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Published in: Inflammation 2/2024

Open Access 27-12-2023 | Atopic Dermatitis | RESEARCH

Characterization of Different Inflammatory Skin Conditions in a Mouse Model of DNCB-Induced Atopic Dermatitis

Authors: Rebecca Riedl, Annika Kühn, Yvonne Hupfer, Betty Hebecker, Lukas K. Peltner, Paul M. Jordan, Oliver Werz, Stefan Lorkowski, Cornelia Wiegand, Maria Wallert

Published in: Inflammation | Issue 2/2024

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Abstract

The mouse model of 2,4-dinitrochlorbenzene (DNCB)-induced human-like atopic dermatitis (hlAD) has been widely used to test novel treatment strategies and compounds. However, the study designs and methods are highly diverse, presenting different hlAD disease patterns that occur after sensitization and repeated challenge with DNCB on dorsal skin. In addition, there is a lack of information about the progression of the disease during the experiment and the achieved pheno- and endotypes, especially at the timepoint when therapeutic treatment is initiated. We here examine hlAD in a DNCB-induced BALB/cJRj model at different timepoints: (i) before starting treatment with dexamethasone, representing a standard drug control (day 12) and (ii) at the end of the experiment (day 22). Both timepoints display typical AD-associated characteristics: skin thickening, spongiosis, hyper- and parakeratosis, altered cytokine and gene expression, increased lipid mediator formation, barrier protein and antimicrobial peptide abnormalities, as well as lymphoid organ hypertrophy. Increased mast cell infiltration into the skin and elevated immunoglobulin E plasma concentrations indicate a type I allergy response. The DNCB-treated skin showed an extrinsic moderate sub-acute hlAD lesion at day 12 and an extrinsic mild sub-acute to chronic pheno- and endotype at day 22 with a dominating Th2 response. A dependency of the filaggrin formation and expression in correlation to the disease severity in the DNCB-treated skin was found. In conclusion, our study reveals a detailed classification of a hlAD at two timepoints with different inflammatory skin conditions and pheno- and endotypes, thereby providing a better understanding of the DNCB-induced hlAD model in BALB/cJRj mice.
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Literature
6.
go back to reference Schonmann, Y., Mansfield, K. E., Hayes, J. F., Abuabara, K., Roberts, A., Smeeth, L., and Langan, S. M. 2020. Atopic eczema in adulthood and risk of depression and anxiety: a population-based cohort study. The Journal of Allergy and Clinical Immunology: In Practice 8, 248–257.e16. https://doi.org/10.1016/j.jaip.2019.08.030. Schonmann, Y., Mansfield, K. E., Hayes, J. F., Abuabara, K., Roberts, A., Smeeth, L., and Langan, S. M. 2020. Atopic eczema in adulthood and risk of depression and anxiety: a population-based cohort study. The Journal of Allergy and Clinical Immunology: In Practice 8, 248–257.e16. https://​doi.​org/​10.​1016/​j.​jaip.​2019.​08.​030.
7.
go back to reference Thyssen, J.P., C.R. Hamann, A. Linneberg, T.M. Dantoft, L. Skov, G.H. Gislason, J.J. Wu, and A. Egeberg. 2018. Atopic Dermatitis is associated with anxiety, depression, and suicidal ideation, but not with psychiatric hospitalization or suicide. Allergy 73: 214–220. https://doi.org/10.1111/all.13231.CrossRefPubMed Thyssen, J.P., C.R. Hamann, A. Linneberg, T.M. Dantoft, L. Skov, G.H. Gislason, J.J. Wu, and A. Egeberg. 2018. Atopic Dermatitis is associated with anxiety, depression, and suicidal ideation, but not with psychiatric hospitalization or suicide. Allergy 73: 214–220. https://​doi.​org/​10.​1111/​all.​13231.CrossRefPubMed
