Hydroxytyrosol induces proliferation and cytoprotection against oxidative injury in vascular endothelial cells: Role of Nrf2 activation and HO-1 induction

Journal of Agricultural and Food Chemistry

Volumn 59, Issue 9, 2011, Pages 4473-4482

  Zrelli, Houda ^a   Matsuoka, Mieko ^a   Kitazaki, Shiho ^a   Araki, Masahiro ^a   Kusunoki, Miki ^a   Zarrouk, Mokhtar ^b   Miyazaki, Hitoshi ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

^b Borj Cedria Higher Institute of Sciences and Technology of Environment   (Tunisia)

Author keywords

Atherosclerosis; Hydroxytyrosol; Nrf2; Oxidative stress; Proliferation; Vascular endothelial cells

Indexed keywords

ATHEROSCLEROSIS; HYDROXYTYROSOL; NRF2; PROLIFERATION; VASCULAR ENDOTHELIAL CELLS;

CELL PROLIFERATION; DISEASES; OXIDATIVE STRESS; OXYGEN; PHENOLS; VEGETABLE OILS;

ENDOTHELIAL CELLS;

3,4-DIHYDROXYPHENYLETHANOL; DRUG DERIVATIVE; HEME OXYGENASE 1; HYDROGEN PEROXIDE; HYDROXYTYROSOL; PHENETHYL ALCOHOL; PROTECTIVE AGENT; TRANSCRIPTION FACTOR NRF2;

ANIMAL; ARTICLE; CELL CULTURE; CELL PROLIFERATION; CYTOLOGY; DRUG EFFECT; ENDOTHELIUM CELL; ENZYMOLOGY; GENE EXPRESSION; GENETICS; METABOLISM; SWINE;

ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; ENDOTHELIAL CELLS; GENE EXPRESSION; HEME OXYGENASE-1; HYDROGEN PEROXIDE; NF-E2-RELATED FACTOR 2; PHENYLETHYL ALCOHOL; PROTECTIVE AGENTS; SWINE;

EID: 79955680290     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf104151d     Document Type: Article

References (45)

