Berberine protects endothelial progenitor cell from damage of TNF-α via the PI3K/AKT/eNOS signaling pathway

European Journal of Pharmacology

Volumn 743, Issue , 2014, Pages 11-16

  Xiao, Min ^a   Men, Li Na ^a   Xu, Ming Guo ^a   Wang, Guo Bing ^a   Lv, Hai Tao ^b   Liu, Cong ^a  

^a Shenzhen Children's Hospital   (China)

^b CHILDREN S HOSPITAL OF SOOCHOW UNIVERSITY   (China)

Author keywords

AKT (Serine threonine protein kinase B); Berberine; Endothelial progenitorcells; eNOS (endothelial Nitric Oxide Synthase); PI3K (Phosphatidyl Inositol 3 kinase); TNF (Tumor Necrosis Factor )

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; BERBERINE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; MESSENGER RNA; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; TUMOR NECROSIS FACTOR ALPHA; NOS3 PROTEIN, HUMAN; PROTECTIVE AGENT;

ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; ENDOTHELIAL PROGENITOR CELL; HUMAN; HUMAN CELL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; CELL CULTURE; DRUG EFFECTS; ENDOTHELIUM; ENDOTHELIUM CELL; METABOLISM;

BERBERINE; CELL PROLIFERATION; CELLS, CULTURED; ENDOTHELIAL CELLS; ENDOTHELIAL PROGENITOR CELLS; ENDOTHELIUM; HUMANS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; PHOSPHATIDYLINOSITOL 3-KINASES; PROTECTIVE AGENTS; PROTO-ONCOGENE PROTEINS C-AKT; RNA, MESSENGER; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84918806524     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2014.09.024     Document Type: Article

References (43)

