Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2016 (2016), Article ID 8214631, 15 pages
http://dx.doi.org/10.1155/2016/8214631
Research Article

The Effect of Lycopene Preexposure on UV-B-Irradiated Human Keratinocytes

1Instituto de Investigação do Medicamento (iMed.ULisboa), Faculdade de Farmácia, Universidade de Lisboa, Avenida Professor Gama Pinto, 1649-003 Lisboa, Portugal
2Departamento de Biologia, Laboratório de Biotecnologia e Citómica, CESAM, Universidade de Aveiro, Campus Universitário de Santiago, 3810-193 Aveiro, Portugal

Received 20 May 2015; Revised 3 July 2015; Accepted 6 July 2015

Academic Editor: Luciano Saso

Copyright © 2016 Andreia Ascenso et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. Svobodová, J. Psotová, and D. Walterová, “Natural phenolics in the prevention of UV-induced skin damage. A review,” Biomedical Papers, vol. 147, no. 2, pp. 137–145, 2003. View at Publisher · View at Google Scholar · View at Scopus
  2. W. Stahl, U. Heinrich, O. Aust, H. Tronnier, and H. Sies, “Lycopene-rich products and dietary photoprotection,” Photochemical & Photobiological Sciences, vol. 5, no. 2, pp. 238–242, 2006. View at Publisher · View at Google Scholar · View at Scopus
  3. F. Afaq and H. Mukhtar, “Botanical antioxidants in the prevention of photocarcinogenesis and photoaging,” Experimental Dermatology, vol. 15, no. 9, pp. 678–684, 2006. View at Publisher · View at Google Scholar · View at Scopus
  4. F. Afaq, D. N. Syed, A. Malik et al., “Delphinidin, an anthocyanidin in pigmented fruits and vegetables, protects human HaCaT keratinocytes and mouse skin against UVB-mediated oxidative stress and apoptosis,” Journal of Investigative Dermatology, vol. 127, no. 1, pp. 222–232, 2007. View at Publisher · View at Google Scholar · View at Scopus
  5. S. Reagan-Shaw, J. Breur, and N. Ahmad, “Enhancement of UVB radiation-mediated apoptosis by sanguinarine in HaCaT human immortalized keratinocytes,” Molecular Cancer Therapeutics, vol. 5, no. 2, pp. 418–429, 2006. View at Publisher · View at Google Scholar · View at Scopus
  6. A. T. Dinkova-Kostova, “Phytochemicals as protectors against ultraviolet radiation: versatility of effects and mechanisms,” Planta Medica, vol. 74, no. 13, pp. 1548–1559, 2008. View at Publisher · View at Google Scholar · View at Scopus
  7. J. R. Mein, F. Lian, and X.-D. Wang, “Biological activity of lycopene metabolites: implications for cancer prevention,” Nutrition Reviews, vol. 66, no. 12, pp. 667–683, 2008. View at Publisher · View at Google Scholar · View at Scopus
  8. W. Stahl and H. Sies, “Carotenoids and flavonoids contribute to nutritional protection against skin damage from sunlight,” Molecular Biotechnology, vol. 37, no. 1, pp. 26–30, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. J. D. Ribaya-Mercado, M. Garmyn, B. A. Gilchrest, and R. M. Russell, “Skin lycopene is destroyed preferentially over β-carotene during ultraviolet irradiation in humans,” The Journal of Nutrition, vol. 125, no. 7, pp. 1854–1859, 1995. View at Google Scholar · View at Scopus
