Activating transcription factor 4 is translationally regulated by hypoxic stress

Molecular and Cellular Biology

Volumn 24, Issue 17, 2004, Pages 7469-7482

  Blais, Jaime D ^a,b   Filipenko, Vasilisa ^b   Bi, Meixia ^c   Harding, Heather P ^d   Ron, David ^d   Koumenis, Costas ^c   Wouters, Bradly G ^e   Bell, John C ^a,f  

^a OTTAWA REGIONAL CANCER CENTRE   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

^c WAKE FOREST SCHOOL OF MEDICINE   (United States)

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

^e MAASTRICHT UNIVERSITY   (Netherlands)

^f ORCC   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; ENDOPLASMIC RETICULUM KINASE; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 34; INITIATION FACTOR 2; INITIATION FACTOR 2ALPHA; MESSENGER RNA; PHOSPHOTRANSFERASE; RNA; SERINE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ADAPTATION; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DNA MICROARRAY; EMBRYO; HELA CELL; HUMAN; HUMAN CELL; HYPOXIA; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYSOME; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS INHIBITION; RNA TRANSLATION; SIGNAL TRANSDUCTION; STRESS; TRANSLATION REGULATION; UNINDEXED SEQUENCE;

ACTIVATING TRANSCRIPTION FACTOR 4; ANIMALS; ANTIGENS, DIFFERENTIATION; CELL CYCLE PROTEINS; CELL HYPOXIA; EIF-2 KINASE; EUKARYOTIC INITIATION FACTOR-2; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HELA CELLS; HUMANS; MICE; NEOPLASM PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXIDATIVE STRESS; PHOSPHORYLATION; POLYRIBOSOMES; PROTEIN BIOSYNTHESIS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

ANIMALIA; EUKARYOTA;

EID: 4344648874     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.17.7469-7482.2004     Document Type: Article

References (64)

