Abstract
Skin is a rather complex, yet useful organ of our body. Besides, skin aging is a complicated process that gains a growing interest as mediates many molecular processes in our body. Thus, an efficient skin model is important to understand skin aging function as well as to develop an effective innovative product for skin aging treatment. In this mini review, we present in vitro methods for assessments of skin aging in an attempt to pinpoint basic molecular mechanisms behind this process achieving both a better understanding of aging function and an effective evaluation of potential products or ingredients that counteract aging. Specifically, this study presents in vitro assays such as 2D or 3D skin models, to evaluate skin aging-related processes such as skin moisturization, photoaging, wound healing, menopause, and skin microbiome as novel efforts in the designing of efficacy assessments in the development of skincare products.
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References
Affinito P, Palomba S, Sorrentino C et al (1999) Effects of postmenopausal hypoestrogenism on skin collagen. Maturitas. https://doi.org/10.1016/S0378-5122(99)00077-8
Albrecht S, Elpelt A, Kasim C et al (2019) Quantification and characterization of radical production in human, animal and 3D skin models during sun irradiation measured by EPR spectroscopy. Free Radic Biol Med. https://doi.org/10.1016/j.freeradbiomed.2018.12.022
Ashrafi M, Hague A, Baguneid M et al (2018) Wound healing and cutaneous scarring models of the human skin. Skin tissue models. Elsevier, Amsterdam
Barbotteau Y, Gontier E, Barberet P et al (2005) Reconstructed human epidermis: a model to study the barrier function. Nucl Instrum Methods Phys Res B. https://doi.org/10.1016/j.nimb.2005.01.072
Bataillon M, Lelièvre D, Chapuis A et al (2019) Characterization of a new reconstructed full thickness skin model, t-skinTM, and its application for investigations of anti-aging compounds. Int J Mol Sci. https://doi.org/10.3390/ijms20092240
Beaven EP, Cox AJ (1965) Organ culture of human skin. J Invest Dermatol 44:151–156
Bellemare J, Roberge CJ, Bergeron D et al (2005) Epidermis promotes dermal fibrosis: role in the pathogenesis of hypertrophic scars. J Pathol. https://doi.org/10.1002/path.1737
Biglari S, Le TYL, Tan RP et al (2019) Simulating inflammation in a wound microenvironment using a dermal wound-on-a-chip model. Adv Healthc Mater. https://doi.org/10.1002/adhm.201801307
Bilal M, Mehmood S, Iqbal HMN (2020) The beast of beauty: environmental and health concerns of toxic components in cosmetics. Cosmetics 7:13. https://doi.org/10.3390/cosmetics7010013
Björklund S, Nowacka A, Bouwstra JA et al (2013) Characterization of stratum corneum molecular dynamics by natural-abundance 13C solid-state NMR. PLoS ONE 8:e61889. https://doi.org/10.1371/journal.pone.0061889
Bogdanowicz P, Haure M-J, Ceruti I et al (2016) Results from in vitro and ex vivo skin aging models assessing the antiglycation and anti-elastase MMP-12 potential of glycylglycine oleamide. Clin Cosmet Investig Dermatol. https://doi.org/10.2147/CCID.S98633
Boncheva M, Damien F, Normand V (2008) Molecular organization of the lipid matrix in intact Stratum corneum using ATR-FTIR spectroscopy. Biochim Biophys Acta - Biomembr 1778:1344–1355. https://doi.org/10.1016/j.bbamem.2008.01.022
