Ionizing radiation activates PERK/eIF2α/ATF4 signaling via ER stress-independent pathway in human vascular endothelial cells

International Journal of Radiation Biology

Volumn 90, Issue 4, 2014, Pages 306-312

  Kim, Eun Ju ^a   Lee, Yoon Jin ^a   Kang, Seongman ^b   Lim, Young Bin ^a  

^a Korea Institute of Radiation and Medical Science   (South Korea)

^b Korea University   (South Korea)

Author keywords

Chemical chaperone; Endoplasmic reticulum stress; Ionizing radiation; Unfolded protein response

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; ACTIVATING TRANSCRIPTION FACTOR 6; GLUCOSE REGULATED PROTEIN 78; GLUCOSE REGULATED PROTEIN 94; INITIATION FACTOR 2ALPHA; PERK PROTEIN; PROTEIN; PROTEIN IRE1; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1;

ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; HUMAN; HUMAN CELL; IONIZING RADIATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN GLYCOSYLATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; UMBILICAL VEIN ENDOTHELIAL CELL; UPREGULATION;

ACTIVATING TRANSCRIPTION FACTOR 4; ASPARTATE-AMMONIA LIGASE; CELL CYCLE PROTEINS; CELLS, CULTURED; EIF-2 KINASE; ENDOPLASMIC RETICULUM STRESS; ENDOTHELIAL CELLS; EUKARYOTIC INITIATION FACTOR-2; HUMANS; PROTEIN-SERINE-THREONINE KINASES; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE;

EID: 84897494593     PISSN: 09553002     EISSN: 13623095     Source Type: Journal    
DOI: 10.3109/09553002.2014.886793     Document Type: Article

References (37)

