Activating Transcription Factor 3 Is Integral to the Eukaryotic Initiation Factor 2 Kinase Stress Response

Molecular and Cellular Biology

Volumn 24, Issue 3, 2004, Pages 1365-1377

  Jiang, Hao Yuan ^a   Wek, Sheree A ^a   McGrath, Barbara C ^b   Lu, Dan ^c   Hai, Tsonwin ^c   Harding, Heather P ^d   Wang, Xiaozhong ^d   Ron, David ^d   Cavener, Douglas R ^b   Wek, Ronald C ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c OHIO STATE UNIVERSITY   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; ACTIVATING TRANSCRIPTION FACTOR 4; AMINO ACID; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; INITIATION FACTOR 2; LEUCINE ZIPPER PROTEIN; PANCREATIC ENDOPLASMIC RETICULUM KINASE; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN GADD34; PROTEIN KINASE; PROTEIN KINASE R; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; EMBRYO; ENDOPLASMIC RETICULUM; FEEDBACK SYSTEM; FIBROBLAST; GENE EXPRESSION; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; STRESS; TRANSCRIPTION REGULATION;

ACTIVATING TRANSCRIPTION FACTOR 3; ACTIVATING TRANSCRIPTION FACTOR 4; ANIMALS; CCAAT-ENHANCER-BINDING PROTEINS; EIF-2 KINASE; EUKARYOTIC INITIATION FACTOR-2; MICE; PHOSPHORYLATION; PHOSPHOTRANSFERASES; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; RNA, MESSENGER; TRANSCRIPTION FACTOR CHOP; TRANSCRIPTION FACTORS;

ANIMALIA; EUKARYOTA; STAPHYLOCOCCUS PHAGE 3A;

EID: 1642458354     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.3.1365-1377.2004     Document Type: Article

References (78)

1. Abastado, J. P., P. F. Miller, B. M. Jackson, and A. G. Hinnebusch. 1991. Suppression of ribosomal reinitiation at upstream open reading frames in amino acid-starved cells forms the basis of GCN4 translational control. Mol. Cell. Biol. 11:486-496.
2. Allen-Jennings, A. E., M. G. Hartman, G. J. Kociba, and T. Hai. 2001. The roles of ATF3 in glucose homeostasis. A transgenic mouse model with liver dysfunction and defects in endocrine pancreas. J. Biol. Chem. 276:29507-29514.
3. Allen-Jennings, A. E., M. G. Hartman, G. J. Kociba, and T. Hai. 2002. The roles of ATF3 in liver dysfunction and the regulation of phosphoenolpyruvate carboxykinase gene expression. J. Biol. Chem. 277:20020-20025.
4. Baltzis, D., L. Suiyang, and A. E. Koromilas. 2002. Functional characterization of pkr gene products expressed in cells from mice with a targeted deletion of the N-terminus or C-terminus of PKR. J. Biol. Chem. 277:38364-38372.
5. Bertolotti, A., Y. Zhang, L. Hendershot, H. Harding, and D. Ron. 2000. Dynamic interaction of BiP and the ER stress transducers in the unfolded protein response. Nat. Cell Biol. 6:326-332.
6. Brewer, J. W., and J. A. Diehl. 2000. PERK mediates cell-cycle exit during the mammalian unfolded protein response. Proc. Natl. Acad. Sci. USA 97:12625-12630.
7. Bruhat, A., J. Averous, V. Carraro, C. Zhong, A. M. Reimold, M. S. Kilberg, and P. Fafournoux. 2002. Differences in the molecular mechanisms involved in the transcriptional activation of CHOP and asparagine synthetase in response to amino acid deprivation or activation of the unfolded protein response. J. Biol. Chem. 277:48107-48114.
8. Bruhat, A., C. Jousse, V. Carraro, A. M. Reimold, M. Ferrara, and P. Fafournoux. 2000. Amino acids control mammalian gene transcription: activating transcription factor 2 is essential for the amino acid responsiveness of the CHOP promoter. Mol. Cell. Biol. 20:7192-7204.
