In Vitro Skin Models for the Evaluation of Sunscreen-Based Skin Photoprotection: Molecular Methodologies and Opportunities

Page: [1874 - 1890] Pages: 17

  • * (Excluding Mailing and Handling)

Abstract

Identifying and understanding the biological events that occur following ultraviolet (UV) exposure are mandatory to elucidate the biological and clinical consequences of sun exposure, and to provide efficient and adequate photoprotection strategies. The main UVinduced biological features (markers related to sunburn, cancer, photoaging immunosuppression, pigmentation), characterized in human skin in vivo, could be reproduced in adapted models of reconstructed skin in vitro, attesting their high relevance in the field of photobiology. In turn, 3D skin models were useful to discover precise biological pathways involved in UV response and were predictive of in vivo situation. Although they did not follow a strict validation process for the determination of protection factors, they enabled to evidence important concepts in photoprotection. Indeed, the use of reconstructed skin model highlighted the importance of broad spectrum sunscreen use to protect essential cellular functions, and biologically proved that SPF value was not predictive of the level of protection in the UVA wavelength domain. New biological approaches, such as transcriptomic or proteomic studies as well as quantitative and qualitative determination of DNA damage, will indisputably increase the added value of such systems for sunscreen efficiency evaluation.

Keywords: Photoprotection, sunscreens, reconstructed skin, organotypic skin, ultraviolet, photoaging.

[1]
Rheinwald, J.G.; Green, H. Formation of a keratinizing epithelium in culture by a cloned cell line derived from a teratoma. Cell, 1975, 6(3), 317-330.
[2]
Prunieras, M. Epidermal cell cultures as models for living epidermis. J. Invest. Dermatol., 1979, 73(2), 135-137.
[3]
Asselineau, D.; Bernhard, B.; Bailly, C.; Darmon, M. Epidermal morphogenesis and induction of the 67 kD keratin polypeptide by culture of human keratinocytes at the liquid-air interface. Exp. Cell Res., 1985, 159(2), 536-539.
[4]
MacNeil, S. Progress and opportunities for tissue-engineered skin. Nature, 2007, 445(7130), 874-880.
[5]
Eungdamrong, N.J.; Higgins, C.; Guo, Z.; Lee, W.H.; Gillette, B.; Sia, S.; Christiano, A.M. Challenges and promises in modeling dermatologic disorders with bioengineered skin. Exp. Biol. Med. (Maywood), 2014, 239(9), 1215-1224.
[6]
Duval, C.; Chagnoleau, C.; Pouradier, F.; Sextius, P.; Condom, E.; Bernerd, F. Human skin model containing melanocytes: essential role of keratinocyte growth factor for constitutive pigmentation-functional response to α-melanocyte stimulating hormone and forskolin. Tissue Eng. Part C Methods, 2012, 18(12), 947-957.
[7]
Egles, C.; Garlick, J.A.; Shamis, Y. Three-dimensional human tissue models of wounded skin. Methods Mol. Biol., 2010, 585, 345-359.
[8]
Cotovio, J.; Pellevoisin, C.; Parsad, D. In vitro skin models. Basic Science for Modern Cosmetic Dermatology, 1st ed; Jaypee Brothers Medical Publishers: New Delhi, India, 2014.
[9]
Commission Internationale de l'Éclairage (CIE) Solar spectral irradiance, CIE N° 85th ed.; Vienna, Austria, 1989
[10]
Frederick, J.E.; Lubin, D. Possible long-term changes in biologically active ultraviolet radiation reaching the ground. Photochem. Photobiol., 1988, 47(4), 571-578.
[11]
Frederick, J.E.; Snell, H.E.; Haywood, E.K. Solar ultraviolet radiation at the Earth’s surface. Photochem. Photobiol., 1989, 50(8), 443-450.
[12]
Lubin, D.; Jensen, E.H. Effects of clouds and stratospheric ozone depletion on ultraviolet radiation trends. Nature, 1995, 377, 710-713.