Botham PA, Earl LK, Fentem JH et al (1998) Alternative methods for skin irritation testing: the current status. Altern Lab Anim 26:195–211. https://doi.org/10.1177/026119299802600205
Buisson AC, Zahm JM, Polette M et al (1996) Gelatinase B is involved in the in vitro wound repair of human respiratory epithelium. J Cell Physiol. https://doi.org/10.1002/(SICI)1097-4652(199602)166:2%3c413::AID-JCP20%3e3.0.CO;2-A
Butler PD, Ly DP, Longaker MT, Yang GP (2008) Use of organotypic coculture to study keloid biology. Am J Surg. https://doi.org/10.1016/j.amjsurg.2007.10.003
Byrd AL, Belkaid Y, Segre JA (2018) The human skin microbiome. Nat Rev Microbiol 16:143–155. https://doi.org/10.1038/nrmicro.2017.157
Calderon M, Lawrence WT, Banes AJ (1996) Increased proliferation in keloid fibroblasts wounded in vitro. J Surg Res. https://doi.org/10.1006/jsre.1996.0127
Capallere C, Plaza C, Meyrignac C et al (2018) Property characterization of reconstructed human epidermis equivalents, and performance as a skin irritation model. Toxicol In Vitro. https://doi.org/10.1016/j.tiv.2018.07.005
Cha D, O’Brien P, O’Toole EA et al (1996) Enhanced modulation of keratinocyte motility by transforming growth factor-α (TGF-α) relative to epidermal growth factor (EGF). J Invest Dermatol. https://doi.org/10.1111/1523-1747.ep12345083
Chaudhuri RK, Bojanowski K (2017) Improvement of hydration and epidermal barrier function in human skin by a novel compound isosorbide dicaprylate. Int J Cosmet Sci. https://doi.org/10.1111/ics.12405
Chen L, Li N, Liu Y et al (2020) A new 3D model for genotoxicity assessment: EpiSkinTM micronucleus assay. Mutagenesis. https://doi.org/10.1093/mutage/geaa003
Chiu LL, Sun CH, Yeh AT et al (2005) Photodynamic therapy on keloid fibroblasts in tissue-engineered keratinocyte-fibroblast co-culture. Lasers Surg Med. https://doi.org/10.1002/lsm.20213
Cho H, Won CH, Chang SE et al (2013) Usefulness and limitations of skin explants to assess laser treatment. Med Lasers 2:58–63. https://doi.org/10.25289/ML.2013.2.2.58
Choi E, Kang YG, Hwang SH et al (2019) In vitro effects of dehydrotrametenolic acid on skin barrier function. Molecules. https://doi.org/10.3390/molecules24244583
Cotovio J, Onno L, Justine P et al (2001) Generation of oxidative stress in human cutaneous models following in vitro ozone exposure. Toxicol In Vitro 15:357–362. https://doi.org/10.1016/S0887-2333(01)00036-4
Davies DJ, Heylings JR, McCarthy TJ, Correa CM (2015) Development of an in vitro model for studying the penetration of chemicals through compromised skin. Toxicol In Vitro. https://doi.org/10.1016/j.tiv.2014.09.012
Davies DJ, Heylings JR, Gayes H et al (2017) Further development of an in vitro model for studying the penetration of chemicals through compromised skin. Toxicol In Vitro. https://doi.org/10.1016/j.tiv.2016.10.004
Damiani E, Brugè F, Cirilli I et al (2018) Modulation of oxidative status by normoxia and hypoxia on cultures of human dermal fibroblasts: how does it affect cell aging? Oxid Med Cell Longev. https://doi.org/10.1155/2018/5469159
Del Carmen Velazquez Pereda M, de Campos Dieamant G, Eberlin S et al (2009) Effect of green Coffea arabica L. seed oil on extracellular matrix components and water-channel expression in in vitro and ex vivo human skin models. J Cosmet Dermatol 8:56–62. https://doi.org/10.1111/j.1473-2165.2009.00425.x
Demirovic D, Rattan SIS (2011) Curcumin induces stress response and hormetically modulates wound healing ability of human skin fibroblasts undergoing ageing in vitro. Biogerontology 12:437–444. https://doi.org/10.1007/s10522-011-9326-7
