Endoplasmic reticulum calcium release potentiates the ER stress and cell death caused by an oxidative stress in MCF-7 cells

Biochemical Pharmacology

Volumn 79, Issue 9, 2010, Pages 1221-1230

  Dejeans, Nicolas ^a   Tajeddine, Nicolas ^a   Beck, Raphaël ^a   Verrax, Julien ^a   Taper, Henryk ^a   Gailly, Philippe ^a   Calderon, Pedro Buc ^a,b  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b UNIVERSIDAD ARTURO PRAT   (Chile)

Author keywords

Ascorbate driven menadione redox cycling; Breast cancer; Calcium homeostasis; Endoplasmic reticulum stress; MCF 7 cells; Oxidative stress

Indexed keywords

ASCORBIC ACID; CALCIUM ION; CHAPERONE; GENE PRODUCT; GLUCOSE REGULATED PROTEIN 94; HISTONE H2AX; MENADIONE; PROPIDIUM IODIDE; PROTEIN ELF2; THAPSIGARGIN; UNCLASSIFIED DRUG;

ARTICLE; CALCIUM CELL LEVEL; CALCIUM MOBILIZATION; CALCIUM TRANSPORT; CELL DEATH; CELL STRAIN MCF 7; CHELATION; CONTROLLED STUDY; CYTOTOXICITY; DNA FRAGMENTATION; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION; HUMAN; HUMAN CELL; MEMBRANE DAMAGE; MICROFLUOROMETRY; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

ASCORBIC ACID; CALCIUM; CALCIUM SIGNALING; CELL DEATH; CELL LINE, TUMOR; EGTAZIC ACID; ENDOPLASMIC RETICULUM; HUMANS; OXIDATIVE STRESS; VITAMIN K 3;

EID: 77649192183     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2009.12.009     Document Type: Article

References (59)