[13]
Christiaens, F.J.; Chardon, A.; Fourtanier, A.; Frederick, J.E. Standard ultraviolet daylight for nonextreme exposure conditions. Photochem. Photobiol., 2005, 81(4), 874-878.
[14]
Marionnet, C.; Tricaud, C.; Bernerd, F. Exposure to non-extreme solar UV daylight: spectral characterization, effects on skin and photoprotection. Int. J. Mol. Sci., 2014, 16(1), 68-90.
[15]
Christiaens, F.; Chardon, A. Ultraviolet radiation for nonextreme exposure conditions: Definition and indoor reproduction. The Sixth Workshop in Davos, Switzerland October 20 - 21, 2005 Newsletter N°8 2006, 11-13. http://metrology. hut. fi/uvnet/source/uvnews8. pdf
[16]
Cadet, J.; Mouret, S.; Ravanat, J.L.; Douki, T. Photoinduced damage to cellular DNA: Direct and photosensitized reactions. Photochem. Photobiol., 2012, 88(5), 1048-1065.
[17]
Melnikova, V.O.; Ananthaswamy, H.N. Cellular and molecular events leading to the development of skin cancer. Mutat. Res., 2005, 571(1-2), 91-106.
[18]
Bruls, W.A.; Slaper, H.; van der Leun, J.C.; Berrens, L. Transmission of human epidermis and stratum corneum as a function of thickness in the ultraviolet and visible wavelengths. Photochem. Photobiol., 1984, 40(4), 485-494.
[19]
Lim, H.W.; Naylor, M.; Hönigsmann, H.; Gilchrest, B.A.; Cooper, K.; Morison, W.; Deleo, V.A.; Scherschun, L. American Academy of Dermatology Consensus Conference on UVA protection of sunscreens: Summary and recommendations. Washington, DC, Feb 4, 2000. J. Am. Acad. Dermatol., 2001, 44(3), 505-508.
[20]
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.
[21]
Tyrrell, R.M.; Keyse, S.M. New trends in photobiology. The interaction of UVA radiation with cultured cells. J. Photochem. Photobiol. B, 1990, 4(4), 349-361.
[22]
Mouret, S.; Bogdanowicz, P.; Haure, M.J.; Castex-Rizzi, N.; Cadet, J.; Favier, A.; Douki, T. Assessment of the photoprotection properties of sunscreens by chromatographic measurement of DNA damage in skin explants. Photochem. Photobiol., 2011, 87(1), 109-116.
[23]
Tewari, A.; Grage, M.M.; Harrison, G.I.; Sarkany, R.; Young, A.R. UVA1 is skin deep: Molecular and clinical implications. Photochem. Photobiol. Sci., 2013, 12(1), 95-103.
[24]
Fisher, G.J.; Datta, S.C.; Talwar, H.S.; Wang, Z.Q.; Varani, J.; Kang, S.; Voorhees, J.J. Molecular basis of sun-induced premature skin ageing and retinoid antagonism. Nature, 1996, 379(6563), 335-339.
[25]
Krutmann, J. The role of UVA rays in skin aging. Eur. J. Dermatol., 2001, 11(2), 170-171.
[26]
Gordon, J.R.; Brieva, J.C. Images in clinical medicine. Unilateral dermatoheliosis. N. Engl. J. Med., 2012, 366(16)e25
[27]
Berneburg, M.; Krutmann, J. Photoimmunology, DNA repair and photocarcinogenesis. J. Photochem. Photobiol. B, 2000, 54(2-3), 87-93.
[28]
Damian, D.L.; Matthews, Y.J.; Phan, T.A.; Halliday, G.M. An action spectrum for ultraviolet radiation-induced immunosuppression in humans. Br. J. Dermatol., 2011, 164(3), 657-659.
[29]
D’Orazio, J.; Jarrett, S.; Amaro-Ortiz, A.; Scott, T. UV radiation and the skin. Int. J. Mol. Sci., 2013, 14(6), 12222-12248.
