Induced expression of manganese superoxide dismutase by non-toxic concentrations of oxidized low-density lipoprotein (oxLDL) protects against oxLDL-mediated cytotoxicity

Biochemical Journal

Volumn 374, Issue 2, 2003, Pages 505-511

  Shatrov, Vladimir A ^a   Brüne, Bernhard ^a  

^a University of Koblenz Landau   (Germany)

Author keywords

Apoptosis; Lipoprotein; Macrophage; Manganese superoxide dismutase (MnSOD); p53; Reactive oxygen species (ROS)

Indexed keywords

ATTENUATION; CELLS; MANGANESE COMPOUNDS; OXYGEN;

APOPTOSIS;

PROTEINS;

ALLOPURINOL; ANTISENSE OLIGONUCLEOTIDE; CYTOCHROME P450; DIPHENYLIODONIUM SALT; ENZYME INHIBITOR; MANGANESE SUPEROXIDE DISMUTASE; METHOXSALEN; OXIDIZED LOW DENSITY LIPOPROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; XANTHINE OXIDASE;

APOPTOSIS; ARTICLE; ATTENUATION; CELL PROTECTION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVITY; ENZYME INDUCTION; ENZYME INHIBITION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MACROPHAGE; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION;

APOPTOSIS; CELL LINE; CELL SURVIVAL; DNA FRAGMENTATION; ENZYME INDUCTION; HUMANS; LIPOPROTEINS, LDL; MACROPHAGES; MANGANESE; OLIGONUCLEOTIDES, ANTISENSE; OXIDATION-REDUCTION; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE; TUMOR SUPPRESSOR PROTEIN P53; UP-REGULATION;

EID: 0042261997     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20030420     Document Type: Article

References (45)