1. Orrenius S., Zhivotovsky B., and Nicotera P. Regulation of cell death: the calcium-apoptosis link. Nat Rev Mol Cell Biol 4 (2003) 552-565
2. 2+ and cell death. Ann N Y Acad Sci 648 (1992) 17-27
3. Berridge M.J., Bootman M.D., and Lipp P. Calcium-a life and death signal. Nature 395 (1998) 645-648
4. Trump B.F., and Berezesky I.K. Calcium-mediated cell injury and cell death. FASEB J 9 (1995) 219-228
5. Ermak G., and Davies K.J. Calcium and oxidative stress: from cell signaling to cell death. Mol Immunol 38 (2002) 713-721
6. Zhang K., and Kaufman R.J. Protein folding in the endoplasmic reticulum and the unfolded protein response. Handb Exp Pharmacol (2006) 69-91
7. Schroder M., and Kaufman R.J. The mammalian unfolded protein response. Annu Rev Biochem 74 (2005) 739-789
8. Ni M., and Lee A.S. ER chaperones in mammalian development and human diseases. FEBS Lett 581 (2007) 3641-3651
9. Dong D., Ko B., Baumeister P., Swenson S., Costa F., Markland F., et al. Vascular targeting and antiangiogenesis agents induce drug resistance effector GRP78 within the tumor microenvironment. Cancer Res 65 (2005) 5785-5791
10. Pyrko P., Schonthal A.H., Hofman F.M., Chen T.C., and Lee A.S. The unfolded protein response regulator GRP78/BiP as a novel target for increasing chemosensitivity in malignant gliomas. Cancer Res 67 (2007) 9809-9816
11. Malhotra J.D., and Kaufman R.J. Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword?. Antioxid Redox Signal 9 (2007) 2277-2293
12. Tagliarino C., Pink J.J., Dubyak G.R., Nieminen A.L., and Boothman D.A. Calcium is a key signaling molecule in beta-lapachone-mediated cell death. J Biol Chem 276 (2001) 19150-19159
13. Doan T.N., Gentry D.L., Taylor A.A., and Elliott S.J. Hydrogen peroxide activates agonist-sensitive Ca(2+)-flux pathways in canine venous endothelial cells. Biochem J 297 Pt 1 (1994) 209-215
14. 2+-ATPase. Am J Physiol Cell Physiol 293 (2007) C938-C950
15. 2+-ATPase of cardiac sarcoplasmic reticulum. Mol Cell Biochem 248 (2003) 41-47
16. 2+-ATPase AT submicromolar iron concentrations: evidence for metal-catalyzed oxidation. Free Radic Biol Med 25 (1998) 554-560
17. van der Vlies D., Makkinje M., Jansens A., Braakman I., Verkleij A.J., Wirtz K.W., et al. Oxidation of ER resident proteins upon oxidative stress: effects of altering cellular redox/antioxidant status and implications for protein maturation. Antioxid Redox Signal 5 (2003) 381-387
18. Merksamer P.I., Trusina A., and Papa F.R. Real-time redox measurements during endoplasmic reticulum stress reveal interlinked protein folding functions. Cell 135 (2008) 933-947
19. Yokouchi M., Hiramatsu N., Hayakawa K., Okamura M., Du S., Kasai A., et al. Involvement of selective reactive oxygen species upstream of proapoptotic branches of unfolded protein response. J Biol Chem 283 (2008) 4252-4260
20. Min S.K., Lee S.K., Park J.S., Lee J., Paeng J.Y., Lee S.I., et al. Endoplasmic reticulum stress is involved in hydrogen peroxide induced apoptosis in immortalized and malignant human oral keratinocytes. J Oral Pathol Med 37 (2008) 490-498
21. Harding H.P., Zhang Y., Zeng H., Novoa I., Lu P.D., Calfon M., et al. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol Cell 11 (2003) 619-633
22. Baker K.M., Chakravarthi S., Langton K.P., Sheppard A.M., Lu H., and Bulleid N.J. Low reduction potential of Ero1alpha regulatory disulphides ensures tight control of substrate oxidation. EMBO J 27 (2008) 2988-2997
23. Gorlach A., Klappa P., and Kietzmann T. The endoplasmic reticulum: folding, calcium homeostasis, signaling, and redox control. Antioxid Redox Signal 8 (2006) 1391-1418
24. Yokouchi M., Hiramatsu N., Hayakawa K., Kasai A., Takano Y., Yao J., et al. Atypical, bidirectional regulation of cadmium-induced apoptosis via distinct signaling of unfolded protein response. Cell Death Differ 14 (2007) 1467-1474
25. Sanson M., Auge N., Vindis C., Muller C., Bando Y., Thiers J.C., et al. Oxidized low-density lipoproteins trigger endoplasmic reticulum stress in vascular cells: prevention by oxygen-regulated protein 150 expression. Circ Res 104 (2009) 328-336
26. Hung C.C., Ichimura T., Stevens J.L., and Bonventre J.V. Protection of renal epithelial cells against oxidative injury by endoplasmic reticulum stress preconditioning is mediated by ERK1/2 activation. J Biol Chem 278 (2003) 29317-29326
27. Kadara H., Lacroix L., Lotan D., and Lotan R. Induction of endoplasmic reticulum stress by the pro-apoptotic retinoid N-(4-hydroxyphenyl)retinamide via a reactive oxygen species-dependent mechanism in human head and neck cancer cells. Cancer Biol Ther 6 (2007) 705-711
28. Wu H.L., Li Y.H., Lin Y.H., Wang R., Li Y.B., Tie L., et al. Salvianolic acid B protects human endothelial cells from oxidative stress damage: a possible protective role of glucose-regulated protein 78 induction. Cardiovasc Res 81 (2009) 148-158
29. Calderon P.B., Cadrobbi J., Marques C., Hong-Ngoc N., Jamison J.M., Gilloteaux J., et al. Potential therapeutic application of the association of vitamins C and K3 in cancer treatment. Curr Med Chem 9 (2002) 2271-2285
30. Taper H.S., de Gerlache J., Lans M., and Roberfroid M. Non-toxic potentiation of cancer chemotherapy by combined C and K3 vitamin pre-treatment. Int J Cancer 40 (1987) 575-579
