Escape from stress granule sequestration: Another way to drug resistance?

Biochemical Society Transactions

Volumn 38, Issue 6, 2010, Pages 1537-1542

  Yagüe, Ernesto ^a   Raguz, Selina ^b  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Drug resistance; Endoplasmic reticulum; Multidrug resistance 1 (MDR1); P glycoprotein; Stress granule; T cell restricted intracellular antigen 1 (TIA 1)

Indexed keywords

BREAST CANCER RESISTANCE PROTEIN; DNA; GLYCOPROTEIN P; INHIBITOR OF APOPTOSIS PROTEIN; INITIATION FACTOR 4E; MESSENGER RNA; MULTIDRUG RESISTANCE PROTEIN 1; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN P53;

BRAIN CORTEX; CELL GRANULE; CONFERENCE PAPER; CYTOTOXICITY; DNA PROTEIN COMPLEX; DNA STRUCTURE; DRUG RESISTANCE; ENDOPLASMIC RETICULUM; HUMAN; LEUKEMIA CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; STRESS; TRANSLATION REGULATION;

ANIMALS; ANTINEOPLASTIC AGENTS; ARSENITES; CYTOPLASMIC GRANULES; DRUG RESISTANCE; GENE EXPRESSION REGULATION; HUMANS; NEOPLASMS; P-GLYCOPROTEIN; PROTEIN BIOSYNTHESIS; RNA, MESSENGER; STRESS, PHYSIOLOGICAL; TERATOGENS;

EID: 78649721959     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST0381537     Document Type: Conference Paper

References (46)

