Cyanidin-3-O-glucoside modulates intracellular redox status and prevents HIF-1 stabilization in endothelial cells in vitro exposed to chronic hypoxia

Toxicology Letters

Volumn 226, Issue 2, 2014, Pages 206-213

  Anwar, S ^a   Speciale, A ^a   Fratantonio, D ^a   Cristani, M ^a   Saija, A ^a   Virgili, F ^b   Cimino, F ^a  

^a UNIVERSITY OF MESSINA   (Italy)

^b ISTITUTO NAZIONALE DELLA NUTRIZIONE   (Italy)

Author keywords

Cellular adaptive response; Cyanidin; Endothelial dysfunction; Hypoxia; Nrf2; Oxidative stress

Indexed keywords

CASPASE 3; CYANIDIN 3 GLUCOSIDE; GELATINASE A; GLUTATHIONE; GLUTATHIONE DISULFIDE; HEME OXYGENASE 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE;

ANGIOGENESIS; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CELL HYPOXIA; CONTROLLED STUDY; CYTOTOXICITY; ENDOTHELIAL DYSFUNCTION; ENZYME ACTIVATION; GLUTATHIONE METABOLISM; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HYDROXYLATION; HYPOXIA; IN VITRO STUDY; LONG TERM EXPOSURE; MOLECULAR WEIGHT; NUCLEOPHILICITY; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN STABILITY; PROTEIN SYNTHESIS; REDOX STRESS; TRANSCRIPTION INITIATION; UMBILICAL VEIN ENDOTHELIAL CELL; UPREGULATION;

CELLULAR ADAPTIVE RESPONSE; CYANIDIN; ENDOTHELIAL DYSFUNCTION; HYPOXIA; NRF2; OXIDATIVE STRESS;

ANTHOCYANINS; ANTIOXIDANTS; CASPASE 3; CELL HYPOXIA; CELLS, CULTURED; CYTOPROTECTION; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUCOSIDES; HEME OXYGENASE-1; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MATRIX METALLOPROTEINASE 2; OXIDATION-REDUCTION; OXIDATIVE STRESS; PROTEIN STABILITY; RNA, MESSENGER;

EID: 84896046653     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2014.01.048     Document Type: Article

References (52)

