Skin models of cutaneous toxicity, transdermal transport and wound repair

Inês Vilela de Sousa; Miguel J S Ferreira; Luís B Bebiano; Sandra Simões; Ana Filipa Matos; Rúben F Pereira; Pedro L Granja

doi:10.1093/burnst/tkad014

您当前的位置：

首页 >

文章列表页 >

Skin models of cutaneous toxicity, transdermal transport and wound repair

更新时间：2023-08-29

- Skin models of cutaneous toxicity, transdermal transport and wound repair
- Skin models of cutaneous toxicity, transdermal transport and wound repair
- Burns & Trauma 2023年11卷第1期
- 作者机构：
  
  1. i3S - Instituto de Investigação e Inovação em Saúde, Universidade do Porto
  2. INEB - Instituto de Engenharia Biomédica, Universidade do Porto
  3. ICBAS – Instituto de Ciências Biomédicas Abel Salazar, Universidade do Porto
  4. FEUP – Faculdade de Engenharia da Universidade do Porto
  5. Department of Mechanical, Aerospace and Civil Engineering, School of Engineering, Faculty of Science and Engineering & Henry Royce Institute, Engineering Building A, The University of Manchester
  6. ISEP - Instituto Superior de Engenharia do Porto, Universidade do Porto
  7. iMed.ULisboa
  8. Universidade de Lisboa
  9. Faculty of Pharmacy, Universidade de Lisboa
- 作者简介：
- 基金信息：
  
  This work was supported by Portuguese funds from the Foundation for Science and Technology (FCT) (projects i3S, ref. UID/BIM/04293/2020;SKINCHIP, ref. PTDC/BBB-BIO/1889/2014;iMed.ULisboa, refs. UID/DTP/04138/2020 and UIDB/DTP/04138/2020);and UK funds from the Engineering and Physical Sciences Research Council (EPSRC) and Medical Research Council (MRC) (projects Centre for Doctoral Training in Regenerative Medicine, ref. EP/L014904/1, and Henry Royce Institute for Advanced Materials, refs. EP/R00661X/1, EP/P025021/1 and EP/P025498/1).
- DOI：10.1093/burnst/tkad014
  中图分类号：
- 纸质出版日期：2023，
  
  网络出版日期：2023-7-28，
扫描看全文
Inês Vilela de Sousa, Miguel J S Ferreira, Luís B Bebiano, 等. Skin models of cutaneous toxicity, transdermal transport and wound repair[J]. Burns & Trauma, 2023,11(1).

Inês Vilela de Sousa, Miguel J S Ferreira, Luís B Bebiano, Sandra Simões, Ana Filipa Matos, Rúben F Pereira, Pedro L Granja, Skin models of cutaneous toxicity, transdermal transport and wound repair, Burns & Trauma, Volume 11, 2023, tkad014, https://doi.org/10.1093/burnst/tkad014
Inês Vilela de Sousa, Miguel J S Ferreira, Luís B Bebiano, 等. Skin models of cutaneous toxicity, transdermal transport and wound repair[J]. Burns & Trauma, 2023,11(1). DOI： 10.1093/burnst/tkad014.

Inês Vilela de Sousa, Miguel J S Ferreira, Luís B Bebiano, Sandra Simões, Ana Filipa Matos, Rúben F Pereira, Pedro L Granja, Skin models of cutaneous toxicity, transdermal transport and wound repair, Burns & Trauma, Volume 11, 2023, tkad014, https://doi.org/10.1093/burnst/tkad014 DOI：

摘要

Abstract

Skin is widely used as a drug delivery route due to its easy access and the possibility of using relatively painless methods for the administration of bioactive molecules. However

the barrier properties of the skin

along with its multilayer structure

impose severe restrictions on drug transport and bioavailability. Thus

bioengineered models aimed at emulating the skin have been developed not only for optimizing the transdermal transport of different drugs and testing the safety and toxicity of substances but also for understanding the biological processes behind skin wounds. Even though in vivo research is often preferred to study biological processes involving the skin

in vitro and ex vivo strategies have been gaining increasing relevance in recent years. Indeed

there is a noticeably increasing adoption of in vitro and ex vivo methods by internationally accepted guidelines. Furthermore

microfluidic organ-on-a-chip devices are nowadays emerging as valuable tools for functional and behavioural skin emulation. Challenges in miniaturization

automation and reliability still need to be addressed in order to create skin models that can predict skin behaviour in a robust

high-throughput manner

while being compliant with regulatory issues

standards and guidelines. In this review

skin models for transdermal transport

wound repair and cutaneous toxicity will be discussed with a focus on high-throughput strategies. Novel microfluidic strategies driven by advancements in microfabrication technologies will also be revised as a way to improve the efficiency of existing models

both in terms of complexity and throughput.

关键词

Keywords

skinIn vitro modelsEx vivo modelsTransdermal transport assaysWound healing assaysToxicity assaysMicrofluidic chipSkin-on-a-chip

references

1.Agache PG, Agache P, Humbert P. Measuring the Skin. Heidelberg:Springer Berlin, 2004, 784.

2.Pereira RF, Sousa A, Barrias CC, Bayat A, Granja PL, Bártolo PJ. Advances in bioprinted cell-laden hydrogels for skin tissue engineering. Biomanufacturing Reviews. 2017;2:1.

3.Metcalfe AD, Ferguson MWJ. Tissue engineering of replacement skin: the crossroads of biomaterials, wound healing, embryonic development, stem cells and regeneration. J R Soc Interface. 2007;4:413–37.

