Pro-oxidative action of polyphenols as action mechanism for their pro-apoptotic activity

Anti-Cancer Agents in Medicinal Chemistry

Volumn 14, Issue 10, 2014, Pages 1363-1375

  Lecci, Raffaella Marina ^a   Logrieco, Antonio ^a   Leone, Antonella ^a  

^a INSTITUTE OF SCIENCES OF FOOD PRODUCTION   (Italy)

Author keywords

Apoptosis; HEKa; Isoverbascoside; ROS; Skin cancer; Tyrosol; UV A verbascoside

Indexed keywords

ACTEOSIDE; ISOVERBASCOSIDE; POLYPHENOL; PROTEIN BCL XL; REACTIVE OXYGEN METABOLITE; TYROSOL; UNCLASSIFIED DRUG; 4-HYDROXYPHENYLETHANOL; ANTINEOPLASTIC AGENT; GLUCOSIDE; PHENETHYL ALCOHOL; PHENOL DERIVATIVE;

ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CELL GROWTH; CELL VIABILITY ASSAY; CHEMICAL STRUCTURE; CONFOCAL LASER SCANNING MICROSCOPY; CONTROLLED STUDY; DNA DAMAGE; DOWN REGULATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; KERATINOCYTE; PROTEIN EXPRESSION; ULTRAVIOLET A RADIATION; ADVERSE EFFECTS; ANALOGS AND DERIVATIVES; CELL LINE; CELL SURVIVAL; DRUG EFFECTS; METABOLISM; OXIDATION REDUCTION REACTION; ULTRAVIOLET RADIATION;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; CELL LINE; CELL SURVIVAL; GLUCOSIDES; HUMANS; OXIDATION-REDUCTION; PHENOLS; PHENYLETHYL ALCOHOL; POLYPHENOLS; REACTIVE OXYGEN SPECIES; ULTRAVIOLET RAYS;

EID: 84935489593     PISSN: 18715206     EISSN: 18755992     Source Type: Journal    
DOI: 10.2174/1871520614666140922121014     Document Type: Article

References (71)

