Salvianolic acid B inhibits macrophage uptake of modified low density lipoprotein (mLDL) in a scavenger receptor CD36-dependent manner

Atherosclerosis

Volumn 223, Issue 1, 2012, Pages 152-159

  Bao, Yi ^a,b   Wang, Li ^a   Xu, Yanni ^a   Yang, Yuan ^a   Wang, Lifei ^a   Si, Shuyi ^a   Cho, Sunghee ^b,c   Hong, Bin ^a  

^a INSTITUTE OF MEDICINAL BIOTECHNOLOGY   (China)

^b Burke Cornell Medical Research Institute   (United States)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Antagonist; Atherosclerosis; CD36; Modified LDL; Salvianolic acid B; Scavenger receptor class B

Indexed keywords

CD36 ANTIGEN; LOW DENSITY LIPOPROTEIN; MODIFIED LOW DENSITY LIPOPROTEIN; SALVIANOLIC ACID B; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CHO CELL; DRUG EFFICACY; DRUG PROTEIN BINDING; DRUG SPECIFICITY; HUMAN; HUMAN CELL; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TRANSPORT; SURFACE PLASMON RESONANCE;

ANIMALS; ANTIGENS, CD36; APOLIPOPROTEINS E; ATHEROSCLEROSIS; BENZOFURANS; BIOLOGICAL TRANSPORT; CELL LINE, TUMOR; CHO CELLS; CRICETINAE; CRICETULUS; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; HYPERLIPIDEMIAS; HYPOLIPIDEMIC AGENTS; LIPOPROTEINS, LDL; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, LDL; RNA INTERFERENCE; SURFACE PLASMON RESONANCE; TETRADECANOYLPHORBOL ACETATE; TIME FACTORS; TRANSFECTION;

EID: 84863225033     PISSN: 00219150     EISSN: 18791484     Source Type: Journal    
DOI: 10.1016/j.atherosclerosis.2012.05.006     Document Type: Article

References (53)

