Ginkgo biloba extract attenuates oxLDL-induced oxidative functional damages in endothelial cells

Journal of Applied Physiology

Volumn 106, Issue 5, 2009, Pages 1674-1685

  Ou, Hsiu Chung ^a   Lee, Wen Jane ^b   Lee, I Te ^b   Chiu, Tsan Hung ^c   Tsai, Kun Ling ^a   Lin, Chih Ying ^a   Sheu, Wayne Huey Herng ^b,d,e,f  

^a CHINA MEDICAL UNIVERSITY   (Taiwan)

^b TAICHUNG VETERANS GENERAL HOSPITAL   (Taiwan)

^c CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^d NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^e CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

^f NATIONAL YANG MING UNIVERSITY   (Taiwan)

Author keywords

Adhesion molecule; Apoptosis; Endothelium; Reactive oxygen species

Indexed keywords

CASPASE 3; COPPER ZINC SUPEROXIDE DISMUTASE; CYTOCHROME C; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; GINKGO BILOBA EXTRACT; INTERCELLULAR ADHESION MOLECULE 1; MAGNESIUM SUPEROXIDE DISMUTASE; NITRIC OXIDE SYNTHASE; OXIDIZED LOW DENSITY LIPOPROTEIN; PROTEIN BCL 2; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1;

ARTICLE; CELL ADHESION; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME RELEASE; HUMAN; HUMAN CELL; IN VITRO STUDY; MEMBRANE PERMEABILITY; MITOCHONDRIAL MEMBRANE POTENTIAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; UMBILICAL VEIN;

ANTIOXIDANTS; APOPTOSIS; CELL ADHESION; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG ANTAGONISM; ENDOTHELIUM, VASCULAR; GINKGO BILOBA; HUMANS; LIPOPROTEINS, LDL; NITRIC OXIDE SYNTHASE TYPE III; OXIDATION-REDUCTION; OXIDATIVE STRESS; PLANT EXTRACTS; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE; UMBILICAL CORD;

EID: 66349092844     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.91415.2008     Document Type: Article

References (61)