Diekmann J, Alili L, Scholz O et al (2016) A three-dimensional skin equivalent reflecting some aspects of in vivo aged skin. Exp Dermatol. https://doi.org/10.1111/exd.12866
Driskell RR, Lichtenberger BM, Hoste E et al (2013) Distinct fibroblast lineages determine dermal architecture in skin development and repair. Nature 504:277–281. https://doi.org/10.1038/nature12783
Duan W, Qiao S, Zhuo M et al (2020) Multifunctional platforms: metal-organic frameworks for cutaneous and cosmetic treatment. Chem. https://doi.org/10.1016/j.chempr.2020.11.018
Duval C, Schmidt R, Regnier M et al (2003) The use of reconstructed human skin to evaluate UV-induced modifications and sunscreen efficacy. Exp Dermatol. https://doi.org/10.1034/j.1600-0625.12.s2.10.x
Duval C, Cohen C, Chagnoleau C et al (2014) Key regulatory role of dermal fibroblasts in pigmentation as demonstrated using a reconstructed skin model: impact of photo-aging. PLoS ONE 9:e114182. https://doi.org/10.1371/journal.pone.0114182
Eckhart L, Zeeuwen PLJM (2018) The skin barrier: epidermis vs environment. Exp Dermatol 27:805–806. https://doi.org/10.1111/exd.13731
Elias PM (2007) The skin barrier as an innate immune element. Semin Immunopathol. https://doi.org/10.1007/s00281-007-0060-9
Farage MA, Miller KW, Elsner P, Maibach HI (2008) Intrinsic and extrinsic factors in skin ageing: a review. Int J Cosmet Sci 30:87–95. https://doi.org/10.1111/j.1468-2494.2007.00415.x
Flanagan M (2013) Wound healing and skin integrity. Wiley, Hoboken
Ghadially R, Reed JT, Elias PM (1996) Stratum corneum structure and function correlates with phenotype in psoriasis. J Invest Dermatol. https://doi.org/10.1111/1523-1747.ep12582813
Ghaffari A, Kilani RT, Ghahary A (2009) Keratinocyte-conditioned media regulate collagen expression in dermal fibroblasts. J Invest Dermatol. https://doi.org/10.1038/jid.2008.253
Gottrup F, Ågren MS, Karlsmark T (2000) Models for use in wound healing research: a survey focusing on in vitro and in vivo adult soft tissue. Wound Repair Regen 8:83–96
Green H, Kehinde O, Thomas J (1979) Growth of cultured human epidermal cells into multiple epithelia suitable for grafting. Proc Natl Acad Sci USA. https://doi.org/10.1073/pnas.76.11.5665
Grice E (2014) The skin microbiome: potential for novel diagnostic and therapeutic approaches to cutaneous disease. Semin Cutan Med Surg 33:98–103. https://doi.org/10.12788/j.sder.0087
Grice EA, Segre JA (2011) The skin microbiome. Nat Rev Microbiol 9:244–253. https://doi.org/10.1038/nrmicro2537
Gruber F, Kremslehner C, Eckhart L, Tschachler E (2020) Cell aging and cellular senescence in skin aging—Recent advances in fibroblast and keratinocyte biology. Exp Gerontol 130:110780. https://doi.org/10.1016/j.exger.2019.110780
Gu Y, Han J, Jiang C, Zhang Y (2020) Biomarkers, oxidative stress and autophagy in skin aging. Ageing Res Rev 59:101036. https://doi.org/10.1016/j.arr.2020.101036
Haensel D, Dai X (2018) Epithelial-to-mesenchymal transition in cutaneous wound healing: where we are and where we are heading. Dev Dyn. https://doi.org/10.1002/dvdy.24561
Henemyre-Harris CL, Adkins AL, Chuang AH, Graham JS (2008) Addition of epidermal growth factor improves the rate of sulfur mustard wound healing in an in vitro model. Eplasty 8:e16