1. Beckman, C.H. Phenolic-storing cells: Keys to programmed cell death and periderm formation in wilt disease resistance and in general defence responses in plants? Physiol. Mol. Plant Pathol., 2000, 57(3), 101-110.
2. Graf, B.A.; Milbury, P.E.; Blumberg, J.B. Flavonols, flavonones, flavanones and human health: Epidemological evidence. J. Med. Food, 2005, 8(3), 281-290.
3. Arts, I.C.; Hollman, P.C. Polyphenols and disease risk in epidemiologic studies. Am. J. Clin. Nutr., 2005, 81(1 Suppl), S317-S325.
4. Nichols, J.A.; Katiyar, S.K. Skin photoprotection by natural polyphenols: Anti-inflammatory, anti-oxidant and DNA repair mechanisms. Arch. Dermatol. Res., 2010, 302(2), 71-83.
5. Afaq, F.; Katiyar, S.K. Polyphenols: Skin Photoprotection and Inhibition of Photocarcinogenesis. Mini Rev. Med. Chem., 2011, 11(14), 1200-1215.
6. Valencia, A.; Kochevar, I.E. Nox1-Based NADPH Oxidase Is the Major Sourceof UVA-Induced Reactive Oxygen Species in Human Keratinocytes. J. Invest. Dermatol., 2008, 128(1), 214-222.
7. Krutmann, J. Ultraviolet a radiation-induced biological effects in human skin: Relevance for photoaging and photodermatosis. J. Dermatol. Sci., 2000, 23 (Suppl. 1), S22-S26.
8. Breuckmann, F.; Gambichler, T.; Altmeyer, P.; Kreuter, A. UVA/UVA1 phototherapy and PUVA photochemotherapy in connective tissue diseases and related disorders: A research based review. BMC Dermatol., 2004, 4(1), 11.
9. De Laat, A.; Van Der Leun, J.C.; De Gruijl, F.R. Carcinogenesis induced by UVA (365-nm) radiation: The dose-time dependence of tumor formation in hairless mice. Carcinogenesis, 1997, 18(5), 1013-1020.
10. Krutmann, J. The role of UVA rays in skin aging. Eur. J. Dermatol., 2001, 11(2), 170-171.
11. Bachelor, M.A.; Bowden, G.T. UVA-mediated activation of signaling pathways involved in skin tumor promotion and progression. Semin. Cancer Biol., 2004, 14(2), 131-138.
12. Allanson, M.; Domanski, D; Reeve, V.E. Photoimmunoprotection by UVA (320-400 nm) radiation is determined by UVA dose and is associated with cutaneous cyclic guanosine monophosphate. J. Invest. Dermatol., 2006, 126(1), 191-197.
13. Einspahr, J.G.; Stratton, S.P.; Bowden, G.T.; Alberts, D.S. Chemoprevention of human skin cancer. Crit. Rev. Oncol. Hematol., 2002, 41(3), 269-285.
14. Sterenborg, H.J.; Van Der Leun, J.C. Tumorigenesis by a long wavelength UV-A source. Photochem. Photobiol., 1990, 51(3), 325-330.
15. Kelfkens, G.; De Gruijl, F.R.; Van Der Leun, J.C. Tumorigenesis by short wave ultraviolet A: Papillomas versus squamous cell carcinomas. Carcinogenesis, 1991, 12(8), 1377-1382.
16. Agar, N.S.; Halliday, G.M.; Barnetson, R.S.; Ananthaswamy H.N.; Wheeler, M.; Jones, A.M. The basal layerin human squamous tumors harbors more UVA than UVB fingerprint mutations: A role for UVA in human skin carcinogenesis. Proc. Natl. Acad. Sci. USA, 2004, 101(14), 4954-4959.
17. Svobodová, A.; Zdarilová, A.; Malisková, J.; Mikulková, H.; Walterová, D.; Vostalová, J. Attenuation of UVA-induced damage to human keratinocytes by silymarin. J. Dermatol. Sci., 2007, 46(1), 21-30.
18. Svobodova, A.; Walterova, D.; Vostalova, J. Ultraviolet light induced alteration to the skin. Biomed. Pap. Med. Fac. Univ. Palacky Olomouc Czech Repub., 2006, 150(1), 25-38.
19. Villiotou, V.; Deliconstantinos, G. Nitric oxide, peroxynitriteand Snitrosothiols formation by ultraviolet A (UVA) irradiated human squamous cell carcinoma: Potential role of nitric oxide in cancer prognosis. Anticancer Res., 1995, 15(3), 931-942.