31. Verrax J., Vanbever S., Stockis J., Taper H., and Calderon P.B. Role of glycolysis inhibition and poly(ADP-ribose) polymerase activation in necrotic-like cell death caused by ascorbate/menadione-induced oxidative stress in K562 human chronic myelogenous leukemic cells. Int J Cancer 120 (2007) 1192-1197
32. Verrax J., Stockis J., Tison A., Taper H.S., and Calderon P.B. Oxidative stress by ascorbate/menadione association kills K562 human chronic myelogenous leukaemia cells and inhibits its tumour growth in nude mice. Biochem Pharmacol 72 (2006) 671-680
33. Verrax J., Cadrobbi J., Marques C., Taper H., Habraken Y., Piette J., et al. Ascorbate potentiates the cytotoxicity of menadione leading to an oxidative stress that kills cancer cells by a non-apoptotic caspase-3 independent form of cell death. Apoptosis 9 (2004) 223-233
34. Verrax J., and Calderon P.B. The controversial place of vitamin C in cancer treatment. Biochem Pharmacol 76 (2008) 1644-1652
35. Verrax J., Delvaux M., Beghein N., Taper H., Gallez B., and Buc Calderon P. Enhancement of quinone redox cycling by ascorbate induces a caspase-3 independent cell death in human leukaemia cells. An in vitro comparative study. Free Radic Res 39 (2005) 649-657
36. Beck R., Verrax J., Dejeans N., Taper H., and Calderon P.B. Menadione reduction by pharmacological doses of ascorbate induces an oxidative stress that kills breast cancer cells. Int J Toxicol 28 (2009) 33-42
37. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65 (1983) 55-63
38. Pigozzi D., Ducret T., Tajeddine N., Gala J.L., Tombal B., and Gailly P. Calcium store contents control the expression of TRPC1. TRPC3 and TRPV6 proteins in LNCaP prostate cancer cell line. Cell Calcium 39 (2006) 401-415
39. 2+ analyzed with an improved genetically encoded fluorescent sensor. Proc Natl Acad Sci USA 101 (2004) 17404-17409
40. 2+ in a breast cancer cell line using a fluorescence microplate reader. J Biochem Biophys Methods 58 (2004) 227-237
41. Britigan B.E., Rasmussen G.T., and Cox C.D. Binding of iron and inhibition of iron-dependent oxidative cell injury by the "calcium chelator" 1,2-bis(2-aminophenoxy)ethane N,N,N′,N′-tetraacetic acid (BAPTA). Biochem Pharmacol 55 (1998) 287-295
42. Glickstein H., El R.B., Shvartsman M., and Cabantchik Z.I. Intracellular labile iron pools as direct targets of iron chelators: a fluorescence study of chelator action in living cells. Blood 106 (2005) 3242-3250
43. 2+ depletion induces endothelial cell apoptosis independently of caspase-12. Cardiovasc Res 69 (2006) 908-915
44. Wei H., Wei W., Bredesen D.E., and Perry D.C. Bcl-2 protects against apoptosis in neuronal cell line caused by thapsigargin-induced depletion of intracellular calcium stores. J Neurochem 70 (1998) 2305-2314
45. Nguyen H.N., Wang C., and Perry D.C. Depletion of intracellular calcium stores is toxic to SH-SY5Y neuronal cells. Brain Res 924 (2002) 159-166
46. Halestrap A.P. Calcium, mitochondria and reperfusion injury: a pore way to die. Biochem Soc Trans 34 (2006) 232-237
47. Lemasters J.J., Theruvath T.P., Zhong Z., and Nieminen A.L. Mitochondrial calcium and the permeability transition in cell death. Biochim Biophys Acta (2009)
48. Persoon-Rothert M., Egas-Kenniphaas J.M., van der Valk-Kokshoorn E.J., Buys J.P., and van der Laarse A. Oxidative stress-induced perturbations of calcium homeostasis and cell death in cultured myocytes: role of extracellular calcium. Mol Cell Biochem 136 (1994) 1-9
49. Kim H.J., and Kim S.G. Alterations in cellular Ca(2+) and free iron pool by sulfur amino acid deprivation: the role of ferritin light chain down-regulation in prooxidant production. Biochem Pharmacol 63 (2002) 647-657
50. Haynes C.M., Titus E.A., and Cooper A.A. Degradation of misfolded proteins prevents ER-derived oxidative stress and cell death. Mol Cell 15 (2004) 767-776
51. Malhotra J.D., Miao H., Zhang K., Wolfson A., Pennathur S., Pipe S.W., et al. Antioxidants reduce endoplasmic reticulum stress and improve protein secretion. Proc Natl Acad Sci USA 105 (2008) 18525-18530
52. Santos C.X., Tanaka L.Y., Wosniak J.J., and Laurindo F.R. Mechanisms and implications of reactive oxygen species generation during the unfolded protein response: roles of endoplasmic reticulum oxidoreductases. Mitochondrial electron transport and NADPH oxidase. Antioxid Redox Signal (2009)
53. Castro J., Bittner C.X., Humeres A., Montecinos V.P., Vera J.C., and Barros L.F. A cytosolic source of calcium unveiled by hydrogen peroxide with relevance for epithelial cell death. Cell Death Differ 11 (2004) 468-478
54. Herson P.S., Lee K., Pinnock R.D., Hughes J., and Ashford M.L. Hydrogen peroxide induces intracellular calcium overload by activation of a non-selective cation channel in an insulin-secreting cell line. J Biol Chem 274 (1999) 833-841
55. 2+-ATPase in pancreatic acinar cells: role of the mitochondria. Am J Physiol Cell Physiol 295 (2008) C1247-C1260
56. 2/ascorbate is not mediated by lipid peroxidation or thiol oxidation and leads to protein fragmentation. Mol Cell Biochem 159 (1996) 105-114
57. + in apoptosis of CHO cells. Cell Calcium 36 (2004) 421-430
58. Taper H.S., Keyeux A., and Roberfroid M. Potentiation of radiotherapy by nontoxic pretreatment with combined vitamins C and K3 in mice bearing solid transplantable tumor. Anticancer Res 16 (1996) 499-503
59. Verrax J., Pedrosa R.C., Beck R., Dejeans N., Taper H., and Calderon P.B. In situ modulation of oxidative stress: a novel and efficient strategy to kill cancer cells. Curr Med Chem 16 (2009) 1821-1830