Homeostatic control of Argonaute stability by microRNA availability

Nature Structural and Molecular Biology

Volumn 20, Issue 7, 2013, Pages 789-795

  Smibert, Peter ^a   Yang, Jr Shiuan ^a   Azzam, Ghows ^a,b,c   Liu, Ji Long ^b   Lai, Eric C ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE PROTEIN; DICER; MICRORNA; PROTEASOME; UBIQUITIN;

ANIMAL CELL; ARTICLE; BIOGENESIS; CLONE; CONTROLLED STUDY; DROSOPHILA; GENE INACTIVATION; HOMEOSTASIS; IN VIVO STUDY; MAMMAL; MOUSE; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN STABILITY; RNA INTERFERENCE; RNA TRANSCRIPTION;

ANIMALS; ARGONAUTE PROTEINS; CELLS, CULTURED; CLONE CELLS; DEAD-BOX RNA HELICASES; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EUKARYOTIC INITIATION FACTORS; FEMALE; IMAGINAL DISCS; LARVA; MICE; MICRORNAS; PROTEASE INHIBITORS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN STABILITY; RECOMBINANT PROTEINS; RIBONUCLEASE III; RNA HELICASES; RNA INTERFERENCE; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, SMALL INTERFERING; TRANSCRIPTION, GENETIC; UBIQUITINATED PROTEINS;

MAMMALIA;

EID: 84880158954     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2606     Document Type: Article

References (56)

