Analysis of biomechanical properties of mouse skin dermis through atomic force microscopy: Application to demonstrate a sexual dimorphism.


Journal

Experimental dermatology
ISSN: 1600-0625
Titre abrégé: Exp Dermatol
Pays: Denmark
ID NLM: 9301549

Informations de publication

Date de publication:
07 2023
Historique:
revised: 10 03 2023
received: 12 10 2022
accepted: 29 03 2023
medline: 11 7 2023
pubmed: 9 4 2023
entrez: 8 4 2023
Statut: ppublish

Résumé

An in-depth understanding of the mechanical properties of the dermis is indispensable to improve wound healing or slow-down skin ageing. Despite crucial research issues for dermatological and cosmetic industries, very little is known about the mechanical behaviour of the dermis at nanoscale level. This knowledge is relevant not only to human skin but also to mouse skin since this animal model is widely used in basic and preclinical studies for skin biology and health. Here, we describe an original protocol that we developed to specifically measure the mechanical properties of mouse dermis using atomic force microscopy-based nano-indentation approach. Using horizontal cryosections (i.e. parallel to the skin surface) performed at different depths through the dermis of dorsal skin, our protocol allowed us to detect nanoscale mechanical changes between female and male dermis samples. We found that the dermis was softer (i) in females than in males and (ii) with depth within the dermis of male mice. We also quantified compositional differences between female and male skin dermis and found that increased extracellular matrix gene expression and type V collagen staining were associated with increased dermal stiffness in male mice, compared with females. Our results demonstrating a sexual dimorphism in the nanomechanical properties and molecular composition of mouse dermis, open the way to better consider sex-related cutaneous differences to understand skin disease and to stimulate the development of female versus male-specific products with more appropriate dermatological treatments and cosmetic interventions.

Identifiants

pubmed: 37029962
doi: 10.1111/exd.14807
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1016-1027

Informations de copyright

© 2023 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.

