α-lipoic acid-induced heme oxygenase-1 expression is mediated by nuclear factor erythroid 2-related factor 2 and p38 mitogen-activated protein kinase in human monocytic cells

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 25, Issue 10, 2005, Pages 2100-2105

  Ogborne, Richard M ^a   Rushworth, Stuart A ^a   O'Connell, Maria A ^a  

^a MRC HUMAN NUTRITION RESEARCH   (United Kingdom)

Author keywords

lipoic acid; Heme oxygenase 1; Monocyte; Nrf2; p38 MAPK

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; HEME OXYGENASE 1; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; MITOGEN ACTIVATED PROTEIN KINASE P38 INHIBITOR; THIOCTIC ACID; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; CELL NUCLEUS; CELL TYPE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DIET; DOSE TIME EFFECT RELATION; HEART PROTECTION; HUMAN; HUMAN CELL; MACROPHAGE; MONOCYTE; PORPHYRIN METABOLISM; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; VASCULAR DISEASE;

ACTIVE TRANSPORT, CELL NUCLEUS; CELL LINE, TUMOR; GENE EXPRESSION; GENES, DOMINANT; HEME OXYGENASE-1; HUMANS; LEUKEMIA; MONOCYTES; NF-E2-RELATED FACTOR 2; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RESPONSE ELEMENTS; RNA, MESSENGER; THIOCTIC ACID;

EID: 26244450392     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.ATV.0000183745.37161.6e     Document Type: Article

References (50)