4.Madison KC. Barrier function of the skin: ‘“La raison d'EOE tre”' of the epidermis. J Investig Dermatol. 2003;121:231–41.

5.Choi E, Nahm FS, Han WK, Lee PB, Jo J. Topical agents: a thoughtful choice for multimodal analgesia. Korean J Anesthesiol. 2020;73:384–93.

6.Friend DR. Transdermal delivery of contraceptives. Crit Rev Ther Drug Carrier Syst. 1990;7:149–86.

7.Prausnitz MR, Langer R. Transdermal drug delivery. Nat Biotechnol. 2008;26:1261–8.

8.Barrett DA, Rutter N. Transdermal delivery and the premature neonate. Crit Rev Ther Drug Carrier Syst. 1994;11:1–30.

9.Arora P, Mukherjee B. Design, development, physicochemical, and in vitro and in vivo evaluation of transdermal patches containing diclofenac diethylammonium salt. J Pharm Sci. 2002;91:2076–89.

10.Lee H, Song C, Baik S, Kim D, Hyeon T, Kim DH. Device-assisted transdermal drug delivery. Adv Drug Deliv Rev. 2018;127:35–45.

11.Bibi N, Ahmed N, Khan GM. Nanostructures in transdermal drug delivery systems. In: Andronescu E, Grumezescu AM (eds). Nanostructures for Drug Delivery.Amsterdam, The Netherlands: Elsevier, 2017, 639–68. https://doi.org/10.1016/B978-0-323-46143-6.00021-X.

12.Manikkath J, Hegde AR, Parekh HS, Mutalik S. Peptide Dendrimers in Delivery of Bioactive Molecules to Skin. In: Hamblin MR, Avci P, Prow TW (eds). Nanoscience in Dermatology. Boston:Academic Press, 2016, 89–97.

13.Sen CK. Human wounds and its burden: an updated compendium of estimates. Adv Wound Care. 2019;8:39–48.

14.United Nations. Globally harmonized system of classification and labelling of chemicals (GHS).United Nations, 2011. https://digitallibrary.un.org/record/660120.

15.Teimouri A, Yeung P, Agu R. 2D vs. 3D Cell Culture Models for In Vitro Topical (Dermatological) Medication Testing. In: Mehanna RA (ed). Cell Culture. Rijeka:IntechOpen, 2019.

16.Bhatia SN, Ingber DE. Microfluidic organs-on-chips. Nat Biotechnol. 2014;32:760–72.

17.Li Z. In Vitro Micro-Tissue and -Organ Models for Toxicity Testing. In: Moo-Young M (ed). Comprehensive Biotechnology (Second Edition), Second edn. Burlington:Academic Press, 2011, 551–63.

18.Risueño I, Valencia L, Jorcano JL, Velasco D. Skin-on-a-chip models: general overview and future perspectives. APL Bioengineering. 2021;5. https://doi.org/10.1063/5.0046376.

19.Moroni L, Burdick JA, Highley C, Lee SJ, Morimoto Y, Takeuchi S, et al. Biofabrication strategies for 3D in vitro models and regenerative medicine. Nature Reviews Materials. 2018;3:21–37.

20.Niehues H, Bouwstra JA, El Ghalbzouri A, Brandner JM, Zeeuwen PLJM, van den Bogaard EH. 3D skin models for 3R research: the potential of 3D reconstructed skin models to study skin barrier function. Exp Dermatol. 2018;27:501–11.

21.Pereira RF, Barrias CC, Granja PL, Bartolo PJ. Advanced biofabrication strategies for skin regeneration and repair. Nanomedicine (Lond). 2013;8:603–21.

22.Edmondson R, Broglie JJ, Adcock AF, Yang L. Three-dimensional cell culture systems and their applications in drug discovery and cell-based biosensors. Assay Drug Dev Technol. 2014;12:207–18.

23.de la Torre RS, Fernández-González A, Quiñones-Vico MI, Montero-Vilchez T, Arias-Santiago S. Bioengineered skin intended as in vitro model for pharmacosmetics, skin disease study and environmental skin impact analysis. Biomedicine. 2020;8:1–28.

24.Esch EW, Bahinski A, Huh D. Organs-on-chips at the frontiers of drug discovery. Nat Rev Drug Discov. 2015;14:248–60.

25.Russell WMS, Burch RL. The principles of humane experimental technique. London, UK: Methuen, 1959.

26.Alépée N, Bahinski A, Daneshian M, De Wever B, Fritsche E, Goldberg A, et al. State-of-the-art of 3D cultures (organs-on-a-chip) in safety testing and pathophysiology. ALTEX - Alternatives to animal experimentation. 2014;31:441–77.

27.Alkilani AZ, McCrudden MTC, Donnelly RF. Transdermal drug delivery: innovative pharmaceutical developments based on disruption of the barrier properties of the stratum corneum. Pharmaceutics. 2015;7:438–70.

28.Yamaguchi T, Ishikawa T, Imai Y (eds). K K. 4 - Biomechanics for Pathology and Treatment. In: Integrated Nano-Biomechanics. Boston:Elsevier, 2018, 101–46.

29.Supe S, Takudage P. Methods for evaluating penetration of drug into the skin: a review. Skin Res Technol. 2021;27:299–308.

30.Bamba FL, Wepierre J. Role of the appendageal pathway in the percutaneous absorption of pyridostigmine bromide in various vehicles. Eur J Drug Metab Pharmacokinet. 1993;18:339–48.

