NAD(P)H oxidase Nox-4 mediates 7-ketocholesterol-induced endoplasmic reticulum stress and apoptosis in human aortic smooth muscle cells

Molecular and Cellular Biology

Volumn 24, Issue 24, 2004, Pages 10703-10717

  Pedruzzi, Eric ^a   Guichard, Cécile ^a   Ollivier, Véronique ^a   Driss, Fathi ^b   Fay, Michèle ^a   Prunet, Céline ^e   Marie, Jean Claude ^a   Pouzet, Cécile ^c   Samadi, Mohammad ^d   Elbim, Carole ^a   O'Dowd, Yvonne ^a   Bens, Marcelle ^a   Vandewalle, Alain ^a   Gougerot Pocidalo, Marie Anne ^a   Lizard, Gérard ^e   Ogier Denis, Eric ^a  

^a INSERM   (France)

^b BICHAT HOSPITAL   (France)

^c Services de Microscopie Confocale   (France)

^d UNIVERSITÉ DE LORRAINE   (France)

^e HÔPITAL DU BOCAGE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

7 OXOCHOLESTEROL; CALCIUM ION; OXIDIZED LOW DENSITY LIPOPROTEIN; OXYSTEROL; PROTEIN IRE1; PROTEIN NOX 4; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR AP 1; UNCLASSIFIED DRUG;

AORTA MEDIA; APOPTOSIS; ARTICLE; ATHEROSCLEROSIS; CALCIUM SIGNALING; CONTROLLED STUDY; CYTOTOXICITY; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; ENZYME INHIBITION; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE;

AORTA; APOPTOSIS; CALCIUM; CCAAT-ENHANCER-BINDING PROTEINS; CELLS, CULTURED; ENDOPLASMIC RETICULUM; ENDOTHELIUM, VASCULAR; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENES, REPORTER; HEAT-SHOCK PROTEINS; HUMANS; IRON REGULATORY PROTEIN 1; JNK MITOGEN-ACTIVATED PROTEIN KINASES; KETOCHOLESTEROLS; KINETICS; LUCIFERASES; MICROSCOPY, FLUORESCENCE; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; MUSCLE, SMOOTH; NADPH OXIDASE; OXIDATIVE STRESS; PROTEIN DENATURATION; REACTIVE OXYGEN SPECIES; RNA, MESSENGER; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR CHOP; TRANSCRIPTION FACTORS;

TRIXIS;

EID: 10044220931     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.24.10703-10717.2004     Document Type: Article

References (56)