[30]
Therrien, J.P.; Rouabhia, M.; Drobetsky, E.A.; Drouin, R. The multilayered organization of engineered human skin does not influence the formation of sunlight-induced cyclobutane pyrimidine dimers in cellular DNA. Cancer Res., 1999, 59(2), 285-289.
[31]
Bernerd, F.; Asselineau, D. Successive alteration and recovery of epidermal differentiation and morphogenesis after specific UVB-damages in skin reconstructed in vitro. Dev. Biol., 1997, 183(2), 123-138.
[32]
Flamand, N.; Marrot, L.; Belaidi, J.P.; Bourouf, L.; Dourille, E.; Feltes, M.; Meunier, J.R. Development of genotoxicity test procedures with Episkin, a reconstructed human skin model: Towards new tools for in vitro risk assessment of dermally applied compounds? Mutat. Res., 2006, 606(1-2), 39-51.
[33]
Bernerd, F.; Asselineau, D.; Vioux, C.; Chevallier-Lagente, O.; Bouadjar, B.; Sarasin, A.; Magnaldo, T. Clues to epidermal cancer proneness revealed by reconstruction of DNA repair-deficient xeroderma pigmentosum skin in vitro. Proc. Natl. Acad. Sci. USA, 2001, 98(14), 7817-7822.
[34]
Podda, M.; Traber, M.G.; Weber, C.; Yan, L.J.; Packer, L. UV-irradiation depletes antioxidants and causes oxidative damage in a model of human skin. Free Radic. Biol. Med., 1998, 24(1), 55-65.
[35]
Bissonauth, V.; Drouin, R.; Mitchell, D.L.; Rhainds, M.; Claveau, J.; Rouabhia, M. The efficacy of a broad-spectrum sunscreen to protect engineered human skin from tissue and DNA damage induced by solar ultraviolet exposure. Clin. Cancer Res., 2000, 6(10), 4128-4135.
[36]
Marrot, L.; Planel, E.; Ginestet, A.C.; Belaïdi, J.P.; Jones, C.; Meunier, J.R. In vitro tools for photobiological testing: molecular responses to simulated solar UV of keratinocytes growing as monolayers or as part of reconstructed skin. Photochem. Photobiol. Sci., 2010, 9(4), 448-458.
[37]
Bernerd, F.; Vioux, C.; Lejeune, F.; Asselineau, D. The sun protection factor (SPF) inadequately defines broad spectrum photoprotection: demonstration using skin reconstructed in vitro exposed to UVA, UVBor UV-solar simulated radiation. Eur. J. Dermatol., 2003, 13(3), 242-249.
[38]
Bacqueville, D.; Douki, T.; Duprat, L.; Rebelo-Moreira, S.; Guiraud, B.; Dromigny, H.; Perier, V.; Bessou-Touya, S.; Duplan, H. A new hair follicle-derived human epidermal model for the evaluation of sunscreen genoprotection. J. Photochem. Photobiol. B, 2015, 151, 31-38.
[39]
Douki, T. The variety of UV-induced pyrimidine dimeric photoproducts in DNA as shown by chromatographic quantification methods. Photochem. Photobiol. Sci., 2013, 12(8), 1286-1302.
[40]
Haake, A.R.; Polakowska, R.R. UV-induced apoptosis in skin equivalents: inhibition by phorbol ester and Bcl-2 overexpression. Cell Death Differ., 1995, 2(3), 183-193.
[41]
Vioux-Chagnoleau, C.; Lejeune, F.; Sok, J.; Pierrard, C.; Marionnet, C.; Bernerd, F. Reconstructed human skin: From photodamage to sunscreen photoprotection and anti-aging molecules. J. Dermatol. Science. Suppl., 2006, 2, S1-S12.
[42]
Bernerd, F.; Sarasin, A.; Magnaldo, T. Galectin-7 overexpression is associated with the apoptotic process in UVB-induced sunburn keratinocytes. Proc. Natl. Acad. Sci. USA, 1999, 96(20), 11329-11334.
