Inhibition of the ubiquitin-proteasome system induces stress granule formation

Molecular Biology of the Cell

Volumn 18, Issue 7, 2007, Pages 2603-2618

  Mazroui, Rachid ^a   Di Marco, Sergio ^a   Kaufman, Randal J ^b   Gallouzi, Imed Eddine ^a  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1; HEAT SHOCK PROTEIN 72; INITIATION FACTOR 2ALPHA; MESSENGER RNA; PROTEASOME; UBIQUITIN;

ANIMAL CELL; ARTICLE; CELL GRANULE; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; ENZYME INHIBITION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RNA DEGRADATION; RNA STABILITY; TRANSLATION REGULATION;

APOPTOSIS; CODON, NONSENSE; CYTOPLASMIC GRANULES; EUKARYOTIC INITIATION FACTOR-2; HELA CELLS; HSP72 HEAT-SHOCK PROTEINS; HUMANS; LEUPEPTINS; PHOSPHORYLATION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BIOSYNTHESIS; PROTEIN FOLDING; PROTEIN TRANSPORT; RESPONSE ELEMENTS; RNA STABILITY; UBIQUITIN;

EID: 34347406608     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E06-12-1079     Document Type: Article

References (80)

1. Adams, J. (2004). The development of proteasome inhibitors as anticancer drugs. Cancer Cell 5, 417-421.
2. Anderson, P., and Kedersha, N. (2002). Visibly stressed: the role of eIF2, TIA-1, and stress granules in protein translation. Cell Stress Chaperones 7, 213-221.
3. Anderson, P., and Kedersha, N. (2006). RNA granules. J. Cell Biol. 172, 803-808.
4. Andrews, G. K., Harding, M. A., Calvet, J. P., and Adamson, E. D. (1987). The heat shock response in HeLa cells is accompanied by elevated expression of the c-fos proto-oncogene. Mol. Cell. Biol. 7, 3452-3458.
5. Barreau, C., Paillard, L., and Osborne, H. B. (2005). AU-rich elements and associated factors: are there unifying principles? Nucleic Acids Res. 33, 7138-7150.
6. Baugh, J. M., and Pilipenko, E. V. (2004). 20S proteasome differentially alters translation of different mRNAs via the cleavage of eIF4F and eIF3. Mol. Cell 16, 575-586.
7. Beere, H. M. (2004). "The stress of dying": the role of heat shock proteins in the regulation of apoptosis. J. Cell Sci. 117, 2641-2651.
8. Bence, N. F., Bennett, E. J., and Kopito, R. R. (2005). Application and analysis of the GFP(u) family of ubiquitin-proteasome system reporters. Methods Enzymol. 399, 481-490.
9. Bevilacqua, A., Ceriani, M. C., Capaccioli, S., and Nicolin, A. (2003). Post-transcriptional regulation of gene expression by degradation of messenger RNAs. J. Cell. Physiol. 195, 356-372.
10. Brengues, M., Teixeira, D., and Parker, R. (2005). Movement of eukaryotic mRNAs between polysomes and cytoplasmic processing bodies. Science 310, 486-489.
11. Briata, P., Forcales, S. V., Ponassi, M., Corte, G., Chen, C. Y., Karin, M., Puri, P. L., and Gherzi, R. (2005). p38-dependent phosphorylation of the mRNA decay-promoting factor KSRP controls the stability of select myogenic transcripts. Mol. Cell 20, 891-903.
12. Cobb, L. J., Salih, D. A., Gonzalez, I., Tripathi, G., Carter, E. J., Lovett, F., Holding, C., and Pell, J. M. (2004). Partitioning of IGFBP-5 actions in myogenesis: IGF-independent anti-apoptotic function. J. Cell Sci. 117, 1737-1746.
13. Cuesta, R., Laroia, G., and Schneider, R. J. (2000). Chaperone hsp27 inhibits translation during heat shock by binding eIF4G and facilitating dissociation of cap-initiation complexes. Genes Dev. 14, 1460-1470.
