Magnesium tanshinoate B protects endothelial cells against oxidized lipoprotein-induced apoptosis

Canadian Journal of Physiology and Pharmacology

Volumn 85, Issue 11, 2007, Pages 1053-1062

  Au Yeung, Kathy K W ^a   Karmin, O ^a   Choy, Patrick C ^a   Zhu, Da Yuan ^b   Siow, Yaw L ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

^b Shanghai Jiao Tong University Affiliated Sixth People s Hospital   (China)

Author keywords

Antioxidant; Apoptosis; Danshen; JNK signaling pathway; Oxidized lipoproteins

Indexed keywords

CASPASE 3; COPPER; CYTOCHROME C; LIPOPROTEIN; MAGNESIUM TANSHINOATE B; SALVIA MILTIORRHIZA EXTRACT; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; VERY LOW DENSITY LIPOPROTEIN;

ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CELL PROTECTION; CHINESE HERB; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; MEDICINAL PLANT; PRIORITY JOURNAL; PROTEIN SECRETION; SALVIA MILTIORRHIZA; UMBILICAL VEIN;

ANTIOXIDANTS; APOPTOSIS; CASPASE 3; CELLS, CULTURED; CYTOCHROMES C; ENDOTHELIAL CELLS; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LIPOPROTEINS, LDL; MAGNESIUM; PHENANTHROLINES;

EID: 38849085104     PISSN: 00084212     EISSN: None     Source Type: Journal    
DOI: 10.1139/Y07-096     Document Type: Article

References (71)

