Cholesterol secoaldehyde induces apoptosis in H9c2 cardiomyoblasts through reactive oxygen species involving mitochondrial and death receptor pathways

Free Radical Biology and Medicine

Volumn 47, Issue 5, 2009, Pages 548-558

  Sathishkumar, K ^a   Gao, Xueli ^a   Raghavamenon, Achuthan C ^a   Parinandi, Narasimham ^b   Pryor, William A ^c   Uppu, Rao M ^a  

^a SOUTHERN UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c LOUISIANA STATE UNIVERSITY   (United States)

Author keywords

Antioxidants; Apoptosis; Cholesterol secoaldehyde; Death receptor pathways; Free radicals; H9c2 cardiomyoblasts; Mitochondrial pathways; Oxysterols; Redox signaling

Indexed keywords

ACETYLCYSTEINE; APOPTOTIC PROTEASE ACTIVATING FACTOR 1; CASPASE 8; CASPASE 9; CHOLESTEROL DERIVATIVE; CHOLESTEROL SECOALDEHYDE; CYTOCHROME C; DEATH RECEPTOR; GLUTATHIONE; REACTIVE OXYGEN METABOLITE; TROLOX C; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DOWN REGULATION; ENZYME ACTIVITY; ENZYME RELEASE; GENE ACTIVATION; GENE OVEREXPRESSION; HEART MITOCHONDRION; HEART MUSCLE CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION;

ALDEHYDES; APOPTOSIS; CASPASES; CELL LINE; CHOLESTANONES; CHOLESTEROL; CYTOCHROMES C; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG EVALUATION, PRECLINICAL; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA, HEART; MODELS, BIOLOGICAL; MYOCYTES, CARDIAC; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; RECEPTORS, DEATH DOMAIN; SECOSTEROIDS; SIGNAL TRANSDUCTION;

EID: 67650738529     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2009.05.020     Document Type: Article

References (65)

