Stress-induced gene expression requires programmed recovery from translational repression

EMBO Journal

Volumn 22, Issue 5, 2003, Pages 1180-1187

  Novoa, Isabel ^a   Zhang, Yuhong ^a   Zeng, Huiqing ^a   Jungreis, Rivka ^a   Harding, Heather P ^a   Ron, David ^a  

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

Author keywords

Protein phosphatases; Protein synthesis; Secretion; Signal transduction

Indexed keywords

PROTEIN; PROTEIN GADD34; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; CELL MUTANT; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENE INDUCTION; GENE REPRESSION; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; STRESS;

3T3 CELLS; ACTIVATING TRANSCRIPTION FACTOR 4; ANIMALS; ANTIGENS, DIFFERENTIATION; ARSENITES; CELL CYCLE PROTEINS; EIF-2 KINASE; ENDOPLASMIC RETICULUM; ENZYME INHIBITORS; EUKARYOTIC INITIATION FACTOR-2; FIBROBLASTS; GENE EXPRESSION REGULATION; GENE TARGETING; MICE; MUTATION; OXIDATIVE STRESS; PHOSPHORYLATION; PROTEIN BIOSYNTHESIS; PROTEINS; THAPSIGARGIN; TRANSCRIPTION FACTORS; TUNICAMYCIN;

EID: 0037416211     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg112     Document Type: Article

References (37)

