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

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1801, Issue 2, 2010, Pages 114-126

  Lo, Ya Hsuan ^a   Pan, Min Hsiung ^b   Li, Shiming ^c   Yen, Jui Hung ^d   Kou, Mei Chun ^a   Ho, Chi Tang ^c   Wu, Ming Jiuan ^a  

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

^b NATIONAL KAOHSIUNG UNIVERSITY OF APPLIED SCIENCES   (Taiwan)

^c RUTGERS UNIVERSITY   (United States)

^d TZU CHI UNIVERSITY   (Taiwan)

Author keywords

Atherogenesis; CD36; Low density lipoprotein (LDL); Scavenger receptor A (SR A)

Indexed keywords

1,1' DIOCTADECYL 3,3,3',3' TETRAMETHYLINDOCARBOCYANINE; 3',4' DIHYDROXY 5,6,7,8 TETRAMETHOXYFLAVONE; CD36 ANTIGEN; DRUG METABOLITE; LOW DENSITY LIPOPROTEIN; NOBILETIN; OXIDIZED LOW DENSITY LIPOPROTEIN; SCAVENGER RECEPTOR; THIOBARBITURIC ACID REACTIVE SUBSTANCE; UNCLASSIFIED DRUG;

ARTICLE; ATHEROGENESIS; CELL DIFFERENTIATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; DRUG STRUCTURE; ELECTROPHORETIC MOBILITY; GENE EXPRESSION; HUMAN; HUMAN TISSUE; LIPID OXIDATION; MACROPHAGE; MONOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; ANTIGENS, CD11B; ANTIGENS, CD36; CELL DIFFERENTIATION; CELLS, CULTURED; DOWN-REGULATION; FLAVONES; FLOW CYTOMETRY; LIPID PEROXIDATION; LIPOPROTEINS, LDL; MACROPHAGES; MICE; MONOCYTES; OXIDATION-REDUCTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SCAVENGER RECEPTORS, CLASS A; SCAVENGER RECEPTORS, CLASS E; TETRADECANOYLPHORBOL ACETATE; THIOBARBITURIC ACID REACTIVE SUBSTANCES;

CITRUS;

EID: 73849107792     PISSN: 13881981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbalip.2009.10.002     Document Type: Article

References (77)

