HSP90 protein stabilizes unloaded argonaute complexes and microscopic P-bodies in human cells

Molecular Biology of the Cell

Volumn 21, Issue 9, 2010, Pages 1462-1469

  Johnston, Michael ^a   Geoffroy, Marie Claude ^a,b   Sobala, Andrew ^a   Hay, Ron ^a   Hutvagner, Gyorgy ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b INSTITUT ANDRÉ LWOFF   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE PROTEIN; GELDANAMYCIN; HEAT SHOCK PROTEIN 90; MICRORNA; SMALL INTERFERING RNA; TANESPIMYCIN;

ARTICLE; GENE EXPRESSION; GENE REPRESSION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STABILITY; RNA BINDING;

AUTOANTIGENS; BENZOQUINONES; BLOTTING, NORTHERN; BLOTTING, WESTERN; CELL LINE; CELL LINE, TUMOR; CYTOPLASMIC GRANULES; EUKARYOTIC INITIATION FACTOR-2; GENE EXPRESSION; HELA CELLS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; LACTAMS, MACROCYCLIC; LUCIFERASES; MICRORNAS; MICROSCOPY, FLUORESCENCE; PROTEIN BINDING; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 77951712353     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E09-10-0885     Document Type: Article

References (53)

1. Banerji, U., Walton, M., Raynaud, F., Grimshaw, R., Kelland, L., Valenti, M., Judson, I., and Workman, P. (2005). Pharmacokinetic-pharmacodynamic relationships for the heat shock protein 90 molecular chaperone inhibitor 17-allylamino, 17-demethoxygeldanamycin in human ovarian cancer xenograft models. Clin. Cancer Res. 11, 7023-7032.
2. 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. (Pubitemid 44079326)
3. Bhattacharyya, S. N., Habermacher, R., Martine, U., Closs, E. I., and Filipowicz, W. (2006). Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell 125, 1111-1124. (Pubitemid 43866197)
4. Chekulaeva, M., Filipowicz, W., and Parker, R. (2009). Multiple independent domains of dGW182 function in miRNA-mediated repression in Drosophila. RNA 15, 794-803.
5. Chu, C., and Rana, T. M. (2006). Translation repression in human cells by microRNA-induced gene silencing requires RCK/p54. PLoS Biol. 4(7), e210. (Pubitemid 44049611)
6. 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. (Pubitemid 41140002)
7. Eulalio, A., Behm-Ansmant, I., and Izaurralde, E. (2007a). P bodies: at the crossroads of post-transcriptional pathways. Nat. Rev. Mol. Cell Biol. 8, 9-22.
8. Eulalio, A., Behm-Ansmant, I., Schweizer, D., and Izaurralde, E. (2007b). P-body formation is a consequence, not the cause, of RNA-mediated gene silencing. Mol. Cell. Biol. 27, 3970-3981.
9. 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.
10. Eulalio, A., Huntzinger, E., and Izaurralde, E. (2008). GW182 interaction with Argonaute is essential for miRNA-mediated translational repression and mRNA decay. Nat. Struct. Mol. Biol. 15, 346-353.
11. 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.
12. Goetz, M. P., Toft, D. O., Ames, M. M., and Erlichman, C. (2003). The Hsp90 chaperone complex as a novel target for cancer therapy. Ann. Oncol. 14, 1169-1176.
13. Hock, J., Weinmann, L., Ender, C., Rudel, S., Kremmer, E., Raabe, M., Urlaub, H., and Meister, G. (2007). Proteomic and functional analysis of Argonaute-containing mRNA-protein complexes in human cells. EMBO Rep. 8, 1052-1060. (Pubitemid 350042341)
14. Hutvagner, G., Simard, M. J., Mello, C. C., and Zamore, P. D. (2004). Sequence-specific inhibition of small RNA function. PLoS Biol. 2, E98. (Pubitemid 39234504)
15. Iwasaki, S., Kawamata, T., and Tomari, Y. (2009). Drosophila argonaute1 and argonaute2 employ distinct mechanisms for translational repression. Mol. Cell 34, 58-67.