9. 2-terminal kinase and promoter response element. Blood 96:2140-2148.
10. Calfon, M., H. Zeng, F. Urano, J. H. Till, S. R. Hubbard, H. P. Harding, S. G. Clark, and D. Ron. 2002. IREI couples endoplasmic reticulum load to secretory capacity by processing of XBP-1 mRNA. Nature 415:92-96.
11. Calkhoven, F. C., C. Muller, and A. Leutz. 2000. Translational control of C/EBPα and C/EBPβ isoform expression. Genes Dev. 14:1920-1932.
12. Castelnau, P., M. Le Merrer, C. Diatlof-Zito, E. Marquis, M. J. Tete, and J. J. Robert. 2000. Wolcott-Rallison syndrome: a case with endocrine and exocrine pancreatic deficiency and pancreatic hypotrophy. Eur. J. Pediatr. 159:631-633.
13. Chen, B. P., C. D. Wolfgang, and T. Hai. 1996. Analysis of ATF3, a transcription factor induced by physiological stresses and modulated by gadd 153/Chop10. Mol. Cell. Biol. 16:1157-1168.
14. Chen, J.-J. 2000. Heme-regulated eIF2α kinase. p. 529-546. In N. Sonenberg, J W. B. Hershey, and M. Mathews (ed.), Translational control of gene expression. Cold Spring Harbor Laboratory Press, Plainview, N.Y.
15. Clemens, M. J. 1996. Protein kinases that phosphorylate eIF2 and eIF2B, and their role in eukaryotic cell translational control, p. 139-172. In J. W. B. Hershey, M. B. Mathews, and N. Soncnberg (ed.), Translational control. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
16. 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.
17. Delepine, M., M. Nicolino, T. Barrett, M. Golamaully, G. M. Lathrop, and C. Julier. 2000. EIF2AK3, encoding translation initiation factor 2-α kinase 3, is mutated in patients with Wolcott-Rallison syndrome. Nat. Genet. 25:406-409.
18. Deng, J., H. Harding, B. Raught, A. Gingras, J. Berlanga, D. Scheuner, R. Kaufman, D. Ron, and N. Sonenberg. 2002. Activation of GCN2 in UV-irradiated cells inhibits translation. Curr. Biol. 12:1279-1286.
19. Dong, J., H. Qiu, M. Garcia-Barrio, J. Anderson, and A. G. Hinnebusch. 2000. Uncharged tRNA activates GCN2 by displacing the protein kinase moiety from a bipartite tRNA-binding domain. Mol. Cell 6:269-279.
20. Fafournoux, P., A. Bruhat, and C. Jousse, 2000. Amino acid regulation of gene expression. Biochem. J. 351:1-12.
21. Fawcett, T. W., H. B. Eastman, J. L. Martindale, and N. J. Holbrook, 1996. Physical and functional association between GADD153 and CCAAT/enhancer-binding protein beta during cellular stress. J. Biol. Chem. 271:14285-14289.
22. Fawcett, T. W., J. L. Martindale, K. Z. Guyton, T. Hai, and N. J. Holbrook, 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. 339:135-141.
23. Fernandez, J., I. Yaman, W. C. Merrick, A. Koromilas, R. C. Wek, R. Sood, J. Hensold, and M. Hatzoglou, 2002. Regulation of internal ribosome entry site-mediated translation by eukaryotic initiation factor-2α phosphorylation and small upstream open reading frame. J. Biol. Chem. 277:2050-2058.
24. Fornace, A. J., D. W. Nebert, M. C. Hollander, J. D. Luethy, M. Papathanasiu, J. Fargnoli, and N. J. Holbrook. 1989. Mammalian genes coordinately regulated by growth arrest signals and DNA-damaging agents. Mol. Cell. Biol. 10:4196-4203.
25. Gong, P., D. Stewart, B. Hu, C. Vinson, and J. Alam. 2002. Multiple basic leucine zipper proteins regulate induction of the mouse heme oxygenase-1 gene by arsenite. Arch. Biochem. Biophys. 405:265-274.