20. Leone, A.; Longo, C.; Trosko, J.E. The chemopreventive role of dietary phytochemicals through gap junctional intercellular communication. Phytochem. Rev., 2012, 11(2-3), 285-307.
21. Trosko, J.E.; Tai, M.H. Adult stem cell theory of the multistage, multi-mechanism theory of carcinogenesis: Role of inflammation on the promotion of initiated stem cells. Contrib. Microbiol., 2006, 13, 45-65.
22. Cheng, K.C.; Cahill, D.S.; Kasai, H.; Nishimura, S.; Loeb, L.A. 8-Hydroxyguanine, an abundant form of oxidative DNA damage, causes G-T and A-C substitutions. J. Biol. Chem., 1992, 267(1), 166-172.
23. Epe, B. Genotoxicity of singlet oxygen. Chem. Biol. Interact., 1991, 80(3), 239-260.
24. Maki, H.; Sekiguchi, M. MutT protein specifically hydrolyses a potent mutagenic substrate for DNA synthesis. Nature, 1992, 355(6357), 273-275.
25. Bouayed, J.; Bohn, T. Exogenous antioxidants-Double-edged swords in cellular redox state.Health beneficial effects at physiologic doses versus deleterious effects at high doses. Oxid. Med. Cell. Longev., 2010, 3(4), 228-237.
26. Offord, E.A.; Gautier, J.C.; Avanti, O.; Scaletta, C.; Runge, F.; Krmer, K.; Applegate L.A. Photoprotective potential of lycopene, b-carotene, vitamin E, vitamin C, and carnosic acid in UVAirradiated human skin fibroblast. Free Radic. Biol. Med., 2002, 32(12), 1293-1303.
27. Basu-Modak, S.; Gordon, M.J.; Dobson, L.H.; Spencer, J.P.; Rice-Evans, C.; Tyrrell, R.M. Epicatechin and its methylated metabolite attenuate UVA-induced oxidative damage to human skin fibroblasts. Free Radic. Biol. Med., 2003, 35(8), 910-921.
28. Tobi, S.E.; Gilbert, M.; Paul, N.; McMillan, T.J. The green tea polyphenol, epigallocatechin-3-gallate, protects against the oxidative cellular and genotoxic damage of UVA radiation. Int. J. Cancer, 2002, 102(5), 439-44.
29. Huang, C.C.; Fang, J.Y.; Wu, W.B.; Chiang, H.S.; Wei, Y.J.; Hung, C.F. Protective effects of (-)-epicatechin-3-gallate on UVA induced damage in HaCaT keratinocytes. Arch. Dermatol. Res., 2005, 296(10), 473-481.
30. Erden, I.M.; Kahramant, A.; Kökent, T. Beneficial effects of quercetin on oxidative stress induced by ultraviolet A. Clin. Exp. Dermatol., 2001, 26(6), 536-539.
31. Halliwell, B. Role of free radicals in the neurodegenerative diseases: Therapeutic implications for antioxidant treatment. Drugs Aging, 2001, 18(9), 685-716.
32. Williams, R.J.; Spencer, J.P.; Rice-Evans, C. Flavonoids: Antioxidants or signalling molecules? Free Radic. Biol. Med., 2004, 36(7), 838-849.
33. Rahman, I.; Chung, S. Dietary polyphenols, deacetylases and chromatin remodeling in inflammation. J. Nutrigenet. Nutrigenom., 2010, 3(4-6), 220-230.
34. Katiyar, S.K.; Singh, T.; Prasad, R.; Sun, Q.; Vaid, M. Epigenetic Alterations in Ultraviolet Radiation-Induced Skin Carcinogenesis: Interaction of Bioactive Dietary Components on Epigenetic Targets. Photochem. Photobiol., 2012, 88(5), 1066-1074.
35. Ayissi, V.B.; Ebrahimi, A.; Schluesenner, H. Epigenetic effects of natural polyphenols: A focus on SIRT1-mediated mechanisms. Mol. Nutr. Food Res., 2014, 58(1), 22-32.
36. Collett, G.P.; Campbell, F.C. Curcumin induces c-jun N-terminal kinase-dependent apoptosis in HCT116 human colon cancer cells. Carcinogenesis, 2004, 25(11), 2183-2189.
37. Cavet, M.E.; Harrington, K.L.; Vollmer, T.R.; Ward, K.W. Zhang, J.Z. Anti-inflammatory and anti-oxidative effects of the green tea polyphenol epigallocatechingallate in human corneal epithelial cells. Mol. Vis., 2011, 17, 533-542.