1. F. Affuso, V. Mercurio, V. Fazio, and S. Fazio Cardiovascular and metabolic effects of Berberine World J. Cardiol. 2 2010 71 77
2. T. Asahara, T. Murohara, A. Sullivan, M. Silver, R. van der Zee, T. Li, B. Witzenbichler, G. Schatteman, and J.M. Isner Isolation of putative progenitor endothelial cells for angiogenesis Science 275 1997 964 967
3. X. Bai, X. Wang, and Q. Xu Endothelial damage and stem cell repair in atherosclerosis Vasc. Pharmacol. 52 2010 224 229
4. W. Bakker, E.C. Eringa, P. Sipkema, and V.W. van Hinsbergh Endothelial dysfunction and diabetes: roles of hyperglycemia, impaired insulin signaling and obesity Cell Tissue Res. 335 2009 165 189
5. B.C. Berk Atheroprotective signaling mechanisms activated by steady laminar flow in endothelial cells Circulation 117 2008 1082 1089
6. H. Bruunsgaard, P. Skinhoj, A.N. Pedersen, M. Schroll, and B.K. Pedersen Ageing, tumour necrosis factor-alpha (TNF-alpha) and atherosclerosis Clin. Exp. Immunol. 121 2000 255 260
7. K. Chen, G. Li, F. Geng, Z. Zhang, J. Li, M. Yang, L. Dong, and F. Gao Berberine reduces ischemia/reperfusion-induced myocardial apoptosis via activating AMPK and PI3K-Akt signaling in diabetic rats Apoptosis 19 2014 946 957
8. X. Chen, Q. Chen, L. Wang, and G. Li Ghrelin induces cell migration through GHSR1a-mediated PI3K/Akt/eNOS/NO signaling pathway in endothelial progenitor cells Metabolism 62 2013 743 752
9. Y.H. Chien, K.W. Chang, Y.H. Yang, M.Y. Lu, Y.T. Lin, and B.L. Chiang Association between levels of TNF-alpha and TNF-alpha promoter -308 A/A polymorphism in children with Kawasaki disease J. Formos. Med. Assoc. 102 2003 147 150
10. M.M. de Resende, L.Y. Huw, H.S. Qian, and K. Kauser Role of endothelial nitric oxide in bone marrow-derived progenitor cell mobilization Handb. Exp. Pharmacol. 2007 37 44
11. G. Derosa, P. Maffioli, and A.F. Cicero Berberine on metabolic and cardiovascular risk factors: an analysis from preclinical evidences to clinical trials Expert Opin. Biol. Ther. 12 2012 1113 1124
12. B.R. Everaert, E.M. Van Craenenbroeck, V.Y. Hoymans, S.E. Haine, L. Van Nassauw, V.M. Conraads, J.P. Timmermans, and C.J. Vrints Current perspective of pathophysiological and interventional effects on endothelial progenitor cell biology: focus on PI3K/AKT/eNOS pathway Int. J. Cardiol. 144 2010 350 366
13. R.S. Frey, M. Ushio-Fukai, and A.B. Malik NADPH oxidase-dependent signaling in endothelial cells: role in physiology and pathophysiology Antioxid. Redox Signal. 11 2009 791 810
14. A.L. George, P. Bangalore-Prakash, S. Rajoria, R. Suriano, A. Shanmugam, A. Mittelman, and R.K. Tiwari Endothelial progenitor cell biology in disease and tissue regeneration J. Hematol. Oncol. 4 2011 24
15. J.M. Hill, G. Zalos, J.P. Halcox, W.H. Schenke, M.A. Waclawiw, A.A. Quyyumi, and T. Finkel Circulating endothelial progenitor cells, vascular function, and cardiovascular risk N. Engl. J. Med. 348 2003 593 600
16. J.S. Hui-Yuen, T.T. Duong, and R.S. Yeung TNF-alpha is necessary for induction of coronary artery inflammation and aneurysm formation in an animal model of Kawasaki disease J. Immunol. 176 2006 6294 6301
17. M. Ii, K. Takeshita, K. Ibusuki, C. Luedemann, A. Wecker, E. Eaton, T. Thorne, T. Asahara, J.K. Liao, and D.W. Losordo Notch signaling regulates endothelial progenitor cell activity during recovery from arterial injury in hypercholesterolemic mice Circulation 121 2010 1104 1112
18. D.G. Kang, E.J. Sohn, E.K. Kwon, J.H. Han, H. Oh, and H.S. Lee Effects of berberine on angiotensin-converting enzyme and NO/cGMP system in vessels Vasc. Pharmacol. 39 2002 281 286
19. R. Kawabe-Yako, M. Ii, O. Masuo, T. Asahara, and T. Itakura Cilostazol activates function of bone marrow-derived endothelial progenitor cell for re-endothelialization in a carotid balloon injury model PLoS One 6 2011 e24646
20. W.H. Ko, X.Q. Yao, C.W. Lau, W.I. Law, Z.Y. Chen, W. Kwok, K. Ho, and Y. Huang Vasorelaxant and antiproliferative effects of berberine Eur. J. Pharmacol. 399 2000 187 196
21. C.W. Lee, P.H. Huang, S.S. Huang, H.B. Leu, C.C. Huang, T.C. Wu, J.W. Chen, and S.J. Lin Decreased circulating endothelial progenitor cell levels and function in essential hypertensive patients with electrocardiographic left ventricular hypertrophy Hypertens. Res. 34 2011 999 1003
22. X.D. Li, Y.T. Cheng, Y.J. Yang, X.M. Meng, J.L. Zhao, H.T. Zhang, Y.J. Wu, S.J. You, and Y.L. Wu PKA-mediated eNOS phosphorylation in the protection of ischemic preconditioning against no-reflow Microvasc. Res. 84 2012 44 54
23. N.R. London, K.J. Whitehead, and D.Y. Li Endogenous endothelial cell signaling systems maintain vascular stability Angiogenesis 12 2009 149 158
