Plants as a source of photoprotective compounds against ultraviolet radiation-induced DNA damage
Portada 43 (168) 2019
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Fuentes Lorenzo, J. L. (2019). Plants as a source of photoprotective compounds against ultraviolet radiation-induced DNA damage. Revista De La Academia Colombiana De Ciencias Exactas, Físicas Y Naturales, 43(168), 550–562. https://doi.org/10.18257/raccefyn.841

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Abstract

Photoprotection is a preventive and therapeutic strategy against skin cancer and photoaging. In the present work, we
review the adverse biological effects of the ultraviolet radiation, the basic concepts with relevance in photoprotection,
and the methods to carry out its measurement. Likewise, we summarized the main results obtained from the radiobiological and genetic characterization of the SOS Chromotest model, which we used for bioprospecting photoprotective activity of plant extracts and molecules. Besides, we showed photoprotective efficacy and/or
antigenotoxicity estimates of plant essential oils and extracts, as well as of the major compounds of promissory oils and extracts analyzed in our study. Finally, action mechanisms of the relevant molecules are postulated. These results are presented and discussed considering their potential use to formulate multifunctional sunscreen.

https://doi.org/10.18257/raccefyn.841

Keywords

Radiación ultravioleta; Fotoprotección; Antigenotoxicidad; Metabolitos secundiarios de plantas | Ultraviolet radiation; Photoprotection; Antigenotoxicity; Plant secondary metabolites.
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References

Adams DH, Shou Q, Wohlmuth H, Cowin AJ. (2016). Data on keratin expression in human cells cultured with Australian native plant extracts. Data inBrief. 7: 848-867.

Adhami, V.M., Syed, D.N., Khan, N., Afaq. F. (2008). Phytochemicals for prevention of solar ultraviolet radiationinduced damages. Photochem. Photobiol. 84: 489-500.

Afaq, F. & Katiyar, S.K. (2011). Polyphenols: Skin Photoprotection and Inhibition of Photocarcinogenesis. Mini Rev. Med. Chem. 11: 1200-1215.

Arad, S., Konnikov, N., Goukassian, D.A., Gilchrest, B.A. (2007). Quantification of inducible SOS-like photoprotective responses in human skin. J. Invest. Dermatol. 127: 2629-2636.

Arad, S., Zattra, E., Hebert, J., Epstein, EH,, Goukassian, D.A., Gilchrest, B.A. (2008). Topical thymidine dinucleotide treatment reduces development of ultraviolet-induced basal cell carcinoma in Ptch-1+/- mice. Am. J. Pathol. 172: 1248-1255.

Bendová, H., Akrman, J., Krejčí, A., Kubáč, L., Jírová, D., Kejlová, K., Kolářová, H., Brabec, M., Malý, M. (2007). In vitro approaches to evaluation of Sun Protection Factor. Toxicology in Vitro. 21: 1268-1275.

Brash, D.E. (2015). UV signature mutations. Photochem. Photobiol. 91: 15-26.

Brem, R., Guven, M., Karran, P. (2017). Oxidatively-generated damage to DNA and proteins mediated by photosensitized UVA. Free Radic. Biol. Med. 107: 101-109.

Bravo, K., Duque, L,., Ferreres, F., Moreno, D.A., Osorio, E. (2017). Passiflora tarminiana fruits reduce UVB-induced photoaging in human skin fibroblasts. J. Photochem. Photobiol. B 168: 78-88.

Bueno-Sánchez, J.G., Martínez-Morales, J.R., Stashenko, E.E., Ribón, W. (2009). Anti-tubercular activity of eleven aromatic and medicinal plants occurring in Colombia. Biomédica. 29: 51-60.

Césarini, J.P. & Demanneville, S. (2000). Toward a genotoxic protection factor. Radiat. Prot. Dosim. 91: 89-91.

Chandra-Pal, H., Athar, M., Elmets, C.A., Afaq, F. (2015). Fisetin inhibits UVB-induced cutaneous inflammation and activation of PI3K/AKT/NFkB signaling pathways in SKH-1 hairless mice. Photochem. Photobiol. 91: 225-234.