26. Hai, T., and M. G. Hartman. 2001. The molecular biology and nomenclature of the activating transcription factor/cAMP responsive element binding family of transcription factors: activating transcription factor proteins and homeostasis. Gene 273:1-11.
27. Hai, T., C. D. Wolfgang, D. K. Marsee, A. E. Allen, and U. Sivaprasad. 1999. ATF3 and stress responses. Gene Expr. 7:321-335.
28. -/- mice reveals a role for translational control in secretory cell survival. Mol. Cell 7:1153-1163.
29. Harding, H. P., M. Calfon, F. Urano, I. Novoa, and D. Ron. 2002. Transcriptional and translational control in the mammalian unfolded protein response. Ann. Rev. Cell Dev. Biol. 18:575-599.
30. 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.
31. Harding, H. P., Y. Zhang, A. Bertolotti, H. Zeng, and D. Ron. 2000. Perk is essential for translation regulation and cell survival during the unfolded protein response. Mol. Cell 5:897-904.
32. 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.
33. Harding, H. P., Y. Zhang, H. Zeng, I. Novoa, P. D. Lu, M. Calfon, N. Sadri, C. Yun, B. Popko, R. Paules, D. F. Stojdl, J. C. Bell, T. Hettmann, J. M. Leiden, and D. Ron. 2003. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol. Cell 11:619-633.
34. Haze, K., H. Yoshida, H. Yanagi, T. Yura, and K. Mori. 1999. Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol. Cell. Biol. 10:3787-3799.
35. Hershey, J. W. B., and W. C. Merrick. 2000. Pathway and mechanism of initiation of protein synthesis, p. 33-88. In N. Sonenberg, J. W. B. Hershey, and M. B. Mathews (ed.), Translational control of gene expression. Cold Spring Harbor Laboratory Press, Plainview, N.Y.
36. 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.
37. Hinnebusch, A. G., and K. Natarajan. 2002. Gcn4p, a master regulator of gene expression, is controlled at multiple levels by diverse signals of starvation and stress. Eukaryot. Cell 1:22-32.
38. Hollander, M. C., Q. Zhan, I. Bae, and A. J. Fornace. 1997. Mammalian GADD34, an apoptosis- and DNA damage-inducible gene. J. Biol. Chem. 272:13731-13737.
39. 1 promoter activity by NF-KB family members. J. Virol. 76:5737-5747.
40. Jiang, H.-Y., S. A. Wek, B. C. McGrath, D. Scheuner, R. J. Kaufmann, D. R. Cavener, and R. C. Wek. 2003. Phosphorylation of the a subunit of eukaryotic initiation factor 2 is required for activation of NF-κB in response to diverse cellular stresses. Mol. Cell. Biol. 23:5651-5663.
41. Kaufman, R. J., D. Scheuner, M. Schroder, X. Shen, K. Lee, C. Y. Lin, and S. M. Arnold. 2002. The unfolded protein response in nutrient sensing and differentiation. Nat. Rev. Mol. Cell Biol. 3:411-421.
42. Lee, K., W. Tirasophon, X. Shen, M. Michalak, R. Prywes, T. Okada, H. Yoshida, K. Mori, and R. J. Kaufman. 2002. IRE1-mediated unconventional mRNA splicing and S2P-mediated ATF6 cleavage merge to regulate XBPI in signaling the unfolded protein response. Genes Dev. 16:452-466.
43. Ma, K., K. M. Vattem, and R. C. Wek. 2002. Dimerization and release of molecular chaperone inhibition facilitate activation of eukaryotic initiation factor-2 kinase in response to endoplasmic reticulum stress. J. Biol. Chem. 277:18728-18735.
44. Ma, Y., J. W. Brewer, J. A. Diehl, and L. M. Hendershot. 2002. Two distinct stress signaling pathways converge upon the CHOP promoter during the mammalian unfolded protein response. J. Mol. Biol. 318:1351-1365.
45. 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.
46. Natarajan, K., M. R. Meyer, B. M. Jackson, D. Slade, C. Robertsw, A. G. Hinnebusch, and M. J. Marton. 2001. Transcriptional profiling shows that Gcn4p is a master controller of gene expression during amino acid starvation in yeast. Mol. Cell. Biol. 21:4347-4368.