31.Winsor T, Burch GE. Differential roles of layers of human epigastric skin on diffusion rate of water. Arch Intern Med. 1944;74:428.

32.Prausnitz MR, Elias PM, Franz TJ, Schmuth M. Tsai J-c, Menon GK, et al. skin barrier and transdermal drug delivery. Dermatology. 2012;2065–73.

33.Fuchs E, Green H. Changes in keratin gene expression during terminal differentiation of the keratinocyte. Cell. 1980;19:1033–42.

34.Elias PM. Epidermal lipids, barrier function, and desquamation. J Invest Dermatol. 1983;80:S44–9.

35.Andrews SN, Jeong E, Prausnitz MR. Transdermal delivery of molecules is limited by full epidermis, not just stratum corneum. Pharm Res. 2013;30:1099–109.

36.Wenkers BP, Lippold BC. Skin penetration of nonsteroidal antiinflammatory drugs out of a lipophilic vehicle: influence of the viable epidermis. J Pharm Sci. 1999;88:1326–31.

37.Todo H. Transdermal permeation of drugs in various animal species. Pharmaceutics. 2017;9:33. https://doi.org/10.3390/pharmaceutics9030033.

38.Abd E, Yousef SA, Pastore MN, Telaprolu K, Mohammed YH, Namjoshi S, et al. Skin models for the testing of transdermal drugs. Clinical Pharmacology: Advances and Applications. 2016;8:163–76.

39.Nakov A, Magalhães C, Faria-Silva C, Ascensão L, Marto J, Ribeiro HM, et al. Lipid-coated membranes as skin surrogates for permeability assessment. Materialia. 2022;21:101354.

40.Oecd. OECD guidlines for the testing of chemicals. 428. Skin Absorption: in vitro Method. OECDi Library, 2004, (April). https://www.oecd-ilibrary.org/environment/test-no-428-skin-absorption-in-vitro-method_9789264071087-en.

41.Byford T. Environmental health criteria 235: dermal absorption. Int J Environ Stud. 2009;66:662–3.

42.Friend DR. In vitro skin permeation techniques. J Control Release. 1992;18:235–48.

43.Bartek MJ, LaBudde JA, Maibach HI. Skin permeability in vivo: comparison in rat, rabbit, pig and man. J Invest Dermatol. 1972;58:114–23.

44.Schmook FP, Meingassner JG, Billich A. Comparison of human skin or epidermis models with human and animal skin in in-vitro percutaneous absorption. Int J Pharm. 2001;215:51–6.

45.Galey WR, Lonsdale HK, Nacht S. The in vitro permeability of skin and buccal mucosa to selected drugs and tritiated water. J Invest Dermatol. 1976;67:713–7.

46.Dick IP, Scott RC. Pig ear skin as an in-vitro model for human skin permeability. J Pharm Pharmacol. 1992;44:640–5.

47.Kaur L, Singh K, Paul S, Singh S, Singh S, Jain SK. A mechanistic study to determine the structural similarities between artificial membrane Strat-M™ and biological membranes and its application to carry out skin permeation study of amphotericin B Nanoformulations. AAPS PharmSciTech. 2018;19:1606–24.

48.Maibach HI, Wester RC. Percutaneous absorption: in vivo methods in humans and animals. J Am Coll Toxicol. 1989;8:803–13.

49.Scott RC, Walker M, Dugard PH. A comparison of the in vitro permeability properties of human and some laboratory animal skins. Int J Cosmet Sci. 1986;8:189–94.

50.Morimoto Y, Hatanaka T, Sugibayashi K, Omiya H. Prediction of skin permeability of drugs: comparison of human and hairless rat skin. J Pharm Pharmacol. 1992;44:634–9.

51.Jung EC, Maibach HI. Animal models for percutaneous absorption. J Appl Toxicol. 2015;35:1–10.

52.Schäfer-Korting M, Mahmoud A, Borgia SL, Brüggener B, Kleuser B, Schreiber S, et al. Reconstructed epidermis and full-thickness skin for absorption testing: influence of the vehicles used on steroid permeation. ATLA Alternatives to Laboratory Animals. 2008;36:441–52.

53.Pereira RF, Barrias CC, Bártolo PJ, Granja PL. Cell-instructive pectin hydrogels crosslinked via thiol-norbornene photo-click chemistry for skin tissue engineering. Acta Biomater. 2018;66:282–93.

54.Schäfer-Korting M, Bock U, Diembeck W, Düsing H-J, Gamer A, Haltner-Ukomadu E, et al. The use of reconstructed human epidermis for skin absorption testing: results of the validation study. Altern Lab Anim. 2008;36:161–87.

55.Salamanca CH, Barrera-Ocampo A, Lasso JC, Camacho N, Yarce CJ. Franz diffusion cell approach for pre-formulation characterisation of Ketoprofen semi-solid dosage forms. Pharmaceutics. 2018;10:148.

56.Pulsoni I, Lubda M, Aiello M, Fedi A, Marzagalli M, von Hagen J, et al. Comparison Between Franz Diffusion Cell and a novel Micro-physiological System for In Vitro Penetration Assay Using Different Skin Models.Illinois, US: SLAS Technology, 2022.

57.Franz TJ. Percutaneous absorption on the relevance of in vitro data. J Invest Dermatol. 1975;64:190–5.

58.Mohammed D, Matts PJ, Hadgraft J, Lane ME. In vitro–in vivo correlation in skin permeation. Pharm Res. 2014;31:394–400.