1. Munro HN, Linder MC. Ferritin: structure, biosynthesis, and role in iron metabolism. Physiol Rev. 1978;58:317-396.
2. Alam J, Cook ML. Transcriptional regulation of the heme oxygenase-1 gene via the stress response element pathway. Curr Pharm Des. 2003;9: 2499-2511.
3. Wagener FA, Volk HD, Willis D, Abraham NG, Soares MP, Adema GJ. Figdor CG. Different faces of the heme-heme oxygenase system in inflammation. Pharmacol Rev. 2003;55:551-571.
4. Wu TW, Fung KP, Yang CC. Unconjugated bilirubin inhibits the oxidation of human low density lipoprotein better than Trolox. Life Sci. 1994;54:477-481.
5. Otterbein LE, Bach FH, Alam J, Soares M, Tao LH, Wysk M, Davis RJ, Flavell RA, Choi AM. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med. 2000; 6:422-428.
6. Duckers HJ, Boehm M, True AL, Yet SF, San H, Park JL, Clinton WR, Lee ME, Nabel GJ, Nabel EG. Heme oxygenase-1 protects against vascular constriction and proliferation. Nat Med. 200l;7:693-698.
7. Morita T, Perrella MA, Lee ME, Kourembanas S. Smooth muscle cell-derived carbon monoxide is a regulator of vascular cGMP. Proc Natl Acad Sci U S A. 1995;92:1475-1479.
8. Neuzil J, Stocker R. Free and albumin-bound bilirubin are efficient co-antioxidants for alpha-tocopherol, inhibiting plasma and low density lipoprotein lipid peroxidation. J Biol Chem. 1994;269:16712-16719.
9. Lee TS, Tsai HL, Chau LY. Induction of heme oxygenase-1 expression in murine macrophages is essential for the anti-inflammatory effect of low dose 15 deoxy-delta 12,14-prostaglandin J2. J Biol Chem. 2003;278: 19325-19330.
10. Lee TS, Chau LY. Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice. Nat Med. 2002;8:240-246.
11. Ishikawa K, Navab M, Leitinger N, Fogelman AM, Lusis AJ. Induction of heme oxygenase-1 inhibits the monocyte transmigration induced by mildly oxidized LDL. J Clin Invest. 1997;100:1209-1216.
12. Ishikawa K, Sugawara D, Wang X, Suzuki K, Habe H, Maruyama Y, Lusis AJ. Heme oxygenase-1 inhibits atherosclerotic lesion formation in LDL-receptor knockout mice. Circ Res. 2001;88:506-512.
13. Yet SF, Layne MD, Liu X, Chen YH, Ith B, Sibinga NE, Perrella MA. Absence of heme oxygase-1 exacerbates atherosclerotic lesion formation and vascular remodeling. FASEB J. 2003;17:1759-1761.
14. Yachie A, Niide Y, Wada T, Igarashi N, Kaneda H, Toma T, Ohta K, Kasahara Y, Koizumi S. Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency. J Clin Invest. 1999;103: 129-135.
15. Exner M, Minar E, Wagner O, Schulungen M. The role of heme oxygenase-1 promoter polymorphisms in human disease. Free Radic Biol Med. 2004;37:1097-1104.
16. Wasserman WW, Fahl WE. Functional antioxidant response elements. Proc Natl Acad Sci U S A. 1997;94:5361-5366.
17. Nguyen T, Sherratt PJ, Pickett CB. Regulatory mechanisms controlling gene expression mediated by the antioxidant response element. Annu Rev Pharmacol Toxicol. 2003;43:233-260.
18. Kraft AD, Johnson DA, Johnson JA. Nuclear factor E2-related factor 2-dependent antioxidant response element activation by tert-butylhydroquinone and sulforaphane occurring preferentially in astrocytes conditions neurons against oxidative insult. J Neurosci. 2004; 24:1101-1112.
19. Scapagnini G, Foresti R, Calabrese V, Giuffrida Stella AM, Green CJ, Motterlini R. Caffeic acid phenethyl ester and curcumin: a novel class of heme oxygenase-1 inducers. Mol Pharmacol. 2002;61:554-561.
20. Ogborne RM, Rushworth SA. Charalambos CA, O'Connell MA. Haem oxygenase-1: a target for dietary antioxidants. Biochem Soc Trans. 2004; 32:1003-1005.
21. Chow JM, Shen SC, Huan SK, Lin HY, Chen YC. Quercetin, but not rutin and quercitrin, prevention of H(2)O(2)-induced apoptosis via anti-oxidant activity and heme oxygenase 1 expression in macrophages. Biochem Pharmacol. 2005;69:1839-1851.
22. Wollin SD, Jones PJ. Alpha-lipoic acid and cardiovascular disease. J Nutr. 2003;133:3327-3330.
23. Lee HA, Hughes DA. Alpha-lipoic acid modulates NF-kappaB activity in human monocytic cells by direct interaction with DNA. Exp Gerontol. 2002;37:401-410.
24. Kiemer AK, Muller C, Vollmar AM. Inhibition of LPS-induced nitric oxide and TNF-alpha production by alpha-lipoic acid in rat Kupffer cells and in RAW264.7 murine macrophages. Immunol Cell Biol. 2002;80: 550-557.
25. Midaoui AE, Elimadi A, Wu L, Haddad PS, de Champlain J. Lipoic acid prevents hypertension, hyperglycemia, and the increase in heart mitochondrial superoxide production. Am J Hypertens. 2003;16:173-179.
26. Vasdev S, Ford CA, Parai S, Longerich L, Gadag V. Dietary alpha-lipoic acid supplementation lowers blood pressure in spontaneously hypetensive rats. J Hypertens. 2000;18:567-573.
27. Skubitz KM, Pessano S, Bottero L, Ferrero D, Rovera G, August JT. Human granulocyte surface molecules identified by murine monoclonal antibodies. J Immunol. 1983;131:1882-1888.
28. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods. 1983;65:55-63.
