Resveratrol prevents endothelial progenitor cells from senescence and reduces the oxidative reaction via PPAR-γ/HO-1 pathways

Molecular Medicine Reports

Volumn 14, Issue 6, 2016, Pages 5528-5534

  Shen, Xiaohua ^a   Wang, Meihui ^a   Bi, Xukun ^a   Zhang, Jiefang ^a   Wen, Shaoxiang ^a   Fu, Guosheng ^a   Xia, Liang ^a  

^a ZHEJIANG UNIVERSITY   (China)

Author keywords

Endothelial progenitor cell; Oxidative reaction; Resveratrol; Senescence

Indexed keywords

HEME OXYGENASE 1; NITRIC OXIDE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; RESVERATROL; ANTIOXIDANT; STILBENE DERIVATIVE; TELOMERASE; TERT PROTEIN, HUMAN;

ADULT; AEROBIC METABOLISM; ANIMAL EXPERIMENT; ARTERY INTIMA PROLIFERATION; ARTICLE; CARDIOVASCULAR SYSTEM; CELL PROTECTION; CONTROLLED STUDY; ENDOTHELIAL PROGENITOR CELL; ENZYME ACTIVITY; FEMALE; HUMAN; HUMAN EXPERIMENT; MALE; MYOCARDIAL ISCHEMIA REPERFUSION INJURY; NONHUMAN; NORMAL HUMAN; SENESCENCE; SIGNAL TRANSDUCTION; THROMBOCYTE ADHESION; THROMBOCYTE AGGREGATION; WESTERN BLOTTING; ANIMAL; CELL AGING; CELL CULTURE; DRUG EFFECTS; GENE EXPRESSION; GENETICS; METABOLISM; OXIDATIVE STRESS; RABBIT;

ADULT; ANIMALS; ANTIOXIDANTS; CELL AGING; CELLS, CULTURED; ENDOTHELIAL PROGENITOR CELLS; FEMALE; GENE EXPRESSION; HEME OXYGENASE-1; HUMANS; MALE; NITRIC OXIDE; OXIDATIVE STRESS; PPAR GAMMA; RABBITS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; STILBENES; TELOMERASE;

EID: 84999176915     PISSN: 17912997     EISSN: 17913004     Source Type: Journal    
DOI: 10.3892/mmr.2016.5929     Document Type: Article

References (38)

