Argonaute and GW182 proteins: An effective alliance in gene silencing

Biochemical Society Transactions

Volumn 41, Issue 4, 2013, Pages 855-860

  Pfaff, Janina ^a,b   Meister, Gunter ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

Argonaute protein; Gene silencing; GW182 protein; MicroRNA (miRNA); RNA interference (RNAi)

Indexed keywords

ARGONAUTE PROTEIN; BINDING PROTEIN; GW182 PROTEIN; MICRORNA; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ARTICLE; GENE FUNCTION; GENE SILENCING; GENETIC CONSERVATION; HUMAN; MESSENGER RNA SYNTHESIS; NONHUMAN; NUCLEOTIDE REPEAT; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; RNA SEQUENCE;

ARGONAUTE PROTEINS; GENE SILENCING; PROTEIN BINDING; RNA;

EID: 84880553183     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20130047     Document Type: Article

References (64)

1. Meister, G. and Tuschl, T. (2004) Mechanisms of gene silencing by double-stranded RNA. Nature 431, 343-349
2. Peters, L. and Meister, G. (2007) Argonaute proteins: mediators of RNA silencing. Mol. Cell 26, 611-623
3. Hutvagner, G. and Simard, M.J. (2008) Argonaute proteins: key players in RNA silencing. Nat. Rev. Mol. Cell Biol. 9, 22-32
4. Krol, J., Loedige, I. and Filipowicz, W. (2010) The widespread regulation of microRNA biogenesis, function and decay. Nat. Rev. Genet. 11, 597-610
5. Bartel, D.P. (2009) MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233
6. Bushati, N. and Cohen, S.M. (2007) microRNA functions. Annu. Rev. Cell Dev. Biol. 23, 175-205
7. Braun, J.E., Huntzinger, E. and Izaurralde, E. (2013) The role of GW182 proteins in miRNA-mediated gene silencing. Adv. Exp. Med. Biol. 768, 147-163
8. 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
9. Ender, C. and Meister, G. (2010) Argonaute proteins at a glance. J. Cell Sci. 123, 1819-1823
10. Siomi, M.C., Sato, K., Pezic, D. and Aravin, A.A. (2011) PIWI-interacting small RNAs: the vanguard of genome defence. Nat. Rev. Mol. Cell Biol. 12, 246-258
11. Tolia, N.H. and Joshua-Tor, L. (2007) Slicer and the argonautes. Nat. Chem. Biol. 3, 36-43
12. Liu, J., Carmell, M.A., Rivas, F.V., Marsden, C.G., Thomson, J.M., Song, J.J., Hammond, S.M., Joshua-Tor, L. and Hannon, G.J. (2004) Argonaute2 is the catalytic engine of mammalian RNAi. Science 305, 1437-1441
13. Meister, G., Landthaler, M., Patkaniowska, A., Dorsett, Y., Teng, G. and Tuschl, T. (2004) Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol. Cell 15, 185-197
14. Jinek, M. and Doudna, J.A. (2009) A three-dimensional view of the molecular machinery of RNA interference. Nature 457, 405-412
15. Kuhn, C.D. and Joshua-Tor, L. (2013) Eukaryotic Argonautes come into focus. Trends Biochem. Sci., doi:10.1016/j.tibs.2013.02.008
16. Schirle, N.T. and MacRae, I.J. (2012) The crystal structure of human Argonaute2. Science 336, 1037-1040
17. Elkayam, E., Kuhn, C.D., Tocilj, A., Haase, A.D., Greene, E.M., Hannon, G.J. and Joshua-Tor, L. (2012) The structure of human argonaute-2 in complex with miR-20a. Cell 150, 100-110
18. Ma, J.B., Ye, K. and Patel, D.J. (2004) Structural basis for overhang-specific small interfering RNA recognition by the PAZ domain. Nature 429, 318-322
19. 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
20. 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
21. Ma, J.B., Yuan, Y.R., Meister, G., Pei, Y., Tuschl, T. and Patel, D.J. (2005) Structural basis for 5-end-specific recognition of guide RNA by the A. fulgidus Piwi protein. Nature 434, 666-670
22. Parker, J.S., Roe, S.M. and Barford, D. (2005) Structural insights into mRNA recognition from a PIWI domain-siRNA guide complex. Nature 434, 663-666
23. 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
24. 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
25. Yuan, Y.R., Pei, Y., Ma, J.B., Kuryavyi, V., Zhadina, M., Meister, G., Chen, H.Y., Dauter, Z., Tuschl, T. and Patel, D.J. (2005) Crystal structure of A. aeolicus Argonaute, a site-specific DNA-guided endoribonuclease, provides insights into RISC-mediated mRNA cleavage. Mol. Cell 19, 405-419
