Use of D-Squame® as a Minimally Invasive Technique to Evaluate Skin Immune Response Biomarkers in Canine Atopic Dermatitis †
Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Ethical Considerations
2.2. Animals
2.2.1. Experimental Model of Canine AD
2.2.2. Dogs Affected Spontaneously with AD
2.3. Study Design
2.3.1. Epicutaneous Sensitization with Dermatophagoides farinae
2.3.2. Stratum Corneum Sample Collection
2.3.3. Cytokines Analysis
2.4. Statistical Methods
3. Results
3.1. Animals
3.2. Sensitization of the Experimental Model of Canine AD
3.3. Total Amount of Proteins and Total Amount of Soluble Proteins
3.3.1. Total Amount of Proteins
3.3.2. Total Amount of Soluble Proteins
3.4. Cytokine Analysis
3.4.1. Canine Experimental Model of AD (Figure 7)
Innate Immune Responses (Alarmins)
Adaptative Immune Responses (Th1)
Adaptative Immune Responses (Th2)
3.4.2. Dogs Spontaneously Affected with Canine AD (Figure 8)
Innate Immune Responses (Alarmins)
Adaptative Immune Responses (Th1)
Adaptative Immune Responses (Th2)
3.4.3. Ratio of Increase
3.5. Effects on Dogs
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Hillier, A.; Griffin, C.E. The ACVD task force on canine atopic dermatitis (X): Is there a relationship between canine atopic dermatitis and cutaneous adverse food reactions? Vet. Immunol. Immunopathol. 2001, 81, 227–231. [Google Scholar] [CrossRef] [PubMed]
- Drechsler, Y.; Dong, C.; Clark, D.E.; Kaur, G. Canine Atopic Dermatitis: Prevalence, Impact, and Management Strategies. Vet. Med. Res. Rep. 2024, 15, 15–29. [Google Scholar] [CrossRef] [PubMed]
- Weidinger, S.; Novak, N. Atopic dermatitis. Lancet 2016, 387, 1109–1122. [Google Scholar] [CrossRef] [PubMed]
- Biomarkers Definitions Working Group. Biomarkers and surrogate endpoints: Preferred definitions and conceptual framework. Clin. Pharmacol. Ther. 2001, 69, 89–95. [Google Scholar] [CrossRef]
- FDA-NIH Biomarker Working Group. BEST (Biomarkers, EndpointS, and Other Tools) Resource; Food and Drug Administration: Silver Spring, MD, USA, 2016. Available online: http://www.ncbi.nlm.nih.gov/books/NBK326791/ (accessed on 23 July 2024).
- Martins, G.D.C.; de Oliveira Melo Júnior, O.A.; Botoni, L.S.; Nogueira, M.M.; da Costa Val, A.P.; Blanco, B.S.; Dutra, W.O.; Giunchetti, R.C.; Melo, M.M.; da Silveira Lemos, D. Clinical-pathological and immunological biomarkers in dogs with atopic dermatitis. Vet. Immunol. Immunopathol. 2018, 205, 58–64. [Google Scholar] [CrossRef]
- Olivry, T.; Mayhew, D.; Paps, J.S.; Linder, K.E.; Peredo, C.; Rajpal, D.; Hofland, H.; Cote-Sierra, J. Early Activation of Th2/Th22 Inflammatory and Pruritogenic Pathways in Acute Canine Atopic Dermatitis Skin Lesions. J. Investig. Dermatol. 2016, 136, 1961–1969. [Google Scholar] [CrossRef]
- Tamamoto-Mochizuki, C.; Santoro, D.; Saridomikelakis, M.N.; Eisenschenk, M.N.C.; Hensel, P.; Pucheu-Haston, C. Update on the role of cytokines and chemokines in canine atopic dermatitis. Vet. Dermatol. 2024, 35, 25–39. [Google Scholar] [CrossRef]
- Kanwal, S.; Singh, S.K.; Soman, S.P.; Choudhury, S.; Kumari, P.; Ram, P.K.; Garg, S.K. Expression of barrier proteins in the skin lesions and inflammatory cytokines in peripheral blood mononuclear cells of atopic dogs. Sci. Rep. 2021, 11, 11418. [Google Scholar] [CrossRef]
- Koury, J.; Ramirez, A.; Xie, C.; Harb, J.; Dong, C.; Maki, C.; Ramos, T.; Izadyar, F.; Clark, D.; Drechsler, Y.; et al. Phosphodiesterase 4D, miR-203 and selected cytokines in the peripheral blood are associated with canine atopic dermatitis. PLoS ONE 2019, 14, e0218670. [Google Scholar] [CrossRef]
- Majewska, A.; Gajewska, M.; Dembele, K.; Maciejewski, H.; Prostek, A.; Jank, M. Lymphocytic, cytokine and transcriptomic profiles in peripheral blood of dogs with atopic dermatitis. BMC Vet. Res. 2016, 12, 174. [Google Scholar] [CrossRef]