1. Czech, B. & Hannon, G.J. Small RNA sorting: matchmaking for Argonautes. Nat. Rev. Genet. 12, 19-31 (2011).
2. Kim, V.N., Han, J. & Siomi, M.C. Biogenesis of small RNAs in animals. Nat. Rev. Mol. Cell Biol. 10, 126-139 (2009).
3. Yang, J.S. & Lai, E.C. Alternative miRNA biogenesis pathways and the interpretation of core miRNA pathway mutants. Mol. Cell 43, 892-903 (2011).
4. Fabian, M.R. & Sonenberg, N. The mechanics of miRNA-mediated gene silencing: a look under the hood of miRISC. Nat. Struct. Mol. Biol. 19, 586-593 (2012).
5. Heo, I. & Kim, V.N. Regulating the regulators: posttranslational modifications of RNA silencing factors. Cell 139, 28-31 (2009).
6. Han, J. et al. Posttranscriptional crossregulation between Drosha and DGCR8. Cell 136, 75-84 (2009).
7. Kadener, S. et al. Genome-wide identification of targets of the drosha-pasha/DGCR8 complex. RNA 15, 537-545 (2009).
8. Smibert, P. et al. A Drosophila genetic screen yields allelic series of core microRNA biogenesis factors and reveals post-developmental roles for microRNAs. RNA 17, 1997-2010 (2011).
9. Iki, T., Yoshikawa, M., Meshi, T. & Ishikawa, M. Cyclophilin 40 facilitates HSP90-mediated RISC assembly in plants. EMBO J. 31, 267-278 (2012).
10. Iki, T. et al. In vitro assembly of plant RNA-induced silencing complexes facilitated by molecular chaperone HSP90. Mol. Cell 39, 282-291 (2010).
11. Miyoshi, T., Takeuchi, A., Siomi, H. & Siomi, M.C. A direct role for Hsp90 in pre-RISC formation in Drosophila. Nat. Struct. Mol. Biol. 17, 1024-1026 (2010).
12. Iwasaki, S. et al. Hsc70/Hsp90 chaperone machinery mediates ATP-dependent RISC loading of small RNA duplexes. Mol. Cell 39, 292-299 (2010).
13. 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, 1462-1469 (2010).
14. Ishizu, H., Siomi, H. & Siomi, M.C. Biology of PIWI-interacting RNAs: new insights into biogenesis and function inside and outside of germlines. Genes Dev. 26, 2361-2373 (2012).
15. Handler, D. et al. A systematic analysis of Drosophila TUDOR domain-containing proteins identifies Vreteno and the Tdrd12 family as essential primary piRNA pathway factors. EMBO J. 30, 3977-3993 (2011).
16. Liu, Q. et al. R2D2, a bridge between the initiation and effector steps of the Drosophila RNAi pathway. Science 301, 1921-1925 (2003).
17. Jiang, F. et al. Dicer-1 and R3D1-L catalyze microRNA maturation in Drosophila. Genes Dev. 19, 1674-1679 (2005).
18. Frstemann, K., Horwich, M.D., Wee, L., Tomari, Y. & Zamore, P.D. Drosophila microRNAs are sorted into functionally distinct argonaute complexes after production by dicer-1. Cell 130, 287-297 (2007).
19. Miyoshi, K., Okada, T.N., Siomi, H. & Siomi, M.C. Characterization of the miRNA-RISC loading complex and miRNA-RISC formed in the Drosophila miRNA pathway. RNA 15, 1282-1291 (2009).
20. Azzam, G., Smibert, P., Lai, E.C. & Liu, J.L. Drosophila Argonaute 1 and its miRNA biogenesis partners are required for oocyte formation and germline cell division. Dev. Biol. 365, 384-394 (2012).
21. Herranz, H. et al. The miRNA machinery targets Mei-P26 and regulates Myc protein levels in the Drosophila wing. EMBO J. 29, 1688-1698 (2010).
22. Yao, B., La, L.B., Chen, Y.C., Chang, L.J. & Chan, E.K. Defining a new role of GW182 in maintaining miRNA stability. EMBO Rep. 13, 1102-1108 (2012).
23. Neumller, R.A. et al. Mei-P26 regulates microRNAs and cell growth in the Drosophila ovarian stem cell lineage. Nature 454, 241-245 (2008).
24. Okamura, K. et al. The Drosophila hairpin RNA pathway generates endogenous short interfering RNAs. Nature 453, 803-806 (2008).
25. Czech, B. et al. Hierarchical rules for Argonaute loading in Drosophila. Mol. Cell 36, 445-456 (2009).
26. Czech, B. et al. An endogenous siRNA pathway in Drosophila. Nature 453, 798-802 (2008).
27. Okamura, K., Robine, N., Liu, Y., Liu, Q. & Lai, E.C. R2D2 organizes small regulatory RNA pathways in Drosophila. Mol. Cell Biol. 31, 884-896 (2011).
28. Lee, Y.S. et al. Distinct roles for Drosophila Dicer-1 and Dicer-2 in the siRNA/miRNA silencing pathways. Cell 117, 69-81 (2004).
29. Yang, J.S. et al. Conserved vertebrate mir-451 provides a platform for Dicer-independent, Ago2-mediated microRNA biogenesis. Proc. Natl. Acad. Sci. USA 107, 15163-15168 (2010).