  10. H. Salman, M. Bergman, M. Djaldetti, and H. Bessler, “Lycopene affects proliferation and apoptosis of four malignant cell lines,” Biomedicine & Pharmacotherapy, vol. 61, no. 6, pp. 366–369, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. R. Zefferino, A. Leone, S. Piccaluga, R. Cincione, and L. Ambrosi, “Mercury modulates interplay between IL-1β, TNF-α, and gap junctional intercellular communication in keratinocytes: mitigation by lycopene,” Journal of Immunotoxicology, vol. 5, no. 4, pp. 353–360, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. D. E. Brash and P. A. Havre, “New careers for antioxidants,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 22, pp. 13969–13971, 2002. View at Publisher · View at Google Scholar · View at Scopus
  13. J. A. McGrath and J. Uitto, “Anatomy and organization of human skin,” in Rook's Textbook of Dermatology, pp. 1–53, Wiley-Blackwell, 2010. View at Google Scholar
  14. M. Andreassi and L. Andreassi, “Antioxidants in dermocosmetology: from the laboratory to clinical application,” Journal of Cosmetic Dermatology, vol. 2, no. 3-4, pp. 153–160, 2003. View at Publisher · View at Google Scholar
  15. T. P. Heffernan, M. Kawasumi, A. Blasina, K. Anderes, A. H. Conney, and P. Nghiem, “ATR-Chk1 pathway inhibition promotes apoptosis after UV treatment in primary human keratinocytes: potential basis for the UV protective effects of caffeine,” Journal of Investigative Dermatology, vol. 129, no. 7, pp. 1805–1815, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. Z. Fazekas, D. Gao, R. N. Saladi, Y. Lu, M. Lebwohl, and H. Wei, “Protective effects of lycopene against ultraviolet B-induced photodamage,” Nutrition and Cancer, vol. 47, no. 2, pp. 181–187, 2003. View at Publisher · View at Google Scholar · View at Scopus
  17. L. Tang, T. Jin, X. Zeng, and J.-S. Wang, “Lycopene inhibits the growth of human androgen-independent prostate cancer cells in vitro and in BALB/c nude mice,” The Journal of Nutrition, vol. 135, no. 2, pp. 287–290, 2005. View at Google Scholar · View at Scopus
  18. I. Pfitzner, P. I. Francz, and H. K. Biesalski, “Carotenoid:methyl-β-cyclodextrin formulations: an improved method for supplementation of cultured cells,” Biochimica et Biophysica Acta—General Subjects, vol. 1474, no. 2, pp. 163–168, 2000. View at Publisher · View at Google Scholar · View at Scopus
  19. E. A. Offord, J.-C. Gautier, O. Avanti et al., “Photoprotective potential of lycopene, β-carotene, vitamin E, vitamin C and carnosic acid in UVA-irradiated human skin fibroblasts,” Free Radical Biology and Medicine, vol. 32, no. 12, pp. 1293–1303, 2002. View at Publisher · View at Google Scholar · View at Scopus
  20. X. Xu, Y. Wang, A. I. Constantinou, M. Stacewicz-Sapuntzakis, P. E. Bowen, and R. B. Van Breemen, “Solubilization and stabilization of carotenoids using micelles: delivery of lycopene to cells in culture,” Lipids, vol. 34, no. 10, pp. 1031–1036, 1999. View at Publisher · View at Google Scholar · View at Scopus
  21. N. Augé, N. Santanam, and S. Parthasarathy, “An efficient method for solubilizing β-carotene in aqueous solutions,” Journal of Medicinal Food, vol. 1, no. 1, pp. 39–43, 1998. View at Publisher · View at Google Scholar
  22. A. W. Williams, T. W.-M. Boileau, S. K. Clinton, and J. W. Erdman Jr., “β-carotene stability and uptake by prostate cancer cells are dependent on delivery vehicle,” Nutrition and Cancer, vol. 36, no. 2, pp. 185–190, 2000. View at Publisher · View at Google Scholar · View at Scopus
  23. A. Junghans, H. Sies, and W. Stahl, “Carotenoid-containing unilamellar liposomes loaded with glutathione: a model to study hydrophobic-hydrophilic antioxidant interaction,” Free Radical Research, vol. 33, no. 6, pp. 801–808, 2000. View at Publisher · View at Google Scholar · View at Scopus
