Eicosapentaenoic acid protects against palmitic acid-induced endothelial dysfunction via activation of the AMPK/eNOS pathway

International Journal of Molecular Sciences

Volumn 15, Issue 6, 2014, Pages 10334-10349

  Lee, Che Hsin ^a   Lee, Shin Da ^b   Ou, Hsiu Chung ^b   Lai, Su Chuan ^b   Cheng, Yu Jung ^b  

^a CHINA MEDICAL UNIVERSITY   (Taiwan)

^b CHINA MEDICAL UNIVERSITY   (Taiwan)

Author keywords

AMP activated protein kinase; Eicosapentaenoic acid; Endothelial dysfunction; Palmitic acid

Indexed keywords

CASPASE 3; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; ICOSAPENTAENOIC ACID; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PALMITIC ACID; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P53; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SMALL INTERFERING RNA; SUPEROXIDE; APOPTOSIS REGULATORY PROTEIN; ENZYME ACTIVATOR; INDUCIBLE NITRIC OXIDE SYNTHASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN KINASE B;

APOPTOSIS; ARTICLE; ATHEROGENESIS; CELL DEATH; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; DENSITOMETRY; DOWN REGULATION; ENDOTHELIAL DYSFUNCTION; FLUOROMETRY; GENE ACTIVATION; GENE TRANSLOCATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; NICK END LABELING; OXIDATIVE STRESS; PHASE CONTRAST MICROSCOPY; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; UPREGULATION; WESTERN BLOTTING; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; GENETICS; METABOLISM; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TOXICITY; UMBILICAL VEIN ENDOTHELIAL CELL;

AMP-ACTIVATED PROTEIN KINASES; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CASPASE 3; DOWN-REGULATION; EICOSAPENTAENOIC ACID; ENZYME ACTIVATORS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; NADPH OXIDASE; NF-KAPPA B; NITRIC OXIDE SYNTHASE TYPE II; NITRIC OXIDE SYNTHASE TYPE III; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PALMITIC ACID; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; REACTIVE OXYGEN SPECIES; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 84902290328     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms150610334     Document Type: Article

References (40)

