Ellagic acid protects human keratinocyte (HaCaT) cells against UVA-induced oxidative stress and apoptosis through the upregulation of the HO-1 and Nrf-2 antioxidant genes

Food and Chemical Toxicology

Volumn 50, Issue 5, 2012, Pages 1245-1255

  Hseu, You Cheng ^a   Chou, Chih Wei ^a   Senthil Kumar, K J ^a   Fu, Ke Ting ^a   Wang, Hui Min ^b   Hsu, Li Sung ^c   Kuo, Yueh Hsiung ^a,d   Wu, Chi Rei ^a   Chen, Ssu Ching ^e   Yang, Hsin Ling ^a  

^a CHINA MEDICAL UNIVERSITY   (Taiwan)

^b KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^c CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

^d NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^e NATIONAL CENTRAL UNIVERSITY   (Taiwan)

Author keywords

Apoptosis; Ellagic acid; Heme oxygenase 1; NF E2 related factor 2; Reactive oxygen species; Ultraviolet A

Indexed keywords

CASPASE 3; ELLAGIC ACID; HEME OXYGENASE 1; KELCH LIKE ECH ASSOCIATED PROTEIN 1; LACTATE DEHYDROGENASE; PROTEIN BAX; PROTEIN BCL 2; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR NRF2;

ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CELL PROTECTION; CELL VIABILITY; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA FRAGMENTATION; DOWN REGULATION; DRUG EFFICACY; DRUG MECHANISM; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; GENE; GENE EXPRESSION; HO 1 GENE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; KERATINOCYTE; NRF 2 GENE; OXIDATIVE STRESS; ULTRAVIOLET A RADIATION; UPREGULATION;

APOPTOSIS; CELL LINE, TRANSFORMED; COMET ASSAY; DNA DAMAGE; ELLAGIC ACID; HEME OXYGENASE (DECYCLIZING); HUMANS; KERATINOCYTES; LIPID PEROXIDATION; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; RNA, SMALL INTERFERING; ULTRAVIOLET RAYS; UP-REGULATION;

EID: 84862805584     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2012.02.020     Document Type: Article

References (62)