1. Babior BM. The NADPH oxidase of endothelial cells. IUBMB Life 50: 267-269, 2000. (Pubitemid 32289084)
2. Bao M, Lou Y. Isorhamnetin prevents endothelial cell injuries from oxidized LDL via activation of p38MAPK. Eur J Pharmacol 547: 22-30, 2006. (Pubitemid 44373898)
3. Bedner E, Li X, Gorczyca W, Melamed MR, Darzynkiewicz Z. Analysis of apoptosis by laser scanning cytometry. Cytometry 35: 181-195, 1999. (Pubitemid 29104396)
4. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254, 1976.
5. Cai H, Griendling KK, Harrison DG. The vascular NAD(P)H oxidases as therapeutic targets in cardiovascular diseases. Trends Pharmacol Sci 24: 471-478, 2003. (Pubitemid 37088172)
6. Chen JW, Chen YH, Lin FY, Chen YL, Lin SJ. Ginkgo biloba extract inhibits tumor necrosis factor-α-induced reactive oxygen species generation, transcription factor activation, and cell adhesion molecule expression in human aortic endothelial cells. Arterioscler Thromb Vasc Biol 23: 1559-1566, 2003. (Pubitemid 37108198)
7. Chen XP, Xun KL, Wu Q, Zhang TT, Shi JS, Du GH. Oxidized low density lipoprotein receptor-1 mediates oxidized low density lipoprotein-induced apoptosis in human umbilical vein endothelial cells: role of reactive oxygen species. Vascul Pharmacol 47: 1-9, 2007. (Pubitemid 46830770)
8. Chen XP, Zhang TT, Du GH. Lectin-like oxidized low-density lipoprotein receptor-1, a new promising target for the therapy of atherosclerosis? Cardiovasc Drug Rev 25: 146-161, 2007. (Pubitemid 47035426)
9. Crespo I, Garcia-Mediavilla MV, Gutierrez B, Sanchez-Campos S, Tunon MJ, Gonzalez-Gallego J. A comparison of the effects of kaempferol and quercetin on cytokine-induced pro-inflammatory status of cultured human endothelial cells. Br J Nutr 100: 968-976, 2008.
10. De Graaf JC, Banga JD, Moncada S, Palmer RM, de Groot PG, Sixma JJ. Nitric oxide functions as an inhibitor of platelet adhesion under flow conditions. Circulation 85: 2284-2290, 1992.
11. Denizot F, Lang R. Rapid colorimetric assay for cell growth and survival. Modifications to the tetrazolium dye procedure giving improved sensitivity and reliability. J Immunol Methods 89: 271-277, 1986. (Pubitemid 16080782)
12. Diamond BJ, Shiflett SC, Feiwel N, Matheis RJ, Noskin O, Richards JA, Schoenberger NE. Ginkgo biloba extract: mechanisms and clinical indications. Arch Phys Med Rehabil 81: 668-678, 2000. (Pubitemid 30257692)
13. Faraci FM, Didion SP. Vascular protection: superoxide dismutase isoforms in the vessel wall. Arterioscler Thromb Vasc Biol 24: 1367-1373, 2004. (Pubitemid 39050427)
14. Fei R, Fei Y, Zheng S, Gao YG, Sun HX, Zeng XL. Purified polysaccharide from Ginkgo biloba leaves inhibits P-selectin-mediated leukocyte adhesion and inflammation. Acta Pharmacol Sin 29: 499-506, 2008.
15. Galle J, Heinloth A, Wanner C, Heermeier K. Dual effect of oxidized LDL on cell cycle in human endothelial cells through oxidative stress. Kidney Int Suppl 78: S120-S123, 2001. (Pubitemid 32144083)
16. 2+ indicators with greatly improved fluorescence properties. J Biol Chem 260: 3440-3450, 1985.
17. Havel RJ, Eder HA, Bragdon JH. The distribution and chemical composition of ultracentrifugally separated lipoproteins in human serum. J Clin Invest 34: 1345-1353, 1955.
18. Hsieh CC, Yen MH, Yen CH, Lau YT. Oxidized low density lipoprotein induces apoptosis via generation of reactive oxygen species in vascular smooth muscle cells. Cardiovasc Res 49: 135-145, 2001.
19. Jaffe EA, Nachman RL, Becker CG, Minick CR. Culture of human endothelial cells derived from umbilical veins. Identification by morphologic and immunologic criteria. J Clin Invest 52: 2745-2756, 1973.
20. 2. Free Radic Biol Med 26: 905-918, 1999.
21. Kim JA, Territo MC, Wayner E, Carlos TM, Parhami F, Smith CW, Haberland ME, Fogelman AM, Berliner JA. Partial characterization of leukocyte binding molecules on endothelial cells induced by minimally oxidized LDL. Arterioscler Thromb 14: 427-433, 1994. (Pubitemid 24083859)
22. Koltermann A, Hartkorn A, Koch E, Furst R, Vollmar AM, Zahler S. Ginkgo biloba extract EGb 761 increases endothelial nitric oxide production in vitro and in vivo. Cell Mol Life Sci 64: 1715-1722, 2007. (Pubitemid 47036943)
23. Kubes P, Suzuki M, Granger DN. Nitric oxide: an endogenous modulator of leukocyte adhesion. Proc Natl Acad Sci USA 88: 4651-4655, 1991. (Pubitemid 21914599)
