Hypoxia inhibits protein synthesis through a 4E-BP1 and elongation factor 2 kinase pathway controlled by mTOR and uncoupled in breast cancer cells

Molecular and Cellular Biology

Volumn 26, Issue 10, 2006, Pages 3955-3965

  Connolly, Eileen ^a   Braunstein, Steve ^a   Formenti, Silvia ^a   Schneider, Robert J ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ELONGATION FACTOR 2; ELONGATION FACTOR 2 KINASE; INITIATION FACTOR 2ALPHA; INITIATION FACTOR 4A; INITIATION FACTOR 4E; INITIATION FACTOR 4E BINDING PROTEIN 1; INITIATION FACTOR 4G; MAMMALIAN TARGET OF RAPAMYCIN; METHIONINE; PROTEIN KINASE; S6 KINASE; SMALL INTERFERING RNA; SULFUR 35; TUBERIN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BREAST CANCER; BREAST EPITHELIUM; CELL IMMORTALIZATION; CELL TRANSFORMATION; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; EPITHELIUM CELL; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; HYPOXIA; IMMUNOBLOTTING; IMMUNOPRECIPITATION; PRIORITY JOURNAL; PROTEIN SYNTHESIS INHIBITION; RETROVIRUS; RNA TRANSLATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANOXIA; BLOTTING, WESTERN; BREAST NEOPLASMS; CARCINOMA, INTRADUCTAL, NONINFILTRATING; CELL LINE, TRANSFORMED; CELL LINE, TUMOR; ENZYME ACTIVATION; FEMALE; GENE SILENCING; HUMANS; METHIONINE; PEPTIDE ELONGATION FACTOR 2; PHOSPHOPROTEINS; PHOSPHORYLATION; PRECIPITIN TESTS; PROTEIN KINASES; RETROVIRIDAE; RIBOSOMAL PROTEIN S6 KINASES; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SULFUR RADIOISOTOPES;

EUKARYOTA;

EID: 33646550165     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.26.10.3955-3965.2006     Document Type: Article

References (51)