16. Jagannath, A., and Wood, M. J. (2009). Localization of double-stranded small interfering RNA to cytoplasmic processing bodies is Ago2 dependent and results in up-regulation of GW182 and Argonaute-2. Mol. Biol. Cell 20, 521-529.
17. 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.
18. Jakymiw, A., Pauley, K. M., Li, S., Ikeda, K., Lian, S., Eystathioy, T., Satoh, M., Fritzler, M. J., and Chan, E. K. (2007). The role of GW/P-bodies in RNA processing and silencing. J. Cell Sci. 120, 1317-1323. (Pubitemid 46780024)
19. Johnson, S. M., Grosshans, H., Shingara, J., Byrom, M., Jarvis, R., Cheng, A., Labourier, E., Reinert, K. L., Brown, D., and Slack, F. J. (2005). RAS is regulated by the let-7 microRNA family. Cell 120, 635-647. (Pubitemid 40343076)
20. Landthaler, M., Gaidatzis, D., Rothballer, A., Chen, P. Y., Soll, S. J., Dinic, L., Ojo, T., Hafner, M., Zavolan, M., and Tuschl, T. (2008). Molecular characterization of human Argonaute-containing ribonucleoprotein complexes and their bound target mRNAs. RNA 14, 2580-2596.
21. 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.
22. Li, S., Lian, S. L., Moser, J. J., Fritzler, M. L., Fritzler, M. J., Satoh, M., and Chan, E. K. (2008). Identification of GW182 and its novel isoform TNGW1 as translational repressors in Ago2-mediated silencing. J. Cell Sci. 121, 4134-4144.
23. Lian, S., Fritzler, M. J., Katz, J., Hamazaki, T., Terada, N., Satoh, M., and Chan, E. K. (2007). Small interfering RNA-mediated silencing induces target-dependent assembly of GW/P bodies. Mol. Biol. Cell 18, 3375-3387.
24. 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.
25. Lingel, A., Simon, B., Izaurralde, E., and Sattler, M. (2003). Structure and nucleicacid binding of the Drosophila Argonaute 2 PAZ domain. Nature 426, 465-469.
26. Lingel, A., Simon, B., Izaurralde, E., and Sattler, M. (2004). Nucleic acid 3′-end recognition by the Argonaute2 PAZ domain. Nat. Struct. Mol. Biol. 11, 576-577.
27. Liu, J., Rivas, F. V., Wohlschlegel, J., Yates, J. R., Parker, R., and Hannon, G. J. (2005a). A role for the P-body component GW182 in microRNA function. Nat. Cell Biol. 7, 1161-1166.
28. Liu, J., Valencia-Sanchez, M. A., Hannon, G. J., and Parker, R. (2005b). MicroRNA-dependent localization of targeted mRNAs to mammalian P-bodies. Nat. Cell Biol. 7, 719-723.
29. Meister, G., Landthaler, M., Dorsett, Y., and Tuschl, T. (2004). Sequence-specific inhibition of microRNA- and siRNA-induced RNA silencing. RNA 10, 544-550.
30. 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.
31. Pall, G. S., Codony-Servat, C., Byrne, J., Ritchie, L., and Hamilton, A. (2007). Carbodiimide-mediated cross-linking of RNA to nylon membranes improves the detection of siRNA, miRNA and piRNA by northern blot. Nucleic Acids Res. 35, e60.
32. Pare, J. M., Tahbaz, N., Lopez-Orozco, J., LaPointe, P., Lasko, P., and Hobman, T. C. (2009). Hsp90 regulates the function of argonaute 2 and its recruitment to stress granules and P-bodies. Mol. Biol. Cell 20, 3273-3284.
33. Pauley, K. M., Eystathioy, T., Jakymiw, A., Hamel, J. C., Fritzler, M. J., and Chan, E. K. (2006). Formation of GW bodies is a consequence of microRNA genesis. EMBO Rep. 7, 904-910.
34. Picard, D. (2002). Heat-shock protein 90, a chaperone for folding and regulation. Cell Mol. Life Sci. 59, 1640-1648.
35. Pillai, R. S., Bhattacharyya, S. N., Artus, C. G., Zoller, T., Cougot, N., Basyuk, E., Bertrand, E., and Filipowicz, W. (2005). Inhibition of translational initiation by Let-7 MicroRNA in human cells. Science 309, 1573-1576.