47. 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.
48. 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.
49. Okada, T., H. Yoshida, R. Akazawa, M. Negishi, and K. Mori. 2002. Distinct roles of activating transcription factor 6 (ATF6) and double-stranded RNA-activated protein kinase-like endoplasmic reticulum kinase (PERK) in transcription during the mammalian unfolded protein response. Biochem. J. 366:585-594.
50. Oyadomari, S., A. Koizumi, K. Takeda, T. Gotoh, S. Akira, E. Araki, and M. Mori. 2002. Targeted disruption of the Chop gene delays endoplasmic reticulum stress-mediated diabetes. J. Clin. Investig. 109:525-532.
51. Pan, Y., H. Chen, F. Siu, and M. S. Kilberg. 2003. Amino acid deprivation and endoplasmic reticulum stress induce expression of multiple activating transcription factor-3 species that, when overexpressed in HepG2 cells, modulate transcription by the human asparagine synthetase promoter. J. Biol. Chem. 278:38402-38412.
52. Patil, C., and P. Walter. 2001. Intracellular signalling from the endoplasmic reticulum to the nucleus: the unfolded protein response in yeast and mammals. Curr. Opin. Cell Biol. 13:349-355.
53. Ron, D., and J. F. Habener. 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.
54. Ron, D., and H. P. Harding. 2000. PERK and translational control by stress in the endoplasmic reticulum, p. 547-560. In N. Sonenberg, J. W. B. Hershey, and M. B. Mathews (ed.), Translational control of gene expression. Cold Spring Harbor Laboratory Press, Plainview, N.Y.
55. Ruegsegger, U., J. H. Leber, and P. Walter. 2001. Block of HACI mRNA translation by long-range base pairing is released by cytoplasmic splicing upon induction of the unfolded protein response. Cell 107:103-114.
56. Schauer, S. L., Z. Wang, G. E. Sonenshein, and T. L. Rothstein. 1996. Maintenance of nuclear factor-κB/Rel and c-myc expression during CD40 ligand rescue of WEHI 231 early B cells from receptor-mediated apoptosis through modulation of IκB proteins. J. Immunol. 157:81-86.
57. Seheuner, D., B. Song, E. McEwen, C. Liu, R. Laybutt, P. Gillespie, T. Saunders, S. Bonner-Weir, and R. J. Kaufman. 2001. Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol. Cell 7:1165-1176.
58. Shi, Y., K. M. Vattem, R. Sood, J. An, J. Liang, L. Stramm, and R. C. Wek. 1998. Identification and characterization of pancreatic eukaryotic initiation factor 2 a-subunit kinase, PEK, involved in translation control. Mol. Cell. Biol. 18:7499-7509.
59. Sidrauski, C., and P. Walter. 1997. The transmembrane kinase Irelp is a site-specific endonuclease that initiates mRNA splicing in the unfolded protein response. Cell 90:1031-1039.
60. Siu, F., P. J. Blain, R. LeBlanc-Chaffin, H. Chen, and M. S. Kilberg. 2002. ATF4 is a mediator of the nutrient-sensing response pathway that activates the human asparagine synthetase gene. J. Biol. Chem. 277:24120-24127.
61. Sood, R., A. C. Porter, K. Ma, L. A. Quilliam, and R. C. Wek. 2000. Pancreatic eukaryotic initiation factor 2α kinase (PEK) homologues in humans, Drosophila melanogaster and Caenorhabditis elegans that mediate translational control in response to ER stress. Biochem. J. 346:281-293.
62. Sood, R., A. C. Porter, D. Olsen, D. R. Cavener, and R. C. Wek. 2000. A mammalian homologue of GCN2 protein kinase important for translational control by phosphorylation of eukaryotic initiation factor 2α. Genetics 154:787-801.
63. Sovak, M. A., R. E. Bellas, D. W. Kim, G. J. Zanieski, A. E. Rogers, A. M. Traish, and G. E. Sonenshein. 1997. Aberrant nuclear factor-κB/Rel expression and the pathogenesis of breast cancer. J. Clin. Investig. 100:2952-2960.
