Astaxanthin, canthaxanthin and β-carotene differently affect UVA-induced oxidative damage and expression of oxidative stress-responsive enzymes

Experimental Dermatology

Volumn 18, Issue 3, 2009, Pages 222-231

  Camera, Emanuela ^a,b   Mastrofrancesco, Arianna ^a   Fabbri, Claudia ^a   Daubrawa, Felicitas ^b   Picardo, Mauro ^a   Sies, Helmut ^b   Stahl, Wilhelm ^b  

^a SAN GALLICANO DERMATOLOGICAL INSTITUTE   (Italy)

^b HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

Antioxidant enzymes; Apoptosis; Carotenes; Skin photodamage; Xanthophylls

Indexed keywords

ASTAXANTHIN; BETA CAROTENE; CANTHAXANTHIN; CASPASE 3; CATALASE; HEME OXYGENASE 1; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE;

ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CELL TRANSPORT; CELL VIABILITY; CELLULAR DISTRIBUTION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG INDICATION; DRUG STRUCTURE; ENZYME ACTIVITY; FIBROBLAST CULTURE; HUMAN; HUMAN CELL; LIGHT DAMAGE; OXIDATIVE STRESS; PHOTOOXIDATION; PHOTOTOXICITY; PROTEIN EXPRESSION; RADIATION DOSE; SKIN PROTECTION; ULTRAVIOLET A RADIATION;

ANTIOXIDANTS; APOPTOSIS; BETA CAROTENE; CANTHAXANTHIN; CASPASE 3; CATALASE; CELLS, CULTURED; DERMIS; DOSE-RESPONSE RELATIONSHIP, DRUG; DOSE-RESPONSE RELATIONSHIP, RADIATION; FIBROBLASTS; HEME OXYGENASE-1; HUMANS; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE; THIOBARBITURIC ACID REACTIVE SUBSTANCES; ULTRAVIOLET RAYS; XANTHOPHYLLS;

EID: 64549119187     PISSN: 09066705     EISSN: 16000625     Source Type: Journal    
DOI: 10.1111/j.1600-0625.2008.00790.x     Document Type: Article

References (60)