1. Aggeli, I.K., Gaitanaki, C., and Beis, I. 2006. Involvement of JNKs and p38-MAPK/MSK1 pathways in H2O2-induced upregulation of heme oxygenase-1 mRNA in H9c2 cells. Cell. Signal. 18: 1801-1812. doi:10.1016/j.cellsig.2006.02. 001.
2. Au-Yeung, K.K., Zhu, D.Y., O, K., and Siow, Y.L. 2001. Inhibition of stress-activated protein kinase in the ischemic/reperfused heart: role of magnesium tanshinoate B in preventing apoptosis. Biochem. Pharmacol. 62: 483-493. doi:10.1016/S0006-2952(01)00686-4.
3. Bensky, D., Clavey, S., Stöger, E., Gamble, A., and Lai-Bensky, L. 2004. Chinese herbal medicine: Materia medica. Eastland Press, Seattle, USA. pp. 602-604.
4. Bradford, M.M. 1976. 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. doi:10.1016/0003-2697(76)90527-3.
5. Chen, J., Mehta, J.L., Haider, N., Zhang, X., Narula, J., and Li, D. 2004. Role of caspases in Ox-LDL-induced apoptotic cascade in human coronary artery endothelial cells. Circ. Res. 94: 370-376. doi:10.1161/01.RES. 0000113782.07824.BE.
6. Chikani, G., Zhu, W., and Smart, E.J. 2004. Lipids: potential regulators of nitric oxide generation. Am. J. Physiol. Endocrinol. Metab. 287: E386-E389. doi:10.1152/ajpendo.00106.2004.
7. Cominacini, L., Rigoni, A., Pasini, A.F., Garbin, U., Davoli, A., Campagnola, M., et al. 2001. The binding of oxidized low density lipoprotein (ox-LDL) to ox-LDL receptor-1 reduces the intracellular concentration of nitric oxide in endothelial cells through an increased production of superoxide. J. Biol. Chem. 276: 13750-13755.
8. Davignon, J., Jacob, R.F., and Mason, R.P. 2004. The antioxidant effects of statins. Coron. Artery Dis. 15: 251-258. doi:10.1097/01.mca. 0000131573.31966.34.
9. Degterev, A., Boyce, M., and Yuan, J. 2003. A decade of caspases. Oncogene, 22: 8543-8567. doi:10.1038/sj.onc.1207107.
10. Dichtl, W., Nilsson, L., Goncalves, I., Ares, M.P., Banfi, C., Calara, F., et al. 1999. Very low-density lipoprotein activates nuclear factor-kappaB in endothelial cells. Circ. Res. 84: 1085-1094.
11. Dimmeler, S., Haendeler, J., Galle, J., and Zeiher, A.M. 1997. Oxidized low-density lipoprotein induces apoptosis of human endothelial cells by activation of CPP32-like proteases. A mechanistic clue to the 'response to injury' hypothesis. Circulation, 95: 1760-1763.
12. Force, T., Pombo, C.M., Avruch, J.A., Bonventre, J.V., and Kyriakis, J.M. 1996. Stress-activated protein kinases in cardiovascular disease. Circ. Res. 78: 947-953.
13. Fung, K.P., Zeng, L.H., Wu, J., Wong, H.N., Lee, C.M., Hon, P.M., Chang, H.M., and Wu, T.W. 1993. Demonstration of the myocardial salvage effect of lithospermic acid B isolated from the aqueous extract of Salvia miltiorrhiza. Life Sci. 52: PL239-PL244. doi:10.1016/0024-3205(93)90471-E.
14. Galle, J., Schneider, R., Heinloth, A., Wanner, C., Galle, P.R., Conzelmann, E., Dimmeler, S., and Heermeier, K. 1999. Lp(a) and LDL induce apoptosis in human endothelial cells and in rabbit aorta: role of oxidative stress. Kidney Int. 55: 1450-1461. doi:10.1046/j.1523-1755. 1999.00351.x.
15. Garrington, T.P., and Johnson, G.L. 1999. Organization and regulation of mitogen-activated protein kinase signaling pathways. Curr. Opin. Cell Biol. 11: 211-218. doi:10.1016/S0955-0674(99)80028-3.
16. Glass, C.K., and Witztum, J.L. 2001. Atherosclerosis. the road ahead. Cell, 104: 503-516. doi:10.1016/S0092-8674(01)00238-0.
17. Go, Y.M., Levonen, A.L., Moellering, D., Ramachandran, A., Patel, R.P., Jo, H., and Darley-Usmar, V.M. 2001. Endothelial NOS-dependent activation of c-Jun NH(2)- terminal kinase by oxidized low-density lipoprotein. Am. J. Physiol. Heart Circ. Physiol. 281: H2705-H2713.
18. Green, D.R., and Reed, J.C. 1998. Mitochondria and apoptosis. Science (Washington, D.C.), 281: 1309-1312. doi:10.1126/science.281.5381.1309.