59.Martins PP, Estrada AD, Smyth HDC. A human skin high-throughput formulation screening method using a model hydrophilic drug. Int J Pharm. 2019;565:557–68.

60.Addicks WJ, Flynn GL, Weiner N. Validation of a flow-through diffusion cell for use in transdermal research. Pharm Res. 1987;4:337–41.

61.Bronaugh RL, Stewart RF. Methods for in vitro percutaneous absorption studies IV: the flow-through diffusion cell. J Pharm Sci. 1985;74:64–7.

62.Bronaugh RL, Stewart RF. Methods for in vitro percutaneous absorption studies V: permeation through damaged skin. J Pharm Sci. 1985;74:1062–6.

63.Karande P, Mitragotri S. High throughput screening of transdermal formulations. Pharm Res. 2002;19:655–60.

64.Karande P, Jain A, Mitragotri S. Discovery of transdermal penetration enhancers by high-throughput screening. Nat Biotechnol. 2004;22:192–7.

65.Andanson J-M, Chan KLA, Kazarian SG. High-throughput spectroscopic imaging applied to permeation through the skin. Appl Spectrosc. 2009;63:512–7.

66.Karande P, Mitragotri S. Dependence of skin permeability on contact area. Pharm Res. 2003;20:257–63.

67.Pastore MN, Kalia YN, Horstmann M, Roberts MS. Transdermal patches: history, development and pharmacology. Br J Pharmacol. 2015;172:2179–209.

68.Gurtner GC, Werner S, Barrandon Y, Longaker MT. Wound repair and regeneration. Nature. 2008;453:314–21.

69.Falanga V. Wound healing and its impairment in the diabetic foot. Lancet. 2005;366:1736–43.

70.Li J, Chen J, Kirsner R. Pathophysiology of acute wound healing. Clin Dermatol. 2007;25:9–18.

71.Martin P. Wound healing–aiming for perfect skin regeneration. Science. 1997;276:75–81.

72.Raja SK, Garcia MS, Isseroff RR. Wound re-epithelialization: modulating keratinocyte migration in wound healing. Front Biosci. 2007;12:2849–68.

73.Zhao M. Electrical fields in wound healing—an overriding signal that directs cell migration. Semin Cell Dev Biol. 2009;20:674–82.

74.Rodero MP, Khosrotehrani K. Skin wound healing modulation by macrophages. Int J Clin Exp Pathol. 2010;3:643–53.

75.Carlson MW, Alt-Holland A, Egles C, Garlick JA. Three-dimensional tissue models of normal and diseased skin. Curr Protoc Cell Biol. 2008;41:1–17.

76.Liang C-C, Park AY, Guan J-L. In vitro scratch assay: a convenient and inexpensive method for analysis of cell migration in vitro. Nat Protoc. 2007;2:329–33.

77.Song S, Han H, Ko UH, Kim J, Shin JH. Collaborative effects of electric field and fluid shear stress on fibroblast migration. Lab Chip. 2013;13:1602–11.

78.Song B, Gu Y, Pu J, Reid B, Zhao Z, Zhao M. Application of direct current electric fields to cells and tissues in vitro and modulation of wound electric field in vivo. Nat Protoc. 2007;2:1479–89.

79.Pastar I, Liang L, Sawaya AP, Wikramanayake TC, Glinos GD, Drakulich S, et al. 10 - Preclinical models for wound-healing studies. In: Marques AP, Pirraco RP, Cerqueira MT, Reis RL (eds). Skin Tissue Models. Boston:Academic Press, 2018, 223–53.

80.Das AM, Eggermont AM, ten Hagen TL. A ring barrier-based migration assay to assess cell migration in vitro. Nat Protoc. 2015;10:904–15.

81.Boyden S. The chemotactic effect of mixtures of antibody and antigen on Polymorphonuclear leucocytes. Assessment. 1962;115:453–66.

82.Kohyama T, Ertl RF, Valenti V, Spurzem J, Kawamoto M, Nakamura Y, et al. Prostaglandin E(2) inhibits fibroblast chemotaxis. Am J Physiol Lung Cell Mol Physiol. 2001;281:L1257–63.

83.Monsuur HN, Boink MA, Weijers EM, Roffel S, Breetveld M, Gefen A, et al. Methods to study differences in cell mobility during skin wound healing in vitro. J Biomech. 2016;49:1381–7.

84.Seppä H, Grotendorst G, Seppä S, Schiffmann E, Martin GR. Platelet-derived growth factor in chemotactic for fibroblasts. J Cell Biol. 1982;92:584–8.

85.Küchler S, Wolf NB, Heilmann S, Weindl G, Helfmann J, Yahya MM, et al. 3D-wound healing model: influence of morphine and solid lipid nanoparticles. J Biotechnol. 2010;148:24–30.

86.Falanga V, Isaacs C, Paquette D, Downing G, Kouttab N, Butmarc J, et al. Wounding of bioengineered skin: cellular and molecular aspects after injury. J Invest Dermatol. 2002;119:653–60.

87.El Ghalbzouri A, Hensbergen P, Gibbs S, Kempenaar J. Schors Rvd, Ponec M. fibroblasts facilitate re-epithelialization in wounded human skin equivalents. Lab Investig. 2004;84:102–12.

88.Arciero JC, Mi Q, Branca MF, Hackam DJ, Swigon D. Continuum model of collective cell migration in wound healing and Colony expansion. Biophys J. 2011;100:535–43.

