Curcuminoids distinctly exhibit antioxidant activities and regulate expression of scavenger receptors and heme oxygenase-1

Molecular Nutrition and Food Research

Volumn 57, Issue 9, 2013, Pages 1598-1610

  Kou, Mei Chun ^a   Chiou, Shu Yuan ^b   Weng, Ching Yi ^a   Wang, Lisu ^a   Ho, Chi Tang ^c   Wu, Ming Jiuan ^a  

^a CHIA NAN UNIVERSITY OF PHARMACY AND SCIENCE   (Taiwan)

^b Laboratory of Plant Protection   (Taiwan)

^c RUTGERS UNIVERSITY   (United States)

Author keywords

CD36; Curcumin; GCLM; HO 1; OxLDL uptake

Indexed keywords

ANTIOXIDANT; BIOLOGICAL MARKER; BIS(4-HYDROXYCINNAMOYL)METHANE; CD36 ANTIGEN; COPPER; CURCUMIN; DEMETHOXYCURCUMIN; DIDEMETHOXYCURCUMIN; DRUG DERIVATIVE; GLUTAMATE CYSTEINE LIGASE; GLUTAMATE CYSTEINE LIGASE MODIFIER SUBUNIT, HUMAN; GLUTAMATE-CYSTEINE LIGASE MODIFIER SUBUNIT, HUMAN; HEME OXYGENASE 1; HMOX1 PROTEIN, HUMAN; LOW DENSITY LIPOPROTEIN; OLR1 PROTEIN, HUMAN; OXIDIZED LOW DENSITY LIPOPROTEIN; OXIDIZED LOW DENSITY LIPOPROTEIN RECEPTOR 1; PHORBOL 13 ACETATE 12 MYRISTATE; PHORBOLOL MYRISTATE ACETATE; SCAVENGER RECEPTOR A; THIOBARBITURIC ACID REACTIVE SUBSTANCE;

ARTICLE; CD36; CELL DIFFERENTIATION; CYTOLOGY; DRUG EFFECT; FOAM CELL; GCLM; GENE EXPRESSION REGULATION; GENETICS; HO-1; HUMAN; LIPID PEROXIDATION; METABOLISM; MONOCYTE; OXLDL UPTAKE; TUMOR CELL LINE; UPREGULATION;

CD36; CURCUMIN; GCLM; HO-1; OXLDL UPTAKE;

ANTIGENS, CD36; ANTIOXIDANTS; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL LINE, TUMOR; COPPER; CURCUMIN; FOAM CELLS; GENE EXPRESSION REGULATION; GLUTAMATE-CYSTEINE LIGASE; HEME OXYGENASE-1; HUMANS; LIPID PEROXIDATION; LIPOPROTEINS, LDL; MONOCYTES; SCAVENGER RECEPTORS, CLASS A; SCAVENGER RECEPTORS, CLASS E; TETRADECANOYLPHORBOL ACETATE; THIOBARBITURIC ACID REACTIVE SUBSTANCES; UP-REGULATION;

EID: 84883452470     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201200227     Document Type: Article

References (69)