1. Covas, M. I. Benefits of the Mediterranean diet on cardiovascular disease. Future Cardiol. 2007, 3, 575-578.
2. Ortega, R. Importance of functional foods in the Mediterranean diet. Public Health Nutr. 2006, 9, 1136-1140.
3. Carluccio, M. A.; Massaro, M.; Scoditti, E.; De Caterina, R. Vasculoprotective potential of olive oil components. Mol. Nutr. Food Res. 2007, 51, 1225-1234. (Pubitemid 350017475)
4. Waterman, E.; Lockwood, B. Active components and clinical applications of olive oil. Altern. Med. Rev. 2007, 12, 331-342.
5. Covas, M. I.; Konstantinidou, V.; Fitó, M. Olive oil and cardiovascular health. J. Cardiovasc. Pharmacol. 2009, 54, 477-482.
6. Fitó, M.; de la Torre, R.; Covas, M. I. Olive oil and oxidative stress. Mol. Nutr. Food Res. 2007, 51, 1215-1224. (Pubitemid 350013169)
7. Perona, J. S.; Cabello-Moruno, R.; Ruiz-Gutierrez, V. J. The role of virgin olive oil components in the modulation of endothelial function. Nutr. Biochem. 2006, 17, 429-445. (Pubitemid 43867255)
8. Granados-Principal, S.; Quiles, J. L.; Ramirez-Tortosa, C. L.; Sanchez-Rovira, P.; Ramirez-Tortosa, M. C. Hydroxytyrosol: from laboratory investigations to future clinical trials. Nutr. Rev. 2010, 68, 191-206.
9. Bullon, P.; Quiles, J. L.; Morillo, J. M.; Rubini, C.; Goteri, G.; Granados-Principal, S.; Battino, M.; Ramirez-Tortosa, M. Gingival vascular damage in atherosclerotic rabbits: hydroxytyrosol and squalene benefits. Food Chem. Toxicol. 2009, 47, 2327-2331.
10. González-Santiago, M.; Martín-Bautista, E.; Carrero, J. J.; Fonollá, J.; Baró, L.; Bartolomé, M. V.; Gil-Loyzaga, P.; López-Huertas, E. One-month administration of hydroxytyrosol, a phenolic antioxidant present in olive oil, to hyperlipemic rabbits improves blood lipid profile, antioxidant status and reduces atherosclerosis development. Atherosclerosis 2006, 188, 35-42. (Pubitemid 44142530)
11. Jemai, H.; Fki, I.; Bouaziz, M.; Bouallagui, Z.; El Feki, A.; Isoda, H.; Sayadi, S. Lipid-lowering and antioxidant effects of hydroxytyrosol and its triacetylated derivative recovered from olive tree leaves in cholesterol-fed rats. J. Agric. Food Chem. 2008, 56, 2630-2636. (Pubitemid 351685203)
12. Rietjens, S. J.; Bast, A.; de Vente, J.; Haenen, G. R. The olive oil antioxidant hydroxytyrosol efficiently protects against the oxidative stress-induced impairment of the NObullet response of isolated rat aorta. Am. J. Physiol. Heart Circ. Physiol. 2007, 292, H1931-H1936. (Pubitemid 46572418)
13. Dell'Agli, M.; Fagnani, R.; Mitro, N.; Scurati, S.; Masciadri, M.; Mussoni, L.; Galli, G. V.; Bosisio, E.; Crestani, M.; De Fabiani, E.; Tremoli, E.; Caruso, D. Minor components of olive oil modulate proatherogenic adhesion molecules involved in endothelial activation. J. Agric. Food Chem. 2006, 54, 3259-3264. (Pubitemid 43798194)
14. Surh, Y. J.; Kundu, J. K.; Na, H. K. Nrf2 as a master redox switch in turning on the cellular signaling involved in the induction of cytoprotective genes by some chemopreventive phytochemicals. Planta Med. 2008, 74, 1526-1539.
15. Mann, G. E.; Niehueser-Saran, J.; Watson, A.; Gao, L.; Ishii, T.; de Winter, P.; Siow, R. C. Nrf2/ARE regulated antioxidant gene expression in endothelial and smooth muscle cells in oxidative stress: implications for atherosclerosis and preeclampsia. Sheng Li Xue Bao 2007, 59, 117-127.
16. Motohashi, H.; Yamamoto, M. Nrf2-Keap1 defines a physiologically important stress response mechanism. Trends Mol. Med. 2004, 11, 549-557. (Pubitemid 39433824)
17. Nguyen, T.; Nioi, P.; Pickett, C. B. The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress. J. Biol. Chem. 2009, 284, 13291-13295.