89.Ansell DM, Campbell L, Thomason HA, Brass A, Hardman MJ. A statistical analysis of murine incisional and excisional acute wound models. Wound Repair Regen. 2014;22:281–7.

90.Barbalho GN, Matos BN, Espirito Santo MEL, Silva VRC, Chaves SB, Gelfuso GM, et al. In vitro skin model for the evaluation of burn healing drug delivery systems. Journal of Drug Delivery Science and Technology. 2021;62:102330.

91.Iljas JD, Röhl J, McGovern JA, Moromizato KH, Parker TJ, Cuttle L. A human skin equivalent burn model to study the effect of a nanocrystalline silver dressing on wound healing. Burns. 2021;47:417–29.

92.Schneider V, Kruse D, de Mattos IB, Zöphel S, Tiltmann KK, Reigl A, et al. A 3D in vitro model for burn wounds: monitoring of regeneration on the epidermal level. Biomedicine. 2021;9:1153. https://doi.org/10.3390/biomedicines9091153.

93.Mastyugin V, McWhinnie E, Labow M, Buxton F. A quantitative high-throughput endothelial cell migration assay. J Biomol Screen. 2004;9:712–8.

94.Yarrow JC, Perlman ZE, Westwood NJ, Mitchison TJ. A high-throughput cell migration assay using scratch wound healing, a comparison of image-based readout methods. BMC Biotechnol. 2004;4:21.

95.Agilent. AccuWound 96 Scratch Tool. California, US: Agilent, 2022 Available from: https://www.agilent.com/en/product/cell-analysis/real-time-cell-analysis/rtca-reagents-kits-accessories/accuwound-96-scratch-tool-741238.

96.Nie F-Q, Yamada M, Kobayashi J, Yamato M, Kikuchi A, Okano T. On-chip cell migration assay using microfluidic channels. Biomaterials. 2007;28:4017–22.

97.Raj MK, Chakraborty S. PDMS microfluidics: a mini review. J Appl Polym Sci. 2020;137:48958.

98.Zordan MD, Mill CP, Riese DJ, Leary JF. A high throughput, interactive imaging, bright-field wound healing assay. Cytometry A. 2011;79:227–32.

99.Acosta S, Canclini L, Galarraga C, Justet C, Alem D. Lab-made 3D printed stoppers as high-throughput cell migration screening tool. SLAS Technology. 2022;27:39–43.

100.PromoCell. Introducing a novel high throughput 3D wound healing model. Heidelberg, Germany: Promo Cell, 2022 Available from: https://promocell.com/blog/introducing-a-novel-high-throughput-3d-wound-healing-model/.

101.OECD. Test No. 439: In Vitro Skin Irritation: Reconstructed Human Epidermis Test Method. OECDiLibrary, 2021. https://www.oecd-ilibrary.org/environment/test-no-439-in-vitro-skin-irritation-reconstructed-human-epidermis-test-method_9789264242845-en.

102.OECD. Test No. 431: In vitro skin corrosion: reconstructed human epidermis (RHE) test method. OECDiLibrary, 2019. https://www.oecd-ilibrary.org/environment/test-no-431-in-vitro-skin-corrosion-reconstructed-human-epidermis-rhe-test-method_9789264242753-en.

103.OECD. Test No. 442D: In Vitro Skin Sensitisation. OECDiLibrary, 2018. https://www.oecd-ilibrary.org/environment/test-no-442d-in-vitro-skin-sensitisation_9789264229822-en.

104.Oecd. OECD Guideline for the Testing of Chemicals. 430. In Vitro Skin Corrosion: Transcutaneous Electrical Resistance Test Method (TER). OECDiLibrary, 2015, 1–15. https://www.oecd-ilibrary.org/environment/test-no-430-in-vitro-skin-corrosion-transcutaneous-electrical-resistance-test-method-ter_9789264242739-en.

105.OECD. Test No. 435: In Vitro Membrane Barrier Test Method for Skin Corrosion. OECDiLibrary, 2015. https://www.oecd-ilibrary.org/environment/test-no-435-in-vitro-membrane-barrier-test-method-for-skincorrosion_9789264242791-en.

106.Regulation (EC) No 1223/2009 of the European Parliament and of the Council of 30 November 2009 on cosmetic products. European Union: Official Journal of the European Union, 2009.

107.Full EU ban on animal testing for cosmetics enters into force [press release]. Brussels, Belgium: European Comission, 11 March 2013, 2013.

108.OECD. Test No. 487: In Vitro Mammalian Cell Micronucleus Test. OECDiLibrary, 2016. https://www.oecd-ilibrary.org/environment/test-no-487-in-vitro-mammalian-cell-micronucleus-test_9789264264861-en.

109.Dahl EL, Curren R, Barnett BC, Khambatta Z, Reisinger K, Ouedraogo G, et al. The reconstructed skin micronucleus assay (RSMN) in EpiDerm™: detailed protocol and harmonized scoring atlas. Mutat Res. 2011;720:42–52.

110.EPISKIN. EpiSkin / Human Epidermis. Lyon, France: EPISKIN, 2022 Available from: https://www.episkin.com/Episkin.

111.MatTek. EpiDerm™. Oregon, US: MatTek, 2022 Available from: https://www.mattek.com/products/epiderm/.

112.EPISKIN. SkinEthic RHE / Human Epidermis. Lyon, France: EPISKIIN, 2022 Available from: https://www.episkin.com/SkinEthic-RHE.