Chen, L., Hu, J.Y., Wang, S.Q. (2012). He role of antioxidants in photoprotection: A critical review. J. Am. Acad. Dermatol. 67: 1013-1024.

Chhabra, G., Ndiaye, M.A., García-Peterson, L.M., Ahmad, N. (2017). Melanoma chemoprevention: Current status and future prospects. Photochem. Photobiol. 93: 975-989.

Chiang, H.M., Chan, S.Y., Chu, Y., Wen, K.C. (2015). Fisetin ameliorated photodamage by suppressing the mitogenactivated protein kinase/matrix metalloproteinase pathway and nuclear factor-κB pathways. J. Agric. Food Chem. 63: 4551-4560.

Chua, L.S., Lee, S.Y., Abdullah, N., Sarmini, M.R. (2012). Review on Labisia pumila (Kacip Fatimah): bioactive phytochemicals and skin collagen synthesis promoting herb. Fitoterapia. 83: 1322-1335.

Cos, P., Vlietinck, A.J., Vanden-Berghe, D., Maes, L. (2006). Antiinfective potential of natural products: How to develop a stronger in vitro ‘proof-of-concept’. J. Ethnopharmacol. 106: 290-302.

Cui, R., Widlund, H.R., Feige, E., Lin, J.Y., Wilensky, D.L., Igras, V.E., D’Orazio, J., Fung, C.Y., Schanbacher, C.F., Granter, S.R., Fisher, D.E. (2007). Central role of p53 in the suntan response and pathologic hyperpigmentation. Cell. 128: 853-864.

Díaz-Durán, L.T., Olivar-Rincón, N., Puerto-Galvis, C.E., Kouznetsov, V., Fuentes, J.L. (2015). Genotoxicity risk assessment of substituted quinolines using the SOS chromotest. Environmental Toxicology. 30: 278-292.

Eastmond, D.A., Hartwig, A., Anderson, D., Anwar, W.A., Cimino, M.C., Dobrev, I., Douglas, G.R., Nohmi, T., Phillips, D.H., Vickers, C. (2009). Mutagenicity testing for chemical risk assessment: update of the WHO/IPCS harmonized scheme. Mutagenesis 24: 341-349.

Eller, M.S., Yaar, M., Gilchrest, B.A. (1997). Enhancement of DNA repair in human skin cells by thymidine dinucleotides: Evidence for a p53-mediated mammalian SOS response. Proc. Natl. Acad. Sci. USA. 94: 12627-12632.

Eller, M.S., Asarch, A., Gilchrest, B.A. (2008). Photoprotection in human skin- A multifaceted SOS response. Photochem. Photobiol. 84: 339-349.

Elmets, C.A., Singh, D., Tubesing, K., Matsui, M., Katiyar, S., Mukhtar, H. (2001). Cutaneous photoprotection from ultraviolet injury by green tea polyphenols. J. Am. Acad. Dermatol. 44: 425-432.

Escobar, P., Leal, S.M., Herrera, L.V., Martínez, J.R., Stashenko, E.E. (2010). Chemical composition and antiprotozoal activities of Colombian Lippia spp essential oils and their major components. Mem. Inst. Oswaldo Cruz. 105: 184-190.

Escobar, P.A., Kemper, R.A., Tarca, J., Nicolette, J., Kenyon, M., Glowienke, S., Sawant, S.G., Christensen, J., Johnson, T.E., McKnight, C., Ward, G., Galloway, S.M., Custer, L., Gocke, E., O’Donovan, M.R., Braun, K., Snyder, R.D., Mahadevan, B. (2013). Bacterial mutagenicity screening in the pharmaceutical industry. Mutat. Res. 752: 99-118.

Estévez-Castro, C.F., Serment-Guerrero, J.H., Fuentes, J.L. 2018. Influence of the uvrA, recJ and recN gene mutations on the nucleoid reorganization in UV-treated Escherichia coli cells. FEMS Microbiology Letters 365: fny110.