38. Cardinali, A.; Cicco, N.; Linsalata, V.; Minervini, F.; Pati, S.; Pieralice, M.; Tursi, N.; Lattanzio, V. Biological activity of high molecular weight phenolics from olive mill wastewater. J. Agric. Food Chem., 2010, 58(15), 8585-8590.
39. Korkina, L.G.; Mikhal’chik, E.; Suprun, M.V.; Pastore, S.; Dal Toso, R. Molecular mechanisms underlying wound healing and antiinflammatory properties of naturally occurring biotechnologically produced phenylpropanoid glycosides. Cell. Mol. Biol. (Noisy-legrand), 2007, 53(5), 84-91.
40. Gyurkovska, V.; Alipieva, K.; Maciuk, A.; Dimitrova, P.; Ivanovska, N.; Haas, C.; Bley, T.; Georgiev, M. Anti-inflammatory activity of Devil’s claw in vitro systems and their active constituents. Food Chem., 2011, 125(1), 171-178.
41. Mazzon, E.; Esposito, E.; Di Paola, R.; Riccardi, L.; Caminiti, R.; Dal Toso, R.; Pressi, G.; Cuzzocrea, S. Effects of verbascoside biotechnologically produced by Syringa vulgaris plant cell cultures in a rodent model of colitis. Naunyn Schmiedebergs Arch. Pharmacol., 2009, 380(1), 79-94.
42. Rui-Chuan, C.; Jin-Hua, S.; Gao-Liang, O.; Ke-Xia, C.; Jin-Quan, L.; Xiao-Guang, X. Induction of Differentiation in Human Hepatocarcinoma Cells by Isoverbascoside. Planta Med., 2002, 68(4), 370-372.
43. Palmieri, D.; Aliakbarian, B.; Casazza, A.A.; Ferrari, N.; Spinella, G.; Pane, B.; Cafueri, G.; Perego, P.; Palombo, D. Effects of polyphenol extract from olive pomace on anoxia-induced endothelial dysfunction. Microvasc. Res., 2012, 83(3), 281-289.
44. Leone, A.; Lecci, R.M.; Durante, M.; Piraino, S. Extract from the zooxanthellate jellyfish Cotylorhiza tuberculata modulates gap junction intercellular communication in human cell cultures. Mar. Drugs, 2013, 11(5), 1728-1762.
45. Long, L.H.; Hoi, A.; Halliwell, B. Instability of, and generation of hydrogen peroxide by, phenolic compounds in cell culture media. Arch. Biochem. Biophys., 2010, 501(1), 162-169.
46. Potapovich, A.I.; Kostyuk, V.A.; Kostyuk, T.V.; De Luca, C.; Korkina, L.G. Effects of pre-and post-treatment with plant polyphenols on human keratinocyte responses to solar UV. Inflamm. Res., 2013, 62(8), 773-780.
47. Bradford, M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of proteindye binding. Analyt. Biochem., 1976, 72, 248-254.
48. Vertuani, S.; Beghelli, E.; Scalambra, E.; Malisardi, G.; Copetti, S.; Dal Toso, R.; Baldisserotto, A.; Manfredini, S. Activity and stability studies of verbascoside, a novel antioxidant, in dermocosmetic and pharmaceutical topical formulations. Molecules, 2011, 16(8), 7068-7080.
49. Surh, Y.J. Cancer chemoprevention with dietary phytochemicals. Nat. Rev. Cancer, 2003, 3(10), 768-780.
50. Nakazato, T.; Ito, K.; Ikeda, Y.; Kizaki, M. Green tea component, catechin, induces apoptosis of human malignant B cells via production of reactive oxygen species. Clin. Cancer Res., 2005, 11(16), 6040-6049.
51. Loo, G. Redox-sensitive mechanisms of phytochemical-mediated inhibition of cancer cell proliferation (review). J. Nutr. Biochem., 2003, 14(2), 64-73.
52. Khan, H.Y.; Zubair, H.; Faisal, M.; Ullah, M.F.; Farhan, M.; Sarkar, F.H.; Ahmad, A.; Hadi, S.M. Plant polyphenol induced cell death in human cancer cells involves mobilization of intracellular copper ions and reactive oxygen species generation: A mechanism for cancer chemopreventive action. Mol. Nutr. Food Res., 2014, 58(3), 437-46.