1. Ross, R. (1999) Atherosclerosis is an inflammatory disease. Am. Heart J. 138, 419-420
2. Lusis, A. J. (2000) Atherosclerosis. Nature (London) 407, 233-241
3. Hegyi, L., Hardwick, S. J., Siow, R. C. and Skepper, J. N. (2001) Macrophage death and the role of apoptosis in human atherosclerosis. J. Hematother. Stem. Cell Res. 10, 27-42
4. Lessner, S. M., Prado, H. L., Waller, E. K. and Galis, Z. S. (2002) Atherosclerotic lesions grow through recruitment and proliferation of circulating monocytes in a murine model. Am. J. Pathol. 160, 2145-2155
5. Hajjar, D. P. and Haberland, M. E. (1997) Lipoprotein trafficking in vascular cells: molecular Trojan horses and cellular saboteurs. J. Biol. Chem. 272, 22975-22978
6. Heinecke, J. W. (1998) Oxidants and antioxidants in the pathogenesis of atherosclerosis: implications for the oxidized low density lipoprotein hypothesis. Atherosclerosis 141, 1-15
7. Kockx, M. M. and Knaapen, M. W. (2000) The role of apoptosis in vascular disease. J. Pathol. 190, 267-280
8. Haberland, M. E., Fong, D. and Cheng, L. (1988) Malondialdehyde-altered protein occurs in atheroma of Watanabe heritable hyperlipidemic rabbits. Science 241, 215-218
9. Steinberg, D. (1999) At last, direct evidence that lipoxygenases play a role in atherogenesis. J. Clin. Invest. 103, 1487-1488
10. Martinet, W. and Kockx, M. M. (2001) Apoptosis in atherosclerosis: focus on oxidized lipids and inflammation. Curr. Opin. Lipidol. 12, 535-541
11. Marchant, C. E., Law, N. S., van der Veen, C., Hardwick, S. J., Carpenter, K. L. H. and Mitchinson, M. J. (1995) Oxidized low-density lipoprotein is cytotoxic to human monocyte-macrophages: protection with lipophilic antioxidants. FEBS Lett. 358, 175-178
12. Fischer, B., von Knethen, A. and Brüne, B. (2002) Dualism of oxidized lipoproteins in provoking and attenuating the oxidative burst in macrophages: role of peroxisome proliferator-activated receptor-γ. J. Immunol. 168, 2828-2834
13. Sen, C. K. and Packer, L. (1996) Antioxidant and redox regulation of gene transcription. FASEB J. 10, 709-720
14. Irani, K. (2000) Oxidant signaling in vascular cell growth, death, and survival: a review of the roles of reactive oxygen species in smooth muscle and endothelial cell mitogenic and apoptotic signaling. Circ. Res. 87, 179-183
15. Robinson, B. H. (1998) The role of manganese superoxide dismutase in health and disease. J. Inherit. Metab. Dis. 21, 598-603
16. Wong, G. H. and Goeddel, D. V. (1988) Induction of manganous superoxide dismutase by tumor necrosis factor: possible protective mechanism. Science 242, 941-944
17. Wong, G. H., Elwell, J. H., Oberley, L. W. and Goeddel, D. V. (1989) Manganous superoxide dismutase is essential for cellular resistance to cytotoxicity of tumor necrosis factor. Cell 58, 923-931
18. Visner, G. A., Dougall, W. C., Wilson, J. M., Burr, I. A. and Nick, H. S. (1990) Regulation of manganese superoxide dismutase by lipopolysaccharide, interleukin-1, and tumor necrosis factor: role in the acute inflammatory response. J. Biol. Chem. 265, 2856-2864
19. Dougall, W. C. and Nick, H. S. (1991) Manganese superoxide dismutase: a hepatic acute phase protein regulated by interleukin-6 and glucocorticoids. Endocrinol. 129, 2376-2384
20. Warner, B. B., Stuart, L., Gebb, S. and Wispe, J. R. (1996) Redox regulation of manganese superoxide dismutase. Am. J. Physiol. 271, 150-158
21. Kinscherf, R., Deigner, H. P., Usinger, C., Pill, J., Wagner, M., Kamencic, H., Hou, D., Chen., M., Schmiedt, W., Schrader, M. et al. (1997) Induction of mitochondrial manganese superoxide dismutase in macrophages by oxidized LDL: its relevance in atherosclerosis of humans and heritable hyperlipidemic rabbits. FASEB J. 11, 1317-1328
22. Lowry, O. H., Rosebrough, N. J., Farr, A. L. and Randall, R. J. (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-275
23. Pirillo, A., Norata, G. D., Zanelli, T. and Catapano, A. L. (2001) Overexpression of inducible heat shock protein 70 in Cos-1 cells fails to protect from cytotoxicity of oxidized LDLs. Arterioscler. Thromb. Vasc. Biol. 21, 348-354
24. Jeney, V., Balla, J., Yachie, A., Varga, Z., Vercellotti, G. M., Eaton, J. W. and Balla, G. (2002) Pro-oxidant and cytotoxic effects of circulating heme. Blood 100, 879-887
25. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254
