Vol 79, No 3 (2020)
Original article
Published online: 2019-11-12

open access

Page views 1544
Article views/downloads 950
Get Citation

Connect on Social Media

Connect on Social Media

The structural characteristics of photoageing in mice caused by the effects of ultraviolet A radiation

S. Savic1, S. Smiljic2, S. Lestarevic1, A. Ilic3, M. Mijovic4, P. Mandic5, B. Djerkovic4
Pubmed: 31724149
Folia Morphol 2020;79(3):548-556.

Abstract

Background: Due to its deep penetration into the dermis, ultraviolet A (UVA) radiation is considered a primary factor in skin photoageing. The aim of this study is to use a qualitative and quantitative analysis to determine the structural parameters of skin photoageing in mice exposed to UVA radiation, with or without the application of a photoprotective cream. Materials and methods: The experiment consisted of the radiation of female BALBc mice in a solarium by UVA rays, up to total dosages of 7800 J/cm2 and 12500 J/cm2. A total of 78 animals were divided into four experimental and two control groups. All animals were shaved and the animals in two experimental groups were treated with a photoprotective cream half an hour before exposure. The samples of the treated skin were stained with haematoxylin eosin and Van-Gieson staining methods. All measurements, except for the presence of dyskeratosis, were taken using ImageJ 150i software. Results: In the study, the signs of skin photoageing were more evident in untreated groups of animals. Dyskeratosis was more frequent in both of the untreated groups of animals (p = 0.004 and p = 0.003). The lowest values of epidermal thickness (13.8 ± 2.6 μm and 12.7 ± 2.3 μm) were present in both of the untreated groups of animals (p < 0.001 and p < 0.001). The highest values of stratum corneum thickness (34.3 ± 8.5 μm) were observed in the untreated, shorter radiated group of animals (p < 0.001) which was irradiated for the shortest period of time. Beside the control groups, the highest length of dermo-epidermal junction was recorded in the group of treated, longer radiated animals (1467.6 ± 94.6 μm; p = 0.373). The lowest values of dermal thickness (115.9 ± 10.5 μm and 134.8 ± 21.8 μm) and volumetric density of the collagen fibres (31.92 ± 3.19% and 29.40 ± 4.54%) were present in both untreated groups of animals (p < 0.001, p < 0.001, p = 0.035). Conclusions: Skin photoageing was most pronounced in the groups of animals irradiated without the application of photoprotective cream.

