Endoplasmic reticulum stress mediates radiation-induced autophagy by perk-eIF2α in caspase-3/7-deficient cells

Oncogene

Volumn 29, Issue 22, 2010, Pages 3241-3251

  Kim, K W ^a   Moretti, L ^a   Mitchell, L R ^a   Jung, D K ^a   Lu, B ^a  

^a VANDERBILT INGRAM CANCER CENTER   (United States)

Author keywords

Autophagy; Cancer; ER stress; PERK; Radiation

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; CASPASE 3; CASPASE 7; INITIATION FACTOR 2ALPHA; INOSITOL REQUIRING ENZYME 1; MEMBRANE PROTEIN; PROTEIN KINASE LIKE ENDOPLASMIC RETICULUM KINASE; TUNICAMYCIN; UNCLASSIFIED DRUG; HEAT SHOCK PROTEIN; PERK KINASE; PROTEIN KINASE R; RADIOSENSITIZING AGENT;

ANIMAL CELL; ARTICLE; AUTOPHAGY; BREAST CANCER; CANCER RADIOTHERAPY; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; RADIOSENSITIVITY; APOPTOSIS; BIOSYNTHESIS; BREAST NEOPLASMS; CELL DEATH; DEFICIENCY; DRUG EFFECTS; FEMALE; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC TRANSFECTION; GENETICS; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGICAL STRESS; PHYSIOLOGY; RADIATION RESPONSE; TUMOR CELL LINE;

APOPTOSIS; AUTOPHAGY; BREAST NEOPLASMS; CASPASE 3; CASPASE 7; CELL DEATH; CELL LINE, TUMOR; EIF-2 KINASE; ENDOPLASMIC RETICULUM; FEMALE; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; HEAT-SHOCK PROTEINS; HUMANS; PHOSPHORYLATION; RADIATION-SENSITIZING AGENTS; STRESS, PHYSIOLOGICAL; TRANSFECTION; TUNICAMYCIN;

EID: 77953232252     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2010.74     Document Type: Article

References (39)