19. Havel, R.J., Eder, H.A., and Bragdon, J.H. 1995. The distribution and chemical composition of ultracentrifugally separated lipoproteins in human serum. J. Clin. Invest. 34: 1345-1353.
20. Heinloth, A., Brune, B., Fischer, B., and Galle, J. 2002. Nitric oxide prevents oxidized LDL-induced p53 accumulation, cytochrome c translocation, and apoptosis in macrophages via guanylate cyclase stimulation. Atherosclerosis, 162: 93-101. doi:10.1016/S0021-9150(01)00687-6.
21. Hu, Y., Cheng, L., Hochleitner, B.W., and Xu, Q. 1997. Activation of mitogen-activated protein kinases (ERK/JNK) and AP-1 transcription factor in rat carotid arteries after balloon injury. Arterioscler. Thromb. Vasc. Biol. 17: 2808-2816.
22. Huang, D., Ou, B., Hampsch-Woodill, M., Flanagan, J.A., and Prior, R.L. 2002. High throughput assay of oxygen radical absorbance capacity (ORAC) using a mutlichannel liquid handling system coupled with a microplate fluorescence reader in 96-well format. J. Agric. Food Chem. 50: 4437-4444. doi:10.1021/jf0201529.
23. Ji, X.Y., Tan, B.K., and Zhu, Y.Z. 2000. Salvia miltiorrhiza and ischemic diseases. Acta Pharmacol. Sin. 21: 1089-1094.
24. Kamata, K., Iizuka, T., Nagai, M., and Kasuya, Y. 1993. Endothelium-dependent vasodilator effects of the extract from Salviae miltiorrhizae radix: A study on the identification of lithospermic acid B in the extracts. Gen. Pharmacol. 24: 977-981.
25. Kamata, K., Noguchi, M., and Nagai, M. 1994. Hypotensive effects of lithospermic acid B isolated from the extract of Salviae miltiorrhizae Radix in the rat. Gen. Pharmacol. 25: 69-73.
26. Kaufmann, S.H., and Hengartner, M.O. 2001. Programmed cell death: alive and well in the new millennium. Trends Cell Biol. 11: 526-534. doi:10.1016/S0962-8924(01)02173-0.
27. Kaur, C., and Kapoor, H.C. 2002. Anti-oxidant activity and total phenolic content of some Asian vegetables. Int. J. Food Sci. Technol. 37: 153-161. doi:10.1046/j.1365-2621.2002.00552.x.
28. Kavurma, M.M., Bhindi, R., Lowe, H.C., Chesterman, C., and Khachigian, L.M. 2005. Vessel wall apoptosis and atherosclerotic plaque instability. J. Thromb. Haemost. 3: 465-472. doi:10.1111/j.1538-7836.2005.01120.x.
29. Kimura, M., Mizukami, Y., Miura, T., Fujimoto, K., Kobayashi, S., and Matsuzaki, M. 2001. Orphan G protein-coupled receptor, GPR41, induces apoptosis via a p53/Bax pathway during ischemic hypoxia and reoxygenation. J. Biol. Chem. 276: 26453-26460. doi:10.1074/jbc.M101289200.
30. Kluck, R.M., Bossy-Wetzel, E., Green, D.R., and Newmeyer, D.D. 1997. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science, 275: 1132-1136. doi:10.1126/science.275.5303.1132.
31. Kotamraju, S., Hogg, N., Joseph, J., Keefer, L.K., and Kalyanaraman, B. 2001. Inhibition of oxidized low-density lipoprotein-induced apoptosis in endothelial cells by nitric oxide. Peroxyl radical scavenging as an antiapoptotic mechanism. J. Biol. Chem. 276: 17316-17323. doi:10.1074/jbc.M011731200.
32. Kuan, C.Y., and Burke, R.E. 2005. Targeting the JNK signaling pathway for stroke and Parkinson's diseases therapy. Curr. Drug Targets CNS Neurol. Disord. 4: 63-67. doi:10.2174/1568007053005145.
33. Kyriakis, J.M., Banerjee, P., Nikolakaki, E., Dai, T., Rubie, E.A., Ahmad, M.F., Avruch, J., and Woodgett, J.R. 1994. The stress-activated protein kinase subfamily of c-Jun kinases. Nature (London), 369: 156-160. doi:10.1038/369156a0.
34. Lei, X.L., and Chiou, G.C. 1986a. Cardiovascular pharmacology of Panax notoginseng (Burk) F.H. Chen and Salvia miltiorrhiza. Am. J. Chin. Med. 14: 145-152. doi:10.1142/S0192415X86000235.
35. Lei, X.L., and Chiou, G.C. 1986b. Studies on cardiovascular actions of Salvia miltiorrhiza. Am. J. Chin. Med. 14: 26-32. doi:10.1142/S0192415X86000053.
