Human TNRC6A is an Argonaute-navigator protein for microRNA-mediated gene silencing in the nucleus

RNA

Volumn 19, Issue 1, 2013, Pages 17-35

  Nishi, Kenji ^a   Nishi, Ai ^a   Nagasawa, Tatsuya ^a   Ui Tei, Kumiko ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

Argonaute; microRNA mediated gene silencing; Nuclear export signal; Nuclear localization signal; TNRC6A

Indexed keywords

ARGONAUTE PROTEIN; MICRORNA; PROTEIN; TRINUCLEOTIDE REPEAT CONTAINING GENE 6A PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; GENE MUTATION; GENE SILENCING; HUMAN; HUMAN CELL; NUCLEAR EXPORT SIGNAL; NUCLEAR LOCALIZATION SIGNAL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

AMINO ACID MOTIFS; ARGONAUTE PROTEINS; AUTOANTIGENS; CELL NUCLEUS; GENE SILENCING; HELA CELLS; HUMANS; MICRORNAS; MUTATION; NUCLEAR EXPORT SIGNALS; NUCLEAR LOCALIZATION SIGNALS; NUCLEOCYTOPLASMIC TRANSPORT PROTEINS; RNA-BINDING PROTEINS;

EID: 84871434154     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.034769.112     Document Type: Article

References (62)