26. Yamashita, N., Nishida, M., Hoshida, S., Igarashi, J., Hori, M., Kuzuya, T. and Tada, M. (1996) α1-Adrenergic stimulation induces cardiac tolerance to hypoxia via induction and activation of Mn-SOD. Am. J. Physiol. 271, 1356-1362
27. Steinberg, D., Parthasarathy, S., Carew, T. E., Khoo, J. C. and Witztum, J. L. (1989) Beyond cholesterol: modifications of low-density lipoprotein that increase its atherogenicity. N. Engl. J. Med. 320, 915-924
28. Kockx, M. M. and Herman, A. G. (2000) Apoptosis in atherosclerosis: beneficial or detrimental? Cardiovasc. Res. 45, 736-746
29. Jovinge, S., Crisby, M., Thyberg, J. and Nilsson, J. (1997) DNA fragmentation and ultrastructural changes of degenerating cells in atherosclerotic lesions and smooth muscle cells exposed to oxidized LDL in vitro. Arterioscler. Thromb. Vasc. Biol. 17, 2225-2231
30. Mitchinson, M. J., Hardwick, S. J. and Bennett, M. R. (1996) Cell death in atherosclerotic plaques. Curr. Opin. Lipidol. 7, 324-329
31. Hardwick, S. J., Hegyi, L., Clare, K., Law, N. S., Carpenter, K. L., Mitchinson, M. J. and Skepper, J. N. (1996) Apoptosis in human monocyte-macrophages exposed to oxidized low density lipoprotein. J. Pathol. 179, 294-302
32. Heermeier, K., Leicht, W., Palmetshofer, A., Ullrich, M., Wanner, C. and Galle, J. (2001) Oxidized LDL suppresses NF-κB and overcomes protection from apoptosis in activated endothelial cells. J. Am. Soc. Nephrol. 12, 456-463
33. Cho, S., Hazama, M., Urata, Y., Goto, S., Horiuchi, S., Sumikawa, K. and Kondo, T. (1999) Protective role of glutathione synthesis in response to oxidized low density lipoprotein in human vascular endothelial cells. Free Radicals Biol. Med. 26, 589-602
34. Moellering, D. R., Levonen, A.-L., Go, Y.-M., Patel, R. P., Dickinson, D. A., Forman, H. J. and Darley-Usmar, V. M. (2002) Induction of glutathione synthesis by oxidized low-density lipoprotein and 1-palmitoyl-2-arachidonyl phosphatidylcholine: protection against quinone-mediated oxidative stress. Biochem. J. 362, 51-59
35. Bea, F., Hudson, F. N., Chait, A., Kavanagh, T. J. and Rosenfeld, M. E. (2003) Induction of glutathione synthesis in macrophages by oxidized low-density lipoproteins is mediated by consensus antioxidant response elements. Circ. Res. 92, 386-393
36. Stuehr, D. J., Fasehun, O. A., Kwon, N. S., Gross, S. S., Gonzalez, J. A., Levi, R. and Nathan, C. F. (1991) Inhibition of macrophage and endothelial cell nitric oxide synthase by diphenyleneiodonium and its analogs. FASEB J. 5, 98-103
37. Chandel, N. S., Maltepe, E., Goldwasser, E., Mathieu, C. E., Simon, M. C. and Schumacker, P. T. (1998) Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc. Natl. Acad. Sci. U.S.A. 95, 11715-11720
38. Lohrum, M. A. and Vousden, K. H. (2000) Regulation and function of the p53-related proteins: same family, different rules. Trends Cell Biol. 10, 197-202
39. Sheikh, M. S. and Fornace, A. J. (2000) Role of p53 family members in apoptosis. J. Cell. Physiol. 182, 171-181
40. Ihling, C., Menzel, G., Wellens, E., Monting, J. S., Schaefer, H. E. and Zeiher, A. M. (1997) Topographical association between the cyclin-dependent kinases inhibitor P21, p53 accumulation, and cellular proliferation in human atherosclerotic tissue. Arterioscler. Thromb. Vasc. Biol. 17, 2218-2224
41. Ihling, C., Haendeler, J., Menzel, G., Hess, R. D., Fraedrich, G., Schaefer, H. E. and Zeiher, A. M. (1998) Co-expression of p53 and MDM2 in human atherosclerosis: implications for the regulation of cellularity of atherosclerotic lesions. J. Pathol. 185, 303-312
42. Guevara, N. V., Kim, H. S., Antonova, E. I. and Chan, L. (1999) The absence of p53 accelerates atherosclerosis by increasing cell proliferation in vivo. Nat. Med. 5, 335-339
43. van Vlijmen, B. J. M., Gerritsen, G., Franken, A. L., Boesten, L. S. M., Kockx, M. M., Gijbels, M. J., Vierboom, M. P., van Eck, M., van de Water, B., van Berkel, T. J. C. and Havekes, L. M. (2001) Macrophage p53 deficiency leads to enhanced atherosclerosis in APOE*3-Leiden transgenic mice. Circ. Res. 88, 780-786
44. Heinloth, A., Brüne, B., Fischer, B. and Galle, J. (2002) Nitric oxide prevents oxidised LDL-induced p53 accumulation, cytochrome c translocation, and apoptosis in macrophages via guanylate cyclase stimulation. Atherosclerosis 162, 93-101
45. Maziere, C., Meignotte, A., Dantin, F., Conte, M. A. and Maziere, J. C. (2000) Oxidized LDL induces an oxidative stress and activates the tumor suppressor p53 in MRC5 human fibroblasts. Biochem. Biophys. Res. Commun. 276, 718-723