1. Aggarwal B.B., Shishodia S. Molecular targets of dietary agents for prevention and therapy of cancer. Biochem. Pharmacol. 2006, 71:1397-1421.
2. Anand S., Chakrabarthi E., Kawamura H., Taylor C.R., Maytin E.V. Ultraviolet light (UVB and UVA) induces the damage responsive transcription factor CHOP/gadd153 in murine and human epidermis: evidence for mechanism specific to intact skin. J. Invest. Dermatol. 2005, 125:323-333.
3. Andreassi M., Andreassi L. Antioxidant in dermocosmetology: from the laboratory to clinical application. J. Cosmet. Dermatol. 2004, 2:153-160.
4. Bachelor M.A., Bowden G.T. UVA-mediated activation of signaling pathways involved in skin tumor promotion and progression. Semin. Cancer Biol. 2004, 14:131-138.
5. Bae J.Y., Choi J.S., Kang S.W., Lee Y.J., Park J., Kang Y.H. Dietary compound ellagic acid alleviates skin wrinkle and inflammation induced by UV-B irradiation. Exp. Dermatol. 2010, 19:e182-e190.
6. Bai J., Meng Z. Expression of apoptosis-related genes in liver from rats exposed to sulfur dioxide. Toxicology 2005, 216:253-260.
7. Breckenridge D., Germain M., Mathai J., Nguyen M., Shore G.C. Regulation of apoptosis by endoplasmic reticulum pathway. Oncogene 2003, 22:8608.
8. Buckman J.F., Hernandez H., Kress G.J., Votyakova T.V., Pal S., Renolds I.J. Mito Tracker labeling in primary neuronal and astrocytic cultures: influence of mitochondrial membrane potential and oxidants. J. Neurosci. Methods 2001, 104:165-176.
9. Camera E., Mastrofrancesco A., Fabbri C., Daubrawa F., Picardo M., Sies H., Stahl W. Astaxanthin, canthaxanthin and beta-carotene differently affect UVA-induced oxidative damage and expression of oxidative stress-responsive enzymes. Exp. Dermatol. 2009, 18:222-231.
10. Chao J., Li H., Cheng K.W., Yu M.S., Chang R.C.C., Wang M. Protective effects of pinostilbene, a resveratrol methylated derivative, against 6-hydroxydopamine-induced neurotoxicity in SH-SY5Y cells. J. Nutr. Biochem. 2010, 21:482-489.
11. Chen X.L., Kunsch C. Induction of cytoprotective genes through Nrf2/antioxidant response element pathway: a new therapeutic approach for the treatment of inflammatory diseases. Curr. Pharm. Des. 2004, 10:879-891.
12. Dinkova-Kostova A.T., Holtzclaw W.D., Kensler T.W. The role of Keap1 in cellular protective responses. Chem. Res. Toxicol. 2005, 18:1779-1791.
13. English J.S.C., Dawe R.S., Ferguson J. Environmental effects and skin disease. Br. Med. Bull. 2003, 68:129-142.
14. Festa F., Aglitti T., Duranti G., Ricordy R., Perticone P., Cozzi R. Strong antioxidant activity of ellagic acid in mammalian cells in vitro revealed by the commet assay. Anticancer Res. 2001, 6A:3903-3908.
15. Han D.H., Lee M.J., Kim J.H. Antioxidant and apoptosis-inducing activities of ellagic acid. Anticancer Res. 2006, 26:3601-3606.
16. Han X., Shen T., Lou H. Dietary polyphenols and their biological significance. Int. J. Mol. Sci. 2007, 8:950-988.
17. Haywood R., Wardman P., Sanders R., Linge C. Sunscreens inadequately protect against ultraviolet-A-induced free radical in skin: implementations for skin aging and melanoma?. J. Invest. Dermatol. 2003, 121:862-868.
18. Heath-Engel H.M., Chang N.C., Shore G.C. The endoplasmic reticulum in apoptosis and autophagy: role of the Bcl-2 protein family. Oncogene 2008, 27:6419-6433.
19. Henderson K., Stella S.L., Kobylewski S., Eckhert C.D. Receptor activated Ca2+ release is inhibited by prostate cancer cells. PLos ONE 2009, 4:e6009.
20. Hirota A., Kawachi Y., Itoh K., Nakamura Y., Xu X., Banno T., Takahashi T., Yamamoto M., Otsuka F. Ultraviolet A irradiation induces NF-E2-related factor-2 activation in dermal fibroblasts: protective role in UVA-induced apoptosis. J. Invest. Dermatol. 2005, 124:825-832.