1. Libby, P., Inflammation in atherosclerosis. Nature 2002, 420, 868-874.
2. Woollard, K. J., Geissmann, F., Monocytes in atherosclerosis: subsets and functions. Nat. Rev. Cardiol. 2010, 7, 77-86.
3. Ross, R., Atherosclerosis-an inflammatory disease. N. Engl. J. Med. 1999, 340, 115-126.
4. Yamada, Y., Doi, T., Hamakubo, T., Kodama, T., Scavenger receptor family proteins: roles for atherosclerosis, host defence and disorders of the central nervous system. Cell. Mol. Life Sci. 1998, 54, 628-640.
5. de Villiers, W. J., Smart, E. J., Macrophage scavenger receptors and foam cell formation. J. Leukoc. Biol. 1999, 66, 740-746.
6. Aviram, M., Macrophage foam cell formation during early atherogenesis is determined by the balance between pro-oxidants and anti-oxidants in arterial cells and blood lipoproteins. Antioxid. Redox. Signal. 1999, 1, 585-594.
7. Diaz, M. N., Frei, B., Vita, J. A., Keaney, J. F., Jr., Antioxidants and atherosclerotic heart disease. N. Engl. J. Med. 1997, 337, 408-416.
8. Kawai, Y., Nishikawa, T., Shiba, Y., Saito, S. et al., Macrophage as a target of quercetin glucuronides in human atherosclerotic arteries: implication in the anti-atherosclerotic mechanism of dietary flavonoids. J. Biol. Chem. 2008, 283, 9424-9434.
9. Lian, T. W., Wang, L., Lo, Y. H., Huang, I. J. et al., Fisetin, morin and myricetin attenuate CD36 expression and oxLDL uptake in U937-derived macrophages. Biochim. Biophys. Acta 2008, 1781, 601-609.
10. Lo, Y. H., Pan, M. H., Li, S., Yen, J. H. et al., Nobiletin metabolite, 3', 4'-dihydroxy-5, 6, 7, 8-tetramethoxyflavone, inhibits LDL oxidation and down-regulates scavenger receptor expression and activity in THP-1 cells. Biochim. Biophys. Acta 2010, 1801, 114-126.
11. Yen, J. H., Weng, C. Y., Li, S., Lo, Y. H. et al., Citrus flavonoid 5-demethylnobiletin suppresses scavenger receptor expression in THP-1 cells and alters lipid homeostasis in HepG2 liver cells. Mol. Nutr. Food Res. 2011, 55, 733-748.
12. Xie, C., Kang, J., Chen, J. R., Lazarenko, O. P. et al., Lowbush blueberries inhibit scavenger receptors CD36 and SR-A expression and attenuate foam cell formation in ApoE-deficient mice. Food Funct. 2011, 2, 588-594.
13. Tu, Y. C., Lian, T. W., Yen, J. H., Chen, Z. T. et al., Antiatherogenic effects of kaempferol and rhamnocitrin. J. Agric. Food Chem. 2007, 55, 9969-9976.
14. Basnet, P., Skalko-Basnet, N., Curcumin: an anti-inflammatory molecule from a curry spice on the path to cancer treatment. Molecules 2011, 16, 4567-4598.
15. Inoue, K., Nomura, C., Ito, S., Nagatsu, A. et al., Purification of curcumin, demethoxycurcumin, and bisdemethoxycurcumin by high-speed countercurrent chromatography. J. Agric. Food Chem. 2008, 56, 9328-9336.
16. Aggarwal, B., Bhatt, I., Ichikawa, H., Ahn, K. et al., Curcumin-Biological and Medicinal Properties, CRC Press, New York 2007.
17. Srivastava, R., Dikshit, M., Srimal, R. C., Dhawan, B. N., Anti-thrombotic effect of curcumin. Thromb. Res. 1985, 40, 413-417.
18. Vasanthi, H. R., Parameswari, R. P., Indian spices for healthy heart-an overview. Curr. Cardiol. Rev. 2010, 6, 274-279.
19. Scapagnini, G., Foresti, R., Calabrese, V., Giuffrida Stella, A. M. et al., Caffeic acid phenethyl ester and curcumin: a novel class of heme oxygenase-1 inducers. Mol. Pharmacol. 2002, 61, 554-561.