1. Bjorkhem I., Heverin M., Leoni V., Meaney S., and Diczfalusy U. Oxysterols and Alzheimer's disease. Acta Neurol. Scand. Suppl. 185 (2006) 43-49
2. Olkkonen V.M., and Lehto M. Oxysterols and oxysterol binding proteins: role in lipid metabolism and atherosclerosis. Ann. Med. 36 (2004) 562-572
3. Schroepfer G.J. Jr. Oxysterols: modulators of cholesterol metabolism and other processes. Physiol. Rev. 80 (2000) 361-554
4. Smith L.L. Review of progress in sterol oxidations: 1987-1995. Lipids 31 (1996) 453-487
5. van Reyk D.M., Brown A.J., Hult'en L.M., Dean R.T., and Jessup W. Oxysterols in biological systems: sources, metabolism and pathophysiological relevance. Redox Rep. 11 (2006) 255-262
6. Wentworth Jr. P., Nieva J., Takeuchi C., Galve R., Wentworth A.D., Dilley R.B., DeLaria G.A., Saven A., Babior B.M., Janda K.D., Eschenmoser A., and Lerner R.A. Evidence for ozone formation in human atherosclerotic arteries. Science 302 (2003) 1053-1056
7. Pryor W.A., Houk K.N., Foote C.S., Fukuto J.M., Ignarro L.J., Squadrito G.L., and Davies K.A.J. Free radical biology and medicine: it's a gas, man!. Free Radic. Biol. Med. 291 (2006) 491-511
8. Smith L.L. Oxygen, oxysterols, ouabain, and ozone: a cautionary tale. Free Radic. Biol. Med. 37 (2004) 318-324
9. Wang K., Bermudez E., and Pryor W.A. The ozonation of cholesterol: separation and identification of 2,4-dinitrophenylhydrazine derivatization products of 3 beta-hydroxy-5-oxo-5,6-secocholestan-6-al. Steroids 58 (1993) 225-229
10. Pulfer M.K., and Murphy R.C. Formation of biologically active oxysterols during ozonolysis of cholesterol present in lung surfactant. J. Biol. Chem. 279 (2004) 26331-26338
11. Pryor W.A., Wang K., and Bermudez E. Cholesterol ozonation products as biomarkers for ozone exposure in rats. Biochem. Biophys. Res. Commun. 188 (1992) 618-623
12. Pulfer M.K., Taube C., Gelfand E., and Murphy R.C. Ozone exposure in vivo and formation of biologically active oxysterols in the lung. J. Pharmacol. Exp. Ther. 312 (2005) 256-265
13. Zhang Q., Powers E.T., Nieva J., Huff M.E., Dendle M.A., Bieschke J., Glabe C.G., Eschenmoser A., Wentworth Jr. P., Lerner R.A., and Kelly J.W. Metabolite-initiated protein misfolding may trigger Alzheimer's disease. Proc. Natl. Acad. Sci. USA 101 (2004) 4752-4757
14. Bosco D.A., Fowler D.M., Zhang Q., Nieva J., Powers E.T., Wentworth Jr. P., Lerner R.A., and Kelly J.W. Elevated levels of oxidized cholesterol metabolites in Lewy body disease brains accelerate alpha-synuclein fibrilization. Nat. Chem. Biol. 2 (2006) 249-253
15. Brinkhorst J., Nara S.J., and Pratt D.A. Hoch cleavage of cholesterol 5α-hydroperoxide: an ozone-free pathway to the cholesterol ozonolysis products identified in arterial plaque and brain tissue. J. Am. Chem. Soc. 130 (2008) 12224-12225
16. Bieschke J., Zhang Q., Bosco D.A., Lerner R.A., Powers E.T., Wentworth Jr. P., and Kelly J.W. Small molecule oxidation products trigger disease-associated protein misfolding. Acc. Chem. Res. 39 (2006) 611-619
17. Sathishkumar K., Xi X., Martin R., and Uppu R.M. Cholesterol secoaldehyde, an ozonation product of cholesterol, induces amyloid aggregation and apoptosis in murine GT1-7 hypothalamic neurons. J. Alzheimer's Dis. 11 (2007) 261-274
18. Takeuchi C., Galve R., Nieva J., Witter D.P., Wentworth A.D., Troseth R.P., Lerner R.A., and Wentworth P. Jr. Proatherogenic effects of the cholesterol ozonolysis products, atheronal-A and atheronal-B. Biochemistry 45 (2006) 7162-7170
19. Sathishkumar K., Haque M., Perumal T.E., Francis J., and Uppu R.M. A major ozonation product of cholesterol, 3beta-hydroxy-5-oxo-5,6-secocholestan-6-al, induces apoptosis in H9c2 cardiomyoblasts. FEBS Lett. 579 (2005) 6444-6450
20. Sathishkumar K., and Uppu R.M. Cholesterol secoaldehyde induces apoptotic signaling through mitochondrial pathway in H9c2 cardiomyoblasts. Toxicologist 90 (2006) S1394
21. Agrawal S., Agarwal M.L., Chatterjee-Kishore M., Stark G.R., and Chisolm G.M. Stat1-dependent, p53-independent expression of p21 (waf1) modulates oxysterol-induced apoptosis. Mol. Cell. Biol. 22 (2002) 1981-1992
22. Yadavilli S., and Muganda P.M. Diepoxybutane induces caspase and p53-mediated apoptosis in human lymphoblasts. Toxicol. Appl. Pharmacol. 195 (2004) 154-165
23. Yuan J.S., Reed A., Chen F., and Stewart C.N. Jr. Statistical analysis of real-time PCR data. BMC Bioinformatics 7 (2006) 85
