Gene expression during acute and prolonged hypoxia is regulated by distinct mechanisms of translational control

EMBO Journal

Volumn 25, Issue 5, 2006, Pages 1114-1125

  Koritzinsky, Marianne ^a   Magagnin, Michaël G ^a   Van Den Beucken, Twan ^a   Seigneuric, Renaud ^a   Savelkouls, Kim ^a   Dostie, Josée ^b   Pyronnet, Stéphane ^b   Kaufman, Randal J ^c   Weppler, Sherry A ^a   Voncken, Jan Willem ^a   Lambin, Philippe ^a   Koumenis, Constantinos ^d   Sonenberg, Nahum ^b   Wouters, Bradly G ^a,e  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^d WAKE FOREST SCHOOL OF MEDICINE   (United States)

^e MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

eIF2 ; eIF4F; Hypoxia; mRNA translation

Indexed keywords

CARRIER PROTEIN; INITIATION FACTOR 2ALPHA; INITIATION FACTOR 4E BINDING PROTEIN 1; INITIATION FACTOR 4E T; INITIATION FACTOR 4F; MESSENGER RNA; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DEPHOSPHORYLATION; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; HYPOXIA; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA TRANSLATION; TRANSLATION INITIATION; TRANSLATION REGULATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADENOCARCINOMA; ANIMALS; ANOXIA; CARRIER PROTEINS; ENDOPLASMIC RETICULUM; EUKARYOTIC INITIATION FACTOR-2; EUKARYOTIC INITIATION FACTOR-4E; EUKARYOTIC INITIATION FACTOR-4F; FIBROBLASTS; GENE EXPRESSION REGULATION; HELA CELLS; HUMANS; LUNG NEOPLASMS; MICE; MICE, KNOCKOUT; NUCLEOCYTOPLASMIC TRANSPORT PROTEINS; PHOSPHOPROTEINS; PHOSPHORYLATION; POLYRIBOSOMES; PROTEIN BIOSYNTHESIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA; TRANSFECTION;

EID: 33644852277     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600998     Document Type: Article

References (51)