13.
go back to reference Gawkrodger, D.J., M. Haftek, P.A. Botham, M.M. Carr, M.-J. Spencer, J.A. Ross, J.A.A. Hunter, and J. Thivolet. 1989. The hapten in contact hypersensitivity to dinitrochlorobenzene: Immunoelectron microscopic and immunofluorescent studies. Dermatology 178: 126–130. https://doi.org/10.1159/000248409.CrossRef Gawkrodger, D.J., M. Haftek, P.A. Botham, M.M. Carr, M.-J. Spencer, J.A. Ross, J.A.A. Hunter, and J. Thivolet. 1989. The hapten in contact hypersensitivity to dinitrochlorobenzene: Immunoelectron microscopic and immunofluorescent studies. Dermatology 178: 126–130. https://​doi.​org/​10.​1159/​000248409.CrossRef
15.
go back to reference Hou, D.-D.; Di, Z.-H.; Qi, R.-Q.; Wang, H.-X.; Zheng, S.; Hong, Y.-X.; Guo, H.; Chen, H.-D.; Gao, X.-H. Sea Buckthorn (Hippophaë Rhamnoides L.) Oil improves atopic dermatitis-like skin lesions via inhibition of NF-κB and STAT1 activation. Skin Pharmacol Physiol 2017, 30, 268–276. https://doi.org/10.1159/000479528. Hou, D.-D.; Di, Z.-H.; Qi, R.-Q.; Wang, H.-X.; Zheng, S.; Hong, Y.-X.; Guo, H.; Chen, H.-D.; Gao, X.-H. Sea Buckthorn (Hippophaë Rhamnoides L.) Oil improves atopic dermatitis-like skin lesions via inhibition of NF-κB and STAT1 activation. Skin Pharmacol Physiol 2017, 30, 268–276. https://​doi.​org/​10.​1159/​000479528.
17.
go back to reference Kim, S.R., H.-S. Choi, H.S. Seo, J.M. Ku, S.H. Hong, H.H. Yoo, Y.C. Shin, and S.-G. Ko. 2014. Oral administration of herbal mixture extract inhibits 2,4-dinitrochlorobenzene-induced atopic dermatitis in BALB/c mice. Mediators of Inflammation 2014: 1–10. https://doi.org/10.1155/2014/319438.CrossRef Kim, S.R., H.-S. Choi, H.S. Seo, J.M. Ku, S.H. Hong, H.H. Yoo, Y.C. Shin, and S.-G. Ko. 2014. Oral administration of herbal mixture extract inhibits 2,4-dinitrochlorobenzene-induced atopic dermatitis in BALB/c mice. Mediators of Inflammation 2014: 1–10. https://​doi.​org/​10.​1155/​2014/​319438.CrossRef
23.
go back to reference Yang, H., C. Ahn, I.-G. Choi, W.-S. Choi, M.-J. Park, S.-S. Lee, D.-H. Choi, and E.-B. Jeung. 2015. Estimation of the environmental effect of natural volatile organic compounds from Chamaecyparis obtusa and their effect on atopic dermatitis-like skin lesions in mice. Molecular Medicine Reports 12: 345–350. https://doi.org/10.3892/mmr.2015.3431.CrossRefPubMed Yang, H., C. Ahn, I.-G. Choi, W.-S. Choi, M.-J. Park, S.-S. Lee, D.-H. Choi, and E.-B. Jeung. 2015. Estimation of the environmental effect of natural volatile organic compounds from Chamaecyparis obtusa and their effect on atopic dermatitis-like skin lesions in mice. Molecular Medicine Reports 12: 345–350. https://​doi.​org/​10.​3892/​mmr.​2015.​3431.CrossRefPubMed
30.
35.
go back to reference Bak, D.-H., E. Lee, B.C. Lee, M.J. Choi, T.-R. Kwon, J. Hong, S. Mun, K. Lee, S. Kim, J. Na, et al. 2019. Therapeutic potential of topically administered γ-AlOOH on 2,4-dinitrochlorobenzene-induced atopic dermatitis-like lesions in Balb/c mice. Experimental Dermatology 28: 169–176. https://doi.org/10.1111/exd.13865.CrossRefPubMed Bak, D.-H., E. Lee, B.C. Lee, M.J. Choi, T.-R. Kwon, J. Hong, S. Mun, K. Lee, S. Kim, J. Na, et al. 2019. Therapeutic potential of topically administered γ-AlOOH on 2,4-dinitrochlorobenzene-induced atopic dermatitis-like lesions in Balb/c mice. Experimental Dermatology 28: 169–176. https://​doi.​org/​10.​1111/​exd.​13865.CrossRefPubMed