26. Nakanishi, K., Weinberg, D.E., Bartel, D.P. and Patel, D.J. (2012) Structure of yeast Argonaute with guide RNA. Nature 486, 368-374
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., doi:10.1038/nsmb.2577
28. Eystathioy, T., Chan, E.K., Tenenbaum, S.A., Keene, J.D., Griffith, K. and Fritzler, M.J. (2002) A phosphorylated cytoplasmic autoantigen, GW182, associates with a unique population of human mRNAs within novel cytoplasmic speckles. Mol. Biol. Cell 13, 1338-1351
29. Eystathioy, T., Jakymiw, A., Chan, E.K., Seraphin, B., Cougot, N. and Fritzler, M.J. (2003) The GW182 protein colocalizes with mRNA degradation associated proteins hDcp1 and hLSm4 in cytoplasmic GW bodies. RNA 9, 1171-1173
30. Sen, G.L. and Blau, H.M. (2005) Argonaute 2/RISC resides in sites of mammalian mRNA decay known as cytoplasmic bodies. Nat. Cell Biol. 7, 633-636
31. Ding, L., Spencer, A., Morita, K. and 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
32. Rehwinkel, J., Behm-Ansmant, I., Gatfield, D. and Izaurralde, E. (2005) A crucial role for GW182 and the DCP1:DCP2 decapping complex in miRNA-mediated gene silencing. RNA 11, 1640-1647
33. Liu, J., Rivas, F.V., Wohlschlegel, J., Yates, 3rd, J.R., Parker, R. and Hannon, G.J. (2005) A role for the P-body component GW182 in microRNA function. Nat. Cell Biol. 7, 1161-1166
34. Liu, J., Valencia-Sanchez, M.A., Hannon, G.J. and Parker, R. (2005) MicroRNA-dependent localization of targeted mRNAs to mammalian P-bodies. Nat. Cell Biol. 7, 719-723
35. Jakymiw, A., Lian, S., Eystathioy, T., Li, S., Satoh, M., Hamel, J.C., Fritzler, M.J. and Chan, E.K. (2005) Disruption of GW bodies impairs mammalian RNA interference. Nat. Cell Biol. 7, 1267-1274
36. Meister, G., Landthaler, M., Peters, L., Chen, P.Y., Urlaub, H., Luhrmann, R. and Tuschl, T. (2005) Identification of novel argonaute-associated proteins. Curr. Biol. 15, 2149-2155
37. Huntzinger, E. and Izaurralde, E. (2011) Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat. Rev. Genet. 12, 99-110
38. Su, V. and Lau, A.F. (2009) Ubiquitin-like and ubiquitin-associated domain proteins: significance in proteasomal degradation. Cell. Mol. Life Sci. 66, 2819-2833
39. Clery, A., Blatter, M. and Allain, F.H. (2008) RNA recognition motifs: boring? Not quite. Curr. Opin. Struct. Biol. 18, 290-298
40. Eulalio, A., Tritschler, F., Buttner, R., Weichenrieder, O., Izaurralde, E. and Truffault, V. (2009) The RRM domain in GW182 proteins contributes to miRNA-mediated gene silencing. Nucleic Acids Res. 37, 2974-2983
41. Behm-Ansmant, I., Rehwinkel, J., Doerks, T., Stark, A., Bork, P. and Izaurralde, E. (2006) mRNA degradation by miRNAs and GW182 requires both CCR4:NOT deadenylase and DCP1:DCP2 decapping complexes. Genes Dev. 20, 1885-1898
42. Lazzaretti, D., Tournier, I. and Izaurralde, E. (2009) The C-terminal domains of human TNRC6A, TNRC6B, and TNRC6C silence bound transcripts independently of Argonaute proteins. RNA 15, 1059-1066
43. Chekulaeva, M., Mathys, H., Zipprich, J.T., Attig, J., Colic, M., Parker, R. and Filipowicz, W. (2011) miRNA repression involves GW182-mediated recruitment of CCR4-NOT through conserved W-containing motifs. Nat. Struct. Mol. Biol. 18, 1218-1226
44. Fabian, M.R., Mathonnet, G., Sundermeier, T., Mathys, H., Zipprich, J.T., Svitkin, Y.V., Rivas, F., Jinek, M., Wohlschlegel, J., Doudna, J.A. et al. (2009) Mammalian miRNA RISC recruits CAF1 and PABP to affect PABP-dependent deadenylation. Mol. Cell 35, 868-880
45. Braun, J.E., Huntzinger, E., Fauser, M. and Izaurralde, E. (2011) GW182 proteins directly recruit cytoplasmic deadenylase complexes to miRNA targets. Mol. Cell 44, 120-133
46. Fabian, M.R., Cieplak, M.K., Frank, F., Morita, M., Green, J., Srikumar, T., Nagar, B., Yamamoto, T., Raught, B., Duchaine, T.F. et al. (2011) miRNA-mediated deadenylation is orchestrated by GW182 through two conserved motifs that interact with CCR4-NOT. Nat. Struct. Mol. Biol. 18, 1211-1217