1. Andrei MA, Ingelfinger D, Heintzmann R, Achsel T, Rivera-Pomar R, Luhrmann R (2005) A role for eIF4E and eIF4E-transporter in targeting mRNPs to mammalian processing bodies. RNA 11: 717-727
2. Arsham AM, Howell JJ, Simon MC (2003) A novel hypoxia-inducible factor-independent hypoxic response regulating mammalian target of rapamycin and its targets. J Biol Chem 278: 29655-29660
3. Bennewith KL, Durand RE (2004) Quantifying transient hypoxia in human tumor xenografts by flow cytometry. Cancer Res 64: 6183-6189
4. Bi M, Naczki C, Koritzinsky M, Fels D, Blais J, Hu N, Harding H, Novoa I, Varia M, Raleigh J, Scheuner D, Kaufman RJ, Bell J, Ron D, Wouters BG, Koumenis C (2005) ER stress-regulated translation increases tolerance to extreme hypoxia and promotes tumor growth. EMBO J 24: 3470-3481
5. Blais JD, Filipenko V, Bi M, Harding HP, Ron D, Koumenis C, Wouters BG, Bell JC (2004) Activating transcription factor 4 is translationally regulated by hypoxic stress. Mol Cell Biol 24: 7469-7482
6. Brugarolas J, Lei K, Hurley RL, Manning BD, Reiling JH, Hafen E, Witters LA, Ellisen LW, Kaelin Jr WG (2004) Regulation of mTOR function in response to hypoxia by REDD1 and the TSC1/TSC2 tumor suppressor complex. Genes Dev 18: 2893-2904
7. Cardenas-Navia LI, Yu D, Braun RD, Brizel DM, Secomb TW, Dewhirst MW (2004) Tumor-dependent kinetics of partial pressure of oxygen fluctuations during air and oxygen breathing. Cancer Res 64: 6010-6017
8. Carter MS, Kuhn KM, Sarnow P (2000) Cellular internal ribosome entry site elements and the use of cDNA microarrays in their investigation. In Translational Control of Gene Expression, Sonenberg N, Hershey JW, Mathews MB (eds) pp 615-636. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press
9. DeGracia DJ, Kumar R, Owen CR, Krause GS, White BC (2002) Molecular pathways of protein synthesis inhibition during brain reperfusion: implications for neuronal survival or death. J Cereb Blood Flow Metab 22: 127-141
10. Dostie J, Ferraiuolo M, Pause A, Adam SA, Sonenberg N (2000) A novel shuttling protein, 4E-T, mediates the nuclear import of the mRNA 5′ cap-binding protein, eIF4E. EMBO J 19: 3142-3156
11. Erler JT, Cawthorne CJ, Williams KJ, Koritzinsky M, Wouters BG, Wilson C, Miller C, Demonacos C, Stratford IJ, Dive C (2004) Hypoxia-mediated down-regulation of Bid and Bax in tumors occurs via hypoxia-inducible factor 1-dependent and -independent mechanisms and contributes to drug resistance. Mol Cell Biol 24: 2875-2889
12. Fawcett TW, Martindale JL, Guyton KZ, Hai T, Holbrook NJ (1999) Complexes containing activating transcription factor (ATF)/cAMP-responsive-element- binding protein (CREB) interact with the CCAAT/enhancer-binding protein (C/EBP)-ATF composite site to regulate Gadd153 expression during the stress response. Biochem J 339 (Part 1): 135-141
13. Ferraiuolo MA, Basak S, Dostie J, Murray EL, Schoenberg DR, 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
14. Gebauer F, Hentze MW (2004) Molecular mechanisms of translational control. Nat Rev Mol Cell Biol 5: 827-835
15. Graeber TG, Osmanian C, Jacks T, Housman DE, Koch CJ, Lowe SW, Giaccia AJ (1996) Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours. Nature 379: 88-91
16. Harding HP, Novoa I, Zhang Y, Zeng H, Wek R, Schapira M, Ron D (2000) Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell 6: 1099-1108
17. Harding HP, Zhang Y, Zeng H, Novoa I, Lu PD, Calfon M, Sadri N, Yun C, Popko B, Paules R, Stojdl DF, Bell JC, Hettmann T, Leiden JM, Ron D (2003) An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol Cell 11: 619-633
18. Harris AL (2002) Hypoxia - a key regulatory factor in tumour growth. Nat Rev Cancer 2: 38-47
19. Hay N, Sonenberg N (2004) Upstream and downstream of mTOR. Genes Dev 18: 1926-1945
20. Holcik M, Sonenberg N (2005) Translational control in stress and apoptosis. Nat Rev Mol Cell Biol 6: 318-327
21. Holland EC, Sonenberg N, Pandolfi PP, Thomas G (2004) Signaling control of mRNA translation in cancer pathogenesis. Oncogene 23: 3138-3144
22. 2-regulated prolyl hydroxylation. Science 292: 468-472
23. Johannes G, Carter MS, Eisen MB, Brown PO, Sarnow P (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
24. Kimball SR, Jefferson LS (2000) Regulation of translation initiation in mammalian cells by amino acids. In Translational Control of Gene Expression, Sonenberg N, Hershey JW, Mathews MB (eds) pp 561-579. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press
25. Koritzinsky M, Seigneuric R, Magagnin MG, Beucken T, Lambin P, Wouters BG (2005) The hypoxic proteome is influenced by gene-specific changes in mRNA translation. Radiother Oncol 76: 177-186
