Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity

Nature Cell Biology

Volumn 11, Issue 9, 2009, Pages 1143-1149

  Gibbings, Derrick J ^a   Ciaudo, Constance ^a   Erhardt, Mathieu ^a   Voinnet, Olivier ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE 2 PROTEIN; CARRIER PROTEIN; ENDOSOMAL SORTING COMPLEX REQUIRED FOR TRANSPORT PROTEIN; MESSENGER RNA; MICRORNA; PROTEIN GW182; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL INCLUSION; CELL MEMBRANE; CELL SECRETION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOSOME; GENE ACTIVITY; GENE REPRESSION; GENE SILENCING; GW BODY; LYSOSOME; MULTIVESICULAR BODY; NONHUMAN; P BODY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN RNA BINDING; PROTEIN TARGETING; RNA ANALYSIS; SECRETORY VESICLE;

AUTOANTIGENS; CELL LINE; ENDORIBONUCLEASES; ENDOSOMES; EUKARYOTIC INITIATION FACTOR-2; EXOSOMES; GENE KNOCKDOWN TECHNIQUES; HUMANS; MICRORNAS; PROTEIN TRANSPORT; TRANS-ACTIVATORS;

ANIMALIA;

EID: 69949117622     PISSN: 14657392     EISSN: None     Source Type: Journal    
DOI: 10.1038/ncb1929     Document Type: Article

References (43)