1. Greaves D.R., Gordon S. The macrophage scavenger receptor at 30 years of age: current knowledge and future challenges. J Lipid Res 2009, 50(Suppl):S282-S286.
2. Kunjathoor V.V., Febbraio M., Podrez E.A., Moore K.J., Andersson L., Koehn S., et al. 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 2002, 277:49982-49988.
3. Kuchibhotla S., Vanegas D., Kennedy D.J., Guy E., Nimako G., Morton R.E., et al. Absence of CD36 protects against atherosclerosis in ApoE knock-out mice with no additional protection provided by absence of scavenger receptor A I/II. Cardiovasc Res 2008, 78:185-196.
4. Febbraio M., Podrez E.A., Smith J.D., Hajjar D.P., Hazen S.L., Hoff H.F., et al. Targeted disruption of the class B scavenger receptor CD36 protects against atherosclerotic lesion development in mice. J Clin Invest 2000, 105:1049-1056.
5. Moore K.J., Kunjathoor V.V., Koehn S.L., Manning J.J., Tseng A.A., Silver J.M., et al. Loss of receptor-mediated lipid uptake via scavenger receptor A or CD36 pathways does not ameliorate atherosclerosis in hyperlipidemic mice. J Clin Invest 2005, 115:2192-2201.
6. Guy E., Kuchibhotla S., Silverstein R., Febbraio M. Continued inhibition of atherosclerotic lesion development in long term western diet fed CD36o/apoEo mice. Atherosclerosis 2007, 192:123-130.
7. Febbraio M., Guy E., Silverstein R.L. Stem cell transplantation reveals that absence of macrophage CD36 is protective against atherosclerosis. Arterioscler Thromb Vasc Biol 2004, 24:2333-2338.
8. Witztum J.L. You are right too!. J Clin Invest 2005, 115:2072-2075.
9. Kim E., Tolhurst A.T., Qin L.Y., Chen X.Y., Febbraio M., Cho S. CD36/fatty acid translocase, an inflammatory mediator, is involved in hyperlipidemia-induced exacerbation in ischemic brain injury. J Neurosci 2008, 28:4661-4670.
10. Cho S., Park E.M., Febbraio M., Anrather J., Park L., Racchumi G., et al. The class B scavenger receptor CD36 mediates free radical production and tissue injury in cerebral ischemia. J Neurosci 2005, 25:2504-2512.
11. Marleau S., Harb D., Bujold K., Avallone R., Iken K., Wang Y., et al. EP 80317, a ligand of the CD36 scavenger receptor, protects apolipoprotein E-deficient mice from developing atherosclerotic lesions. FASEB J 2005, 19:1869-1871.
12. Bodart V., Febbraio M., Demers A., McNicoll N., Pohankova P., Perreault A., et al. CD36 mediates the cardiovascular action of growth hormone-releasing peptides in the heart. Circ Res 2002, 90:844-849.
13. Endemann G., Stanton L.W., Madden K.S., Bryant C.M., White R.T., Protter A.A. CD36 is a receptor for oxidized low density lipoprotein. J Biol Chem 1993, 268:11811-11816.
14. Huh H.Y., Pearce S.F., Yesner L.M., Schindler J.L., Silverstein R.L. Regulated expression of CD36 during monocyte-to-macrophage differentiation: potential role of CD36 in foam cell formation. Blood 1996, 87:2020-2028.
15. Abumrad N.A., el-Maghrabi M.R., Amri E.Z., Lopez E., Grimaldi P.A. Cloning of a rat adipocyte membrane protein implicated in binding or transport of long-chain fatty acids that is induced during preadipocyte differentiation. Homology with human CD36. J Biol Chem 1993, 268:17665-17668.
16. Bolin R.B., Medina F., Cheney B.A. Glycoprotein changes in fresh vs. room temperature-stored platelets and their buoyant density cohorts. J Lab Clin Med 1981, 98:500-510.
17. Swerlick R.A., Lee K.H., Wick T.M., Lawley T.J. Human dermal microvascular endothelial but not human umbilical vein endothelial cells express CD36 in vivo and in vitro. J Immunol 1992, 148:78-83.
18. Van Nieuwenhoven F.A., Verstijnen C.P., Abumrad N.A., Willemsen P.H., Van Eys G.J., Van der Vusse G.J. Putative membrane fatty acid translocase and cytoplasmic fatty acid-binding protein are co-expressed in rat heart and skeletal muscles. Biochem Biophys Res Commun 1995, 207:747-752.