30. Castilla-Llorente, V. et al. Mammalian GW220/TNGW1 is essential for the formation of GW/P bodies containing miRISC. J. Cell Biol. 198, 529-544 (2012).
31. Gibbings, D. et al. Selective autophagy degrades DICER and AGO2 and regulates miRNA activity. Nat. Cell Biol. 14, 1314-1321 (2012).
32. Yang, J.S. & Lai, E.C. Dicer-independent, Ago2-mediated microRNA biogenesis in vertebrates. Cell Cycle 9, 4455-4460 (2010).
33. Maurin, T., Cazalla, D., Yang, J.S., Bortolamiol-Becet, D. & Lai, E.C. RNase III-independent microRNA biogenesis in mammalian cells. RNA 18, 2166-2173 (2012).
34. Okamura, K., Liu, N. & Lai, E.C. Distinct mechanisms for microRNA strand selection by Drosophila Argonautes. Mol. Cell 36, 431-444 (2009).
35. Okamura, K. et al. The regulatory activity of microRNA species has substantial influence on microRNA and 3 UTR evolution. Nat. Struct. Mol. Biol. 15, 354-363 (2008).
36. Elkayam, E. et al. The structure of human Argonaute-2 in complex with miR-20a. Cell 150, 100-110 (2012).
37. Schirle, N.T. & MacRae, I.J. The crystal structure of human Argonaute2. Science 336, 1037-1040 (2012).
38. Martinez, N.J. & Gregory, R.I. Argonaute2 expression is post-transcriptionally coupled to microRNA abundance. RNA 19, 605-612 (2013).
39. Yigit, E. et al. Analysis of the C. elegans Argonaute family reveals that distinct Argonautes act sequentially during RNAi. Cell 127, 747-757 (2006).
40. Diederichs, S. & Haber, D.A. Dual role for Argonautes in microRNA processing and posttranscriptional regulation of microRNA expression. Cell 131, 1097-1108 (2007).
41. Yang, J.S., Maurin, T. & Lai, E.C. Functional parameters of Dicer-independent microRNA biogenesis. RNA 18, 945-957 (2012).
42. Janas, M.M. et al. Alternative RISC assembly: binding and repression of microRNA-mRNA duplexes by human Ago proteins. RNA 18, 2041-2055 (2012).
43. Wang, D. et al. Quantitative functions of Argonaute proteins in mammalian development. Genes Dev. 26, 693-704 (2012).
44. Ameres, S.L., Hung, J.H., Xu, J., Weng, Z. & Zamore, P.D. Target RNA-directed tailing and trimming purifies the sorting of endo-siRNAs between the two Drosophila Argonaute proteins. RNA 17, 54-63 (2011).
45. Zhao, S. et al. piRNA-triggered MIWI ubiquitination and removal by APC/C in late spermatogenesis. Dev. Cell 24, 13-25 (2013).
46. Bronevetsky, Y. et al. T cell activation induces proteasomal degradation of Argonaute and rapid remodeling of the microRNA repertoire. J. Exp. Med. 210, 417-432 (2013).
47. Tan, G.S. et al. Expanded RNA-binding activities of mammalian Argonaute Nucleic Acids Res. 37, 7533-7545 (2009).
48. Kataoka, Y., Takeichi, M. & Uemura, T. Developmental roles and molecular characterization of a Drosophila homologue of Arabidopsis Argonaute1, the founder of a novel gene superfamily. Genes Cells 6, 313-325 (2001).
49. Yang, L. et al. Argonaute 1 regulates the fate of germline stem cells in Drosophila. Development 134, 4265-4272 (2007).
50. Martin, R. et al. A Drosophila pasha mutant distinguishes the canonical miRNA and mirtron pathways. Mol. Cell Biol. 29, 861-870 (2009).
51. Schweisguth, F. Dominant-negative mutation in the b2 and b6 proteasome-subunit genes affect alternative cell fate decisions in the Drosophila sense organ lineage. Proc. Natl. Acad. Sci. USA 96, 11382-11386 (1999).
52. Xu, X.L., Li, Y., Wang, F. & Gao, F.B. The steady-state level of the nervous-system-specific microRNA-124a is regulated by dFMR1 in Drosophila. J. Neurosci. 28, 11883-11889 (2008).
53. Bejarano, F. et al. A genome-wide transgenic resource for conditional expression of Drosophila microRNAs. Development 139, 2821-2831 (2012).
54. Lai, E.C. & Rubin, G.M. neuralized functions cell-autonomously to regulate a subset of Notch-dependent processes during adult Drosophila development. Dev. Biol. 231, 217-233 (2001).
55. Liu, N., Han, H. & Lasko, P. Vasa promotes Drosophila germline stem cell differentiation by activating mei-P26 translation by directly interacting with a (U)-rich motif in its 3 UTR. Genes Dev. 23, 2742-2752 (2009).
56. Okamura, K., Hagen, J.W., Duan, H., Tyler, D.M. & Lai, E.C. The mirtron pathway generates microRNA-class regulatory RNAs in Drosophila. Cell 130, 89-100 (2007).