47. Till, S., Lejeune, E., Thermann, R., Bortfeld, M., Hothorn, M., Enderle, D., Heinrich, C., Hentze, M.W. and Ladurner, A.G. (2007) A conserved motif in Argonaute-interacting proteins mediates functional interactions through the Argonaute PIWI domain. Nat. Struct. Mol. Biol. 14, 897-903
48. Takimoto, K., Wakiyama, M. and Yokoyama, S. (2009) Mammalian GW182 contains multiple Argonaute-binding sites and functions in microRNA-mediated translational repression. RNA 15, 1078-1089
49. Eulalio, A., Helms, S., Fritzsch, C., Fauser, M. and Izaurralde, E. (2009) A C-terminal silencing domain in GW182 is essential for miRNA function. RNA 15, 1067-1077
50. Lian, S.L., Li, S., Abadal, G.X., Pauley, B.A., Fritzler, M.J. and Chan, E.K. (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
51. Braun, J.E., Truffault, V., Boland, A., Huntzinger, E., Chang, C.T., Haas, G., Weichenrieder, O., Coles, M. and Izaurralde, E. (2012) A direct interaction between DCP1 and XRN1 couples mRNA decapping to 5-exonucleolytic degradation. Nat. Struct. Mol. Biol. 19, 1324-1331
52. Diella, F., Haslam, N., Chica, C., Budd, A., Michael, S., Brown, N.P., Trave, G. and Gibson, T.J. (2008) Understanding eukaryotic linear motifs and their role in cell signaling and regulation. Front. Biosci. 13, 6580-6603
53. Fromm, S.A., Truffault, V., Kamenz, J., Braun, J.E., Hoffmann, N.A., Izaurralde, E. and Sprangers, R. (2012) The structural basis of Edc3-and Scd6-mediated activation of the Dcp1:Dcp2 mRNA decapping complex. EMBO J. 31, 279-290
54. Baillat, D. and Shiekhattar, R. (2009) Functional dissection of the human TNRC6 (GW182-related) family of proteins. Mol. Cell. Biol. 29, 4144-4155
55. El-Shami, M., Pontier, D., Lahmy, S., Braun, L., Picart, C., Vega, D., Hakimi, M.A., Jacobsen, S.E., Cooke, R. and Lagrange, T. (2007) Reiterated WG/GW motifs form functionally and evolutionarily conserved ARGONAUTE-binding platforms in RNAi-related components. Genes Dev. 21, 2539-2544
56. Zielezinski, A. and Karlowski, W.M. (2011) Agos: a universal web tool for GW Argonaute-binding domain prediction. Bioinformatics 27, 1318-1319
57. Verdel, A., Jia, S., Gerber, S., Sugiyama, T., Gygi, S., Grewal, S.I. and Moazed, D. (2004) RNAi-mediated targeting of heterochromatin by the RITS complex. Science 303, 672-676
58. Partridge, J.F., DeBeauchamp, J.L., Kosinski, A.M., Ulrich, D.L., Hadler, M.J. and Noffsinger, V.J. (2007) Functional separation of the requirements for establishment and maintenance of centromeric heterochromatin. Mol. Cell 26, 593-602
59. Brodersen, P. and Voinnet, O. (2006) The diversity of RNA silencing pathways in plants. Trends Genet. 22, 268-280
60. He, X.J., Hsu, Y.F., Zhu, S., Wierzbicki, A.T., Pontes, O., Pikaard, C.S., Liu, H.L., Wang, C.S., Jin, H. and Zhu, J.K. (2009) An effector of RNA-directed DNA methylation in arabidopsis is an ARGONAUTE 4-and RNA-binding protein. Cell 137, 498-508
61. Bednenko, J., Noto, T., DeSouza, L.V., Siu, K.W., Pearlman, R.E., Mochizuki, K. and Gorovsky, M.A. (2009) Two GW repeat proteins interact with Tetrahymena thermophila argonaute and promote genome rearrangement. Mol. Cell. Biol. 29, 5020-5030
62. Gibbings, D., Leblanc, P., Jay, F., Pontier, D., Michel, F., Schwab, Y., Alais, S., Lagrange, T. and Voinnet, O. (2012) Human prion protein binds Argonaute and promotes accumulation of microRNA effector complexes. Nat. Struct. Mol. Biol. 19, 517-524, S511
63. Azevedo, J., Garcia, D., Pontier, D., Ohnesorge, S., Yu, A., Garcia, S., Braun, L., Bergdoll, M., Hakimi, M.A., Lagrange, T. et al. (2010) Argonaute quenching and global changes in Dicer homeostasis caused by a pathogen-encoded GW repeat protein. Genes Dev. 24, 904-915
64. Giner, A., Lakatos, L., Garcia-Chapa, M., Lopez-Moya, J.J. and Burgyan, J. (2010) Viral protein inhibits RISC activity by argonaute binding through conserved WG/GW motifs. PLoS Pathog. 6, e1000996