  24. P. Palozza, R. Muzzalupo, S. Trombino, A. Valdannini, and N. Picci, “Solubilization and stabilization of β-carotene in niosomes: delivery to cultured cells,” Chemistry and Physics of Lipids, vol. 139, no. 1, pp. 32–42, 2006. View at Publisher · View at Google Scholar · View at Scopus
  25. Y. Rahimpour and H. Hamishehkar, “Liposomes in cosmeceutics,” Expert Opinion on Drug Delivery, vol. 9, no. 4, pp. 443–455, 2012. View at Publisher · View at Google Scholar · View at Scopus
  26. E. B. Souto, R. H. Müller, and A. J. Almeida, “Topical delivery of oily actives using solid lipid particles,” Pharmaceutical Technology Europe, vol. 19, no. 12, pp. 28–32, 2007. View at Google Scholar · View at Scopus
  27. C.-Y. Lin, C.-S. Huang, and M.-L. Hu, “The use of fetal bovine serum as delivery vehicle to improve the uptake and stability of lycopene in cell culture studies,” British Journal of Nutrition, vol. 98, no. 1, pp. 226–232, 2007. View at Publisher · View at Google Scholar · View at Scopus
  28. S.-L. Yeh, C.-S. Huang, and M.-L. Hu, “Lycopene enhances UVA-induced DNA damage and expression of heme oxygenase-1 in cultured mouse embryo fibroblasts,” European Journal of Nutrition, vol. 44, no. 6, pp. 365–370, 2005. View at Publisher · View at Google Scholar · View at Scopus
  29. S. Shahrzad, E. Cadenas, A. Sevanian, and L. Packer, “Impact of water-dispersible beadlets as a vehicle for the delivery of carotenoids to cultured cells,” BioFactors, vol. 16, no. 3-4, pp. 83–91, 2002. View at Publisher · View at Google Scholar · View at Scopus
  30. J. S. Hurst, J. E. Centreras, W. G. Siems, and F. J. G. M. Van Kuijk, “Oxidation of carotenoids by heat and tobacco smoke,” BioFactors, vol. 20, no. 1, pp. 23–35, 2004. View at Publisher · View at Google Scholar · View at Scopus
  31. S. M. O'Sullivan, J. A. Woods, and N. M. O'Brien, “Use of Tween 40 and Tween 80 to deliver a mixture of phytochemicals to human colonic adenocarcinoma cell (CaCo-2) monolayers,” British Journal of Nutrition, vol. 91, no. 5, pp. 757–764, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. C.-S. Huang, M.-K. Shih, C.-H. Chuang, and M.-L. Hu, “Lycopene inhibits cell migration and invasion and upregulates Nm23-H1 in a highly invasive hepatocarcinoma, SK-Hep-1 cells,” The Journal of Nutrition, vol. 135, no. 9, pp. 2119–2123, 2005. View at Google Scholar · View at Scopus
  33. G. Da Violante, N. Zerrouk, I. Richard, G. Provot, J. C. Chaumeil, and P. Arnaud, “Evaluation of the cytotoxicity effect of dimethyl sulfoxide (DMSO) on Caco2/TC7 colon tumor cell cultures,” Biological and Pharmaceutical Bulletin, vol. 25, no. 12, pp. 1600–1603, 2002. View at Publisher · View at Google Scholar · View at Scopus
  34. A. M. Rodríguez, S. Sastre, J. Ribot, and A. Palou, “Beta-carotene uptake and metabolism in human lung bronchial epithelial cultured cells depending on delivery vehicle,” Biochimica et Biophysica Acta—Molecular Basis of Disease, vol. 1740, no. 2, pp. 132–138, 2005. View at Publisher · View at Google Scholar · View at Scopus
  35. M. D. Gross, T. D. Bishop, J. D. Belcher, and D. R. Jacobs Jr., “Solubilization of β-carotene in culture media,” Nutrition and Cancer, vol. 27, no. 2, pp. 174–176, 1997. View at Publisher · View at Google Scholar · View at Scopus
  36. K. R. Martin, G. Loo, and M. L. Failla, “Human lipoproteins as a vehicle for the delivery of β-carotene and α-tocopherol to HepG2 cells,” Proceedings of the Society for Experimental Biology and Medicine, vol. 214, no. 4, pp. 367–378, 1997. View at Publisher · View at Google Scholar · View at Scopus