European Cosmetic, Toiletry and Perfumery Association (COLIPA). (2011). Method for In Vitro Determination of UVA Protection. In vitro method for the determination of the UVA protection factor and “critical wavelength” values of sunscreen products. Guidelines March 2011.

Food and Drug Administration. (2011). Department of Health and Human Services. 21 CFR Parts 201 and 310. [Docket No. FDA–1978–N–0018-0698]. Labeling and Effectiveness Testing; Sunscreen Drug Products for Over-the-Counter Human Use. Final Rule. Fed. Regist. 76: 35620-35665.

Fourtanier, A., Moyal, D., Maccario, J., Compan, D., Wolf, P., Quehenberger, F., Cooper, K., Baron, E., Halliday, G., Poon, T., Seed, P., Walker, S.L., Young, A.R. (2005). Measurement of Sunscreen Immune Protection Factors in Humans: A Consensus Paper. J. Invest. Dermatol. 125:403-409.

Fuentes, J.L., Vernhe, M., Cuetara, E.B., Sánchez-Lamar, A., Santana, J.L., Llagostera, M. (2006a). Tannins from barks of Pinus caribeae Morelet protect Escherichia coli cells against DNA damage induced by γ-rays. Fitoterapia. 77:116-120.

Fuentes, J.L., Alonso, A., Cuétara, E., Vernhe, M., Álvarez, N., Sánchez-Lamar, A., Llagostera, M. (2006b). Usefulness of SOS Chromotest in the study of medicinal plant as radioprotectors. Int. J. Radiat. Biol. 82: 323-329.

Fuentes, J.L., García-Forero, A., Quintero-Ruiz, N., Prada-Medina, C.A., Rey-Castellanos, N., Franco-Niño, D.A., Contreras-García, D.A., Córdoba-Campo, Y., Stashenko EE. (2017). The SOS Chromotest applied for screening plant antigenotoxic agents against ultraviolet radiation. Photochem. Photobiol. Sci. 16: 1424-1434.

Ganesan, A. & Hanawalt P. (2016). Photobiological origins of the field of genomic maintenance. Photochem. Photobiol. 92: 52-60.

García-Bores, A.M., Espinosa-González, A.M., Reyna-Campos, A., Cruz-Toscano, S., Benítez-Flores, J.C., Hernández-Delgado, C.T., Flores-Maya, S., Urzúa-Meza, M., Peñalosa-Castro, I., Céspedes-Acuña, C.L., Ávila-Acevedo, J.G. (2017). Lippia graveolens photochemopreventive effect against UVB radiation-induced skin carcinogénesis. J. Photochem. Photobiol. B 167: 72-81.

García-Forero, A., Villamizar-Mantilla, D.A., Núñez, L.A., Ocazionez, R.E., Stashenko, E.E., Fuentes, J.L. (2019). Photoprotective and antigenotoxic effects of the flavonoids apigenin, naringenin, and pinocembrin. Photochem. Photobiol. 95: 1010-1018. Doi: 10.1111/php.13085.

Gatz, S.A. & Wiesmuller, L. (2006). p53 in recombination and repair. Cell Death Differ. 13: 1003-1016. Giampieri, F., Álvarez-Suárez, J.M., Tulipani, S., Gonzàles-Paramàs, A.M., Santos-Buelga, C., Bompadre, S., Quiles, J.L., Mezzetti, B., Battino, M. (2012). Photoprotective potential of strawberry (Fragaria × Ananassa) extract against UV-A irradiation damage on human fibroblasts. J. Agric. Food Chem. 60: 2322-2327.

Goukassian, D.A., Sharov, A., Rhodes, J., Coleman, C., Eller, M.S., Sharova, T., Bhawan, J., Gilchrest, B.A. (2012). Topical application of thymidine dinucleotide to newborn mice reduces and delays development of UV-induced melanomas. J. Invest. Dermatol. 132: 2664-2666.

