Korean Red Ginseng protects endothelial cells from serum-deprived apoptosis by regulating BcL-2 family protein dynamics and caspase S-nitrosylation

Journal of Ginseng Research

Volumn 37, Issue 4, 2013, Pages 413-424

  Kim, Young Mi ^a   Kim, Jung Hwan ^a   Kwon, Hyuk Min ^a   Lee, Dong Heon ^a   Won, Moo Ho ^a   Kwon, Young Guen ^b   Kim, Young Myeong ^a  

^a Kangwon National University   (South Korea)

^b Yonsei University   (South Korea)

Author keywords

Apoptosis; Bcl 2 family; Endothelial cells; Nitric oxide; Panax ginseng

Indexed keywords

PANAX GINSENG; PANAX QUINQUEFOLIUS;

EID: 84885594557     PISSN: 12268453     EISSN: None     Source Type: Journal    
DOI: 10.5142/jgr.2013.37.413     Document Type: Article

References (35)

1. Cines DB, Pollak ES, Buck CA, Loscalzo J, Zimmer-man GA, McEver RP, Pober JS, Wick TM, Konkle BA, Schwartz BS et al. Endothelial cells in physiology and in the pathophysiology of vascular disorders. Blood 1998;91:3527-3561.
2. Stoneman VE, Bennett MR. Role of apoptosis in atherosclerosis and its therapeutic implications. Clin Sci (Lond) 2004;107:343-354.
3. Williams TA, Verhovez A, Milan A, Veglio F, Mulatero P. Protective effect of spironolactone on endothelial cell apoptosis. Endocrinology 2006;147:2496-2505.
4. Desagher S, Martinou JC. Mitochondria as the central control point of apoptosis. Trends Cell Biol 2000;10:369-377.
5. Fujio Y, Nguyen T, Wencker D, Kitsis RN, Walsh K. Akt promotes survival of cardiomyocytes in vitro and protects against ischemia-reperfusion injury in mouse heart. Circulation 2000;101:660-667.
6. Stefanec T. Endothelial apoptosis: the missing link between atherosclerosis and SLE? Blood 2004;103:3608-3609.
7. Kim YM, Bombeck CA, Billiar TR. Nitric oxide as a bifunctional regulator of apoptosis. Circ Res 1999;84:253-256.
8. Lee SJ, Kim KM, Namkoong S, Kim CK, Kang YC, Lee H, Ha KS, Han JA, Chung HT, Kwon YG et al. Nitric oxide inhibition of homocysteine-induced human endothelial cell apoptosis by down-regulation of p53-dependent Noxa expression through the formation of S-nitrosohomocysteine. J Biol Chem 2005;280:5781-5788.
9. Hoffmann J, Haendeler J, Aicher A, Rossig L, Vasa M, Zeiher AM, Dimmeler S. Aging enhances the sensitivity of endothelial cells toward apoptotic stimuli: important role of nitric oxide. Circ Res 2001;89:709-715.
10. Sung J, Han KH, Zo JH, Park HJ, Kim CH, Oh BH. Effects of red ginseng upon vascular endothelial function in patients with essential hypertension. Am J Chin Med 2000;28:205-216.
11. Kim YM, Namkoong S, Yun YG, Hong HD, Lee YC, Ha KS, Lee H, Kwon HJ, Kwon YG, Kim YM. Water extract of Korean red ginseng stimulates angiogenesis by activating the PI3K/Akt-dependent ERK1/2 and eNOS pathways in human umbilical vein endothelial cells. Biol Pharm Bull 2007;30:1674-1679.
12. Lee SJ, Namkoong S, Kim YM, Kim CK, Lee H, Ha KS, Chung HT, Kwon YG, Kim YM. Fractalkine stimulates angiogenesis by activating the Raf-1/MEK/ERK- and PI3K/Akt/eNOS-dependent signal pathways. Am J Physiol Heart Circ Physiol 2006;291:H2836-H2846.
13. Qian J, Chen F, Kovalenkov Y, Pandey D, Moseley MA, Foster MW, Black SM, Venema RC, Stepp DW, Fulton DJ. Nitric oxide reduces NADPH oxidase 5 (Nox5) activity by reversible S-nitrosylation. Free Radic Biol Med 2012;52:1806-1819.
14. Crow MT, Mani K, Nam YJ, Kitsis RN. The mitochondrial death pathway and cardiac myocyte apoptosis. Circ Res 2004;95:957-970.
15. Gross A, McDonnell JM, Korsmeyer SJ. BCL-2 family members and the mitochondria in apoptosis. Genes Dev 1999;13:1899-1911.
16. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM. Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 1999;399:601-605.
