Probucol enhances selective uptake of HDL-associated cholesteryl esters in vitro by a scavenger receptor B-I-dependent mechanism

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 19, Issue 5, 1999, Pages 1325-1332

  Rinninger, Franz ^a,b   Wang, Nan ^a   Ramakrishnan, Rajasekhar ^a   Jiang, Xian Cheng ^a   Tall, Alan R ^a,c  

^a New York Presbyterian Columbia University Medical Center   (United States)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^c Department of Medicine ^*  (United States)

Author keywords

HDL; Probucol; Scavenger receptor BI; Selective uptake

Indexed keywords

CHOLESTEROL ESTER; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; PROBUCOL; SCAVENGER RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTERY WALL; ARTICLE; ATHEROSCLEROSIS; CHO CELL; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; FEMALE; LIVER METABOLISM; MOUSE; NONHUMAN; ORAL DRUG ADMINISTRATION; PRIORITY JOURNAL; RESTENOSIS; STEROIDOGENESIS;

EID: 0032941071     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.ATV.19.5.1325     Document Type: Article

References (56)

1. Johnson WJ, Mahlberg FH, Rothblat GH, Phillips, MC. Cholesterol transport between cells and high-density lipoproteins. Biochim Biophys Acta. 1991;1085:273-298.
2. Oram JF, Yokoyama S. Apolipoprotein-mediated removal of cellular cholesterol and phospholipids. J Lipid Res. 1996;37:2473-2491.
3. Tall AR. Plasma lipid transfer proteins. Annu Rev Biochem. 1995;64: 235-257.
4. Glass CK, Pittman RC, Civen M, Steinberg D. Uptake of high-density lipoprotein-associated apoprotein A-I and cholesterol esters by 16 tissues of the rat in vivo and by adrenal cells and hepatocytes in vitro. J Biol Chem. 1985;260:744-750.
5. Pittman RC, Knecht TP, Rosenbaum MS, Taylor CA Jr. A non-endocytotic mechanism for the selective uptake of high density lipoprotein-associated cholesterol esters. J Biol Chem. 1987;262: 2443-2450.
6. Acton S, Rigotti A, Landschulz KT, Xu S, Hobbs HH, Krieger M. Identification of scavenger receptor SR-BI as a high density lipoprotein receptor. Science. 1996;271:518-520.
7. Babitt J, Trigatti B, Rigotti A, Smart EJ, Anderson RGW, Xu S, Krieger M. Murine SR-BI, a high density lipoprotein receptor that mediates selective lipid uptake, is N-glycosylated and fatty acylated and colocalizes with plasma membrane caveolae. J Biol Chem. 1997;272: 13242-13249.
8. Khoo JC, Pittman RC, Rubin EM. Selective uptake of HDL cholesteryl esters is active in transgenic mice expressing human apolipoprotein A-I. J Lipid Res. 1995;36:593-600.
9. Landschulz KT, Pathak RK, Rigotti A, Krieger M, Hobbs HH. Regulation of scavenger receptor, class B, type I, a high density lipoprotein receptor, in liver and steroidogenic tissues of rats. J Clin Invest. 1996;98:984-995.
10. Wang N, Weng W, Breslow JL, Tall AR. Scavenger receptor BI (SR-BI) is up-regulated in adrenal gland in apolipoprotein A-I and hepatic lipase knock-out mice as a response to depletion of cholesterol stores. J Biol Chem. 1996;271:21001-21004.
11. Rigotti A, Edelman ER, Seifert P, Iqbal SN, DeMattos RB, Temel RE, Krieger M, Williams DL. Regulation by adrenocorticotrophic hormone of the in vivo expression of scavenger receptor class B type I (SR-BI), a high density lipoprotein receptor, in steroidogenic cells of the murine adrenal gland. J Biol Chem. 1996;271:33545-33549.
12. Kozarsky KF, Donahee MH, Rigotti A, Iqbal SN, Edelman ER, Krieger M. Overexpression of the HDL receptor SR-BI alters plasma HDL and bile cholesterol levels. Nature. 1997;387:414-417.
13. Rigotti A, Trigatti BL, Penman M, Rayburn H, Herz J, Krieger M. A targeted mutation in the gene encoding the high density lipoprotein (HDL) receptor scavenger receptor class B type I reveals its key role in HDL metabolism. Proc Natl Acad Sci U S A. 1997;94:12610-12615.
14. Varban ML, Rinninger F, Wang N, Fairchild-Huntress V, Dunmore JH, Fang Q, Gosselin ML, Dixon KL, Deeds JD, Acton SL, Tall AR, Huszar D. Targeted mutation reveals a central role for SR-BI in hepatic selective uptake of HDL cholesterol. Proc Natl Acad Sci U S A. 1998;95: 4619-4624.