1. Libby P. Inflammation in atherosclerosis. Nature 420 (2002) 868-874
2. Kaplan M., and Aviram M. Oxidized low density lipoprotein: atherogenic and proinflammatory characteristics during macrophage foam cell formation. An inhibitory role for nutritional antioxidants and serum paraoxonase. Clin. Chem. Lab. Med. 37 (1999) 777-787
3. Ross R. Atherosclerosis-an inflammatory disease. N. Engl. J. Med. 340 (1999) 115-126
4. Yamada Y., Doi T., Hamakubo T., and Kodama T. Scavenger receptor family proteins: roles for atherosclerosis, host defence and disorders of the central nervous system. Cell. Mol. Life Sci. 54 (1998) 628-640
5. de Villiers W.J., and Smart E.J. Macrophage scavenger receptors and foam cell formation. J. Leukoc. Biol. 66 (1999) 740-746
6. Endemann G., Stanton L.W., Madden K.S., Bryant C.M., White R.T., and Protter A.A. CD36 is a receptor for oxidized low density lipoprotein. J. Biol. Chem. 268 (1993) 11811-11816
7. Zeng Y., Tao N., Chung K.N., Heuser J.E., and Lublin D.M. Endocytosis of oxidized low density lipoprotein through scavenger receptor CD36 utilizes a lipid raft pathway that does not require caveolin-1. J. Biol. Chem. 278 (2003) 45931-45936
8. Nakata A., Nakagawa Y., Nishida M., Nozaki S., Miyagawa J., Nakagawa T., Tamura R., Matsumoto K., Kameda-Takemura K., Yamashita S., and Matsuzawa Y. CD36, a novel receptor for oxidized low-density lipoproteins, is highly expressed on lipid-laden macrophages in human atherosclerotic aorta. Arterioscler. Thromb. Vasc. Biol. 19 (1999) 1333-1339
9. 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
10. Han J., Hajjar D.P., Febbraio M., and Nicholson A.C. Native and modified low density lipoproteins increase the functional expression of the macrophage class B scavenger receptor, CD36. J. Biol. Chem. 272 (1997) 21654-21659
11. Platt N., and Gordon S. Is the class A macrophage scavenger receptor (SR-A) multifunctional?-the mouse's tale. J. Clin. Invest. 108 (2001) 649-654
12. Kume N., Murase T., Moriwaki H., Aoyama T., Sawamura T., Masaki T., and Kita T. Inducible expression of lectin-like oxidized LDL receptor-1 in vascular endothelial cells. Circ. Res. 83 (1998) 322-327
13. Kataoka H., Kume N., Miyamoto S., Minami M., Moriwaki H., Murase T., Sawamura T., Masaki T., Hashimoto N., and Kita T. Expression of lectinlike oxidized low-density lipoprotein receptor-1 in human atherosclerotic lesions. Circulation 99 (1999) 3110-3117
14. Moriwaki H., Kume N., Sawamura T., Aoyama T., Hoshikawa H., Ochi H., Nishi E., Masaki T., and Kita T. Ligand specificity of LOX-1, a novel endothelial receptor for oxidized low density lipoprotein. Arterioscler. Thromb. Vasc. Biol. 18 (1998) 1541-1547
15. Febbraio M., Podrez E.A., Smith J.D., Hajjar D.P., Hazen S.L., Hoff H.F., Sharma K., and Silverstein R.L. Targeted disruption of the class B scavenger receptor CD36 protects against atherosclerotic lesion development in mice. J. Clin. Invest. 105 (2000) 1049-1056
16. Suzuki H., Kurihara Y., Takeya M., Kamada N., Kataoka M., Jishage K., Ueda O., Sakaguchi H., Higashi T., Suzuki T., Takashima Y., Kawabe Y., Cynshi O., Wada Y., Honda M., Kurihara H., Aburatani H., Doi T., Matsumoto A., Azuma S., Noda T., Toyoda Y., Itakura H., Yazaki Y., Kodama T., et al. A role for macrophage scavenger receptors in atherosclerosis and susceptibility to infection. Nature 386 (1997) 292-296
17. Babaev V.R., Gleaves L.A., Carter K.J., Suzuki H., Kodama T., Fazio S., and Linton M.F. Reduced atherosclerotic lesions in mice deficient for total or macrophage-specific expression of scavenger receptor-A. Arterioscler. Thromb. Vasc. Biol. 20 (2000) 2593-2599
18. Sakaguchi H., Takeya M., Suzuki H., Hakamata H., Kodama T., Horiuchi S., Gordon S., van der Laan L.J., Kraal G., Ishibashi S., Kitamura N., and Takahashi K. Role of macrophage scavenger receptors in diet-induced atherosclerosis in mice. Lab. Invest. 78 (1998) 423-434