1. Afonina E, Stauber R, Pavlakis GN. 1998. The human poly(A)-binding protein 1 shuttles between the nucleus and the cytoplasm. J Biol Chem 273: 13015-13021.
2. Behm-Ansmant I, Rehwinkel J, Doerks T, Stark A, Bork P, Izaurralde E. 2006. mRNA degradation by miRNAs and GW182 requires both CCR4:NOT deadenylase and DCP1:DCP2 decapping complexes. Genes Dev 20: 1885-1898.
3. Bohnsack MT, Czaplinski K, Gorlich D. 2004. Exportin 5 is a RanGTP-dependent dsRNA-binding protein that mediates nuclear export of pre-miRNAs. RNA 10: 185-191.
4. Chekulaeva M, Filipowicz W, Parker R. 2009. Multiple independent domains of dGW182 function in miRNA-mediated repression in Drosophila. RNA 15: 794-803.
5. Chen C, Ridzon DA, Broomer AJ, Zhou Z, Lee DH, Nguyen JT, Barbisin M, Xu NL, Mahuvakar VR, Andersen MR, et al. 2005. Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res 33: e179. doi: 10.1093/nar/gni178.
6. Chen CY, Zheng D, Xia Z, Shyu AB. 2009. Ago-TNRC6 triggers microRNA-mediated decay by promoting two deadenylation steps. Nat Struct Mol Biol 16: 1160-1166.
7. Chi SW, Zang JB, Mele A, Darnell RB. 2009. Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature 460: 479-486.
8. Chu CY, Rana TM. 2006. Translation repression in human cells by microRNA-induced gene silencing requires RCK/p54. PLoS Biol 4: e210. doi: 10.1371/journal.pbio.0040210.
9. Davis LI. 1995. The nuclear pore complex. Annu Rev Biochem 64: 865-896.
10. Ding L, Han M. 2007. GW182 family proteins are crucial for microRNA-mediated gene silencing. Trends Cell Biol 17: 411-416.
11. Ding L, Spencer A, Morita K, Han M. 2005. The developmental timing regulator AIN-1 interacts with miRISCs and may target the argonaute protein ALG-1 to cytoplasmic P bodies in C. elegans. Mol Cell 19: 437-447.
12. Doench JG, Petersen CP, Sharp PA. 2003. siRNAs can function as miRNAs. Genes Dev 17: 438-442.
13. Eulalio A, Tritschler F, Izaurralde E. 2009a. The GW182 protein family in animal cells: New insights into domains required for miRNA-mediated gene silencing. RNA 15: 1433-1442.
14. Eulalio A, Helms S, Fritzsch C, Fauser M, Izaurralde E. 2009b. A C-terminal silencing domain in GW182 is essential for miRNA function. RNA 15: 1067-1077.
15. Eystathioy T, Chan EK, Tenenbaum SA, Keene JD, Griffith K, Fritzler MJ. 2002. A phosphorylated cytoplasmic autoantigen, GW182, associates with a unique population of human mRNAs within novel cytoplasmic speckles. Mol Biol Cell 13: 1338-1351.
16. Eystathioy T, Jakymiw A, Chan EK, Séraphin B, Cougot N, Fritzler MJ. 2003. The GW182 protein colocalizes with mRNA degradation associated proteins hDcp1 and hLSm4 in cytoplasmic GW bodies. RNA 9: 1171-1173.
17. Fabian MR, Mathonnet G, Sundermeier T, Mathys H, Zipprich JT, Svitkin YV, Rivas F, Jinek M, Wohlschlegel J, Doudna JA, et al. 2009. Mammalian miRNA RISC recruits CAF1 and PABP to affect PABP-dependent deadenylation. Mol Cell 35: 868-880.
18. Fornerod M, Ohno M, Yoshida M, Mattaj IW. 1997. CRM1 is an export receptor for leucine-rich nuclear export signals. Cell 90: 1051-1060.
19. Han J, Kim D, Morris KV. 2007. Promoter-associated RNA is required for RNA-directed transcriptional gene silencing in human cells. Proc Natl Acad Sci 104: 12422-12427.
20. Huntzinger E, Braun JE, Heimstädt S, Zekri L, Izaurralde E. 2010. Two PABPC1-binding sites in GW182 proteins promote miRNA-mediated gene silencing. EMBO J 29: 4146-4160.
21. Hwang HW, Wentzel EA, Mendell JT. 2007. A hexanucleotide element directs microRNA nuclear import. Science 315: 97-100.
22. Jakymiw A, Lian S, Eystathioy T, Li S, Satoh M, Hamel JC, Fritzler MJ, Chan EK. 2005. Disruption of GW bodies impairs mammalian RNA interference. Nat Cell Biol 7: 1267-1274.
23. Jeffries CD, Fried HM, Perkins DO. 2011. Nuclear and cytoplasmic localization of neural stem cell microRNAs. RNA 17: 675-686.
