Delphinidin-3-glucoside protects human umbilical vein endothelial cells against oxidized low-density lipoprotein-induced injury by autophagy upregulation via the AMPK/SIRT1 signaling pathway

Molecular Nutrition and Food Research

Volumn 58, Issue 10, 2014, Pages 1941-1951

  Jin, Xin ^a   Chen, Mingliang ^a   Yi, Long ^a   Chang, Hui ^a   Zhang, Ting ^a   Wang, Li ^a   Ma, Wanqiang ^b   Peng, Xiaoli ^a,c   Zhou, Yong ^a   Mi, Mantian ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

^b The 210th Hospital of PLA   (China)

^c CHENGDU MEDICAL COLLEGE   (China)

Author keywords

Atherosclerosis; Autophagy; Delphinidin 3 glucoside; Endothelial cells; Injury

Indexed keywords

ANTHOCYANIN; ANTIOXIDANT; DELPHINIDIN 3-O-GLUCOPYRANOSIDE; GLUCOSIDE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; LOW DENSITY LIPOPROTEIN; OXIDIZED LOW DENSITY LIPOPROTEIN; SIRT1 PROTEIN, HUMAN; SIRTUIN 1; SMALL INTERFERING RNA;

ANTAGONISTS AND INHIBITORS; APOPTOSIS; ATHEROSCLEROSIS; AUTOPHAGY; CELL CULTURE; CELL SURVIVAL; CHEMISTRY; CYTOLOGY; DIET SUPPLEMENTATION; GENETICS; HUMAN; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PROTEIN PROCESSING; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULAR ENDOTHELIUM;

AMP-ACTIVATED PROTEIN KINASES; ANTHOCYANINS; ANTIOXIDANTS; APOPTOSIS; ATHEROSCLEROSIS; AUTOPHAGY; CELL SURVIVAL; CELLS, CULTURED; DIETARY SUPPLEMENTS; ENDOTHELIUM, VASCULAR; GLUCOSIDES; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; LIPOPROTEINS, LDL; MICROSCOPY, ELECTRON, TRANSMISSION; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SIRTUIN 1;

EID: 84908431088     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201400161     Document Type: Article

References (57)