17. Lu JM, Yao Q, Chen C. Ginseng compounds: an update on their molecular mechanisms and medical applications. Curr Vasc Pharmacol 2009;7:293-302.
18. Yan J, Liu Q, Dou Y, Hsieh Y, Liu Y, Tao R, Zhu D, Lou Y. Activating glucocorticoid receptor-ERK signaling pathway contributes to ginsenoside Rg1 protection against β-amyloid peptide-induced human endothelial cells apoptosis. J Ethnopharmacol 2013;147:456-466.
19. Kwok HH, Ng WY, Yang MS, Mak NK, Wong RN, Yue PY. The ginsenoside protopanaxatriol protects endothelial cells from hydrogen peroxide-induced cell injury and cell death by modulating intracellular redox status. Free Radic Biol Med 2010;48:437-445.
20. Min JK, Kim JH, Cho YL, Maeng YS, Lee SJ, Pyun BJ, Kim YM, Park JH, Kwon YG. 20(S)-ginsenoside Rg3 prevents endothelial cell apoptosis via inhibition of a mitochondrial caspase pathway. Biochem Biophys Res Commun 2006;349:987-994.
21. Dimmeler S, Haendeler J, Nehls M, Zeiher AM. Suppression of apoptosis by nitric oxide via inhibition of interleukin-1beta-converting enzyme (ICE)-like and cysteine protease protein (CPP)-32-like proteases. J Exp Med 1997;185:601-607.
22. Sengupta S, Toh SA, Sellers LA, Skepper JN, Koolwijk P, Leung HW, Yeung HW, Wong RN, Sasisekharan R, Fan TP. Modulating angiogenesis: the yin and the yang in ginseng. Circulation 2004;110:1219-1225.
23. Kim WY, Kim JM, Han SB, Lee SK, Kim ND, Park MK, Kim CK, Park JH. Steaming of ginseng at high temperature enhances biological activity. J Nat Prod 2000;63: 1702-1704.
24. Kim SN, Ha YW, Shin H, Son SH, Wu SJ, Kim YS. Si-multaneous quantification of 14 ginsenosides in Panax ginseng C.A. Meyer (Korean red ginseng) by HPLC-ELSD and its application to quality control. J Pharm Biomed Anal 2007;45:164-170.
25. Zinkel S, Gross A, Yang E. BCL2 family in DNA damage and cell cycle control. Cell Death Differ 2006;13:1351-1359.
26. Li H, Zhu H, Xu CJ, Yuan J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 1998;94:491-501.
27. Zha J, Harada H, Yang E, Jockel J, Korsmeyer SJ. Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not BCL-X(L). Cell 1996;87:619-628.
28. Moncada S, Radomski MW, Palmer RM. Endothelium-derived relaxing factor. Identification as nitric oxide and role in the control of vascular tone and platelet function. Biochem Pharmacol 1988;37:2495-2501.
29. Shin W, Yoon J, Oh GT, Ryoo S. Korean red ginseng inhibits arginase and contributes to endotheliumdependent vasorelaxation through endothelial nitric oxide synthase coupling. J Ginseng Res 2013;37:64-73.
30. Hellermann GR, Solomonson LP. Calmodulin promotes dimerization of the oxygenase domain of human endothelial nitric-oxide synthase. J Biol Chem 1997;272:12030-12034.
31. Kwon YG, Min JK, Kim KM, Lee DJ, Billiar TR, Kim YM. Sphingosine 1-phosphate protects human umbilical vein endothelial cells from serum-deprived apoptosis by nitric oxide production. J Biol Chem 2001;276:10627-10633.
32. Ceneviva GD, Tzeng E, Hoyt DG, Yee E, Gallagher A, Engelhardt JF, Kim YM, Billiar TR, Watkins SA, Pitt BR. Nitric oxide inhibits lipopolysaccharide-induced apoptosis in pulmonary artery endothelial cells. Am J Physiol 1998;275:L717-L728.
33. Granger DL, Taintor RR, Cook JL, Hibbs JB Jr. Injury of neoplastic cells by murine macrophages leads to inhibition of mitochondrial respiration. J Clin Invest 1980;65:357-370.
34. Kim YM, Talanian RV, Billiar TR. Nitric oxide inhibits apoptosis by preventing increases in caspase-3-like activity via two distinct mechanisms. J Biol Chem 1997;272: 31138-31148.
35. Mannick JB, Hausladen A, Liu L, Hess DT, Zeng M, Miao QX, Kane LS, Gow AJ, Stamler JS. Fas-induced caspase denitrosylation. Science 1999;284:651-654.