[43]
Fernandez, T.L.; Van Lonkhuyzen, D.R.; Dawson, R.A.; Kimlin, M.G.; Upton, Z. Characterization of a human skin equivalent model to study the effects of ultraviolet B radiation on keratinocytes. Tissue Eng. Part C Methods, 2014, 20(7), 588-598.
[44]
Archambault, M.; Yaar, M.; Gilchrest, B.A. Keratinocytes and fibroblasts in a human skin equivalent model enhance melanocyte survival and melanin synthesis after ultraviolet irradiation. J. Invest. Dermatol., 1995, 104(5), 859-867.
[45]
Duval, C.; Schmidt, R.; Regnier, M.; Facy, V.; Asselineau, D.; Bernerd, F. The use of reconstructed human skin to evaluate UV-induced modifications and sunscreen efficacy. Exp. Dermatol., 2003, 12(2)(Suppl. 2), 64-70.
[46]
Bernerd, F.; Marionnet, C.; Duval, C. Solar ultraviolet radiation induces biological alterations in human skin in vitro: Relevance of a well-balanced UVA/UVB protection. Indian J. Dermatol. Venereol. Leprol., 2012, (78), S15-S23.
[47]
Tao, S.; Justiniano, R.; Zhang, D.D.; Wondrak, G.T. The Nrf2-inducers tanshinone I and dihydrotanshinone protect human skin cells and reconstructed human skin against solar simulated UV. Redox Biol., 2013, 1, 532-541.
[48]
Lejeune, F.; Christiaens, F.; Bernerd, F. Evaluation of sunscreen products using a reconstructed skin model exposed to simulated daily ultraviolet radiation: relevance of filtration profile and SPF value for daily photoprotection. Photodermatol. Photoimmunol. Photomed., 2008, 24(5), 249-255.
[49]
Marionnet, C.; Pierrard, C.; Lejeune, F.; Sok, J.; Thomas, M.; Bernerd, F. Different oxidative stress response in keratinocytes and fibroblasts of reconstructed skin exposed to non extreme daily-ultraviolet radiation. PLoS One, 2010, 5(8)e12059
[50]
Seite, S.; Zucchi, H.; Septier, D.; Igondjo-Tchen, S.; Senni, K.; Godeau, G. Elastin changes during chronological and photo-ageing: The important role of lysozyme. J. Eur. Acad. Dermatol. Venereol., 2006, 20(8), 980-987.
[51]
Tewari, A.; Sarkany, R.P.; Young, A.R. UVA1 induces cyclobutane pyrimidine dimers but not 6-4 photoproducts in human skin in vivo. J. Invest. Dermatol., 2012, 132(2), 394-400.
[52]
Marionnet, C.; Pierrard, C.; Golebiewski, C.; Bernerd, F. Diversity of biological effects induced by longwave UVA rays (UVA1) in reconstructed skin. PLoS One, 2014, 9(8)e105263
[53]
Dekker, P.; Parish, W.E.; Green, M.R. Protection by food-derived antioxidants from UV-A1-induced photodamage, measured using living skin equivalents. Photochem. Photobiol., 2005, 81(4), 837-842.
[54]
Huang, X.X.; Bernerd, F.; Halliday, G.M. Ultraviolet A within sunlight induces mutations in the epidermal basal layer of engineered human skin. Am. J. Pathol., 2009, 174(4), 1534-1543.
[55]
Coulomb, B.; Lebreton, C.; Mathieu, N.; Morlière, P. UVA-induced oxidative damage in fibroblasts cultured in a 3-dimensional collagen matrix. Exp. Dermatol., 1996, 5(3), 161-167.
[56]
Gruber, F.; Oskolkova, O.; Leitner, A.; Mildner, M.; Mlitz, V.; Lengauer, B.; Kadl, A.; Mrass, P.; Krönke, G.; Binder, B.R.; Bochkov, V.N.; Leitinger, N.; Tschachler, E. Photooxidation generates biologically active phospholipids that induce heme oxygenase-1 in skin cells. J. Biol. Chem., 2007, 282(23), 16934-16941.
