Synthetic pre-microRNAs reveal dual-strand activity of miR-34a on TNF-α

RNA

Volumn 20, Issue 1, 2014, Pages 61-75

  Guennewig, Boris ^a,c   Roos, Martina ^a   Dogar, Afzal M ^a   Gebert, Luca F R ^a   Zagalak, Julian A ^a   Vongrad, Valentina ^b   Metzner, Karin J ^b   Hall, Jonathan ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^c GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

3p strand; Macrophages; MiR 34a; MiRNA biogenesis; Pre miRNA; TNF

Indexed keywords

DICER; LIPOPOLYSACCHARIDE; MICRORNA; MICRORNA 34A; MICRORNA 34A 3P; MICRORNA 34A 5P; RNA PRECURSOR; SIRTUIN 1; SYNTHETIC PRECURSOR MICRORNA; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; MACROPHAGE ACTIVATION; PRIORITY JOURNAL; RNA PROCESSING; RNA STRUCTURE; SIGNAL TRANSDUCTION;

EID: 84890780224     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.038968.113     Document Type: Article

References (82)

1. Almeida MI, Nicoloso MS, Zeng L, Ivan C, Spizzo R, Gafà R, Xiao L, Zhang X, Vannini I, Fanini F, et al. 2012. Strand-specific miR-28-5p and miR-28-3p have distinct effects in colorectal cancer cells. Gastroenterology 142: 886-896.
2. Azuma-Mukai A, Oguri H, Mituyama T, Qian ZR, Asai K, Siomi H, Siomi MC. 2008. Characterization of endogenous human Argonautes and their miRNA partners in RNA silencing. Proc Natl Acad Sci 105: 7964-7969.
3. Bartel DP. 2009. MicroRNAs: Target recognition and regulatory functions. Cell 136: 215-233.
4. Betel D, Koppal A, Agius P, Sander C, Leslie C. 2010. Comprehensive modeling of microRNA targets predicts functional non-conserved and non-canonical sites. Genome Biol 11: R90.
5. Beutler B, Greenwald D, Hulmes JD, Chang M, Pan YC, Mathison J, Ulevitch R, Cerami A. 1985. Identity of tumour necrosis factor and the macrophage-secreted factor cachectin. Nature 316: 552-554.
6. Birikh KR, Heaton PA, Eckstein F. 1997. The structure, function and application of the hammerhead ribozyme. Eur J Biochem 245: 1-16.
7. Birmingham A, Anderson E, Sullivan K, Reynolds A, Boese Q, Leake D, Karpilow J, Khvorova A. 2007. A protocol for designing siRNAs with high functionality and specificity. Nat Protoc 2: 2068-2078.
8. Byrd AE, Aragon IV, Brewer JW. 2012. MicroRNA-30c-2 limits expression of proadaptive factor XBP1 in the unfolded protein response. J Cell Biol 196: 689-698.
9. Calin GA. 2004. Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proc Natl Acad Sci 101: 2999-3004.
10. Chen F, Hu S-J. 2012. Effect of microRNA-34a in cell cycle, differentiation, and apoptosis: A review. J Biochem Mol Toxicol 26: 79-86.
11. Chiang HR, Schoenfeld LW, Ruby JG, Auyeung VC, Spies N, Baek D, Johnston WK, Russ C, Luo S, Babiarz JE, et al. 2010. Mammalian microRNAs: Experimental evaluation of novel and previously annotated genes. Genes Dev 24: 992-1009.
12. Davies BP, Arenz C. 2008. A fluorescence probe for assaying micro RNA maturation. Bioorg Med Chem 16: 49-55.
13. Denli AM, Tops BB, Plasterk RH, Ketting RF, Hannon GJ. 2004. Processing of primary microRNAs by the Microprocessor complex. Nature 432: 231-235.
14. Djuranovic S, Nahvi A, Green R. 2012. miRNA-mediated gene silencing by translational repression followed by mRNA deadenylation and decay. Science 336: 237-240.
15. Doench JG, Petersen CP, Sharp PA. 2003. siRNAs can function as miRNAs. Genes Dev 17: 438-442.
16. Dogar AM, Towbin H, Hall J. 2011. Suppression of latent transforming growth factor (TGF)-1 restores growth inhibitory TGF- signaling through microRNAs. J Biol Chem 286: 16447-16458.
17. Esau C, Davis S, Murray SF, Yu XX, Pandey SK. 2006. miR-122 regulation of lipid metabolism revealed by in vivo antisense targeting. Cell Metab 3: 87-98.
