Alteration of miRNA activity via context-specific modifications of Argonaute proteins

Trends in Cell Biology

Volumn 24, Issue 9, 2014, Pages 546-553

  Jee, David ^a,b   Lai, Eric C ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b Weill Cornell Medical Center   (United States)

Author keywords

Argonaute; Hydroxylation; MiRNA; PARylation; Phosphorylation; Ubiquitination

Indexed keywords

ARGONAUTE PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; MICRORNA; PROLINE DERIVATIVE; RNA INDUCED SILENCING COMPLEX; RNA;

ADENOSINE DIPHOSPHATE RIBOSYLATION; BIOGENESIS; GENE CONTROL; HUMAN; HYDROXYLATION; HYPOXIA; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; REVIEW; T LYMPHOCYTE ACTIVATION; UBIQUITINATION; VIRUS INFECTION; ANIMAL; GENETICS; METABOLISM; PHOSPHORYLATION; PROTEIN PROCESSING; RNA INTERFERENCE;

MAMMALIA;

ANIMALS; ARGONAUTE PROTEINS; HUMANS; MICRORNAS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA; RNA INTERFERENCE; UBIQUITINATION;

EID: 84906936068     PISSN: 09628924     EISSN: 18793088     Source Type: Journal    
DOI: 10.1016/j.tcb.2014.04.008     Document Type: Review

References (74)