20. Ungvari, Z., Orosz, Z., Rivera, A., Labinskyy, N. et al., Resveratrol increases vascular oxidative stress resistance. Am. J. Physiol. Heart Circ. Physiol. 2007, 292, H2417-H2424.
21. Lin, H. Y., Juan, S. H., Shen, S. C., Hsu, F. L. et al., Inhibition of lipopolysaccharide-induced nitric oxide production by flavonoids in RAW264.7 macrophages involves heme oxygenase-1. Biochem. Pharmacol. 2003, 66, 1821-1832.
22. Ryter, S. W., Alam, J., Choi, A. M., Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol. Rev. 2006, 86, 583-650.
23. Durante, W., Targeting heme oxygenase-1 in vascular disease. Curr. Drug Targets 2010, 11, 1504-1516.
24. Araujo, J. A., Zhang, M., Yin, F., Heme oxygenase-1, oxidation, inflammation, and atherosclerosis. Front. Pharmacol. 2012, 3, 119.
25. Soni, K. B., Kuttan, R., Effect of oral curcumin administration on serum peroxides and cholesterol levels in human volunteers. Indian J. Physiol. Pharmacol. 1992, 36, 273-275.
26. Ramirez Bosca, A., Soler, A., Carrion-Gutierrez, M. A., Pamies Mira, D. et al., An hydroalcoholic extract of Curcuma longa lowers the abnormally high values of human-plasma fibrinogen. Mech. Ageing Dev. 2000, 114, 207-210.
27. Ramirez-Tortosa, M. C., Mesa, M. D., Aguilera, M. C., Quiles, J. L. et al., Oral administration of a turmeric extract inhibits LDL oxidation and has hypocholesterolemic effects in rabbits with experimental atherosclerosis. Atherosclerosis 1999, 147, 371-378.
28. Quiles, J. L., Mesa, M. D., Ramirez-Tortosa, C. L., Aguilera, C. M. et al., Curcuma longa extract supplementation reduces oxidative stress and attenuates aortic fatty streak development in rabbits. Arterioscler. Thromb. Vasc. Biol. 2002, 22, 1225-1231.
29. Zingg, J.-M., Hasan, S. T., Cowan, D., Ricciarelli, R. et al., Regulatory effects of curcumin on lipid accumulation in monocytes/macrophages. J. Cell. Biochem. 2012, 113, 833-840.
30. Na, L. X., Zhang, Y. L., Li, Y., Liu, L. Y. et al., Curcumin improves insulin resistance in skeletal muscle of rats. Nutr. Metab. Cardiovasc. Dis. 2011, 21, 526-533.
31. Peschel, D., Koerting, R., Nass, N., Curcumin induces changes in expression of genes involved in cholesterol homeostasis. J. Nutr. Biochem. 2007, 18, 113-119.
32. Mimche, P. N., Thompson, E., Taramelli, D., Vivas, L., Curcumin enhances non-opsonic phagocytosis of Plasmodium falciparum through up-regulation of CD36 surface expression on monocytes/macrophages. J. Antimicrob. Chemother. 2012, 67, 1895-1904.
33. Gotto, A. M., Jr., Pownall, H. J., Havel, R. J., Introduction to the plasma lipoproteins. Methods Enzymol. 1986, 128, 3-41.
34. Bradford, M. M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72, 248-254.
35. Hermann, M., Gmeiner, B., Altered susceptibility to in vitro oxidation of LDL in LDL complexes and LDL aggregates. Ann. N. Y. Acad. Sci. 1993, 683, 363-364.
36. Holvoet, P., Macy, E., Landeloos, M., Jones, D. et al., Analytical performance and diagnostic accuracy of immunometric assays for the measurement of circulating oxidized LDL. Clin. Chem. 2006, 52, 760-764.
37. Devaraj, S., Hugou, I., Jialal, I., Alpha-tocopherol decreases CD36 expression in human monocyte-derived macrophages. J. Lipid Res. 2001, 42, 521-527.