1. Ichihashi M, Ueda M, Budiyanto A et al. UV-induced skin damage. Toxicology 2003: 189: 21-39.
2. Dalle Carbonare M, Pathak M A. Skin photosensitizing agents and the role of reactive oxygen species in photoaging. J Photochem Photobiol B 1992: 14: 105-124.
3. Wondrak G T, Jacobson M K, Jacobson E L. Endogenous UVA-photosensitizers: Mediators of skin photodamage and novel targets for skin photoprotection. Photochem Photobiol Sci 2006: 5: 215-237.
4. Berneburg M, Grether-Beck S, Kurten V et al. Singlet oxygen mediates the UVA-induced generation of the photoaging-associated mitochondrial common deletion. J Biol Chem 1999: 2742: 15345-15349.
5. Wlaschek M, Briviba K, Stricklin G P, Sies H, Scharffetter-Kochanek K. Singlet oxygen may mediate the ultraviolet A-induced synthesis of interstitial collagenase. J Invest Dermatol 1995: 104: 194-198.
6. Scharffetter-Kochanek K, Wlaschek M, Brenneisen P et al. UV-induced reactive oxygen species in photocarcinogenesis and photoaging. Biol Chem 1997: 378: 1247-1257.
7. Fisher G J, Datta S C, Talwar H S et al. Molecular basis of sun-induced premature aging and retinoid antagonism. Nature 1996: 379: 335-339.
8. Shindo Y, Witt E, Han D, Packer L. Dose-response effects of acute ultraviolet irradiation on antioxidants and molecular markers of oxidation in murine epidermis and dermis. J Invest Dermatol 1994: 102: 470-475.
9. Steenvoorden D P, van Henegouwen G M. The use of endogenous antioxidants to improve photoprotection. J Photochem Photobiol B 1997: 41: 1-10.
10. Stahl W, Heinrich U, Wiseman S, Eichler O, Sies H, Tronnier H. Dietary tomato paste protects against ultraviolet light-induced erythema in humans. J Nutr 2001: 131: 1449-1451.
11. Jańczyk A, Garcia-Lopez M A, Fernandez-Peñas P et al. A Polypodium leucotomos extract inhibits solar-simulated radiation-induced TNF-alpha and iNOS expression, transcriptional activation and apoptosis. Exp Dermatol 2007: 16: 823-829.
12. Di Mascio P, Kaiser S, Sies H. Lycopene as the most efficient biological carotenoid singlet oxygen quencher. Arch Biochem Biophys 1989: 274: 532-538.
13. Sies H, Stahl W. Nutritional protection against skin damage from sunlight. Annu Rev Nutr 2004: 24: 173-200.
14. Greul A K, Grundmann J U, Heinrich F et al. Photoprotection of UV-irradiated human skin: An antioxidative combination of vitamins E and C, carotenoids, selenium and proanthocyanidins. Skin Pharmacol Appl Skin Physiol 2002: 15: 307-315.
15. Jacobson M K, Kim H, Coyle W R et al. Effect of myristyl nicotinate on retinoic acid therapy for facial photodamage. Exp Dermatol 2007: 16: 927-935.
16. Burton G W, Ingold K U. beta-Carotene: An unusual type of lipid antioxidant. Science 1984: 224: 569-573.
17. Biesalski H K, Obermüller-Jevic U C. UV light, beta-carotene and human skinbeneficial and potentially harmful effects. Arch Biochem Biophys 2001: 389: 1-6.
18. Fuchs J. Potentials and limitations of the natural antioxidants RRR-alphatocopherol, L-ascorbic acid and beta-carotene in cutaneous photoprotection. Free Radic Biol Med 1998: 25: 848-873.
19. Eicker J, Kürten V, Wild S et al. Betacarotene supplementation protects from photoaging-associated mitochondrial DNA mutation. Photochem Photobiol Sci 2003: 2: 655-659.
20. Césarini J P, Michel L, Maurette J M, Adhoute H, Béjot M. Immediate effects of UV radiation on the skin: Modification by an antioxidant complex containing carotenoids. Photodermatol Photoimmunol Photomed 2003: 19: 182-189.
21. Swindells K, Rhodes L E. Influence of oral antioxidants on ultraviolet radiationinduced skin damage in humans. Photodermatol Photoimmunol Photomed 2004: 20: 297-304.
22. Wertz K, Hunziker P B, Seifert N et al. beta-Carotene interferes with ultraviolet light A-induced gene expression by multiple pathways. J Invest Dermatol 2005: 124: 428-434.
23. Palozza P, Krinsky N I. Astaxanthin and canthaxanthin are potent antioxidants in a membrane model. Arch Biochem Biophys 1992: 297: 291-295.
24. Mathews-Roth M M. Carotenoids in erythropoietic protoporphyria and other photosensitivity diseases. Ann N Y Acad Sci 1993: 691: 127-138.
25. Kennedy A R, Krinsky N I. Effects of retinoids, beta-carotene, and canthaxanthin on UV- and X-ray-induced transformation of C3H10T1/2 cells in vitro. Nutr Cancer 1994: 22: 219-232.
26. Savouré N, Briand G, Amory-Touz M C, Combre A, Maudet M, Nicol M. Vitamin A status and metabolism of cutaneous polyamines in the hairless mouse after UV irradiation: Action of beta-carotene and astaxanthin. Int J Vitam Nutr Res 1995: 65: 79-86.
27. Eichler O, Sies H, Stahl W. Divergent optimum levels of lycopene, beta-carotene and lutein protecting against UVB irradiation in human fibroblastst. Photochem Photobiol 2002: 75: 503-506.
28. Zhang L X, Cooney R V, Bertram J S. Carotenoids up-regulate connexin43 gene expression independent of their provitamin A or antioxidant properties. Cancer Res 1992: 52: 5707-5712.
29. Stahl W, von Laar J, Martin H D, Emmerich T, Sies H. Stimulation of gap junctional communication: Comparison of acyclo-retinoic acid and lycopene. Arch Biochem Biophys 2000: 373: 271-274.