24. Jinek M, Fabian MR, Coyle SM, Sonenberg N, Doudna JA. 2010. Structural insights into the human GW182-PABC interaction in microRNA-mediated deadenylation. Nat Struct Mol Biol 17: 238-240.
25. Kim DH, Villeneuve LM, Morris KV, Rossi JJ. 2006. Argonaute-1 directs siRNA-mediated transcriptional gene silencing in human cells. Nat Struct Mol Biol 13: 793-797.
26. Kim DH, Saetrom P, Snove O Jr, Rossi JJ. 2008. MicroRNA-directed transcriptional gene silencing in mammalian cells. Proc Natl Acad Sci 105: 16230-16235.
27. Kozlov G, Safaee N, Rosenauer A, Gehring K. 2010. Structural basis of binding of P-body associated proteins GW182 and Ataxin-2 by the Mlle domain of poly(A)-binding protein. J Biol Chem 285: 13599-13606.
28. Kudo N, Matsumori N, Taoka H, Fujiwara D, Schreiner EP, Wolff B, Yoshida M, Horinouchi S. 1999. Leptomycin B inactivates CRM1/exportin 1 by covalent modification at a cysteine residue in the central conserved region. Proc Natl Acad Sci 96: 9112-9117.
29. Kutay U, Güttinger S. 2005. Leucine-rich nuclear-export signals: Born to be weak. Trends Cell Biol 15: 121-124.
30. Landthaler M, Gaidatzis D, Rothballer A, Chen PY, Soll SJ, Dinic L, Ojo T, Hafner M, Zavolan M, Tuschl T. 2008. Molecular characterization of human Argonaute-containing ribonucleoprotein complexes and their bound target mRNAs. RNA 14: 2580-2596.
31. Lange A, Mills RE, Lange CJ, Stewart M, Devine SE, Corbett AH. 2007. Classical nuclear localization signals: Definition, function, and interaction with importin a. J Biol Chem 282: 5101-5105.
32. Lazzaretti D, Tournier I, Izaurralde E. 2009. The C-terminal domains of human TNRC6A, TNRC6B, and TNRC6C silence bound transcripts independently of Argonaute proteins. RNA 15: 1059-1066.
33. Lian SL, Li S, Abadal GX, Pauley BA, Fritzler MJ, Chan EK. 2009. The C-terminal half of human Ago2 binds to multiple GW-rich regions of GW182 and requires GW182 to mediate silencing. RNA 15: 804-813.
34. Liao JY, Ma LM, Guo YH, Zhang YC, Zhou H, Shao P, Chen YQ, Qu LH. 2010. Deep sequencing of human nuclear and cytoplasmic small RNAs reveals an unexpectedly complex subcellular distribution of miRNAs and tRNA 39 trailers. PLoS ONE 5: e10563. doi:10.1371/journal.pone.0010563.
35. Liu J, Rivas FV, Wohlschlegel J, Yates JR III, Parker R, Hannon GJ. 2005. A role for the P-body component GW182 in microRNA function. Nat Cell Biol 7: 1261-1266.
36. Lund E, Güttinger S, Calado A, Dahlberg JE, Kutay U. 2004. Nuclear export of microRNA precursors. Science 303: 95-98.
37. 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: 185-197.
38. Meister G, Landthaler M, Peters L, Chen PY, Urlaub H, Lührmann R, Tuschl T. 2005. Identification of novel argonaute-associated proteins. Curr Biol 15: 2149-2155.
39. Miyagawa R, Tano K, Mizuno R, Nakamura Y, Ijiri K, Rakwal R, Shibato J, Masuo Y, Mayeda A, Hirose T, et al. 2012. Identification of cis- and trans -acting factors involved in the localization of MALAT-1 noncoding RNA to nuclear speckles. RNA 18: 738-751.
40. Naito Y, Yoshimura J, Morishita S, Ui-Tei K. 2009. siDirect 2.0: Updated software for designing functional siRNA with reduced seed-dependent off-target effect. BMC Bioinformatics 10: 392. doi:10.1186/1471-2105-10-392.
41. Nathans R, Chu CY, Serquina AK, Lu CC, Cao H, Rana TM. 2009. Cellular microRNA and P bodies modulate host-HIV-1 interactions. Mol Cell 34: 696-709.
42. Nishi K, Saigo K. 2007. Cellular internalization of green fluorescent protein fused with herpes simplex virus protein VP22 via a lipid raft-mediated endocytic pathway independent of caveolae and Rho family GTPases but dependent on dynamin and Arf6. J Biol Chem 282: 27503-27517.