19. Mehta J.L., Sanada N., Hu C.P., Chen J., Dandapat A., Sugawara F., Satoh H., Inoue K., Kawase Y., Jishage K., Suzuki H., Takeya M., Schnackenberg L., Beger R., Hermonat P.L., Thomas M., and Sawamura T. Deletion of LOX-1 reduces atherogenesis in LDLR knockout mice fed high cholesterol diet. Circ. Res. 100 (2007) 1634-1642
20. Hu C., Chen J., Dandapat A., Fujita Y., Inoue N., Kawase Y., Jishage K., Suzuki H., Li D., Hermonat P.L., Sawamura T., and Mehta J.L. LOX-1 abrogation reduces myocardial ischemia-reperfusion injury in mice. J. Mol. Cell. Cardiol. 44 (2008) 76-83
21. 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. 1 (1999) 585-594
22. Diaz M.N., Frei B., Vita J.A., and Keaney Jr. J.F. Antioxidants and atherosclerotic heart disease. N. Engl. J. Med. 337 (1997) 408-416
23. Fuhrman B., Volkova N., Coleman R., and Aviram M. Grape powder polyphenols attenuate atherosclerosis development in apolipoprotein E deficient (E0) mice and reduce macrophage atherogenicity. J. Nutr. 135 (2005) 722-728
24. Fuhrman B., and Aviram M. Anti-atherogenicity of nutritional antioxidants. IDrugs 4 (2001) 82-92
25. Fuhrman B., and Aviram M. Flavonoids protect LDL from oxidation and attenuate atherosclerosis. Curr. Opin. Lipidol. 12 (2001) 41-48
26. Munteanu A., Zingg J.M., Ricciarelli R., and Azzi A. CD36 overexpression in ritonavir-treated THP-1 cells is reversed by alpha-tocopherol. Free Radic. Biol. Med. 38 (2005) 1047-1056
27. Kawai Y., Nishikawa T., Shiba Y., Saito S., Murota K., Shibata N., Kobayashi M., Kanayama M., Uchida K., and Terao J. Macrophage as a target of quercetin glucuronides in human atherosclerotic arteries: implication in the anti-atherosclerotic mechanism of dietary flavonoids. J. Biol. Chem. 283 (2008) 9424-9434
28. Lian T.W., Wang L., Lo Y.H., Huang I.J., and Wu M.J. Fisetin, morin and myricetin attenuate CD36 expression and oxLDL uptake in U937-derived macrophages. Biochim. Biophys. Acta 1781 (2008) 601-609
29. Munteanu A., Taddei M., Tamburini I., Bergamini E., Azzi A., and Zingg J.M. Antagonistic effects of oxidized low density lipoprotein and alpha-tocopherol on CD36 scavenger receptor expression in monocytes: involvement of protein kinase B and peroxisome proliferator-activated receptor-gamma. J. Biol. Chem. 281 (2006) 6489-6497
30. Devaraj S., Hugou I., and Jialal I. Alpha-tocopherol decreases CD36 expression in human monocyte-derived macrophages. J. Lipid Res. 42 (2001) 521-527
31. Kurowska E.M., and Manthey J.A. Hypolipidemic effects and absorption of citrus polymethoxylated flavones in hamsters with diet-induced hypercholesterolemia. J. Agric. Food Chem. 52 (2004) 2879-2886
32. Roza J.M., Xian-Liu Z., and Guthrie N. Effect of citrus flavonoids and tocotrienols on serum cholesterol levels in hypercholesterolemic subjects. Altern. Ther. Health Med. 13 (2007) 44-48
33. Wilcox L.J., Borradaile N.M., de Dreu L.E., and Huff M.W. Secretion of hepatocyte apoB is inhibited by the flavonoids, naringenin and hesperetin, via reduced activity and expression of ACAT2 and MTP. J. Lipid Res. 42 (2001) 725-734
34. Morin B., Nichols L.A., Zalasky K.M., Davis J.W., Manthey J.A., and Holland L.J. The citrus flavonoids hesperetin and nobiletin differentially regulate low density lipoprotein receptor gene transcription in HepG2 liver cells. J. Nutr. 138 (2008) 1274-1281
35. Eguchi A., Murakami A., and Ohigashi H. Nobiletin, a citrus flavonoid, suppresses phorbol ester-induced expression of multiple scavenger receptor genes in THP-1 human monocytic cells. FEBS Lett. 580 (2006) 3321-3328
36. Whitman S.C., Kurowska E.M., Manthey J.A., and Daugherty A. Nobiletin, a citrus flavonoid isolated from tangerines, selectively inhibits class A scavenger receptor-mediated metabolism of acetylated LDL by mouse macrophages. Atherosclerosis 178 (2005) 25-32
