Selective autophagy degrades DICER and AGO2 and regulates miRNA activity

Nature Cell Biology

Volumn 14, Issue 12, 2012, Pages 1314-1321

  Gibbings, Derrick ^a,b   Mostowy, Serge ^c,d,e,f   Jay, Florence ^a   Schwab, Yannick ^g   Cossart, Pascale ^c,d,e   Voinnet, Olivier ^a,h  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF OTTAWA   (Canada)

^c INSTITUT PASTEUR   (France)

^d INSERM   (France)

^e USC2020 Paris   (France)

^f IMPERIAL COLLEGE LONDON   (United Kingdom)

^g CNRS   (France)

^h INST DE BIOL MOLEC DES PLANTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE 2 PROTEIN; CELL PROTEIN; DICER; MESSENGER RNA; MICRORNA; PROTEIN NDP52; UNCLASSIFIED DRUG;

ARTICLE; AUTOPHAGOSOME; CONTROLLED STUDY; DICER GENE; GENE EXPRESSION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; RNA DEGRADATION; SELECTIVE AUTOPHAGY; TRANSCRIPTION REGULATION;

ARGONAUTE PROTEINS; AUTOPHAGY; CELL LINE; CELL LINE, TUMOR; HELA CELLS; HUMANS; IMMUNOPRECIPITATION; MICRORNAS; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; NUCLEAR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RIBONUCLEASE III;

EUKARYOTA;

EID: 84870601009     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2611     Document Type: Article

References (50)