37.
go back to reference Wollenberg, A., S. Christen-Zäch, A. Taieb, C. Paul, J.P. Thyssen, M. De Bruin-Weller, C. Vestergaard, J. Seneschal, T. Werfel, M.J. Cork, et al. 2020. ETFAD/EADV Eczema Task Force 2020 Position Paper on diagnosis and treatment of atopic dermatitis in adults and children. Acad Dermatol Venereol 34: 2717–2744. https://doi.org/10.1111/jdv.16892.CrossRef Wollenberg, A., S. Christen-Zäch, A. Taieb, C. Paul, J.P. Thyssen, M. De Bruin-Weller, C. Vestergaard, J. Seneschal, T. Werfel, M.J. Cork, et al. 2020. ETFAD/EADV Eczema Task Force 2020 Position Paper on diagnosis and treatment of atopic dermatitis in adults and children. Acad Dermatol Venereol 34: 2717–2744. https://​doi.​org/​10.​1111/​jdv.​16892.CrossRef
42.
go back to reference Gittler, J.K., Shemer, A., Suárez-Fariñas, M., Fuentes-Duculan, J., Gulewicz, K.J., Wang, C.Q.F., Mitsui, H., Cardinale, I., de Guzman Strong, C., Krueger, J.G., et al. 2012. Progressive activation of TH2/TH22 cytokines and selective epidermal proteins characterizes acute and chronic atopic dermatitis. Journal of Allergy and Clinical Immunology 130: 1344–1354. https://doi.org/10.1016/j.jaci.2012.07.012. Gittler, J.K., Shemer, A., Suárez-Fariñas, M., Fuentes-Duculan, J., Gulewicz, K.J., Wang, C.Q.F., Mitsui, H., Cardinale, I., de Guzman Strong, C., Krueger, J.G., et al. 2012. Progressive activation of TH2/TH22 cytokines and selective epidermal proteins characterizes acute and chronic atopic dermatitis. Journal of Allergy and Clinical Immunology  130: 1344–1354. https://​doi.​org/​10.​1016/​j.​jaci.​2012.​07.​012.
61.
go back to reference An, H.-J., J.-Y. Kim, W.-H. Kim, M.-G. Gwon, H.M. Gu, M.J. Jeon, S.-M. Han, S.C. Pak, C.-K. Lee, I.S. Park, et al. 2018. Therapeutic effects of bee venom and its major component, melittin, on atopic dermatitis in vivo and in vitro: Effects of bee venom and melittin on atopic eczema. British Journal of Pharmacology 175: 4310–4324. https://doi.org/10.1111/bph.14487.CrossRefPubMedPubMedCentral An, H.-J., J.-Y. Kim, W.-H. Kim, M.-G. Gwon, H.M. Gu, M.J. Jeon, S.-M. Han, S.C. Pak, C.-K. Lee, I.S. Park, et al. 2018. Therapeutic effects of bee venom and its major component, melittin, on atopic dermatitis in vivo and in vitro: Effects of bee venom and melittin on atopic eczema. British Journal of Pharmacology 175: 4310–4324. https://​doi.​org/​10.​1111/​bph.​14487.CrossRefPubMedPubMedCentral
62.
65.
go back to reference Coffman, R.L., and J. Carty. 1986. A T cell activity that enhances polyclonal IgE production and its inhibition by interferon-gamma. The Journal of Immunology 136: 949–954.CrossRefPubMed Coffman, R.L., and J. Carty. 1986. A T cell activity that enhances polyclonal IgE production and its inhibition by interferon-gamma. The Journal of Immunology 136: 949–954.CrossRefPubMed
68.
go back to reference Yamanaka, K., and Mizutani, H. 2011. The role of cytokines/chemokines in the pathogenesis of atopic dermatitis. In Current Problems in Dermatology; Shiohara, T., Ed.; S. Karger AG, Vol. 41, pp. 80–92 ISBN 978–3–8055–9686–2. Yamanaka, K., and Mizutani, H. 2011. The role of cytokines/chemokines in the pathogenesis of atopic dermatitis. In Current Problems in Dermatology; Shiohara, T., Ed.; S. Karger AG, Vol. 41, pp. 80–92 ISBN 978–3–8055–9686–2.