26. Koumenis C, Naczki C, Koritzinsky M, Rastani S, Diehl A, Sonenberg N, Koromilas A, Wouters BG (2002) Regulation of protein synthesis by hypoxia via activation of the endoplasmic reticulum kinase PERK and phosphorylation of the translation initiation factor eIF2alpha. Mol Cell Biol 22: 7405-7416
27. Lang KJ, Kappel A, Goodall GJ (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
28. Lawson TG, Cladaras MH, Ray BK, Lee KA, Abramson RD, Merrick WC, Thach RE (1988) Discriminatory interaction of purified eukaryotic initiation factors 4F plus 4A with the 5′ ends of reovirus messenger RNAs. J Biol Chem 263: 7266-7276
29. Leek RD, Stratford I, Harris AL (2005) The role of hypoxia-inducible factor-1 in three-dimensional tumor growth, apoptosis, and regulation by the insulin-signaling pathway. Cancer Res 65: 4147-4152
30. 2 levels. Arch Biochem Biophys 304: 322-331
31. Lejbkowicz F, Goyer C, Darveau A, Neron S, Lemieux R, Sonenberg N (1992) A fraction of the mRNA 5′ cap-binding protein, eukaryotic initiation factor 4E, localizes to the nucleus. Proc Natl Acad Sci USA 89: 9612-9616
32. Lu PD, Harding HP, Ron D (2004) Translation reinitiation at alternative open reading frames regulates gene expression in an integrated stress response. J Cell Biol 167: 27-33
33. Marciniak SJ, Yun CY, Oyadomari S, Novoa I, Zhang Y, Jungreis R, Nagata K, Harding HP, Ron D (2004) CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes Dev 18: 3066-3077
34. Martin de la Vega C, Burda J, Nemethova M, Quevedo C, Alcazar A, Martin ME, Danielisova V, Fando JL, Salinas M (2001) Possible mechanisms involved in the down-regulation of translation during transient global ischaemia in the rat brain. Biochem J 357: 819-826
35. Martin ME, Munoz FM, Salinas M, Fando JL (2000) Ischaemia induces changes in the association of the binding protein 4E-BP1 and eukaryotic initiation factor (eIF) 4G to eIF4E in differentiated PC12 cells. Biochem J 351 (Part 2): 327-334
36. Meyuhas O, Hornstein E (2000) Translational control of TOP mRNAs. In Translational Control of Gene Expression, Sonenberg N, Hershey JW, Mathews MB (eds) pp 671-694. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press
37. Neumar RW, DeGracia DJ, Konkoly LL, Khoury JI, White BC, Krause GS (1998) Calpain mediates eukaryotic initiation factor 4G degradation during global brain ischemia. J Cereb Blood Flow Metab 18: 876-881
38. Novoa I, Zeng H, Harding HP, Ron D (2001) Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2alpha. J Cell Biol 153: 1011-1022
39. Novoa I, Zhang Y, Zeng H, Jungreis R, Harding HP, Ron D (2003) Stress-induced gene expression requires programmed recovery from translational repression. EMBO J 22: 1180-1187
40. Pause A, Belsham GJ, Gingras AC, Douze O, Lin TA, Lawrence Jr JC, Sonenberg N (1994) Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5′-cap function. Nature 371: 762-767
41. Robertson N, Potter C, Harris AL (2004) Role of carbonic anhydrase IX in human tumor cell growth, survival, and invasion. Cancer Res 64: 6160-6165
42. Romero-Ramirez L, Cao H, Nelson D, Hammond E, Lee AH, Yoshida H, Mori K, Glimcher LH, Denko NC, Giaccia AJ, Le QT, Koong AC (2004) XBP1 is essential for survival under hypoxic conditions and is required for tumor growth. Cancer Res 64: 5943-5947
43. Ryan HE, Lo J, Johnson RS (1998) HIF-1 alpha is required for solid tumor formation and embryonic vascularization. EMBO J 17: 3005-3015
44. Scheuner D, Song B, McEwen E, Liu C, Laybutt R, Gillespie P, Saunders T, Bonner-Weir S, Kaufman RJ (2001) Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol Cell 7: 1165-1176
45. Schroder M, Kaufman RJ (2005) The mammalian unfolded protein response. Annu Rev Biochem 74: 739-789
46. Semenza GL (2003) Targeting HIF-1 for cancer therapy. Nat Rev Cancer 3: 721-732
47. Stein I, Itin A, Einat P, Skaliter R, Grossman Z, Keshet E (1998) Translation of vascular endothelial growth factor mRNA by internal ribosome entry: implications for translation under hypoxia. Mol Cell Biol 18: 3112-3119
48. Tang N, Wang L, Esko J, Giordano FJ, Huang Y, Gerber HP, Ferrara N, Johnson RS (2004) Loss of HIF-1alpha in endothelial cells disrupts a hypoxia-driven VEGF autocrine loop necessary for tumorigenesis. Cancer Cell 6: 485-495
49. Tinton SA, Buc-Calderon PM (1999) Hypoxia increases the association of 4E-binding protein 1 with the initiation factor 4E in isolated rat hepatocytes. FEBS Lett 446: 55-59
50. Wouters BG, van den Beucken T, Magagnin MG, Koritzinsky M, Fels D, Koumenis C (2005) Control of the hypoxic response through regulation of mRNA translation. Semin Cell Dev Biol 16: 487-501
51. Wouters BG, Weppler SA, Koritzinsky M, Landuyt W, Nuyts S, Theys J, Chiu RK, Lambin P (2002) Hypoxia as a target for combined modality treatments. Eur J Cancer 38: 240-257