Epithelial cell survival by activating transcription factor 3 (ATF3) in response to chemical ribosome-inactivating stress

Biochemical Pharmacology

Volumn 77, Issue 6, 2009, Pages 1105-1115

  Yang, Hyun ^a   Park, Seong Hwan ^a   Choi, Hye Jin ^a   Moon, Yuseok ^a  

^a Pusan National University School of Medicine   (South Korea)

Author keywords

Activating transcription factor 3 (ATF3); Double stranded RNA (dsRNA) activated protein kinase (PKR); Epithelial cell survival; p38 MAP kinase; Ribotoxic stress

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ACTIVATING TRANSCRIPTION FACTOR 3; GLYCOGEN SYNTHASE KINASE 3BETA; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38;

APOPTOSIS; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; EPITHELIUM CELL; GENE EXPRESSION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN STABILITY; RIBOSOME; STRESS; UPREGULATION;

ACTIVATING TRANSCRIPTION FACTOR 3; ANISOMYCIN; CELL LINE; CELL SURVIVAL; DNA DAMAGE; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; HUMANS; INTESTINAL MUCOSA; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RIBOSOMES; TRICHOTHECENES; UP-REGULATION;

EID: 60649096104     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2008.11.028     Document Type: Article

References (49)

1. Laskin J.D., Heck D.E., and Laskin D.L. The ribotoxic stress response as a potential mechanism for MAP kinase activation in xenobiotic toxicity. Toxicol Sci 69 2 (2002) 289-291
2. Shifrin V.I., and Anderson P. Trichothecene mycotoxins trigger a ribotoxic stress response that activates c-Jun N-terminal kinase and p38 mitogen-activated protein kinase and induces apoptosis. J Biol Chem 274 20 (1999) 13985-13992
3. Iordanov M.S., Pribnow D., Magun J.L., Dinh T.H., Pearson J.A., Chen S.L., et al. Ribotoxic stress response: activation of the stress-activated protein kinase JNK1 by inhibitors of the peptidyl transferase reaction and by sequence-specific RNA damage to the alpha-sarcin/ricin loop in the 28S rRNA. Mol Cell Biol 17 6 (1997) 3373-3381
4. Iordanov M.S., Pribnow D., Magun J.L., Dinh T.H., Pearson J.A., and Magun B.E. Ultraviolet radiation triggers the ribotoxic stress response in mammalian cells. J Biol Chem 273 25 (1998) 15794-15803
5. Liang G., Wolfgang C.D., Chen B.P., Chen T.H., and Hai T. ATF3 gene. Genomic organization, promoter, and regulation. J Biol Chem 271 3 (1996) 1695-1701
6. Jiang H.Y., Wek S.A., McGrath B.C., Lu D., Hai T., Harding H.P., et al. Activating transcription factor 3 is integral to the eukaryotic initiation factor 2 kinase stress response. Mol Cell Biol 24 3 (2004) 1365-1377
7. Yin X., Dewille J.W., and Hai T. A potential dichotomous role of ATF3, an adaptive-response gene, in cancer development. Oncogene 27 15 (2008) 2118-2127
8. Duggan S.P., Gallagher W.M., Fox E.J., Abdel-Latif M.M., Reynolds J.V., and Kelleher D. Low pH induces co-ordinate regulation of gene expression in oesophageal cells. Carcinogenesis 27 2 (2006) 319-327
9. Harper E.G., Alvares S.M., and Carter W.G. Wounding activates p38 map kinase and activation transcription factor 3 in leading keratinocytes. J Cell Sci 118 Pt 15 (2005) 3471-3485
10. Brigotti M., Carnicelli D., Ravanelli E., Vara A.G., Martinelli C., Alfieri R.R., et al. Molecular damage and induction of proinflammatory cytokines in human endothelial cells exposed to Shiga toxin 1, Shiga toxin 2, and alpha-sarcin. Infect Immun 75 5 (2007) 2201-2207
11. 2-terminal kinase and Bim. Mol Cancer Res 5 8 (2007) 783-792
12. Bhat R.V., Beedu S.R., Ramakrishna Y., and Munshi K.L. Outbreak of trichothecene mycotoxicosis associated with consumption of mould-damaged wheat production in Kashmir Valley, India. Lancet 1 8628 (1989) 35-37
13. Pestka J.J., and Smolinski A.T. Deoxynivalenol: toxicology and potential effects on humans. J Toxicol Environ Health B Crit Rev 8 1 (2005) 39-69
