mRNA escape from stress granule sequestration is dictated by localization to the endoplasmic reticulum

FASEB Journal

Volumn 24, Issue 9, 2010, Pages 3370-3380

  Unsworth, H ^a,c   Raguz, S ^a   Edwards, H J ^a   Higgins, C F ^a,d   Yague E ^a,b  

^a MEDICAL RESEARCH COUNCIL   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d DURHAM UNIVERSITY   (United Kingdom)

Author keywords

Drug resistance; Membrane proteins; P glycoprotein; RNA localization; TIA 1

Indexed keywords

GLYCOPROTEIN P; INITIATION FACTOR 2ALPHA; MEMBRANE PROTEIN; MESSENGER RNA; MULTIDRUG RESISTANCE PROTEIN 1; NUCLEAR RNA; PUROMYCIN; RNA BINDING PROTEIN;

ARTICLE; CELL SURVIVAL; CELLULAR DISTRIBUTION; CHIMERA; CONTROLLED STUDY; CYTOPLASM; CYTOSOL; DETOXIFICATION; ENDOPLASMIC RETICULUM; HUMAN; HUMAN TISSUE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; STRESS;

ARSENITES; BIOLOGICAL TRANSPORT; CELL LINE; CELL LINE, TUMOR; CYTOPLASMIC GRANULES; ENDOPLASMIC RETICULUM; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MEMBRANE PROTEINS; P-GLYCOPROTEIN; POLYRIBOSOMES; PUROMYCIN; RNA, MESSENGER;

MAMMALIA;

EID: 77956621599     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.09-151142     Document Type: Article

References (34)

