Induction of heme oxygenase 1 by moderately oxidized low-density lipoproteins in human vascular smooth muscle cells: Role of mitogen-activated protein kinases and Nrf2

Free Radical Biology and Medicine

Volumn 39, Issue 2, 2005, Pages 227-236

  Anwar, Anila A ^a   Li, Francois Y L ^a   Leake, David S ^b   Ishii, Tetsuro ^c   Mann, Giovanni E ^a   Siow, Richard C M ^a  

^a UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY OF READING   (United Kingdom)

^c UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

Atherosclerosis; Glutathione; Heme oxygenase; Mitogen activated protein kinase; Nrf2; Oxidized low density lipoproteins; Vascular smooth muscle; Vitamin C

Indexed keywords

ADENOSINE TRIPHOSPHATE; ASCORBIC ACID; GLUTATHIONE; HEME OXYGENASE; LECTIN; LOW DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR; MITOCHONDRIAL ENZYME; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; OXIDOREDUCTASE; PROTEIN KINASE C; PROTEIN KINASE C INHIBITOR; STRESS ACTIVATED PROTEIN KINASE 1; TRANSCRIPTION FACTOR NRF2;

ACETYLATION; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME BLOOD LEVEL; ENZYME INDUCTION; HUMAN; HUMAN CELL; LIPID PEROXIDATION; NORMAL HUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; VASCULAR SMOOTH MUSCLE;

ACTIVE TRANSPORT, CELL NUCLEUS; ADENOSINE TRIPHOSPHATE; ANTIOXIDANTS; ARTERIOSCLEROSIS; ASCORBIC ACID; BLOTTING, WESTERN; CELL SURVIVAL; CELLS, CULTURED; DNA-BINDING PROTEINS; ENDOTHELIUM, VASCULAR; ENZYME INHIBITORS; GLUTATHIONE; HEME OXYGENASE (DECYCLIZING); HEME OXYGENASE-1; HUMANS; HYDROGEN PEROXIDE; LECTINS; LIPID METABOLISM; LIPOPROTEINS, LDL; MAP KINASE SIGNALING SYSTEM; MEMBRANE PROTEINS; MICROSCOPY, FLUORESCENCE; MITOCHONDRIA; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MYOCYTES, SMOOTH MUSCLE; NF-E2-RELATED FACTOR 2; OXYGEN; P38 MITOGEN-ACTIVATED PROTEIN KINASES; TIME FACTORS; TRANS-ACTIVATORS;

EID: 20444456655     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2005.03.012     Document Type: Article

References (44)