18. 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: 235-240.
19. Griffiths-Jones S. 2006. miRBase: MicroRNA sequences, targets and gene nomenclature. Nucleic Acids Res 34: D140-D144.
20. Griffiths-Jones S, Hui JHL, Marco A, Ronshaugen M. 2011. MicroRNA evolution by arm switching. EMBO Rep 12: 172-177.
21. Grimson A, Srivastava M, Fahey B, Woodcroft BJ, Chiang HR, King N, Degnan BM, Rokhsar DS, Bartel DP. 2008. Early origins and evolution of microRNAs and Piwi-interacting RNAs in animals. Nature 455: 1193-1197.
22. Guled M, Lahti L, Lindholm PM, Salmenkivi K, Bagwan I, Nicholson AG, Knuutila S. 2009. CDKN2A, NF2, and JUN are dysregulated among other genes by miRNAs in malignant mesothelioma - a miRNA microarray analysis. Genes Chromosomes Cancer 48: 615-623.
23. Gurtan AM, Lu V, Bhutkar A, Sharp PA. 2012. In vivo structure-function analysis of human Dicer reveals directional processing of precursor miRNAs. RNA 8: 1116-1122.
24. Han J, Lee Y, Yeom K-H, Kim Y-K, Jin H, Kim VN. 2004. The Drosha-DGCR8 complex in primary microRNA processing. Genes Dev 18: 3016-3027.
25. Helm M, Brule H, Giege R, Florentz C. 1999. More mistakes by T7 RNA polymerase at the 5 ends of in vitro-transcribed RNAs. RNA 5: 618-621.
26. Hu H, Yan Z, Xu Y, Hu H, Menzel C, Zhou Y, Chen W, Khaitovich P. 2009. Sequence features associated with microRNA strand selection in humans and flies. BMC Genomics 10: 413.
27. Hutvágner G, McLachlan J, Pasquinelli AE, Bálint E, Tuschl T, Zamore PD. 2001. A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science 293: 834-838.
28. Ivanovska I, Ball AS, Diaz RL, Magnus JF, Kibukawa M, Schelter JM, Kobayashi SV, Lim L, Burchard J, Jackson AL, et al. 2008. MicroRNAs in the miR-106b family regulate p21/CDKN1A and promote cell cycle progression. Mol Cell Biol 28: 2167-2174.
29. Jiang L, Huang Q, Zhang S, Zhang Q, Chang J, Qiu X, Wang E. 2010. Hsa-miR-125a-3p and hsa-miR-125a-5p are downregulated in non-small cell lung cancer and have inverse effects on invasion and migration of lung cancer cells. BMC Cancer 10: 318.
30. Jiang P, Liu R, Zheng Y, Liu X, Chang L, Xiong S, Chu Y. 2012. MiR-34a inhibits lipopolysaccharide-induced inflammatory response through targeting Notch1 in murine macrophages. Exp Cell Res 318: 1175-1184.
31. Khvorova A, Reynolds A, Jayasena SD. 2003. Functional siRNAs and miRNAs exhibit strand bias. Cell 115: 209-216.
32. Kim S, Lee UJ, Kim MN, Lee E-J, Kim JY, Lee MY, Choung S, Kim YJ, Choi Y-C. 2008. MicroRNA miR-199a regulates the MET protooncogene and the downstream extracellular signal-regulated kinase 2 (ERK2). J Biol Chem 283: 18158-18166.
33. Koscianska E, Starega-Roslan J, Krzyzosiak WJ. 2011. The role of Dicer protein partners in the processing of microRNA precursors. PLoS One 6: E28548.
34. Krol J, Loedige I, Filipowicz W. 2010. The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet 11: 597-610.
35. Kuchenbauer F, Mah SM, Heuser M, McPherson A, Rüschmann J, Rouhi A, Berg T, Bullinger L, Argiropoulos B, Morin RD, et al. 2011. Comprehensive analysis of mammalian miRNA species and their role in myeloid cells. Blood 118: 3350-3358.
36. Landgraf P, Rusu M, Sheridan R, Sewer A, Iovino N, Aravin A, Pfeffer S, Rice A, Kamphorst AO, Landthaler M, et al. 2007. A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 129: 1401-1414.
37. Lau P-W, Guiley KZ, De N, Potter CS, Carragher B, Macrae IJ. 2012. The molecular architecture of human Dicer. Nat Struct Mol Biol 19: 436-440.
38. Lee HY, Doudna JA. 2012. TRBP alters human precursor microRNA processing in vitro. RNA 18: 2012-2019.
39. Lindsay MA. 2008. microRNAs and the immune response. Trends Immunol 29: 343-351.
40. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-C(T) method. Methods 25: 402-408.