21. Hoerter J.D., Ward C.S., Bale K.D., Gizachew A.N., Graham R., Reynolds J., Ward M.E., Choi C., Kagab J.L., Sauer M., Kuipers T., Hotchkiss T., Baner N., Chellson R.A., Ohaeri T., Gant L., Vanderhill L. Effect of UVA fluence rate on indicators of oxidative stress in human dermal fibroblasts. Int. J. Biol. Sci. 2008, 4:63-70.
22. 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, 296:473-481.
23. Ichihashi M., Ueda M., Budiyanto A., Bito T., Oka M., Fukunaga M., Tsuru K., Horikawa T. UV-induced skin damage. Toxicology 2003, 189:21-39.
24. Itoh T., Horio T. DNA-dependent protein kinase catalytic subunit is cleaved during UV-induced apoptosis. J. Dermatol. Sci. 2001, 25:72-77.
25. Kim J., Cha Y.N., Surh Y.J. A protective role of nuclear factor erythroid 2-related factor-2 (Nrf2) in inflammatory disorders. Mutat. Res. 2010, 690:12-23.
26. Kimura S., Warabi E., Yanagawa T., Ma D., Itoh K., Ishii Y., Kawachi Y., Ishii T. Essential role of Nrf2 in keratinocyte protection from UVA by quercetin. Biochem. Biophys. Res. Commun. 2009, 387:109-1014.
27. Kulms D., Schwarz T. Molecular mechanisms of UV-induced apoptosis. Photodermatol. Photoimmunol. Photomed. 2000, 16:195-201.
28. Kulms D., Zeise E., Poppelmann B., Schwarz T. DNA damage, death receptor activation and reactive oxygen species contribute to ultraviolet radiation-induced apoptosis in an essential and independent way. Oncogene 2002, 21:5844-5851.
29. Lansky E.P. Beware of promegranates bearing 40% of ellagic acid. J. Med. Food. 2006, 1:119-122.
30. Ly J.D., Grubb D.R., Lawen A. The mitochondrial membrane potential (deltapsi(m)) in apoptosis; an update. Apoptosis 2003, 8:115-128.
31. McMillan T.J., Leatherman E., Ridley A., Shorrocks J., Tobi S.E., Whiteside J.R. Cellular effects of long wavelength UV light (UVA) in mammalian cells. J. Pharm. Pharmacol. 2008, 60:969-976.
32. Meewes C., Brenneisen P., Wenk J., Kuhr L., Ma W., Alikoski J., Poswing A., Krieg T., Scharffetter-Kochanek K. Adaptive antioxidant response protects dermal fibroblasts from UVA-induced phototoxicity. Free. Rad. Bio. Med. 2001, 30:238-247.
33. Morley N., Rapp A., Dittmar H., Salter L., Gould D., Greulich K.O., Curnow A. UVA-induced apoptosis studied by the new apo/necro-Comet-assay which distinguishes viable, apoptotic and necrotic cells. Mutagenesis 2006, 21:105-114.
34. Mutanen M., Pajari A.M., Pairarinta E., Misikangas M., Rajakangas J., Marttinen M., Oikarinen S. Berries as chemopreventive dieatary constituensts- a mechanistic approach with the ApcMin/+mice. Asia. Pac. J. Clin. Nutr. 2008, 17:123-125.
35. Na H.K., Surh Y.J. Modulation of Nrf2-mediated antioxidant and detoxifying enzyme induction by the green tea polyphenol EGCG. Food. Chem. Toxicol. 2008, 46:1271-1278.
36. 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, 11:6040-6049.
37. Narayanan B.A., Narayanan K.N., Davis L., Nargi D. RNA interference-mediated cyclooxygenase-2 inhibition presents prostate cancer growth and induces differentiation: modulation of neuronal protein synaptophysin, cyclin D1, and androgen receptor. Mol. Cancer Ther. 2006, 5:1117-1125.
38. Nishimura H., Yasui H., Sakurai H. Generation and distribution of reactive oxygen species in the skin of hair less mice under UVA: studies on in vivo chemiluminescent detection and tape stripping methods. Exp. Dermatol. 2006, 15:891-899.
39. Patton W.P., Chakravarthy U., Davies R.J.H., Archer D.B. Comet assay of UV-induced DNA damage in retinal pigment epithelial cells. Invest. Opthalmol. Vis. Sci. 1999, 40:3268-3275.
40. Pillai S., Oresajo C., Hayward J. Ultraviolet radiation and skin ageing: role of reactive oxygen species, inflammation and protease activation, and strategies for prevention of inflammation-induced matrix degradation-a review. Int. J. Cosmet. Sci. 2005, 27:17-34.