1. Cawley K, Deegan S, Samali A, Gupta S. 2011. Assays for detecting the unfolded protein response. Meth Enzymol 490:31-51.
2. Chen JJ, London IM. 1995. Regulation of protein synthesis by heme-regulated eIF-2 alpha kinase. Trends Biochem Sci 20: 105-108.
3. Clemens MJ. 1997. PKR-a protein kinase regulated by double-stranded RNA. Int J Biochem 29:945-949.
4. Daly MJ, Gaidamakova EK, Matrosova VY, Vasilenko A, Zhai M, Leapman RD, Lai B, Ravel B, Li S-MW, Kemner KM, et al. 2007. Protein oxidation implicated as the primary determinant of bacterial radioresistance. PLoS Biol 5:e92.
5. Du J, Gebicki JM. 2004. Proteins are major initial cell targets of hydroxyl free radicals. Int J Biochem Cell Biol 36: 2334-2343.
6. Engin F, Hotamisligil GS. 2010. Restoring endoplasmic reticulum function by chemical chaperones: An emerging therapeutic approach for metabolic diseases. Diabetes, Obes Metabolism 12: 108-115.
7. Harding HP, Zhang Y, Zeng H, Novoa I, Lu PD, Calfon M, Sadri N, Yun C, Popko B, Paules R, et al. 2003. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Molec Cell 11:619-633.
8. Heifetz A, Keenan RW, Elbein AD. 1979. Mechanism of action of tunicamycin on the UDP-GlcNAc:dolichyl-phosphate Glc-NAc-1-phosphate transferase. Biochemistry 18:2186-2192.
9. Hotamisligil GS. 2010. Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 140: 900-917.
10. Kaser A, Blumberg RS. 2010. Endoplasmic reticulum stress and intestinal infammation. Mucosal Immunol 3:11-16.
11. Kaser A, Lee AH, Franke A, Glickman JN, Zeissig S, Tilg H, Nieuwenhuis EE, Higgins DE, Schreiber S, Glimcher LH, et al. 2008. XBP1 links ER stress to intestinal inflammation and confers genetic risk for human infammatory bowel disease. Cell 134:743-756.
12. Kergonou JF, Bernard P, Braquet M, Rocquet G. 1981. effect of whole-body gamma irradiation on lipid peroxidation in rat tissues. Biochimie 63:555-559.
13. Kilberg MS, Shan J, Su N. 2009. ATF4-dependent transcription mediates signaling of amino acid limitation. Trends Endocrinol Metabolism 20: 436-443.
14. Kim KW, Moretti L, Mitchell LR, Jung DK, Lu B. 2010. Endoplasmic reticulum stress mediates radiation-induced autophagy by perk-eIF2 α in caspase-3/7-defcient cells. Oncogene 29:3241-3251.
15. Lee AH, Iwakoshi NN, Glimcher LH. 2003. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Molec Cellular Biol 23:7448-7459.
16. Lee AS. 2005. The ER chaperone and signaling regulator GRP78/BiP as a monitor of endoplasmic reticulum stress. Methods 35:373-381.
17. Lim YB, Kang SS, Park TK, Lee YS, Chun JS, Sonn JK. 2000. Disruption of actin cytoskeleton induces chondrogenesis of mesenchymal cells by activating protein kinase C-alpha signaling. Biochem Biophys Res Communic 273:609-613.
18. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402-408.
19. Lo SS, Fakiris AJ, Chang EL, Mayr NA, Wang JZ, Papiez L, Teh BS, McGarry RC, Cardenes HR, Timmerman RD 2010. Stereotactic body radiation therapy: A novel treatment modality. Nature Rev. Clin Oncol 7:44-54.
20. Nagelkerke A, Bussink J, van der Kogel AJ, Sweep FC, Span PN. 2013. The PERK/ATF4/LAMP3-arm of the unfolded protein response af ects radioresistance by interfering with the DNA damage response. Radiother Oncol 108: 415-421.
21. Nakazawa T, Nagatsuka S. 1980. Radiation-induced lipid peroxida-tion and membrane permeability in liposomes. Int J Radiat Biol 38: 537-544.
22. Ohoka N, Yoshii S, Hattori T, Onozaki K, Hayashi H. 2005. TRB3, a novel ER stress-inducible gene, is induced via ATF4-CHOP pathway and is involved in cell death. EMBO J 24: 1243-1255.
23. Ozcan U. 2006. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 313:1137-1140.
24. Panganiban RAM, Mungunsukh O, Day RM. 2013. X-irradiation induces ER stress, apoptosis, and senescence in pulmonary artery endothelial cells. Int J Radiat Biol 89: 656-667.
25. Papp E, Csermely P. 2006. Chemical chaperones: Mechanisms of action and potential use. Handbook Experim Pharmacol 172: 405-416.
26. Park HJ, Griffin RJ, Hui S, Levitt SH, Song CW. 2012. Radiation-induced vascular damage in tumors: Implications of vascular damage in ablative hypofractionated radiotherapy (SBRT and SRS). Radiat Res 177:311-327.
27. Samali A, FitzGerald U, Deegan S, Gupta S. 2010. Methods for monitoring endoplasmic reticulum stress and the unfolded protein response. Int J Cell Biol 2010:1-11.
28. Scian MJ, Stagliano KER, Deb D, Ellis MA, Carchman EH, Das A, Valerie K, Deb SP, Deb S. 2004. Tumor-derived p53 mutants induce oncogenesis by transactivating growth-promoting genes. Oncogene 23:4430-4443.
29. Shoulders MD, Ryno LM, Genereux JC, Moresco JJ, Tu PG, Wu C, Yates JR 3rd, Su AI, Kelly JW, Wiseman RL. 2013. Stress-independent activation of XBP1s and/or ATF6 reveals three functionally diverse ER proteostasis environments. Cell Rep 3:1279-1292.
30. Song CW, Cho LC, Yuan J, Dusenbery KE, Grifn RJ, Levitt SH. 2013. Radiobiology of stereotactic body radiation therapy/stereotactic radiosurgery and the linear-quadratic model. Int J Radiat Oncol, Biol, Phys 87:18-19.
31. Volmer R, van der Ploeg K, Ron D. 2013. Membrane lipid saturation activates endoplasmic reticulum unfolded protein response transducers through their transmembrane domains. Proc Nat Acad Sci USA 110:4628-4633.
32. Walter P, Ron D. 2011. The unfolded protein response: From stress pathway to homeostatic regulation. Science 334:1081-1086.
33. Wek RC, Cavener DR. 2007. Translational control and the unfolded protein response. Antioxid Redox Signal 9: 2357-2371.
34. Wek RC, Jiang H-Y, Anthony TG. 2006. Coping with stress: eIF2 kinases and translational control. Biochem Soc Transact 34(Pt 1):7-11
35. Wills ED. 1970. effects of irradiation on sub-cellular components. I. Lipid peroxide formation in the endoplasmic reticulum. Int J Radiat Biol 17:217-228.
36. Ye J, Kumanova M, Hart LS, Sloane K, Zhang H, De Panis DN, Bobrovnikova-Marjon E, Diehl JA, Ron D, Koumenis C. 2010. The GCN2-ATF4 pathway is critical for tumour cell survival and proliferation in response to nutrient deprivation. EMBO J 29:2082-2096.
37. Zhang B, Wang Y, Pang X, Su Y, Ai G, Wang T. 2010. ER stress induced by ionising radiation in IEC-6 cells. Int J Radiat Biol 86:429-435.