14. Li M., Harkema J.R., Cuff C.F., and Pestka J.J. Deoxynivalenol exacerbates viral bronchopneumonia induced by respiratory reovirus infection. Toxicol Sci 95 2 (2007) 412-426
15. Maresca M., Mahfoud R., Garmy N., and Fantini J. The mycotoxin deoxynivalenol affects nutrient absorption in human intestinal epithelial cells. J Nutr 132 9 (2002) 2723-2731
16. Sergent T., Parys M., Garsou S., Pussemier L., Schneider Y.J., and Larondelle Y. Deoxynivalenol transport across human intestinal Caco-2 cells and its effects on cellular metabolism at realistic intestinal concentrations. Toxicol Lett 164 2 (2006) 167-176
17. Yang H., Chung D.H., Kim Y.B., Choi Y.H., and Moon Y. Ribotoxic mycotoxin deoxynivalenol induces G2/M cell cycle arrest via p21Cip/WAF1 mRNA stabilization in human epithelial cells. Toxicology 243 1-2 (2008) 145-154
18. Reimertz C., Kogel D., Rami A., Chittenden T., and Prehn J.H. Gene expression during ER stress-induced apoptosis in neurons: induction of the BH3-only protein Bbc3/PUMA and activation of the mitochondrial apoptosis pathway. J Cell Biol 162 4 (2003) 587-597
19. Zhang F., Hamanaka R.B., Bobrovnikova-Marjon E., Gordan J.D., Dai M.S., Lu H., et al. Ribosomal stress couples the unfolded protein response to p53-dependent cell cycle arrest. J Biol Chem 281 40 (2006) 30036-30045
20. Seijffers R., Mills C.D., and Woolf C.J. ATF3 increases the intrinsic growth state of DRG neurons to enhance peripheral nerve regeneration. J Neurosci 27 30 (2007) 7911-7920
21. Yoshida T., Sugiura H., Mitobe M., Tsuchiya K., Shirota S., Nishimura S., et al. ATF3 protects against renal ischemia-reperfusion injury. J Am Soc Nephrol 19 2 (2008) 217-224
22. Smith W.E., Kane A.V., Campbell S.T., Acheson D.W., Cochran B.H., and Thorpe C.M. Shiga toxin 1 triggers a ribotoxic stress response leading to p38 and JNK activation and induction of apoptosis in intestinal epithelial cells. Infect Immun 71 3 (2003) 1497-1504
23. Wang L., Li T., and Lu L. UV-induced corneal epithelial cell death by activation of potassium channels. Invest Ophthalmol Vis Sci 44 12 (2003) 5095-5101
24. Lin Z., Crockett D.K., Jenson S.D., Lim M.S., and Elenitoba-Johnson K.S. Quantitative proteomic and transcriptional analysis of the response to the p38 mitogen-activated protein kinase inhibitor SB203580 in transformed follicular lymphoma cells. Mol Cell Proteomics 3 8 (2004) 820-833
25. Iordanov M.S., Paranjape J.M., Zhou A., Wong J., Williams B.R., Meurs E.F., et al. Activation of p38 mitogen-activated protein kinase and c-Jun NH(2)-terminal kinase by double-stranded RNA and encephalomyocarditis virus: involvement of RNase L, protein kinase R, and alternative pathways. Mol Cell Biol 20 2 (2000) 617-627
26. Iordanov M.S., Wong J., Bell J.C., and Magun B.E. Activation of NF-kappaB by double-stranded RNA (dsRNA) in the absence of protein kinase R and RNase L demonstrates the existence of two separate dsRNA-triggered antiviral programs. Mol Cell Biol 21 1 (2001) 61-72
27. Lu D., Wolfgang C.D., and Hai T. Activating transcription factor 3, a stress-inducible gene, suppresses Ras-stimulated tumorigenesis. J Biol Chem 281 15 (2006) 10473-10481
28. Yan C., Lu D., Hai T., and Boyd D.D. Activating transcription factor 3, a stress sensor, activates p53 by blocking its ubiquitination. Embo J 24 13 (2005) 2425-2435
29. Kawauchi J., Zhang C., Nobori K., Hashimoto Y., Adachi M.T., Noda A., et al. Transcriptional repressor activating transcription factor 3 protects human umbilical vein endothelial cells from tumor necrosis factor-alpha-induced apoptosis through down-regulation of p53 transcription. J Biol Chem 277 41 (2002) 39025-39034
30. Lu D., Chen J., and Hai T. The regulation of ATF3 gene expression by mitogen-activated protein kinases. Biochem J 401 2 (2007) 559-567