Horii I, Nakayama Y, Obata M, Tagami H (1989) Stratum corneum hydration and amino acid content in xerotic skin. Br J Dermatol. https://doi.org/10.1111/j.1365-2133.1989.tb08190.x
Iyer K, Chen Z, Ganapa T et al (2018) Keratinocyte migration in a three-dimensional in vitro wound healing model co-cultured with fibroblasts. Tissue Eng Regen Med. https://doi.org/10.1007/s13770-018-0145-7
Jenkins G (2002) Molecular mechanisms of skin ageing. Mech Ageing Dev 123:801–810. https://doi.org/10.1016/S0047-6374(01)00425-0
Juliano C, Magrini G (2017) Cosmetic ingredients as emerging pollutants of environmental and health concern. A mini-review. Cosmetics 4:11. https://doi.org/10.3390/cosmetics4020011
Kammeyer A, Luiten RM (2015) Oxidation events and skin aging. Ageing Res Rev 21:16–29. https://doi.org/10.1016/j.arr.2015.01.001
Karapetsas A, Voulgaridou G-P, Konialis M et al (2019) Propolis extracts inhibit UV-induced photodamage in human experimental in vitro skin models. Antioxidants 8:125. https://doi.org/10.3390/antiox8050125
Kim WS, Lee JS, Bae GY et al (2013) Extract of Aneilema keisak inhibits transforming growth factor-β-dependent signalling by inducing Smad2 downregulation in keloid fibroblasts. Exp Dermatol. https://doi.org/10.1111/exd.12063
Kim HS, Sun X, Lee JH et al (2019) Advanced drug delivery systems and artificial skin grafts for skin wound healing. Adv Drug Deliv Rev. https://doi.org/10.1016/j.addr.2018.12.014
Knazek RA, Gullino PM, Kohler PO, Dedrick RL (1972) Cell culture on artificial capillaries: an approach to tissue growth in vitro. Science. https://doi.org/10.1126/science.178.4056.65
Kong HH, Oh J, Deming C et al (2012) Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis. Genome Res 22:850–859. https://doi.org/10.1101/gr.131029.111
Kostyuk V, Potapovich A, Albuhaydar AR et al (2018) Natural substances for prevention of skin photoaging: screening systems in the development of sunscreen and rejuvenation cosmetics. Rejuvenation Res. https://doi.org/10.1089/rej.2017.1931
Kovacs D, Cardinali G, Aspite N et al (2010) Role of fibroblast-derived growth factors in regulating hyperpigmentation of solar lentigo. Br J Dermatol. https://doi.org/10.1111/j.1365-2133.2010.09946.x
Lago JC, Puzzi MB (2019) The effect of aging in primary human dermal fibroblasts. PLoS ONE 14:e0219165. https://doi.org/10.1371/journal.pone.0219165
Lai-Cheong JE, McGrath JA (2017) Structure and function of skin, hair and nails. Medicine (Baltimore) 45:347–351. https://doi.org/10.1016/j.mpmed.2017.03.004
Lebonvallet N, Jeanmaire C, Danoux L et al (2010) The evolution and use of skin explants: potential and limitations for dermatological research. Eur J Dermatol 20:671–684. https://doi.org/10.1684/ejd.2010.1054
Lee CM, Watson REB, Kleyn CE (2020a) The impact of perceived stress on skin ageing. J Eur Acad Dermatol Venereol 34:54–58. https://doi.org/10.1111/jdv.15865
Lee JY, Lee J, Min D et al (2020b) Tyrosinase-targeting gallacetophenone inhibits melanogenesis in melanocytes and human skin-equivalents. Int J Mol Sci. https://doi.org/10.3390/ijms21093144
Letsiou S, Bakea A, Le GG et al (2020a) Marine fungus Aspergillus chevalieri TM2-S6 extract protects skin fibroblasts from oxidative stress. Mar Drugs 18:460. https://doi.org/10.3390/md18090460
Letsiou S, Bakea A, Holefors A, Rembiesa J (2020b) In vitro protective effects of Paeonia mascula subsp. hellenica callus extract on human keratinocytes. Sci Rep 10:19213. https://doi.org/10.1038/s41598-020-76169-0