19. Ryeom S.W., Sparrow J.R., Silverstein R.L. CD36 participates in the phagocytosis of rod outer segments by retinal pigment epithelium. J Cell Sci 1996, 109(Pt 2):387-395.
20. Ge Y., Elghetany M.T. CD36: a multiligand molecule. Lab Hematol 2005, 11:31-37.
21. Febbraio M., Silverstein R.L. CD36: implications in cardiovascular disease. Int J Biochem Cell Biol 2007, 39:2012-2030.
22. Febbraio M., Hajjar D.P., Silverstein R.L. CD36: a class B scavenger receptor involved in angiogenesis, atherosclerosis, inflammation, and lipid metabolism. J Clin Invest 2001, 108:785-791.
23. Demers A., McNicoll N., Febbraio M., Servant M., Marleau S., Silverstein R., et al. Identification of the growth hormone-releasing peptide binding site in CD36: a photoaffinity cross-linking study. Biochem J 2004, 382:417-424.
24. Avallone R., Demers A., Rodrigue-Way A., Bujold K., Harb D., Anghel S., et al. A growth hormone-releasing peptide that binds scavenger receptor CD36 and ghrelin receptor up-regulates sterol transporters and cholesterol efflux in macrophages through a peroxisome proliferator-activated receptor gamma-dependent pathway. Mol Endocrinol 2006, 20:3165-3178.
25. Szeto H.H. Cell-permeable, mitochondrial-targeted, peptide antioxidants. AAPS J 2006, 8:E277-E283.
26. Zhao K., Zhao G.M., Wu D., Soong Y., Birk A.V., Schiller P.W., et al. Cell-permeable peptide antioxidants targeted to inner mitochondrial membrane inhibit mitochondrial swelling, oxidative cell death, and reperfusion injury. J Biol Chem 2004, 279:34682-34690.
27. Cho S., Szeto H.H., Kim E., Kim H., Tolhurst A.T., Pinto J.T. A novel cell-permeable antioxidant peptide, SS31, attenuates ischemic brain injury by down-regulating CD36. J Biol Chem 2007, 282:4634-4642.
28. Fuhrman B., Volkova N., Aviram M. Oxidative stress increases the expression of the CD36 scavenger receptor and the cellular uptake of oxidized low-density lipoprotein in macrophages from atherosclerotic mice: protective role of antioxidants and of paraoxonase. Atherosclerosis 2002, 161:307-316.
29. Venugopal S.K., Devaraj S., Jialal I. RRR-alpha-tocopherol decreases the expression of the major scavenger receptor, CD36, in human macrophages via inhibition of tyrosine kinase (Tyk2). Atherosclerosis 2004, 175:213-220.
30. Ricciarelli R., Zingg J.M., Azzi A. Vitamin E reduces the uptake of oxidized LDL by inhibiting CD36 scavenger receptor expression in cultured aortic smooth muscle cells. Circulation 2000, 102:82-87.
31. Lian T.W., Wang L., Lo Y.H., Huang I.J., Wu M.J. Fisetin, morin and myricetin attenuate CD36 expression and oxLDL uptake in U937-derived macrophages. Biochim Biophys Acta 2008, 1781:601-609.
32. Lo Y.H., Pan M.H., Li S., Yen J.H., Kou M.C., Ho C.T., 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.
33. Wu Y.J., Hong C.Y., Lin S.J., Wu P., Shiao M.S. Increase of vitamin E content in LDL and reduction of atherosclerosis in cholesterol-fed rabbits by a water-soluble antioxidant-rich fraction of Salvia miltiorrhiza. Arterioscler Thromb Vasc Biol 1998, 18:481-486.
34. Zhou L., Zuo Z., Chow M.S. Danshen: an overview of its chemistry, pharmacology, pharmacokinetics, and clinical use. J Clin Pharmacol 2005, 45:1345-1359.
35. O.K., Lynn E.G., Vazhappilly R., Au-Yeung K.K., Zhu D.Y., Siow Y.L. Magnesium tanshinoate B (MTB) inhibits low density lipoprotein oxidation. Life Sci 2001, 68:903-912.
36. Kang D.G., Oh H., Sohn E.J., Hur T.Y., Lee K.C., Kim K.J., et al. Lithospermic acid B isolated from Salvia miltiorrhiza ameliorates ischemia/reperfusion-induced renal injury in rats. Life Sci 2004, 75:1801-1816.