37. Lai C.S., Li S., Chai C.Y., Lo C.Y., Dushenkov S., Ho C.T., Pan M.H., and Wang Y.J. Anti-inflammatory and antitumor promotional effects of a novel urinary metabolite, 3′,4′-didemethylnobiletin, derived from nobiletin. Carcinogenesis 29 (2008) 2415-2424
38. Li S., Sang S., Pan M.H., Lai C.S., Lo C.Y., Yang C.S., and Ho C.T. Anti-inflammatory property of the urinary metabolites of nobiletin in mouse. Bioorg. Med. Chem. Lett. 17 (2007) 5177-5181
39. Eguchi A., Murakami A., Li S., Ho C.T., and Ohigashi H. Suppressive effects of demethylated metabolites of nobiletin on phorbol ester-induced expression of scavenger receptor genes in THP-1 human monocytic cells. Biofactors 31 (2007) 107-116
40. Esterbauer H., Striegl G., Puhl H., and Rotheneder M. Continuous monitoring of in vitro oxidation of human low density lipoprotein. Free Radic. Res. Commun. 6 (1989) 67-75
41. Knipping G., Rotheneder M., Striegl G., and Esterbauer H. Antioxidants and resistance against oxidation of porcine LDL subfractions. J. Lipid Res. 31 (1990) 1965-1972
42. Lanningham-Foster L., Chen C., Chance D.S., and Loo G. Grape extract inhibits lipid peroxidation of human low density lipoprotein. Biol. Pharm. Bull. 18 (1995) 1347-1351
43. Gotto Jr. A.M., Pownall H.J., and Havel R.J. Introduction to the plasma lipoproteins. Methods Enzymol. 128 (1986) 3-41
44. 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. 72 (1976) 248-254
45. Kleinveld H.A., Hak-Lemmers H.L., Stalenhoef A.F., and Demacker P.N. Improved measurement of low-density-lipoprotein susceptibility to copper-induced oxidation: application of a short procedure for isolating low-density lipoprotein. Clin. Chem. 38 (1992) 2066-2072
46. Hermann M., and Gmeiner B. Altered susceptibility to in vitro oxidation of LDL in LDL complexes and LDL aggregates. Ann. N. Y. Acad. Sci. 683 (1993) 363-364
47. Fuhrman B., Partoush A., Volkova N., and Aviram M. Ox-LDL induces monocyte-to-macrophage differentiation in vivo: Possible role for the macrophage colony stimulating factor receptor (M-CSF-R). Atherosclerosis 196 (2008) 598-607
48. Wang X., and Seed B. A PCR primer bank for quantitative gene expression analysis. Nucl. Acids Res. 31 (2003) e154
49. Teupser D., Thiery J., Walli A.K., and 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 1303 (1996) 193-198
50. Basu S.K., Goldstein J.L., Anderson G.W., and Brown M.S. Degradation of cationized low density lipoprotein and regulation of cholesterol metabolism in homozygous familial hypercholesterolemia fibroblasts. Proc. Natl. Acad. Sci. U. S. A. 73 (1976) 3178-3182
51. Steinbrecher U.P., Zhang H.F., and Lougheed M. Role of oxidatively modified LDL in atherosclerosis. Free Radic. Biol. Med. 9 (1990) 155-168
52. Abuja P.M., and Esterbauer H. Simulation of lipid peroxidation in low-density lipoprotein by a basic "skeleton" of reactions. Chem. Res. Toxicol. 8 (1995) 753-763
53. Ziouzenkova O., Sevanian A., Abuja P.M., Ramos P., and Esterbauer H. Copper can promote oxidation of LDL by markedly different mechanisms. Free Radic. Biol. Med. 24 (1998) 607-623
54. Auwerx J. The human leukemia cell line, THP-1: a multifacetted model for the study of monocyte-macrophage differentiation. Experientia 47 (1991) 22-31
55. Carmichael J., DeGraff W.G., Gazdar A.F., Minna J.D., and Mitchell J.B. Evaluation of a tetrazolium-based semiautomated colorimetric assay: assessment of chemosensitivity testing. Cancer Res. 47 (1987) 936-942
56. Arnaout M.A. Structure and function of the leukocyte adhesion molecules CD11/CD18. Blood 75 (1990) 1037-1050
57. Kunjathoor V.V., Febbraio M., Podrez E.A., Moore K.J., Andersson L., Koehn S., Rhee J.S., Silverstein R., Hoff H.F., and Freeman M.W. Scavenger receptors class A-I/II and CD36 are the principal receptors responsible for the uptake of modified low density lipoprotein leading to lipid loading in macrophages. J. Biol. Chem. 277 (2002) 49982-49988