29. O'Connell MA, Bennett BL, Mercurio F, Manning AM. Mackman N. Role of IKK1 and IKK 2 in lipopolysaccharide signaling in human monocytic cells. J Biol Chem. 1998;273:30410-30414.
30. Guha M, O'Connell MA, Pawlinski R, Hollis A, McGovern P, Yan SF, Stern D, Mackman N. Lipopolysaccharide activation of the MEK-ERK 1/2 pathway in human monocytic cells mediates tissue factor and tumor necrosis factor alpha expression by inducing Elk-1 phosphorylation and Egr-1 expression. Blood. 2001;98:1429-1439.
31. Chen XL, Varner SE, Rao AS, Grey JY, Thomas S, Cook CK, Wasserman MA, Medford RM, Jaiswal AK, Kunsch C. Laminar flow induction of antioxidant response element-mediated genes in endothelial cells. A novel anti-inflammatory mechanism. J Biol Chem. 2003;278: 703-711.
32. Alam J, Stewart D, Touchard C, Boinapally S, Choi AM, Cook JL. Nrf2, a Cap'n'Collar transcription factor, regulates induction of the heme oxygenase-1 gene. J Biol Chem. 1999;274:26071-26078.
33. Chen CY, Jang JH, Li MH, Surh YJ. Resveratrol upregulates heme oxygenase-1 expression via activation of NF-E2-related factor 2 in PC12 cells. Biochem Biophys Res Commun. 2005;331:993-1000.
34. Juan SH, Cheng TH, Lin HC, Chu YL. Lee WS. Mechanism of concentration-dependent induction of heme oxygenase-1 by resveratrol in human aortic smooth muscle cells. Biochem Pharmacol. 2005;69:41-48.
35. Zhang WJ, Frei B. Alpha-lipoic acid inhibits TNF-alpha-induced-NF-kappaB activation and adhesion molecule expression in human aortic endothelial cells. FASEB J. 2001;15:2423-2432.
36. Teichert J, Kern J, Tritschler HJ, Ulrich H, Preiss R. Investigations on the pharmacokinetics of alpha-lipoic acid in healthy volunteers. Int J Clin Pharmacol Ther. 1998;36:625-628.
37. Peter G, Borbe HO. Absorption of [7,8-14C]rac-a-lipoic acid from in situ ligated segments of the gastrointestinal tract of the rat. Arzneimittelforschung. 1995;45:293-299.
38. Biewenga GP, Haenan GR. Bast A. The pharmacology of the antioxidant lipoic acid. Gen Pharmacol. 1997;29:315-331.
39. Ziegler D, Reljanovic M, Mehnert H, Gries FA. Alpha-lipoic acid in the treatment of diabetic polyneuropathy in Germany: current evidence from clinical trials. Exp Clin Endocrinol Diabetes. 1999;107:421-430.
40. Hendler S, Rorvik D. PDR for Nutritional Supplements. Montvale, NJ: Medical Economics Company; 2001.
41. Martin D, Rojo AI, Saunas M, Diaz R, Gallardo G, Alani J, de Galarreta CM, Cuadrado A. Regulation of heme oxygenase-1 expression through the phosphatidylinositol 3-kinase/Akt pathway and the Nrf2 transcription factor in response to the antioxidant phytochemical carnosol. J Biol Chem. 2004;279:8919-8929.
42. Balogun E, Hoque M, Gong P, Killeen E, Green CJ, Foresti R, Alani J, Motterlini R. Curcumin activates the haem oxygenase-1 gene via regulation of Nrf2 and the anioxidant-responsive element. Biochem J. 2003; 371:887-895.
43. Kobayashi A, Kang MI, Okawa H, Ohtsuji M, Zenke Y, Chiba T, Igarashi K, Yamamoto M. Oxidative stress sensor keap1 functions as an adaptor for cu13-based E3 ligase to regulate proteasomal degradation of Nrf2. Mol Cell Biol. 2004;24:7130-7139.
44. Li N, Alam J, Venkatesan MI, Eiguren-Fernandez A, Schmitz D, Di Stefano E, Slaughter N, Killeen E, Wang X, Huang A, Wang M, Miguel AH, Cho A, Sioutas C, Nel AE. Nrf2 is a key transcription factor that regulates antioxidant defense in macrophages and epithelial cells: protecting against the proinflamniatory and oxidizing effects of diesel exhaust particles. J Immunol. 2004;173:3467-3481.
45. Itoh K, Wakabayashi N. Katoh Y, Ishii T, O'Connor T, Yamamotot M. Keap1 regulates both cytoplasmic-nuclear shuttling and degradation of Nrf2 in response to electrophiles. Genes Cells. 2003;8:379-391.
46. Huang HC, Nguyen T, Pickett CB. Regulation of the antioxidant response element by protein kinase C-mediated phosphorylation of NF-E2-related factor 2. Proc Natl Acad Sci U S A. 2000;97:12475-12480.
47. Bloom DA, Jaiswal AK. Phosphorylation of Nrf2S40 by PKC in response to antioxidants leads to the release of Nrf2 from INrf2 but not required for Nrf2 stabilization/accumulation in the nucleus and transcriptional activation of ARE-mediated NQOI gene expression. J Biol Chem. 2003;278: 44675-44682.
48. Ng D, Kokot N, Hiura T, Faris M, Saxon A, Nel A. Macrophage activation by polycyclic aromatic hydrocarbons: evidence for the involvement of stress-activated protein kinases, activator protein-1, and antioxidant response elements. J Immunol. 1998;161:942-951.
49. Konrad D, Somwar R, Sweeney G, Yaworsky K, Hayashi M, Ramlal T, Klip A. The antihyperglycemic drug alpha-lipoic acid stimulates glucose uptake via both GLUT4 translocation and GLUT4 activation: potential role of p38 mitogen-activated protein kinase in GLUT4 activation. Diabetes. 2001;50:1464-1471.
50. Soares MP, Seldon MP, Gregoire IP, Vassilevskaia T, Berberat PO, Yu J, Tsui TY, Bach FH. Heme oxygenase-1 modulates the expression of adhesion molecules associated with endothelial cell activation. J Immunol. 2004;172:3553-3563.