Herrera-Moreno, A.M., Carranza, C.E., Chacón-Sánchez, M.I. (2013). Establishment of propagation methods for growing promising aromatic plant species of the Lippia (Verbenaceae) and Tagetes (Asteraceae) genera in Colombia. Agronomía Colombiana. 31: 27-37.

Herrling, T., Jung, K., Chatelain, E., Langenauer, M. (2006). Radical Skin/Sun Protection Factor RSF –Protection against UV-induced Free Radicals in Skin. SÖFW-Journal. 132: 24-30.

Huang, D., Ou, B., Hampsch-Woodill, M., Flanagan, J.A., Prior, R.L. (2002). High-throughput assay of oxygen radical absorbance capacity (ORAC) using a multichannel liquid handling system coupled with a microplate fluorescence reader in 96-well format. J. Agric. Food Chem. 50:4437-4444.

Huisman, O. & D’Ari, R. (1981). An inducible DNA replicationcell division coupling mechanism in Escherichia coli. Nature. 290: 797-799.

Ikehata, H., Higashi, S., Nakamura, S., Daigaku, Y., Furusawa, Y., Kamei, Y., Watanabe, M., Yamamoto, K., Hieda, K., Munakata, N., Ono, T. (2013). Action spectrum analysis of UVR genotoxicity for skin: The border wavelengths between UVA and UVB can bring serious mutation loads to skin. J. Invest. Dermat. 133: 1850-1856.

Jansen, R., Osterwalder, U., Wang, S.Q., Burnett, M., Lim, H.W. (2013). Photoprotection: Part II. Sunscreen: development, efficacy, and controversies. J. Am. Acad. Dermatol. 69: 867.e1-14.

Jarzycka, A., Lewińska, A., Gancarz, R., Wilk, K.A. (2013). Assessment of extracts of Helichrysum arenarium, Crataegus monogyna, Sambucus nigra in photoprotective UVA and UVB; photostability in cosmetic emulsions. J. Photochem. Photobiol. B 128: 50-57.

Jonason, A.S., Kunala, S., Price, G.J., Restifo, R.J., Spinell, H.M., Persing, J.A., Leffell, D.J., Tarone, R.E., Brash, D.E. (1996). Frequent clones of p53-mutated keratinocytes in normal human skin. Proc. Natl. Acad. Sci. USA. 93: 14025-14029.

Kada, T. & Shimoi K. (1987). Desmutagens and bio-antimutagens - Their modes of action. BioEssays. 7: 113-116.

Kneuttinger, A.C., Kashiwazaki, G., Prill, S., Heil, K., Müller, M., Carell, T. (2014). Formation and direct repair of UVinduced dimeric DNA pyrimidine lesions. Photochem. Photobiol. 90: 1-14.

Korać, R.R. & Khambholja, K.M. (2011). Potential of herbs in skin protection from ultraviolet radiation. Pharmacognosy Reviews. 5: 164-173.

Linos, E., Swetter, S.M., Cockburn, M.G., Colditz, G.A., Clarke, C.A. (2009). Increasing burden of melanoma in the United States. J. Invest. Dermat. 129: 1666-1674.

López, M.A., Stashenko, E.E., Fuentes, J.L. (2011). Chemical composition and antigenotoxic properties of the Lippia alba essential oils. Genet. Mol. Biol. 34: 479-488.

Lund, L.P. & Timmins, G.S. (2007). Melanoma, long wavelength ultraviolet and sunscreens: Controversies and potential resolutions. Pharmacol. Ther. 114: 198-207.

Mayer, S., Eller, M.S., Gilchrest, B.A. (2001). The SOS response in human skin. Curr. Probl. Dermatol. 13: 153-158.

Mejía‐Giraldo, J.C., Henao‐Zuluaga, K., Gallardo, C., Atehortúa, L., Puertas‐Mejía, M.A. (2016a). Novel in vitro antioxidant and photoprotection capacity of plants from high altitude ecosystems of Colombia. Photochem. Photobiol. 92: 150-157.

Mejía‐Giraldo, J.C., Winkler, R., Gallardo, C., Sánchez-Zapata, A.M., Puertas-Mejía, M.A. (2016b). Photoprotective potential of Baccharis antioquensis (Asteraceae) as natural sunscreen. Photochem. Photobiol. 92: 742-752.