1. Gebauer, F., and Hentze, M. W. (2004) Molecular mechanisms of translational control. Nat. Rev. Mol. Cell. Biol. 5, 827-835
2. Proud, C. G. (2005) eIF2 and the control of cell physiology. Semin. Cell. Dev. Biol. 16, 3-12
3. Anderson, P., and Kedersha, N. (2002) Stressful initiations. J. Cell Sci. 115, 3227-3234
4. Anderson, P., and Kedersha, N. (2006) RNA granules. J. Cell Biol. 172, 803-808
5. 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
6. Kedersha, N., Stoecklin, G., Ayodele, M., Yacono, P., Lykke-Andersen, J., Fritzler, 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
7. 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
8. Modok, S., Mellor, H. R., and Callaghan, R. (2006) Modulation of multidrug resistance efflux pump activity to overcome chemoresistance in cancer. Curr. Opin. Pharmacol. 6, 350-354 (Pubitemid 44026037)
9. Callaghan, R., Crowley, E., Potter, S., and Kerr, I. D. (2008) Pglycoprotein: so many ways to turn it on. J. Clin. Pharmacol. 48, 365-378
10. Liscovitch, M., and Ravid, D. (2007) A case study in misidentification of cancer cell lines: MCF-7/AdrR cells (re-designated NCI/ADR-RES) are derived from OVCAR-8 human ovarian carcinoma cells. Cancer Lett. 245, 350-352 (Pubitemid 44959366)
11. Raguz, S., Randle, R. A., Sharpe, E. R., Foekens, J. A., Sieuwerts, A. M., Meijer-van Gelder, M. E., Melo, J. V., Higgins, C. F., and Yague, E. (2008) Production of P-glycoprotein from the MDR1 upstream promoter is insufficient to affect the response to first-line chemotherapy in advanced breast cancer. Int. J. Cancer 122, 1058-1067 (Pubitemid 351214003)
12. Randle, R. A., Raguz, S., Higgins, C. F., and Yague, E. (2007) Role of the highly structured 5′-end region of MDR1 mRNA on P-glycoprotein expression. Biochem. J. 406, 445-455 (Pubitemid 47425451)
13. Kostenko, E. V., Beabealashvilly, R. S., Vlassov, V. V., and Zenkova, M. A. (2000) Secondary structure of the 5′-region of PGY1/MDR1 mRNA. FEBS Lett. 475, 181-186
14. Blott, E. J., Higgins, C. F., and Linton, K. J. (1999) Cysteine-scanning mutagenesis provides no evidence for the extracellular accessibility of the nucleotide-binding domains of the multidrug resistance transporter P-glycoprotein. EMBO J. 18, 6800-6808
15. Yague, E., Armesilla, A. L., Harrison, G., Elliott, J., Sardini, A., Higgins, C. F., and Raguz, S. (2003) P-glycoprotein (MDR1) expression in leukemic cells is regulated at two distinct steps, mRNA stabilization and translational initiation. J. Biol. Chem. 278, 10344-10352 (Pubitemid 36800297)
16. Stoneley, M., Subkhankulova, T., Le Quesne, J. P., Coldwell, M. J., Jopling, C. L., Belsham, G. J., and Willis, A. E. (2000) Analysis of the c-myc IRES: a potential role for cell-type specific trans-acting factors and the nuclear compartment. Nucleic Acids Res. 28, 687-694
17. Bonifacino, J. S. (1998) Metabolic labelling with amino acids. In Current Protocols in Molecular Biology (Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A., and Struhl, K., eds), sec. 10.18.1-10.18.10, John Wiley and Sons, New York
18. Lerner, R. S., Seiser, R. M., Zheng, T., Lager, P. J., Reedy, M. C., Keene, J. D., and Nicchitta, C. V. (2003) Partitioning and translation of mRNAs encoding soluble proteins on membrane-bound ribosomes. RNA 9, 1123-1137
19. Vattem, K. M., and Wek, R. C. (2004) Reinitiation involving upstream ORFs regulates ATF4 mRNA translation in mammalian cells. Proc. Natl. Acad. Sci. U. S. A. 101, 11269-11274
20. 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
21. Eulalio, A., Behm-Ansmant, I., and Izaurralde, E. (2007) P bodies: at the crossroads of post-transcriptional pathways. Nat. Rev. Mol. Cell. Biol. 8, 9-22
22. Lopez de Silanes, I., Galban, S., Martindale, J. L., Yang, X., Mazan-Mamczarz, K., Indig, F. E., Falco, G., Zhan, M., and Gorospe, M. (2005) Identification and functional outcome of mRNAs associated with RNA-binding protein TIA-1. Mol. Cell. Biol. 25, 9520-9531
23. Egea, P. F., Stroud, R. M., and Walter, P. (2005) Targeting proteins to membranes: structure of the signal recognition particle. Curr. Opin. Struct. Biol. 15, 213-220
24. Skach, W. R., and Lingappa, V. R. (1993) Amino-terminal assembly of human P-glycoprotein at the endoplasmic reticulum is directed by cooperative actions of two internal sequences. J. Biol. Chem. 268, 23552-23561
25. Nicchitta, C. V., Lerner, R. S., Stephens, S. B., Dodd, R. D., and Pyhtila, B. (2005) Pathways for compartmentalizing protein synthesis in eukaryotic cells: the template-partitioning model. Biochem. Cell Biol. 83, 687-695
26. Sivan, G., Kedersha, N., and Elroy-Stein, O. (2007) Ribosomal slowdown mediates translational arrest during cellular division. Mol. Cell. Biol. 27, 6639-6646
27. Lerner, R. S., and Nicchitta, C. V. (2006) mRNA translation is compartmentalized to the endoplasmic reticulum following physiological inhibition of cap-dependent translation. RNA 12, 775-789
28. Stephens, S. B., Dodd, R. D., Brewer, J. W., Lager, P. J., Keene, J. D., and Nicchitta, C. V. (2005) Stable ribosome binding to the endoplasmic reticulum enables compartment-specific regulation of mRNA translation. Mol. Biol. Cell 16, 5819-5831
29. Thermann, R., and Hentze, M. W. (2007) Drosophila miR2 induces pseudo-polysomes and inhibits translation initiation. Nature 447, 875-878
30. Zhang, J. T. (1996) Sequence requirements for membrane assembly of polytopic membrane proteins: molecular dissection of the membrane insertion process and topogenesis of the human MDR3 P-glycoprotein. Mol. Biol. Cell 7, 1709-1721
31. Anthony, V., and Skach, W. R. (2002) Molecular mechanism of P-glycoprotein assembly into cellular membranes. Curr. Protein Pept. Sci. 3, 485-501
32. Borgese, N., Brambillasca, S., and Colombo, S. (2007) How tails guide tail-anchored proteins to their destinations. Curr. Opin. Cell Biol. 19, 368-375
33. Mambula, S. S., Stevenson, M. A., Ogawa, K., and Calderwood, S. K. (2007) Mechanisms for Hsp70 secretion: crossing membranes without a leader. Methods 43, 168-175
34. Heinrich, S. U., and Rapoport, T. A. (2003) Cooperation of transmembrane segments during the integration of a double-spanning protein into the ER membrane. EMBO J. 22, 3654-3663