64. Thornton, C. M., D. J. Carson, and F. J. Stewart. 1997. Autopsy findings in the Wolcott-Rallison syndrome. Pediatr. Pathol. Lab. Med. 17:487-496.
65. Ung, T. L., C. Cao, J. Lu, K. Ozato, and T. E. Dever. 2001. Heterologous dimerization domains functionally substitute for the double-stranded RNA binding domains of the kinase PKR. EMBO J. 20:3728-3737.
66. Vattem, K., K. A. Staschke, and R. C. Wek. 2001. Mechanism of activation of the double-stranded-RNA-dependent protein kinase. PKR: role of dimerization and cellular localization in the stimulation of PKR phosphorylation of eukaryotic initiation factor 2α (eIF2α). Eur. J. Biochem. 268:3674-3684.
67. Wek, R. C. 1994. eIF-2 kinases: regulators of general and gene-specific translation initiation. Trends Biochem. Sci. 19:491-496.
68. Wek, S. A., S. Zhu, and R. C. Wek. 1995. The histidyl-tRNA synthetaserelated sequence in eIF-2α protein kinase GCN2 interacts with tRNA and is required for activation in response to starvation for different amino acids. Mol. Cell. Biol. 15:4497-4506.
69. Williams, B. R. 1999. PKR: a sentinel kinase for cellular stress. Oncogene 18:6112-6120.
70. Williams, D. A., M. F. Rosenblatt, D. R. Beier, and R. D. Cone. 1988. Generation of murine stromal cell lines supporting hemampoietic stem cell proliferation by use of recombinant retrovirus vectors encoding simian virus 40 large T antigen. Mol. Cell. Biol. 8:3864-3871.
71. Willnow, T. E., and J. Herz. 1994. Homologous recombination for gene replacement in mouse cell lines. Methods Cell Biol. 43:305-334.
72. Wu, S., Y. Hu, J. L. Wang, M. Chatterjee, Y. Shi, and R. J. Kaufman. 2002. Ultraviolet light inhibits translation through activation of the unfolded protein response kinase PERK in the lumen of the endoplasmic reticulum. J. Biol. Chem. 277:18077-18083.
73. Yang, Y.-L., Y. F. L. Reis, J. Pavlovie, A. Aguzzi, R. Schafer, A. Kumar, B. R. G. Williams, M. Aguet, and C. Weissman. 1995. Deficient signalling in mice devoid of double-stranded RNA-dependent protein kinase. EMBO J. 14:6095-6106.
74. Yoshida, H., T. Matsui, A. Yamamotot, T. Okada, and K. Mori. 2001. XPBI mRNA is induced by ATF6 and spliced by IREI in response to ER stress to produce a highly active transcription factor. Cell 107:881-891.
75. Zhang, P., B. McGrath, S. Li, A. Frank, F. Zambito, J. Reinert, M. Gannon, K. Ma, K. McNaughton, and D. R. Cavener. 2002. The PERK eukaryotic initiation factor 2α kinase is required for the development of the skeletal system, postnatal growth, and the function and viability of the pancreas. Mol. Cell. Biol. 22:3864-3874.
76. Zhang, P., B. C. McGrath, J. Reinert, D. S. Olsen, L. Lei, S. Gill, S. A. Wek, K. M. Vattem, R. C. Wek, S. R. Kimball, L. S. Jefferson, and D. R. Cavener. 2002. The GCN2 eIF2α kinase is required for adaptation to amino acid deprivation in mice. Mol. Cell. Biol. 22:6681-6688.
77. Zhu, S., A. Y. Sobolev, and R. C. Wek. 1996. Histidyl-tRNA synthetaserelated sequences in GCN2 protein kinasc regulate in vitro phosphorylation of eIF-2. J. Biol. Chem. 271:24989-24994.
78. Zinszner, H., M. Kuroda, X. Z. Wang, N. Batchvarova, R. T. Lightfoot, H. Remotti, J. L. Stevens, and D. Ron. 1998. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev. 12:982-995.