30. Offord E A, Gautier J C, Avanti O et al. Photoprotective potential of lycopene, beta-carotene, vitamin E, vitamin C and carnosic acid in UVA-irradiated human skin fibroblasts. Free Radic Biol Med 2002: 32: 1293-1303.
31. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 1983: 652: 55-63.
32. Ohshima S. Apoptosis and necrosis in senescent human fibroblasts. Ann N Y Acad Sci 2006: 1067: 228-234.
33. Didier C, Kerblat I, Drouet C, Favier A, Beani J C, Richard M J. Induction of thioredoxin by ultraviolet-A radiation prevents oxidative-mediated cell death in human skin fibroblasts. Free Radic Biol Med 2001: 31: 585-598.
34. Larsson P, Andersson E, Johansson U, Öllinger K, Rosdahl I. Ultraviolet A and B affect human melanocytes and keratinocytes differently. A study of oxidative alterations and apoptosis. Exp Dermatol 2005: 14: 117-123.
35. Jentzsch A M, Bachmann H, Fürst P, Biesalski H K. Improved analysis of malondialdehyde in human body fluids. Free Radic Biol Med 1996: 20: 251-256.
36. Claiborne A. Catalase activity. In: Greenwald R A, ed. Handbook of Methods for Oxygen Radical Research. Boca Raton: CRC Press, 1985: 283-284.
37. Spitz D R, Oberley L W. An assay for superoxide dismutase activity in mammalian tissue homogenates. Anal Biochem 1989: 179: 8-18.
38. Keyse S M, Tyrrell R M. Heme oxygenase is the major 32-kDa stress protein induced in human skin fibroblasts by UVA radiation, hydrogen peroxide, and sodium arsenite. Proc Natl Acad Sci U S A 1989: 86: 99-103.
39. Trekli M C, Riss G, Goralczyk R, Tyrrell R M. Beta-carotene suppresses UVA induced HO-1 gene expression in cultured FEK4. Free Radic Biol Med 2003: 34: 456-464.
40. Steghens J-P, van Kappel A L, Riboli E, Collombel C. Simultaneous measurement of seven carotenoids, retinol and a-tocopherol in serum by high-performance liquid chromatography. J Chromatogr B 1997: 694: 71-81.
41. O'Sullivan L, Ryan L, O'Brien N. Comparison of the uptake and secretion of carotene and xanthophyll carotenoids by Caco-2 intestinal cells. Br J Nutr 2007: 98: 38-44.
42. Godar D E. UV doses worldwide. Photochem Photobiol 2005: 81: 736-749.
43. Maresca V, Flori E, Briganti S et al. UVA-induced modification of catalase charge properties in the epidermis is correlated with the skin phototype. J Invest Dermatol 2006: 126: 182-190.
44. Miller N J, Sampson J, Candeias L P, Bramley P M, Rice-Evans C A. Antioxidant activities of carotenes and xanthophylls. FEBS Lett 1996: 384: 240-242.
45. Chew B P, Park J S, Wong M W, Wong T S. A comparison of the anticancer activities of dietary beta-carotene, canthaxanthin and astaxanthin in mice in vivo. Anticancer Res 1999: 19: 1849-1853.
46. Ohshima S. Apoptosis in stress-induced and spontaneously senescent human fibroblasts. Biochem Biophys Res Commun 2004: 324: 241-246.
47. Thornberry N A, Lazebnik Y. Caspases: Enemies within. Science 1998: 281: 1312-1316.
48. Gaboriau F, Morlière P, Marquis I, Moysan A, Gèze M, Dubertret L. Membrane damage induced in cultured human skin fibroblasts by UVA irradiation. Photochem Photobiol 1993: 58: 515-520.
49. Woodall A A, Britton G, Jackson M J. Carotenoids and protection of phospholipids in solution or in liposomes against oxidation by peroxyl radicals: Relationship between carotenoid structure and protective ability. Biochim Biophys Acta 1997: 1336: 575-586.
50. Woodall A A, Lee S W, Weesie R J, Jackson M J, Britton G. Oxidation of carotenoids by free radicals: Relationship between structure and reactivity. Biochim Biophys Acta 1997: 1336: 33-42.
51. Lim B P, Nagao A, Terao J, Tanaka K, Suzuki T, Takama K. Antioxidant activity of xanthophylls on peroxyl radical-mediated phospholipids peroxidation. Biochim Biophys Acta 1992: 1126: 178-184.
52. Young A J, Lowe G M. Antioxidant and prooxidant properties of carotenoids. Arch Biochem Biophys 2001: 385: 20-27.
53. El-Agamey A, Lowe G M, McGarvey D J et al. Carotenoid radical chemistry and antioxidant/pro-oxidant properties. Arch Biochem Biophys 2004: 430: 37-48.
54. Palozza P, Calviello G, Serini S et al. beta-carotene at high concentrations induces apoptosis by enhancing oxy-radical production in human adenocarcinoma cells. Free Radic Biol Med 2001: 30: 1000-1007.
55. Applegate L A, Luscher P, Tyrrell R M. Induction of heme oxygenase: A general response to oxidant stress in cultured mammalian cells. Cancer Res 1991: 51: 974-978.
56. Alam J, Stewart D, Touchard C, Boinapally S, Choi A M, Cook J L. Nrf2, a Cap'n'Collar transcription factor, regulates induction of the heme oxygenase-1 gene. J Biol Chem 1999: 274: 26071-26078.
57. Obermüller-Jevic U C, Francz P I, Frank J, Flaccus A, Biesalski H K. Enhancement of the UVA induction of haem oxygenase-1 expression by beta-carotene in human skin fibroblasts. FEBS Lett 1999: 460: 212-216.
58. Obermüller-Jevic U C, Schlegel B, Flaccus A, Biesalski H K. The effect of betacarotene on the expression of interleukin-6 and heme oxygenase-1 in UV-irradiated human skin fibroblasts in vitro. FEBS Lett 2001: 509: 186-190.
59. Basu-Modak S, Lüscher P, Tyrrell R M. Lipid metabolite involvement in the activation of the human heme oxygenase-1 gene. Free Radic Biol Med 1996: 20: 887-897.
60. Köpcke W, Krutmann J. Protection from Sunburn with beta-Carotene-A Metaanalysis. Photochem Photobiol 2008: 84: 284-288.