1. Shi Q, Rafli S, Wu MH, Wijelath ES, Yu C, Ishida A, Fujita Y, Kothari S, Mohle R, Sauvage LR, et al: Evidence for circulating bone marrow-derived endothelial cells. Blood 92: 362-367, 1998.
2. Asahara T, Masuda H, Takahashi T, Kalka C, Pastore C, Silver M, Kearne M, Magner M and Isner JM: 'Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization'. Circ Res 85: 221-228, 1999.
3. Werner N and Nickenig G: Influence of cardiovascular risk factors on endothelial progenitor cells: Limitations for therapy? Arterioscler Thromb Vasc Biol 26: 257-266, 2006.
4. Thum T and Bauersachs J: Endothelial progenitor cells as potential drug targets. Curr Drug Targets Cardiovasc Haematol Disord 5: 277-286, 2005.
5. Agarwal B and Baur JA: Resveratrol and life extension. Ann N Y Acad Sci 1215: 138-143, 2011.
6. Borriello A, Bencivenga D, Caldarelli I, Tramontano A, Borgia A, Zappia V and Della Ragione F: Resveratrol: From basic studies to bedside. Cancer Treat Res 159: 167-184, 2014.
7. Marques FZ, Markus MA and Morris BJ: Resveratrol: Cellular actions of a potent natural chemical that confers a diversity of health benefits. Int J Biochem Cell Biol 41: 2125-2128, 2009.
8. Xia L, Wang XX, Hu XS, Guo XG, Shang YP, Chen HJ, Zeng CL, Zhang FR and Chen JZ: Resveratrol reduces endothelial progenitor cells senescence through augmentation of telomerase activity by Akt-dependent mechanisms. Br J Pharmacol 155: 387-394, 2008.
9. Zheng H, Fu G, Dai T and Huang H: Migration of endothelial progenitor cells mediated by stromal cell-derived factor-1alpha/CXCR4 via PI3K/Akt/eNOS signal transduction pathway. J Cardiovasc Pharmacol 50: 274-280, 2007.
10. Zheng H, Dai T, Zhou B, Zhu J, Huang H, Wang M and Fu G: SDF-1alpha/CXCR4 decreases endothelial progenitor cells apoptosis under serum deprivation by PI3K/Akt/eNOS pathway. Atherosclerosis 201: 36-42, 2008.
11. Assmus B, Urbich C, Aicher A, Hofmann WK, Haendeler J, Rössig L, Spyridopoulos I, Zeiher AM and Dimmeler S: HMG-CoA reductase inhibitors reduce senescence and increase proliferation of endothelial progenitor cells via regulation of cell cycle regulatory genes. Circ Res 92: 1049-1055, 2003.
12. Lindner V, Fingerle J and Reidy MA: Mouse model of arterial injury. Circ Res 73: 792-796, 1993.
13. Opie LH and Lecour S: The red wine hypothesis: From concepts to protective signalling molecules. Eur Heart J 28: 1683-1693, 2007.
14. Wang XB, Huang J, Zou JG, Su EB, Shan QJ, Yang ZJ and Cao KJ: Effects of resveratrol on number and activity of endothelial progenitor cells from human peripheral blood. Clin Exp Pharmacol Physiol 34: 1109-1115, 2007.
15. Aggarwal BB, Bhardwaj A, Aggarwal RS, Seeram NP, Shishodia S and Takada Y: Role of resveratrol in prevention and therapy of cancer: Preclinical and clinical studies. Anticancer Res 24: 2783-2840, 2004.
16. Wang Q, Li H, Wang XW, Wu DC, Chen XY and Liu J: Resveratrol promotes differentiation and induces Fas-independent apoptosis of human medulloblastoma cells. Neurosci Lett 351: 83-86, 2003.
17. Delmas D, Rébé C, Lacour S, Filomenko R, Athias A, Gambert P, Cherkaoui-Malki M, Jannin B, Dubrez-Daloz L, Latruffe N and Solary E: Resveratrol-induced apoptosis isassociated with Fas redistribution in the rafts and the formation of a death-inducing signaling complex in colon cancer cells. J Biol Chem 278: 41482-41490, 2003.
18. Bernhard D, Tinhofer I, Tonko M, Hübl H, Ausserlechner MJ, Greil R, Kofler R and Csordas A: Resveratrol causes arrest in the S-phase prior to Fas-independent apoptosis in CEM-C7H2 acute leukemia cells. Cell Death Differ 7: 834-842, 2000.
19. Dörrie J, Gerauer H, Wachter Y and Zunino SJ: Resveratrol induces extensive apoptosis by depolarizing mitochondrial membranes and activating caspase-9 in acute lymphoblastic leukemia cells. Cancer Res 61: 4731-4739, 2001.
20. Borriello A, Bencivenga D, Caldarelli I, Tramontano A, Borgia A, Zappia V and Della Ragione F: Resveratrol: From basic studies to bedside. Cancer Treat Res 159: 167-184, 2014.
21. Balestrieri ML, Schiano C, Felice F, Casamassimi A, Balestrieri A, Milone L, Servillo L and Napoli C: Effect of low doses of red wine and pure resveratrol on circulating endothelial progenitor cells. J Biochem 143: 179-186, 2008.