113.phenion. Reconstructed Tissues. Düsseldorf, Alemanha: phenion, 2022 Available from: https://www.phenion.com/products/reconstructed-tissues#Tab-754224_5.

114.J-TEC. LabCyte EPI-MODEL. Japan: J-TECL, 2022 Available from: https://www.jpte.co.jp/en/business/LabCyte/epi-model/index.html.

115.OECD. Guidance Document on an Integrated Approach on Testing and Assessment (IATA) for Skin Corrosion and Irritation. OECDiLibrary, 2017. https://www.oecd-ilibrary.org/environment/guidance-document-on-an-integrated-approach-on-testing-and-assessment-iata-for-skin-corrosion-and-irritation_9789264274693-en.

116.Sterlab-Store. Human Reconstructed Epidermis. Vallauris, France: Sterlab-Store, 2022 Available from: https://www.sterlab-store.com/Products/reconstructed-tissues/epidermis/.

117.Biosolution. Skin model. Seoul, South Korea: Biosolution Co., Ltd., 2022 Available from: http://www.keraskin.co.kr/eng/product/skin_model.asp.

118.Mehling A, Adriaens E, Casati S, Hubesch B, Irizar A, Klaric M, et al. In vitro RHE skin sensitisation assays: applicability to challenging substances. Regul Toxicol Pharmacol. 2019;108:104473.

119.Natsch A, Emter R, Gfeller H, Haupt T, Ellis G. Predicting skin sensitizer potency based on in vitro data from KeratinoSens and kinetic peptide binding: global versus domain-based assessment. Toxicol Sci. 2014;143:319–32.

120.Bauch C, Kolle SN, Ramirez T, Eltze T, Fabian E, Mehling A, et al. Putting the parts together: combining in vitro methods to test for skin sensitizing potentials. Regul Toxicol Pharmacol. 2012;63:489–504.

121.Natsch A, Emter R, Ellis G. Filling the concept with data: integrating data from different in vitro and in Silico assays on skin sensitizers to explore the battery approach for animal-free skin sensitization testing. Toxicol Sci. 2008;107:106–21.

122.Huh D, Matthews BD, Mammoto A, Montoya-Zavala M, Hsin HY, Ingber DE. Reconstituting organ-level lung functions on a Chip. Science. 2010;328:1662–8.

123.Huh DD. A human breathing lung-on-a-chip. Ann Am Thorac Soc. 2015;12:S42–4.

124.Zamprogno P, Wüthrich S, Achenbach S, Thoma G, Stucki JD, Hobi N, et al. Second-generation lung-on-a-chip with an array of stretchable alveoli made with a biological membrane. Communications Biology. 2021;4:168.

125.Huang D, Liu T, Liao J, Maharjan S, Xie X, Pérez M, et al. Reversed-engineered human alveolar lung-on-a-chip model. Proc Natl Acad Sci. 2021;118:e2016146118.

126.Zhang M, Xu C, Jiang L, Qin JH. A 3D human lung-on-a-chip model for nanotoxicity testing. Toxicology Research. 2018;7:1048–60.

127.Huh D, Kim HJ, Fraser JP, Shea DE, Khan M, Bahinski A, et al. Microfabrication of human organs-on-chips. Nat Protoc. 2013;8:2135–57.

128.Benam KH, Villenave R, Lucchesi C, Varone A, Hubeau C, Lee HH, et al. Small airway-on-a-chip enables analysis of human lung inflammation and drug responses in vitro. Nat Methods. 2016;13:151–7.

129.Jang K-J, Suh K-Y. A multi-layer microfluidic device for efficient culture and analysis of renal tubular cells. Lab Chip. 2010;10:36–42.

130.Jang K-J, Mehr AP, Hamilton GA, McPartlin LA, Chung S, Suh K-Y, et al. Human kidney proximal tubule-on-a-chip for drug transport and nephrotoxicity assessment. Integr Biol. 2013;5:1119.

131.Rayner SG, Phong KT, Xue J, Lih D, Shankland SJ, Kelly EJ, et al. Reconstructing the human renal vascular-tubular unit in vitro. Adv Healthc Mater. 2018;7:1801120.

132.Musah S, Dimitrakak N, Camacho DM, Church GM, Ingber DE. Directed differentiation of human induced pluripotent stem cells into mature kidney podocytes and establishment of a glomerulus Chip. Nat Protoc. 2018;13:1662–85.

133.Nieskens TTG, Wilmer MJ. Kidney-on-a-chip technology for renal proximal tubule tissue reconstruction. Eur J Pharmacol. 2016;790:46–56.

134.Lee PJ, Hung PJ, Lee LP. An artificial liver sinusoid with a microfluidic endothelial-like barrier for primary hepatocyte culture. Biotechnol Bioeng. 2007;97:1340–6.

135.Lee H, Chae S, Kim JY, Han W, Kim J, Choi Y, et al. Cell-printed 3D liver-on-a-chip possessing a liver microenvironment and biliary system. Biofabrication. 2019;11:025001.

136.Prodanov L, Jindal R, Bale SS, Hegde M, McCarty WJ, Golberg I, et al. Long-term maintenance of a microfluidic 3D human liver sinusoid. Biotechnol Bioeng. 2016;113:241–6.

137.Choe A, Ha SK, Choi I, Choi N, Sung JH. Microfluidic gut-liver chip for reproducing the first pass metabolism. Biomed Microdevices. 2017;19:4.