Letsiou S, Bakea A, Le Goff G et al (2020c) In vitro protective effects of marine-derived Aspergillus puulaauensis TM124-S4 extract on H2O2-stressed primary human fibroblasts. Toxicol In Vitro 66:104869. https://doi.org/10.1016/j.tiv.2020.104869
Letsiou S, Félix RC, Cardoso JCR et al (2020d) Cartilage acidic protein 1 promotes increased cell viability, cell proliferation and energy metabolism in primary human dermal fibroblasts. Biochimie 171–172:72–78. https://doi.org/10.1016/j.biochi.2020.02.008
Letsiou S, Kapazoglou A, Tsaftaris A (2020e) Transcriptional and epigenetic effects of Vitis vinifera L. leaf extract on UV-stressed human dermal fibroblasts. Mol Biol Rep 47:5763–5772. https://doi.org/10.1007/s11033-020-05645-7
Letsiou S, Kalliampakou K, Gardikis K et al (2017) Skin protective effects of nannochloropsis gaditana extract on H2O2-stressed human dermal fibroblasts. Front Mar Sci. https://doi.org/10.3389/fmars.2017.00221
Li Z, Bai X, Peng T et al (2020) New insights into the skin microbial communities and skin aging. Front Microbiol. https://doi.org/10.3389/fmicb.2020.565549
Liebsch M, Döring B, Donelly TA et al (1995) Application of the human dermal model skin2 ZK 1350 to phototoxicity and skin corrosivity testing. Toxicol In Vitro. https://doi.org/10.1016/0887-2333(95)00042-7
Líšková A (2020) Evaluation of phototoxic and cytotoxic potential of TiO2 nanosheets in a 3D reconstructed human skin model. Altex. https://doi.org/10.14573/altex.1910012
López-Otín C, Blasco MA, Partridge L et al (2013) The hallmarks of aging. Cell 153:1194–1217. https://doi.org/10.1016/j.cell.2013.05.039
Löwenau LJ, Zoschke C, Brodwolf R et al (2017) Increased permeability of reconstructed human epidermis from UVB-irradiated keratinocytes. Eur J Pharm Biopharm 116:149–154. https://doi.org/10.1016/j.ejpb.2016.12.017
Maeno K (2019) Direct quantification of natural moisturizing factors in stratum corneum using direct analysis in real time mass spectrometry with inkjet-printing technique. Sci Rep. https://doi.org/10.1038/s41598-019-54454-x
Mainzer C, Remoué N, Molinari J et al (2018) In vitro epidermis model mimicking IGF-1–specific age-related decline. Exp Dermatol. https://doi.org/10.1111/exd.13547
Martin P (1997) Wound healing—aiming for perfect skin regeneration. Science. https://doi.org/10.1126/science.276.5309.75
Mojumdar EH, Pham QD, Topgaard D, Sparr E (2017) Skin hydration: interplay between molecular dynamics, structure and water uptake in the stratum corneum. Sci Rep 7:15712. https://doi.org/10.1038/s41598-017-15921-5
Murai M, Tsuji G, Hashimoto-Hachiya A et al (2018) An endogenous tryptophan photo-product, FICZ, is potentially involved in photo-aging by reducing TGF-β-regulated collagen homeostasis. J Dermatol Sci 89:19–26. https://doi.org/10.1016/j.jdermsci.2017.10.002
Nakamura M, Haarmann-Stemmann T, Krutmann J, Morita A (2018) Alternative test models for skin ageing research. Exp Dermatol. https://doi.org/10.1111/exd.13519
Nayak S, Dey S, Kundu SC (2013) Skin equivalent tissue-engineered construct: co-cultured fibroblasts/keratinocytes on 3D matrices of sericin hope cocoons. PLoS ONE. https://doi.org/10.1371/journal.pone.0074779
Neil JE, Brown MB, Williams AC (2020) Human skin explant model for the investigation of topical therapeutics. Sci Rep 10:21192. https://doi.org/10.1038/s41598-020-78292-4