1. Artwohl, M.; Roden, M.; Waldhausl, W.; Freudenthaler, A.; Baumgartner-Parzer, S.M. Free fatty acids trigger apoptosis and inhibit cell cycle progression in human vascular endothelial cells. FASEB J. 2004, 18, 146-148.
2. Kim, F.; Tysseling, K.A.; Rice, J.; Pham, M.; Haji, L.; Gallis, B.M.; Baas, A.S.; Paramsothy, P.; Giachelli, C.M.; Corson, M.A.; et al. Free fatty acid impairment of nitric oxide production in endothelial cells is mediated by IKKbeta. Arterioscler. Thromb. Vasc. Biol. 2005, 25, 989-994.
3. Steinberg, H.O.; Paradisi, G.; Hook, G.; Crowder, K.; Cronin, J.; Baron, A.D. Free fatty acid elevation impairs insulin-mediated vasodilation and nitric oxide production. Diabetes 2000, 49, 1231-1238.
4. 2+ signaling and NO production in endothelial cells. Antioxid. Redox. Signal. 2003, 5, 147-153.
5. Lobo, V.; Patil, A.; Phatak, A.; Chandra, N. Free radicals, antioxidants and functional foods: Impact on human health. Pharmacogn. Rev. 2010, 4, 118-126.
6. Khan, M.J.; Rizwan Alam, M.; Waldeck-Weiermair, M.; Karsten, F.; Groschner, L.; Riederer, M.; Hallstrom, S.; Rockenfeller, P.; Konya, V.; Heinemann, A.; et al. Inhibition of autophagy rescues palmitic acid-induced necroptosis of endothelial cells. J. Biol. Chem. 2012, 287, 21110-21120.
7. Staiger, H.; Staiger, K.; Stefan, N.; Wahl, H.G.; Machicao, F.; Kellerer, M.; Haring, H.U. Palmitate-induced interleukin-6 expression in human coronary artery endothelial cells. Diabetes 2004, 53, 3209-3216.
8. Cacicedo, J.M.; Benjachareowong, S.; Chou, E.; Ruderman, N.B.; Ido, Y. Palmitate-induced apoptosis in cultured bovine retinal pericytes: roles of NAD(P)H oxidase, oxidant stress, and ceramide. Diabetes 2005, 54, 1838-1845.
9. Kris-Etherton, P.M.; Harris, W.S.; Appel, L.J. Fish consumption, fish oil, omega-3 fatty acids, and cardiovascular disease. Circulation 2002, 106, 2747-2757.
10. Holub, B.J. Dietary fish oils containing eicosapentaenoic acid and the prevention of atherosclerosis and thrombosis. CMAJ 1988, 139, 377-381.
11. Howe, P.R.; Rogers, P.F.; Lungershausen, Y. Blood pressure reduction by fish oil in adult rats with established hypertension--dependence on sodium intake. Prostaglandins Leukot. Essent. Fatty Acids 1991, 44, 113-117.
12. Li, H.; Ruan, X.Z.; Powis, S.H.; Fernando, R.; Mon, W.Y.; Wheeler, D.C.; Moorhead, J.F.; Varghese, Z. EPA and DHA reduce LPS-induced inflammation responses in HK-2 cells: evidence for a PPAR-gamma-dependent mechanism. Kidney Int. 2005, 67, 867-874.
13. Devaraj, S.; Chien, A.; Rao, B.; Chen, X.; Jialal, I. Modulation of endothelial progenitor cell number and function with n-3 polyunsaturated fatty acids. Atherosclerosis 2013, 228, 94-97.
14. Okuda, Y.; Kawashima, K.; Sawada, T.; Tsurumaru, K.; Asano, M.; Suzuki, S.; Soma, M.; Nakajima, T.; Yamashita, K. Eicosapentaenoic acid enhances nitric oxide production by cultured human endothelial cells. Biochem. Biophys. Res. Commun. 1997, 232, 487-491.
15. Balakumar, P.; Taneja, G. Fish oil and vascular endothelial protection: Bench to bedside. Free Radic. Biol. Med. 2012, 53, 271-279.
16. Dyerberg, J.; Bang, H.O.; Stoffersen, E.; Moncada, S.; Vane, J.R. Eicosapentaenoic acid and prevention of thrombosis and atherosclerosis? Lancet 1978, 2, 117-119.
17. Nakajima, K.; Yamashita, T.; Kita, T.; Takeda, M.; Sasaki, N.; Kasahara, K.; Shinohara, M.; Rikitake, Y.; Ishida, T.; Yokoyama, M.; et al. Orally administered eicosapentaenoic acid induces rapid regression of atherosclerosis via modulating the phenotype of dendritic cells in LDL receptor-deficient mice. Arterioscler. Thromb. Vasc. Biol. 2011, 31, 1963-1972.
18. Seifert, R.; Schultz, G. Fatty-acid-induced activation of NADPH oxidase in plasma membranes of human neutrophils depends on neutrophil cytosol and is potentiated by stable guanine nucleotides. Eur. J. Biochem. 1987, 162, 563-569.
19. Yilmaz, A.; Kliche, S.; Mayr-Beyrle, U.; Fellbrich, G.; Waltenberger, J. p38 MAPK inhibition is critically involved in VEGFR-2-mediated endothelial cell survival. Biochem. Biophys. Res. Commun. 2003, 306, 730-736.
20. Xiao, G.F.; Xu, S.H.; Chao, Y.; Xie, L.D.; Xu, C.S.; Wang, H.J. PPARdelta activation inhibits homocysteine-induced p22 expression in EA. hy926 cells through reactive oxygen species/p38MAPK pathway. Eur. J. Pharmacol. 2014, doi:10.1016/j.ejphar.2014.01.051.