1. Ansó E., Zuazo A., Irigoyen M., Urdaci M.C., Rouzaut A., Martínez-Irujo J.J. Flavonoids inhibit hypoxia-induced vascular endothelial growth factor expression by a HIF-1 independent mechanism. Biochem. Pharmacol. 2010, 79(11):1600-1609.
2. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
3. Brahimi-Horn M.C., Pouysségur J. HIF at a glance. J. Cell Sci. 2009, 122(Pt 8):1055-1057.
4. Carmeliet P. Mechanisms of angiogenesis and arteriogenesis. Nat. Med. 2000, 6(4):389-395.
5. Cervellati F., Cervellati C., Romani A., Cremonini E., Sticozzi C., Belmonte G., Pessina F., Valacchi G. Hypoxia induces cell damage via oxidative stress in retinal epithelial cells. Free Radic. Res. 2014, [Epub ahead of print].
6. 2 sensing. J. Biol. Chem. 2000, 275:25130-25138.
7. Chen G., Zhang W., Li Y.P., Ren J.G., Xu N., Liu H., Wang F.Q., Sun Z.J., Jia J., Zhao Y.F. Hypoxia-induced autophagy in endothelial cells: a double-edged sword in the progression of infantile haemangioma?. Cardiovasc. Res. 2013, 98(3):437-448.
8. Cimino F., Balestra C., Germonpré P., De Bels D., Tillmans F., Saija A., Speciale A., Virgili F. Pulsed high oxygen induces a hypoxic-like response in human umbilical endothelial cells and in humans. J. Appl. Physiol. 2012, 113(11):1684-1689.
9. Cimino F., Speciale A., Anwar S., Canali R., Ricciardi E., Virgili F., Trombetta D., Saija A. Anthocyanins protect human endothelial cells from mild hyperoxia damage through modulation of Nrf2 pathway. Genes Nutr. 2013, 8(4):391-399.
10. Daleprane J.B., Schmid T., Dehne N., Rudnicki M., Menrad H., Geis T., Ikegaki M., Ong T.P., Brüne B., Abdalla D.S. Suppression of hypoxia-inducible factor-1α contributes to the antiangiogenic activity of red propolis polyphenols in human endothelial cells. J. Nutr. 2012, 142(3):441-447.
11. Faller D.V. Endothelial cell responses to hypoxic stress. Clin. Exp. Pharmacol. Physiol. 1999, 26(1):74-84.
12. Fang J., Xia C., Cao Z., Zheng J.Z., Reed E., Jiang B.H. Apigenin inhibits VEGF and HIF-1 expression via PI3K/AKT/p70S6K1 and HDM2/p53 pathways. FASEB J. 2005, 19:342-353.
13. Flammer A.J., Luscher T.F. Three decades of endothelium research: from the detection of nitric oxide to the everyday implementation of endothelial function measurements in cardiovascular diseases. Swiss Med. Wkly. 2010, 140:w13122.
14. Forman H.J., Davies K.J., Ursini F. How do nutritional antioxidants really work: nucleophilic tone and para-hormesis versus free radical scavenging in vivo. Free Radic. Biol. Med. 2013, pii:S0891-5849(13)00273-6. 10.1016/j.freeradbiomed.2013.05.045.
15. Garcia-Alonso M., Minihane A.M., Rimbach G., Rivas-Gonzalo J.C., de Pascual-Teresa S. Red wine anthocyanins are rapidly absorbed in humans and affect monocyte chemoattractant protein 1 levels and antioxidant capacity of plasma. J. Nutr. Biochem. 2009, 20(7):521-529. 10.1016/j.jnutbio.2008.05.011.
16. García-Alonso M., Rimbach G., Rivas-Gonzalo J.C., De Pascual-Teresa S. Antioxidant and cellular activities of anthocyanins and their corresponding vitisins A - Studies in platelets, monocytes, and human endothelial cells. J. Agric. Food Chem. 2004, 52(11):3378-3384.
17. Greijer A.E., van der Wall E. The role of hypoxia inducible factor 1 (HIF-1) in hypoxia induced apoptosis. J. Clin. Pathol. 2004, 57(10):1009-1014.
18. Hooper L., Kroon P.A., Rimm E.B., Cohn J.S., Harvey I., Le Cornu K.A., Ryder J.J., Hall W.L., Cassidy A. Flavonoids, flavonoid-rich foods, and cardiovascular risk: a meta-analysis of randomized controlled trials. Am. J. Clin. Nutr. 2008, 88(1):38-50.