36. Pratt, W. B., Morishima, Y., and Osawa, Y. (2008). The Hsp90 chaperone machinery regulates signaling by modulating ligand binding clefts. J. Biol. Chem. 283, 22885-22889.
37. Rehwinkel, J., Behm-Ansmant, I., Gatfield, D., and Izaurralde, E. (2005). A crucial role for GW182 and the DCP 1, DCP2 decapping complex in miRNA-mediated gene silencing. RNA 11, 1640-1647.
38. Robb, G. B., and Rana, T. M. (2007). RNA helicase A interacts with RISC in human cells and functions in RISC loading. Mol. Cell 26, 523-537.
39. Rudel, S., Flatley, A., Weinmann, L., Kremmer, E., and Meister, G. (2008). A multifunctional human Argonaute2-specific monoclonal antibody. RNA 14, 1244-1253.
40. Schulte, T. W., Blagosklonny, M. V., Ingui, C., and Neckers, L. (1995). Disruption of the Raf-1-Hsp90 molecular complex results in destabilization of Raf-1 and loss of Raf-1-Ras association. J. Biol. Chem. 270, 24585-24588.
41. 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.
42. Smith, D. F., Whitesell, L., Nair, S. C., Chen, S., Prapapanich, V., and Rimerman, R. A. (1995). Progesterone receptor structure and function altered by geldanamycin, an hsp90-binding agent. Mol. Cell Biol. 15, 6804-6812.
43. Smith, M. R., Willmann, M. R., Wu, G., Berardini, T. Z., Moller, B., Weijers, D., and Poethig, R. S. (2009). Cyclophilin 40 is required for microRNA activity in Arabidopsis. Proc. Natl. Acad. Sci. USA 106, 5424-5429.
44. Song, J. J., Liu, J., Tolia, N. H., Schneiderman, J., Smith, S. K., Martienssen, R. A., Hannon, G. J., and Joshua-Tor, L. (2003). The crystal structure of the Argonaute2 PAZ domain reveals an RNA binding motif in RNAi effector complexes. Nat. Struct. Biol. 10, 1026-1032.
45. Sotiropoulou, G., Pampalakis, G., Lianidou, E., and Mourelatos, Z. (2009). Emerging roles of microRNAs as molecular switches in the integrated circuit of the cancer cell. RNA 15, 1443-1461.
46. Suzuki, Y., Minami, M., Suzuki, M., Abe, K., Zenno, S., Tsujimoto, M., Matsumoto, K., and Minami, Y. (2009). The Hsp90 inhibitor geldanamycin abrogates colocalization of eIF4E and eIF4E-transporter into stress granules and association of eIF4E with eIF4G. J. Biol. Chem. 284, 35597-35604.
47. Tahbaz, N., Carmichael, J. B., and Hobman, T. C. (2001). GERp95 belongs to a family of signal-transducing proteins and requires Hsp90 activity for stability and Golgi localization. J. Biol. Chem. 276, 43294-43299.
48. Tahbaz, N., Kolb, F. A., Zhang, H., Jaronczyk, K., Filipowicz, W., and Hobman, T. C. (2004). Characterization of the interactions between mammalian PAZ PIWI domain proteins and Dicer. EMBO Rep. 5, 189-194.
49. Vagin, V. V., Wohlschlegel, J., Qu, J., Jonsson, Z., Huang, X., Chuma, S., Girard, A., Sachidanandam, R., Hannon, G. J., and Aravin, A. A. (2009). Proteomic analysis of murine Piwi proteins reveals a role for arginine methylation in specifying interaction with Tudor family members. Genes Dev. 23, 1749-1762.
50. Workman, P., Burrows, F., Neckers, L., and Rosen, N. (2007). Drugging the cancer chaperone HSP 90, combinatorial therapeutic exploitation of oncogene addiction and tumor stress. Ann. NY Acad. Sci. 1113, 202-216.
51. 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.
52. Yoda, M., Kawamata, T., Paroo, Z., Ye, X., Iwasaki, S., Liu, Q., and Tomari, Y. (2010). ATP-dependent human RISC assembly pathways. Nat. Struct. Mol. Biol. 17, 17-23.
53. Zipprich, J. T., Bhattacharyya, S., Mathys, H., and Filipowicz, W. (2009). Importance of the C-terminal domain of the human GW182 protein TNRC6C for translational repression. RNA 15, 781-793.