Références

Deniz AAH, Abdik EA, Abdik H, Aydın S, Şahin F, Taşlı PN. Zooming in across the skin: a macro-to-molecular panorama. Adv Exp Med Biol. 2020;1247:157-200. doi:10.1007/5584_2019_442
Karamanos NK, Theocharis AD, Piperigkou Z, et al. A guide to the composition and functions of the extracellular matrix. FEBS J. 2021;288(24):6850-6912. doi:10.1111/febs.15776
Biggs LC, Kim CS, Miroshnikova YA, Wickström SA. Mechanical forces in the skin: roles in tissue architecture, stability, and function. J Invest Dermatol. 2020;140(2):284-290. doi:10.1016/j.jid.2019.06.137
Gosline J, Lillie M, Carrington E, Guerette P, Ortlepp C, Savage K. Elastic proteins: biological roles and mechanical properties. Philos Trans R Soc Lond B Biol Sci. 2002;357(1418):121-132. doi:10.1098/rstb.2001.1022
Kenny FN, Drymoussi Z, Delaine-Smith R, et al. Tissue stiffening promotes keratinocyte proliferation through activation of epidermal growth factor signaling. J Cell Sci. 2018;131(10):jcs215780. doi:10.1242/jcs.215780
Mostafavi Yazdi SJ, Baqersad J. Mechanical modeling and characterization of human skin: a review. J Biomech. 2022;130:110864. doi:10.1016/j.jbiomech.2021.110864
Smolyakov G, Formosa-Dague C, Severac C, Duval RE, Dague E. High speed indentation measures by FV, QI and QNM introduce a new understanding of bionanomechanical experiments. Micron. 2016;85:8-14. doi:10.1016/j.micron.2016.03.002
Gavara N. A beginner's guide to atomic force microscopy probing for cell mechanics. Microsc Res Tech. 2017;80(1):75-84. doi:10.1002/jemt.22776
Connelly JT, Gavara N, Sliogeryte K, Blowes LM. Research techniques made simple: analysis of skin cell and tissue mechanics using atomic force microscopy. J Invest Dermatol. 2021;141(8):1867-1871.e1. doi:10.1016/j.jid.2021.02.750
Milani P, Chlasta J, Abdayem R, Kezic S, Haftek M. Changes in nano-mechanical properties of human epidermal cornified cells depending on their proximity to the skin surface. J Mol Recognit. 2018;31(9):e2722. doi:10.1002/jmr.2722
Laly AC, Sliogeryte K, Pundel OJ, et al. The keratin network of intermediate filaments regulates keratinocyte rigidity sensing and nuclear mechanotransduction. Sci Adv. 2021;7(5):eabd6187. doi:10.1126/sciadv.abd6187
Homberg M, Ramms L, Schwarz N, et al. Distinct impact of two keratin mutations causing epidermolysis bullosa simplex on keratinocyte adhesion and stiffness. J Invest Dermatol. 2015;135(10):2437-2445. doi:10.1038/jid.2015.184
Haftek M, McAleer MA, Jakasa I, McLean WI, Kezic S, Irvine AD. Changes in nano-mechanical properties of human epidermal cornified cells in children with atopic dermatitis. Wellcome Open Res. 2020;5:97. doi:10.12688/wellcomeopenres.15729.2
Masson-Meyers DS, Andrade TAM, Caetano GF, et al. Experimental models and methods for cutaneous wound healing assessment. Int J Exp Pathol. 2020;101(1-2):21-37. doi:10.1111/iep.12346
Griffin MF, desJardins-Park HE, Mascharak S, Borrelli MR, Longaker MT. Understanding the impact of fibroblast heterogeneity on skin fibrosis. Dis Model Mech. 2020;13(6):dmm044164. doi:10.1242/dmm.044164
Mao JR, Taylor G, Dean WB, et al. Tenascin-X deficiency mimics Ehlers-Danlos syndrome in mice through alteration of collagen deposition. Nat Genet. 2002;30(4):421-425. doi:10.1038/ng850
Wenstrup RJ, Florer JB, Davidson JM, et al. Murine model of the Ehlers-Danlos syndrome. col5a1 haploinsufficiency disrupts collagen fibril assembly at multiple stages. J Biol Chem. 2006;281(18):12888-12895. doi:10.1074/jbc.M511528200
Schindelin J, Arganda-Carreras I, Frise E, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012;9(7):676-682. doi:10.1038/nmeth.2019
Schneider CA, Rasband WS, Eliceiri KW. NIH image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9(7):671-675. doi:10.1038/nmeth.2089
Sader JE, Borgani R, Gibson CT, et al. A virtual instrument to standardise the calibration of atomic force microscope cantilevers. Rev Sci Instrum. 2016;87(9):093711. doi:10.1063/1.4962866
Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001;25(4):402-408. doi:10.1006/meth.2001.1262
Nallasamy S, Yoshida K, Akins M, Myers K, Iozzo R, Mahendroo M. Steroid hormones are key modulators of tissue mechanical function via regulation of collagen and elastic fibers. Endocrinology. 2017;158(4):950-962. doi:10.1210/en.2016-1930
Sun M, Zafrullah N, Devaux F, et al. Collagen XII is a regulator of corneal stroma structure and function. Invest Ophthalmol Vis Sci. 2020;61(5):61. doi:10.1167/iovs.61.5.61
Valcourt U, Thuault S, Pardali K, Heldin CH, Moustakas A. Functional role of Meox2 during the epithelial cytostatic response to TGF-beta. Mol Oncol. 2007;1(1):55-71. doi:10.1016/j.molonc.2007.02.002
Azzi L, El-Alfy M, Martel C, Labrie F. Gender differences in mouse skin morphology and specific effects of sex steroids and dehydroepiandrosterone. J Invest Dermatol. 2005;124(1):22-27. doi:10.1111/j.0022-202X.2004.23545.x
Zou Y, Maibach HI. Dermal-epidermal separation methods: research implications. Arch Dermatol Res. 2018;310(1):1-9. doi:10.1007/s00403-017-1774-8
Kao AP, Connelly JT, Barber AH. 3D nanomechanical evaluations of dermal structures in skin. J Mech Behav Biomed Mater. 2016;57:14-23. doi:10.1016/j.jmbbm.2015.11.017
Boyle CJ, Plotczyk M, Villalta SF, et al. Morphology and composition play distinct and complementary roles in the tolerance of plantar skin to mechanical load. Sci Adv. 2019;5(10):eaay0244. doi:10.1126/sciadv.aay0244
Ní Annaidh A, Bruyère K, Destrade M, et al. Automated estimation of collagen fibre dispersion in the dermis and its contribution to the anisotropic behaviour of skin. Ann Biomed Eng. 2012;40(8):1666-1678. doi:10.1007/s10439-012-0542-3
McConnell JC, O'Connell OV, Brennan K, et al. Increased peri-ductal collagen micro-organization may contribute to raised mammographic density. Breast Cancer Res. 2016;18(1):5. doi:10.1186/s13058-015-0664-2
Ojha S, Pribyl J, Klimovic S, Hadraba D, Jirouskova M, Gregor M. Measurement of liver stiffness using atomic force microscopy coupled with polarization microscopy. J Vis Exp. 2022;185:63974. doi:10.3791/63974
Wenstrup RJ, Smith SM, Florer JB, et al. Regulation of collagen fibril nucleation and initial fibril assembly involves coordinate interactions with collagens V and XI in developing tendon. J Biol Chem. 2011;286(23):20455-20465. doi:10.1074/jbc.M111.223693
Connizzo BK, Freedman BR, Fried JH, Sun M, Birk DE, Soslowsky LJ. Regulatory role of collagen V in establishing mechanical properties of tendons and ligaments is tissue dependent. J Orthop Res. 2015;33(6):882-888. doi:10.1002/jor.22893
Bonod-Bidaud C, Roulet M, Hansen U, et al. In vivo evidence for a bridging role of a collagen V subtype at the epidermis-dermis interface. J Invest Dermatol. 2012;132(7):1841-1849. doi:10.1038/jid.2012.56
Peñuela L, Negro C, Massa M, et al. Atomic force microscopy for biomechanical and structural analysis of human dermis: a complementary tool for medical diagnosis and therapy monitoring. Exp Dermatol. 2018;27(2):150-155. doi:10.1111/exd.13468
Muñoz MJ, Bea JA, Rodríguez JF, et al. An experimental study of the mouse skin behaviour: damage and inelastic aspects. J Biomech. 2008;41(1):93-99. doi:10.1016/j.jbiomech.2007.07.013
Oftadeh R, Connizzo BK, Nia HT, Ortiz C, Grodzinsky AJ. Biological connective tissues exhibit viscoelastic and poroelastic behavior at different frequency regimes: application to tendon and skin biophysics. Acta Biomater. 2018;70:249-259. doi:10.1016/j.actbio.2018.01.041
Hansen LS, Coggle JE, Wells J, Charles MW. The influence of the hair cycle on the thickness of mouse skin. Anat Rec. 1984;210(4):569-573. doi:10.1002/ar.1092100404
Müller-Röver S, Handjiski B, van der Veen C, et al. A comprehensive guide for the accurate classification of murine hair follicles in distinct hair cycle stages. J Invest Dermatol. 2001;117(1):3-15. doi:10.1046/j.0022-202x.2001.01377.x
Hadjipanayi E, Mudera V, Brown RA. Guiding cell migration in 3D: a collagen matrix with graded directional stiffness. Cell Motil Cytoskeleton. 2009;66(3):121-128. doi:10.1002/cm.20331
Shuster S, Black MM, McVitie E. The influence of age and sex on skin thickness, skin collagen and density. Br J Dermatol. 1975;93(6):639-643. doi:10.1111/j.1365-2133.1975.tb05113.x
Vitellaro-Zuccarello L, Cappelletti S, Dal Pozzo RV, Sari-Gorla M. Stereological analysis of collagen and elastic fibers in the normal human dermis: variability with age, sex, and body region. Anat Rec. 1994;238(2):153-162. doi:10.1002/ar.1092380202
Castori M, Camerota F, Celletti C, Grammatico P, Padua L. Ehlers-Danlos syndrome hypermobility type and the excess of affected females: possible mechanisms and perspectives. Am J Med Genet A. 2010;152A(9):2406-2408. doi:10.1002/ajmg.a.33585
Green C, Ghali N, Akilapa R, et al. Classical-like Ehlers-Danlos syndrome: a clinical description of 20 newly identified individuals with evidence of tissue fragility. Genet Med. 2020;22(10):1576-1582. doi:10.1038/s41436-020-0850-1