38. Teupser, D., Thiery, J., Walli, A. K., Seidel, D., Determination of LDL- and scavenger-receptor activity in adherent and non-adherent cultured cells with a new single-step fluorometric assay. Biochim. Biophys. Acta 1996, 1303, 193-198.
39. Steinbrecher, U. P., Zhang, H. F., Lougheed, M., Role of oxidatively modified LDL in atherosclerosis. Free Radic. Biol. Med. 1990, 9, 155-168.
40. Carmichael, J., DeGraff, W. G., Gazdar, A. F., Minna, J. D. et al., Evaluation of a tetrazolium-based semiautomated colorimetric assay: assessment of chemosensitivity testing. Cancer Res. 1987, 47, 936-942.
41. Yang, C. W., Chang, C. L., Lee, H. C., Chi, C. W. et al., Curcumin induces the apoptosis of human monocytic leukemia THP-1 cells via the activation of JNK/ERK pathways. BMC Complement. Altern. Med. 2012, 12, 22.
42. Hsu, H. Y., Chu, L. C., Hua, K. F., Chao, L. K., Heme oxygenase-1 mediates the anti-inflammatory effect of Curcumin within LPS-stimulated human monocytes. J. Cell. Physiol. 2008, 215, 603-612.
43. Rushworth, S. A., Ogborne, R. M., Charalambos, C. A., O'Connell, M. A., Role of protein kinase C delta in curcumin-induced antioxidant response element-mediated gene expression in human monocytes. Biochem. Biophys. Res. Commun. 2006, 341, 1007-1016.
44. Lo, Y. H., Pan, M. H., Li, S., Yen, J. H. et al., Nobiletin metabolite, 3', 4'-dihydroxy-5, 6, 7, 8-tetramethoxyflavone, inhibits LDL oxidation and down-regulates scavenger receptor expression and activity in THP-1 cells. Biochim. Biophys. Acta 2010, 1801, 114-126.
45. Pou, J., Rebollo, A., Roglans, N., Sanchez, R. M. et al., Ritonavir Increases CD36, ABCA1 and CYP27 Expression in THP-1 macrophages. Exp. Biol. Med. 2008, 233, 1572-1582.
46. Tu, Y. C., Lian, T. W., Yen, J. H., Chen, Z. T. et al., Antiatherogenic effects of kaempferol and rhamnocitrin. J. Agric. Food Chem. 2007, 55, 9969-9976.
47. Vinals, M., Bermudez, I., Llaverias, G., Alegret, M. et al., Aspirin increases CD36, SR-BI, and ABCA1 expression in human THP-1 macrophages. Cardiovasc. Res. 2005, 66, 141-149.
48. Jeong, G. S., Oh, G. S., Pae, H. O., Jeong, S. O. et al., Comparative effects of curcuminoids on endothelial heme oxygenase-1 expression: ortho-methoxy groups are essential to enhance heme oxygenase activity and protection. Exp. Mol. Med. 2006, 38, 393-400.
49. Ishii, T., Itoh, K., Ruiz, E., Leake, D. S. et al., 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. 2004, 94, 609-616.
50. Anand, P., Kunnumakkara, A. B., Newman, R. A., Aggarwal, B. B., Bioavailability of curcumin: problems and promises. Mol. Pharm. 2007, 4, 807-818.
51. Shen, L., Ji, H. F., The pharmacology of curcumin: is it the degradation products? Trends Mol. Med. 2012, 18, 138-144.
52. Burkitt, M. J., A critical overview of the chemistry of copper-dependent low density lipoprotein oxidation: roles of lipid hydroperoxides, alpha-tocopherol, thiols, and ceruloplasmin. Arch. Biochem. Biophys. 2001, 394, 117-135.
53. Fuhrman, B., Lavy, A., Aviram, M., Consumption of red wine with meals reduces the susceptibility of human plasma and low-density lipoprotein to lipid peroxidation. Am. J. Clin. Nutr. 1995, 61, 549-554.