31. Alvarado-Kristensson M., Melander F., Leandersson K., Ronnstrand L., Wernstedt C., and Andersson T. p38-MAPK signals survival by phosphorylation of caspase-8 and caspase-3 in human neutrophils. J Exp Med 199 4 (2004) 449-458
32. Colombara M., Antonini V., Riviera A.P., Mainiero F., Strippoli R., Merola M., et al. Constitutive activation of p38 and ERK1/2 MAPKs in epithelial cells of myasthenic thymus leads to IL-6 and RANTES overexpression: effects on survival and migration of peripheral T and B cells. J Immunol 175 10 (2005) 7021-7028
33. Guo X., Ramirez A., Waddell D.S., Li Z., Liu X., and Wang XF. Axin and GSK3-control Smad3 protein stability and modulate TGF-signaling. Genes Dev 22 1 (2008) 106-120
34. Ha N.C., Tonozuka T., Stamos J.L., Choi H.J., and Weis W.I. Mechanism of phosphorylation-dependent binding of APC to beta-catenin and its role in beta-catenin degradation. Mol Cell 15 4 (2004) 511-521
35. Topol L., Jiang X., Choi H., Garrett-Beal L., Carolan P.J., and Yang Y. Wnt-5a inhibits the canonical Wnt pathway by promoting GSK-3-independent beta-catenin degradation. J Cell Biol 162 5 (2003) 899-908
36. Doble B.W., and Woodgett J.R. GSK-3: tricks of the trade for a multi-tasking kinase. J Cell Sci 116 Pt 7 (2003) 1175-1186
37. Kockeritz L., Doble B., Patel S., and Woodgett J.R. Glycogen synthase kinase-3-an overview of an over-achieving protein kinase. Curr Drug Targets 7 11 (2006) 1377-1388
38. Lali F.V., Hunt A.E., Turner S.J., and Foxwell B.M. The pyridinyl imidazole inhibitor SB203580 blocks phosphoinositide-dependent protein kinase activity, protein kinase B phosphorylation, and retinoblastoma hyperphosphorylation in interleukin-2-stimulated T cells independently of p38 mitogen-activated protein kinase. J Biol Chem 275 10 (2000) 7395-7402
39. Park C.M., Park M.J., Kwak H.J., Lee H.C., Kim M.S., Lee S.H., et al. Ionizing radiation enhances matrix metalloproteinase-2 secretion and invasion of glioma cells through Src/epidermal growth factor receptor-mediated p38/Akt and phosphatidylinositol 3-kinase/Akt signaling pathways. Cancer Res 66 17 (2006) 8511-8519
40. Rane M.J., Coxon P.Y., Powell D.W., Webster R., Klein J.B., Pierce W., et al. p38 kinase-dependent MAPKAPK-2 activation functions as 3-phosphoinositide-dependent kinase-2 for Akt in human neutrophils. J Biol Chem 276 5 (2001) 3517-3523
41. Garcia M.A., Gil J., Ventoso I., Guerra S., Domingo E., Rivas C., et al. Impact of protein kinase PKR in cell biology: from antiviral to antiproliferative action. Microbiol Mol Biol Rev 70 4 (2006) 1032-1060
42. Williams B.R. Signal integration via PKR. Sci STKE 2001 89 (2001) RE2
43. Barber G.N. The dsRNA-dependent protein kinase, PKR and cell death. Cell Death Differ 12 6 (2005) 563-570
44. Williams B.R. PKR; a sentinel kinase for cellular stress. Oncogene 18 45 (1999) 6112-6120
45. Dewitte-Orr S.J., Zorzitto J.R., Sutton L.P., and Bols N.C. Preferential induction of apoptosis in the rainbow trout macrophage cell line, RTS11, by actinomycin D, cycloheximide and double stranded RNA. Fish Shellfish Immunol 18 4 (2005) 279-295
46. Gray J.S., Bae H.K., Li J.C., Lau A.S., and Pestka J.J. Double-stranded RNA-activated protein kinase mediates induction of interleukin-8 expression by deoxynivalenol, Shiga toxin 1, and ricin in monocytes. Toxicol Sci 105 2 (2008) 322-330
47. Zhou H.R., Lau A.S., and Pestka J.J. Role of double-stranded RNA-activated protein kinase R (PKR) in deoxynivalenol-induced ribotoxic stress response. Toxicol Sci 74 2 (2003) 335-344
48. Donze O., Deng J., Curran J., Sladek R., Picard D., and Sonenberg N. The protein kinase PKR: a molecular clock that sequentially activates survival and death programs. EMBO J 23 3 (2004) 564-571
49. Ruller S., Stahl C., Kohler G., Eickhoff B., Breder J., Schlaak M., et al. Sensitization of tumor cells to ribotoxic stress-induced apoptotic cell death: a new therapeutic strategy. Clin Cancer Res 5 10 (1999) 2714-2725