[57]
Maresca, V.; Flori, E.; Briganti, S.; Camera, E.; Cario-André, M.; Taïeb, A.; Picardo, M. UVA-induced modification of catalase charge properties in the epidermis is correlated with the skin phototype. J. Invest. Dermatol., 2006, 126(1), 182-190.
[58]
Seité, S.; Popovic, E.; Verdier, M.P.; Roguet, R.; Portes, P.; Cohen, C.; Fourtanier, A.; Galey, J.B. Iron chelation can modulate UVA-induced lipid peroxidation and ferritin expression in human reconstructed epidermis. Photodermatol. Photoimmunol. Photomed., 2004, 20(1), 47-52.
[59]
Meloni, M.; Farina, A.; de Servi, B. Molecular modifications of dermal and epidermal biomarkers following UVA exposures on reconstructed full-thickness human skin. Photochem. Photobiol. Sci., 2010, 9(4), 439-447.
[60]
Marionnet, C.; Lejeune, F.; Pierrard, C.; Vioux-Chagnoleau, C.; Bernerd, F. Biological contribution of UVA wavelengths in non extreme daily UV exposure. J. Dermatol. Sci., 2012, 66(3), 238-240.
[61]
Lavker, R.M.; Veres, D.A.; Irwin, C.J.; Kaidbey, K.H. Quantitative assessment of cumulative damage from repetitive exposures to suberythemogenic doses of UVA in human skin. Photochem. Photobiol., 1995, 62(2), 348-352.
[62]
Lowe, N.J.; Meyers, D.P.; Wieder, J.M.; Luftman, D.; Borget, T.; Lehman, M.D.; Johnson, A.W.; Scott, I.R. Low doses of repetitive ultraviolet A induce morphologic changes in human skin. J. Invest. Dermatol., 1995, 105(6), 739-743.
[63]
Berneburg, M.; Kurten, V.; Grether-Beck, S.; Ruzicka, T.; Klotz, L-O.; Sies, H.; Krutmann, J. Induction of mitochondrial(MT) DNA mutations in human fibroblasts by in vitro ultraviolet A irradiation. J. Invest. Dermatol., 1998, 110(4), 489.
[64]
Moysan, A.; Clément-Lacroix, P.; Michel, L.; Dubertret, L.; Morlière, P. Effects of ultraviolet A and antioxidant defense in cultured fibroblasts and keratinocytes. Photodermatol. Photoimmunol. Photomed., 1996, 11(5-6), 192-197.
[65]
Bernerd, F.; Asselineau, D. UVA exposure of human skin reconstructed in vitro induces apoptosis of dermal fibroblasts: subsequent connective tissue repair and implications in photoaging. Cell Death Differ., 1998, 5(9), 792-802.
[66]
Evans-Johnson, J.A.; Garlick, J.A.; Johnson, E.J.; Wang, X.D.; Oliver Chen, C.Y. A pilot study of the photoprotective effect of almond phytochemicals in a 3D human skin equivalent. J. Photochem. Photobiol. B, 2013, 126, 17-25.
[67]
Marionnet, C.; Grether-Beck, S.; Seité, S.; Marini, A.; Jaenicke, T.; Lejeune, F.; Bastien, P.; Rougier, A.; Bernerd, F.; Krutmann, J. A broad-spectrum sunscreen prevents UVA radiation-induced gene expression in reconstructed skin in vitro and in human skin in vivo. Exp. Dermatol., 2011, 20(6), 477-482.
[68]
Imparato, G.; Casale, C.; Scamardella, S.; Urciuolo, F.; Bimonte, M.; Apone, F.; Colucci, G.; Netti, P.A. A novel engineered dermis for in vitro photodamage research. J. Tissue Eng. Regen. Med., 2017, 11(8), 2276-2285.
[69]
Quan, T.; Qin, Z.; Xia, W.; Shao, Y.; Voorhees, J.J.; Fisher, G.J. Matrix-degrading metalloproteinases in photoaging. J. Investig. Dermatol. Symp. Proc., 2009, 14(1), 20-24.