54. Goulinet, S., Chapman, M. J., Plasma LDL and HDL subspecies are heterogenous in particle content of tocopherols and oxygenated and hydrocarbon carotenoids. Relevance to oxidative resistance and atherogenesis. Arterioscler. Thromb. Vasc. Biol. 1997, 17, 786-796.
55. Cuvelier, M.-E., Richard, H., Berset, C., Comparison of the antioxidative activity of some acid-phenols: structure-activity relationship. Biosci. Biotechnol. Biochem. 1992, 56, 324-325.
56. Shehzad, A., Ha, T., Subhan, F., Lee, Y. S., New mechanisms and the anti-inflammatory role of curcumin in obesity and obesity-related metabolic diseases. Eur. J. Nutr. 2011, 50, 151-161.
57. Balogun, E., Hoque, M., Gong, P., Killeen, E. et al., Curcumin activates the haem oxygenase-1 gene via regulation of Nrf2 and the antioxidant-responsive element. Biochem. J. 2003, 371, 887-895.
58. Orozco, L. D., Kapturczak, M. H., Barajas, B., Wang, X. et al., Heme oxygenase-1 expression in macrophages plays a beneficial role in atherosclerosis. Circ. Res. 2007, 100, 1703-1711.
59. Botta, D., Franklin, C. C., White, C. C., Krejsa, C. M. et al., Glutamate-cysteine ligase attenuates TNF-induced mitochondrial injury and apoptosis. Free Radic. Biol. Med. 2004, 37, 632-642.
60. Callegari, A., Liu, Y., White, C. C., Chait, A. et al., Gain and loss of function for glutathione synthesis: impact on advanced atherosclerosis in apolipoprotein E-deficient mice. Arterioscler. Thromb. Vasc. Biol. 2011, 31, 2473-2482.
61. Barajas, B., Che, N., Yin, F., Rowshanrad, A. et al., NF-E2-related factor 2 promotes atherosclerosis by effects on plasma lipoproteins and cholesterol transport that overshadow antioxidant protection. Arterioscler. Thromb. Vasc. Biol. 2011, 31, 58-66.
62. Schwende, H., Fitzke, E., Ambs, P., Dieter, P., Differences in the state of differentiation of THP-1 cells induced by phorbol ester and 1, 25-dihydroxyvitamin D3. J. Leukoc. Biol. 1996, 59, 555-561.
63. Yesner, L. M., Huh, H. Y., Pearce, S. F., Silverstein, R. L., Regulation of monocyte CD36 and thrombospondin-1 expression by soluble mediators. Arterioscler. Thromb. Vasc. Biol. 1996, 16, 1019-1025.
64. Lin, C. S., Lin, F. Y., Ho, L. J., Tsai, C. S. et al., PKCdelta signalling regulates SR-A and CD36 expression and foam cell formation. Cardiovasc. Res. 2012, 95, 346-355.
65. Feng, J., Han, J., Pearce, S. F. A., Silverstein, R. L. et al., Induction of CD36 expression by oxidized LDL and IL-4 by a common signaling pathway dependent on protein kinase C and PPAR-{gamma}. J. Lipid Res. 2000, 41, 688-696.
66. Liu, J. Y., Lin, S. J., Lin, J. K., Inhibitory effects of curcumin on protein kinase C activity induced by 12-O-tetradecanoyl-phorbol-13-acetate in NIH 3T3 cells. Carcinogenesis 1993, 14, 857-861.
67. Ali, R. E., Rattan, S. I., Curcumin's biphasic hormetic response on proteasome activity and heat-shock protein synthesis in human keratinocytes. Ann. N. Y. Acad. Sci. 2006, 1067, 394-399.
68. Collot-Teixeira, S., Martin, J., McDermott-Roe, C., Poston, R. et al., CD36 and macrophages in atherosclerosis. Cardiovasc. Res. 2007, 75, 468-477.
69. Wang, Y. J., Pan, M. H., Cheng, A. L., Lin, L. I. et al., Stability of curcumin in buffer solutions and characterization of its degradation products. J. Pharm. Biomed. Anal. 1997, 15, 1867-1876.