1. Kim, V. N., Han, J. & Siomi, M. C. Biogenesis of small RNAs in animals. Nat. Rev. Mol. Cell Biol. 10, 126-39 (2009).
2. Krol, J., Loedige, I. & Filipowicz, W. The widespread regulation of microRNA biogenesis, function and decay. Nat. Rev. Gene. 11, 597-610 (2010).
3. Siomi, H. & Siomi, M. C. Post transcriptional regulation of microRNA biogenesis in animals. Mol. Cell 38, 323-32 (2010).
4. Eulalio, A., Huntzinger, E. & Izaurralde, E. GW182 interaction with Argonaute is essential for miRNA-mediated translational repression and mRNA decay. Nat. Struct. Mol. Biol. 15, 346-53 (2008). (Pubitemid 351483394)
5. Bazzini, A. A., Lee, M. T. & Giraldez, A. J. Ribosome pro-ling shows that miR-430 reduces translation before causing mRNA decay in zebra-sh. Science 336, 233-237 (2012).
6. Ameres, S. L. et al. Target RNA-directed trimming and tailing of small silencing RNAs. Science 328, 1534-9 (2010).
7. Chatterjee, S. & Grosshans, H. Active turnover modulates mature microRNA activity in Caenorhabditis elegans. Nature 461, 546-9 (2009).
8. Johnston, M., Geoffroy, M. C., Sobala, A., Hay, R. & Hutvagner, G. HSP90 protein stabilizes unloaded argonaute complexes and microscopic P-bodies in human cells. Mol. Biol. Cell 21, 1462-9 (2010).
9. Mayr, C. & Bartel, D. P. Widespread shortening of 30UTRs by alternative cleavage and polyadenylation activates oncogenes in cancer cells. Cell 138, 673-84 (2009).
10. Vaucheret, H., Vazquez, F., Crete, P. & Bartel, D. P. The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development. Genes Dev. 18, 1187-97 (2004). (Pubitemid 38669039)
11. Mizushima, N. & Komatsu, M. Autophagy: renovation of cells and tissues. Cell 147, 728-41 (2011).
12. Pankiv, S. et al. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J. Biol. Chem. 282, 24131-45 (2007).
13. Thurston, T. L., Wandel, M. P., von Muhlinen, N., Foeglein, A. & Randow, F. Galectin 8 targets damaged vesicles for autophagy to defend cells against bacterial invasion. Nature 482, 414-8 (2012).
14. Shaid, S., Brandts, C. H., Serve, H. & Dikic, I. Ubiquitination and selective autophagy. Cell Death Diff. http://dx.doi.org/10.1038 (2012).
15. Watanabe, Y. & Tanaka, M. p62/SQSTM1 in autophagic clearance of a nonubiquitylated substrate. J. Cell Sci. 124, 2692-701 (2011).
16. Gibbings, D. J., Ciaudo, C., Erhardt, M. & Voinnet, O. Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat. Cell Biol. 11, 1143-9 (2009).
17. Haase, A. D. et al. TRBP, a regulator of cellular PKR and HIV-1 virus expression, interacts with Dicer and functions in RNA silencing. EMBO Rep. 6, 961-7 (2005). (Pubitemid 41521952)
18. Lee, Y. S. et al. Silencing by small RNAs is linked to endosomal traf-cking. Nat. Cell Biol. 11, 1150-6 (2009).
19. Gibbings, D. & Voinnet, O. Control of RNA silencing and localization by endolysosomes. Trends Cell Biol. 20, 491-501 (2010).
20. Friend, K. et al. A conserved PUF-Ago-eEF1A complex attenuates translation elongation. Nat. Struct. Mol. Biol. 19, 176-83 (2012).
21. Pare, J. M. et al. Hsp90 regulates the function of argonaute 2 and its recruitment to stress granules and P-bodies. Mol. Biol. Cell 20, 3273-84 (2009).
22. Liu, J., Valencia-Sanchez, M. A., Hannon, G. J. & Parker, R. MicroRNA-dependent localization of targeted mRNAs to mammalian P-bodies. Nat. Cell Biol. 7, 719-23 (2005). (Pubitemid 40975754)
23. Mizushima, N., Yoshimori, T. & Levine, B. Methods in mammalian autophagy research. Cell 140, 313-26 (2010).
24. Marzella, L., Ahlberg, J. & Glaumann, H. Isolation of autophagic vacuoles from rat liver: morphological and biochemical characterization. J. Cell Biol. 93, 144-54 (1982). (Pubitemid 12117051)
25. Di, Y. et al. HCC-associated protein HCAP1, a variant of GEMIN4, interacts with zincinger proteins. J. Biochem. 133, 713-8 (2003). (Pubitemid 36898642)
26. Meister, G. et al. Identi-cation of novel argonaute-associated proteins. Curr. Biol. 15, 2149-55 (2005).
27. Mourelatos, Z. et al. miRNPs: a novel class of ribonucleoproteins containing numerous microRNAs. Genes Dev. 16, 720-8 (2002). (Pubitemid 34274041)
28. Gantier, M. P. et al. Analysis of microRNA turnover in mammalian cells following Dicer1 ablation. Nucleic Acids Res. 39, 5692-703 (2011).
29. Chendrimada, T. P. et al. TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing. Nature 436, 740-4 (2005). (Pubitemid 41117280)
30. Sakurai, K. et al. A role for human Dicer in pre-RISC loading of siRNAs. Nucleic Acids Res. 39, 1510-25 (2011).
31. Noland, C. L., Ma, E. & Doudna, J. A. siRNA repositioning for guide strand selection by human Dicer complexes. Mol. Cell 43, 110-21 (2011).
32. Iwasaki, S. et al. Hsc70/Hsp90 chaperone machinery mediates ATP-dependent RISC loading of small RNA duplexes. Mol. Cell 39, 292-9 (2010).
33. Mamane, Y., Petroulakis, E., LeBacquer, O. & Sonenberg, N. mTOR, translation initiation and cancer. Oncogene 25, 6416-22 (2006). (Pubitemid 44582285)
34. Doench, J. G. & Sharp, P. A. Specificity of microRNA target selection in translational repression. Genes Dev. 18, 504-11 (2004). (Pubitemid 38372808)
35. Slack, F. let-7 microRNA reduces tumor growth. Cell Cycle 8, 1823 (2009).
36. Obad, S. et al. Silencing of microRNA families by seed-targeting tiny LNAs. Nat. Genet. 43, 371-8 (2011).
37. Csorba, T., Lozsa, R., Hutvagner, G. & Burgyan, J. Polerovirus protein P0 prevents the assembly of small RNA-containing RISC complexes and leads to degradation of ARGONAUTE1. Plant J. Cell Mol. Biol. 62, 463-72 (2010).
38. Derrien, B. et al. Degradation of the antiviral component ARGONAUTE1 by the autophagy pathway. Proc. Natl Acad. Sci. USA 109, 15942-15946 (2012).
39. Wander, S. A., Hennessy, B. T. & Slingerland, J. M. Next-generation mTOR inhibitors in clinical oncology: how pathway complexity informs therapeutic strategy. J. Clin. Inv. 121, 1231-41 (2011).
40. Lu, J. et al. MicroRNA expression pro-les classify human cancers. Nature 435, 834-8 (2005). (Pubitemid 40839735)
41. Rudel, S., Flatley, A., Weinmann, L., Kremmer, E. & Meister, G. A multifunctional human Argonaute2-specific monoclonal antibody. RNA 14, 1244-53 (2008). (Pubitemid 351717503)
42. Eystathioy, T. et al. A phosphorylated cytoplasmic autoantigen, GW182, associates with a unique population of human mRNAs within novel cytoplasmic speckles. Mol. Biol. Cell 13, 1338-51 (2002). (Pubitemid 34309627)
43. Doench, J. G., Petersen, C. P. & Sharp, P. A. siRNAs can function as miRNAs. Gen. Dev. 17, 438-42 (2003). (Pubitemid 36258757)
44. Klionsky, D. J., Elazar, Z., Seglen, P. O. & Rubinsztein, D. C. Does ba-lomycin A1 block the fusion of autophagosomes with lysosomes? Autophagy 4, 849-950 (2008).
45. Jakymiw, A. et al. Disruption of GW bodies impairs mammalian RNA interference. Nat. Cell Biol. 7, 1267-74 (2005).
46. Mesquita, F. S. et al. The Salmonella deubiquitinase SseL inhibits selective autophagy of cytosolic aggregates. PLoS Pathog. 8, e1002743 (2012).
47. Costes, S. V. et al. Automatic and quantitative measurement of protein-protein colocalization in live cells. Biophys. J. 86, 3993-4003 (2004). (Pubitemid 38780275)
48. Spiegelhalter, C. et al. From dynamic live cell imaging to 3D ultrastructure: novel integrated methods for high pressure freezing and correlative light-electron microscopy. PLoS ONE 5, e9014 (2010).
49. Sahu, R. et al. Microautophagy of cytosolic proteins by late endosomes. Dev. Cell. 20, 131-9 (2011).
50. Chi, S. W., Zang, J. B., Mele, A. & Darnell, R. B. Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature 460, 479-86 (2009).