1. Raguz, S. and Yagüe, E. (2008) Resistance to chemotherapy: new treatments and novel insights into an old problem. Br. J. Cancer 99, 387-391
2. Gottesman, M.M. and Ling, V. (2006) The molecular basis of multidrug resistance in cancer: the early years of P-glycoprotein research. FEBS Lett. 580, 998-1009
3. Leslie, E.M., Deeley, R.G. and Cole, S.P. (2005) Multidrug resistance proteins: role of P-glycoprotein, MRP1, MRP2, and BCRP (ABCG2) in tissue defenseToxicol. Appl. Pharmacol. 204, 216-237
4. 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
5. Aller, S.G., Yu, J., Ward, A., Weng, Y., Chittaboina, S., Zhuo, R., Harrell, P.M., Trinh, Y.T., Zhang, Q., Urbatsch, I.L. and Chang, G. (2009) Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding. Science 323, 1718-1722
6. Szakacs, G., Paterson, J.K., Ludwig, J.A., Booth-Genthe, C. and Gottesman, M.M. (2006) Targeting multidrug resistance in cancer. Nat. Rev. Drug Discov. 5, 219-234
7. Pallis, M., Fisher, J., Truran, L., Grundy, M., Russell, N. and Burnett, A. (2005) Reproducible measurements of AML blast p-glycoprotein function in 2 center analyses. Blood 105, 1367-1368
8. Jin, S., Gorfajn, B., Faircloth, G. and Scotto, K.W. (2000) Ecteinascidin 743, a transcription-targeted chemotherapeutic that inhibits MDR1 activation. Proc. Natl. Acad. Sci. U.S.A. 97, 6775-6779
9. Le Cesne, A., Blay, J.Y., Judson, I., Van Oosterom, A., Verweij, J., Radford, J., Lorigan, P., Rodenhuis, S., Ray-Coquard, I., Bonvalot, S. et al. (2005) Phase II study of ET-743 in advanced soft tissue sarcomas: a European Organisation for the Research and Treatment of Cancer (EORTC) soft tissue and bone sarcoma group trial. J. Clin. Oncol. 23, 576-584
10. Lee, C.H., Bradley, G. and Ling, V. (1998) Increased P-glycoprotein messenger RNA stability in rat liver tumors in vivo. J. Cell. Physiol. 177, 1-12
11. Zhang, Z., Wu, J.-Y., Hait, W.N. and Yang, J.-M. (2004) Regulation of the stability of P-glycoprotein by ubiquitination. Mol. Pharmacol. 66, 395-403
12. Meschini, S., Calcabrini, A., Monti, E., Del Bufalo, D., Stringaro, A., Dolfini, E. and Arancia, G. (2000) Intracellular P-glycoprotein expression is associated with the intrinsic multidrug resistance phenotype in human colon adenocarcinoma cells. Int. J. Cancer 87, 615-628
13. Jin, S. and Scotto, K.W. (1998) Transcriptional regulation of the MDR1 gene by histone acetyltransferase and deacetylase is mediated by NF-Y. Mol. Cell. Biol. 18, 4377-4384
14. van Kalken, C., Giaccone, G., van der Valk, P., Kuiper, C.M., Hadisaputro, M.M., Bosma, S.A., Scheper, R.J., Meijer, C.J. and Pinedo, H.M. (1992) Multidrug resistance gene (P-glycoprotein) expression in the human fetus. Am. J. Pathol. 141, 1063-1072
15. Nakayama, M., Wada, M., Harada, T., Nagayama, J., Kusaba, H., Ohshima, K., Kozuru, M., Komatsu, H., Ueda, R. and Kuwano, M. (1998) Hypomethylation status of CpG sites at the promoter region and overexpression of the human MDR1 gene in acute myeloid leukemias. Blood 92, 4296-4307
16. Yagüe, 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
17. Gebauer, F. and Hentze, M.W. (2004) Molecular mechanisms of translational control. Nat. Rev. Mol. Cell Biol. 5, 827-835
18. Randle, R.A., Raguz, S., Higgins, C.F. and Yagüe, E. (2007) Role of the highly structured 5′-end region of MDR1 mRNA on P-glycoprotein expression. Biochem. J. 406, 445-455
19. 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
20. Kondo, T., Setoguchi, T. and Taga, T. (2004) Persistence of a small subpopulation of cancer stem-like cells in the C6 glioma cell line. Proc. Natl. Acad. Sci. U.S.A. 101, 781-786
21. Baker, E.K., Johnstone, R.W., Zalcberg, J.R. and El-Osta, A. (2005) Epigenetic changes to the MDR1 locus in response to chemotherapeutic drugs. Oncogene 24, 8061-8075
22. Chaudhary, P.M. and Roninson, I.B. (1991) Expression and activity of P-glycoprotein, a multidrug efflux pump, in human hematopoietic stem cells. Cell 66, 85-94
23. Graff, J.R., Konicek, B.W., Carter, J.H. and Marcusson, E.G. (2008) Targeting the eukaryotic translation initiation factor 4E for cancer therapy. Cancer Res. 68, 631-634
24. Soni, A., Akcakanat, A., Singh, G., Luyimbazi, D., Zheng, Y., Kim, D., Gonzalez-Angulo, A. and Meric-Bernstam, F. (2008) eIF4E knockdown decreases breast cancer cell growth without activating Akt signaling. Mol. Cancer Ther. 7, 1782-1788
25. Dong, K., Wang, R., Wang, X., Lin, F., Shen, J.J., Gao, P. and Zhang, H.Z. (2009) Tumor-specific RNAi targeting eIF4E suppresses tumor growth, induces apoptosis and enhances cisplatin cytotoxicity in human breast carcinoma cells. Breast Cancer Res. Treat. 113, 443-456
26. Tan, K., Culjkovic, B., Amri, A. and Borden, K.L.B. (2008) Ribavirin targets eIF4E dependent Akt survival signaling. Biochem. Biophys. Res. Commun. 375, 341-345
27. Assouline, S., Culjkovic, B., Cocolakis, E., Rousseau, C., Beslu, N., Amri, A., Caplan, S., Leber, B., Roy, D.C., Miller, Jr, W.H. and Borden, K.L. (2009) Molecular targeting of the oncogene eIF4E in acute myeloid leukemia (AML): a proof-of-principle clinical trial with ribavirin. Blood 114, 257-260
28. Callaghan, R., Crowley, E., Potter, S. and Kerr, I.D. (2008) P-glycoprotein: so many ways to turn it on. J. Clin. Pharmacol. 48, 365-378
29. Proud, C.G. (2005) eIF2 and the control of cell physiology. Semin. Cell Dev. Biol. 16, 3-12
30. Anderson, P. and Kedersha, N. (2002) Stressful initiations. J. Cell Sci. 115, 3227-3234
31. Anderson, P. and Kedersha, N. (2009) RNA granules: post-transcriptional and epigenetic modulators of gene expression. Nat. Rev. Mol. Cell Biol. 10, 430-436
32. Buchan, J.R. and Parker, R. (2009) Eukaryotic stress granules: the ins and outs of translation. Mol. Cell 36, 932-941
33. 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
34. 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-2α to the assembly of mammalian stress granules. J. Cell Biol. 147, 1431-1442
35. Anderson, P. and Kedersha, N. (2006) RNA granules. J. Cell Biol. 172, 803-808
36. Anderson, P. and Kedersha, N. (2008) Stress granules: the Tao of RNA triage. Trends Biochem. Sci. 33, 141-150
37. 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
38. 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
39. 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
40. Unsworth, H., Raguz, S., Edwards, H.J., Higgins, C.F. and Yagüe, E. (2010) mRNA escape from stress granule sequestration is dictated by localization to the endoplasmic reticulum. FASEB J. 24, 3370-3380
41. Stoneley, M. and Willis, A.E. (2004) Cellular internal ribosome entry segments: structures, trans-acting factors and regulation of gene expression. Oncogene 23, 3200-3207
42. Sivan, G., Kedersha, N. and Elroy-Stein, O. (2007) Ribosomal slowdown mediates translational arrest during cellular division. Mol. Cell. Biol. 27, 6639-6646
43. 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
44. Thermann, R. and Hentze, M.W. (2007) Drosophila miR2 induces pseudo-polysomes and inhibits translation initiation. Nature 447, 875-878
45. 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
46. 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