Meneses, R., Ocazionez, R.E., Martínez, J.R., Stashenko, E.E. (2009). Inhibitory effect of essential oils obtained from plants grown in Colombia on yellow fever virus replication in vitro. Ann. Clin. Microbiol. Antimicrob. 8: 8.

Metral, E., Rachidi, W., Damour, O., Demarne, F., Bechetoille, N. (2018). Long-term genoprotection effect of Sechium edule fruit extract against UVA irradiation in keratinocytes. Photochem. Photobiol. 94: 343-350.

Meza-Joya, F.L., Ramírez-Pinilla, M.P., Fuentes, J.L. (2017). The direct-developing frog Eleutherodactylus johnstonei (Eleutherodactylidae) as biological model for the study of toxic, cytotoxic, and genotoxic effects of agrochemicals. In: Ecotoxicological and Genotoxicological Non-traditional Terrestrial Models, Issues in Toxicology 32, Marcelo L. Larramendy (editors), Chapter 10, Royal Society of Chemistry (RSC) Publishers, Cambridge, United Kingdom, p. 211-227.

Mesa, F.L., Ramírez, M.P., Fuentes, J.L. (2013). Toxic, cytotoxic and genotoxic effects of a glyphosate formulation (Roundup®SL-Cosmoflux®411F) in the direct developing frog Eleutherodactylus johnstonei. Environ. Mol. Mutagen. 54: 362-373.

Montes de Oca, M.K., Pearlman, R.L., McClees, S.F., Strickland, R., Afaq, F. (2017). Phytochemicals for the prevention of photocarcinogenesis. Photochem. Photobiol. 93: 956-974.

Mukherjee, P.K., Maity, N., Nema, N.K., Sarkar, B.K. (2011). Bioactive compounds from natural resources against skin aging. Phytomedicine. 19: 64-73.

Naranjo-Gómez, E.J., Puertas-Mejía, M.A., Mejía-Giraldo, J.C., Amaya-Nieto, A.Z., Atehortúa, L. (2018). Micropropagation of Baccharis antioquensis (Asteraceae) and photoinduction of polyphenols by UV radiation. Rev. Biol. Trop. 66: 754-764.

Narayanan, D.L., Saladi, R.N., Fox, J.L. (2010). Ultraviolet radiation and skin cancer. Int. J. Dermatol. 49: 978-986.

Nunes, A.R., Rodrigues, A.L.M., Brito de Queiroz, D., Vieira, I.G.P., Neto, J.F.C., Calixto Junior, J.T., Tintino, S.R., Maia de Morais, S., Coutinho, H.D.M. (2018). Photoprotective potential of medicinal plants from Cerrado biome (Brazil) in relation to phenolic content and antioxidant activity. J. Photochem. Photobiol. B 189: 119-123.

Parrish, J., Jaenicke, K.F., Anderson, R.R. (1982). Erythema and melanogenesis action spectra of normal human skin. Photochem. Photobiol. 36: 187-191.

Pereira, B.K., Rosa, R.M., da Silva, J., Guecheva, T.N., de Oliveira, I.M., Ianistcki, M., Benvegnú, V.C., Furtado, G.V., Ferraz, A., Richter, M.F., Schroder, N., Pereira, A.B., Henriques, J.A.P. (2009). Protective effects of three extracts from Antarctic plants against ultraviolet radiation in several biological models. J. Photochem. Photobiol. B 96:117-129.

Poon, F., Kang, S., Chien, A.L. (2015). Mechanisms and treatments of photoaging, Photodermatol. Photoimmunol. Photomed. 31: 65-74.

Prada-Medina, C.A., Aristizábal-Tessmer, E.T., Quintero-Ruiz, N., Serment-Guerrero, J., Fuentes, J.L. (2016). Survival and SOS response induction in ultraviolet B irradiated Escherichia coli cells with defective repair mechanisms. Int. J. Radiat. Biol. 92: 321-328.