[70]
Fisher, G.J.; Datta, S.; Wang, Z.; Li, X.Y.; Quan, T.; Chung, J.H.; Kang, S.; Voorhees, J.J. c-Jun-dependent inhibition of cutaneous procollagen transcription following ultraviolet irradiation is reversed by all-trans retinoic acid. J. Clin. Invest., 2000, 106(5), 663-670.
[71]
Chen, V.L.; Fleischmajer, R.; Schwartz, E.; Palaia, M.; Timpl, R. Immunochemistry of elastotic material in sun-damaged skin. J. Invest. Dermatol., 1986, 87(3), 334-337.
[72]
Fagot, D.; Asselineau, D.; Bernerd, F. Direct role of human dermal fibroblasts and indirect participation of epidermal keratinocytes in MMP-1 production after UV-B irradiation. Arch. Dermatol. Res., 2002, 293(11), 576-583.
[73]
Fagot, D.; Asselineau, D.; Bernerd, F. Matrix metalloproteinase-1 production observed after solar-simulated radiation exposure is assumed by dermal fibroblasts but involves a paracrine activation through epidermal keratinocytes. Photochem. Photobiol., 2004, 79(6), 499-505.
[74]
Topol, B.M.; Haimes, H.B.; Dubertret, L.; Bell, E. Transfer of melanosomes in a skin equivalent model in vitro. J. Invest. Dermatol., 1986, 87(5), 642-647.
[75]
Todd, C.; Hewitt, S.D.; Kempenaar, J.; Noz, K.; Thody, A.J.; Ponec, M. Co-culture of human melanocytes and keratinocytes in a skin equivalent model: Effect of ultraviolet radiation. Arch. Dermatol. Res., 1993, 285(8), 455-459.
[76]
Gibbs, S.; Murli, S.; De Boer, G.; Mulder, A.; Mommaas, A.M.; Ponec, M. Melanosome capping of keratinocytes in pigmented reconstructed epidermis--effect of ultraviolet radiation and 3-isobutyl-1-methyl-xanthine on melanogenesis. Pigment Cell Res., 2000, 13(6), 458-466.
[77]
Bessou, S.; Surlève-Bazeille, J.E.; Sorbier, E.; Taïeb, A. Ex vivo reconstruction of the epidermis with melanocytes and the influence of UVB. Pigment Cell Res., 1995, 8(5), 241-249.
[78]
Bessou, S.; Surlève-Bazeille, J.E.; Pain, C.; Donatien, P.; Taïeb, A. Ex vivo study of skin phototypes. J. Invest. Dermatol., 1996, 107(5), 684-688.
[79]
Nakazawa, K.; Nakazawa, H.; Sahuc, F.; Lepavec, A.; Collombel, C.; Damour, O. Pigmented human skin equivalent: New method of reconstitution by grafting an epithelial sheet onto a non-contractile dermal equivalent. Pigment Cell Res., 1997, 10(6), 382-390.
[80]
Duval, C.; Régnier, M.; Schmidt, R. Distinct melanogenic response of human melanocytes in mono-culture, in co-culture with keratinocytes and in reconstructed epidermis, to UV exposure. Pigment Cell Res., 2001, 14(5), 348-355.
[81]
Pathak, M.A.; Fanselow, D.L. Photobiology of melanin pigmentation: Dose/response of skin to sunlight and its contents. J. Am. Acad. Dermatol., 1983, 9(5), 724-733.
[82]
Bechetoille, N.; Dezutter-Dambuyant, C.; Damour, O.; André, V.; Orly, I.; Perrier, E. Effects of solar ultraviolet radiation on engineered human skin equivalent containing both Langerhans cells and dermal dendritic cells. Tissue Eng., 2007, 13(11), 2667-2679.
[83]
Mahns, A.; Wolber, R.; Stäb, F.; Klotz, L.O.; Sies, H. Contribution of UVB and UVA to UV-dependent stimulation of cyclooxygenase-2 expression in artificial epidermis. Photochem. Photobiol. Sci., 2004, 3(3), 257-262.