24. Ohtsuka M., Miyashita Y., and Shirai K. Lipids deposited in human atheromatous lesions induce apoptosis of human vascular smooth muscle cells. J. Atheroscler. Thromb. 13 (2006) 256-262
25. Prunet C., Petit J.M., Ecarnot-Laubriet A., Athias A., Miguet-Alfonsi C., Rohmer J.F., Steinmetz E., Neel D., Gambert P., and Lizard G. High circulating levels of 7beta- and 7alpha-hydroxycholesterol and presence of apoptotic and oxidative markers in arterial lesions of normocholesterolemic atherosclerotic patients undergoing endarterectomy. Pathol. Biol. (Paris) 54 (2006) 22-32
26. Matsui H., Okumura K., Mukawa H., Hibino M., Toki Y., and Ito T. Increased oxysterol contents in diabetic rat hearts: their involvement in diabetic cardiomyopathy. Can. J. Cardiol. 13 (1997) 373-379
27. Ruidavets J.B., Cournot M., Cassadou S., Giroux M., Meybeck M., and Ferrières J. Ozone air pollution is associated with acute myocardial infarction. Circulation 111 (2005) 563-569
28. Sies H. Ozone in arteriosclerotic plaques: searching for the "smoking gun". Angew. Chem. Int. Ed. 43 (2004) 3514-3515
29. Loscalzo J. Ozone-from environmental pollutant to atherogenic determinant. N. Engl. J. Med. 350 (2004) 834-835
30. Pryor W.A., Squadrito G.L., and Friedman M. The cascade mechanism to explain ozone toxicity: role of lipid ozonation products. Free Radic. Biol. Med. 19 (1995) 935-940
31. Hescheler J., Meyer R., Plant S., Krautwurst D., Rosenthal W., and Schultz G. Morphological, biochemical, and electrophysiological characterization of a clonal cell (H9c2) line from rat heart. Circ. Res. 69 (1991) 1476-1486
32. Sipido K.R., and Marban E. L-type calcium channels, potassium channels, and novel nonspecific cation channels in a clonal muscle cell line derived from embryonic rat ventricle. Circ. Res. 69 (1991) 1487-1499
33. Wu M.L., Tsai K.L., Wang S.M., Wu J.C., Wang B.S., and Lee Y.T. Mechanism of hydrogen peroxide and hydroxyl free radical-induced intracellular acidification in cultured rat cardiac myoblasts. Circ. Res. 78 (1996) 564-572
34. Kimes B.W., and Brandt B.L. Properties of a clonal muscle cell line from rat heart. Exp. Cell Res. 98 (1976) 367-381
35. Hajjar D.P., and Haberland M.E. Lipoprotein trafficking in vascular cells: molecular Trojan horses and cellular saboteurs. J. Biol. Chem. 272 (1997) 22975-22978
36. Roussi S., Gosse F., Aoude-Werner D., Zhang X., Marchioni E., Geoffroy P., Miesch M., and Raul F. Mitochondrial perturbation, oxidative stress and lysosomal destabilization are involved in 7beta-hydroxysitosterol and 7beta-hydroxycholesterol triggered apoptosis in human colon cancer cells. Apoptosis 12 (2007) 87-96
37. Pieczenik S.R., and Neustadt J. Mitochondrial dysfunction and molecular pathways of disease. Exp. Mol. Pathol. 83 (2007) 84-92
38. Gutierrez J., Ballinger S.W., Darley-Usmar V.M., and Landar A. Free radicals, mitochondria, and oxidized lipids: the emerging role in signal transduction in vascular cells. Circ. Res. 99 (2006) 924-932
39. Garrido C., Galluzzi L., Brunet M., Puig P.E., Didelot C., and Kroemer G. Mechanisms of cytochrome c release from mitochondria. Cell Death Differ. 13 (2006) 1423-1433
40. Miguet-Alfonsi C., Prunet C., Monier S., Bessede G., Lemaire-Ewing S., Berthier A., Menetrier F., Neel D., Gambert P., and Lizard G. Analysis of oxidative processes and of myelin figures formation before and after the loss of mitochondrial transmembrane potential during 7beta-hydroxycholesterol and 7-ketocholesterol-induced apoptosis: comparison with various pro-apoptotic chemicals. Biochem. Pharmacol. 64 (2002) 527-541
41. Lizard G., Miguet C., Bessede G., Monier S., Gueldry S., Neel D., and Gambert P. 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 (2000) 743-753
42. Leonarduzzi G., Biasi F., Chiarpotto E., and Poli G. Trojan horse-like behavior of a biologically representative mixture of oxysterols. Mol. Aspects Med. 25 (2004) 155-167
43. Scaffidi C., Medema J.P., Krmmer P.H., and Peter M.F. FLICE is predominantly expressed as two functionally active isoforms, caspase-8/a and caspase-8/b. J. Biol. Chem. 272 (1997) 26953-26958
44. Kuida K., Zheng T.S., Na S., Kuan C., Yang D., Karasuyama H., Rakic P., and Flavell R.A. Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature 384 (1996) 368-372
