Induction of ER stress-mediated apoptosis by ceramide via disruption of ER Ca2+ homeostasis in human adenoid cystic carcinoma cells

Cell and Bioscience

Volumn 4, Issue 1, 2014, Pages

  Liu, Zhe ^a   Xia, Yichao ^a   Li, Bo ^a   Xu, Hui ^a   Wang, Chenxing ^a   Liu, Ying ^a   Li, Yi ^a   Li, Chunjie ^a   Gao, Ning ^a   Li, Longjiang ^a  

^a SICHUAN UNIVERSITY   (China)

Author keywords

Apoptosis; Cancer; Ceramide; ER calcium; ER stress; Unfolded protein response

Indexed keywords

EID: 84928778302     PISSN: None     EISSN: 20453701     Source Type: Journal    
DOI: 10.1186/2045-3701-4-71     Document Type: Article

References (41)

1. Luo B, Lee AS: The critical roles of endoplasmic reticulum chaperones and unfolded protein response in tumorigenesis and anticancer therapies. Oncogene 2013, 32:805-818. 10.1038/onc.2012.130.
2. McCullough KD, Martindale JL, Klotz LO, Aw TY, Holbrook NJ: Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol Cell Biol 2001, 21:1249-1259. 10.1128/MCB.21.4.1249-1259.2001.
3. Puthalakath H, O'Reilly LA, Gunn P, Lee L, Kelly PN, Huntington ND, Hughes PD, Michalak EM, McKimm-Breschkin J, Motoyama N, Gotoh T, Akira S, Bouillet P, Strasser A: ER stress triggers apoptosis by activating BH3-only protein Bim. Cell 2007, 129:1337-1349. 10.1016/j.cell.2007.04.027.
4. Chan CP, Kok KH, Jin DY: CREB3 subfamily transcription factors are not created equal: Recent insights from global analyses and animal models. Cell Biosci 2011, 17:6.
5. Sekine Y, Takeda K, Ichijo H: The ASK1-MAP kinase signaling in ER stress and neurodegenerative diseases. Curr Mol Med 2006, 6:87-97. 10.2174/156652406775574541.
6. Timmins JM, Ozcan L, Seimon TA, Li G, Malagelada C, Backs J, Backs T, Bassel-Duby R, Olson EN, Anderson ME, Tabas I: Calcium/calmodulin-dependent protein kinase II links endoplasmic reticulum stress with Fas and mitochondrial apoptosis pathways. J. Clin. Invest 2009, 119:2925-2941. 10.1172/JCI38857.
7. Li G, Scull C, Ozcan L, Tabas I: NADPH oxidase links endoplasmic reticulum stress, oxidative stress, and PKR activation to induce apoptosis. J Cell Biol 2010, 191:1113-1125. 10.1083/jcb.201006121.
8. Nakagawa T, Zhu H, Morishima N, Li E, Xu J, Yankner BA, Yuan J: Caspase-12 mediates endoplasmic-reticulum specific apoptosis and cytotoxicity by amyloid-beta. Nature 2000, 403:98-103. 10.1038/47513.
9. Hitomi J, Katayama T, Eguchi Y, Kudo T, Taniguchi M, Koyama Y, Manabe T, Yamagishi S, Bando Y, Imaizumi K, Tsujimoto Y, Tohyama M: Involvement of caspase-4 in endoplasmic reticulum stress-induced apoptosis and Aβ-induced cell death. J Cell Biol 2004, 165:347-356. 10.1083/jcb.200310015.
10. Hitomi J, Katayama T, Taniguchi M, Honda A, Imaizumi K, Tohyama M: Apoptosis induced by endoplasmic reticulum stress depends on activation of caspase-3 via caspase-12. Neurosci Lett 2004, 357:127-130. 10.1016/j.neulet.2003.12.080.
11. Guo X, Zhao B: Integration of mechanical and chemical signals by YAP and TAZ transcription coactivators. Cell Biosci 2013, 3:33. 10.1186/2045-3701-3-33.