[84]
Cooper, K.D.; Oberhelman, L.; Hamilton, T.A.; Baadsgaard, O.; Terhune, M.; LeVee, G.; Anderson, T.; Koren, H. UV exposure reduces immunization rates and promotes tolerance to epicutaneous antigens in humans: relationship to dose, CD1a-DR+ epidermal macrophage induction, and Langerhans cell depletion. Proc. Natl. Acad. Sci. USA, 1992, 89(18), 8497-8501.
[85]
Seité, S.; Zucchi, H.; Moyal, D.; Tison, S.; Compan, D.; Christiaens, F.; Gueniche, A.; Fourtanier, A. Alterations in human epidermal Langerhans cells by ultraviolet radiation: Quantitative and morphological study. Br. J. Dermatol., 2003, 148(2), 291-299.
[86]
Sesto, A.; Navarro, M.; Burslem, F.; Jorcano, J.L. Analysis of the ultraviolet B response in primary human keratinocytes using oligonucleotide microarrays. Proc. Natl. Acad. Sci. USA, 2002, 99(5), 2965-2970.
[87]
Enk, C.D.; Jacob-Hirsch, J.; Gal, H.; Verbovetski, I.; Amariglio, N.; Mevorach, D.; Ingber, A.; Givol, D.; Rechavi, G.; Hochberg, M. The UVB-induced gene expression profile of human epidermis in vivo is different from that of cultured keratinocytes. Oncogene, 2006, 25(18), 2601-2614.
[88]
Bart, G.; Hämäläinen, L.; Rauhala, L.; Salonen, P.; Kokkonen, M.; Dunlop, T.W.; Pehkonen, P.; Kumlin, T.; Tammi, M.I.; Pasonen-Seppänen, S.; Tammi, R.H. rClca2 is associated with epidermal differentiation and is strongly downregulated by ultraviolet radiation. Br. J. Dermatol., 2014, 171(2), 376-387.
[89]
Marionnet, C.; Pierrard, C.; Lejeune, F.; Bernerd, F. Modulations of gene expression induced by daily ultraviolet light can be prevented by a broad spectrum sunscreen. J. Photochem. Photobiol. B, 2012, 116, 37-47.
[90]
Seité, S.; Medaisko, C.; Christiaens, F.; Bredoux, C.; Compan, D.; Zucchi, H.; Lombard, D.; Fourtanier, A. Biological effects of simulated ultraviolet daylight: a new approach to investigate daily photoprotection. Photodermatol. Photoimmunol. Photomed., 2006, 22(2), 67-77.
[91]
Hensbergen, P.; Alewijnse, A.; Kempenaar, J.; van der Schors, R.C.; Balog, C.A.; Deelder, A.; Beumer, G.; Ponec, M.; Tensen, C.P. Proteomic profiling identifies an UV-induced activation of cofilin-1 and destrin in human epidermis. J. Invest. Dermatol., 2005, 124(4), 818-824.
[92]
Osterwalder, U.; Hareng, L. Global UV Filters: Current Technologies and Future Innovations. In: Principles and Practice of Photoprotection; Steven Q, Wang; Henry W., Lim, Eds.; SpringerLink: Switzerland, 2016; pp. 179-197.
[93]
Moyal, D. Need for a well-balanced sunscreen to protect human skin from both ultraviolet A and ultraviolet B damage. Indian J. Dermatol. Venereol. Leprol., 2012, 78(Suppl. 1), S24-S30.
[94]
Cosmetic Toiletry & Fragrance Association of South Africa (CTFA-SA); The European Cosmetic and Toiletry Association (Colipa); Japan Cosmetic Industry Association (JCIA). International Sun Protection factor (SPF) test method, 2006.
[95]
Matts, P.J.; Alard, V.; Brown, M.W.; Ferrero, L.; Gers-Barlag, H.; Issachar, N.; Moyal, D.; Wolber, R. The COLIPA in vitro UVA method: A standard and reproducible measure of sunscreen UVA protection. Int. J. Cosmet. Sci., 2010, 32(1), 35-46.