Auteurs

Laura Prigent (L)

Laboratoire de Biologie Tissulaire et Ingénierie Thérapeutique (LBTI), UMR CNRS 5305, Université Claude Bernard Lyon 1 (UCBL1), Institut de Biologie et Chimie des Protéines, Lyon, France.

Perrine Mercier-Gouy (P)

Laboratoire de Biologie Tissulaire et Ingénierie Thérapeutique (LBTI), UMR CNRS 5305, Université Claude Bernard Lyon 1 (UCBL1), Institut de Biologie et Chimie des Protéines, Lyon, France.

Simone Bovio (S)

RDP, Université de Lyon, ENS de Lyon, UCBL1, INRAE, CNRS, Lyon, France.
PLATIM-LyMIC, Université de Lyon, ENS de Lyon, Inserm, CNRS, SFR Biosciences US8 UAR3444, UCBL1, Lyon, France.

Alexandre Aubert (A)

Laboratoire de Biologie Tissulaire et Ingénierie Thérapeutique (LBTI), UMR CNRS 5305, Université Claude Bernard Lyon 1 (UCBL1), Institut de Biologie et Chimie des Protéines, Lyon, France.

Sophie Liot (S)

Laboratoire de Biologie Tissulaire et Ingénierie Thérapeutique (LBTI), UMR CNRS 5305, Université Claude Bernard Lyon 1 (UCBL1), Institut de Biologie et Chimie des Protéines, Lyon, France.

Elise Lambert (E)

Laboratoire de Biologie Tissulaire et Ingénierie Thérapeutique (LBTI), UMR CNRS 5305, Université Claude Bernard Lyon 1 (UCBL1), Institut de Biologie et Chimie des Protéines, Lyon, France.

Ulrich Valcourt (U)

Laboratoire de Biologie Tissulaire et Ingénierie Thérapeutique (LBTI), UMR CNRS 5305, Université Claude Bernard Lyon 1 (UCBL1), Institut de Biologie et Chimie des Protéines, Lyon, France.

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