1. Andreassi, M. G., and N. Botto. 2003. DNA damage as a new emerging risk factor in atherosclerosis. Trends Cardiovasc. Med. 13:270-275.
2. 2+ oscillations, MAP kinase activation, and apoptosis in human aortic smooth muscle cells. Atherosclerosis 153:23-35.
3. 2+ channel blockers verapamil and nifedipine inhibit apoptosis induced by 25-hydroxycholesterol in human aortic smooth muscle cells. J. Lipid Res. 38:2049-2061.
4. Baeuerle, P. A., and D. Baltimore. 1996. NF-κB: ten years after. Cell 87:13-20.
5. Banfi, B., A. Maturana, S. Jaconi, S. Arnaudeau, T. Laforge, B. Sinha, E. Ligeti, N. Demaurex, and K. H. Krause. 2000. A mammalian H+ channel generated through alternative splicing of the NADPH oxidase homolog NOH-1. Science 287:138-142.
6. Bjorkhem, I., and U. Diczfalusy. 2002. Oxysterols: friends, foes, or just fellow passengers? Arterioscler. Thromb. Vasc. Biol. 22:734-742.
7. Brenner, D. A., M. O'Hara, P. Angel, M. Chojkier, and M. Karin. 1989. Prolonged activation of jun and collagenase genes by tumour necrosis factor alpha. Nature 337:661-663.
8. Brewer, J. W., J. L. Cleveland, and L. M. Hendershot. 1997. A pathway distinct from the mammalian unfolded protein response regulates expression of endoplasmic reticulum chaperones in non-stressed cells. EMBO J. 16:7207-7216.
9. Brown, A. J., and W. Jessup. 1999. Oxysterols and atherosclerosis. Atherosclerosis 142:1-28.
10. Bush, K. T., S. H. Keller, and S. K. Nigam. 2000. Genesis and reversal of the ischemic phenotype in epithelial cells. J. Clin. Investig. 106:621-626.
11. Cheng, G., Z. Cao, X. Xu, E. G. van Meir, and J. D. Lambeth. 2001. Homologs of gp91phox: cloning and tissue expression of Nox3, Nox4, and Nox5. Gene 269:131-140.
12. de Nigris, F., A. Lerman, L. J. Ignarro, S. Williams-Ignarro, V. Sica, A. H. Baker, L. O. Lerman, Y. J. Geng, and C. Napoli. 2003. Oxidation-sensitive mechanisms, vascular apoptosis, and atherosclerosis. Trends Mol. Med. 9:351-359.
13. Feng, B., P. M. Yao, Y. Li, C. M. Devlin, D. Zhang, H. P. Harding, M. Sweeney, J. X. Rong, G. Kuriakose, E. A. Fisher, A. R. Marks, D. Ron, and I. Tabas. 2003. The endoplasmic reticulum is the site of cholesterol-induced cytotoxicity in macrophages. Nat. Cell Biol. 5:781-792.
14. Geiszt, M., J. B. Kopp, P. Varnai, and T. L. Leto. 2000. Identification of renox, an NAD(P)H oxidase in kidney. Proc. Natl. Acad. Sci. USA 97:8010-8014.
15. Green, D., and G. Kroemer. 1998. The central executioners of apoptosis: caspases or mitochondria? Trends Cell Biol. 8:267-271.
16. Griendling, K. K., D. Sorescu, and M. Ushio-Fukai. 2000. NAD(P)H oxidase: role in cardiovascular biology and disease. Circ. Res. 86:494-501.
17. Guzik, T. J., N. E. West, E. Black, D. McDonald, C. Ratnatunga, R. Pillai, and K. M. Channon. 2000. Vascular superoxide production by NAD(P)H oxidase: association with endothelial dysfunction and clinical risk factors. Circ. Res. 86:E85-E90.
18. Hilenski, L. L., R. E. Clempus, M. T. Quinn, J. D. Lambeth, and K. K. Griendling. 2004. Distinct subcellular localizations of Nox1 and Nox4 in vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 24:677-683.
19. Hodis, H. N., D. W. Crawford, and A. Sevanian. 1991. Cholesterol feeding increases plasma and aortic tissue cholesterol oxide levels in parallel: further evidence for the role of cholesterol oxidation in atherosclerosis. Atherosclerosis 89:117-126.
20. Kalinina, N., A. Agrotis, E. Tararak, Y. Antropova, P. Kanellakis, O. Ilyinskaya, M. T. Quinn, V. Smirnov, and A. Bobik. 2002. Cytochrome b558-dependent NAD(P)H oxidase-phox units in smooth muscle and macrophages of atherosclerotic lesions. Arterioscler. Thromb. Vasc. Biol. 22:2037-2043.
21. Kaufman, R. J. 1999. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev. 13:1211-1233.
22. Kockx, M. M., and A. G. Herman. 2000. Apoptosis in atherosclerosis: beneficial or detrimental? Cardiovasc. Res. 45:736-746.