14. Dang, Y., Kedersha, N., Low, W. K., Romo, D., Gorospe, M., Kaufman, R., Anderson, P., and Liu, J. O. (2006). Eukaryotic initiation factor 2alpha-independent pathway of stress granule induction by the natural product pateamine A. J. Biol. Chem. 281, 32870-32878.
15. Di Marco, S., Mazroui, R., Dallaire, P., Chittur, S., Tenenbaum, S. A., Radzioch, D., Marette, A., and Gallouzi, I. E. (2005). NF-(kappa)B-mediated MyoD decay during muscle wasting requires nitric oxide synthase mRNA stabilization, HuR protein, and nitric oxide release. Mol. Cell. Biol. 25, 6533-6545.
16. Ding, Q., Dimayuga, E., Markesbery, W. R., and Keller, J. N. (2006). Proteasome inhibition induces reversible impairments in protein synthesis. FASEB J. 20, 1055-1063.
17. Fan, X. C., and Steitz, J. A. (1998). Overexpression of HuR, a nuclear-cytoplasmic shuttling protein, increases the in vivo stability of ARE-containing mRNAs. EMBO J. 17, 3448-3460.
18. Fenger-Gron, M., Fillman, C., Norrild, B., and Lykke-Andersen, J. (2005). Multiple processing body factors and the ARE binding protein TTP activate mRNA decapping. Mol. Cell 20, 905-915.
19. Ferraiuolo, M. A., Basak, S., Dostie, J., Murray, E. L., Schoenberg, D. R., and Sonenberg, N. (2005). A role for the eIF4E-binding protein 4E-T in P-body formation and mRNA decay. J. Cell Biol. 170, 913-924.
20. Gabai, V. L., and Sherman, M. Y. (2002). Invited review: Interplay between molecular chaperones and signaling pathways in survival of heat shock. J. Appl. Physiol. 92, 1743-1748.
21. Gallouzi, I. E., Brennan, C. M., and Steitz, J. A. (2001). Protein ligands mediate the CRM1-dependent export of HuR in response to heat shock. RNA 7, 1348-1361.
22. Gallouzi, I. E., Brennan, C. M., Stenberg, M. G., Swanson, M. S., Eversole, A., Maizels, N., and Steitz, J. A. (2000). HuR binding to cytoplasmic mRNA is perturbed by heat shock. Proc. Natl. Acad. Sci. USA 97, 3073-3078.
23. Gallouzi, I. E., Parker, F., Chebli, K., Maurier, F., Labourier, E., Barlat, I., Capony, J. P., Tocque, B., and Tazi, J. (1998). A novel phosphorylation-dependent RNase activity of GAP-SH3 binding protein: a potential link between signal transduction and RNA stability. Mol. Cell. Biol. 18, 3956-3965.
24. Ghosh, S., and Karin, M. (2002). Missing pieces in the NF-kappaB puzzle. Cell 109(Suppl), S81-S96.
25. Gilks, N., Kedersha, N., Ayodele, M., Shen, L., Stoecklin, G., Dember, L. M., and Anderson, P. (2004). Stress granule assembly is mediated by prion-like aggregation of TIA-1. Mol. Biol. Cell 15, 5383-5398.
26. Glickman, M. H., and Maytal, V. (2002). Regulating the 26S proteasome. Curr. Top. Microbiol. Immunol. 268, 43-72.
27. Green, A. M., and Steinmetz, N. D. (2002). Monitoring apoptosis in real time. Cancer J. 8, 82-92.
28. Hershko, A. (2005). The ubiquitin system for protein degradation and some of its roles in the control of the cell division cycle. Cell Death Differ. 12, 1191-1197.
29. Hershko, A., and Ciechanover, A. (1998). The ubiquitin system. Annu. Rev. Biochem. 67, 425-479.
30. Holcik, M., and Sonenberg, N. (2005). Translational control in stress and apoptosis. Nat. Rev. Mol. Cell Biol. 6, 318-327.
31. Hougardy, B. M., Maduro, J. H., van der Zee, A. G., de Groot, D. J., van den Heuvel, F. A., de Vries, E. G., and de Jong, S. (2006). Proteasome inhibitor MG132 sensitizes HPV-positive human cervical cancer cells to rhTRAIL-induced apoptosis. Int. J. Cancer 118, 1892-1900.