1. D. Steinberg Atherogenesis in perspective: hypercholesterolemia and inflammation as partners in crime Nat. Med. 8 2002 1211 1217
2. R.C. Siow, H. Sato, and G.E. Mann Heme oxygenase-carbon monoxide signaling pathway in atherosclerosis: anti-atherogenic actions of bilirubin and carbon monoxide? Cardiovasc. Res. 41 1999 385 394
3. MD. Maines The heme oxygenase system: a regulator of second messenger gases Annu. Rev. Pharmacol. Toxicol. 37 1997 517 554
4. D.E. Baranano, M. Rao, C.D. Ferris, and S.H. Snyder Biliverdin reductase: a major physiologic cytoprotectant Proc. Natl. Acad. Sci. USA 99 2002 16093 16098
5. L.E. Otterbein, F.H. Bach, and J. Alam Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway Nat. Med. 6 2000 422 428
6. I.A. Sammut, R. Foresti, and J.E. Clark Carbon monoxide is a major contributor to the regulation of vascular tone in aortas expressing high levels of haeme oxygenase-1 Br. J. Pharmacol. 125 1998 1437 1444
7. L. Wang, T. Lee, F. Lee, R. Pai, and L. Chau Expression of heme oxygenase-1 in atherosclerotic lesions Am. J. Pathol. 152 1998 711 720
8. S.H. Juan, T.S. Lee, and K.W. Tseng Adenovirus-mediated heme oxygenase-1 gene transfer inhibits the development of atherosclerosis in apolipoprotein E-deficient mice Circulation 104 2001 1519 1525
9. L.E. Otterbein, B.S. Zuckerbraun, and M. Haga Carbon monoxide suppresses arteriosclerotic lesions associated with chronic graft rejection and with balloon injury Nat. Med. 9 2003 183 190
10. A. Kawashima, Y. Oda, A. Yachie, S. Koizumi, and I. Nakanishi Heme oxygenase-1 deficiency: the first autopsy case Hum. Pathol. 33 2002 125 130
11. J.G. Kim, W.R. Taylor, and S. Parthasarathy Demonstration of the presence of lipid peroxide-modified proteins in human atherosclerotic lesions using a novel lipid peroxide-modified anti-peptide antibody Atherosclerosis 143 1999 335 340
12. N. Hill-Kapturczak, C. Voakes, J. Garcia, G. Visner, H.S. Nick, and A. Agarwal A cis-acting region regulates oxidized lipid-mediated induction of the human heme oxygenase-1 gene in endothelial cells Arterioscler Thromb. Vasc. Biol. 23 2003 1416 1422
13. D.A. Dickinson, and H.J. Forman Glutathione in defense and signaling: lessons from a small thiol Ann. N.Y. Acad. Sci. 973 2002 488 504
14. R.C. Siow, H. Sato, D.S. Leake, J.D. Pearson, S. Bannai, and G.E. Mann Vitamin C protects human arterial smooth muscle cells against atherogenic lipoproteins: effects of antioxidant vitamins C and E on oxidized LDL-induced adaptive increases in cystine transport and glutathione Arterioscler. Thromb. Vasc. Biol. 18 1998 1662 1670
15. T. Nguyen, P.J. Sherratt, and C.B. Pickett Regulatory mechanisms controlling gene expression mediated by the antioxidant response element Annu. Rev. Pharmacol. Toxicol. 43 2003 233 260
16. T. Ishii, K. Itoh, and E. Ruiz Role of Nrf2 in the regulation of CD36 and stress protein expression in murine macrophages: activation by oxidatively modified LDL and 4-hydroxynonenal Circ. Res. 94 2004 609 616
17. R. Yu, C. Chen, and Y.Y. Mo Activation of mitogen-activated protein kinase pathways induces antioxidant response element-mediated gene expression via a Nrf2-dependent mechanism J. Biol. Chem. 275 2000 39907 39913
18. C.M. Yang, C.S. Chien, and L.D. Hsiao Mitogenic effect of oxidized low-density lipoprotein on vascular smooth muscle cells mediated by activation of Ras/Raf/MEK/MAPK pathway Br. J. Pharmacol. 132 2001 1531 1541
19. V. Velarde, A.J. Jenkins, J. Christopher, T.J. Lyons, and A.A. Jaffa Activation of MAPK by modified low-density lipoproteins in vascular smooth muscle cells J. Appl. Physiol. 91 2001 1412 1420
20. S. Cho, M. Hazama, Y. Urata, S. Goto, S. Horiuchi, K. Sumikawa, and T. Kondo Protective role of glutathione synthesis in response to oxidized low density lipoprotein in human vascular endothelial cells Free Radic. Biol. Med. 26 1999 589 602
21. T. Kietzmann, A. Samoylenko, and S. Immenschuh Transcriptional regulation of heme oxygenase-1 gene expression by MAP kinases of the JNK and p38 pathways in primary cultures of rat hepatocytes J. Biol. Chem. 278 2003 17927 17936
22. X. Zhang, E.L. Bedard, and R. Potter Mitogen-activated protein kinases regulate HO-1 gene transcription after ischemia-reperfusion lung injury Am. J. Physiol. 283 2002 L815 L829