12. Young MM, Kester M, Wang HG: Sphingolipids: regulators of crosstalk between apoptosis and autophagy. J Lipid Res 2013, 54:5-19. 10.1194/jlr.R031278.
13. Senkal CE, Ponnusamy S, Bielawski J, Hannun YA, Ogretmen B: Antiapoptotic roles of ceramide-synthase-6-generated C16-ceramide via selective regulation of the ATF6/CHOP arm of ER-stress-response pathways. FASEB 2010, 24:296-308. 10.1096/fj.09-135087.
14. + and ER/Golgi membrane network. J Biol Chem 2011, 286:42446-42458. 10.1074/jbc.M111.287383.
15. Park MA, Zhang G, Martin AP, Hamed H, Mitchell C, Hylemon PB, Graf M, Rahmani M, Ryan K, Liu X, Spiegel S, Norris J, Fisher PB, Grant S, Dent P: Vorinostat and sorafenib increase ER stress, autophagy and apoptosis via ceramide-dependent CD95 and PERK activation. Cancer Biol Ther 2008, 7:1648-1662. 10.4161/cbt.7.10.6623.
16. Margariti A, Li H, Chen T, Martin D, Vizcay-Barrena G, Alam S, Karamariti E, Xiao Q, Zampetaki A, Zhang Z, Wang W, Jiang Z, Gao C, Ma B, Chen YG, Cockerill G, Hu Y, Xu Q, Zeng L: XBP1 mRNA splicing triggers an autophagic response in endothelial cells through BECLIN-1 transcriptional activation. J Biol Chem 2013, 288:859-872. 10.1074/jbc.M112.412783.
17. Shang J, Lehrman MA: Discordance of UPR signaling by ATF6 and Ire1p-XBP1 with levels of target transcripts. Biochem Biophys Res Commun 2004, 317:390-396. 10.1016/j.bbrc.2004.03.058.
18. Back SH, Schröder M, Lee K, Zhang K, Kaufman RJ: ER stress signaling by regulated splicing: IRE1/HAC1/XBP1. Methods 2005, 35:395-416. 10.1016/j.ymeth.2005.03.001.
19. Fu D, Yu JY, Wu M, Du M, Chen Y, Abdelsamie SA, Li Y, Chen J, Boulton ME, Ma JX, Lopes-Virella MF, Virella G, Lyons TJ: Immune complex formation in human diabetic retina enhances toxicity of oxidized LDL towards retinal capillary pericytes. J Lipid Res 2014, 55:860-869. 10.1194/jlr.M045401.
20. Wu J, Kaufman RJ: From acute ER stress to physiological roles of the unfolded protein response. Cell Death Differ 2006, 13:374-384. 10.1038/sj.cdd.4401840.
21. Xu C, Bailly-Maitre B, Reed JC: Endoplasmic reticulum stress: cell life and death decisions. J Clin Invest 2005, 115:2656-2664. 10.1172/JCI26373.
22. Jakobsen CH, Storvold GL, Bremseth H, Follestad T, Sand K, Mack M, Olsen KS, Lundemo AG, Iversen JG, Krokan HE, Schonberg SA: DHA induces ER stress and growth arrest in human colon cancer cells: associations with cholesterol and calcium homeostasis. J Lipid Res 2008, 49:2089-2100. 10.1194/jlr.M700389-JLR200.
23. Urano F, Wang X, Bertolotti A, Zhang Y, Chung P, Harding HP, Ron D: Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 2000, 287:664-666. 10.1126/science.287.5453.664.
24. Yoo HH, Son J, Kim DH: Liquid chromatography-tandem mass spectrometric determination of ceramides and related lipid species in cellular extracts. J Chromatogr B Analyt Technol Biomed Life Sci 2006, 843:327-333. 10.1016/j.jchromb.2006.06.025.
25. Lépine S, Allegood JC, Park M, Dent P, Milstien S, Spiegel S: Sphingosine-1- phosphate phosphohydrolase-1 regulates ER stress-induced autophagy. Cell Death Differ 2011, 18:350-361. 10.1038/cdd.2010.104.