  37. R. V. Cooney, T. J. Kappock, A. Pung, and J. S. Bertram, “[6] Solubilization, cellular uptake, and activity of β-carotene and other carotenoids as inhibitors of neoplastic transformation in cultured cells,” in Methods in Enzymology, P. Lester, Ed., vol. 214, pp. 55–68, Academic Press, 1993. View at Publisher · View at Google Scholar
  38. R. R. Wei, W. G. Wamer, L. A. Lambert, and A. Kernhauser, “β-Carotene uptake and effects on intracellular levels of retinol in vitro,” Nutrition and Cancer, vol. 30, no. 1, pp. 53–58, 1998. View at Publisher · View at Google Scholar · View at Scopus
  39. R. B. van Breemen and N. Pajkovic, “Multitargeted therapy of cancer by lycopene,” Cancer Letters, vol. 269, no. 2, pp. 339–351, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. P. Boukamp, R. T. Petrussevska, D. Breitkreutz, J. Hornung, A. Markham, and N. E. Fusenig, “Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line,” Journal of Cell Biology, vol. 106, no. 3, pp. 761–771, 1988. View at Publisher · View at Google Scholar · View at Scopus
  41. K. Park and J.-H. Lee, “Protective effects of resveratrol on UVB-irradiated HaCaT cells through attenuation of the caspase pathway,” Oncology Reports, vol. 19, no. 2, pp. 413–417, 2008. View at Google Scholar · View at Scopus
  42. L. Struijk, E. van der Meijden, S. Kazem et al., “Specific betapapillomaviruses associated with squamous cell carcinoma of the skin inhibit UVB-induced apoptosis of primary human keratinocytes,” Journal of General Virology, vol. 89, no. 9, pp. 2303–2314, 2008. View at Publisher · View at Google Scholar · View at Scopus
  43. K. Park and J.-H. Lee, “Photosensitizer effect of curcumin on UVB-irradiated HaCaT cells through activation of caspase pathways,” Oncology Reports, vol. 17, no. 3, pp. 537–540, 2007. View at Google Scholar · View at Scopus
  44. E. M. Bruzell, E. Morisbak, and H. H. Tønnesen, “Studies on curcumin and curcuminoids. XXIX. Photoinduced cytotoxicity of curcumin in selected aqueous preparations,” Photochemical & Photobiological Sciences, vol. 4, no. 7, pp. 523–530, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. M. Athar, A. L. Kim, N. Ahmad, H. Mukhtar, J. Gautier, and D. R. Bickers, “Mechanism of ultraviolet B-induced cell cycle arrest in G2/M phase in immortalized skin keratinocytes with defective p53,” Biochemical and Biophysical Research Communications, vol. 277, no. 1, pp. 107–111, 2000. View at Publisher · View at Google Scholar · View at Scopus
  46. J. M. P. F. de Oliveira, C. Remédios, H. Oliveira et al., “Sulforaphane induces DNA damage and mitotic abnormalities in human osteosarcoma MG-63 cells: correlation with cell cycle arrest and apoptosis,” Nutrition and Cancer, vol. 66, no. 2, pp. 325–334, 2014. View at Publisher · View at Google Scholar · View at Scopus
  47. J. M. P. Ferreira de Oliveira, M. Costa, T. Pedrosa et al., “Sulforaphane induces oxidative stress and death by p53-independent mechanism: Implication of impaired glutathione recycling,” PLoS ONE, vol. 9, no. 3, Article ID e92980, 2014. View at Publisher · View at Google Scholar · View at Scopus
  48. S. Rozen and H. Skaletsky, “Primer3 on the WWW for general users and for biologist programmers,” Methods in Molecular Biology, vol. 132, pp. 365–386, 2000. View at Google Scholar