24. Lan WJ, Zheng XX. Activity of Ginkgo biloba extract and quercetin on thrombomodulin expression and tissue-type plasminogen activator secretion by human umbilical vein endothelial cells. Biomed Environ Sci 19: 249-253, 2006. (Pubitemid 44505560)
25. Le Bars PL, Katz MM, Berman N, Itil TM, Freedman AM, Schatzberg AF. A placebo-controlled, double-blind, randomized trial of an extract of Ginkgo biloba for dementia. North American EGb Study Group. JAMA 278: 1327-1332, 1997. (Pubitemid 27449692)
26. Li D, Yang B, Mehta JL. Ox-LDL induces apoptosis in human coronary artery endothelial cells: role of PKC, PTK, bcl-2, and Fas. Am J Physiol Heart Circ Physiol 275: H568-H576, 1998. (Pubitemid 28394822)
27. Li JM, Shah AM. Endothelial cell superoxide generation: regulation and relevance for cardiovascular pathophysiology. Am J Physiol Regul Integr Comp Physiol 287: R1014-R1030, 2004. (Pubitemid 39391043)
28. Lin FY, Chen YH, Chen YL, Wu TC, Li CY, Chen JW, Lin SJ. Ginkgo biloba extract inhibits endotoxin-induced human aortic smooth muscle cell proliferation via suppression of Toll-like receptor 4 expression and NADPH oxidase activation. J Agric Food Chem 55: 1977-1984, 2007.
29. Lin SJ, Shyue SK, Liu PL, Chen YH, Ku HH, Chen JW, Tam KB, Chen YL. Adenovirus-mediated overexpression of catalase attenuates oxLDL-induced apoptosis in human aortic endothelial cells via AP-1 and C-Jun N-terminal kinase/extracellular signal-regulated kinase mitogen-activated protein kinase pathways. J Mol Cell Cardiol 36: 129-139, 2004. (Pubitemid 38084798)
30. Littlewood TD, Bennett MR. Apoptotic cell death in atherosclerosis. Curr Opin Lipidol 14: 469-475, 2003. (Pubitemid 37297301)
31. Liu KX, He W, Rinne T, Liu Y, Zhao MQ, Wu WK. The effect of Ginkgo biloba extract (EGb 761) pretreatment on intestinal epithelial apoptosis induced by intestinal ischemia/reperfusion in rats: role of ceramide. Am J Chin Med 35: 805-819, 2007. (Pubitemid 350028176)
32. Liu TJ, Yeh YC, Ting CT, Lee WL, Wang LC, Lee HW, Wang KY, Lai HC, Lai HC. Ginkgo biloba extract 761 reduces doxorubicin-induced apoptotic damage in rat hearts and neonatal cardiomyocytes. Cardiovasc Res 80: 227-235, 2008.
33. Madamanchi NR, Vendrov A, Runge MS. Oxidative stress and vascular disease. Arterioscler Thromb Vasc Biol 25: 29-38, 2005. (Pubitemid 40054251)
34. Matsui T, Yamagishi S, Nakamura K, Inoue H, Takeuchi M. Nifedipine, a calcium-channel blocker, inhibits advanced glycation end-product-induced expression of monocyte chemoattractant protein-1 in human cultured mesangial cells. J Int Med Res 35: 107-112, 2007. (Pubitemid 46477534)
35. Morgenstern C, Biermann E. The efficacy of Ginkgo special extract EGb 761 in patients with tinnitus. Int J Clin Pharmacol Ther 40: 188-197, 2002. (Pubitemid 34467677)
36. Muir AH, Robb R, McLaren M, Daly F, Belch JJ. The use of Ginkgo biloba in Raynaud's disease: a double-blind placebo-controlled trial. Vasc Med 7: 265-267, 2002. (Pubitemid 36469489)
37. Mukherjee S, Coaxum SD, Maleque M, Das SK. Effects of oxidized low-density lipoprotein on nitric oxide synthetase and protein kinase C activities in bovine endothelial cells. Cell Mol Biol (Noisy-le-grand) 47: 1051-1058, 2001.
38. Naik SR, Panda VS. Antioxidant and hepatoprotective effects of Ginkgo biloba phytosomes in carbon tetrachloride-induced liver injury in rodents. Liver Int 27: 393-399, 2007. (Pubitemid 46416631)
39. Ohta H, Wada H, Niwa T, Kirii H, Iwamoto N, Fujii H, Saito K, Sekikawa K, Seishima M. Disruption of tumor necrosis factor-alpha gene diminishes the development of atherosclerosis in ApoE-deficient mice. Atherosclerosis 180: 11-17, 2005. (Pubitemid 40501347)
40. Pincemail J, Dupuis M, Nasr C, Hans P, Haag-Berrurier M, Anton R, Deby C. Superoxide anion scavenging effect and superoxide dismutase activity of Ginkgo biloba extract. Experientia 45: 708-712, 1989. (Pubitemid 19198311)
41. Ross R. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature 362: 801-809, 1993. (Pubitemid 23132154)
42. Salvayre R, Auge N, Benoist H, Negre-Salvayre A. Oxidized low-density lipoprotein-induced apoptosis. Biochim Biophys Acta 1585: 213-221, 2002. (Pubitemid 36092085)