18. Osburn, W. O.; Kensler, T. W. Nrf2 signaling: an adaptive response pathway for protection against environmental toxic insults. Mutat. Res. 2009, 659, 31-39.
19. Satoh, T.; Kosaka, K.; Itoh, K.; Kobayashi, A.; Yamamoto, M.; Shimojo, Y.; Kitajima, C.; Cui, J.; Kamins, J.; Okamoto, S.; Izumi, M.; Shirasawa, T.; Lipton, S. A. Carnosic acid, a catechol-type electrophilic compound, protects neurons both in vitro and in vivo through activation of the Keap1/Nrf2 pathway via S-alkylation of targeted cysteines on Keap1. J. Neurochem. 2008, 104, 1116-1131. (Pubitemid 351143643)
20. 2-induced apoptosis through Nrf2-mediated upregulation of heme oxygenase-1: potential roles of Akt and ERK1/ 2. Biochem. Pharmacol. 2008, 76, 1577-1589.
21. Kim, K. C.; Kang, K. A.; Zhang, R.; Piao, M. J.; Kim, G. Y.; Kang, M. Y.; Lee, S. J.; Lee, N. H.; Surh, Y. J.; Hyun, J. W. Up-regulation of Nrf2-mediated heme oxygenase-1 expression by eckol, a phlorotannin compound, through activation of Erk and PI3K/Akt. Int. J. Biochem. Cell Biol. 2010, 42, 297-305.
22. Na, H. K.; Kim, E. H.; Jung, J. H.; Lee, H. H.; Hyun, J. W.; Surh, Y. J. (-)-Epigallocatechin gallate induces Nrf2-mediated antioxidant enzyme expression via activation of PI3K and ERK in human mammary epithelial cells. Arch. Biochem. Biophys. 2008, 476, 171-177.
23. Niture, S. K.; Jain, A. K.; Jaiswal, A. K. Antioxidant-induced modification of INrf2 cysteine 151 and PKC-δ-mediated phosphorylation of Nrf2 serine 40 are both required for stabilization and nuclear translocation of Nrf2 and increased drug resistance. J. Cell Sci. 2009, 122, 4452-4464.
24. Carluccio, M. A.; Ancora, M. A.; Massaro, M.; Carluccio, M.; Scoditti, E.; Distante, A.; Storelli, C.; De Caterina, R. Homocysteine induces VCAM-1 gene expression through NF-κB andNAD(P)Hoxidase activation: protective role ofMediterranean diet polyphenolic antioxidants. Am. J. Physiol. Heart Circ. Physiol. 2007, 293, H2344-H2354. (Pubitemid 47605880)
25. Carluccio, M. A.; Siculella, L.; Ancora, M. A.; Massaro, M.; Scoditti, E.; Storelli, C.; Visioli, F.; Distante, A.; De Caterina, R. Olive oil and red wine antioxidant polyphenols inhibit endothelial activation: antiatherogenic properties of Mediterranean diet phytochemicals. Arterioscler. Thromb. Vasc. Biol. 2003, 23, 622-629. (Pubitemid 36438075)
26. Manna, C.; Napoli, D.; Cacciapuoti, G.; Porcelli, M.; Zappia, V. Olive oil phenolic compounds inhibit homocysteine-induced endothelial cell adhesion regardless of their different antioxidant activity. J. Agric. Food Chem. 2009, 57, 3478-3482.
27. Watanabe, H.; Kuhne, W.; Spahr, R.; Schwartz, P.; Piper, H. M. Macromolecule permeability of coronary and aortic endothelial monolayers under energy depletion. Am. J. Physiol. 1991, 260, H1344-H1352.
28. Shimizu, H.; Toyama, O.; Shiota, M.; Kim-Mitsuyama, S.; Miyazaki, H. Protein tyrosine phosphatase LMW-PTP exhibits distinct roles between vascular endothelial and smooth muscle cells. J. Recept. Signal Transduct Res. 2005, 25, 19-33. (Pubitemid 40780995)
29. Shimizu, H.; Hirose, Y.; Nishijima, F.; Tsubakihara, Y.; Miyazaki, H. ROS and PDGF-beta receptors are critically involved in indoxyl sulfate actions that promote vascular smooth muscle cell proliferation and migration. Am. J. Physiol. Cell Physiol. 2009, 297, C389-C396.
30. Lee, H.; Goetzl, E. J.; An, S. Lysophosphatidic acid and sphingosine 1-phosphate stimulate endothelial cell wound healing. Am. J. Physiol. Cell Physiol. 2000, 278, C612-C618. (Pubitemid 30154941)