32. Iakova, P., Wang, G. L., Timchenko, L., Michalak, M., Pereira-Smith, O. M., Smith, J. R., and Timchenko, N. A. (2004). Competition of CUGBP1 and calreticulin for the regulation of p21 translation determines cell fate. EMBO J. 23, 406-417.
33. Jiang, H. Y., and Wek, R. C. (2005). Phosphorylation of the alpha-subunit of the eukaryotic initiation factor-2 (eIF2alpha) reduces protein synthesis and enhances apoptosis in response to proteasome inhibition. J. Biol. Chem. 280, 14189-14202.
34. Kedersha, N., and Anderson, P. (2002). Stress granules: sites of mRNA triage that regulate mRNA stability and translatability. Biochem. Soc. Trans. 30, 963-969.
35. Kedersha, N., Chen, S., Gilks, N., Li, W., Miller, I. J., Stahl, J., and Anderson, P. (2002). Evidence that ternary complex (eIF2-GTP-tRNA(i)(Met))- deficient preinitiation complexes are core constituents of mammalian stress granules. Mol. Biol. Cell 13, 195-210.
36. Kedersha, N., Cho, M. R., Li, W., Yacono, P. W., Chen, S., Gilks, N., Golan, D. E., and Anderson, P. (2000). Dynamic shuttling of TIA-1 accompanies the recruitment of mRNA to mammalian stress granules. J. Cell Biol. 151, 1257-1268.
37. Kedersha, N., Stoecklin, G., Ayodele, M., Yacono, P., Lykke-Andersen, J., Fitzler, M. J., Scheuner, D., Kaufman, R. J., Golan, D. E., and Anderson, P. (2005). Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J. Cell Biol. 169, 871-884.
38. Kedersha, N. L., Gupta, M., Li, W., Miller, I., and Anderson, P. (1999). RNA-binding proteins TIA-1 and TIAR link the phosphorylation of eIF-2 alpha to the assembly of mammalian stress granules. J. Cell Biol. 147, 1431-1442.
39. Kimball, S. R., Horetsky, R. L., Ron, D., Jefferson, L. S., and Harding, H. P. (2003). Mammalian stress granules represent sites of accumulation of stalled translation initiation complexes. Am. J. Physiol. Cell Physiol. 284, C273-C284.
40. Kodiha, M., Chu, A., Lazrak, O., and Stochaj, U. (2005). Stress inhibits nucleocytoplasmic shuttling of heat shock protein hsc70. Am. J. Physiol. Cell Physiol. 289, C1034-C1041.
41. Kuballa, P., Matentzoglu, K., and Scheffner, M. (2007). The role of the ubiquitin ligase E6-AP in human papillomavirus E6-mediated degradation of PDZ domain-containing proteins. J. Biol. Chem. 282, 65-71.
42. Laroia, G., Cuesta, R., Brewer, G., and Schneider, R. J. (1999). Control of mRNA decay by heat shock-ubiquitin-proteasome pathway. Science 284, 499-502.
43. Laroia, G., Sarkar, B., and Schneider, R. J. (2002). Ubiquitin-dependent mechanism regulates rapid turnover of AU-rich cytokine mRNAs. Proc. Natl. Acad. Sci. USA 99, 1842-1846.
44. Lee, A. H., Iwakoshi, N. N., Anderson, K. C., and Glimcher, L. H. (2003). Proteasome inhibitors disrupt the unfolded protein response in myeloma cells. Proc. Natl. Acad. Sci. USA 100, 9946-9951.
45. Li, S., Leonard, D., and Wilkinson, M. F. (1997). T cell receptor (TCR) minigene mRNA expression regulated by nonsense codons: a nuclear-associated translation-like mechanism. J. Exp. Med. 185, 985-992.
46. Lin, J. C., Hsu, M., and Tarn, W. Y. (2007). Cell stress modulates the function of splicing regulatory protein RBM4 in translation control. Proc. Natl. Acad. Sci. USA 104, 2235-2240.
47. Lykke-Andersen, J. (2002). Identification of a human decapping complex associated with hUpf proteins in nonsense-mediated decay. Mol. Cell. Biol. 22, 8114-8121.