19. Hultén L.M., Levin M. The role of hypoxia in atherosclerosis. Curr. Opin. Lipidol. 2009, 20(5):409-414.
20. Ji Q., Yang L., Zhou J., Lin R., Zhang J., Lin Q., Wang W., Zhang K. Protective effects of paeoniflorin against cobalt chloride-induced apoptosis of endothelial cells via HIF-1α pathway. Toxicol. In Vitro 2012, 26(3):455-461.
21. Jun J., Reinke C., Bedja D., Berkowitz D., Bevans-Fonti S., Li J., Barouch L.A., Gabrielson K., Polotsky V.Y. Effect of intermittent hypoxia on atherosclerosis in apolipoprotein E-deficient mice. Atherosclerosis 2010, 209(2):381-386.
22. Lamy S., Blanchette M., Michaud-Levesque J., Lafleur R., Durocher Y., Moghrabi A., Barrette S., Gingras D., Béliveau R. Delphinidin, a dietary anthocyanidin, inhibits vascular endothelial growth factor receptor-2 phosphorylation. Carcinogenesis 2006, 27(5):989-996.
23. Lazzé M.C., Pizzala R., Savio M., Stivala L.A., Prosperi E., Bianchi L. Anthocyanins protect against DNA damage induced by tert-butyl-hydroperoxide in rat smooth muscle and hepatoma cells. Mutat. Res. 2003, 535:103-115.
24. Lazzé M.C., Savio M., Pizzala R., Cazzalini O., Perucca P., Scovassi A.I., Stivala L.A., Bianchi L. Anthocyanins induce cell cycle perturbations and apoptosis in different human cell lines. Carcinogenesis 2004, 25:1427-1433.
25. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25(4):402-408.
26. Lu J., Zhang K., Chen S., Wen W. Grape seed extract inhibits VEGF expression via reducing HIF-1alpha protein expression. Carcinogenesis 2009, 30(4):636-644.
27. Mansfield K.D., Simon M.C., Keith B. Hypoxic reduction in cellular glutathione levels requires mitochondrial reactive oxygen species. J. Appl. Physiol. 2004, 97(4):1358-1366.
28. Matsunaga N., Tsuruma K., Shimazawa M., Yokota S., Hara H. Inhibitory actions of bilberry anthocyanidins on angiogenesis. Phytother. Res. 2010, 24(1):S42-S47.
29. Matsushita H., Morishita R., Nata T., Aoki M., Nakagami H., Taniyama Y., Yamamoto K., Higaki J., Yasufumi K., Ogihara T. Hypoxia-induced endothelial apoptosis through nuclear factor-kappaB (NF-kappaB)-mediated bcl-2 suppression: in vivo evidence of the importance of NF-kappaB in endothelial cell regulation. Circ. Res. 2000, 86(9):974-981.
30. Nakano D., Hayashi T., Tazawa N., Yamashita C., Inamoto S., Okuda N., Mori T., Sohmiya K., Kitaura Y., Okada Y., Matsumura Y. Chronic hypoxia accelerates the progression of atherosclerosis in apolipoprotein E-knockout mice. Hypertens. Res. 2005, 28(10):837-845.
31. Nguyen M., Arkell J., Jackson C.J. Human endothelial gelatinases and angiogenesis. Int. J. Biochem. Cell Biol. 2001, 33(10):960-970.
32. Nozik-Grayck E., Suliman H.B., Majka S., Albietz J., Van Rheen Z., Roush K., Stenmark K.R. Lung EC-SOD overexpression attenuates hypoxic induction of Egr-1 and chronic hypoxic pulmonary vascular remodeling. Am. J. Physiol. Lung Cell. Mol. Physiol. 2008, 295(3):L422-L430.
33. Palmieri D., Pane B., Barisione C., Spinella G., Garibaldi S., Ghigliotti G., Brunelli C., Fulcheri E., Palombo D. Resveratrol counteracts systemic and local inflammation involved in early abdominal aortic aneurysm development. J. Surg. Res. 2011, 171(2):e237-e246.
34. Pialoux V., Mounier R., Brown A.D., Steinback C.D., Rawling J.M., Poulin M.J. Relationship between oxidative stress and HIF-1 alpha mRNA during sustained hypoxia in humans. Free Radic. Biol. Med. 2009, 46(2):321-326.
35. Pojer E., Mattivi F., Johnson D., Stockley C.S. The case for anthocyanin consumption to promote human health: a review. Compr. Rev. Food Sci. Food Saf. 2013, 12(5):483-508.