58. Quinn M.T., Parthasarathy S., Fong L.G., and Steinberg D. Oxidatively modified low density lipoproteins: a potential role in recruitment and retention of monocyte/macrophages during atherogenesis. Proc. Natl. Acad. Sci. U. S. A. 84 (1987) 2995-2998
59. Hayden J.M., Brachova L., Higgins K., Obermiller L., Sevanian A., Khandrika S., and Reaven P.D. Induction of monocyte differentiation and foam cell formation in vitro by 7-ketocholesterol. J. Lipid Res. 43 (2002) 26-35
60. Frostegard J., Nilsson J., Haegerstrand A., Hamsten A., Wigzell H., and Gidlund M. Oxidized low density lipoprotein induces differentiation and adhesion of human monocytes and the monocytic cell line U937. Proc. Natl. Acad. Sci. U. S. A. 87 (1990) 904-908
61. Pou J., Rebollo A., Roglans N., Sanchez R.M., Vazquez-Carrera M., Laguna J.C., Pedro-Botet J., and Alegret M. Ritonavir increases CD36, ABCA1 and CYP27 expression in THP-1 macrophages. Exp. Biol. Med. (Maywood) 233 (2008) 1572-1582
62. Tu Y.C., Lian T.W., Yen J.H., Chen Z.T., and Wu M.J. Antiatherogenic effects of kaempferol and rhamnocitrin. J. Agric. Food Chem. 55 (2007) 9969-9976
63. Vinals M., Bermudez I., Llaverias G., Alegret M., Sanchez R.M., Vazquez-Carrera M., and Laguna J.C. Aspirin increases CD36, SR-BI, and ABCA1 expression in human THP-1 macrophages. Cardiovasc. Res. 66 (2005) 141-149
64. Steinberg D., Parthasarathy S., Carew T., Khoo J., and Witztum J. Beyond cholesterol. Modifications of low density lipoprotein that increase its atherogenicity. N. Engl. J. Med. 320 (1989) 915-924
65. de Whalley C.V., Rankin S.M., Hoult J.R., Jessup W., and Leake D.S. Flavonoids inhibit the oxidative modification of low density lipoproteins by macrophages. Biochem. Pharmacol. 39 (1990) 1743-1750
66. Safari M.R., and Sheikh N. Effects of flavonoids on the susceptibility of low-density lipoprotein to oxidative modification. Prostaglandins Leukot. Essent. Fatty Acids 69 (2003) 73-77
67. Naderi G.A., Asgary S., Sarraf-Zadegan N., and Shirvany H. Anti-oxidant effect of flavonoids on the susceptibility of LDL oxidation. Mol. Cell. Biochem. 246 (2003) 193-196
68. (2+)-mediated oxidative modification of low density lipoprotein. Biol. Pharm. Bull. 18 (1995) 1-4
69. Steinbrecher U.P., Witztum J.L., Parthasarathy S., and Steinberg D. Decrease in reactive amino groups during oxidation or endothelial cell modification of LDL. Correlation with changes in receptor-mediated catabolism. Arteriosclerosis 7 (1987) 135-143
70. Steinberg D. Low density lipoprotein oxidation and its pathobiological significance. J. Biol. Chem. 272 (1997) 20963-20966
71. Esterbauer H. Cytotoxicity and genotoxicity of lipid-oxidation products. Am. J. Clin. Nutr. 57 (1993) 779S-785S discussion 785S-786S
72. Tuomisto T.T., Riekkinen M.S., Viita H., Levonen A.-L., and Yl?Herttuala S. Analysis of gene and protein expression during monocyte-macrophage differentiation and cholesterol loading-cDNA and protein array study. Atherosclerosis 180 (2005) 283-291
73. Zhang J., Chu W., and Crandall I. Lipoprotein binding preference of CD36 is altered by filipin treatment. Lipids Health Dis. 7 (2008) 23
74. Klein D. Quantification using real-time PCR technology: applications and limitations. Trends Mol. Med. 8 (2002) 257-260
75. Munteanu A., Taddei M., Tamburini I., Bergamini E., Azzi A., and Zingg J.-M. Antagonistic effects of oxLDL and alpha-tocopherol on CD36 scavenger receptor expression in monocytes; involvement of PKB and PPARgamma. J. Biol. Chem. 281 (2006) 6489-6497
76. Schwende H., Fitzke E., Ambs P., and Dieter P. Differences in the state of differentiation of THP-1 cells induced by phorbol ester and 1,25-dihydroxyvitamin D3. J. Leukoc. Biol. 59 (1996) 555-561
77. Koga N., Matsuo M., Ohta C., Haraguchi K., Matsuoka M., Kato Y., Ishii T., Yano M., and Ohta H. Comparative study on nobiletin metabolism with liver microsomes from rats, guinea gigs and hamsters and rat cytochrome P450. Biol. Pharm. Bull. 30 (2007) 2317-2323