53. Cardinali, A.; Pati, S.; Minervini, F.; D’Antuono, I.; Linsalata, V.; Lattanzio, V. Verbascoside, Isoverbascoside and their derivatives recovered from Olive Mill Wastewater as possible food antioxidants. J. Agric. Food Chem., 2012, 60(7), 1822-1829.
54. Covas, M.I.; Miró-Casas, E.; Fitó, M.; Farré-Albadalejo, M.; Gimeno, E.; Marrugat, J.; De La Torre, R. Bioavailability of tyrosol, an antioxidant phenolic compound present in wine and olive oil, in humans. Drugs Exp. Clin. Res., 2003, 29(5-6), 203-206.
55. Chen, C.H.; Lin, Y.S.; Chien, M.Y.; Hou, W.C.; Hu, M.L. Antioxidant and antihypertensive activities of acteoside and its analogs. Bot. Stud., 2012, 53, 421-429.
56. Fresco, P.; Borges, F.; Diniz, C.; Marques, M.P. New insights on the anticancer properties of dietary polyphenols. Med. Res. Rev., 2006, 26(6), 747-766.
57. Giovannini, C.; Masella, R. Role of polyphenols in cell death control. Nutr. Neurosci., 2012, 15(3), 134-49.
58. Yoshida, M.; Yamamoto, M; Nikaido, T. Quercetin arrests human leukemic T-cells in late G1 phase of the cell cycle. Cancer Res., 1992, 52(23), 6676-6681.
59. Musk, S.R.; Stephenson, P.; Smith, T.K.; Stening, P.; Fyfe, D, Johnson, I.T. Selective toxicity of compounds naturally present in food toward the transformed phenotype of human colorectal cell line HT29. Nutr. Cancer, 1995, 24(3), 289-298.
60. Kuntz, S.; Wenzel, U.; Daniel, H. Comparative analysis of the effects of flavonoids on proliferation, cytotoxicity, and apoptosis in human colon cancer cell lines. Eur. J. Nutr., 1999, 38(3), 133-142.
61. Wenzel, U.; Kuntz, S.; Brendel, M.D.; Daniel, H. Dietary flavone is a potent apoptosis inducer in human colon carcinoma cells. Cancer Res., 2000, 60(14), 3823-3831.
62. Manson, M. Cancer prevention-the potential for diet to modulate molecular signaling. Trends Mol. Med., 2003, 9(1), 11-18.
63. Della Ragione, F.; Cucciolla, V.; Borriello, A.; Della Pietra, V.; Pontoni, G.; Racioppi, L.; Manna, C.; Galletti, P.; Zappia, V. Hydroxytyrosol, a natural molecule occurring in olive oil, induces cytochrome c-dependent apoptosis. Biochem. Biophys. Res. Commun., 2000, 278 (3) 733-739.
64. Ramos, S. Cancer chemoprevention and chemotherapy: Dietary polyphenols and signalling pathways. Mol. Nutr. Food Res., 2008, 52(5), 507-526.
65. Ishikawa, Y.; Kitamura, M. Bioflavonoid quercetin inhibits mitosis and apoptosis of glomerular cells in vitro and in vivo. Biochem. Biophys. Res. Commun., 2000, 279(2), 629-634.
66. Spencer, J.P.; Schroeter, H.; Kuhnle, G.; Srai, S.K.; Tyrrell, R. M.; Hahn, U.; Rice-Evans, C. Epicatechin and its in vivo metabolite, 3_-O-methyl epicatechin, protect human fibroblasts from oxidative-stress induced cell death involving caspase-3 activation. Biochem. J., 2001, 354(Pt 3), 493-500.
67. Scalbert, A.; Manach, C.; Morand, C.; Rémésy, C.; Jiménez, L. Dietary polyphenols and the prevention of diseases. Crit. Rev. Food Sci. Nutr., 2005, 45(4), 287-306.
68. Bode, A.M.; Dong, Z. Targeting signal transduction pathways by chemopreventive agents. Mutat. Res., 2004, 555(1-2), 33-51.
69. Haupt, S.; Berger, M.; Goldberg, Z.; Haupt, Y. Apoptosis-the p53 network. J. Cell. Sci., 2003, 116(Part 20), 4077-4085.
70. Hainaut, P.; Mann, K. Zinc binding and redox control of p53 structure and function. Antioxid. Redox Signal., 2001, 3(4), 611-623.
71. Liu, Z.; Lu, H.; Shi, H.; Du, Y.; Yu, J.; Gu, S.; Chen, X.; Liu, K.J., Hu, C.A. PUMA overexpression induces reactive oxygen species generation and proteasome-mediated stathmin degradation in colorectal cancer cells. Cancer Res., 2005, 65(5), 1647-1654.