22. Xia L, Wang XX, Hu XS, Guo XG, Shang YP, Chen HJ, Zeng CL, Zhang FR and Chen JZ: Resveratrol reduces endothelial progenitor cells senescence through augmentation of telomerase activity by Akt-dependent mechanisms. Br J Pharmacol 155: 387-394, 2008.
23. Imanishi T, Hano T, Sawamura T and Nishio I: Oxidized low-density lipoprotein induces endothelial progenitor cell senescence, leading to cellular dysfunction. Clin Exp Pharmacol Physiol 31: 407-413, 2004.
24. Imanishi T, Hano T and Nishio I: Angiotensin II accelerates endothelial progenitor cell senescence through induction of oxidative stress. J Hypertens 23: 97-104, 2005.
25. Bao XM, Wu CF and Lu GP: Atorvastatin inhibits homocysteine-induced oxidative stress and apoptosis in endothelial progenitor cells involving Nox4 and p38MAPK. Atherosclerosis 210: 114-121, 2010.
26. Sorrentino SA, Bahlmann FH, Besler C, Müller M, Schulz S, Kirchhoff N, Doerries C, Horváth T, Limbourg A, Limbourg F, et al: Oxidant stress impairs in vivo reendothelialization capacity of endothelial progenitor cells from patients with type 2 diabetes mellitus: Restoration by the peroxisome proliferator-activated receptor-gamma agonist rosiglitazone. Circulation 116: 163-173, 2007.
27. Carluccio MA, Ancora MA, Massaro M, Carluccio M, Scoditti E, Distante A, Storelli C and De Caterina R: Homocysteine induces VCAM-1 gene expression through NF-kappaB and NAD(P)H oxidase activation: protective role of Mediterranean diet polyphenolic antioxidants. Am J Physiol Heart Circ Physiol 293: H2344-H2354, 2007.
28. Zhang H, Zhang J, Ungvari Z and Zhang C: Resveratrol improves endothelial function: Role of TNF{alpha} and vascular oxidative stress. Arterioscler Thromb Vasc Biol 29: 1164-171, 2009.
29. Werner C, Kamani CH, Gensch C, Böhm M and Laufs U: The peroxisome proliferator-activated receptor-gamma agonist pioglitazone increases number and function of endothelial progenitor cells in patients with coronary artery disease and normal glucose tolerance. Diabetes 56: 2609-2615, 2007.
30. Imanishi T, Kobayashi K, Kuroi A, Ikejima H and Akasaka T: Pioglitazone inhibits angiotensin II-induced senescence of endothelial progenitor cell. Hypertens Res 31: 757-765, 2008.
31. Honda A, Matsuura K, Fukushima N, Tsurumi Y, Kasanuki H and Hagiwara N: Telmisartan induces proliferation of human endothelial progenitor cells via PPARgamma-dependent PI3K/Akt pathway. Atherosclerosis 205: 376-384, 2009.
32. Krönke G, Kadl A, Ikonomu E, Blüml S, Fürnkranz A, Sarembock IJ, Bochkov VN, Exner M, Binder BR and Leitinger N: Expression of heme oxygenase-1 in human vascular cells is regulated by peroxisome proliferator-activated receptors. Arterioscler Thromb Vasc Biol 27: 1276-1282, 2007.
33. Abraham NG and Kappas A: Pharmacological and clinical aspects of heme oxygenase. Pharmacol Rev 60: 79-127, 2008.
34. Kruger AL, Peterson SJ, Schwartzman ML, Fusco H, McClung JA, Weiss M, Shenouda S, Goodman AI, Goligorsky MS, Kappas A and Abraham NG: Up-regulation of heme oxygenase provides vascular protection in an animal model of diabetes through its antioxidant and antiapoptotic effects. J Pharmacol Exp Ther 319: 1144-1152, 2006.
35. Thirunavukkarasu M, Penumathsa SV, Koneru S, Juhasz B, Zhan L, Otani H, Bagchi D, Das DK and Maulik N: Resveratrol alleviates cardiac dysfunction in streptozotocin-induced diabetes: Role of nitric oxide, thioredoxin, and heme oxygenase. Free Radic Biol Med 43: 720-729, 2007.
36. Das S, Fraga CG and Das DK: Cardioprotective effect of resveratrol via HO-1 expression involves p38 map kinase and PI-3-kinase signaling, but does not involve NFkappaB. Free Radic Res 40: 1066-1075, 2006.
37. Deshane J, Chen S, Caballero S, Grochot-Przeczek A, Was H, Li Calzi S, Lach R, Hock TD, Chen B, Hill-Kapturczak N, et al: Stromal cell-derived factor 1 promotes angiogenesis via a heme oxygenase 1-dependent mechanism. J Exp Med 204: 605-618, 2007.
38. Wu BJ, Midwinter RG, Cassano C, Beck K, Wang Y, Changsiri D, Gamble JR and Stocker R: Heme oxygenase-1 increases endothelial progenitor cells. Arterioscler Thromb Vasc Biol 29: 1537-1542, 2009.