23. Lambeth, J. D., G. Cheng, R. S. Arnold, and W. A. Edens. 2000. Novel homologs of gp91phox. Trends Biochem. Sci. 25:459-461.
24. Lange, Y., J. Ye, M. Rigney, and T. L. Steck. 1999. Regulation of endoplasmic reticulum cholesterol by plasma membrane cholesterol. J. Lipid Res. 40:2264-2270.
25. Lassegue, B., and R. E. Clempus. 2003. Vascular NAD(P)H oxidases: specific features, expression, and regulation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 285:R277-R297.
26. phox homologues in vascular smooth muscle cells: nox1 mediates angiotensin II-induced superoxide formation and redox-sensitive signaling pathways. Circ. Res. 88:888-894.
27. Littlewood, T. D., and M. R. Bennett. 2003. Apoptotic cell death in atherosclerosis. Curr. Opin. Lipidol. 14:469-475.
28. Lizard, G., S. Gueldry, O. Sordet, S. Monier, A. Athias, C. Miguet, G. Bessede, S. Lemaire, E. Solary, and P. Gambert. 1998. Glutathione is implied in the control of 7-ketocholesterol-induced apoptosis, which is associated with radical oxygen species production. FASEB J. 12:1651-1663.
29. Lizard, G., C. Miguet, G. Bessede, S. Monier, S. Gueldry, D. Neel, and P. Gambert. 2000. Impairment with various antioxidants of the loss of mitochondrial transmembrane potential and of the cytosolic release of cytochrome c occurring during 7-ketocholesterol-induced apoptosis. Free Radic. Biol. Med. 28:743-753.
30. Lizard, G., S. Monier, C. Cordelet, L. Gesquiere, V. Deckert, S. Gueldry, L. Lagrost, and P. Gambert. 1999. Characterization and comparison of the mode of cell death, apoptosis versus necrosis, induced by 7β-hydroxycholesterol and 7-ketocholesterol in the cells of the vascular wall. Arterioscler. Thromb. Vasc. Biol. 19:1190-1200.
31. Mallat, Z., and A. Tedgui. 2000. Apoptosis in the vasculature: mechanisms and functional importance. Br. J. Pharmacol. 130:947-962.
32. Martinet, W., D. M. Schrijvers, G. R. De Meyer, J. Thielemans, M. W. Knaapen, A. G. Herman, and M. M. Kockx. 2002. Gene expression profiling of apoptosis-related genes in human atherosclerosis: upregulation of death-associated protein kinase. Arterioscler. Thromb. Vasc. Biol. 22:2023-2029.
33. McCullough, K. D., J. L. Martindale, L. O. Klotz, T. Y. Aw, and N. J. Holbrook. 2001. Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol. Cell. Biol. 21:1249-1259.
34. Miguel, C., S. Monier, A. Bettaieb, A. Athias, G. Bessede, A. Laubriet, S. Lemaire, D. Neel, P. Gambert, and G. Lizard. 2001. Ceramide generation occurring during 7β-hydroxycholesterol- and 7-ketocholesterol-induced apoptosis is caspase independent and is not required to trigger cell death. Cell Death Differ. 8:83-99.
35. Miguet-Alfonsi, C., C. Prunet, S. Monier, G. Bessede, S. Lemaire-Ewing, A. Berthier, F. Menetrier, D. Neel, P. Gambert, and G. Lizard. 2002. Analysis of oxidative processes and of myelin figures formation before and after the loss of mitochondrial transmembrane potential during 7β-hydroxycholesterol and 7-ketocholesterol-induced apoptosis: comparison with various proapoptotic chemicals. Biochem. Pharmacol. 64:527-541.
36. Mollnau, H., M. Wendt, K. Szocs, B. Lassegue, E. Schulz, M. Oelze, H. Li, M. Bodenschatz, M. August, A. L. Kleschyov, N. Tsilimingas, U. Walter, U. Forstermann, T. Meinertz, K. Griendling, and T. Munzel. 2002. Effects of angiotensin II infusion on the expression and function of NAD(P)H oxidase and components of nitric oxide/cGMP signaling. Circ. Res. 90:E58-E65.
37. Monier, S., M. Samadi, C. Prunet, M. Denance, A. Laubriet, A. Athias, A. Berthier, E. Steinmetz, G. Jurgens, A. Negre-Salvayre, G. Bessede, S. Lemaire-Ewing, D. Neel, P. Gambert, and G. Lizard. 2003. Impairment of the cytotoxic and oxidative activities of 7β-hydroxycholesterol and 7-ketocholesterol by esterification with oleate. Biochem. Biophys. Res. Commun. 303:814-824.
38. Pahl, H. L., and P. A. Baeuerle. 1997. The ER-overload response: activation of NF-κB. Trends Biochem. Sci. 22:63-67.