1. Bernales S, McDonald KL, Walter P. (2006). Autophagy counterbalances endoplasmic reticulum expansion during the unfolded protein response. PLoS Biol 4: e423.
2. Cao C, Subhawong T, Albert JM, Kim KW, Geng L, Sekhar KR et al. (2006). Inhibition of mammalian target of rapamycin or apoptotic pathway induces autophagy and radiosensitizes PTEN null prostate cancer cells. Cancer Res 66: 10040-10047.
3. Dahmer MK. (2005). Caspases-2,-3, and-7 are involved in thapsigargin-induced apoptosis of SH-SY5Y neuroblastoma cells. J Neurosci Res 80: 576-583.
4. Daido S, Yamamoto A, Fujiwara K, Sawaya R, Kondo S, Kondo Y. (2005). Inhibition of the DNA-dependent protein kinase catalytic subunit radiosensitizes malignant glioma cells by inducing auto-phagy. Cancer Res 65: 4368-4375.
5. Delom F, Emadali A, Cocolakis E, Lebrun JJ, Nantel A, Chevet E. (2007a). Calnexin-dependent regulation of tunicamycin-induced apo-ptosis in breast carcinoma MCF-7 cells. Cell Death Differ 14: 586-596.
6. Delom F, Fessart D, Chevet E. (2007b). Regulation of calnexin sub-cellular localization modulates endoplasmic reticulum stress-induced apoptosis in MCF-7 cells. Apoptosis 12: 293-305.
7. Devarajan E, Sahin AA, Chen JS, Krishnamurthy RR, Aggarwal N, Brun AM et al. (2002). Down-regulation of caspase 3 in breast cancer: a possible mechanism for chemoresistance. Oncogene 21: 8843-8851.
8. Ding WX, Ni HM, Gao W, Hou YF, Melan MA, Chen X et al. (2007). Differential effects of endoplasmic reticulum stress-induced auto-phagy on cell survival. J Biol Chem 282: 4702-4710.
9. Eisenberg-Lerner A, Bialik S, Simon HU, Kimchi A. (2009). Life and death partners: apoptosis, autophagy and the cross-talk between them. Cell Death Differ 16: 966-975.
10. Elbein AD. (1987). Inhibitors of the biosynthesis and processing of N-linked oligosaccharide chains. Annu Rev Biochem 56: 497-534.
11. Essmann F, Engels IH, Totzke G, Schulze-Osthoff K, Janicke RU. (2004). Apoptosis resistance of mcf-7 breast carcinoma cells to ionizing radiation is independent of p53 and cell cycle control but caused by the lack of caspase-3 and a caffeine-inhibitable event. Cancer Res 64: 7065-7072.
12. Gelebart P, Opas M, Michalak M. (2005). Calreticulin, a Ca2+-binding chaperone of the endoplasmic reticulum. Int J Biochem Cell Biol 37: 260-266.
13. Harding HP, Zhang Y, Ron D. (1999). Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397: 271-274.
14. Hitomi J, Katayama T, Taniguchi M, Honda A, Imaizumi K, Tohyama M. (2004). Apoptosis induced by endoplasmic reticulum stress depends on activation of caspase-3 via caspase-12. Neurosci Lett 357: 127-130.
15. Janicke RU, Sprengart ML, Wati MR, Porter AG. (1998). Caspase-3 is required for DNA fragmentation and morphological changes associated with apoptosis. J Biol Chem 273: 9357-9360.
16. Kaufman RJ. (1999). Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev 13: 1211-1233.
17. Kim I, Shu CW, Xu W, Shiau CW, Grant D, Vasile S et al. (2009). Chemical biology investigation of cell death pathways activated by endoplasmic reticulum stress reveals cytoprotective modulators of ASK1. J Biol Chem 284: 1593-1603.
18. Kim I, Xu W, Reed JC. (2008a). Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities. Nat Rev Drug Discov 7: 1013-1030.
19. Kim KW, Hwang M, Moretti L, Jaboin JJ, Cha YI, Lu B. (2008b). Autophagy upregulation by inhibitors of caspase-3 and mTOR enhances radiotherapy in a mouse model of lung cancer. Autophagy 4: 659-668.
20. Kim KW, Moretti L, Lu B. (2008c). M867, a novel selective inhibitor of caspase-3 enhances cell death and extends tumor growth delay in irradiated lung cancer models. PLoS ONE 3: e2275.
21. Kim KW, Mutter RW, Cao C, Albert JM, Freeman M, Hallahan DE et al. (2006). Autophagy for cancer therapy through inhibition of pro-apoptotic proteins and mammalian target of rapamycin signaling. J Biol Chem 281: 36883-36890. (Pubitemid 46042156)
22. Kouroku Y, Fujita E, Tanida I, Ueno T, Isoai A, Kumagai H et al. (2007). ER stress (PERK/eIF2alpha phosphorylation) mediates the polyglutamine-induced LC3 conversion, an essential step for autophagy formation. Cell Death Differ 14: 230-239.
23. Lai E, Teodoro T, Volchuk A. (2007). Endoplasmic reticulum stress: signaling the unfolded protein response. Physiology (Bethesda) 22: 193-201.
24. Lee AS. (2005). The ER chaperone and signaling regulator GRP78/BiP as a monitor of endoplasmic reticulum stress. Methods 35: 373-381.
25. Lee AS. (2007). GRP78 Induction in cancer: therapeutic and prognostic implications. Cancer Res 67: 3496-3499.
26. Ma Y, Brewer JW, Diehl JA, Hendershot LM. (2002). Two distinct stress signaling pathways converge upon the CHOP promoter during the mammalian unfolded protein response. J Mol Biol 318: 1351-1365.
27. Marissen WE, Guo Y, Thomas AA, Matts RL, Lloyd RE. (2000). Identification of caspase 3-mediated cleavage and functional alteration of eukaryotic initiation factor 2alpha in apoptosis. J Biol Chem 275: 9314-9323.
28. Mizushima N, Ohsumi Y, Yoshimori T. (2002). Autophagosome formation in mammalian cells. Cell Struct Funct 27: 421-429.
29. Mizushima N, Yamamoto A, Hatano M, Kobayashi Y, Kabeya Y, Suzuki K et al. (2001). Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. J Cell Biol 152: 657-668.
30. Ogata M, Hino S, Saito A, Morikawa K, Kondo S, Kanemoto S et al. (2006). Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol Cell Biol 26: 9220-9231.
31. Ostenfeld MS, Fehrenbacher N, Hoyer-Hansen M, Thomsen C, Farkas T, Jaattela M. (2005). Effective tumor cell death by {sigma}-2 receptor ligand siramesine involves lysosomal leakage and oxidative stress. Cancer Res 65: 8975-8983.
32. Paglin S, Hollister T, Delohery T, Hackett N, McMahill M, Sphicas E et al. (2001). A novel response of cancer cells to radiation involves autophagy and formation of acidic vesicles. Cancer Res 61: 439-444.
33. Palmerini F, Devilard E, Jarry A, Birg F, Xerri L. (2001). Caspase 7, downregulation as an immunohistochemical marker of colonic carcinoma. Hum Pathol 32: 461-467.
34. Romero-Ramirez L, Cao H, Nelson D, Hammond E, Lee A-H, Yoshida H et al. (2004). XBP1 Is essential for survival under hypoxic conditions and is required for tumor growth. Cancer Res 64: 5943-5947.
35. Satoh S, Hijikata M, Handa H, Shimotohno K. (1999). Caspase-mediated cleavage of eukaryotic translation initiation factor subunit 2alpha. Biochem J 342(Part 1): 65-70.
36. Scheuner D, Song B, McEwen E, Liu C, Laybutt R, Gillespie P et al. (2001). Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol Cell 7: 1165-1176.
37. Talloczy Z, Jiang W, Virgin HWt, Leib DA, Scheuner D, Kaufman RJ et al. (2002). Regulation of starvation-and virus-induced autophagy by the eIF2alpha kinase signaling pathway. Proc Natl Acad Sci USA 99: 190-195.
38. Ullman E, Fan Y, Stawowczyk M, Chen HM, Yue Z, Zong WX. (2008). Autophagy promotes necrosis in apoptosis-deficient cells in response to ER stress. Cell Death Differ 15: 422-425.
39. Yorimitsu T, Nair U, Yang Z, Klionsky DJ. (2006). Endoplasmic reticulum stress triggers autophagy. J Biol Chem 281: 30299-30304.