23. R.C. Siow, J.P. Richards, K.C. Pedley, D.S. Leake, and G.E. Mann Vitamin C protects human vascular smooth muscle cells against apoptosis induced by moderately oxidized LDL containing high levels of lipid hydroperoxides Arterioscler. Thromb. Vasc. Biol. 19 1999 2387 2394
24. A.C. Carr, B.Z. Zhu, and B. Frei Potential antiatherogenic mechanisms of ascorbate (vitamin C) and alpha-tocopherol (vitamin E) Circ. Res. 87 2000 349 354
25. J.A. Vita, J.F. Keaney Jr., and K.E. Raby Low plasma ascorbic acid independently predicts the presence of an unstable coronary syndrome J. Am. Coll. Cardiol. 31 1998 980 986
26. M.W. Chien, C.S. Chien, L.D. Hsiao, C.H. Lin, and C.M. Yang OxLDL induces mitogen-activated protein kinase activation mediated via PI3-kinase/Akt in vascular smooth muscle cells J. Lipid. Res. 44 2003 1667 1675
27. R. Natarajan, M.A. Reddy, K.U. Malik, S. Fatima, and B.V. Khan Signaling mechanisms of nuclear factor-κB-mediated activation of inflammatory genes by 13-hydroperoxyoctadecadienoic acid in cultured vascular smooth muscle cells Arterioscler. Thromb. Vasc. Biol. 21 2001 1408 1413
28. M. El-Saadani, H. Esterbauer, M. El-Sayed, M. Goher, A.Y. Nassar, and G. Jurgens Spectrophotometric assay for lipid peroxides in serum lipoproteins using a commercially available reagent J. Lipid Res. 30 1989 627 630
29. A.M. Jenner, J.E. Ruiz, C. Dunster, B. Halliwell, G.E. Mann, and R.C. Siow Vitamin C protects against hypochlorous acid-induced glutathione depletion and DNA base and protein damage in human vascular smooth muscle cells Arterioscler. Thromb. Vasc. Biol. 22 2002 574 580
30. R. Motterlini, R. Foresti, M. Intaglietta, and R.M. Winslow NO-mediated activation of heme oxygenase: endogenous cytoprotection against oxidative stress to endothelium Am. J. Physiol. 270 1996 H107 H114
31. K.L.H. Carpenter, G.M. Wilkins, and B. Fussell Production of oxidized lipids during modification of low-density lipoprotein by macrophages or copper Biochem. J. 304 1994 625 633
32. R. Stocker, Y. Yamamoto, A.F. McDonagh, A.N. Glazer, and B.N. Ames Bilirubin is an antioxidant of possible physiological importance Science 235 1987 1043 1046
33. J. Neuzil, and R. Stocker Free and albumin-bound bilirubin are efficient co-antioxidants for alpha-tocopherol, inhibiting plasma and low density lipoprotein lipid peroxidation J. Biol. Chem. 269 1994 16712 16719
34. A. Meister Glutathione-ascorbic acid antioxidant system in animals J. Biol. Chem. 269 1994 9397 9400
35. 2-terminal kinase activation via a glutathione reductase-mediated mechanism Circ. Res. 91 2002 712 718
36. M. Mayr, R.C. Siow, Y.L. Chung, U. Mayr, J.R. Griffiths, and Q. Xu Proteomic and metabolomic analysis of vascular smooth muscle cells: role of PKCδ Circ. Res. 94 2004 e87 e96
37. H. Huang, T. Nguyen, and C.B. Pickett Phosphorylation of Nrf2 at Ser-40 by protein kinase C regulates antioxidant response element-mediated transcription J. Biol. Chem. 277 2002 42769 42774
38. F. Bea, F.N. Hudson, A. Chait, T.J. Kavanagh, and M.E. Rosenfeld Induction of glutathione synthesis in macrophages by oxidized low-density lipoproteins is mediated by consensus antioxidant response elements Circ. Res. 92 2003 386 393
39. H. Kataoka, N. Kume, and S. Miyamoto Oxidized LDL modulates Bax/Bcl-2 through the lectin-like Ox-LDL receptor-1 in vascular smooth muscle cells Arterioscler. Thromb. Vasc. Biol. 21 2001 955 960
40. B. Metzler, C. Li, Y. Hu, G. Sturm, N. Ghaffari-Tabrizi, and Q. Xu LDL stimulates mitogen-activated protein kinase phosphatase-1 expression, independent of LDL receptors, in vascular smooth muscle cells Arterioscler. Thromb. Vasc. Biol. 19 1999 1862 1871
41. G. Shen, V. Hebbar, and S. Nair Regulation of Nrf2 transactivation domain activity: the differential effects of mitogen-activated protein kinase cascades and synergistic stimulatory effect of Raf and CREB-binding protein J. Biol. Chem. 279 2004 23052 23060
42. A. Yachie, Y. Niida, and T. Wada Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency J. Clin. Invest. 103 1999 129 135
43. C.A. Rice-Evans, D.S. Leake, K.R. Bruckdorfer, and A.T. Diplock Practical approaches to low density lipoprotein oxidation: whys, wherefores and pitfalls Free Radic. Res. 25 1996 285 311
44. M. Langlois, D. Duprez, J. Delanghe, M. De Buyzere, and D.L. Clement Serum vitamin C concentration is low in peripheral arterial disease and is associated with inflammation and severity of atherosclerosis Circulation 103 2001 1863 1868