.0710869105.
  • Macrae IJ, Zhou K, Li F, Repic A, Brooks AN, Cande WZ, Adams PD, Doudna JA (2006b) Structural basis for double-stranded RNA processing by Dicer. Science 311: 195-198. https://doi.org/10.1126/science.1121638.
  • Maniataki E, Mourelatos Z (2005) A human, ATP-independent, RISC assembly machine fueled by pre-miRNA. Genes Dev 19: 2979-2990. https://doi.org/10.1101/gad.1384005.
  • Mathews DH, Burkard ME, Freier SM, Wyatt JR, Turner DH (1999a) Predicting oligonucleotide affinity to nucleic acid targets. RNA 5: 1458-1469.
  • Mathews DH, Sabina J, Zuker M, Turner DH (1999b) Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J Mol Biol 288: 911-940.
  • Miazga A, Hamy F, Louvel S, Klimkait T, Pietrusiewicz Z, Kurzynska-Kokorniak A, Figlerowicz M, Winska P, Kulikowski T (2011) Thiated derivatives of 2',3'-dideoxy-3'-fluorothymidine: synthesis, in vitro anti-HIV-1 activity and interaction with recombinant drug resistant HIV-1 reverse transcriptase forms. Antiviral Res 92: 57-63. https://doi.org/10.1016/j.antiviral.2011.05.012.
  • Noland CL, Ma E, Doudna JA (2011) siRNA repositioning for guide strand selection by human Dicer complexes. Mol Cell 43: 110-121. https://doi.org/10.1016/j.molcel.2011.05.028.
  • Nowacka M, Jackowiak P, Rybarczyk A, Magacz T, Strozycki PM, Barciszewski J, Figlerowicz M (2012) 2D-PAGE as an effective method of RNA degradome analysis. Mol Biol Rep 39: 139-146. https://doi.org/10.1007/s11033-011-0718-1.
  • Ota H, Sakurai M, Gupta R, Valente L, Wulff BE, Ariyoshi K, Iizasa H, Davuluri RV, Nishikura K (2013) ADAR1 Forms a complex with Dicer to promote microRNA processing and RNA-induced gene silencing. Cell 153: 575-589. https://doi.org/10.1016/j.cell.2013.03.024.
  • Pink RC, Samuel P, Massa D, Caley DP, Brooks SA, Carter DR (2015) The passenger strand, miR-21-3p, plays a role in mediating cisplatin resistance in ovarian cancer cells. Gynecol Oncol 137: 143-151. https://doi.org/10.1016/j.ygyno.2014.12.042.
  • Provost P, Dishart D, Doucet J, Frendewey D, Samuelsson B, Radmark O (2002) Ribonuclease activity and RNA binding of recombinant human Dicer. EMBO J 21: 5864-5874.
  • Reuter JS, Mathews DH (2010) RNAstructure: software for RNA secondary structure prediction and analysis. BMC Bioinformatics 11: 1-9. https://doi.org/10.1186/1471-2105-11-129.
  • Rybak-Wolf A, Jens M, Murakawa Y, Herzog M, Landthaler M, Rajewsky N (2014) A Variety of dicer substrates in human and C. elegans. Cell 159: 1153-1167. https://doi.org/10.1016/j.cell.2014.10.040.
  • Tang R, Li L, Zhu D, Hou D, Cao T, Gu H, Zhang J, Chen J, Zhang CY, Zen K (2011) 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: 504-515. https://doi.org/10.1038/cr.2011.137.
  • Taylor DW, Ma E, Shigematsu H, Cianfrocco MA, Noland CL, Nagayama K, Nogales E, Doudna JA, Wang HW (2013) Substrate-specific structural rearrangements of human Dicer. Nat Struct Mol Biol 20: 662-670. https://doi.org/10.1038/nsmb.2564.
  • Tian Y, Simanshu DK, Ma JB, Park JE, Heo I, Kim VN, Patel DJ (2014) A phosphate-binding pocket within the platform-PAZ-connector helix cassette of human Dicer. Mol Cell 53: 606-616. https://doi.org/10.1016/j.molcel.2014.01.003.
  • Tili E, Michaille JJ, Costinean S, Croce CM (2008) MicroRNAs, the immune system and rheumatic disease. Nat Clin Pract Rheumatol 4: 534-541. https://doi.org/10.1038/ncprheum0885.
  • Tsutsumi A, Kawamata T, Izumi N, Seitz H, Tomari Y (2011) Recognition of the pre-miRNA structure by Drosophila Dicer-1. Nat Struct Mol Biol 18: 1153-1158. https://doi.org/10.1038/nsmb.2125.
  • Tyczewska A, Kurzynska-Kokorniak A, Koralewska N, Szopa A, Kietrys AM, Wrzesinski J, Twardowski T, Figlerowicz M (2011) Selection of RNA oligonucleotides that can modulate human dicer activity in vitro. Nucleic Acid Ther 21: 333-346. https://doi.org/10.1089/nat.2011.0304.
  • Vermeulen A, Behlen L, Reynolds A, Wolfson A, Marshall WS, Karpilow J, Khvorova A (2005) The contributions of dsRNA structure to Dicer specificity and efficiency. RNA 11: 674-682. https://doi.org/10.1261/rna.7272305.
  • Wostenberg C, Lary JW, Sahu D, Acevedo R, Quarles KA, Cole JL, Showalter SA (2012) The role of human Dicer-dsRBD in processing small regulatory RNAs. PLoS One 7: e51829. https://doi.org/10.1371/journal.pone.0051829.
  • Yan KS, Yan S, Farooq A, Han A, Zeng L, Zhou MM (2003) Structure and conserved RNA binding of the PAZ domain. Nature 426: 468-474. https://doi.org/10.1038/nature02129.
  • Zhang H, Kolb FA, Brondani V, Billy E, Filipowicz W (2002) Human Dicer preferentially cleaves dsRNAs at their termini without a requirement for ATP. EMBO J 21: 5875-5885.
  • Zhang H, Kolb FA, Jaskiewicz L, Westhof E, Filipowicz W (2004) Single processing center models for human Dicer and bacterial RNase III. Cell 118: 57-68. https://doi.org/10.1016/j.cell.2004.06.017.
  • Zisoulis DG, Kai ZS, Chang RK, Pasquinelli AE (2012) Autoregulation of microRNA biogenesis by let-7 and Argonaute. Nature 486: 541-544. https://doi.org/10.1038/nature11134.
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bwmeta1.element.bwnjournal-article-abpv63p773kz
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