Netzlaff F, Lehr C-M, Wertz PW, Schaefer UF (2005) The human epidermis models EpiSkin®, SkinEthic® and EpiDerm®: an evaluation of morphology and their suitability for testing phototoxicity, irritancy, corrosivity, and substance transport. Eur J Pharm Biopharm 60:167–178. https://doi.org/10.1016/j.ejpb.2005.03.004
Newton VL, Mcconnell JC, Hibbert SA et al (2015) Skin aging: molecular pathology, dermal remodelling and the imaging revolution. G Ital Dermatol Venereol 150:665–674
Olesen CM, Fuchs CSK, Philipsen PA et al (2019) Advancement through epidermis using tape stripping technique and reflectance confocal microscopy. Sci Rep 9:12217. https://doi.org/10.1038/s41598-019-48698-w
Pageon H, Zucchi H, Rousset F et al (2017) Glycation stimulates cutaneous monocyte differentiation in reconstructed skin in vitro. Mech Ageing Dev. https://doi.org/10.1016/j.mad.2017.02.001
Paige DG, Morse-Fisher N, Harper JI (1994) Quantification of stratum corneum ceramides and lipid envelope ceramides in the hereditary ichthyoses. Br J Dermatol. https://doi.org/10.1111/j.1365-2133.1994.tb08452.x
Park G-H, Chang SE, Bang S et al (2015) Usefulness of skin explants for histologic analysis after fractional photothermolysis. Ann Dermatol 27:283. https://doi.org/10.5021/ad.2015.27.3.283
Park DJ, Jeon G, Bang SH et al (2020) Cellular lysosomes’ activity for melanin reduction on artificial skin tissue. Mol Biotechnol. https://doi.org/10.1007/s12033-019-00235-w
Pastar I, Liang L, Sawaya AP et al (2017) Preclinical models for wound-healing studies. Skin tissue models. Elsevier, Amsterdam
Peter Jorgensen SRI (2014) Extracellular matrix modulates morphology, growth, oxidative stress response and functionality of human skin fibroblasts during aging in vitro. J Aging Sci. https://doi.org/10.4172/2329-8847.1000122
Pfuhler S, Pirow R, Downs TR et al (2020) Validation of the 3D reconstructed human skin comet assay, an animal-free alternative for following-up positive results from standard in vitro genotoxicity assays. Mutagenesis. https://doi.org/10.1093/mutage/geaa009
Pittayapruek P, Meephansan J, Prapapan O et al (2016) Role of matrix metalloproteinases in photoaging and photocarcinogenesis. Int J Mol Sci. https://doi.org/10.3390/ijms17060868
Poumay Y, Coquette A (2006) Modelling the human epidermis in vitro: tools for basic and applied research. Arch Dermatol Res 298:361–369. https://doi.org/10.1007/s00403-006-0709-6
Prescott SL, Larcombe D-L, Logan AC et al (2017) The skin microbiome: impact of modern environments on skin ecology, barrier integrity, and systemic immune programming. World Allergy Organ J 10:29. https://doi.org/10.1186/s40413-017-0160-5
Proksch E, Brandner JM, Jensen J-M (2008) The skin: an indispensable barrier. Exp Dermatol 17:1063–1072. https://doi.org/10.1111/j.1600-0625.2008.00786.x
Prunieras M (1979) Epidermal cell cultures as models for living epidermis. J Invest Dermatol. https://doi.org/10.1111/1523-1747.ep12556751
Rattan SIS (2015) Aging and Senescence of skin cells in culture. Textbook of aging skin. Springer, Berlin, pp 1–8
Régnier M, Caron D, Reichert U, Schaefer H (1992) Reconstructed human epidermis: a model to study in vitro the barrier function of the skin. Skin Pharmacol Physiol. https://doi.org/10.1159/000211017
Remoué N, Molinari J, Andres E et al (2013) Development of an in vitro model of menopause using primary human dermal fibroblasts. Int J Cosmet Sci. https://doi.org/10.1111/ics.12075