74.
go back to reference Gambichler, T., M. Skrygan, N.S. Tomi, N. Othlinghaus, N.H. Brockmeyer, P. Altmeyer, and A. Kreuter. 2008. Differential mRNA expression of antimicrobial peptides and proteins in atopic dermatitis as compared to psoriasis vulgaris and healthy skin. International Archives of Allergy and Immunology 147: 17–24. https://doi.org/10.1159/000128582.CrossRefPubMed Gambichler, T., M. Skrygan, N.S. Tomi, N. Othlinghaus, N.H. Brockmeyer, P. Altmeyer, and A. Kreuter. 2008. Differential mRNA expression of antimicrobial peptides and proteins in atopic dermatitis as compared to psoriasis vulgaris and healthy skin. International Archives of Allergy and Immunology 147: 17–24. https://​doi.​org/​10.​1159/​000128582.CrossRefPubMed
75.
go back to reference Di Rosa, M., Persico, P., Carnuccio, R., and Pinto, A. 1980. Mechanism of inhibition of prostaglandin biosynthesis by anti-inflammatory steroids. In Inflammation: Mechanisms and Treatment; Willoughby, D.A., Giroud, J.P., Eds.; Springer Netherlands: Dordrecht, pp. 261–265 ISBN 978–94–010–9425–2. Di Rosa, M., Persico, P., Carnuccio, R., and Pinto, A. 1980. Mechanism of inhibition of prostaglandin biosynthesis by anti-inflammatory steroids. In Inflammation: Mechanisms and Treatment; Willoughby, D.A., Giroud, J.P., Eds.; Springer Netherlands: Dordrecht, pp. 261–265 ISBN 978–94–010–9425–2.
77.
go back to reference Weisshaar, E., Bentz, P., Apfelbacher, C., Haufe, E., Heinrich, L., Heratizadeh, A., et al. 2023. Itching in atopic dermatitis: patient- and physician-reported outcomes in the German Atopic Dermatitis Registry TREATgermany. Acta Derm Venereol 2023, 103: adv00854. https://doi.org/10.2340/actadv.v103.4426. Weisshaar, E., Bentz, P., Apfelbacher, C., Haufe, E., Heinrich, L., Heratizadeh, A., et al. 2023. Itching in atopic dermatitis: patient- and physician-reported outcomes in the German Atopic Dermatitis Registry TREATgermany. Acta Derm Venereol 2023, 103: adv00854. https://​doi.​org/​10.​2340/​actadv.​v103.​4426.
80.
go back to reference FELASA working group on revision of guidelines for health monitoring of rodents and rabbits; Mähler (Convenor), M., Berard, M., Feinstein, R., Gallagher, A., Illgen-Wilcke, B., Pritchett-Corning, K., and Raspa, M. 2014. FELASA Recommendations for the health monitoring of mouse, rat, hamster, guinea pig and rabbit colonies in breeding and experimental units. Laboratory Animals 48: 178–192. https://doi.org/10.1177/0023677213516312. FELASA working group on revision of guidelines for health monitoring of rodents and rabbits; Mähler (Convenor), M., Berard, M., Feinstein, R., Gallagher, A., Illgen-Wilcke, B., Pritchett-Corning, K., and Raspa, M. 2014. FELASA Recommendations for the health monitoring of mouse, rat, hamster, guinea pig and rabbit colonies in breeding and experimental units. Laboratory Animals 48: 178–192. https://​doi.​org/​10.​1177/​0023677213516312​.
81.
Metadata
Title
Characterization of Different Inflammatory Skin Conditions in a Mouse Model of DNCB-Induced Atopic Dermatitis
Authors
Rebecca Riedl
Annika Kühn
Yvonne Hupfer
Betty Hebecker
Lukas K. Peltner
Paul M. Jordan
Oliver Werz
Stefan Lorkowski
Cornelia Wiegand
Maria Wallert
Publication date
27-12-2023
Publisher
Springer US
Published in
Inflammation / Issue 2/2024
Print ISSN: 0360-3997
Electronic ISSN: 1573-2576
DOI
https://doi.org/10.1007/s10753-023-01943-x

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