1. Brostrom, C.O. and Brostrom, M.A. (1998) Regulation of translational initiation during cellular responses to stress. Prog. Nucleic Acid Res. Mol. Biol., 58, 79-125.
2. Brostrom, M.A., Lin, X.J., Cade, C., Gmitter, D. and Brostrom, C.O. (1989) Loss of a calcium requirement for protein synthesis in pituitary cells following thermal or chemical stress. J. Biol. Chem., 264, 1638-1643.
3. Calfon, M., Zeng, H., Urano, F., Till, J.H., Hubbard, S.R., Harding, H.P., Clark, S.G. and Ron, D. (2002) IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature, 415, 92-96.
4. Connor, J.H., Weiser, D.C., Li, S., Hallenbeck, J.M. and Shenolikar, S. (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.
5. DeGracia, D.J., Kumar, R., Owen, C.R., Krause, G.S. and White, B.C. (2002) Molecular pathways of protein synthesis inhibition during brain reperfusion: implications for neuronal survival or death. J. Cereb. Blood Flow Metab., 22, 127-141.
6. Dever, T.E., Chen, J.J., Barber, G.N., Cigan, A.M., Feng, L., Donahue, T.F., London, I.M., Katze, M.G. and Hinnebusch, A.G. (1993) Mammalian eukaryotic initiation factor 2 α kinases functionally substitute for GCN2 protein kinase in the GCN4 translational control mechanism of yeast. Proc. Natl Acad. Sci. USA, 90, 4616-4620.
7. Doutheil, J., Gissel, C., Oschlies, U., Hossmann, K.A. and Paschen, W. (1997) Relation of neuronal endoplasmic reticulum calcium homeostasis to ribosomal aggregation and protein synthesis: implications for stress-induced suppression of protein synthesis. Brain Res., 775, 43-51.
8. Frerichs, K.U., Smith, C.B., Brenner, M., DeGracia, D.J., Krause, G.S., Marrone, L., Dever, T.E. and Hallenbeck, J.M. (1998) Suppression of protein synthesis in brain during hibernation involves inhibition of protein initiation and elongation. Proc. Natl Acad. Sci. USA, 95, 14511-14516.
9. Han, A.P. et al. (2001) Heme-regulated eIF2α kinase (HRI) is required for translational regulation and survival of erythroid precursors in iron deficiency. EMBO J., 20, 6909-6918.
10. Harding, H., Zhang, Y. and Ron, D. (1999) Translation and protein folding are coupled by an endoplasmic reticulum resident kinase. Nature, 397, 271-274.
11. Harding, H., Novoa, I., Zhang, Y., Zeng, H., Wek, R.C., Schapira, M. and Ron, D. (2000a) Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell, 6, 1099-1108.
12. Harding, H., Zhang, Y., Bertolotti, A., Zeng, H. and Ron, D. (2000b) Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol. Cell., 5, 897-904.
13. Harding, H., Zeng, H., Zhang, Y., Jungreis, R., Chung, P., Plesken, H., Sabatini, D. and Ron, D. (2001a) Diabetes mellitus and excocrine pancreatic dysfunction in Perk-/- mice reveals a role for translational control in survival of secretory cells. Mol. Cell., 7, 1153-1163.
14. Harding, H.P., Novoa, I., Bertolotfi, A., Zeng, H., Zhang, A., Urano, F., Jousse, C. and Ron, D. (2001b) Translational regulation in the cellular response to biosynthetic load on the endoplasmic reticulum. Cold Spring Harb. Symp. Quant. Biol., 66, 499-508.
15. He, B., Chou, J., Liebermann, D.A., Hoffman, B. and Roizman, B. (1996) The carboxyl terminus of the murine MyD116 gene substitutes for the corresponding domain of the γ(1)34.5 gene of herpes simplex virus to preclude the premature shutoff of total protein synthesis in infected human cells. J. Virol., 70, 84-90.
16. Hinnebusch, A. (1996) Translational control of GCN4: gene-specific regulation by phosphorylation of eIF2. In Hershey, J., Mathews, M. and Sonenberg,N. (eds), Translational Control. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 199-244.
17. Hinnebusch, A.G. (2000) Mechanism and regulation of initiator methionyl-tRNA binding to ribosomes. In Sonenberg, N., Hershey, J.W.B. and Mathews, M.B. (eds), Translational control of gene expression. CSHL Press, Cold Spring Harbor, NY, pp. 185-243.
18. Kaufman, R.J. (1999) Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev., 13, 1211-1233.
19. Kumar, R. et al. (2001) Brain ischemia and reperfusion activates the eukaryotic initiation factor 2α kinase, PERK. J. Neurochem., 77, 1418-1421.
20. Levinson, W., Oppermann, H. and Jackson, J. (1980) Transition series metals and sulfhydryl reagents induce the synthesis of four proteins in eukaryotic cells. Biochim. Biophys. Acta, 606, 170-180.
21. Macejak, D.G. and Sarnow, P. (1990) Translational regulation of the immunoglobulin heavy-chain binding protein mRNA. Enzymes, 44, 310-319.
22. McCullough, K.D., Martindale, J.L., Klotz, L.O., Aw, T.Y. and Holbrook, N.J. (2001) Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol. Cell. Biol., 21, 1249-1259.
23. Mori, K. (2000) Tripartite management of unfolded proteins in the endoplasmic reticulum. Cell, 101, 451-454.
24. Morimoto, R.I. (1998) Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev., 12, 3788-3796.
25. Novoa, I., Zeng, H., Harding, H. and Ron, D. (2001) Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2α. J. Cell Biol., 153, 1011-1022.
26. Oyadomari, S., Takeda, K., Takiguchi, M., Gotoh, T., Matsumoto, M., Wada, I., Akira, S., Araki, E. and Mori, M. (2001) Nitric oxide-induced apoptosis in pancreatic β-cells is mediated by the endoplasmic reticulum stress pathway. Proc. Natl Acad. Sci. USA, 98, 10845-10850.
27. Patil, C. and Walter, P. (2001) Intracellular signaling from the endoplasmic reticulum to the nucleus: the unfolded protein response in yeast and mammals. Curr. Opin. Cell Biol., 13, 349-355.
28. Prostko, C.R., Brostrom, M.A. and Brostrom, C.O. (1993) Reversible phosphorylation of eukaryotic initiation factor 2 α in response to endoplasmic reticular signaling. Mol. Cell Biochem., 127, 255-265.
29. Roizman, B. (1999) HSV gene functions: what have we learned that could be generally applicable to its near and distant cousins? Acta Virol., 43, 75-80.
30. Ron, D. and Habener, J.F. (1992) CHOP, a novel developmentally regulated nuclear protein that dimerizes with transcription factors C/EBP and LAP and functions as a dominant negative inhibitor of gene transcription. Genes Dev., 6, 439-453.
31. Scheuner, D., Song, B., McEwen, E., Gillespie, P., Saunders, T., BonnerWeir, S. and Kaufman, R.J. (2001) Translational control is required for the unfolded protein response and in-vivo glucose homeostasis. Mol. Cell, 7, 1165-1176.
32. Scorsone, K.A., Panniers, R., Rowlands, A.G. and Henshaw, E.C. (1987) Phosphorylation of eukaryotic initiation factor 2 during physiological stresses which affect protein synthesis. J. Biol. Chem., 262, 14538-14543.
33. Sok, J., Calfon, M., Lu, J., Lichtlen, P., Clark, S. and Ron, D. (2001) Arsenite-inducible RNA-associated protein (AIRAP) protects cells from arsenite toxicity. Cell Stress Chaperones, 6, 6-15.
34. Vallejo, M., Ron, D., Miller, C.P. and Habener, J.F. (1993) C/ATF, a member of the activating transcription factor family of DNA-binding proteins, dimerizes with CAAT/enhancer-binding proteins and directs their binding to cAMP response elements. Proc. Natl Acad. Sci. USA, 90, 4679-4683.
35. Wang, X.-Z. et al. (1996) Signals from the stressed endoplasmic reticulum induce C/EBP homologous protein (CHOP/GADD153). Mol. Cell. Biol., 16, 4273-4280.
36. Yoshida, H., Matsui, T., Yamamoto, A., Okada, T. and Mori, K. (2001) XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell, 107, 881-891.
37. Zinszner, H., Kuroda, M., Wang, X., Batchvarova, N., Lightfoot, R.T., Remotti, H., Stevens, J.L. and Ron, D. (1998) CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev., 12, 982-995.