36. Russo A., La Fauci L., Acquaviva R., Campisi A., Raciti G., Scifo C., Renis M., Galvano G., Vanella A., Galvano F. Ochratoxin A-induced DNA damage in human fibroblast: protective effect of cyanidin-3-O-beta-d-glucoside. J. Nutr. Biochem. 2005, 16:31-33.
37. Sceneay J., Liu M.C., Chen A., Wong C.S., Bowtell D.D., Möller A. The antioxidant N-acetylcysteine prevents HIF-1 stabilization under hypoxia in vitro but does not affect tumorigenesis in multiple breast cancer models in vivo. PLoS ONE 2013, 8(6):e66388.
38. Semenza G.L. HIF-1 and mechanisms of hypoxia sensing. Curr. Opin. Cell Biol. 2001, 13(2):167-171.
39. Singh M., Thomas P., Shukla D., Tulsawani R., Saxena S., Bansal A. Effect of subchronic hypobaric hypoxia on oxidative stress in rat heart. Appl. Biochem. Biotechnol. 2013, 169(8):2405-2419.
40. Sluimer J.C., Daemen M.J. Novel concepts in atherogenesis: angiogenesis and hypoxia in atherosclerosis. J. Pathol. 2009, 218(1):7-29.
41. Sluimer J.C., Gasc J.M., van Wanroij J.L., Kisters N., Groeneweg M., Sollewijn Gelpke M.D., Cleutjens J.P., van den Akker L.H., Corvol P., Wouters B.G., Daemen M.J., Bijnens A.P. Hypoxia, hypoxia-inducible transcription factor, and macrophages in human atherosclerotic plaques are correlated with intraplaque angiogenesis. J. Am. Coll. Cardiol. 2008, 51(13):1258-1265.
42. Sohn H.Y., Krotz F., Gloe T., Keller M., Theisen K., Klauss V., Pohl U. Differential regulation of xanthine and NAD(P)H oxidase by hypoxia in human umbilical vein endothelial cells. Role of nitric oxide and adenosine. Cardiovasc. Res. 2003, 58:638-646.
43. Song Z.C., Zhou W., Shu R., Ni J. Hypoxia induces apoptosis and autophagic cell death in human periodontal ligament cells through HIF-1α pathway. Cell Prolif. 2012, 45(3):239-248.
44. Speciale A., Anwar S., Canali R., Chirafisi J., Saija A., Virgili F., Cimino F. Cyanidin-3-O-glucoside counters the response to TNF-alpha of endothelial cells by activating Nrf2 pathway. Mol. Nutr. Food Res. 2013, 57(11):1979-1987.
45. Speciale A., Anwar S., Ricciardi E., Chirafisi J., Saija A., Cimino F. Cellular adaptive response to glutathione depletion modulates endothelial dysfunction triggered by TNF-α. Toxicol. Lett. 2011, 207(3):291-297.
46. Speciale A., Canali R., Chirafisi J., Saija A., Virgili F., Cimino F. Cyanidin-3-O-glucoside protection against TNF-α-induced endothelial dysfunction: involvement of nuclear factor-κB signaling. J. Agric. Food Chem. 2010, 58(22):12048-12054.
47. Speciale A., Chirafisi J., Saija A., Cimino F. Nutritional antioxidants and adaptive cell responses: an update. Curr. Mol. Med. 2011, 11(9):770-789.
48. Stoclet J.C., Chataigneau T., Ndiaye M., Oak M.H., El Bedoui J., Chataigneau M., Schini-Kerth V.B. Vascular protection by dietary polyphenols. Eur. J. Pharmacol. 2004, 500(1-3):299-313.
49. Tan C.B., Gao M., Xu W.R., Yang X.Y., Zhu X.M., Du G.H. Protective effects of salidroside on endothelial cell apoptosis induced by cobalt chloride. Biol. Pharm. Bull. 2009, 32(8):1359-1363.
50. Trombetta D., Cimino F., Cristani M., Mandalari G., Saija A., Ginestra G., Speciale A., Chirafisi J., Bisignano G., Waldron K., Narbad A., Faulds C.B. In vitro protective effects of two extracts from bergamot peels on human endothelial cells exposed to tumor necrosis factor-alpha (TNF-alpha). J. Agric. Food Chem. 2010, 58(14):8430-8436.
51. van den Oever I.A., Raterman H.G., Nurmohamed M.T., Simsek S. Endothelial dysfunction, inflammation, and apoptosis in diabetes mellitus. Mediators Inflamm. 2010, 2010:792393.
52. Vita J.A. Polyphenols and cardiovascular disease: effects on endothelial and platelet function. Am. J. Clin. Nutr. 2005, 81(1 Suppl.):292S-297S.