41. López JA, Alvarez-Salas LM. 2011. Differential effects of miR-34c-3p and miR-34c-5p on SiHa cells proliferation apoptosis, migration and invasion. Biochem Biophys Res Commun 409: 513-519.
42. Lund E, Güttinger S, Calado A, Dahlberg JE, Kutay U. 2004. Nuclear export of microRNA precursors. Science 303: 95-98.
43. 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.
44. Macrae IJ, Li F, Zhou K, Cande WZ, Doudna JA. 2006. Structure of Dicer and mechanistic implications for RNAi. Cold Spring Harb Symp Quant Biol 71: 73-80.
45. Macrae IJ, Ma E, Zhou M, Robinson CV, Doudna JA. 2008. In vitro reconstitution of the human RISC-loading complex. Proc Natl Acad Sci 105: 512-517.
46. Marco A, Macpherson JI, Ronshaugen M, Griffiths-Jones S. 2012. MicroRNAs from the same precursor have different targeting properties. Silence 3: 8.
47. Mathonnet G, Fabian MR, Svitkin YV, Parsyan A, Huck L, Murata T, Biffo S, Merrick WC, Darzynkiewicz E, Pillai RS, et al. 2007. MicroRNA inhibition of translation initiation in vitro by targeting the cap-binding complex eIF4F. Science 317: 1764-1767.
48. McManus MT, Petersen CP, Haines BB, Chen J, Sharp PA. 2002. Gene silencing using micro-RNA designed hairpins. RNA 8: 842-850.
49. Mestdagh P, Van Vlierberghe P, De Weer A, Muth D, Westermann F, Speleman F, Vandesompele J. 2009. A novel and universal method for microRNA RT-qPCR data normalization. Genome Biol 10: R64.
50. Milligan JF, Uhlenbeck OC. 1989. Synthesis of small RNAs using T7 RNA polymerase. Methods Enzymol 180: 51-62.
51. Montag J, Hitt R, Opitz L, Schulz-Schaeffer WJ, Hunsmann G, Motzkus D. 2009. Upregulation of miRNA hsa-miR-342-3p in experimental and idiopathic prion disease. Mol Neurodegener 4: 36.
52. Newman MA, Mani V, Hammond SM. 2011. Deep sequencing of microRNA precursors reveals extensive 3 end modification. RNA 17: 1795-1803.
53. Niederer F, Ospelt C, Brentano F, Hottiger MO, Gay RE, Gay S, Detmar M, Kyburz D. 2011a. SIRT1 overexpression in the rheumatoid arthritis synovium contributes to proinflammatory cytokine production and apoptosis resistance. Ann Rheum Dis 70: 1866-1873.
54. Niederer F, Trenkmann M, Ospelt C, Karouzakis E, Neidhart M, Stanczyk J, Kolling C, Gay RE, Detmar M, Gay S, et al. 2011b. Downregulation of microRNA-34a in rheumatoid arthritis synovial fibroblasts promotes apoptosis resistance. Arthritis Rheum 64: 1771-1779.
55. Okamura K, Balla S, Martin R, Liu N, Lai EC. 2008a. Two distinct mechanisms generate endogenous siRNAs from bidirectional transcription in Drosophila melanogaster. Nat Struct Mol Biol 15: 581-590.
56. Okamura K, Phillips MD, Tyler DM, Duan H, Chou Y-t, Lai EC. 2008b. The regulatory activity of microRNA species has substantial influence on microRNA and 3 UTR evolution. Nat Struct Mol Biol 15: 354-363.
57. Packer AN, Xing Y, Harper SQ, Jones L, Davidson BL. 2008. The bifunctional microRNA miR-9/miR-9 regulates REST and CoREST and is downregulated in Huntington's disease. J Neurosci 28: 14341-14346.
58. Park J-E, Heo I, Tian Y, Simanshu DK, Chang H, Jee D, Patel DJ, Kim VN. 2011. Dicer recognizes the 5 end of RNA for efficient and accurate processing. Nature 475: 201-205.
59. Peltier HJ, Latham GJ. 2008. Normalization of microRNA expression levels in quantitative RT-PCR assays: Identification of suitable reference RNA targets in normal and cancerous human solid tissues. RNA 14: 844-852.
60. Pradère U, Brunschweiger A, Gebert LFR, Lucic M, Roos M, Hall J. 2013. Chemical synthesis of mono-and bis-labeled premicroRNAs. Angew Chem Int Ed doi: 10.1002/anie.201304986.
61. Raabe T, Bukrinsky M, Currie RA. 1998. Relative contribution of transcription and translation to the induction of tumor necrosis factor- by lipopolysaccharide. J Biol Chem 273: 974-980.