26. Scarlatti F, Bauvy C, Ventruti A, Sala G, Cluzeaud F, Vandewalle A, Ghidoni R, Codogno P: Ceramide- mediated macroautophagy involves inhibition of protein kinase B and up-regulation of Beclin 1. J Biol Chem 2004, 279:18384-18391. 10.1074/jbc.M313561200.
27. Goldfinger M, Laviad EL, Hadar R, Shmuel M, Dagan A, Park H, Merrill AH Jr, Ringel I, Futerman AH, Tirosh B: De novo ceramide synthesis is required for N-linked glycosylation in plasma cells. J Immunol 2009, 182:7038-7047. 10.4049/jimmunol.0802990.
28. 2+ , leading to induction of endoplasmic reticulum stress in pancreatic beta-cells. Diabetes 2005, 54:452-461. 10.2337/diabetes.54.2.452.
29. 2+ activity in human cardiac fibroblasts. J Cell Physiol 2010, 223:68-75.
30. Subramanian M, Javakumar S, Richhariva S, Hasan G: Loss of IP3 receptor function in neuropeptide secreting neurons leads to obesity in adult Drosophila. BMC Neurosci 2013, 18:157.
31. 2+ concentration of the endoplasmic reticulum is a key determinant of ceramide-induced apoptosis: significance for the molecular mechanism of Bcl-2 action. EMBO J 2001, 20:2690-2701. 10.1093/emboj/20.11.2690.
32. 2+ : a control point for apoptosis. Science 2003, 300:135-139. 10.1126/science.1081208.
33. Wei H, Kim SJ, Zhang Z, Tsai PC, Wisniewski KE, Mukherjee AB: ER and oxidative stresses are common mediators of apoptosis in both neurodegenerative and non- neurodegenerative lysosomal storage disorders and are alleviated by chemical chaperones. Hum Mol Genet 2008, 17:469-477.
34. Ozcan U, Yilmaz E, Ozcan L, Furuhashi M, Vaillancourt E, Smith RO, Görgün CZ, Hotamisligil GS: Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 2006, 313:1137-1140. 10.1126/science.1128294.
35. Ben Mosban I, Alfany-Fernández I, Martel C, Zaouali MA, Bintanel-Morcillo M, Rimola A, Rodés J, Brenner C, Roselló-Catafau J, Peralta C: Endoplasmic reticulum stress inhibition protects steatotic and non-steatotic livers in partial hepatectomy under ischemia- reperfusion. Cell Death Dis 2010, 1:e52. 10.1038/cddis.2010.29.
36. Ozcan L, Ergin AS, Lu A, Chung J, Sarkar S, Nie D, Myers MG Jr, Ozcan U: Endoplasmic reticulum stress plays a central role in development of leptin resistance. Cell Metab 2009, 9:35-51. 10.1016/j.cmet.2008.12.004.
37. Basseri S, Lhoták S, Sharma AM, Austin RC: The chemical chaperone 4-phenylbutyrate inhibits adipogenesis by modulating the unfolded protein response. J Lipid Res 2009, 50:2486-2501. 10.1194/jlr.M900216-JLR200.
38. Xie Q, Khaoustov VI, Chung CC, Sohn J, Krishnan B, Lewis DE, Yoffe B: Effect of tauroursodeoxycholic acid on endoplasmic reticulum stress-induced caspase-12 activation. Hepatology 2002, 36:592-601. 10.1053/jhep.2002.35441.
39. Masuda M, Ting TC, Levi M, Saunders SJ, Miyazaki-Anzai S, Miyazaki M: Activating transcription factor 4 regulates stearate-induced vascular calcification. J Lipid Res 2012, 53:1543-1552. 10.1194/jlr.M025981.
40. Orrenius S, Zhivotovsky B, Nicotera P: Regulation of cell death: the calcium-apoptosis link. Nat Rev Mol Cell Biol 2003, 4:552-565. 10.1038/nrm1150.
41. Rutkowski DT, Kaufman RJ: A trip to the ER: coping with stress. Trends Cell Biol 2004, 14:20-28. 10.1016/j.tcb.2003.11.001.