36. Lin, A. 2003. Activation of the JNK signaling pathway: breaking the brake on apoptosis. Bioessays, 25: 17-24. doi:10.1002/bies. 10204.
37. Lin, A., and Dibling, B. 2002. The true face of JNK activation in apoptosis. Aging Cell, 1: 112-116. doi:10.1046/j.1474-9728. 2002.00014.x.
38. Lin, S.J., Shyue, S.K., Liu, P.L., Chen, Y.H., Ku, H.H., Chen, J.W., Tam, K.B., and Chen, Y.L. 2004. 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. doi:10.1016/j.yjmcc.2003.10.011.
39. Lin, S.J., Shyue, S.K., Shih, M.C., Chu, T.H., Chen, Y.H., Ku, H.H., et al. 2007. Superoxide dismutase and catalase inhibit oxidized low-density lipoprotein-induced human aortic smooth muscle cell proliferation: role of cell-cycle regulation, mitogen-activated protein kinases, and transcription factors. Atherosclerosis, 190: 124-134. doi:10.1016/j.atherosclerosis. 2006.02.044.
40. Lu, Y., and Foo, L.Y. 2002. Polyphenolics of Salvia - a review. Phytochemistry, 59: 117-140. doi:10.1016/S0031-9422(01)00415-0.
41. Lupo, G., Nicotra, A., Giurdanella, G., Anfuso, C.D., Romeo, L., Biondi, G., et al. 2005. Activation of phospholipase A(2) and MAP kinases by oxidized low-density lipoproteins in immortalized GP8.39 endothelial cells. Biochim. Biophys. Acta, 1735: 135-150.
42. McNamara, J.R., Shah, P.K., Nakajima, K., Cupples, L.A., Wilson, P.W., Ordovas, J.M., and Schaefer, E.J. 2001. Remnant-like particle (RLP) cholesterol is an independent cardiovascular disease risk factor in women: results from the Framingham Heart Study. Atherosclerosis, 154: 229-236. doi:10.1016/S0021-9150(00)00484-6.
43. Metzler, B., Hu, Y., Dietrich, H., and Xu, Q. 2000. Increased expression and activation of stress-activated protein kinases/c-Jun NH(2)-terminal protein kinases in atherosclerotic lesions coincide with p53. Am. J. Pathol. 156: 1875-1886.
44. Napoli, C. 2003. Oxidation of LDL, atherogenesis, and apoptosis. Ann. N. Y. Acad. Sci. 1010: 698-709. doi:10.1196/annals.1299.127.
45. Napoli, C., Quehenberger, O., De Nigris, F., Abete, P., Glass, C.K., and Palinski, W. 2000. Mildly oxidized low density lipoprotein activates multiple apoptotic signaling pathways in human coronary cells. FASEB J. 14: 1996-2007. doi:10.1096/fj.99-0986com.
46. Naseem, K.M. 2005. The role of nitric oxide in cardiovascular diseases. Mol. Aspects Med. 26: 33-65. doi:10.1016/j.mam.2004.09.003.
47. Navab, M., Berliner, J.A., Watson, A.D., Hama, S.Y., Territo, M.C., Lusis, A.J., et al. 1996. The Yin and Yang of oxidation in the development of the fatty streak. A review based on the 1994 George Lyman Duff Memorial Lecture. Arterioscler. Thromb. Vasc. Biol. 16: 831-842.
48. Norata, G.D., Pirillo, A., Callegari, E., Hamsten, A., Catapano, A.L., and Eriksson, P. 2003. Gene expression and intracellular pathways involved in endothelial dysfunction induced by VLDL and oxidized VLDL. Cardiovasc. Res. 59: 169-180. doi:10.1016/S0008-6363(03)00335-3.
49. O, K., Lynn, E.G., Vazhappilly, R., Au-Yeung, K.K., Zhu, D.Y., and Siow, Y.L. 2001. Magnesium tanshinoate B (MTB) inhibits low density lipoprotein oxidation. Life Sci. 68: 903-912. doi:10.1016/S0024-3205(00)00989-9.
50. Pharmacopoeia Commission of the PRC. 2000. Pharmacopoeia of People's Republic of China. Chemical Industry Press, Beijing. pp. 192-3, A35-8.
51. Renz, A., Berdel, W.E., Kreuter, M., Belka, C., Schulze-Osthoff, K., and Los, M. 2001. Rapid extracellular release of cytochrome c is specific for apoptosis and marks cell death in vivo. Blood, 98: 1542-1548. doi:10.1182/blood.V98.5.1542.
52. Rice-Evans, C.A., Miller, N.J., and Paganga, G. 1997. Antioxidant properties of phenolic compounds. Trends Plant Sci. 2: 152-159. doi:10.1016/S1360-1385(97)01018-2.
53. Ross, R. 1999. Atherosclerosis - an inflammatory disease. N. Engl. J. Med. 340: 115-126. doi:10.1056/NEJM199901143400207.