37. Yang T.L., Lin F.Y., Chen Y.H., Chiu J.J., Shiao M.S., Tsai C.S., et al. Salvianolic acid B inhibits low-density lipoprotein oxidation and neointimal hyperplasia in endothelium-denuded hypercholesterolaemic rabbits. J Sci Food Agric 2011, 91:134-141.
38. Chen Y.L., Hu C.S., Lin F.Y., Chen Y.H., Sheu L.M., Ku H.H., et al. Salvianolic acid B attenuates cyclooxygenase-2 expression in vitro in LPS-treated human aortic smooth muscle cells and in vivo in the apolipoprotein-E-deficient mouse aorta. J Cell Biochem 2006, 98:618-631.
39. Lin S.J., Lee I.T., Chen Y.H., Lin F.Y., Sheu L.M., Ku H.H., et al. Salvianolic acid B attenuates MMP-2 and MMP-9 expression in vivo in apolipoprotein-E-deficient mouse aorta and in vitro in LPS-treated human aortic smooth muscle cells. J Cell Biochem 2007, 100:372-384.
40. Wang Q.L., Tao Y.Y., Yuan J.L., Shen L., Liu C.H. Salvianolic acid B prevents epithelial-to-mesenchymal transition through the TGF-beta1 signal transduction pathway in vivo and in vitro. BMC Cell Biol 2010, 11:31.
41. Wang S.X., Hu L.M., Gao X.M., Guo H., Fan G.W. Anti-inflammatory activity of salvianolic acid B in microglia contributes to its neuroprotective effect. Neurochem Res 2010, 35:1029-1037.
42. Wang L., Bao Y., Yang Y., Wu Y., Chen X., Si S., et al. Discovery of antagonists for human scavenger receptor CD36 via an ELISA-like high-throughput screening assay. J Biomol Screen 2010, 15:239-250.
43. Xu Y., Wang J., Bao Y., Jiang W., Zuo L., Song D., et al. Identification of two antagonists of the scavenger receptor CD36 using a high-throughput screening model. Anal Biochem 2010, 400:207-212.
44. Bao Y., Yang Y., Wang L., Gao L., Jiang W., Wang L., et al. Identification of trichostatin A as a novel transcriptional up-regulator of scavenger receptor BI both in HepG2 and RAW 264.7 cells. Atherosclerosis 2009, 204:127-135.
45. Febbraio M., Abumrad N.A., Hajjar D.P., Sharma K., Cheng W., Pearce S.F., et al. A null mutation in murine CD36 reveals an important role in fatty acid and lipoprotein metabolism. J Biol Chem 1999, 274:19055-19062.
46. Collot-Teixeira S., Martin J., rmott-Roe C., Poston R., McGregor J.L. CD36 and macrophages in atherosclerosis. Cardiovasc Res 2007, 75:468-477.
47. Makinen P.I., Lappalainen J.P., Heinonen S.E., Leppanen P., Lahteenvuo M.T., Aarnio J.V., et al. Silencing of either SR-A or CD36 reduces atherosclerosis in hyperlipidaemic mice and reveals reciprocal upregulation of these receptors. Cardiovasc Res 2010, 88:530-538.
48. Demers A., Rodrigue-Way A., Tremblay A. Hexarelin signaling to PPARgamma in metabolic diseases. PPAR Res 2008, 2008:364784.
49. Podrez E.A., Byzova T.V., Febbraio M., Salomon R.G., Ma Y., Valiyaveettil M., et al. Platelet CD36 links hyperlipidemia, oxidant stress and a prothrombotic phenotype. Nat Med 2007, 13:1086-1095.
50. Stewart C.R., Stuart L.M., Wilkinson K., van Gils J.M., Deng J., Halle A., et al. CD36 ligands promote sterile inflammation through assembly of a Toll-like receptor 4 and 6 heterodimer. Nat Immunol 2010, 11:155-161.
51. Zhou Z., Liu Y., Miao A.D., Wang S.Q. Salvianolic acid B attenuates plasminogen activator inhibitor type 1 production in TNF-alpha treated human umbilical vein endothelial cells. J Cell Biochem 2005, 96:109-116.
52. Chen Y.H., Lin S.J., Ku H.H., Shiao M.S., Lin F.Y., Chen J.W., et al. Salvianolic acid B attenuates VCAM-1 and ICAM-1 expression in TNF-alpha-treated human aortic endothelial cells. J Cell Biochem 2001, 82:512-521.
53. Jia J.Y., Lu Y.L., Li X.C., Liu G.Y., Li S.J., Liu Y., et al. Pharmacokinetics of depside salts from Salvia miltiorrhiza in healthy Chinese volunteers: a randomized, open-label, single-dose study. Curr Ther Res 2010, 71:260-271.