[96]
Diffey, B.L.; Tanner, P.R.; Matts, P.J.; Nash, J.F. In vitro assessment of the broad-spectrum ultraviolet protection of sunscreen products. J. Am. Acad. Dermatol., 2000, 43(6), 1024-1035.
[97]
Moyal, D.; Chardon, A.; Kollias, N. UVA protection efficacy of sunscreens can be determined by the persistent pigment darkening (PPD) method. (Part 2). Photodermatol. Photoimmunol. Photomed., 2000, 16(6), 250-255.
[98]
EC, Commission Recommendation of 22 September. 2006 on the efficacy of sunscreen products and the claims made relating thereto. Text with EEA relevance. J. Eur. Union, 2006, L265, 39-43.
[99]
Nelson, D.; Gay, R.J. Effects of UV irradiation on a living skin equivalent. Photochem. Photobiol., 1993, 57(5), 830-837.
[100]
Cole, C.; VanFossen, R. Measurement of sunscreen UVA protection: An unsensitized human model. J. Am. Acad. Dermatol., 1992, 26(2 Pt 1), 178-184.
[101]
Augustin, C.; Collombel, C.; Damour, O. Measurements of the protective effect of topically applied sunscreens using in vitro three-dimensional dermal and skin equivalents. Photochem. Photobiol., 1997, 66(6), 853-859.
[102]
Bernerd, F.; Vioux, C.; Asselineau, D. Evaluation of the protective effect of sunscreens on in vitro reconstructed human skin exposed to UVB or UVA irradiation. Photochem. Photobiol., 2000, 71(3), 314-320.
[103]
Cario-André, M.; Briganti, S.; Picardo, M.; Nikaido, O.; Gall, Y.; Ginestar, J.; Taïeb, A. Epidermal reconstructs: A new tool to study topical and systemic photoprotective molecules. J. Photochem. Photobiol. B, 2002, 68(2-3), 79-87.
[104]
Rouabhia, M.; Mitchell, D.L.; Rhainds, M.; Claveau, J.; Drouin, R. A physical sunscreen protects engineered human skin against artificial solar ultraviolet radiation-induced tissue and DNA damage. Photochem. Photobiol. Sci., 2002, 1(7), 471-477.
[105]
Schuch, A.P.; Lago, J.C.; Yagura, T.; Menck, C.F. DNA dosimetry assessment for sunscreen genotoxic photoprotection. PLoS One, 2012, 7(6)e40344
[106]
Gelis, C.; Mavon, A.; Vicendo, P. Evaluation of biological effects of ultraviolet radiations and of photoprotection on human reconstructed epidermis. Nouvelles Dermatol, 2003, 22(61), 351.
[107]
Bacqueville, D.; Mavon, A. Comparative analysis of solar radiation-induced cellular damage between ex vivo porcine skin organ culture and in vitro reconstructed human epidermis. Int. J. Cosmet. Sci., 2009, 31(4), 293-302.
[108]
Bernerd, F.; Asselineau, D. Reconstructed human skin: Effect of solar UV light and use to evaluate efficiency of sunscreens in vitro. Cosmet. Dermatol, 2001, 14, 15-19.
[109]
Séite, S.; Moyal, D.; Richard, S.; de Rigal, J.; Lévêque, J.L.; Hourseau, C.; Fourtanier, A. Mexoryl SX: a broad absorption UVA filter protects human skin from the effects of repeated suberythemal doses of UVA. J. Photochem. Photobiol. B, 1998, 44(1), 69-76.
[110]
Seité, S.; Moyal, D.; Verdier, M.P.; Hourseau, C.; Fourtanier, A. Accumulated p53 protein and UVA protection level of sunscreens. Photodermatol. Photoimmunol. Photomed., 2000, 16(1), 3-9.
[111]
Facy, V.; Flouret, V.; Régnier, M.; Schmidt, R. Reactivity of Langerhans cells in human reconstructed epidermis to known allergens and UV radiation. Toxicol. In Vitro, 2005, 19(6), 787-795.