138.Torisawa Y-S, Spina CS, Mammoto T, Mammoto A, Weaver JC, Tat T, et al. Bone marrow-on-a-chip replicates hematopoietic niche physiology in vitro. Nat Methods. 2014;11:663–9.

139.Kim J, Lee H, Selimovic S, Gauvin R, Bae H. Organ-on-A-Chip: development and clinical prospects toward toxicity assessment with an emphasis on bone marrow. Drug Saf. 2015;38:409–18.

140.Sieber S, Wirth L, Cavak N, Koenigsmark M, Marx U, Lauster R, et al. Bone marrow-on-a-chip: long-term culture of human haematopoietic stem cells in a three-dimensional microfluidic environment. J Tissue Eng Regen Med. 2018;12:479–89.

141.Kim HJ, Li H, Collins JJ, Ingber DE. Contributions of microbiome and mechanical deformation to intestinal bacterial overgrowth and inflammation in a human gut-on-a-chip. Proc Natl Acad Sci. 2016;113:201522193.

142.Ferreira DA, Rothbauer M, Conde JP, Ertl P, Oliveira C, Granja PL. A fast alternative to soft lithography for the fabrication of organ-on-a-Chip elastomeric-based devices and microactuators. Adv Sci. 2021;8:2003273.

143.Kim HJ, Huh D, Hamilton G, Ingber DE. Human gut-on-a-chip inhabited by microbial flora that experiences intestinal peristalsis-like motions and flow. Lab Chip. 2012;12:2165.

144.Shim KY, Lee D, Han J, Nguyen NT, Park S, Sung JH. Microfluidic gut-on-a-chip with three-dimensional villi structure. Biomed Microdevices. 2017;19:37.

145.Beaurivage C, Naumovska E, Chang YX, Elstak ED, Nicolas A, Wouters H, et al. Development of a gut-on-a-Chip model for high throughput disease Modeling and drug discovery. Int J Mol Sci. 2019;20:5661. https://doi.org/10.3390/ijms20225661.

146.Abaci HE, Gledhill K, Guo Z, Christiano AM, Shuler ML. Pumpless microfluidic platform for drug testing on human skin equivalents. Lab Chip. 2015;15:882–8.

147.Ataç B, Wagner I, Horland R, Lauster R, Marx U, Tonevitsky AG, et al. Skin and hair on-a-chip: in vitro skin models versus ex vivo tissue maintenance with dynamic perfusion. Lab Chip. 2013;13:3555–61.

148.Wufuer M, Lee G, Hur W, Jeon B, Kim BJ, Choi TH, et al. Skin-on-a-chip model simulating inflammation, edema and drug-based treatment. Sci Rep. 2016;6:37471.

149.Ramadan Q, Ting FCW. In vitro micro-physiological immune-competent model of the human skin. Lab Chip. 2016;16:1899–908.

150.Zhang J, Chen Z, Zhang Y, Wang X, Ouyang J, Zhu J, et al. Construction of a high fidelity epidermis-on-a-chip for scalable in vitro irritation evaluation. Lab Chip. 2021;21:3804–18.

151.Zajdel TJ, Shim G, Cohen DJ. Come together: on-chip bioelectric wound closure. Biosens Bioelectron. 2021;192:113479.

152.O'Neill AT, Monteiro-Riviere NA, Walker GM. Characterization of microfluidic human epidermal keratinocyte culture. Cytotechnology. 2008;56:197–207.

153.Kim L, Vahey MD, Lee H-Y, Voldman J. Microfluidic arrays for logarithmically perfused embryonic stem cell culture. Lab Chip. 2006;6:394.

154.Lu H, Koo LY, Wang WM. Lauffenburger Da, Griffith LG, Jensen KF. Microfluidic shear devices for quantitative analysis of cell adhesion. Anal Chem. 2004;76:5257–64.

155.Lin J-Y, Lo K-Y, Sun Y-S. A microfluidics-based wound-healing assay for studying the effects of shear stresses, wound widths, and chemicals on the wound-healing process. Sci Rep. 2019;9:20016.

156.Alexander FA, Eggert S, Wiest J. Skin-on-a-Chip: Transepithelial electrical resistance and extracellular acidification measurements through an automated air-liquid Interface. Genes. 2018;9:114. https://doi.org/10.3390/genes9020114.

157.Lukacs B, Bajza A, Kocsis D, Csorba A, Antal I, Ivan K, et al. Skin-on-a-Chip device for ex vivo monitoring of transdermal delivery of drugs-design, fabrication, and testing. Pharmaceutics. 2019;11:445.

158.Kim JJ, Ellett F, Thomas CN, Jalali F, Anderson RR, Irimia D, et al. A microscale, full-thickness, human skin on a chip assay simulating neutrophil responses to skin infection and antibiotic treatments. Lab Chip. 2019;19:3094–103.

159.Wagner I, Atac B, Lindner G, Horland R, Busek M, Sonntag F, et al. Skin and hair-on-a-chip: hair and skin assembly versus native skin maintenance in a chip-based perfusion system. BMC Proc. 2013;7:P93.

160.Maschmeyer I, Lorenz AK, Schimek K, Hasenberg T, Ramme AP, Hübner J, et al. A four-organ-chip for interconnected long-term co-culture of human intestine, liver, skin and kidney equivalents. Lab Chip. 2015;15:2688–99.