54. Salvayre, R., Auge, N., Benoist, H., and Negre-Salvayre, A. 2002. Oxidized low-density lipoprotein-induced apoptosis. Biochim. Biophys. Acta, 1585: 213-221.
55. Sattar, N., Petrie, J.R., and Jaap, A.J. 1998. The atherogenic lipoprotein phenotype and vascular endothelial dysfunction. Atherosclerosis, 138: 229-235. doi:10.1016/S0021-9150(98)00037-9.
56. Schroeter, H., Spencer, J.P., Rice-Evans, C., and Williams, R.J. 2001. Flavonoids protect neurons from oxidized low-densitylipoprotein-induced apoptosis involving c-Jun N-terminal kinase (JNK), c-Jun and caspase-3. Biochem. J. 358: 547-557. doi:10.1042/0264-6021:3580547.
57. Shanghai Cooperative Group. 1984. The Study of Tanshinone IIA. Therapeutic effect of sodium tanshinone IIA sulfonate in patients with coronary heart disease. A double blind study. J. Tradit. Chin. Med. 4: 20-24.
58. Singleton, V.L., and Rossi, J.A., Jr. 1965. Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am. J. Enol. Vitic. 16: 144-158.
59. Stoneman, V.E., and Bennett, M.R. 2004. Role of apoptosis in atherosclerosis and its therapeutic implications. Clin. Sci. (Lond.), 107: 343-354.
60. Valgimigli, M., Agnoletti, L., Curello, S., Comini, L., Francolini, G., Mastrorilli, F., et al. 2003. Serum from patients with acute coronary syndromes displays a proapoptotic effect on human endothelial cells: a possible link to pan-coronary syndromes. Circulation, 107: 264-270. doi:10.1161/01.CIR. 0000045665.57256.86.
61. Waetzig, V., and Herdegen, T. 2003. A single c-Jun N-terminal kinase isoform (JNK3-p54) is an effector in both neuronal differentiation and cell death. J. Biol. Chem. 278: 567-572. doi:10.1074/jbc.M207391200.
62. Waetzig, V., and Herdegen, T. 2005. Context-specific inhibition of JNKs: overcoming the dilemma of protection and damage. Trends Pharmacol. Sci. 26: 455-461.
63. Walter, D.H., Haendeler, J., Galle, J., Zeiher, A.M., and Dimmeler, S. 1998. Cyclosporin A inhibits apoptosis of human endothelial cells by preventing release of cytochrome C from mitochondria. Circulation, 98: 1153-1157.
64. Wang, X., Zelenski, N.G., Yang, J., Sakai, J., Brown, M.S., and Goldstein, J.L. 1996. Cleavage of sterol regulatory element binding proteins (SREBPs) by CPP32 during apoptosis. EMBO J. 15: 1012-1020.
65. Wu, X., Beecher, G.R., Holden, J.M., Haytowitz, D.B., Gebhardt, S.E., and Prior, R.L. 2004. Lipophilic and hydrophilic antioxidant capacities of common foods in the United States. J. Agric. Food Chem. 52: 4026-4037. doi:10.1021/jf049696w.
66. Xia, Z., Dickens, M., Raingeaud, J., Davis, R.J., and Greenberg, M.E. 1995. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science (Washington, D.C.), 270: 1326-1331. doi:10.1126/science.270.5240.1326.
67. Xu, S., and Cobb, M.H. 1997. MEKK1 binds directly to the c-Jun N-terminal kinases/stress-activated protein kinases. J. Biol. Chem. 272: 32056-32060. doi:10.1074/jbc.272.51.32056.
68. Zhang, C., Hein, T.W., Wang, W., Ren, Y., Shipley, R.D., and Kuo, L. 2006. Activation of JNK and xanthine oxidase by TNFalpha impairs nitric oxide-mediated dilation of coronary arterioles. J. Mol. Cell. Cardiol. 40: 247-257. doi:10.1016/j.yjmcc.2005.11.010.
69. Zhao, G.-R., Zhang, H.-M., Ye, T.-X., Xiang, Z.-J., Yuan, Y.-J., Guo, Z.-X., and Zhao, L.-B. 2007. Characterization of the radical scavenging and antioxidant activities of danshensu and salvianolic acid B. Food Chem. Toxicol.. doi:10.1016/j.fct.2007.06.034.
70. Zhou, W., and Ruigrok, T.J. 1990. Protective effect of danshen during myocardial ischemia and reperfusion: an isolated rat heart study. Am. J. Chin. Med. 18: 19-24. doi:10.1142/S0192415X90000046.
71. Zou, H., Li, Y., Liu, X., and Wang, X. 1999. An APAF-1.cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J. Biol. Chem. 274: 11549-11556. doi:10.1074/jbc.274.17. 11549.