24. T. Nystrom, A. Nygren, and A. Sjoholm Increased levels of tumour necrosis factor-alpha (TNF-alpha) in patients with Type II diabetes mellitus after myocardial infarction are related to endothelial dysfunction Clin. Sci. 110 2006 673 681
25. T. Oharaseki, Y. Yokouchi, H. Yamada, H. Mamada, S. Muto, K. Sadamoto, N. Miura, N. Ohno, T. Saji, S. Naoe, and K. Takahashi The role of TNF-alpha in a murine model of Kawasaki disease arteritis induced with a Candida albicans cell wall polysaccharide Mod. Rheumatol. 24 2014 120 128
26. A. Petrelli, R. Di Fenza, M. Carvello, F. Gatti, A. Secchi, and P. Fiorina Strategies to reverse endothelial progenitor cell dysfunction in diabetes Exp. Diabetes Res. 2012 2012 471823
27. D.M. Smadja, A. Cornet, J. Emmerich, M. Aiach, and P. Gaussem Endothelial progenitor cells: characterization, in vitro expansion, and prospects for autologous cell therapy Cell. Biol. Toxicol. 23 2007 223 239
28. K. Strehlow, N. Werner, J. Berweiler, A. Link, U. Dirnagl, J. Priller, K. Laufs, L. Ghaeni, M. Milosevic, M. Bohm, and G. Nickenig Estrogen increases bone marrow-derived endothelial progenitor cell production and diminishes neointima formation Circulation 107 2003 3059 3065
29. Y. Tang, B. Huang, L. Sun, X. Peng, X. Chen, and X. Zou Ginkgolide B promotes proliferation and functional activities of bone marrow-derived endothelial progenitor cells: involvement of Akt/eNOS and MAPK/p38 signaling pathways Eur. Cell Mater. 21 2011 459 469
30. B. Thors, H. Halldorsson, and G. Thorgeirsson eNOS activation mediated by AMPK after stimulation of endothelial cells with histamine or thrombin is dependent on LKB1 Biochim. Biophys. Acta 1813 2011 322 331
31. Y. Wang, W. Yan, X. Lu, C. Qian, J. Zhang, P. Li, L. Shi, P. Zhao, Z. Fu, P. Pu, C. Kang, T. Jiang, N. Liu, and Y. You Overexpression of osteopontin induces angiogenesis of endothelial progenitor cells via the avbeta3/PI3K/AKT/eNOS/NO signaling pathway in glioma cells Eur. J. Cell. Biol. 90 2011 642 648
32. P.E. Westerweel, and M.C. Verhaar Endothelial progenitor cell dysfunction in rheumatic disease Nat. Rev. Rheumatol. 5 2009 332 340
33. M.G. Xu, L.N. Men, C.Y. Zhao, X. Zhao, Y.X. Wang, X.C. Meng, D.R. Shen, B.Y. Meng, Q. Zhang, and T. Wang The number and function of circulating endothelial progenitor cells in patients with Kawasaki disease Eur. J. Pediatr. 169 2010 289 296
34. M.G. Xu, L.N. Men, Y. Zu, C.Y. Zhao, X.C. Meng, and T. Wang The functions of endothelial progenitor cells were significantly improved after treatment with intravenous immunoglobulin and aspirin in children with Kawasaki disease Pediatr. Cardiol. 32 2011 455 460
35. M.G. Xu, J.M. Wang, L. Chen, Y. Wang, Z. Yang, and J. Tao Berberine-induced upregulation of circulating endothelial progenitor cells is related to nitric oxide production in healthy subjects Cardiology 112 2009 279 286
36. S. Xu, H. Jiang, B. Wu, J. Yang, and S. Chen Urotensin II induces migration of endothelial progenitor cells via activation of the RhoA/Rho kinase pathway Tohoku J. Exp. Med. 219 2009 283 288
37. S. Xu, Y. Zhao, L. Yu, X. Shen, F. Ding, and G. Fu Rosiglitazone attenuates endothelial progenitor cell apoptosis induced by TNF-alpha via ERK/MAPK and NF-kappaB signal pathways J. Pharmacol. Sci. 117 2011 265 274
38. N. Yang, S. Qin, M. Wang, B. Chen, N. Yuan, Y. Fang, S. Yao, P. Jiao, Y. Yu, Y. Zhang, and J. Wang Pinocembrin, a major flavonoid in propolis, improves the biological functions of EPCs derived from rat bone marrow through the PI3K-eNOS-NO signaling pathway Cytotechnology 65 2013 541 551
39. S. Yu, S.L. Wong, C.W. Lau, Y. Huang, and C.M. Yu Oxidized LDL at low concentration promotes in-vitro angiogenesis and activates nitric oxide synthase through PI3K/Akt/eNOS pathway in human coronary artery endothelial cells Biochem. Biophys. Res. Commun. 407 2011 44 48
40. X. Yu, M. Song, J. Chen, G. Zhu, G. Zhao, H. Wang, and L. Hunag Hepatocyte growth factor protects endothelial progenitor cell from damage of low-density lipoprotein cholesterol via the PI3K/Akt signaling pathway Mol. Biol. Rep. 37 2010 2423 2429
41. Y. Zhang, B.S. Herbert, G. Rajashekhar, D.A. Ingram, M.C. Yoder, M. Clauss, and J. Rehman Premature senescence of highly proliferative endothelial progenitor cells is induced by tumor necrosis factor-alpha via the p38 mitogen-activated protein kinase pathway FASEB J. 23 2009 1358 1365
42. X. Zhao, D. Qian, N. Wu, Y. Yin, J. Chen, B. Cui, and L. Huang The spleen recruits endothelial progenitor cell via SDF-1/CXCR4 axis in mice J. Recept. Signal Transduct. Res. 30 2010 246 254
43. H. Zheng, G. Fu, T. Dai, and H. Huang Migration of endothelial progenitor cells mediated by stromal cell-derived factor-1alpha/CXCR4 via PI3K/Akt/eNOS signal transduction pathway J. Cardiovasc. Pharmacol. 50 2007 274 280