Puertas-Mejía, M.A., Gutiérrez-Villegas, M.A., Mejía-Giraldo J.C., Winkler, R., Rojano, B. (2018). In vitro UV absorption properties and radical scavenging capacity of Morella parvifolia (Benth.) Parra-Os. extracts. Brazilian Journal of Pharmaceutical Sciences. 54: e17498.

Pfuhler, S., Fautz, R., Ouedraogo, G., Latil, A., Kenny, J., Moore, C., Diembeck, W., Hewitt, N.J., Reisinger, K., Barroso, J. (2014). The Cosmetics Europe strategy for animal-free genotoxicity testing: Project status up-date. Toxicology in Vitro. 28: 18-23.

Quillardet, P., Huisman, O., D´Ari, R., Hofnung, M. (1982). SOS chromotest, a direct assay of induction of an SOS function in Escherichia coli K-12 to measure genotoxicity. Proc. Natl. Acad. Sci. USA. 79: 5971-5975.

Quillardet, P. & Hofnung, M. (1984). Induction by UV light of the SOS funtion sfiA in Escherichia coli strains deficient or proficient in excision repair. J. Bacteriol. 157: 35-38.

Quintero, N., Stashenko, E.E., Fuentes, J.L. (2012). The influence of organic solvents on genotoxicity and antigenotoxicityestimates in the SOS Chromotest. Genet. Mol. Biol. 35:503-514.

Quintero-Ruiz, N., Córdoba-Campo, Y., Stashenko, E.E., Fuentes, J.L. (2017). Antigenotoxicity effect against ultraviolet radiation-induced DNA damage of the essential oils from Lippia species, Photochem. Photobiol. 93: 1063-1072.

Raman, V., Fuentes, J.L., Stashenko, E.E., Levy, M., Levy, M.M., Camarillo, I.G. (2017). A Lippia origanoides extract induces cell cycle arrest, apoptosis and suppresses NF-κB signaling in MDA-MB-231 triple-negative breast cancer cells. Int. J. Oncol. 51: 1801-1808.

Raman, V., Aryal, U.K., Hedrick, V., Mohallem-Ferreira, R., Fuentes, J.L., Stashenko, E.E., Levy, M., Levy, M.M., Camarillo, I.G. (2018). Proteomic analysis reveals an extract of the plant Lippia origanoides suppresses mitochondrial metabolism in triple-negative breast cancer cells. J. Proteome Res. 17: 3370-3383.

Reis Mansur, M.C.P.P., Guimarães Leitão, S., Cerqueira-Couthino, C., Vermelho, A.B., Silva, R.S., Presgrave, O.A.F., Leitão, A.A.C., Leitão, G.G., Ricci-Junior, E., Santos, E.P. (2016). In vitro and in vivo evaluation of efficacy and safety of photoprotective formulation containing antioxidant extracts. Rev. Bras. Farmacogn. 26: 251-258.

Saewan, N. & Jimtaisong, A. (2013). Photoprotection of natural flavonoids. J. Appl. Pharm. Sci. 3: 129-141.

Said, T., Dutot, M., Martin, C., Beaudeux, J.L., Boucher, C., Enee, E., Baudouin, C., Warnet, J.M., Rat, P. (2007). Cytoprotective effect against UV-induced DNA damage and oxidative stress: Role of new biological UV filter. Eur. J. Pharm. Sci. 30: 203-210.

Sánchez-Lamar, A., Fonseca, G., Fuentes, J.L., Cozzi, R., Cundari, E., Fiore, M., Ricordy, R., Perticone, P., Degrassi, F., De Salvia, R. (2008). Assessment of the genotoxic risk of Punica granatum L. (Punicaceae) whole fruit extracts. J. Ethnopharmacol. 115: 416-422.

Sánchez-Lamar, A., Fuentes, J.L., Fonseca, G., Alonso, A., Cápiro, N., Ferrer, M., Baluja, L., Fiore, M., De Salvia, R., Cozzi, R., Llagostera, M. (2002). Assessment of the potential genotoxic risk of Phyllantus orbicularis HBK aqueous extract using in vitro and in vivo assays. Toxicol. Lett. 136: 87-96.