62. Ro S, Park C, Young D, Sanders KM, Yan W. 2007. Tissue-dependent paired expression of miRNAs. Nucleic Acids Res 35: 5944-5953.
63. Ruby JG, Stark A, Johnston WK, Kellis M, Bartel DP, Lai EC. 2007. Evolution, biogenesis, expression, and target predictions of a substantially expanded set of Drosophila microRNAs. Genome Res 17: 1850-1864.
64. Sakurai K, Furukawa C, Haraguchi T, Inada K, Shiogama K, Tagawa T, Fujita S, Ueno Y, Ogata A, Ito M, et al. 2011. MicroRNAs miR-199a-5p and-3p target the Brm subunit of SWI/SNF to generate a doublenegative feedback loop in a variety of human cancers. Cancer Res 71: 1680-1689.
65. Schwarz DS, Hutvágner G, Du T, Xu Z, Aronin N, Zamore PD. 2003. Asymmetry in the assembly of the RNAi enzyme complex. Cell 115: 199-208.
66. Shan SW, Lee DY, Deng Z, Shatseva T, Jeyapalan Z, Du WW, Zhang Y, Xuan JW, Yee S-P, Siragam V, et al. 2009. MicroRNA MiR-17 retards tissue growth and represses fibronectin expression. Nat Cell Biol 11: 1031-1038.
67. Shiba Y, Masuda H, Watanabe N, Ego T, Takagaki K, Ishiyama K, Ohgi T, Yano J. 2007. Chemical synthesis of a very long oligoribonucleotide with 2-cyanoethoxymethyl (CEM) as the 2-O-protecting group: Structural identification and biological activity of a synthetic 110mer precursor-microRNA candidate. Nucleic Acids Res 35: 3287-3296.
68. Siolas D, Lerner C, Burchard J, Ge W, Linsley PS, Paddison PJ, Hannon GJ, Cleary MA. 2005. Synthetic shRNAs as potent RNAi triggers. Nat Biotechnol 23: 227-231.
69. Starega-Roslan J, Krol J, Koscianska E, Kozlowski P, Szlachcic WJ, Sobczak K, Krzyzosiak WJ. 2011. Structural basis of microRNA length variety. Nucleic Acids Res 39: 257-268.
70. Sundaram P, Hultine S, Smith LM, Dews M, Fox JL, Biyashev D, Schelter JM, Huang Q, Cleary MA, Volpert OV, et al. 2011. p53-responsive miR-194 inhibits thrombospondin-1 and promotes angiogenesis in colon cancers. Cancer Res 71: 7490-7501.
71. Terasawa K, Shimizu K, Tsujimoto G. 2011. Synthetic pre-miRNAbased shRNA as potent RNAi triggers. J Nucleic Acids 2011: 131579.
72. Tsang WP, Kwok TT. 2009. The miR-18a microRNA functions as a potential tumor suppressor by targeting on K-Ras. Carcinogenesis 30: 953-959.
73. Uchino K, Takeshita F, Takahashi R-u, Kosaka N, Fujiwara K, Naruoka H, Sonoke S, Yano J, Sasaki H, Nozawa S, et al. 2013. Therapeutic effects of microRNA-582-5p and-3p on the inhibition of bladder cancer progression. Mol Ther 21: 610-619.
74. 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.
75. Walsh G. 2010. Biopharmaceutical benchmarks 2010. Nat Biotechnol 28: 917-924.
76. Wotschofsky Z, Meyer HA, Jung M, Fendler A, Wagner I, Stephan C, Busch J, Erbersdobler A, Disch AC, Mollenkopf HJ, et al. 2011.
77. Reference genes for the relative quantification of microRNAs in renal cell carcinomas and their metastases. Anal Biochem 417: 233-241.
78. Wu H, Ye C, Ramirez D, Manjunath N. 2009. Alternative processing of primary microRNA transcripts by Drosha generates 5 end variation of mature microRNA. PLoS One 4: E7566.
79. Yamakuchi M, Ferlito M, Lowenstein CJ. 2008. miR-34a repression of SIRT1 regulates apoptosis. Proc Natl Acad Sci 105: 13421-13426.
80. Yang J-S, Phillips MD, Betel D, Mu P, Ventura A, Siepel AC, Chen KC, Lai EC. 2011. Widespread regulatory activity of vertebrate microRNA species. RNA 17: 312-326.
81. 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.
82. Zhou H, Huang X, Cui H, Luo X, Tang Y, Chen S, Wu L, Shen N. 2010. miR-155 and its star-form partner miR-155 cooperatively regulate type I interferon production by human plasmacytoid dendritic cells. Blood 116: 5885-5894.