45. Sathishkumar K., Murthy S.N., and Uppu R.M. Cytotoxic effects of oxysterols produced during ozonolysis of cholesterol in murine GT1-7 hypothalamic neurons. Free Radic. Res. 41 (2007) 82-88
46. Sathishkumar, K.; Raghavamenon, A. C.; Ganeshkumar, K.; Telaprolu, R.; Uppu, R.M. Simultaneous analysis of multiple redox-sensitive and apoptotic gene expression in hypothalamic neurons exposed to cholesterol ozonation products. Methods Mol. Biol. accepted for publication.
47. Salvayre R., Auge N., Benoist H., and Negre-Salvayre A. Oxidized low-density lipoprotein-induced apoptosis. Biochim. Biophys. Acta 1585 (2002) 213-221
48. Bjorkhem I., and Diczfalusy U. Oxysterols: friends, foes, or just fellow passengers?. Arterioscler. Thromb. Vasc. Biol. 22 (2002) 734-742
49. Yamamoto K., Ichijo H., and Korsmeyer S.J. BCL-2 is phosphorylated and inactivated by an ASK1/Jun N-terminal protein kinase pathway normally activated at G(2)/M. Mol. Cell. Biol. 19 (1999) 8469-8478
50. Suhara T., Fukuo K., Sugimoto T., Morimoto S., Nakahashi T., Hata S., Shimizu M., and Ogihara T. Hydrogen peroxide induces up-regulation of Fas in human endothelial cells. J. Immunol. 160 (1998) 4042-4047
51. O'Callaghan Y.C., Woods J.A., and O'Brien N.M. Characteristics of 7b-hydroxycholesterol-induced cell death in a human monocytic blood cell line, U937, and a human hepatoma cell line, HepG2. Toxicol. in Vitro 16 (2002) 245-251
52. Lee T.S., and Chau L.Y. Fas/Fas ligand-mediated pathway is involved in oxLDL-induced apoptosis in vascular smooth muscle cells. Am. J. Physiol. Cell Physiol. 280 (2001) 709-718
53. Bansal G., Singh U., and Bansal M.P. Effect of 7b-hydroxycholesterol on cellular redox status and heat shock protein 70 expression in macrophages. Cell. Physiol. Biochem. 11 (2001) 241-246
54. Lizard G., Gueldry S., Sordet O., Monier S., Athias A., Miguet C., Bessede G., Lemaire S., Solary E., and Gambert P. Glutathione is implied in 7-ketocholesterol-induced apoptosis, which is associated with radical oxygen species production. FASEB J. 12 (1998) 1651-1663
55. Lizard G., Miguet C., Besséde G., Monier S., Gueldry S., Neel D., and Gambert P. 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 (2000) 743-756
56. McCluskey S., Hall M., Stanton C., and Devery R. Alpha-tocopherol inhibits oxidative stress induced by cholestanetriol and 25-hydroxycholesterol in porcine ovarian granulosa cells. Mol. Cell. Biochem. 194 (2001) 217-225
57. Lyons N.M., Woods J.A., and O'Brien N.M. Alpha-tocopherol, but not gamma-tocopherol inhibits 7b-hydroxycholesterol-induced apoptosis in human U937 cells. Free Radic. Res. 35 (2001) 329-339
58. Berthier A., Lemaire-Ewing S., Prunet C., Montange T., Vejux A., Pais de Barros J.P., Monier S., Gambert P., and Lizard G. Néel, D. 7-Ketocholesterol-induced apoptosis: involvement of several pro-apoptotic but also anti-apoptotic calcium-dependent transduction pathways. FEBS J. 272 (2005) 3093-30104
59. Ryter S.W., Kim H.P., Hoetzel A., Park J.W., Nakahira K., Wang X., and Choi A.M. Mechanisms of cell death in oxidative stress. Antioxid. Redox Signaling 9 (2007) 49-89
60. 2+ channel blockers verapamil and nifedipine inhibit apoptosis induced by 25-hydroxycholesterol in human aortic smooth muscle cells. J. Lipid Res. 38 (1997) 2049-2061
61. Halestrap A.P., McStay G.P., and Clarke S.J. The permeability transition pore complex: another view. Biochimie 84 (2002) 153-166
62. Berthier A., Lemaire-Ewing S., Prunet C., Monier S., Athias A., Bessede G., Pais de Barros J.P., Laubriet A., Gambert P., Lizard G., and Neel D. Involvement of a calcium-dependent dephosphorylation of BAD associated with the localization of Trpc-1 within lipid rafts in 7-ketocholesterol-induced THP-1 cell apoptosis. Cell Death Differ. 11 (2004) 897-905
63. Wachtel E., Bach D., Epand R.F., Tishbee A., and Epand R.M. A product of ozonolysis of cholesterol alters the biophysical properties of phosphatidylethanolamine membranes. Biochemistry 45 (2006) 1345-1351
64. Pignatelli M., Sanchez-Rodriguez J., Santos A., and Perez-Castillo A. 15-Deoxy-delta-12,14-prostaglandin J2 induces programmed cell death of breast cancer cells by a pleiotropic mechanism. Carcinogenesis 26 (2005) 81-92
65. Wang J., Silva J.P., Gustafsson C.M., Rustin P., and Larsson N.G. Increased in vivo apoptosis in cells lacking mitochondrial DNA gene expression. Proc. Natl. Acad. Sci. USA 98 (2001) 4038-4043