1. Ameri, K., C. E. Lewis, M. Raida, H. Sowter, T. Hai, and A. L. Harris. 2003. Anoxic induction of ATF-4 via HIF-1 independent pathways of protein stabilization in human cancer cells. Blood 103:1876-1882.
2. Bernstein, J., O. Sella, S. Y. Le, and O. Elroy-Stein. 1997. PDGF2/c-sis mRNA leader contains a differentiation-linked internal ribosomal entry site (D-IRES). J. Biol. Chem. 272:9356-9362.
3. Bowers, A. J., S. Scully, and J. F. Boylan. 2003. SKIP3, a novel Drosophila tribbles ortholog, is overexpressed in human tumors and is regulated by hypoxia. Oncogene 22:2823-2835.
4. Brown, J. M., and A. J. Giaccia. 1998. The unique physiology of solid tumors: opportunities (and problems) for cancer therapy. Cancer Res. 58:1408-1416.
5. Brown, J. M., and Q. T. Le. 2002. Tumor hypoxia is important in radiotherapy, but how should we measure it? Int. J. Radiat. Oncol. Biol. Phys. 54: 1299-1301.
6. Bruick, R. K. 2000. Expression of the gene encoding the proapoptotic Nip3 protein is induced by hypoxia. Proc. Natl. Acad. Sci. USA 97:9082-9087.
7. Carmeliet, P., Y. Dor, J. M. Herbert, D. Fukumura, K. Brusselmans, M. Dewerchin, M. Neeman, F. Bono, R. Abramovitch, P. Maxwell, C. J. Koch, P. Ratcliffe, L. Moons, R. K. Jain, D. Collen, E. Keshert, and E. Keshet. 1998. Role of HIF-1α in hypoxia-mediated apoptosis, cell proliferation, and tumour angiogenesis. Nature 394:485-490.
8. Coldwell, M. J., S. A. Mitchell, M. Stoneley, M. MacFarlane, and A. E. Willis. 2000. Initiation of Apaf-1 translation by internal ribosome entry. Oncogene 19:899-905.
9. Connor, J. H., D. C. Weiser, S. Li, J. M. Hallenbeck, and S. Shenolikar. 2001. Growth arrest and DNA damage-inducible protein GADD34 assembles a novel signaling complex containing protein phosphatase 1 and inhibitor 1. Mol. Cell. Biol. 21:6841-6850.
10. Cormier-Regard, S., S. V. Nguyen, and W. C. Claycomb. 1998. Adrenomedullin gene expression is developmentally regulated and induced by hypoxia in rat ventricular cardiac myocytes. J. Biol. Chem. 273:17787-17792.
11. DeGracia, D. J., R. Kumar, C. R. Owen, G. S. Krause, and B. C. White. 2002. Molecular pathways of protein synthesis inhibition during brain reperfusion: implications for neuronal survival or death. J. Cereb. Blood Flow Metab. 22:127-141.
12. Douglas, R. M., T. Xu, and G. G. Haddad. 2001. Cell cycle progression and cell division are sensitive to hypoxia in Drosophila melanogaster embryos. Am. J. Physiol. Regul. Integr. Comp. Physiol. 280:R1555-R1563.
13. Feldser, D., F. Agani, N. V. Iyer, B. Pak, G. Ferreira, and G. L. Semenza. 1999. Reciprocal positive regulation of hypoxia-inducible factor 1α and insulin-like growth factor 2. Cancer Res. 59:3915-3918.
14. Firth, J. D., B. L. Ebert, C. W. Pugh, and P. J. Ratcliffe. 1994. Oxygen-regulated control elements in the phosphoglycerate kinase 1 and lactate dehydrogenase A genes: similarities with the erythropoietin 3′ enhancer. Proc. Natl. Acad. Sci. USA 91:6496-6500.
15. Galban, S., J. Fan, J. L. Martindale, C. Cheadle, B. Hoffman, M. P. Woods, G. Temeles, J. Brieger, J. Decker, and M. Gorospe. 2003. von Hippel-Lindau protein-mediated repression of tumor necrosis factor alpha translation revealed through use of cDNA arrays. Mol. Cell. Biol. 23:2316-2328.
16. Graeber, T. G., O. C. Jacks, T. Housman, D. E. Koch, C. J. Lowe, and A. J Giaccia. 1996. Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours. Nature 379:88-91.
17. Harding, H. P., M. Calfon, F. Urano, I. Novoa, and D. Ron. 2002. Transcriptional and translational control in the mammalian unfolded protein response. Annu. Rev. Cell Dev. Biol. 18:575-599.
18. Harding, H. P., I. Novoa, Y. Zhang, H. Zeng, R. Wek, M. Schapira, and D. Ron. 2000. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell 6:1099-1108.
19. Harding, H. P., Y. Zhang, and D. Ron. 1999. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397:271-274.
20. Hartmann, A., M. Kunz, S. Kostlin, R. Gillitzer, A. Toksoy, E. B. Brocker, and C. E. Klein. 1999. Hypoxia-induced up-regulation of angiogenin in human malignant melanoma. Cancer Res. 59:1578-1583.