Article available in PDF format

View PDF Download PDF file

References

  1. Amano S. Characterization and mechanisms of photoageing-related changes in skin. Damages of basement membrane and dermal structures. Exp Dermatol. 2016; 25 Suppl 3: 14–19.
  2. Amaro-Ortiz A, Yan B, D'Orazio JA. Ultraviolet radiation, aging and the skin: prevention of damage by topical cAMP manipulation. Molecules. 2014; 19(5): 6202–6219.
  3. Battie C, Jitsukawa S, Bernerd F, et al. New insights in photoaging, UVA induced damage and skin types. Exp Dermatol. 2014; 23 Suppl 1: 7–12.
  4. Battie C, Verschoore M. Cutaneous solar ultraviolet exposure and clinical aspects of photodamage. Indian J Dermatol Venereol Leprol. 2012; 78 Suppl 1: S9–SS14.
  5. Beani JC. [Ultraviolet A-induced DNA damage: role in skin cancer]. Bull Acad Natl Med. 2014; 198(2): 273–295.
  6. Bertsch S, Csontos K, Schweizer J, et al. Effect of mechanical stimulation on cell proliferation in mouse epidermis and on growth regulation by endogenous factors (chalones). Cell Tissue Kinet. 1976; 9(5): 445–457.
  7. Bilaç C, Şahin MT, Öztürkcan S. Chronic actinic damage of facial skin. Clin Dermatol. 2014; 32(6): 752–762.
  8. Bosch R, Philips N, Suárez-Pérez JA, et al. Mechanisms of photoaging and cutaneous photocarcinogenesis, and photoprotective strategies with phytochemicals. Antioxidants (Basel). 2015; 4(2): 248–268.
  9. Caberlotto E, Ruiz L, Miller Z, et al. Effects of a skin-massaging device on the ex-vivo expression of human dermis proteins and in-vivo facial wrinkles. PLoS One. 2017; 12(3): e0172624.
  10. Chen CYO, Smith A, Liu Y, et al. Photoprotection by pistachio bioactives in a 3-dimensional human skin equivalent tissue model. Int J Food Sci Nutr. 2017; 68(6): 712–718.
  11. Chen J, Luo J, Tan Y, et al. Effects of low-dose ALA-PDT on fibroblast photoaging induced by UVA irradiation and the underlying mechanisms. Photodiagnosis Photodyn Ther. 2019; 27: 79–84.
  12. Cortat B, Garcia CC, Quinet A, et al. The relative roles of DNA damage induced by UVA irradiation in human cells. Photochem Photobiol Sci. 2013; 12(8): 1483–1495.
  13. Duarte I, Rotter A, Malvestiti A, et al. The role of glass as a barrier against the transmission of ultraviolet radiation: an experimental study. Photodermatol Photoimmunol Photomed. 2009; 25(4): 181–184.
  14. Dupont E, Gomez J, Bilodeau D. Beyond UV radiation: a skin under challenge. Int J Cosmet Sci. 2013; 35(3): 224–232.
  15. Eckhart L, Tschachler E, Gruber F. Autophagic control of skin aging. Front Cell Dev Biol. 2019; 7: 143.
  16. Evans-Johnson JA, Garlick JA, Johnson EJ, et al. A pilot study of the photoprotective effect of almond phytochemicals in a 3D human skin equivalent. J Photochem Photobiol B. 2013; 126: 17–25.
  17. Gomes-Neto A, Aguilera P, Prieto L, et al. Efficacy of a daily protective moisturizer with high UVB and UVA photoprotection in decreasing ultraviolet damage: evaluation by reflectance confocal microscopy. Acta Derm Venereol. 2017; 97(10): 1196–1201.
  18. Gonzaga ER. Role of UV light in photodamage, skin aging, and skin cancer: importance of photoprotection. Am J Clin Dermatol. 2009; 10 Suppl 1: 19–24.
  19. Harberts E, Fishelevich R, Liu J, et al. MyD88 mediates the decision to die by apoptosis or necroptosis after UV irradiation. Innate Immun. 2014; 20(5): 529–539.
  20. Hung CF, Fang CL, Al-Suwayeh SA, et al. Evaluation of drug and sunscreen permeation via skin irradiated with UVA and UVB: comparisons of normal skin and chronologically aged skin. J Dermatol Sci. 2012; 68(3): 135–148.
  21. Kammeyer A, Luiten RM. Oxidation events and skin aging. Ageing Res Rev. 2015; 21: 16–29.
  22. Karran P, Brem R. Protein oxidation, UVA and human DNA repair. DNA Repair. 2016; 44: 178–185.
  23. Khavkin J, Ellis DAF. Aging skin: histology, physiology, and pathology. Facial Plast Surg Clin North Am. 2011; 19(2): 229–234.
  24. Kligman LH, Gebre M, Alper R, et al. Collagen metabolism in ultraviolet irradiated hairless mouse skin and its correlation to histochemical observations. J Invest Dermatol. 1989; 93(2): 210–214.
  25. Kligman L. The hairless mouse model for photoaging. Clin Dermatol. 1996; 14(2): 183–195.
  26. Lagarrigue SG, George J, Questel E, et al. In vivo quantification of epidermis pigmentation and dermis papilla density with reflectance confocal microscopy: variations with age and skin phototype. Exp Dermatol. 2012; 21(4): 281–286.
  27. Lan CCE, Hung YT, Fang AH, et al. Effects of irradiance on UVA-induced skin aging. J Dermatol Sci. 2019; 94(1): 220–228.
  28. Leccia MT, Lebbe C, Claudel JP, et al. New Vision in Photoprotection and Photorepair. Dermatol Ther (Heidelb). 2019; 9(1): 103–115.
  29. Liu Y, Chan F, Sun H, et al. Resveratrol protects human keratinocytes HaCaT cells from UVA-induced oxidative stress damage by downregulating Keap1 expression. Eur J Pharmacol. 2011; 650(1): 130–137.
  30. Longo C, Casari A, Beretti F, et al. Skin aging: in vivo microscopic assessment of epidermal and dermal changes by means of confocal microscopy. J Am Acad Dermatol. 2013; 68(3): e73–e82.
  31. Marionnet C, Pierrard C, Lejeune F, et al. 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.
  32. Mouret S, Leccia MT, Bourrain JL, et al. Individual photosensitivity of human skin and UVA-induced pyrimidine dimers in DNA. J Invest Dermatol. 2011; 131(7): 1539–1546.
  33. Nechifor MT, Niculiţe CM, Urs AO, et al. UVA irradiation of dysplastic keratinocytes: oxidative damage versus antioxidant defense. Int J Mol Sci. 2012; 13(12): 16718–16736.
  34. Ou-Yang H, Stamatas G, Kollias N. Dermal contributions to UVA-induced oxidative stress in skin. Photodermatol Photoimmunol Photomed. 2009; 25(2): 65–70.
  35. Pattison DI, Rahmanto AS, Davies MJ. Photo-oxidation of proteins. Photochem Photobiol Sci. 2012; 11(1): 38–53.
  36. Pittayapruek P, Meephansan J, Prapapan O, et al. Role of matrix metalloproteinases in photoaging and photocarcinogenesis. Int J Mol Sci. 2016; 17(6).
  37. Prasedya ES, Syafitri SM, Geraldine BA, et al. UVA Photoprotective Activity of Brown Macroalgae . Biomedicines. 2019; 7(4): 77.
  38. Quan T, Little E, Quan H, et al. Elevated matrix metalloproteinases and collagen fragmentation in photodamaged human skin: impact of altered extracellular matrix microenvironment on dermal fibroblast function. J Invest Dermatol. 2013; 133(5): 1362–1366.
  39. Rünger TM, Farahvash B, Hatvani Z, et al. Comparison of DNA damage responses following equimutagenic doses of UVA and UVB: a less effective cell cycle arrest with UVA may render UVA-induced pyrimidine dimers more mutagenic than UVB-induced ones. Photochem Photobiol Sci. 2012; 11(1): 207–215.
  40. Schuch AP, Lago JC, Yagura T, et al. DNA dosimetry assessment for sunscreen genotoxic photoprotection. PLoS One. 2012; 7(6): e40344.
  41. Scott TL, Christian PA, Kesler MV, et al. Pigment-independent cAMP-mediated epidermal thickening protects against cutaneous UV injury by keratinocyte proliferation. Exp Dermatol. 2012; 21(10): 771–777.
  42. Wurm EMT, Longo C, Curchin C, et al. In vivo assessment of chronological ageing and photoageing in forearm skin using reflectance confocal microscopy. Br J Dermatol. 2012; 167(2): 270–279.
  43. Xia Q, Chiang HM, Yin JJ, et al. UVA photoirradiation of benzo[a]pyrene metabolites: induction of cytotoxicity, reactive oxygen species, and lipid peroxidation. Toxicol Ind Health. 2015; 31(10): 898–910.