31. Martín,M.A.;Ramos,S.;Granado-Serrano,A.B.;Rodríguez-Ramiro, I.; Trujillo, M.; Bravo, L.; Goya, L. Hydroxytyrosol induces antioxidant/ detoxificant enzymes and Nrf2 translocation via extracellular regulated kinases and phosphatidylinositol-3-kinase/protein kinase B pathways in HepG2 cells. Mol. Nutr. Food Res. 2010, 54, 956-966.
32. Itoh, K.; Tong, K. I.; Yamamoto, M. Molecular mechanism activating Nrf2-Keap1 pathway in regulation of adaptive response to electrophiles. Free Radic. Biol. Med. 2004, 36, 1208-1213. (Pubitemid 38526314)
33. Jaiswal, A. K. Nrf2 signaling in coordinated activation of antioxidant gene expression. Free Radical Biol. Med. 2004, 36, 1199-1207. (Pubitemid 38526313)
34. Homma, S.; Ishii, Y.; Morishima, Y.; Yamadori, T.; Matsuno, Y.; Haraguchi, N.; Kikuchi, N.; Satoh, H.; Sakamoto, T.; Hizawa, N.; Itoh, K.; Yamamoto, M. Nrf2 enhances cell proliferation and resistance to anticancer drugs in human lung cancer. Clin. Cancer Res. 2009, 15, 3423-3432.
35. Reddy, N. M.; Kleeberger, S. R.; Bream, J. H.; Fallon, P. G.; Kensler, T. W.; Yamamoto, M.; Reddy, S. P. Genetic disruption of the Nrf2 compromises cell-cycle progression by impairing GSH-induced redox signaling. Oncogene 2008, 27, 5821-5832.
36. Choi, B. M.; Kim, B. R. Upregulation of heme oxygenase-1 by brazilin via the phosphatidylinositol 3-kinase/Akt and ERK pathways and its protective effect against oxidative injury. Eur. J. Pharmacol. 2008, 580, 12-18.
37. Hwang, Y. P.; Jeong, H. G. The coffee diterpene kahweol induces heme oxygenase-1 via the PI3K and p38/Nrf2 pathway to protect human dopaminergic neurons from 6-hydroxydopamine-derived oxidative stress. FEBS Lett. 2008, 582, 2655-2662.
38. Ogborne,R.M.;Rushworth, S.A.;O'Connell, M. A. Epigallocatechin activates haem oxygenase-1 expression via protein kinase Cδ and Nrf2. Biochem. Biophys. Res. Commun. 2008, 373, 584-588.
39. Chen, M. C.; Ye, Y. Y.; Ji, G.; Liu, J. W. Hesperidin upregulates heme oxygenase-1 to attenuate hydrogen peroxide-induced cell damage in hepatic L02 cells. J. Agric. Food Chem. 2010, 58, 3330-3335.
40. Furukawa, Y.; Urano, T.; Minamimura, M.; Nakajima, M.; Okuyama, S.; Furukawa, S. 4-Methylcatechol-induced heme oxygenase-1 exerts a protective effect against oxidative stress in cultured neural stem/progenitor cells via PI3 kinase/Akt pathway. Biomed. Res. 2010, 31, 45-52.
41. Wei, Y.; Liu, X. M.; Peyton, K. J.; Wang, H.; Johnson, F. K.; Johnson, R. A.; Durante, W. Hypochlorous acid-induced heme oxygenase-1 gene expression promotes human endothelial cell survival. Am. J. Physiol. Cell Physiol. 2009, 297, C907-C915.
42. Lei, X. G.; Cheng, W. H.; McClung, J. P. Metabolic regulation and function of glutathione peroxidase-1. Annu. Rev. Nutr. 2007, 27, 41-61. (Pubitemid 351373347)
43. Harada, H.; Sugimoto, R.; Watanabe, A.; Taketani, S.; Okada, K.; Warabi, E.; Siow, R.; Itoh, K.; Yamamoto, M.; Ishii, T. Differential roles for Nrf2 and AP-1 in upregulation of HO-1 expression by arsenite in murine embryonic fibroblasts. Free Radical Res. 2008, 42, 297-304.
44. Covas, M. I.; de la Torre, K.; Farré-Albaladejo, M.; Kaikkonen, J.; Fitó, M.; López-Sabater, C.; Pujadas-Bastardes, M. A.; Joglar, J.; Weinbrenner, T.; Lamuela-Raventós, R. M.; de la Torre, R. Postprandial LDL phenolic content and LDL oxidation are modulated by olive oil phenolic compounds in humans. Free Radical Biol. Med. 2006, 40, 608-616. (Pubitemid 43170812)
45. Visioli, F.; Galli, C.; Grande, S.; Colonnelli, K.; Patelli, C.; Galli, G.; Caruso, D. Hydroxytyrosol excretion differs between rats and humans and depends on the vehicle of administration. J. Nutr. 2003, 133, 2612-2615. (Pubitemid 36935979)