41. Pinnell S.R. Cutaneous photodamage oxidative stress and topical antioxidant protection. J. Am. Acad. Dermatol. 2003, 48:1-19.
42. Porter A.G., Janicke R.U. Emerging roles of caspase-3 in apoptosis. Cell. Death. Differ. 1999, 6:99-104.
43. Pygmalion M.J., Ruiz L., Popovic E., Gizard J., Portes P., Marat X., Lucet-Levannier K., Muller B., Galey J.B. Skin cell protection against UVA by sideroxyl, a new antioxidant complementary to sunscreens. Free. Radical. Biol. Med. 2010, 49:1629-1637.
44. Rao R.V., Ellerby H.M., Bredesen D.E. Coupling endoplasmic reticulum stress to the cell death program. Cell. Death. Differ. 2004, 11:372-380.
45. Roberston J.D., Orrenius S. Molecular mechanisms of apoptosis induced by cytotoxic chemicals. Crit. Rev. Toxicol. 2000, 30:609-627.
46. Rosentein B.S. The induction of DNA strand breaks in normal human skin fibroblasts exposed to solor ultraviolet radiation. Radiat. Res. 1988, 116:313-319.
47. Saladi R.N., Persaud A.N. The causes of skin cancer: A comprehensive review. Drug. Today 2005, 41:37-53.
48. Sasaki H., Akamatsu H., Horis T. Protective role of copper, zinc superoxide dismutase against UVB-induced injury of the human keratinocyte cell line HaCaT. J. Invest. Dermatol. 2000, 114:502-507.
49. Scapagnini G., Sonya V., Nader A.G., Calogero C., Zella D., Fabio G. Modulation of Nrf2/ARE pathway by food polyphenols: A nutritional neuroprotective strategy for congnitive and neurodegenerative disorders. Mol. Neurobiol. 2011, 10.1007/s12035-011-8181-5.
50. Seeram N.P., Adams L.S., Henning S.M., Niu Y., Zhang Y., Nair M.G., Heber D. In vitro antiproliferative, apoptotic and antioxidant activities of punicalagin, ellagic acid and a total pomegranate tannin extract are enhanced in combination with other polyphenols as found in pomegranate juice. J. Nutr. Biochem. 2005, 16:360-367.
51. Singh N.P., McCoy M.T., Tice R.R., Schneider E.L. A simple technique for quantification of low levels of DNA damage in individual cells. Exp. Cell. Res. 1988, 175:184-191.
52. Stoner G.D., Mukhtar H. Polyphenols as cancer chemopreventive agents. J. Cell. Biochem. 1995, 2:169-180.
53. Surh Y.J. Cancer chemoprevention with dietary phytochemicals. Nat. Rev. Cancer 2003, 3:768-780.
54. Svobodova A., Psotova J., Walterova D. Natural phenolics in the prevention of UV-induced skin damage. A review. Biomed. Pap. 2003, 147:137-145.
55. Svobodova A., Zdarilova A., Walterova D., Vostalova J. Flavonolignans from Silybum marianum moderate UVA-induced oxidative damage to HaCaT keratinocytes. J. Dermatol. Sci. 2007, 48:213-224.
56. Syed D.N., Malik A., Hadi N., Safaraz S., Afaq F., Mukhtar H. Photochemopreventive effect of pomegranate fruit extract on UVA-mediated activation of cellular pathways in normal epidermal keratinocytes. Photochem. Photobiol. 2006, 82:398-405.
57. Tebbe B., Wu S., Geilen C.C., Eberle J., Kodelja V., Orfanos C.E. L-ascorbic acid inhibits UVA-induced lipid peroxidation and secretion of IL-1α and IL-6 in cultured human keratinocytes in vitro. J. Invest. Dermatol. 1997, 108:302-306.
58. Vattam D.A., Shetty K. Biological functionality of ellagic acid: a review. J. Food. Biochem. 2005, 29:234-266.
59. Yuan C.Q., Li Y.N., Zhang X.F. Down-regulation of apoptosis-inducing factor protein by RNA interference inhibits UVA-induced cell death. Biochem. Biophys. Res. Commun. 2004, 317:1108-1113.
60. Zhang D.D. Mechanistic studies of the Nrf2-Keap1 signaling pathway. Drug. Metabol. Rev. 2006, 38:769-789.
61. Zhong J.L., Edwards G.P., Raval C., Li H., Tyrrell R.M. The role of Nrf2 in ultraviolet-A mediated hemeoxygenase-1 induction in human skin fibroblasts. Photochem. Photobiol. Sci. 2010, 9:18-24.
62. Zhuang L., Wang B., Sauder D.N. Molecular mechanism of ultraviolet-induced keratinocyte apoptosis. J. Interf. Cytok. Res. 2000, 20:445-454.