  49. J. Kent, UCSC in Silico PCR, 2013, http://genome.ucsc.edu/cgi-bin/hgPcr?command=start.
  50. S. Zhao and R. D. Fernald, “Comprehensive algorithm for quantitative real-time polymerase chain reaction,” Journal of Computational Biology, vol. 12, no. 8, pp. 1047–1064, 2005. View at Publisher · View at Google Scholar · View at Scopus
  51. M. W. Pfaffl, “A new mathematical model for relative quantification in real-time RT-PCR,” Nucleic Acids Research, vol. 29, no. 9, article e45, 2001. View at Publisher · View at Google Scholar · View at Scopus
  52. W. Stahl and H. Sies, “Lycopene: a biologically important carotenoid for humans?” Archives of Biochemistry and Biophysics, vol. 336, no. 1, pp. 1–9, 1996. View at Publisher · View at Google Scholar · View at Scopus
  53. W. H. F. Sutherland, R. J. Walker, S. A. De Jong, and J. E. Upritchard, “Supplementation with tomato juice increases plasma lycopene but does not alter susceptibility to oxidation of low-density lipoproteins from renal transplant recipients,” Clinical Nephrology, vol. 52, no. 1, pp. 30–36, 1999. View at Google Scholar · View at Scopus
  54. E.-S. Hwang and H. J. Lee, “Inhibitory effects of lycopene on the adhesion, invasion, and migration of SK-Hep1 human hepatoma cells,” Experimental Biology and Medicine, vol. 231, no. 3, pp. 322–327, 2006. View at Google Scholar
  55. B. Halliwell, “Oxidative stress in cell culture: an under-appreciated problem?” FEBS Letters, vol. 540, no. 1–3, pp. 3–6, 2003. View at Publisher · View at Google Scholar · View at Scopus
  56. L. K. Henry, N. L. Puspitasari-Nienaber, M. Jaren-Galan, R. B. Van Breemen, G. L. Catignani, and S. J. Schwartz, “Effects of ozone and oxygen on the degradation of carotenoids in an aqueous model system,” Journal of Agricultural and Food Chemistry, vol. 48, no. 10, pp. 5008–5013, 2000. View at Publisher · View at Google Scholar · View at Scopus
  57. P. Palozza, “Prooxidant actions of carotenoids in biologic systems,” Nutrition Reviews, vol. 56, no. 9, pp. 257–265, 1998. View at Google Scholar · View at Scopus
  58. C. S. Boon, D. J. McClements, J. Weiss, and E. A. Decker, “Role of iron and hydroperoxides in the degradation of lycopene in oil-in-water emulsions,” Journal of Agricultural and Food Chemistry, vol. 57, no. 7, pp. 2993–2998, 2009. View at Publisher · View at Google Scholar · View at Scopus
  59. C. S. Boon, D. J. McClements, J. Weiss, and E. A. Decker, “Factors influencing the chemical stability of carotenoids in foods,” Critical Reviews in Food Science and Nutrition, vol. 50, no. 6, pp. 515–532, 2010. View at Publisher · View at Google Scholar · View at Scopus
  60. D. B. Lovejoy and D. R. Richardson, “Iron chelators as anti-neoplastic agents: current developments and promise of the PIH class of chelators,” Current Medicinal Chemistry, vol. 10, no. 12, pp. 1035–1049, 2003. View at Publisher · View at Google Scholar · View at Scopus
  61. M. Valko, C. J. Rhodes, J. Moncol, M. Izakovic, and M. Mazur, “Free radicals, metals and antioxidants in oxidative stress-induced cancer,” Chemico-Biological Interactions, vol. 160, no. 1, pp. 1–40, 2006. View at Publisher · View at Google Scholar · View at Scopus