1. Zernecke, A., Weber, C., Improving the treatment of atherosclerosis by linking anti-inflammatory and lipid modulating strategies. Heart. 2012, 98, 1600-1606.
2. Libby, P., Inflammation in atherosclerosis. Arteriosclr. Thromb. Vasc. Biol. 2012, 32, 2045-2051.
3. Liu, S., Shen, H., Xu, M., Liu, O. et al., FRP inhibits ox-LDLinduced endothelial cell apoptosis through an Akt-NF-kappa B-Bcl-2 pathway and inhibits endothelial cell apoptosis in an apoE-knockout mousemodel. Am. J. Physiol. Endocrinol. Metab. 2010, 299, E351-E363.
4. Rajagopalan, S., Somers, E. C., Brook, R. D., Kehrer, C. et al., Endothelial cell apoptosis in systemic lupus erythematosus:a common pathway for abnormal vascular function and thrombosis propensity. Blood. 2004, 103, 3677-3683.
5. Durand, E., Scoazec, A., Lafont, A., Boddaert, J. et al., In vivo induction of endothelial apoptosis leads to vessel thrombosis and endothelial denudation-A clue to the understanding of themechanisms of thrombotic plaque erosion. Circulation. 2004, 109, 2503-2506.
6. Tsai, K. L., Chen, L. H., Chiou, S. H., Chiou, G. Y. et al., Coenzyme Q10 suppresses oxLDL-induced endothelial oxidative injuries by the modulation of LOX-1-mediated ROS generation via the AMPK/PKC/NADPH oxidase signaling pathway. Mol. Nutr. Food Res. 2011, 55, S227-S240.
7. Galvano, F., La Fauci, L., Lazzarino, G., Fogliano, V. et al., Cyanidins: metabolism and biological properties. J. Nutr. Biochem. 2004, 15, 2-11.
8. Zapolska-Downar, D., Nowicka, G., Sygitowicz, G., Jarosz, M., Anthocyanin-rich aronox extract from Aronia melanocarpa E protects against 7 beta-hydroxycholesterolinduced apoptosis of endothelial cells. Ann. Nutr. Metab. 2008, 53, 283-294.
9. Wang, Y., Zhang, Y. H., Wang, X. M., Liu, Y. et al., Supplementation with Cyanidin-3-O-beta-glucoside protects against hypercholesterolemia-mediated endothelial dysfunction and attenuates atherosclerosis in Apolipoprotein E-deficient mice. J. Nutr. 2012, 142, 1033-1037.
10. Mauray, A., Felgines, C., Morand, C., Mazur, A. et al., Bilberry anthocyanin-rich extract alters expression of genes related to atherosclerosis development in aorta of apo E-deficient mice. Nutr. Metab. Cardiovas. 2012, 22, 72-80.
11. Xia, X. D., Ling, W. H., Ma, J., Xia, M. et al., An anthocyaninrich extract from black rice enhances atherosclerotic plaque stabilization in apolipoprotein e-deficientmice. J. Nutr. 2006, 136, 2220-2225.
12. Yi, L., Chen, C. Y., Jin, X., Mi, M. T. et al., Structural requirements of anthocyanins in relation to inhibition of endothelial injury induced by oxidized low-density lipoprotein and correlation with radical scavenging activity. FEBS Lett. 2010, 584, 583-590.
13. Chen, C. Y., Yi, L., Jin, X., Mi, M. T. et al., Delphinidin attenuates stress injury induced by oxidized low-density lipoprotein in human umbilical vein endothelial cells. Chem. Biol. Interact. 2010, 183, 105-112.
14. Guo, J. Y., Xia, B., White, E., Autophagy-mediated tumor promotion. Cell. 2013, 155, 1216-1219.
15. Razani, B., Feng, C., Coleman, T., Emanuel, R. et al., Autophagy links inflammasomes to atherosclerotic progression. Cell Metabolism. 2012, 15, 534-544.
16. Lee, I. H., Cao, L., Mostoslavsky, R., Lombard, D. B. et al., A role for the NAD-dependent deacetylase Sirt1 in the regulation of autophagy. Proc. Natl. Acad. Sci. USA. 2008, 105, 3374-3379.
17. Canto, C., Gerhart-Hines, Z., Feige, J. N., Lagouge, M. et al., AMPK regulates energy expenditure by modulating NAD(+) metabolism and SIRT1 activity. Nature. 2009, 458, 1056-U1140.
18. Takeda-Watanabe, A., Kitada, M., Kanasaki, K., Koya, D., SIRT1 inactivation induces inflammation through the dysregulation of autophagy in human THP-1 cells. Biochem. Biophys. Res. Commun. 2012, 427, 191-196.
19. Wu, Y. C., Li, X. Q., Zhu, J. X., Xie, W. J. et al., Resveratrolactivated AMPK/SIRT1/autophagy in cellular models of Parkinson's disease. Neurosignals. 2011, 19, 163-174.