43. Schmitt A, Salvayre R, Delchambre J, Negre-Salvayre A. Prevention by alpha-tocopherol and rutin of glutathione and ATP depletion induced by oxidized LDL in cultured endothelial cells. Br J Pharmacol 116: 1985-1990, 1995.
44. Schneider R, Welt K, Aust W, Loster H, Fitzl G. Cardiac ischemia and reperfusion in spontaneously diabetic rats with and without application of EGb 761. I. Cardiomyocytes. Histol Histopathol 23: 807-817, 2008.
45. Sigurdardottir V, Fagerberg B, Hulthe J. Circulating oxidized low-density lipoprotein (LDL) is associated with risk factors of the metabolic syndrome and LDL size in clinically healthy 58-year-old men (AIR study). J Intern Med 252: 440-447, 2002. (Pubitemid 36706575)
46. Soulie C, Nicole A, Christen Y, Ceballos-Picot I. The Ginkgo biloba extract EGb 761 increases viability of hnt human neurons in culture and affects the expression of genes implicated in the stress response. Cell Mol Biol (Noisy-le-grand) 48: 641-646, 2002.
47. Tang F, Wu X, Wang T, Wang P, Li R, Zhang H, Gao J, Chen S, Bao L, Huang H, Liu P. Tanshinone II A attenuates atherosclerotic calcification in a rat model by inhibition of oxidative stress. Vascul Pharmacol 46: 427-438, 2007. (Pubitemid 46552282)
48. Telford WG, Komoriya A, Packard BZ. Detection of localized caspase activity in early apoptotic cells by laser scanning cytometry. Cytometry 47: 81-88, 2002. (Pubitemid 34117037)
49. Toshima SI, Hasegawa A, Kurabayashi M, Itabe H, Takano T, Sugano J, Shimamura K, Kimura J, Michishita I, Suzuki T, Nagai R. Circulating oxidized low density lipoprotein levels: a biochemical risk marker for coronary heart disease. Arterioscler Thromb Vasc Biol 20: 2243-2247, 2000.
50. Tunali-Akbay T, Sener G, Salvarli H, Sehirli O, Yarat A. Protective effects of Ginkgo biloba extract against mercury(II)-induced cardiovascular oxidative damage in rats. Phytother Res 21: 26-31, 2007. (Pubitemid 46173904)
51. Vendrov AE, Madamanchi NR, Hakim ZS, Rojas M, Runge MS. Thrombin and NAD(P)H oxidase-mediated regulation of CD44 and BMP4-Id pathway in VSMC, restenosis, and atherosclerosis. Circ Res 98: 1254-1263, 2006. (Pubitemid 43948080)
52. Vindis C, Elbaz M, Escargueil-Blanc I, Auge N, Heniquez A, Thiers JC, Negre-Salvayre A, Salvayre R. Two distinct calcium-dependent mitochondrial pathways are involved in oxidized LDL-induced apoptosis. Arterioscler Thromb Vasc Biol 25: 639-645, 2005. (Pubitemid 40315691)
53. Vora DK, Fang ZT, Liva SM, Tyner TR, Parhami F, Watson AD, Drake TA, Territo MC, Berliner JA. Induction of P-selectin by oxidized lipoproteins: separate effects on synthesis and surface expression. Circ Res 80: 810-818, 1997. (Pubitemid 27230055)
54. Wu Y, Li S, Cui W, Zu X, Du J, Wang F. Ginkgo biloba extract improves coronary blood flow in healthy elderly adults: role of endothelium-dependent vasodilation. Phytomedicine 15: 164-169, 2008.
55. Yla-Herttuala S, Palinski W, Rosenfeld ME, Steinberg D, Witztum JL. Lipoproteins in normal and atherosclerotic aorta. Eur Heart J 11, Suppl E: 88-99, 1990. (Pubitemid 20287945)
56. Wu YZ, Li SQ, Zu XG, Du J, Wang FF. Ginkgo biloba extract improves coronary artery circulation in patients with coronary artery disease: contribution of plasma nitric oxide and endothelin-1. Phytother Res 22: 734-739, 2008.
57. Zeiher AM, Fisslthaler B, Schray-Utz B, Busse R. Nitric oxide modulates the expression of monocyte chemoattractant protein-1 in cultured human endothelial cells. Circ Res 76: 980-986, 1995.
58. Zhang L, Rui YC, Yang PY, Qiu Y, Li TJ, Liu HC. Inhibitory effects of Ginkgo biloba extract on vascular endothelial growth factor in rat aortic endothelial cells. Acta Pharmacol Sin 23: 919-923, 2002.
59. Zhang Y, Chen AY, Li M, Chen C, Yao Q. Ginkgo biloba extract kaempferol inhibits cell proliferation and induces apoptosis in pancreatic cancer cells. J Surg Res 148: 17-23, 2008.
60. Zhou W, Chai H, Lin PH, Lumsden AB, Yao Q, Chen C. Clinical use and molecular mechanisms of action of extract of Ginkgo biloba leaves in cardiovascular diseases. Cardiovasc Drug Rev 22: 309-319, 2004. (Pubitemid 40123300)
61. Zhu QX, Shen T, Tu DY, Ding R, Liang ZZ, Zhang XJ. Protective effects of Ginkgo biloba leaf extracts on trichloroethylene-induced human keratinocyte cytotoxicity and apoptosis. Skin Pharmacol Physiol 18: 160-169, 2005. (Pubitemid 40869126)