1. Yang J.S., Lai E.C. Alternative miRNA biogenesis pathways and the interpretation of core miRNA pathway mutants. Mol. Cell 2011, 43:892-903.
2. Meister G. Argonaute proteins: functional insights and emerging roles. Nat. Rev. Genet. 2013, 14:447-459.
3. Brennecke J., et al. Principles of microRNA-target recognition. PLoS Biol. 2005, 3:e85.
4. Doench J.G., Sharp P.A. Specificity of microRNA target selection in translational repression. Genes Dev. 2004, 18:504-511.
5. Lai E.C. MicroRNAs are complementary to 3' UTR sequence motifs that mediate negative post-transcriptional regulation. Nat. Genet. 2002, 30:363-364.
6. Bartel D.P. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233.
7. Aboobaker A.A., et al. Drosophila microRNAs exhibit diverse spatial expression patterns during embryonic development. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:18017-18022.
8. Wienholds E., et al. MicroRNA expression in zebrafish embryonic development. Science 2005, 309:310-311.
9. Lu J., et al. MicroRNA expression profiles classify human cancers. Nature 2005, 435:834-838.
10. Suh N., et al. MicroRNA function is globally suppressed in mouse oocytes and early embryos. Curr. Biol. 2010, 20:271-277.
11. Ma J., et al. MicroRNA activity is suppressed in mouse oocytes. Curr. Biol. 2010, 20:265-270.
12. Su X., et al. TAp63 suppresses metastasis through coordinate regulation of Dicer and miRNAs. Nature 2010, 467:986-990.
13. Levy C., et al. Lineage-specific transcriptional regulation of DICER by MITF in melanocytes. Cell 2010, 141:994-1005.
14. Wang X., et al. c-Myc modulates microRNA processing via the transcriptional regulation of Drosha. Sci. Rep. 2013, 3:1942.
15. Kim Y.K., et al. Modifications of small RNAs and their associated proteins. Cell 2010, 143:703-709.
16. Heo I., Kim V.N. Regulating the regulators: posttranslational modifications of RNA silencing factors. Cell 2009, 139:28-31.
17. Paroo Z., et al. Phosphorylation of the human microRNA-generating complex mediates MAPK/Erk signaling. Cell 2009, 139:112-122.
18. Heo I., et al. TUT4 in concert with Lin28 suppresses microRNA biogenesis through pre-microRNA uridylation. Cell 2009, 138:696-708.
19. Hagan J.P., et al. Lin28 recruits the TUTase Zcchc11 to inhibit let-7 maturation in mouse embryonic stem cells. Nat. Struct. Mol. Biol. 2009, 16:1021-1025.
20. Thornton J.E., et al. Lin28-mediated control of let-7 microRNA expression by alternative TUTases Zcchc11 (TUT4) and Zcchc6 (TUT7). RNA 2012, 18:1875-1885.
21. Chang H.M., et al. A role for the Perlman syndrome exonuclease Dis3l2 in the Lin28-let-7 pathway. Nature 2013, 497:244-248.
22. Ustianenko D., et al. Mammalian DIS3L2 exoribonuclease targets the uridylated precursors of let-7 miRNAs. RNA 2013, 19:1632-1638.
23. Qi H.H., et al. Prolyl 4-hydroxylation regulates Argonaute 2 stability. Nature 2008, 455:421-424.
24. Wu C., et al. Hypoxia potentiates microRNA-mediated gene silencing through posttranslational modification of Argonaute2. Mol. Cell. Biol. 2011, 31:4760-4774.
25. Yang J.S., Lai E.C. Dicer-independent, Ago2-mediated microRNA biogenesis in vertebrates. Cell Cycle 2010, 9:4455-4460.
26. Rudel S., et al. Phosphorylation of human Argonaute proteins affects small RNA binding. Nucleic Acids Res. 2011, 39:2330-2343.
27. Zeng Y., et al. Phosphorylation of Argonaute 2 at serine-387 facilitates its localization to processing bodies. Biochem. J. 2008, 413:429-436.
28. Horman S.R., et al. Akt-mediated phosphorylation of Argonaute 2 downregulates cleavage and upregulates translational repression of microRNA targets. Mol. Cell 2013, 50:356-367.
29. Mazumder A., et al. A transient reversal of miRNA-mediated repression controls macrophage activation. EMBO Rep. 2013, 14:1008-1016.
30. Shen J., et al. EGFR modulates microRNA maturation in response to hypoxia through phosphorylation of AGO2. Nature 2013, 497:383-387.
31. Betancur J.G., Tomari Y. Dicer is dispensable for asymmetric RISC loading in mammals. RNA 2012, 18:24-30.
32. Noland C.L., Doudna J.A. Multiple sensors ensure guide strand selection in human RNAi pathways. RNA 2013, 19:639-648.
33. Rybak A., et al. The let-7 target gene mouse lin-41 is a stem cell specific E3 ubiquitin ligase for the miRNA pathway protein Ago2. Nat. Cell Biol. 2009, 11:1411-1420.
34. Reinhart B.J., et al. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 2000, 403:901-906.
35. Ecsedi M., Grosshans H. LIN-41/TRIM71: emancipation of a miRNA target. Genes Dev. 2013, 27:581-589.
36. Chang H.M., et al. Trim71 cooperates with microRNAs to repress Cdkn1a expression and promote embryonic stem cell proliferation. Nat. Commun. 2012, 3:923.
37. Loedige I., et al. The mammalian TRIM-NHL protein TRIM71/LIN-41 is a repressor of mRNA function. Nucleic Acids Res. 2013, 41:518-532.
38. Chen J., et al. The ubiquitin ligase mLin41 temporally promotes neural progenitor cell maintenance through FGF signaling. Genes Dev. 2012, 26:803-815.