Reus TL, Brohem CA, Schuck DC, Lorencini M (2020) Revisiting the effects of menopause on the skin: functional changes, clinical studies, in vitro models and therapeutic alternatives. Mech Ageing Dev 185:111193. https://doi.org/10.1016/j.mad.2019.111193
Rincón-Fontán M, Rodríguez-López L, Vecino X et al (2020) Potential application of a multifunctional biosurfactant extract obtained from corn as stabilizing agent of vitamin C in cosmetic formulations. Sustain Chem Pharm 16:100248. https://doi.org/10.1016/j.scp.2020.100248
Rinnerthaler M, Bischof J, Streubel M et al (2015) Oxidative stress in aging human skin. Biomolecules 5:545–589. https://doi.org/10.3390/biom5020545
Rittié L, Fisher GJ (2015) Natural and sun-induced aging of human skin. Cold Spring Harb Perspect Med. https://doi.org/10.1101/cshperspect.a015370
Rocha MA, Bagatin E (2018) Skin barrier and microbiome in acne. Arch Dermatol Res 310:181–185. https://doi.org/10.1007/s00403-017-1795-3
Rognoni E, Watt FM (2018) Skin cell heterogeneity in development, wound healing, and cancer. Trends Cell Biol 28:709–722. https://doi.org/10.1016/j.tcb.2018.05.002
Sami DG, Heiba HH, Abdellatif A (2019) Wound healing models: a systematic review of animal and non-animal models. Wound Med 24:8–17. https://doi.org/10.1016/j.wndm.2018.12.001
Schommer NN, Gallo RL (2013) Structure and function of the human skin microbiome. Trends Microbiol 21:660–668. https://doi.org/10.1016/j.tim.2013.10.001
Shibagaki N, Suda W, Clavaud C et al (2017) Aging-related changes in the diversity of women’s skin microbiomes associated with oral bacteria. Sci Rep 7:10567. https://doi.org/10.1038/s41598-017-10834-9
Sugiyama Y, Yamazaki K, Kusaka-Kikushima A et al (2014) Analysis of aquaporin 9 expression in human epidermis and cultured keratinocytes. FEBS Open Bio. https://doi.org/10.1016/j.fob.2014.06.004
Sukseree S, Bergmann S, Pajdzik K et al (2018a) Suppression of epithelial autophagy compromises the homeostasis of sweat glands during aging. J Invest Dermatol 138:2061–2063. https://doi.org/10.1016/j.jid.2018.03.1502
Sukseree S, Bergmann S, Pajdzik K et al (2018b) Suppression of autophagy perturbs turnover of sequestosome-1/p62 in Merkel cells but not in keratinocytes. J Dermatol Sci 90:209–211. https://doi.org/10.1016/j.jdermsci.2018.01.008
Sundaram H, Mackiewicz N, Burton E et al (2016) Pilot comparative study of the topical action of a novel, crosslinked resilient hyaluronic acid on skin hydration and barrier function in a dynamic, three-dimensional human explant model. J Drugs Dermatol 15:434–441
Taylor SC (2005) Photoaging and pigmentary changes of the skin. Cosmetic dermatology. Springer, Berlin, pp 29–51
Tett A, Pasolli E, Farina S et al (2017) Unexplored diversity and strain-level structure of the skin microbiome associated with psoriasis. NPJ Biofilms Microb 3:14. https://doi.org/10.1038/s41522-017-0022-5
Thune P (1989) Evaluation of the hydration and the water-holding capacity in atopic skin and so-called dry skin. Acta Dermato-Venereol 144:133–135
Tigges J, Krutmann J, Fritsche E et al (2014) The hallmarks of fibroblast ageing. Mech Ageing Dev 138:26–44. https://doi.org/10.1016/j.mad.2014.03.004
Torricelli P, Fini M, Fanti PA et al (2017) Protective effects of polypodium leucotomos extract against UVB-induced damage in a model of reconstructed human epidermis. Photodermatol Photoimmunol Photomed 33:156–163. https://doi.org/10.1111/phpp.12297