48. Lykke-Andersen, J. (2004). Making structural sense of nonsense-mediated decay. Nat. Struct. Mol. Biol. 11, 305-306.
49. Lykke-Andersen, J., and Wagner, E. (2005). 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.
50. MacCallum, P. R., Jack, S. C., Egan, P. A., McDermott, B. T., Elliott, R. M., and Chan, S. W. (2006). Cap-dependent and hepatitis C virus internal ribosome entry site-mediated translation are modulated by phosphorylation of eIF2alpha under oxidative stress. J. Gen. Virol. 87, 3251-3262.
51. Martin, S. J., Reutelingsperger, C. P., McGahon, A. J., Rader, J. A., van Schie, R. C., LaFace, D. M., and Green, D. R. (1995). Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. J. Exp. Med. 182, 1545-1556.
52. Mazroui, R., Huot, M. E., Tremblay, S., Boilard, N., Labelle, Y., and Khandjian, E. W. (2003). Fragile X Mental Retardation protein determinants required for its association with polyribosomal mRNPs. Hum. Mol. Genet. 12, 3087-3096.
53. Mazroui, R., Huot, M. E., Tremblay, S., Filion, C., Labelle, Y., and Khandjian, E. W. (2002). Trapping of messenger RNA by Fragile X Mental Retardation protein into cytoplasmic granules induces translation repression. Hum. Mol. Genet. 11, 3007-3017.
54. Mazroui, R., Sukarieh, R., Bordeleau, M. E., Kaufman, R. J., Northcote, P., Tanaka, J., Gallouzi, I., and Pelletier, J. (2006). Inhibition of ribosome recruitment induces stress granule formation independently of eukaryotic initiation factor 2alpha phosphorylation. Mol. Biol. Cell 17, 4212-4219.
55. McInerney, G. M., Kedersha, N. L., Kaufman, R. J., Anderson, P., and Liljestrom, P. (2005). Importance of eIF2alpha phosphorylation and stress granule assembly in alphavirus translation regulation. Mol. Biol. Cell 16, 3753-3763.
56. Merita, A. B., Gabai, V. L., Yaglom, J., Shifrin, V. I., and Sherman, M. Y. (1998). Proteasome inhibitors activate stress kinases and induce Hsp72. Diverse effects on apoptosis. J. Biol. Chem. 273, 6373-6379.
57. Nandi, D., Tahiliani, P., Kumar, A., and Chandu, D. (2006). The ubiquitin-proteasome system. J. Biosci. 31, 137-155.
58. Nylandsted, J., Gyrd-Hansen, M., Danielewicz, A., Fehrenbacher, N., Lademann, U., Hoyer-Hansen, M., Weber, E., Multhoff, G., Rohde, M., and Jaattela, M. (2004). Heat shock protein 70 promotes cell survival by inhibiting lysosomal membrane permeabilization. J. Exp. Med. 200, 425-435.
59. Pritts, T. A., Hungness, E. S., Hershko, D. D., Robb, B. W., Sun, X., Luo, G. J., Fischer, J. E., Wong, H. R., and Hasselgren, P. O. (2002). Proteasome inhibitors induce heat shock response and increase IL-6 expression in human intestinal epithelial cells. Am. J. Physiol. Regul. Integr. Comp. Physiol. 282, R1016-R1026.
60. Raineri, I., Wegmueller, D., Gross, B., Certa, U., and Moroni, C. (2004). Roles of AUF1 isoforms, HuR and BRF1 in ARE-dependent mRNA turnover studied by RNA interference. Nucleic Acids Res. 32, 1279-1288.
61. Rylander, M. N., Diller, K. R., Wang, S., and Aggarwal, S. J. (2005a). Correlation of HSP70 expression and cell viability following thermal stimulation of bovine aortic endothelial cells. J. Biomech. Eng. 127, 751-757.
62. Rylander, M. N., Feng, Y., Bass, J., and Diller, K. R. (2005b). Thermally induced injury and heat-shock protein expression in cells and tissues. Ann. NY Acad. Sci. 1066, 222-242.