Santamaría-Acebedo, L., Prada-Medina, C.A., Rondón-González, F., Stashenko, E.E., Martínez-Pérez, F.J., Levy, M., Levy, M.M., Fuentes, J.L. (2018). Interspecific variation and genetic relationships among Colombian Lippia species based on Small Ribosomal Subunit (SRS) gene sequence analysis. J. Herbs Spices Med. Plants. 24: 99-108.

Sayre, R.M., Agin, P.P., LeeVee, G.J., Morlowe, E. (1979). A comparison of in vivo and in vitro testing of sunscreens formulas. Photochem. Photobiol. 29: 559-566.

Schärer, O.D. (2013). Nucleotide excision repair in eukaryotes. Cold Spring Harb Perspect Biol. 5: a012609.

Schlacher, K. & Goodman MF. (2007). Lessons from 50 years of SOS DNA-damage-induced mutagenesis. Nature Reviews. 8: 587-594.

Schuch, A.P., Moraes, M.C.S., Yagura, T., Menck, C.F.M. (2014). Highly sensitive biological assay for determining the photoprotective efficacy of sunscreen. Environ. Sci. Technol. 48: 11584-11590.

Schuch, A.P., Moreno, N.C., Schuch, N.J., Menck, C.F.M., GarcÍa, C.C.M. (2017). Sunlight damage to cellular DNA: Focus on oxidatively generated lesions. Free Radic. Biol. Med. 107: 110-124.

Stashenko, E.E., Ruiz, C., Muñoz, A., Castañeda, M., Martínez, J. (2008). Composition and antioxidant activity of essential oils of Lippia origanoides HBK grown in Colombia. Nat. Prod. Commun. 3: 563-566.

Stashenko, E.E., Martínez, J.R., Cala, M.P., Durán, D.C., Caballero, D. (2013). Chromatographic and mass spectrometric characterization of essential oils and extracts from Lippia (Verbenaceae) aromatic plants. J. Sep.Sci. 36:192-202.

Stashenko, E.E. & Martínez, J.R. (2018). The expression of biodiversity in the secondary metabolites of aromatic plants and flowers growing in Colombia. In: Potential of essential oils, Hany A. El-Shemy (Ed.), Chapther 4, Intechopen, pp:59-86. Doi: 10.5772/intechopen.78001.

Stanfield, J., Osterwalder, U., Herzog, B. (2010). In vitro measurements of sunscreen protection. Photochem. Photobiol. Sci. 9: 489-494.

Stevanato, R., Bertelle, M., Fabris, S. (2014). Photoprotective characteristics of natural antioxidant polyphenols. Regul. Toxicol. Pharmacol. 69: 71-77.

Sundari, J., Selvaraj, R., Rajendra-Prasad, N., Elumalai, R. (2013). Jatropha curcas, leaf and bark fractions protect against ultraviolet radiation-B induced DNA damage in human peripheral blood lymphocytes. Environ. Toxicol. Pharmacol. 36: 875-882.

Sykora, P., Witt, K.L., Revanna, P., Smith-Roe, S.L., Dismukes, J., Lloyd, D.G., Engelward, B.P., Sobol, R.W. (2018). Next generation high throughput DNA damage detection platform for genotoxic compound screening. Scientific Reports. 8: 2771.

Tewari, A., Sarkany, R.P., Young, A.R. (2012). UVA1 induces cyclobutane pyrimidine dimers but not 6-4 photoproducts in human skin in vivo. J. Invest. Dermatol. 132: 394-400.

Ullrich, S.E. (2005). Mechanisms underlying UV-induced immune suppression. Mutat. Res. 571: 185-205.

Vaid, M., Sharma, S.D., Katiyar, S.K. (2010). Proanthocyanidins inhibit photocarcinogenesis through enhancement of DNA repair and Xeroderma Pigmentosum group A–dependent mechanism. Cancer Prev. Res. 3: 1621-1619.