20. Guo, H., Chen, Y., Liao, L., Wu, W., Resveratrol protects HUVECs from oxidized-LDL induced oxidative damage by autophagy upregulation via the AMPK/SIRT1 pathway. Cardiovas. Drugs Ther. 2013, 27, 189-198.
21. Tsuyuki, S., Fukui, S., Watanabe, A., Akune, S. et al., Delphinidin induces autolysosome as well as autophagosome formation and Delphinidin-induced autophagy exerts a cell protective role. J. Biochem. Mol. Toxic. 2012, 26, 445-453.
22. Ross, R., The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature. 1993, 362, 801-809.
23. Zhang, L., Zhou, G., Song,W., Tan, X. et al., Pterostilbene protects vascular endothelial cells against oxidized low-density lipoprotein-induced apoptosis in vitro and in vivo. Apoptosis. 2012, 17, 25-36.
24. Chen, M. L., Yi, L., Jin, X., Liang, X. Y. et al., Resveratrol attenuates vascular endothelial inflammation by inducing autophagy through the cAMP signaling pathway. Autophagy. 2013, 9, 2033-2045.
25. Chen, C. Y., Yi, L., Jin, X., Zhang, T. et al., Inhibitory effect of Delphinidin on monocyte-endothelial cell adhesion induced by oxidized low-density lipoprotein via ROS/p38MAPK/NFkappa B Pathway. Cell Biochem. Biophys. 2011, 61, 337-348.
26. Chen, C. Y., Yi, L., Jin, X., Mi, M. T. et al., Delphinidin attenuates stress injury induced by oxidized low-density lipoprotein in human umbilical vein endothelial cells. Chem. Biol. Interact. 2010, 183, 105-112.
27. Ou, H. C., Lee,W. J., Lee, I. T., Chiu, T. H. et al., Ginkgo biloba extract attenuates oxLDL-induced oxidative functional damages in endothelial cells. J. Appl. Physiol. 2009, 106, 1674-1685.
28. Xie, X. P., Zhao, R. Z., Shen, G. X., Influence of delphinidin-3-glucoside on oxidized low-density lipoprotein-induced oxidative stress and apoptosis in cultured endothelial cells. J. Agr. Food Chem. 2012, 60, 1850-1856.
29. Jin, Y., Alimbetov, D., George, T., Gordon, M. H. et al., A randomised trial to investigate the effects of acute consumption of a blackcurrant juice drink onmarkers of vascular reactivity and bioavailability of anthocyanins in human subjects. Eur. J. Clin. Nutr. 2011, 65, 849-856.
30. Gonzalez-Barrio, R., Borges, G., Mullen, W., Crozier, A., Bioavailability of anthocyanins and ellagitannins following consumption of raspberries by healthy humans and subjects with an ileostomy. J. Agric. Food Chem. 2010, 58, 3933-3939.
31. Charron, C. S., Kurilich, A. C., Clevidence, B. A., Simon, P. W. et al., Bioavailability of anthocyanins from purple carrot juice: effects of acylation and plant matrix. J. Agric. Food Chem. 2009, 57, 1226-1230.
32. Jin, X., Yi, L., Chen, M. L., Chen, C. Y. et al., Delphinidin-3- glucoside protects against oxidized low-density lipoproteininduced mitochondrial dysfunction in vascular endothelial cells via the sodium-dependent glucose transporter SGLT1. PloS One. 2013, 8, e68617.
33. Nielsen, I. L., Dragsted, L.O., Ravn-Haren, G., Freese, R. et al., Absorption and excretion of black currant anthocyanins in humans and watanabe heritable hyperlipidemic rabbits. J. Agric. Food Chem. 2003, 51, 2813-2820.
34. Chen, C. Y., Yi, L., Jin, X., Zhang, T. et al., Inhibitory effect of Delphinidin on monocyte-endothelial cell adhesion induced by oxidized low-density lipoprotein via ROS/p38MAPK/NFkappa B Pathway. Cell Biochem. Biophys. 2011, 61, 337-348.
35. Yi, L., Jin, X., Chen, C. Y., Fu, Y. J. et al., Chemical structures of 4-oxo-flavonoids in relation to inhibition of oxidized low-density lipoprotein (LDL)-induced vascular endothelial dysfunction. Int. J. Mol. Sci. 2011, 12, 5471-5489.
36. Paixao, J., Dinis, T. C., Almeida, L. M., Dietary anthocyanins protect endothelial cells against peroxynitrite-induced mitochondrial apoptosis pathway and Bax nuclear translocation:an in vitro approach. Apoptosis. 2011, 16, 976-989.
37. Lamy, S., Blanchette, M., Michaud-Levesque, J., Lafleur, R. et al., Delphinidin, a dietary anthocyanidin, inhibits vascular endothelial growth factor receptor-2 phosphorylation. Carcinogenesis. 2006, 27, 989-996.