21. Mugabo, Y.; Mukaneza, Y.; Renier, G. Palmitate induces C-reactive protein expression in human aortic endothelial cells. Relevance to fatty acid-induced endothelial dysfunction. Metabolism 2011, 60, 640-648.
22. Violi, F.; Basili, S.; Nigro, C.; Pignatelli, P. Role of NADPH oxidase in atherosclerosis. Future Cardiol. 2009, 5, 83-92.
23. Ceolotto, G.; Gallo, A.; Papparella, I.; Franco, L.; Murphy, E.; Iori, E.; Pagnin, E.; Fadini, G.P.; Albiero, M.; Semplicini, A.; et al. Rosiglitazone reduces glucose-induced oxidative stress mediated by NAD(P)H oxidase via AMPK-dependent mechanism. Arterioscler. Thromb. Vasc. Biol. 2007, 27, 2627-2633.
24. Kukidome, D.; Nishikawa, T.; Sonoda, K.; Imoto, K.; Fujisawa, K.; Yano, M.; Motoshima, H.; Taguchi, T.; Matsumura, T.; Araki, E. Activation of AMP-activated protein kinase reduces hyperglycemia-induced mitochondrial reactive oxygen species production and promotes mitochondrial biogenesis in human umbilical vein endothelial cells. Diabetes 2006, 55, 120-127.
25. Ou, H.C.; Lee, W.J.; Wu, C.M.; Chen, J.F.; Sheu, W.H. Aspirin prevents resistin-induced endothelial dysfunction by modulating AMPK, ROS, and Akt/eNOS signaling. J. Vasc. Surg. 2012, 55, 1104-1115.
26. Lu, Y.; Qian, L.; Zhang, Q.; Chen, B.; Gui, L.; Huang, D.; Chen, G.; Chen, L. Palmitate induces apoptosis in mouse aortic endothelial cells and endothelial dysfunction in mice fed high-calorie and high-cholesterol diets. Life Sci. 2013, 92, 1165-1173.
27. Chai, W.; Liu, Z. p38 mitogen-activated protein kinase mediates palmitate-induced apoptosis but not inhibitor of nuclear factor-kappaB degradation in human coronary artery endothelial cells. Endocrinology 2007, 148, 1622-1628.
28. Yuzefovych, L.; Wilson, G.; Rachek, L. Different effects of oleate vs. palmitate on mitochondrial function, apoptosis, and insulin signaling in L6 skeletal muscle cells: role of oxidative stress. Am. J. Physiol. Endocrinol. MeTable 2010, 299, E1096-E1105.
29. Peng, H.B.; Libby, P.; Liao, J.K. Induction and stabilization of I kappa B alpha by nitric oxide mediates inhibition of NF-kappa B. J. Biol. Chem. 1995, 270, 14214-14219.
30. Kempe, S.; Kestler, H.; Lasar, A.; Wirth, T. NF-kappaB controls the global pro-inflammatory response in endothelial cells: evidence for the regulation of a pro-atherogenic program. Nucleic Acids Res. 2005, 33, 5308-5319.
31. Wu, Y.; Zhang, C.; Dong, Y.; Wang, S.; Song, P.; Viollet, B.; Zou, M.H. Activation of the AMP-activated protein kinase by eicosapentaenoic acid (EPA, 20:5 n-3) improves endothelial function in vivo. PLoS One 2012, 7, e35508.
32. Libby, P.; Ridker, P.M.; Maseri, A. Inflammation and atherosclerosis. Circulation 2002, 105, 1135-1143.
33. Calder, P.C. The role of marine omega-3 (n-3) fatty acids in inflammatory processes, atherosclerosis and plaque stability. Mol. Nutr. Food Res. 2012, 56, 1073-1080.
34. Liu, W.; Peng, Y.; Yin, Y.; Zhou, Z.; Zhou, W.; Dai, Y. The Involvement of NADPH Oxidase-Mediated ROS in Cytokine Secretion from Macrophages Induced by Mycobacterium tuberculosis ESAT-6. Inflammation 2014, doi:10.1007/s10753-013-9808-7.
35. Kuo, W.W.; Huang, C.Y.; Chung, J.G.; Yang, S.F.; Tsai, K.L.; Chiu, T.H.; Lee, S.D.; Ou, H.C. Crude extracts of Solanum lyratum protect endothelial cells against oxidized low-density lipoprotein-induced injury by direct antioxidant action. J. Vasc. Surg. 2009, 50, 849-860.
36. 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 1986, 89, 271-277.
37. Huang, H.M.; Ou, H.C.; Hsueh, S.J. Amyloid beta peptide enhanced bradykinin-mediated inositol (1,4,5)trisphosphate formation and cytosolic free calcium. Life Sci. 1998, 63, 195-203.
38. Gavrieli, Y.; Sherman, Y.; Ben-Sasson, S.A. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 1992, 119, 493-501.
39. Wang, L.; Gill, R.; Pedersen, T.L.; Higgins, L.J.; Newman, J.W.; Rutledge, J.C. Triglyceride-rich lipoprotein lipolysis releases neutral and oxidized FFAs that induce endothelial cell inflammation. J. Lipid Res. 2009, 50, 204-213.
40. Chang, W.W.; Liu, J.J.; Liu, C.F.; Liu, W.S.; Lim, Y.P.; Cheng, Y.J.; Lee, C.H. An Extract of Rhodobacter sphaeroides Reduces Cisplatin-Induced Nephrotoxicity in Mice. Toxins 2013, 5, 2353-2365.