21. Hinnebusch, A. G. 1997. Translational regulation of yeast GCN4: a window on factors that control initiator-tRNA binding to the ribosome. J. Biol. Chem. 272:21661-21664.
22. 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.
23. Holcik, M., C. Lefebvre, C. Yeh, T. Chow, and R. G. Korneluk. 1999. A new internal-ribosome-entry-site motif potentiates XIAP-mediated cytoprotection. Nat. Cell Biol. 1:190-192.
24. Iyer, N. V., L. E. Kotch, F. Agani, S. W. Leung, E. Laughner, R. H. Wenger, M. Gassmann, J. D. Gearhart, A. M. Lawler, A. Y. Yu, and G. L. Semenza. 1998. Cellular and developmental control of 02 homeostasis by hypoxia-inducible factor 1α. Genes Dev. 12:149-162.
25. Jang, S. K., H. G. Krausslich, M. J. Nicklin, G. M. Duke, A. C. Palmenberg, and E. Wimmer. 1988. A segment of the 5′ nontranslated region of encephatomyocarditis virus RNA directs internal entry of ribosomes during in vitro translation. J. Virol. 62:2636-2643.
26. Johannes, G., M. S. Carter, M. B. Eisen, P. O. Brown, and P. Sarnow. 1999. Identification of eukaryotic mRNAs that are translated at reduced cap binding complex eIF4F concentrations using a cDNA microarray. Proc. Natl. Acad. Sci. USA 96:13118-13123.
27. Koong, A. C., N. C. Denko, K. M. Hudson, C. Schindler, L. Swiersz, C. Koch, S. Evans, H. Ibrahim, Q. T. Le, D. J. Terris, and A. J. Giaccia. 2000. Candidate genes for the hypoxic tumor phenotype. Cancer Res. 60:883-887.
28. Koumenis, C., N. C. Denko, 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.
29. Kozak, M. 1999. Initiation of translation in prokaryotes and eukaryotes. Gene 234:187-208.
30. Kraggerud, S. M., J. A. Sandvik, and E. O. Pettersen. 1995. Regulation of protein synthesis in human cells exposed to extreme hypoxia. Anticancer Res. 15:683-686.
31. Lang, W. H., and R. H. Reeder. 1993. The REB1 site is an essential component of a terminator for RNA polymerase I in Saccharomyces cerevisiae. Mol. Cell. Biol. 13:649-658.
32. Lassot, I., E. Segeral, C. Berlioz-Torrent, H. Durand, L. Groussin, T. Hai, R. Benarous, and F. Margottin-Goguet. 2001. ATF4 degradation relies on a phosphorylation-dependent interaction with the SCF(βTrCP) ubiquitin ligase. Mol. Cell. Biol. 21:2192-2202.
33. 2 levels. Arch. Biochem. Biophys. 304:322-331.
34. Liebermann, D. A., and B. Hoffman. 2002. Myeloid differentiation (MyD)/ growth arrest DNA damage (GADD) genes in tumor suppression, immunity and inflammation. Leukemia 16:527-541.
35. Ma, Y., and L. M. Hendershot. 2003. Delineation of a negative feedback regulatory loop that controls protein translation during endoplasmic reticulum stress. J. Biol. Chem. 278:34864-34873.
36. Macejak, D. G., and P. Sarnow. 1991. Internal initiation of translation mediated by the 5′ leader of a cellular mRNA. Nature 353:90-94.
37. Maxwell, P. H., C. W. Pugh, and P. J. Ratcliffe. 2001. Activation of the HIF pathway in cancer. Curr. Opin. Genet. Dev. 11:293-299.
38. Mikulits, W., B. Pradet-Balade, B. Habermann, H. Beug, J. A. Garcia-Sanz, and E. W. Mullner. 2000. Isolation of translationally controlled mRNAs by differential screening. FASEB J. 14:1641-1652.
39. Nielsen, F. C., L. Ostergaard, J. Nielsen, and J. Christiansen. 1995. Growth-dependent translation of IGF-II mRNA by a rapamycin-sensitive pathway. Nature 377:358-362.
40. Novoa, I., H. Zeng, H. P. Harding, and D. Ron. 2001. Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2α. J. Cell Biol. 153:1011-1022.
41. Novoa, I., Y. Zhang, H. Zeng, R. Jungreis, H. P. Harding, and D. Ron. 2003. Stress-induced gene expression requires programmed recovery from translational repression. EMBO J. 22:1180-1187.
42. O'Rourke, J. F., C. W. Pugh, S. M. Bartlett, and P. J. Ratcliffe. 1996. Identification of hypoxically inducible mRNAs in HeLa cells using differential-display PCR: role of hypoxia-inducible factor-1. Eur. J. Biochem. 241: 403-410.