15. Nestel PJ, Billington T. Effects of probucol on low density lipoprotein removal and high density lipoprotein synthesis. Atherosclerosis. 1981;38: 203-209.
16. McLean LR, Thomas CE, Weintraub B, Hagaman KA. Modulation of the physical state of cellular cholesteryl esters by 4,4′-(isopropylidenedithio)bis(2,6-di-t-butylphenol) (probucol). J Biol Chem. 1992;267:12291-12298.
17. Kesäniemi YA, Grundy SM. Influence of probucol on cholesterol and lipoprotein metabolism in man. J Lipid Res. 1984;25:780-790.
18. Hayek T, Chajek-Shaul T, Walsh A, Azrolan N, Breslow JL. Probucol decreases apolipoprotein A-I transport rate and increases high density lipoprotein cholesteryl ester fractional catabolic rate in control and human apolipoprotein A-I transgenic mice. Arterioscler Thromb. 1991;11: 1295-1302.
19. Richard BM, Pfeuffer MA, Pittman RC. Transport of HDL cholesterol esters to the liver is not diminished by probucol treatment in rats. Arterioscler Thromb. 1992;12:862-869.
20. Pfeuffer MA, Richard BM, Pittman RC. Probucol increases the selective uptake of HDL cholesterol esters by Hep G2 human hepatoma cells. Arterioscler Thromb. 1992;12:870-878.
21. Parthasarathy S, Young SG, Witztum JL, Pittman RC, Steinberg D. Probucol inhibits oxidative modification of low density lipoprotein. J Clin Invest. 1986;77:641-644.
22. Carew TE, Schwenke DC, Steinberg D. Antiatherogenic effect of probucol unrelated to its hypocholesterolemic effect: evidence that antioxidants in vivo can selectively inhibit low density lipoprotein degradation in macrophage-rich fatty streaks slowing the progression of atherosclerosis in the Watanabe heritable hyperlipidemic (WHHL) rabbit. Proc Natl Acad Sci U S A. 1987;84:7725-7729.
23. Witztum JL, Steinberg D. Role of oxidized low density lipoprotein in atherogenesis. J Clin Invest. 1991;88:1785-1792.
24. Tardif JC, Coté G, Lespérance J, Bourassa M, Lambert J, Doucet S, Bilodeau L, Nattel S, De Guise P. Probucol and multivitamins in the prevention of restenosis after coronary angioplasty. N Engl J Med. 1997; 337:365-372.
25. Havel RJ, Eder HA, Bragdon JH. The distribution and chemical composition of ultracentrifugally separated lipoproteins in human serum. J Clin Invest. 1955;34:1345-1353.
26. Pittman RC, Taylor CA. Methods for assessment of tissue sites of lipoprotein degradation. Methods Enzymol. 1986;129:612-627.
27. Rinninger F, Brundert M, Jäckle S, Galle PR, Busch C, Izbicki JR, Rogiers X, Henne-Bruns D, Kremer B, Broelsch CE, Greten H. Selective uptake of high-density lipoprotein-associated cholesteryl esters by human hepatocytes in primary culture. Hepatology. 1994;19:1100-1114.
28. Bellamy MF, Nealis AS, Aitken JW, Bruckdorfer KR, Perkins SJ. Structural changes in oxidised low-density lipoproteins and the effect of the antiatherosclerotic drug probucol observed by synchrotron x-ray and neutron solutions scattering. Eur J Biochem. 1989;183:321-329.
29. Tsujita M, Yokoyama S. Selective inhibition of free apolipoprotein-mediated cellular lipid efflux by probucol. Biochemistry. 1996;35: 13011-13020.
30. Folch J, Lees M, Sloane Stanley GH. A simple method for preparation of total pure lipid extracts from brain. Fed Proc. 1954;13:209. Abstract.
31. Rinninger F, Pittman RC. Regulation of the selective uptake of high density lipoprotein-associated cholesteryl esters. J Lipid Res. 1987;28: 1313-1325.
32. Dole VP. A relation between non-esterified fatty acids in plasma and the metabolism of glucose. J Clin Invest. 1956;35:150-154.
33. Goldberg IJ, Blaner WS, Vanni TM, Moukides M, Ramakrishnan, R. Role of lipoprotein lipase in the regulation of high density lipoprotein apolipoprotein metabolism. J Clin Invest. 1990;86:463-473.
34. Ji Y, Jian B, Wang N, Sun Y, de la Liera Moya M, Phillips MC, Rothblat GH, Swaney JB, Tall AR. Scavenger receptor BI promotes high density lipoprotein-mediated cellular cholesterol efflux. J Biol Chem. 1997;272: 20982-20985.
35. Schimmer BP. Adrenocortical Y1 cells. Methods Enzymol. 1979;58: 570-574.
36. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin reagent. J Biol Chem. 1957;193:265-275.
37. Nichols AV, Krauss RM, Musliner T. Non-denaturing polyacrylamide gel electrophoresis. Methods Enzymol. 1986;128:417-431.
38. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227:680-685.
39. Ishigami M, Yamashiata S, Sakai N, Hirano KI, Arai R, Maruyama T, Takami S, Koyama M, Kameda-Takemura K, Matsuzawa Y. High-density lipoproteins from probucol-treated patients have increased capacity to promote cholesterol efflux from mouse peritoneal macrophages loaded with acetylated low-density lipoproteins. Eur J Clin Invest. 1997;27:285-292.
40. Kita T, Nagano Y, Yokode M, Ishii K, Kume N, Oshima A, Yoshida H, Kawai C. Probucol prevents the progression of atherosclerosis in Watanabe heritable hyperlipidemic rabbit, an animal model for familial hypercholesterolemia. Proc Natl Acad Sci U S A. 1987;84:5928-5931.
41. Sasahara M, Raines EW, Chait A, Carew TE, Steinberg D, Wahl PW, Ross R. Inhibition of hypercholesterolemia-induced atherosclerosis in the nonhuman primate by probucol: is the extent of atherosclerosis related to resistance of LDL to oxidation? J Clin Invest. 1994;94:155-164.
42. Temel RE, Trigatti B, DeMattos RB, Azhar S, Krieger M, Williams DL. Scavenger receptor class B, type I (SR-BI) is the major route for the delivery of high density lipoprotein cholesterol to the steroidogenic pathway in cultured mouse adrenocortical cells. Proc Natl Acad Sci U S A. 1997;94:13600-13605.
43. Deckelbaum RJ, Shipley GG, Samll DM. Structure and interactions of lipids in human plasma low density lipoproteins. J Biol Chem. 1977;252: 744-754.
44. Fruebis J, Steinberg D, Dresel HA, Carew TE. A comparison of the antiatherogenic effects of probucol and of a structural analogue of probucol in low density lipoprotein-deficient rabbits. J Clin Invest. 1994; 94:392-398.
45. Feher MD, Webb JC, Patel DD, Lant AF, Mayne PD, Knight BL, Soutar AK. Cholesterol-lowering drug therapy in a patient with receptor-negative homozygous familial hypercholesterolemia. Atherosclerosis. 1993;103:171-180.
46. Naruszewicz M, Carew TE, Pittman RC, Witztum JL, Steinberg D. A novel mechanism by which probucol lowers low density lipoprotein levels demonstrated in the LDL receptor-deficient rabbit. J Lipid Res. 1984;25:1206-1212.
47. Acton SL, Scherer PE, Lodish HF, Krieger M. Expression cloning of SR-BI, a CD36-related class B scavenger receptor. J Biol Chem. 1994; 269:21003-21009.
48. Wang N, Arai T, Ji Y, Rinninger F, Tall AR. Transgenic mice with liver-specific overexpression of scavenger receptor BI show markedly decreased VLDL and LDL apoB levels on chow and high fat diets, as well as reduced HDL levels. J Biol Chem. 1998;273:32920-32926.
49. Yamamoto A, Matsuzawa Y, Yokoyama S, Funahashi T, Yamamura T, Kishino BI. Effects of probucol on xanthomata regression in familial hypercholesterolemia. Am J Cardiol. 1986;57:29H-35H.
50. Regnström J, Walldius G, Nilsson S, Elinder LS, Johansson J, Molgaard J, Holme I, Olsson AG, Nilsson J. The effect of probucol on low density lipoprotein oxidation and femoral atherosclerosis. Atherosclerosis. 1996; 125:217-229.
51. Zhang SH, Reddick RL, Avdievich E, Surles LK, Jones RG, Reynolds JB, Quarfordt SH, Maeda N. Paradoxical enhancement of atherosclerosis by probucol treatment in apolipoprotein E-deficient mice. J Clin Invest. 1997;99:2858-2866.
52. O'Brien K, Nagano Y, Gown A, Kita T, Chait A. Probucol treatment affects the cellular composition but not antioxidized low density lipoprotein immunoreactivity of plaques from Watanabe heritable hyperlipidemic rabbits. Arterioscler Thromb. 1991;11:751-759.
53. Chang MY, Sasahara M, Chait A, Raines EW, Ross R. Inhibition of hypercholesterolemia-induced atherosclerosis in the nonhuman primate by probucol, II: cellular composition and proliferation. Arterioscler Thromb Vasc Biol. 1995;15:1631-1640.
54. Shaish A, Daugherty A, O'Sullivan F, Schonfeld G, Heineke JW. β-Carotene inhibits atherosclerosis in hypercholesterolemic rabbits. J Clin Invest. 1995;96:2075-2082.
55. Fruebis J, Carew TE, Palinski W. Effect of vitamin E on atherogenesis in LDL receptor-deficient rabbits. Atherosclerosis. 1995;117:217-224.
56. McPherson R, Hogue M, Milne RW, Tall AR, Marcel YL. Increase in plasma cholesteryl ester transfer protein during probucol treatment. Arterioscler Thromb. 1991;11:476-481.