38. Martin, S., Favot, L., Matz, R., Lugnier, C. et al., Delphinidin inhibits endothelial cell proliferation and cell cycle progression through a transient activation of ERK-1/-2. Biochem. Pharmacol. 2003, 65, 669-675.
39. Matsunaga, N., Tsuruma, K., Shimazawa, M., Yokota, S. et al., Inhibitory actions of bilberry anthocyanidins on angiogenesis. Phytother. Res. 2010, 24, S42-S47.
40. Scott, R. C., Juhasz, G., Neufeld, T. P., Direct induction of autophagy by Atg1 inhibits cell growth and induces apoptotic cell death. Curr. Biol. 2007, 17, 1-11.
41. Levine, B., Yuan, J. Y., Autophagy in cell death: an innocent convict? J. Clin. Invest. 2005, 115, 2679-2688.
42. Zhang, Y. L., Cao, Y. J., Zhang, X., Liu, H. H. et al., The autophagy-lysosome pathway: a novel mechanism involved in the processing of oxidized LDL in human vascular endothelial cells. Biochem. Biophys. Res. Commun. 2010, 394, 377-382.
43. Ou, H. C., Chou, F. P., Sheu,W. H. H., Hsu, S. L. et al., Protective effects of magnolol against oxidized LDL-induced apoptosis in endothelial cells. Arch. Toxicol. 2007, 81, 421-432.
44. Marzetti, E., Csiszar, A., Dutta, D., Balagopal, G. et al., Role of mitochondrial dysfunction and altered autophagy in cardiovascular aging and disease: from mechanisms to therapeutics. Am. J. Physiol. 2013, 305, H459-H476.
45. Giovannini, C., Matarrese, P., Scazzocchio, B., Sanchez, M. et al., Mitochondria hyperpolarization is an early event in oxidized low-density lipoprotein-induced apoptosis in Caco-2 intestinal cells. FEBS Lett. 2002, 523, 200-206.
46. Ou, H. C., Lee,W. J., Lee, I. T., Chiu, T. H. et al., Ginkgo biloba extract attenuates oxLDL-induced oxidative functional damages in endothelial cells. J. Appl. Physiol. 2009, 106, 1674-1685.
47. Marzetti, E., Csiszar, A., Dutta, D., Balagopal, G. et al., Role of mitochondrial dysfunction and altered autophagy in cardiovascular aging and disease: from mechanisms to therapeutics. Am. J. Physiol. 2013, 305, H459-H476.
48. Guarente, L., Franklin, H. Epstein lecture: sirtuins, aging, and medicine. N. Eng. J. Med. 2011, 364, 2235-2244.
49. Lee, I. H., Cao, L., Mostoslavsky, R., Lombard, D. B. et al., A role for the NAD-dependent deacetylase Sirt1 in the regulation of autophagy. Proc. Natl. Acad. Sci. USA. 2008, 105, 3374-3379.
50. Canto, C., Gerhart-Hines, Z., Feige, J. N., Lagouge, M. et al., AMPK regulates energy expenditure by modulating NAD +metabolism and SIRT1 activity. Nature. 2009, 458, 1056-1060.
51. Xu, J. W., Ikeda, K., Yamori, Y., Upregulation of endothelial nitric oxide synthase by cyanidin-3-glucoside, a typical anthocyanin pigment. Hypertension. 2004, 44, 217-222.
52. Xu, J. W., Ikeda, K., Yamori, Y., Cyanidin-3-glucoside regulates phosphorylation of endothelial nitric oxide synthase. FEBS Lett. 2004, 574, 176-180.
53. Sorrenti, V., Mazza, F., Campisi, A., Di Giacomo, C. et al., Heme oxygenase induction by cyanidin-3-O-beta-glucoside in cultured human endothelial cells. Mol. Nutr. Food Res. 2007, 51, 580-586.
54. Wang, D., Xia, M., Yan, X., Li, D. et al., Gut microbiota metabolism of anthocyanin promotes reverse cholesterol transport in mice via repressing miRNA-10b. Circ. Res. 2012, 111, 967-981.
55. Martin, S., Giannone, G., Andriantsitohaina, R., Martinez, M. C., Delphinidin, an active compound of red wine, inhibits endothelial cell apoptosis via nitric oxide pathway and regulation of calcium homeostasis. Br. J. Pharmacol. 2003, 139, 1095-1102.
56. Hou, D. X., Tong, X., Terahara, N., Luo, D. et al., Delphinidin 3-sambubioside, a Hibiscus anthocyanin, induces apoptosis in human leukemia cells through reactive oxygen speciesmediated mitochondrial pathway. Arch. Biochem. Biophys. 2005, 440, 101-109.
57. Yun, J. M., Afaq, F., Khan, N., Mukhtar, H., Delphinidin, an anthocyanidin in pigmented fruits and vegetables, induces apoptosis and cell cycle arrest in human colon cancer HCT116 cells. Mol. Carcinogen. 2009, 48, 260-270.