43. Pettersen, E. O., N. O. Juul, and O. W. Ronning. 1986. Regulation of protein metabolism of human cells during and after acute hypoxia. Cancer Res. 46:4346-4351.
44. Prostko, C. R., M. A. Brostrom, E. M. Malara, and C. O. Brostrom. 1992. Phosphorylation of eukaryotic initiation factor (eIF) 2α and inhibition of eIF-2B in GH3 pituitary cells by perturbants of early protein processing that induce GRP78. J. Biol. Chem. 267:16751-16754.
45. Pyronnet, S., L. Pradayrol, and N. Sonenberg. 2000. A cell cycle-dependent internal ribosome entry site. Mol. Cell 5:607-616.
46. 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.
47. Richter, J. D. 1993. Translational control in development: a perspective. Dev. Genet. 14:407-411.
48. Rosenwald, I. B., N. A. Setkov, V. N. Kazakov, J. J. Chen, A. G. Ryazanov, I. M. London, and O. I. Epifanova. 1995. Transient inhibition of protein synthesis induces expression of proto-oncogenes and stimulates resting cells to enter the cell cycle. Cell Prolif. 28:631-644.
49. Ruzinova, M. B., R. A. Schoer, W. Gerald, J. E. Egan, P. P. Pandolfi, S. Rafii, K. Manova, V. Mittal, and R. Benezra. 2003. Effect of angiogenesis inhibition by Id loss and the contribution of bone-marrow-derived endothelial cells in spontaneous murine tumors. Cancer Cell 4:277-289.
50. Ryan, H. E., J. Lo, and R. S. Johnson. 1998. HIF-1 alpha is required for solid tumor formation and embryonic vascularization. EMBO J. 17:3005-3015.
51. Sella, O., G. Gerlitz, S. Y. Le, and O. Elroy-Stein. 1999. Differentiation-induced internal translation of c-sis mRNA: analysis of the cis elements and their differentiation-linked binding to the hnRNP C protein. Mol. Cell. Biol. 19:5429-5440.
52. Semenza, G. L. 2000. HIF-1 and human disease: one highly involved factor. Genes Dev. 14:1983-1991.
53. 2 homeostasis. Curr. Opin. Genet. Dev. 8:588-594.
54. Semenza, G. L., P. H. Roth, H. M. Fang, and G. L. Wang. 1994. Transcriptional regulation of genes encoding glycolytic enzymes by hypoxia-inducible factor 1. J. Biol. Chem. 269:23757-23763.
55. Sheets, M. D., C. A. Fox, T. Hunt, G. Vande Woude, and M. Wickens. 1994. The 3′-untranslated regions of c-mos and cyclin mRNAs stimulate translation by regulating cytoplasmic polyadenylation. Genes Dev. 8:926-938.
56. Sivitz, W. I., D. D. Lund, B. Yorek, M. Grover-McKay, and P. G. Schmid. 1992. Pretranslational regulation of two cardiac glucose transporters in rats exposed to hypobaric hypoxia. Am. J. Physiol. 263:E562-E569.
57. Srivastava, S. P., K. U. Kumar, and R. J. Kaufman. 1998. Phosphorylation of eukaryotic translation initiation factor 2 mediates apoptosis in response to activation of the double-stranded RNA-dependent protein kinase. J. Biol. Chem. 273:2416-2423.
58. 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.
59. Stoneley, M., S. A. Chappell, C. L. Jopling, M. Dickens, M. MacFarlane, and A. E. Willis. 2000. c-Myc protein synthesis is initiated from the internal ribosome entry segment during apoptosis. Mol. Cell. Biol. 20:1162-1169.
60. Takahashi, Y., S. Takahashi, Y. Shiga, T. Yoshimi, and T. Miura. 2000. Hypoxic induction of prolyl 4-hydroxylase alpha (I) in cultured cells. J. Biol. Chem. 275:14139-14146.
61. Wood, S. M., M. S. Wiesener, K. M. Yeates, N. Okada, C. W. Pugh, P. H. Maxwell, and P. J. Ratclitfe. 1998. Selection and analysis of a mutant cell line defective in the hypoxia-inducible factor-1α-subunit (HIF-1α): characterization of HIF-1α-dependent and -independent hypoxia-inducible gene expression. J. Biol. Chem. 273:8360-8368.
62. Wouters, B. G., M. Koritzinsky, R. K. Chiu, J. Theys, J. Buijsen, and P. Lambin. 2003. Modulation of cell death in the tumor microenvironment. Semin. Radial. Oncol. 13:31-41.
63. a. 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.
64. Wykoff, C. C., N. J. Beasley, P. H. Watson, K. J. Turner, J. Pastorek, A. Sibtain, G. D. Wilson, H. Turley, K. L. Talks, P. H. Maxwell, C. W. Pugh, P. J. Ratcliffe, and A. L. Harris. 2000. Hypoxia-inducible expression of tumor-associated carbonic anhydrases. Cancer Res. 60:7075-7083.