161.Maschmeyer I, Hasenberg T, Jaenicke A, Lindner M, Lorenz AK, Zech J, et al. Chip-based human liver-intestine and liver-skin co-cultures--a first step toward systemic repeated dose substance testing in vitro. Eur J Pharm Biopharm. 2015;95:77–87.

162.Huang W-Y, Huang J-P, Lin C-C, Lin Y-S. A transdermal measurement platform based on microfluidics. J Chem. 2017;2017:8.

163.Sriram G, Alberti M, Dancik Y, Wu B, Wu R, Feng Z, et al. Full-thickness human skin-on-chip with enhanced epidermal morphogenesis and barrier function. Mater Today. 2018;21:326–40.

164.Sasaki N, Tsuchiya K, Kobayashi H. Photolithography-free skin-on-a-Chip for parallel permeation assays. Sensors and Materials. 2019;31:107.

165.Jeon HM, Kim K, Choi KC, Sung GY. Side-effect test of sorafenib using 3-D skin equivalent based on microfluidic skin-on-a-chip. J Ind Eng Chem. 2020;82:71–80.

166.Jeon B, Lee G, Wufuer M, Huang Y, Choi Y, Kim S, et al. Enhanced predictive capacity using dual-parameter chip model that simulates physiological skin irritation. Toxicol in Vitro. 2020;68:104955.

167.Zoio P, Lopes-Ventura S, Oliva A. Barrier-on-a-Chip with a modular architecture and integrated sensors for real-time measurement of biological barrier function. Micromachines. 2021;12:816. https://doi.org/10.3390/mi12070816.

168.Kim K, Kim H, Sung GY. An Interleukin-4 and Interleukin-13 induced atopic dermatitis human skin equivalent model by a skin-on-A-Chip. Int J Mol Sci. 2022;23:2116. https://doi.org/10.3390/ijms23042116.

169.Lim HY, Kim J, Song HJ, Kim K, Choi KC, Park S, et al. Development of wrinkled skin-on-a-chip (WSOC) by cyclic uniaxial stretching. J Ind Eng Chem. 2018;68:238–45.

170.Kwak BS, Jin SP, Kim SJ, Kim EJ, Chung JH, Sung JH. Microfluidic skin chip with vasculature for recapitulating the immune response of the skin tissue. Biotechnol Bioeng. 2020;117:1853–63.

171.Trinh KTL, Thai DA, Chae WR, Lee NY. Rapid fabrication of poly(methyl methacrylate) devices for lab-on-a-Chip applications using acetic acid and UV treatment. ACS Omega. 2020;5:17396–404.

172.Sun Y-S, Peng S-W, Cheng J-Y. In vitro electrical-stimulated wound-healing chip for studying electric field-assisted wound-healing process. Biomicrofluidics. 2012;6:34117.

173.Miller JS, Stevens KR, Yang MT, Baker BM, Nguyen D-HT, Cohen DM, et al. Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues. Nat Mater. 2012;11:768–74.

174.Bhise NS, Manoharan V, Massa S, Tamayol A, Ghaderi M, Miscuglio M, et al. A liver-on-a-chip platform with bioprinted hepatic spheroids. Biofabrication. 2016;8:014101.

175.Lee H, Cho D-W. One-step fabrication of an organ-on-a-chip with spatial heterogeneity using a 3D bioprinting technology. Lab Chip. 2016;16:2618–25.

176.Skardal A, Murphy SV, Devarasetty M, Mead I, Kang H-W, Seol Y-J, et al. Multi-tissue interactions in an integrated three-tissue organ-on-a-chip platform. Sci Rep. 2017;7:8837.

177.Pereira RF, Sousa A, Barrias CC, Bártolo PJ, Granja PL. A single-component hydrogel bioink for bioprinting of bioengineered 3D constructs for dermal tissue engineering. Materials Horizons. 2018;5:1100–11.

178.Pereira RF, Lourenço BN, Bártolo PJ, Granja PL. Bioprinting a multifunctional bioink to engineer clickable 3D cellular niches with Tunable matrix microenvironmental cues. Adv Healthc Mater. 2021;10:2001176.

179.Song HJ, Lim HY, Chun W, Choi KC, Sung JH, Sung GY. Fabrication of a pumpless, microfluidic skin chip from different collagen sources. J Ind Eng Chem. 2017;56:375–81.

180.Lee S, Jin S-P, Kim YK, Sung GY, Chung JH, Sung JH. Construction of 3D multicellular microfluidic chip for an in vitro skin model. Biomed Microdevices. 2017;19:22.

181.Song HJ, Lim HY, Chun W, Choi KC, Lee T-Y, Sung JH, et al. Development of 3D skin-equivalent in a pump-less microfluidic chip. J Ind Eng Chem. 2018;60:355–9.

182.Gupta S, Patel L, Mitra K, Bit A. Fibroblast derived skin wound healing Modeling on Chip under the influence of micro-capillary shear stress. Micromachines. 2022;13:305. https://doi.org/10.3390/mi13020305.

查看原文

浏览量

下载量

CSCD

文章被引用时，请邮件提醒。

提交

工具集

关联资源

Metabolic reprogramming in skin wound healing

A single-stage bilayered skin reconstruction using Glyaderm® as an acellular dermal regeneration template results in improved scar quality: an intra-individual randomized controlled trial

Amphibian-derived peptide homodimer OA-GL17d promotes skin wound regeneration through the miR-663a/TGF-β1/Smad axis

Vascularization is the next challenge for skin tissue engineering as a solution for burn management

PC4 serves as a negative regulator of skin wound healing in mice