39. Panini, S. R., and M. S. Sinensky. 2001. Mechanisms of oxysterol-induced apoptosis. Curr. Opin. Lipidol. 12:529-533.
40. Paschen, W. 2001. Dependence of vital cell function on endoplasmic reticulum calcium levels: implications for the mechanisms underlying neuronal cell injury in different pathological states. Cell Calcium 29:1-11.
41. Rong, J. X., L. Shen, Y. H. Chang, A. Richters, H. N. Hodis, and A. Sevanian. 1999. Cholesterol oxidation products induce vascular foam cell lesion formation in hypercholesterolemic New Zealand White rabbits. Arterioscler. Thromb. Vasc. Biol. 19:2179-2188.
42. Rusinol, A. E., L. Yang, D. Thewke, S. R. Panini, M. F. Kramer, and M. S. Sinensky. 2000. Isolation of a somatic cell mutant resistant to the induction of apoptosis by oxidized low-density lipoprotein. J. Biol. Chem. 275:7296-7303.
43. Rusinol, A. R., D. Thewke, J. Liu, N. Freeman, S. R. Panini, and M. S. Sinensky. 2004. Akt/PKB regulation of Bcl family members during oxysterol induced apoptosis. J. Biol. Chem. 279:1392-1399.
44. Shi, Y., R. Niculescu, D. Wang, S. Patel, K. L. Davenpeck, and A. Zalewski. 2001. Increased NAD(P)H oxidase and reactive oxygen species in coronary arteries after balloon injury. Arterioscler. Thromb. Vasc. Biol. 21:739-745.
45. Sorescu, D., D. Weiss, B. Lassegue, R. E. Clempus, K. Szocs, G. P. Sorescu, L. Valppu, M. T. Quinn, J. D. Lambeth, J. D. Vega, W. R. Taylor, and K. K. Griendling. 2002. Superoxide production and expression of nox family proteins in human atherosclerosis. Circulation 105:1429-1435.
46. Suh, Y. A., R. S. Arnold, B. Lassegue, J. Shi, X. Xu, D. Sorescu, A. B. Chung, K. K. Griendling, and J. D. Lambeth. 1999. Cell transformation by the superoxide-generating oxidase Mox1. Nature 401:79-82.
47. Szocs, K., B. Lassegue, D. Sorescu, L. L. Hilenski, L. Valppu, T. L. Couse, J. N. Wilcox, M. T. Quinn, J. D. Lambeth, and K. K. Griendling. 2002. Upregulation of Nox-based NAD(P)H oxidases in restenosis after carotid injury. Arterioscler. Thromb. Vasc. Biol. 22:21-27.
48. Tabas, I. 2002. Consequences of cellular cholesterol accumulation: basic concepts and physiological implications. J. Clin. Investig. 110:905-911.
49. Tobiume, K., A. Matsuzawa, T. Takahashi, H. Nishitoh, K. Morita, K. Takeda, O. Minowa, K. Miyazono, T. Noda, and H. Ichijo. 2001. ASK1 is required for sustained activations of JNK/p38 MAP kinases and apoptosis. EMBO Rep. 2:222-228.
50. Treiman, M. 2002. Regulation of the endoplasmic reticulum calcium storage during the unfolded protein response-significance in tissue ischemia? Trends Cardiovasc. Med. 12:57-62.
51. Urano, F., X. Wang, A. Bertolotti, Y. Zhang, P. Chung, H. P. Harding, and D. Ron. 2000. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287:664-666.
52. Wei, M. C., W. X. Zong, E. H. Cheng, T. Lindsten, V. Panoutsakopoulou, A. J. Ross, K. A. Roth, G. R. MacGregor, C. B. Thompson, and S. J. Korsmeyer. 2001. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292:727-730.
53. Wingler, K., S. Wunsch, R. Kreutz, L. Rothermund, M. Paul, and H. H. Schmidt. 2001. Upregulation of the vascular NAD(P)H-oxidase isoforms Nox1 and Nox4 by the renin-angiotensin system in vitro and in vivo. Free Radic. Biol. Med. 31:1456-1464.
54. Zhang, Y., C. Yu, J. Liu, T. A. Spencer, C. C. Chang, and T. Y. Chang. 2003. Cholesterol is superior to 7-ketocholesterol or 7α- hydroxycholesterol as an allosteric activator for acyl-coenzyme A:cholesterol acyltransferase 1. J. Biol. Chem. 278:11642-11647.
55. Zhou, Q., E. Wasowicz, B. Handler, L. Fleischer, and F. A. Kummerow. 2000. An excess concentration of oxysterols in the plasma is cytotoxic to cultured endothelial cells. Atherosclerosis 149:191-197.
56. Zinszner, H., M. Kuroda, X. Wang, N. Batchvarova, R. T. Lightfoot, H. Remotti, J. L. Stevens, and D. Ron. 1998. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev. 12:982-995.