Ud-Din S, Bayat A (2017a) Non-animal models of wound healing in cutaneous repair: in silico, in vitro, ex vivo, and in vivo models of wounds and scars in human skin. Wound Repair Regen. https://doi.org/10.1111/wrr.12513
Ud-Din S, Bayat A (2017b) Non-animal models of wound healing in cutaneous repair: in silico, in vitro, ex vivo, and in vivo models of wounds and scars in human skin. Wound Repair Regen 25:164–176. https://doi.org/10.1111/wrr.12513
Van Den Broek LJ, Niessen FB, Scheper RJ, Gibbs S (2012) Development, validation, and testing of a human tissue engineered hypertrophic scar model. Altex. https://doi.org/10.14573/altex.2012.4.389
Van Wezel AL (1967) Growth of cell-strains and primary cells on micro-carriers in homogeneous culture. Nature. https://doi.org/10.1038/216064a0
Verdier-Sévrain S, Bonté F (2007) Skin hydration: a review on its molecular mechanisms. JCosmet Dermatol. https://doi.org/10.1111/j.1473-2165.2007.00300.x
Vita NA, Brohem CA, Canavez ADPM et al (2018) Parameters for assessing the aquatic environmental impact of cosmetic products. Toxicol Lett 287:70–82. https://doi.org/10.1016/j.toxlet.2018.01.015
Vostálová J, Cukr M, Zálešák B et al (2018) Comparison of various methods to analyse toxic effects in human skin explants: rediscovery of TTC assay. J Photochem Photobiol B 178:530–536. https://doi.org/10.1016/j.jphotobiol.2017.12.011
Wang PH, Huang BS, Horng HC et al (2018) Wound healing. J Chin Med Assoc. https://doi.org/10.1016/j.jcma.2017.11.002
Watanabe M, Tagami H, Horii I et al (1991) Functional analyses of the superficial stratum corneum in atopic xerosis. Arch Dermatol. https://doi.org/10.1001/archderm.1991.01680100089010
Xie Y, Rizzi SC, Dawson R et al (2010) Development of a three-dimensional human skin equivalent wound model for investigating novel wound healing therapies. Tissue Eng C. https://doi.org/10.1089/ten.tec.2009.0725
Xu W, Jong Hong S, Jia S et al (2012) Application of a partial-thickness human ex vivo skin culture model in cutaneous wound healing study. Lab Investig 92:584–599. https://doi.org/10.1038/labinvest.2011.184
Yoshimoto S, Yoshida M, Ando H, Ichihashi M (2018) Establishment of photoaging in vitro by repetitive UVA irradiation: induction of characteristic markers of senescence and its prevention by PAPLAL with potent catalase activity. Photochem Photobiol. https://doi.org/10.1111/php.12871
Yousuf Y, Amini-Nik S, Jeschke MG (2018) Overall perspective on the clinical importance of skin models. Skin tissue models for regenerative medicine. Elsevier, Amsterdam, pp 39–54
Zeitoun H, Michael-Jubeli R, El Khoury R et al (2020) Skin lightening effect of natural extracts coming from Senegal botanical biodiversity. Int J Dermatol. https://doi.org/10.1111/ijd.14699
Zhai W, Huang Y, Zhang X et al (2018) Profile of the skin microbiota in a healthy Chinese population. J Dermatol 45:1289–1300. https://doi.org/10.1111/1346-8138.14594
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This study was supported by APIVITA SA.
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Sophia Letsiou conceived, planned and wrote the manuscript.
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Letsiou, S. Tracing skin aging process: a mini- review of in vitro approaches. Biogerontology 22, 261–272 (2021). https://doi.org/10.1007/s10522-021-09916-z
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DOI: https://doi.org/10.1007/s10522-021-09916-z