1. Arora, S., J. M. Yang, and W. N. Hait. 2005. Identification of the ubiquitin-proteasome pathway in the regulation of the stability of eukaryoke elongation factor-2 kinase. Cancer Res. 65:3806-3810.
2. 1a. Arsham, A. M., J. J. Howell, and M. C. Simon. 2003. A novel hypoxia-inducible factor-independent hypoxic response regulating mammalian target of rapamycin and its targets. J. Biol. Chem. 278:29655-29660.
3. Blais, J. D., V. Filipenko, M. Bi, H. P. Harding, D. Ron, C. Koumenis, B. G. Wouters, and J. C. Bell. 2004. Activating transcription factor 4 is translationally regulated by hypoxic stress. Mol. Cell. Biol. 24:7469-7482.
4. Bolster, D. R., S. J. Crozier, S. R. Kimball, and L. S. Jefferson. 2002. AMP-activated protein kinase suppresses protein synthesis in rat skeletal muscle through down-regulated mammalian target of rapamycin (mTOR) signaling. J. Biol. Chem. 277:23977-23980.
5. Browne, G. J., and C. G. Proud. 2004. A novel mTOR-regulated phosphorylation site in elongation factor 2 kinase modulates the activity of the kinase and its binding to calmodulin. Mol. Cell. Biol. 24:2986-2997.
6. Browne, G. J., and C. G. Proud. 2002. Regulation of peptide-chain elongation in mammalian cells. Eur. J. Biochem. 269:5360-5368.
7. Brugarolas, J., K. Lei, R. L. Hurley, B. D. Manning, J. H. Reiling, E. Hafen, L. A. Witters, L. W. Ellisen, and W. G. Kaelin, Jr. 2004. Regulation of mTOR function in response to hypoxia by REDD1 and the TSC1/TSC2 tumor suppressor complex. Genes Dev. 18:2893-2904.
8. Brugarolas, J. B., F. Vazquez, A. Reddy, W. R. Sellers, and W. G. Kaelin, Jr. 2003. TSC2 regulates VEGF through mTOR-dependent and -independent pathways. Cancer Cell 4:147-158.
9. Burdall, S. E., A. M. Hanby, M. R. Lansdown, and V. Speirs. 2003. Breast cancer cell lines: friend or foe? Breast Cancer Res. 5:89-95.
10. Carsillo, T., A. Astrinidis, and E. P. Henske. 2000. Mutations in the tuberous sclerosis complex gene TSC2 are a cause of sporadic pulmonary lymphangioleiomyomatosis. Proc. Natl. Acad. Sci. USA 97:6085-6090.
11. Chiang, G. G., and R. T. Abraham. 2005. Phosphorylation of mammalian target of rapamycin (mTOR) at Ser-2448 is mediated by p70S6 kinase. J. Biol. Chem. 280:25485-25490.
12. Clemens, M. J. 2004. Targets and mechanisms for the regulation of translation in malignant transformation. Oncogene 23:3180-3188.
13. Corradetti, M. N., K. Inoki, and K. L. Guan. 2005. The stress-inducted proteins RTP801 and RTP801L are negative regulators of the mammalian target of rapamycin pathway. J. Biol. Chem. 280:9769-9772.
14. Cuesta, R., G. Laroia, and R. J. Schneider. 2000. Chaperone Hsp27 promotes disassembly of translation cap initiation complex during heat shock. Genes Dev. 14:1460-1470.
15. Elbashir, S. M., J. Harborth, W. Lendeckel, A. Yalcin, K. Weber, and T. Tuschl. 2001. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411:494-498.
16. Gingras, A.-C., B. Raught, and N. Sonenberg. 1999. elF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu. Rev. Biochem. 68:913-963.
17. Hay, N., and N. Sonenberg. 2004. Upstream and downstream of mTOR. Genes Dev. 18:1926-1945.
18. Hochachka, P. W., L. T. Buck, C. J. Doll, and S. C. Land. 1996. Unifying theory of hypoxia tolerance: molecular/metabolic defense and rescue mechanisms for surviving oxygen lack. Proc. Natl. Acad. Sci. USA 93:9493-9498.
19. Hochachka, P. W., and P. L. Lutz. 2001. Mechanism, origin, and evolution of anoxia tolerance in animals. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 130:435-459.
20. Hockel, M., and P. Vaupel. 2001. Tumor hypoxia: definitions and current clinical, biologic, and molecular aspects. J. Natl. Cancer Inst. 93:266-276.
21. Holz, M. K., and J. Blenis. 2005. Identification of S6 kinase 1 as a novel mammalian target of rapamycin (mTOR)-phosphorylating kinase. J. Biol. Chem. 280:26089-26093.
22. Herman, S., G. Browne, U. Krause, J. Patel, D. Vertommen, L. Bertrand, A. Lavoinne, L. Hue, C. Proud, and M. Rider. 2002. Activation of AMP-activated protein kinase leads to the phosphorylation of elongation factor 2 and an inhibition of protein synthesis. Curr. Biol. 12:1419-1423.
23. Huez, I., L. Créancier, S. Audigier, M.-C. Gensac, A.-C. Prats, and H. Prats. 1998. Two independent internal ribosome entry sites are involved in translation initiation of vascular endothelial growth factor mRNA. Mol. Cell. Biol. 18:6178-6190.
24. Inoki, K., M. N. Corradetti, and K. L. Guan. 2005. Dysregulation of the TSC-mTOR pathway in human disease. Nat. Genet. 37:19-24.
25. Inoki, K., T. Zhu, and K. L. Guan. 2003. TSC2 mediates cellular energy response to control cell growth and survival. Cell 115:577-590.
26. Koumenis, C., C. Naczki, M. Koritzinsky, S. Rastani, A. Diehl, N. Sonenberg, A. Koromilas, and B. G. Wouters. 2002. Regulation of protein synthesis by hypoxia via activation of the endoplasmic reticulum kinase PERK and phosphorylation of the translation initiation factor eIF2α. Mol. Cell. Biol. 22:7405-7416.