63. Sabourin, L. A., Tamai, K., Seale, P., Wagner, J., and Rudnicki, M. A. (2000). Caspase 3 cleavage of the Ste20-related kinase SLK releases and activates an apoptosis-inducing kinase domain and an actin-disassembling region. Mol. Cell. Biol. 20, 684-696.
64. Salomons, F. A., Verhoef, L. G., and Dantuma, N. P. (2005). Fluorescent reporters for the ubiquitin-proteasome system. Essays Biochem. 41, 113-128.
65. Scheuner, D., Song, B., McEwen, E., Liu, C., Laybutt, R., Gillespie, P., Saunders, T., Bonner-Weir, S., and Kaufman, R. J. (2001). Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol. Cell 7, 1165-1176.
66. Sheth, U., and Parker, R. (2006). Targeting of aberrant mRNAs to cytoplasmic processing bodies. Cell 125, 1095-1109.
67. Sonenberg, N., and Dever, T. E. (2003). Eukaryotic translation initiation factors and regulators. Curr. Opin. Struct. Biol. 13, 56-63.
68. Stoecklin, G., Gross, B., Ming, X. F., and Moroni, C. (2003). A novel mechanism of tumor suppression by destabilizing AU-rich growth factor mRNA. Oncogene 22, 3554-3561.
69. Stoecklin, G., Stubbs, T., Kedersha, N., Wax, S., Rigby, W. F., Blackwell, T. K., and Anderson, P. (2004). MK2-induced tristetraprolin:14-3-3 complexes prevent stress granule association and ARE-mRNA decay. EMBO J. 23, 1313-1324.
70. Stohr, N., Lederer, M., Reinke, C., Meyer, S., Hatzfeld, M., Singer, R. H., and Huttelmaier, S. (2006). ZBP1 regulates mRNA stability during cellular stress. J. Cell Biol. 175, 527-534.
71. Suzuki, K., Kostin, S., Person, V., Elsasser, A., and Schaper, J. (2001). Time course of the apoptotic cascade and effects of caspase inhibitors in adult rat ventricular cardiomyocytes. J. Mol. Cell. Cardiol. 33, 983-994.
72. Takimoto, C. H., and Diggikar, S. (2002). Heat shock protein and proteasome targeting agents. Hematol. Oncol. Clin. North Am. 16, 1269-1285.
73. Tourriere, H., Chebli, K., and Tazi, J. (2002). mRNA degradation machines in eukaryotic cells. Biochimie 84, 821-837.
74. Vabulas, R. M., and Hartl, F. U. (2005). Protein synthesis upon acute nutrient restriction relies on proteasome function. Science 310, 1960-1963.
75. Voorhees, P. M., and Orlowski, R. Z. (2006). The proteasome and proteasome inhibitors in cancer therapy. Annu. Rev. Pharmacol. Toxicol. 46, 189-213.
76. Wang, W., Furneaux, H., Cheng, H., Caldwell, M. C., Hutter, D., Liu, Y., Holbrook, N., and Gorospe, M. (2000). HuR regulates p21 mRNA stabilization by UV light. Mol. Cell. Biol. 20, 760-769.
77. Wek, R. C., Jiang, H. Y., and Anthony, T. G. (2006). Coping with stress: eIF2 kinases and translational control. Biochem. Soc. Trans. 34, 7-11.
78. Yoshida, M., Yoshida, K., Kozlov, G., Lim, N. S., De Crescenzo, G., Pang, Z., Berlanga, J. J., Kahvejian, A., Gehring, K., Wing, S. S., and Sonenberg, N. (2006). Poly(A) binding protein (PABP) homeostasis is mediated by the stability of its inhibitor, Paip2. EMBO J. 25, 1934-1944.
79. Zimmermann, J., Erdmann, D., Lalande, I., Grossenbacher, R., Noorani, M., and Furst, P. (2000). Proteasome inhibitor induced gene expression profiles reveal overexpression of transcriptional regulators ATF3, GADD153 and MAD1. Oncogene 19, 2913-2920.
80. Zou, H., Henzel, W. J., Liu, X., Lutschg, A., and Wang, X. (1997). Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell 90, 405-413.