43. Okada-Katsuhata Y, Yamashita A, Kutsuzawa K, Izumi N, Hirahara F, Ohno S. 2012. N- and C-terminal Upf1 phosphorylations create binding platforms for SMG-6 and SMG-5:SMG-7 during NMD. Nucleic Acids Res 40: 1251-1266.
44. Politz JC, Hogan EM, Pederson T. 2009. MicroRNAs with a nucleolar location. RNA 15: 1705-1715.
45. Provost P, Dishart D, Doucet J, Frendewey D, Samuelsson B, Rådmark O. 2002. Ribonuclease activity and RNA binding of recombinant human Dicer. EMBO J 21: 5864-5874.
46. Robb GB, Brown KM, Khurana J, Rana TM. 2005. Specific and potent RNAi in the nucleus of human cells. Nat Struct Mol Biol 12: 133-137.
47. Rüdel S, Flatley A, Weinmann L, Kremmer E, Meister G. 2008. A multifunctional human Argonaute2-specific monoclonal antibody. RNA 14: 1244-1253.
48. Su H, Meng S, Lu Y, Trombly MI, Chen J, Lin C, Turk A, Wang X. 2011. Mammalian hyperplastic discs homolog EDD regulates miRNA-mediated gene silencing. Mol Cell 43: 97-109.
49. Taft RJ, Simons C, Nahkuri S, Oey H, Korbie DJ, Mercer TR, Holst J, Ritchie W, Wong JJ, Rasko JE, et al. 2010. Nuclear-localized tiny RNAs are associated with transcription initiation and splice sites in metazoans. Nat Struct Mol Biol 17: 1030-1034.
50. Takimoto K, Wakiyama M, Yokoyama S. 2009. Mammalian GW182 contains multiple Argonaute-binding sites and functions in microRNA-mediated translational repression. RNA 15: 1078-1089.
51. Till S, Lejeune E, Thermann R, Bortfeld M, Hothorn M, Enderle D, Heinrich C, Hentze MW, Ladurner AG. 2007. A conserved motif in Argonaute-interacting proteins mediates functional interactions through the Argonaute PIWI domain. Nat Struct Mol Biol 14: 897-903.
52. Ui-Tei K, Naito Y, Takahashi F, Haraguchi T, Ohki-Hamazaki H, Juni A, Ueda R, Saigo K. 2004. Guidelines for the selection of highly effective siRNA sequences for mammalian and chick RNA interference. Nucleic Acids Res 32: 936-948.
53. Ui-Tei K, Naito Y, Nishi K, Juni A, Saigo K. 2008. Thermodynamic stability and Watson-Crick base pairing in the seed duplex are major determinants of the efficiency of the siRNA-based off-target effect. Nucleic Acids Res 36: 7100-7109.
54. Wakiyama M, Takimoto K, Ohara O, Yokoyama S. 2007. Let-7 microRNA-mediated mRNA deadenylation and translational repression in a mammalian cell-free system. Genes Dev 21: 1857-1862.
55. Weinmann L, Höck J, Ivacevic T, Ohrt T, Mütze J, Schwille P, Kremmer E, Benes V, Urlaub H, Meister G. 2009. Importin 8 is a gene silencing factor that targets argonaute proteins to distinct mRNAs. Cell 136: 496-507.
56. Yamashita A, Chang TC, Yamashita Y, Zhu W, Zhong Z, Chen CY, Shyu AB. 2005. Concerted action of poly(A) nucleases and decapping enzyme in mammalian mRNA turnover. Nat Struct Mol Biol 12: 1054-1063.
57. 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: 3011-3016.
58. Younger ST, Corey DR. 2011. Transcriptional gene silencing in mammalian cells by miRNA mimics that target gene promoters. Nucleic Acids Res 39: 5682-5691.
59. Yoo NJ, Hur SY, Kim MS, Lee JY, Lee SH. 2010. Immunohistochemical analysis of RNA-induced silencing complex-related proteins AGO2 and TNRC6A in prostate and esophageal cancers. APMIS 118: 271-276.
60. Zekri L, Huntzinger E, Heimstädt S, Izaurralde E. 2009. The silencing domain of GW182 interacts with PABPC1 to promote translational repression and degradation of microRNA targets and is required for target release. Mol Cell Biol 29: 6220-6231.
61. Zhang L, Ding L, Cheung TH, Dong MQ, Chen J, Sewell AK, Liu X, Yates JR 3rd, Han M. 2007. Systematic identification of C. elegans miRISC proteins, miRNAs, and mRNA targets by their interactions with GW182 proteins AIN-1 and AIN-2. Mol Cell 28: 598-613.
62. Zipprich JT, Bhattacharyya S, Mathys H, Filipowicz W. 2009. Importance of the C-terminal domain of the human GW182 protein TNRC6C for translational repression. RNA 15: 781-793.