27. Krause, U., L. Bertrand, and L. Hue. 2002. Control of p70 ribosomal protein S6 kinase and acetyl-CoA carboxylase by AMP-activated protein kinase and protein phosphatases in isolated hepatocytes. Eur. J. Biochem. 269:3751-3759.
28. Lang, K. J., A. Kappel, and G. J. Goodall. 2002. Hypoxia-inducible factor-1alpha mRNA contains an internal ribosome entry site that allows efficient translation during normoxia and hypoxia. Mol. Biol. Cell 13:1792-1801.
29. Le, Q. T., N. C. Denko, and A. J. Giaccia. 2004. Hypoxic gene expression and metastasis. Cancer Metastasis Rev. 23:293-310.
30. Liu, L., T. P. Cash, R. G. Jones, B. Keith, C. B. Thompson, and M. C. Simon. 2006. Hypoxia-induced energy stress regulates mRNA translation and cell growth. Mol. Cell 21:521-531.
31. Liu, L., and M. C. Simon. 2004. Regulation of transcription and translation by hypoxia. Cancer Biol. Ther. 3:492-497.
32. Manning, B. D., A. R. Tee, M. N. Logsdon, J. Blenis, and L. C. Cantley. 2002. Identification of the tuberous sclerosis complex-2 tumor suppressor gene product tuberin as a target of the phosphoinositide 3-kinase/akt pathway. Mol. Cell 10:151-162.
33. Marienfeld, C., Y. Yamagiwa, Y. Ueno, V. Chiasson, L. Brooks, F. Meng, and T. Patel. 2004. Translational regulation of XIAP expression and cell survival during hypoxia in human cholangiocarcinoma. Gastroenterology 127:1787-1797.
34. Novoa, I., H. Zeng, H. P. Harding, and D. Ron. 2001. Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2alpha. J. Cell Biol. 153:1011-1022.
35. Pestova, T. V., V. G. Kolupaeva, I. B. Lomakin, E. V. Pilipenko, I. N. Shatsky, V. I. Agol, and C. U. Hellen. 2001. Molecular mechanisms of translation initiation in eukaryotes. Proc. Natl. Acad. Sci. USA 98:7029-7036.
36. Proud, C. G. 2004. The multifaceted role of mTOR in cellular stress responses. DNA Repair (Amsterdam) 3:927-934.
37. Rajasekhar, V. K., A. Viale, N. D. Socci, M. Wiedmann, X. Hu, and E. C. Holland. 2003. Oncogenic Ras and Akt signaling contribute to glioblastoma formation by differential recruitment of existing mRNAs to polysomes. Mol. Cell 12:889-901.
38. Reynolds, T. H., IV, S. C. Bodine, and J. C. Lawrence, Jr. 2002. Control of Ser2448 phosphorylation in the mammalian target of rapamycin by insulin and skeletal muscle load. J. Biol. Chem. 277:17657-17662.
39. Rosenwald, I. B. 2004. The role of translation in neoplastic transformation from a pathologist's point of view. Oncogene 23:3230-3247.
40. Scavelli, C., A. Vacca, G. Di Pietro, F. Dammacco, and D. Ribatti. 2004. Crosstalk between angiogenesis and lymphangiogenesis in tumor progression. Leukemia 18:1054-1058.
41. Schwarzer, R., D. Tondera, W. Arnold, K. Giese, A. Klippel, and J. Kaufmann. 2005. REDD1 integrates hypoxia-mediated survival signaling down-stream of phosphatidylinositol 3-kinase. Oncogene 24:1138-1149.
42. Sekulic, A., C. C. Hudson, J. L. Homme, P. Yin, D. M. Otterness, L. M. Karnitz, and R. T. Abraham. 2000. A direct linkage between the phosphoinositide 3-kinase-AKT signaling pathway and the mammalian target of rapamycin in mitogen-stimulated and transformed cells. Cancer Res. 60: 3504-3513.
43. Sofer, A., K. Lei, C. M. Johannessen, and L. W. Ellisen. 2005. Regulation of mTOR and cell growth in response to energy stress by REDD1. Mol. Cell. Biol. 25:5834-5845.
44. Soule, H. D., T. M. Maloney, S. R. Wolman, W. D. Peterson, Jr., R. Brenz, C. M. McGrath, J. Russo, R. J. Pauley, R. F. Jones, and S. C. Brooks. 1990. Isolation and characterization of a spontaneously immortalized human breast epithelial cell line, MCF-10. Cancer Res. 50:6075-6086.
45. Stein, I., A. Itin, P. Einat, R. Skaliter, Z. Grossman, and E. Keshet. 1998. Translation of vascular endothelial growth factor mRNA by internal ribosome entry: implications for translation under hypoxia. Mol. Cell. Biol. 18:3112-3119.
46. Tinton, S. A., and P. M. Buc-Calderon. 1999. Hypoxia increases the association of 4E-binding protein 1 with the initiation factor 4E in isolated rat hepatocytes. FEBS Lett. 446:55-59.
47. Wang, X., W. Li, M. Williams, N. Terada, D. R. Alessi, and C. G. Proud. 2001. Regulation of elongation factor 2 kinase by p90(RSK1) and p70 S6 kinase. EMBO J. 20:4370-4379.
48. Willis, A. E. 1999. Translational control of growth factor and proto-oncogene expression. Int. J. Biochem. Cell. Biol. 31:73-86.
49. Winder, W. W. 2001. Energy-sensing and signaling by AMP-activated protein kinase in skeletal muscle. J. Appl. Physiol. 91:1017-1028.
50. Wouters, B. G., T. van den Beucken, M. G. Magagnin, P. Lambin, and C. Koumenis. 2004. Targeting hypoxia tolerance in cancer. Drug Resist. Updates 7:25-40.
51. Zimonjic, D. B., C. L. Keck-Waggoner, B. Z. Yuan, M. H. Kraus, and N. C. Popescu. 2000. Profile of genetic alterations and tumorigenicity of human breast cancer cells. Int. J. Oncol. 16:221-230.