  62. O. Livny, I. Kaplan, R. Reifen, S. Polak-Charcon, Z. Madar, and B. Schwartz, “Lycopene inhibits proliferation and enhances gap-junction communication of KB-1 human oral tumor cells,” The Journal of Nutrition, vol. 132, no. 12, pp. 3754–3759, 2002. View at Google Scholar · View at Scopus
  63. M. A. Al-Mohanna, F. M. Al-Khodairy, Z. Krezolek, P.-A. Bertilsson, A. Al-Houssein, and A. Aboussekhra, “P53 is dispensable for UV-induced cell cycle arrest at late G1 in mammalian cells,” Carcinogenesis, vol. 22, no. 4, pp. 573–578, 2001. View at Publisher · View at Google Scholar · View at Scopus
  64. S. Pavey, T. Russell, and B. Gabrielli, “G2 phase cell cycle arrest in human skin following UV irradiation,” Oncogene, vol. 20, no. 43, pp. 6103–6110, 2001. View at Publisher · View at Google Scholar · View at Scopus
  65. T. Pötter, W. Göhde, N. Wedemeyer, and W. Köhnlein, “Keratinocytes exposed to ultraviolet radiation reveal three down-regulated genes with potential function in differentiation and cell cycle control,” Radiation Research, vol. 154, no. 2, pp. 151–158, 2000. View at Google Scholar · View at Scopus
  66. A. Nahum, L. Zeller, M. Danilenko et al., “Lycopene inhibition of IGF-induced cancer cell growth depends on the level of cyclin D1,” European Journal of Nutrition, vol. 45, no. 5, pp. 275–282, 2006. View at Publisher · View at Google Scholar · View at Scopus
  67. Y.-A. Choi, B. R. Chin, D. H. Rhee et al., “Methyl-β-cyclodextrin inhibits cell growth and cell cycle arrest via a prostaglandin E2 independent pathway,” Experimental and Molecular Medicine, vol. 36, no. 1, pp. 78–84, 2004. View at Publisher · View at Google Scholar · View at Scopus
  68. A. R. Bowen, A. N. Hanks, S. M. Allen, A. Alexander, M. J. Diedrich, and D. Grossman, “Apoptosis regulators and responses in human melanocytic and keratinocytic cells,” Journal of Investigative Dermatology, vol. 120, no. 1, pp. 48–55, 2003. View at Publisher · View at Google Scholar · View at Scopus
  69. D. Raj, D. E. Brash, and D. Grossman, “Keratinocyte apoptosis in epidermal development and disease,” Journal of Investigative Dermatology, vol. 126, no. 2, pp. 243–257, 2006. View at Publisher · View at Google Scholar · View at Scopus
  70. V. Chaturvedi, P. Bacon, B. Bodner, and B. J. Nickoloff, “Proliferating cultured human keratinocytes are more susceptible to apoptosis compared with mouse keratinocytes,” Journal of Investigative Dermatology, vol. 123, no. 6, pp. 1200–1203, 2004. View at Publisher · View at Google Scholar · View at Scopus
  71. R. Challa, A. Ahuja, J. Ali, and R. K. Khar, “Cyclodextrins in drug delivery: an updated review,” AAPS PharmSciTech, vol. 6, no. 2, pp. E329–E357, 2005. View at Publisher · View at Google Scholar · View at Scopus
  72. A. Vyas, S. Saraf, and S. Saraf, “Cyclodextrin based novel drug delivery systems,” Journal of Inclusion Phenomena and Macrocyclic Chemistry, vol. 62, no. 1-2, pp. 23–42, 2008. View at Publisher · View at Google Scholar · View at Scopus
  73. K. S. George, W. Elyassaki, Q. Wu, and S. Wu, “The role of cholesterol in UV light B-induced apoptosis,” Photochemistry and Photobiology, vol. 88, no. 5, pp. 1191–1197, 2012. View at Publisher · View at Google Scholar · View at Scopus