Vaisman, A. & Woodgate, R. (2017). Translesion DNA polymerases in eukaryotes: what makes them tick?. Crit. Rev. Biochem. Mol. Biol. 52: 274-303.

Valencia, L., García, A., Ramírez, M.P., Fuentes, J.L. (2011). Estimates of DNA damage by the comet assay in the directdeveloping frog Eleutherodactylus johnstonei (Anura: Eleutherodactylidae). Genet. Mol. Biol. 34: 681-688.

Velasco, M.V.R., Sarruf, F.D., Salgado-Santos, I.M.N., Haroutiounian-Filho, C.A., Kaneko, T.M., Baby, A.R. (2008). Broad spectrum bioactive sunscreens. Int. J. Pharm. 363: 50-57.

Vernhes, M., González-Pumariega, M., Andrade, L., Schuch, A.P., de Lima-Bessa, K.M., Menck, C.F.M., Sánchez Lamar, A. (2013). Protective effect of a Phyllanthus orbicularis, aqueous extract against UVB light in human cells. Pharm. Biol. 51: 1-7.

Vicuña, G.C., Stashenko, E.E., Fuentes, J.L. (2010). Chemical composition of the Lippia origanoides essential oils and their antigenotoxicity against bleomycin-induced DNA damage. Fitoterapia. 81: 343-349.

Vink, A.A. & Roza, L. (2001). Biological consequences of cyclobutane pyrimidine dimers. J. Photochem. Photobiol. B. 65: 101-104.

Wang, S.Q., Xu, H., Stanfield, J.W., Osterwalder, U., Herzog, B. (2017). Comparison of ultraviolet A light protection standards in the Unites States and European Union through in vitro measurements of commercial sunscreens. J. Am. Acad. Dermatol. 77: 42-47.

White, P.A. & Rasmussen, J.B. (1996). SOS Chromotest results in a broader context: Empirical relationships between genotoxic potency, mutagenic potency, and carcinogenic potency. Environ. Mol. Mutagen. 27: 270-305.

White, P.A., Rasmussen, J.B., Blaise, C. (1996). A semiautomated, microplate version of the SOS Chromotest for the analysis of complex environmental extracts. Mutat. Res. 360: 51-74.

Yamaba, H., Haba, M., Kunita, M., Sakaida, T., Tanaka, H., Yashiro, Y., Nakata, S. (2016). Morphological change of skin fibroblasts induced by UV Irradiation is involved in photoaging. Exp. Dermatol. 25 (Suppl 3): 45-51.

Yamaguchi, L.F., Kato, M.J., Di Mascio, P. (2009). Biflavonoids from Araucaria angustifolia protect against DNA UV induced damage. Phytochemistry. 70: 615-620.

Yeeles, J.T.P., Poli, J., Marians, K.J., Pasero, P. (2013). Rescuing Stalled or Damaged Replication Forks. Cold Spring Harb. Perspect. Biol. 5: a012815.

Young, A.R., Chadwick, C.A., Harrison, G.I., Nikaido, O., Ramsden, J., Potteni, C.S. (1998). The similarity of action spectra for thymine dimers in human epidermis and erythema suggests that DNA is the chromophore for erythema. J. Invest. Dermatol. 111: 982-988.

Zaidi, M.R., Day, C.P., Merlino, G. (2008). From UVs to metastases: modeling melanoma initiation and progressin in the mouse. J. Invest. Dermat. 128: 2381-2391.

Zeiger, E. (2007). What is needed for an acceptable antimutagenicity manuscript? Mutat. Res. 626: 1-3.

Zhang, W.J. & Björn, L.O. (2009). The effect of ultraviolet radiation on the accumulation of medicinal compounds in plants. Fitoterapia. 80: 207-218.

Ziegler, A., Jonason, A.S., Leffell, D.J., Simon, J.A., Sharma, H.W., Kimmelman, J., Remington, L., Jacks, T., Brash, D.E. (1994). Sunburn and p53 in the onset of skin cancer. Nature. 372: 773-776.

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