1. Thery, C., Zitvogel, L. & Amigorena, S. Exosomes: Composition, biogenesis and function. Nature Rev. Immunol. 2, 569-579 (2002).
2. Skog, J. et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nature Cell Biol. 10, 1470-1476 (2008).
3. Islam, A. et al. The brefeldin A-inhibited guanine nucleotide-exchange protein, BIG2, regulates the constitutive release of TNFR1 exosome-like vesicles. J. Biol. Chem. 282, 9591-9599 (2007).
4. El-Shami, M. et al. Reiterated WG/GW motifs form functionally and evolutionarily conserved ARGONAUTE-binding platforms in RNAi-related components. Genes Dev. 21, 2539-2544 (2007).
5. Yu, J. H., Yang, W. H., Gulick, T., Bloch, K. D. & Bloch, D. B. Ge-1 is a central component of the mammalian cytoplasmic mRNA processing body. RNA 11, 1795-1802 (2005).
6. Valadi, H. et al. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nature Cell Biol. 9, 654-659 (2007).
7. Taylor, D. D. & Gercel-Taylor, C. MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol. Oncol. 110, 13-21 (2008).
8. Augustin, R., Riley, J. & Moley, K. H. GLUT8 contains a [DE]XXXL[LI] sorting motif and localizes to a late endosomal/lysosomal compartment. Traffic 6, 1196-1212 (2005).
9. Sherer, N. M. et al. Visualization of retroviral replication in living cells reveals budding into multivesicular bodies. Traffic 4, 785-801 (2003).
10. Laurino, C. C. et al. Human autoantibodies to diacyl-phosphatidylethanolamine recognize a specific set of discrete cytoplasmic domains. Clin. Exp. Immunol. 143, 572-584 (2006).
11. Kedersha, N. et al. Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J. Cell Biol. 169 871-884 (2005).
12. Vasudevan, S. & Steitz, J. A. AU-rich-element-mediated upregulation of translation by FXR1 and Argonaute 2. Cell 128, 1105-1118 (2007).
13. Bloch, D. B., Gulick, T., Bloch, K. D. & Yang, W. H. Processing body autoantibodies reconsidered. RNA 12, 707-709 (2006).
14. Lykke-Andersen, J. & Wagner, E. Recruitment and activation of mRNA decay enzymes by two ARE-mediated decay activation domains in the proteins TTP and BRF-1. Genes Dev. 19, 351-361 (2005).
15. Escola, J. M. et al. Selective enrichment of tetraspan proteins on the internal vesicles of multivesicular endosomes and on exosomes secreted by human B-lymphocytes. J. Biol. Chem. 273, 20121-20127 (1998).
16. Doench, J. G. & Sharp, P. A. Specificity of microRNA target selection in translational repression. Genes Dev. 18, 504-511 (2004).
17. Farh, K. K. et al. The widespread impact of mammalian MicroRNAs on mRNA repression and evolution. Science 310, 1817-1821 (2005).
18. Matsumoto, M. et al. Large-scale analysis of the human ubiquitin-related proteome. Proteomics 5, 4145-4151 (2005).
19. Hock, J. et al. Proteomic and functional analysis of Argonaute-containing mRNA-protein complexes in human cells. EMBO Rep. 8, 1052-1060 (2007).
20. Razi, M. & Futter, C. E. Distinct roles for Tsg101 and Hrs in multivesicular body formation and inward vesiculation. Mol. Biol. Cell 17, 3469-3483 (2006).
21. Cabezas, A., Bache, K. G., Brech, A. & Stenmark, H. Alix regulates cortical actin and the spatial distribution of endosomes. J. Cell Sci. 118, 2625-2635 (2005).
22. Liu, J. et al. A role for the P-body component GW182 in microRNA function. Nature Cell Biol. 7, 1261-1266 (2005).
23. Doyotte, A., Mironov, A., McKenzie, E. & Woodman, P. The Bro1-related protein HD-PTP/PTPN23 is required for endosomal cargo sorting and multivesicular body morphogenesis. Proc. Natl Acad. Sci. USA 105, 6308-6313 (2008).
24. Adams, B. D., Furneaux, H. & White, B. A. The micro-ribonucleic acid (miRNA) miR-206 targets the human estrogen receptor-alpha (ERα) and represses ERα messenger RNA and protein expression in breast cancer cell lines. Mol. Endocrinol. 21, 1132-1147 (2007).
25. Buchet-Poyau, K. et al. Identification and characterization of human Mex.-3 proteins, a novel family of evolutionarily conserved RNA-binding proteins differentially localized to processing bodies. Nucleic Acids Res. 35, 1289-1300 (2007).
26. Vasudevan, S., Tong, Y. & Steitz, J. A. Cell-cycle control of microRNA-mediated translation regulation. Cell Cycle 7, 1545-1549 (2008).
27. Sen, G. L. & Blau, H. M. Argonaute 2/RISC resides in sites of mammalian mRNA decay known as cytoplasmic bodies. Nature Cell Biol. 7, 633-636 (2005).
28. Lee, S. L. et al. Silencing by small RNAs is linked to endosomal trafficking. Nature Cell Biol. 11, 1150-1156 (2009).
29. Li, S. et al. Identification of GW182 and its novel isoform TNGW1 as translational repressors in Ago2-mediated silencing. J. Cell Sci. 121, 4134-4144 (2008).
30. Till, S. et al. A conserved motif in Argonaute-interacting proteins mediates functional interactions through the Argonaute PIWI domain. Nature Struct. Mol. Biol. 14, 897-903 (2007).
31. Eulalio, A., Huntzinger, E. & Izaurralde, E. GW182 interaction with Argonaute is essential for miRNA-mediated translational repression and mRNA decay. Nature Struct. Mol. Biol. 15, 346-353 (2008).
32. Eulalio, A. et al. Target-specific requirements for enhancers of decapping in miRNA-mediated gene silencing. Genes Dev. 21, 2558-2570 (2007).
33. Chu, C. Y. & Rana, T. M. Translation repression in human cells by microRNA-induced gene silencing requires RCK/p54. PLoS Biol. 4 e210 (2006).
34. Schwamborn, J. C., Berezikov, E. & Knoblich, J. A. The TRIM-NHL protein TRIM32 activates microRNAs and prevents self-renewal in mouse neural progenitors. Cell 136, 913-925 (2009).
35. Hammell, C. M., Lubin, I., Boag, P. R., Blackwell, T. K. & Ambros, V. nhl-2 Modulates microRNA activity in Caenorhabditis elegans. Cell 136, 926-938 (2009).
36. Raposo, G. et al. B lymphocytes secrete antigen-presenting vesicles. J. Exp. Med. 183, 1161-1172 (1996).
37. Vidal, M., Mangeat, P. & Hoekstra, D. Aggregation reroutes molecules from a recycling to a vesicle-mediated secretion pathway during reticulocyte maturation. J. Cell Sci. 110 (Pt 16), 1867-1877 (1997).
38. Jakymiw, A. et al. Disruption of GW bodies impairs mammalian RNA interference. Nature Cell Biol. 7, 1267-1274 (2005).
39. Kedersha, N. & Anderson, P. Mammalian stress granules and processing bodies. Methods Enzymol. 431, 61-81 (2007).
40. Srivastava, S. P., Kumar, K. U. & Kaufman, R. J. Phosphorylation of eukaryotic translation initiation factor 2 mediates apoptosis in response to activation of the double-stranded RNA-dependent protein kinase. J. Biol. Chem. 273, 2416-2423 (1998).
41. Pfeffer, S., Lagos-Quintana, M. & Tuschl, T. Cloning of small RNA molecules. Curr. Protoc. Mol. Biol. ch26, Unit 26.4 (2005).
42. Zhou, F. C. et al. Efficient infection by a recombinant Kaposi's sarcoma-associated herpesvirus cloned in a bacterial artificial chromosome: Application for genetic analysis. J. Virol. 76, 6185-6196 (2002).
43. Eisenberg, E. & Levanon, E. Y. Human housekeeping genes are compact. Trends Genet. 19, 362-365 (2003).