  74. M. H. Aziz, H. T. Manoharan, and A. K. Verma, “Protein kinase Cε, which sensitizes skin to sun's UV radiation—induced cutaneous damage and development of squamous cell carcinomas, associates with Stat3,” Cancer Research, vol. 67, no. 3, pp. 1385–1394, 2007. View at Publisher · View at Google Scholar · View at Scopus
  75. T. Karlsson, A. Vahlquist, and H. Törmä, “Keratinocyte differentiation induced by calcium, phorbol ester or interferon-γ elicits distinct changes in the retinoid signalling pathways,” Journal of Dermatological Science, vol. 57, no. 3, pp. 207–213, 2010. View at Publisher · View at Google Scholar · View at Scopus
  76. F. Afaq and H. Mukhtar, “Effects of solar radiation on cutaneous detoxification pathways,” Journal of Photochemistry and Photobiology B: Biology, vol. 63, no. 1–3, pp. 61–69, 2001. View at Publisher · View at Google Scholar · View at Scopus
  77. A. B. Petersen, R. Gniadecki, J. Vicanova, T. Thorn, and H. C. Wulf, “Hydrogen peroxide is responsible for UVA-induced DNA damage measured by alkaline comet assay in HaCaT keratinocytes,” Journal of Photochemistry and Photobiology B: Biology, vol. 59, no. 1–3, pp. 123–131, 2000. View at Publisher · View at Google Scholar · View at Scopus
  78. H. Sies and C. F. M. Menck, “Singlet oxygen induced DNA damage,” Mutation Research DNAging, vol. 275, no. 3–6, pp. 367–375, 1992. View at Publisher · View at Google Scholar · View at Scopus
  79. S. Onoue, Y. Seto, A. Oishi, and S. Yamada, “Novel methodology for predicting photogenotoxic risk of pharmaceutical substances based on reactive oxygen species (ROS) and DNA-binding assay,” Journal of Pharmaceutical Sciences, vol. 98, no. 10, pp. 3647–3658, 2009. View at Publisher · View at Google Scholar · View at Scopus
  80. B. Harang, Composition Having Tanning and Photoprotective Activity, and Its Cosmetic Applications, Laboratoire Oenobiol, 2000.
  81. A. Nagao, “Oxidative conversion of carotenoids to retinoids and other products,” Journal of Nutrition, vol. 134, no. 1, pp. 237S–240S, 2004. View at Google Scholar · View at Scopus
  82. H. L. Hantz, L. F. Young, and K. R. Martin, “Physiologically attainable concentrations of lycopene induce mitochondrial apoptosis in LNCaP human prostate cancer cells,” Experimental Biology and Medicine, vol. 230, no. 3, pp. 171–179, 2005. View at Google Scholar · View at Scopus
  83. A. D. Rhim and A. K. Rustgi, “Three-dimensional organotypic culture of stratified epithelia,” Cold Spring Harbor Protocols, vol. 2015, no. 4, pp. 349–353, 2015. View at Publisher · View at Google Scholar
  84. A. Acheva, M. Ghita, G. Patel, K. M. Prise, and G. Schettino, “Mechanisms of DNA damage response to targeted irradiation in organotypic 3D skin cultures,” PLoS ONE, vol. 9, no. 2, Article ID e86092, 2014. View at Publisher · View at Google Scholar · View at Scopus
  85. H. Vörsmann, F. Groeber, H. Walles et al., “Development of a human three-dimensional organotypic skin-melanoma spheroid model for in vitro drug testing,” Cell Death and Disease, vol. 4, no. 7, article e719, 2013. View at Publisher · View at Google Scholar · View at Scopus