39. Smibert P., et al. Homeostatic control of Argonaute stability by microRNA availability. Nat. Struct. Mol. Biol. 2013, 20:789-795.
40. Johnston M., et al. HSP90 protein stabilizes unloaded Argonaute complexes and microscopic P-bodies in human cells. Mol. Biol. Cell 2010, 21:1462-1469.
41. Martinez N.J., Gregory R.I. Argonaute2 expression is post-transcriptionally coupled to microRNA abundance. RNA 2013, 19:605-612.
42. Zhang P., Zhang H. Autophagy modulates miRNA-mediated gene silencing and selectively degrades AIN-1/GW182 in C. elegans. EMBO Rep. 2013, 14:568-576.
43. Gibbings D., et al. Selective autophagy degrades DICER and AGO2 and regulates miRNA activity. Nat. Cell Biol. 2012, 14:1314-1321.
44. Chong M.M., et al. The RNAseIII enzyme Drosha is critical in T cells for preventing lethal inflammatory disease. J. Exp. Med. 2008, 205:2005-2017.
45. Muljo S.A., et al. Aberrant T cell differentiation in the absence of Dicer. J. Exp. Med. 2005, 202:261-269.
46. Monticelli S., et al. MicroRNA profiling of the murine hematopoietic system. Genome Biol. 2005, 6:R71.
47. Olejniczak S.H., et al. Long-lived microRNA-Argonaute complexes in quiescent cells can be activated to regulate mitogenic responses. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:157-162.
48. van Rooij E., et al. Control of stress-dependent cardiac growth and gene expression by a microRNA. Science 2007, 316:575-579.
49. Bronevetsky Y., et al. T cell activation induces proteasomal degradation of Argonaute and rapid remodeling of the microRNA repertoire. J. Exp. Med. 2013, 210:417-432.
50. Baumberger N., et al. The Polerovirus silencing suppressor P0 targets ARGONAUTE proteins for degradation. Curr. Biol. 2007, 17:1609-1614.
51. Bortolamiol D., et al. The Polerovirus F box protein P0 targets ARGONAUTE1 to suppress RNA silencing. Curr. Biol. 2007, 17:1615-1621.
52. Zhao S., et al. piRNA-triggered MIWI ubiquitination and removal by APC/C in late spermatogenesis. Dev. Cell 2013, 24:13-25.
53. Leung A.K., et al. Poly(ADP-ribose) regulates stress responses and microRNA activity in the cytoplasm. Mol. Cell 2011, 42:489-499.
54. Leung A.K., et al. Quantitative analysis of Argonaute protein reveals microRNA-dependent localization to stress granules. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:18125-18130.
55. Karginov F.V., Hannon G.J. Remodeling of Ago2-mRNA interactions upon cellular stress reflects miRNA complementarity and correlates with altered translation rates. Genes Dev. 2013, 27:1624-1632.
56. Wu P.H., et al. Functionally diverse microRNA effector complexes are regulated by extracellular signaling. Mol. Cell 2013, 52:113-123.
57. Cullen B.R., et al. Is RNA interference a physiologically relevant innate antiviral immune response in mammals?. Cell Host Microbe 2013, 14:374-378.
58. Sadler A.J., Williams B.R. Interferon-inducible antiviral effectors. Nat. Rev. Immunol. 2008, 8:559-568.
59. Parameswaran P., et al. Six RNA viruses and forty-one hosts: viral small RNAs and modulation of small RNA repertoires in vertebrate and invertebrate systems. PLoS Pathog. 2010, 6:e1000764.
60. Cullen B.R. Viral and cellular messenger RNA targets of viral microRNAs. Nature 2009, 457:421-425.
61. Yeung M.L., et al. siRNA, miRNA and HIV: promises and challenges. Cell Res. 2005, 15:935-946.
62. Trobaugh D.W., et al. RNA viruses can hijack vertebrate microRNAs to suppress innate immunity. Nature 2013, 506:245-248.
63. Jopling C.L., et al. Modulation of hepatitis C virus RNA abundance by a liver-specific microRNA. Science 2005, 309:1577-1581.
64. Seo G.J., et al. Reciprocal inhibition between intracellular antiviral signaling and the RNAi machinery in mammalian cells. Cell Host Microbe 2013, 14:435-445.
65. Gottwein E., et al. Viral microRNA targetome of KSHV-infected primary effusion lymphoma cell lines. Cell Host Microbe 2011, 10:515-526.
66. Skalsky R.L., et al. The viral and cellular microRNA targetome in lymphoblastoid cell lines. PLoS Pathog. 2012, 8:e1002484.
67. Maillard P.V., et al. Antiviral RNA interference in mammalian cells. Science 2013, 342:235-238.
68. Li Y., et al. RNA interference functions as an antiviral immunity mechanism in mammals. Science 2013, 342:231-234.
69. Babiarz J.E., et al. Mouse ES cells express endogenous shRNAs, siRNAs, and other Microprocessor-independent, Dicer-dependent small RNAs. Genes Dev. 2008, 22:2773-2785.
70. Flemr M., et al. A retrotransposon-driven Dicer isoform directs endogenous small interfering RNA production in mouse oocytes. Cell 2013, 155:807-816.
71. Vagin V.V., et al. Arginine methylation as a molecular signature of the Piwi small RNA pathway. Cell Cycle 2009, 8:4003-4004.
72. Wada T., et al. Histone deacetylase 1 enhances microRNA processing via deacetylation of DGCR8. EMBO Rep. 2012, 13:142-149.
73. Tang X., et al. Acetylation of Drosha on the N-terminus inhibits its degradation by ubiquitination. PLoS ONE 2013, 8:e72503.
74. Cheloufi S., et al. A Dicer-independent miRNA biogenesis pathway that requires Ago catalysis. Nature 2010, 465:584-589.