- Kaur, G.; Xie, C.; Dong, C.; Najera, J.; Nguyen, J.T.; Hao, J. PDE4D and miR-203 are promising biomarkers for canine atopic dermatitis. Mol. Biol. Rep. 2024, 51, 651. [Google Scholar] [CrossRef] [PubMed]
- Asahina, R.; Ueda, K.; Oshima, Y.; Kanei, T.; Kato, M.; Furue, M.; Tsukui, T.; Nagata, M.; Maeda, S. Serum canine thymus and activation-regulated chemokine (TARC/CCL17) concentrations correlate with disease severity and therapeutic responses in dogs with atopic dermatitis. Vet. Dermatol. 2020, 31, 446–455. [Google Scholar] [CrossRef] [PubMed]
- Kakinuma, T.; Nakamura, K.; Wakugawa, M.; Mitsui, H.; Tada, Y.; Saeki, H.; Torii, H.; Asahina, A.; Onai, N.; Matsushima, K.; et al. Thymus and activation-regulated chemokine in atopic dermatitis: Serum thymus and activation-regulated chemokine level is closely related with disease activity. J. Allergy Clin. Immunol. 2001, 107, 535–541. [Google Scholar] [CrossRef] [PubMed]
- Borek, F.; Nagashima, S.; Villalobos, W.R.; Gmyterco, V.C.; Sell, T.; de Farias, M.R.; Bechara, G.H. Immunoexpression of IL-33 in the different clinical aspects of canine atopic dermatitis. Vet. Immunol. Immunopathol. 2024, 273, 110786. [Google Scholar] [CrossRef] [PubMed]
- Chung, T.-H.; Oh, J.-S.; Lee, Y.-S.; Kang, K.-S.; Jung, J.-W.; Youn, H.-Y.; Hwang, C.-Y. Elevated Serum Levels of S100 Calcium Binding Protein A8 (S100A8) Reflect Disease Severity in Canine Atopic Dermatitis. J. Vet. Med. Sci. 2010, 72, 693–700. [Google Scholar] [CrossRef]
- Wood, S.H.; Clements, D.N.; Ollier, W.E.; Nuttall, T.; McEwan, N.A.; Carter, S.D. Gene expression in canine atopic dermatitis and correlation with clinical severity scores. J. Dermatol. Sci. 2009, 55, 27–33. [Google Scholar] [CrossRef]
- Guttman-Yassky, E.; Diaz, A.; Pavel, A.B.; Fernandes, M.; Lefferdink, R.; Erickson, T.; Canter, T.; Rangel, S.; Peng, X.; Li, R.; et al. Use of Tape Strips to Detect Immune and Barrier Abnormalities in the Skin of Children With Early-Onset Atopic Dermatitis. JAMA Dermatol. 2019, 155, 1358–1370. [Google Scholar] [CrossRef]
- Hulshof, L.; Hack, D.P.; Hasnoe, Q.C.J.; Dontje, B.; Jakasa, I.; Riethmüller, C.; McLean, W.H.I.; van Aalderen, W.M.; van’t Land, B.; Kezic, S.; et al. A minimally invasive tool to study immune response and skin barrier in children with atopic dermatitis. Br. J. Dermatol. 2019, 180, 621–630. [Google Scholar] [CrossRef]
- Andersson, A.M.; Sølberg, J.; Koch, A.; Skov, L.; Jakasa, I.; Kezic, S.; Thyssen, J.P. Assessment of biomarkers in pediatric atopic dermatitis by tape strips and skin biopsies. Allergy 2022, 77, 1499–1509. [Google Scholar] [CrossRef]
- Clausen, M.-L.; Kezic, S.; Olesen, C.M.; Agner, T. Cytokine concentration across the stratum corneum in atopic dermatitis and healthy controls. Sci. Rep. 2020, 10, 21895. [Google Scholar] [CrossRef]
- Lyubchenko, T.; Collins, H.K.; Goleva, E.; Leung, D.Y.M. Skin tape sampling technique identifies proinflammatory cytokines in atopic dermatitis skin. Ann. Allergy. Asthma. Immunol. 2021, 126, 46–53.e2. [Google Scholar] [CrossRef] [PubMed]
- McEwan, N.A.; Lu, Y.-F.; Nuttall, T. A two-dimensional morphological study of corneocytes from healthy dogs and cats and from dogs with atopic dermatitis. Vet. Dermatol. 2009, 20, 360–368. [Google Scholar] [CrossRef] [PubMed]
- Mosca, M.; Legain, M.; Noël, G.; Idée, A.; Pin, D. Macroscopic Skin Examination Can Determine the Number of Strips Necessary to Study the stratum corneum in Dogs. Vet. Sci. 2023, 10, 547. [Google Scholar] [CrossRef]
- Favrot, C.; Steffan, J.; Seewald, W.; Picco, F. A prospective study on the clinical features of chronic canine atopic dermatitis and its diagnosis. Vet. Dermatol. 2010, 21, 23–31. [Google Scholar] [CrossRef]
- Panzuti, P.; Mosca, M.; Milhau, N.; Sabry, H.; Mutez, V.; Gamradt, P.; Vocanson, M.; Nicolas, J.F.; Pin, D. Abstracts of the 30th Annual Congress of the ECVD-ESVD, 27–29 September 2018, Dubrovnik, Croatia. Vet. Dermatol. 2018, 29, 355–374. [Google Scholar] [CrossRef]
- Hennino, A.; Vocanson, M.; Toussaint, Y.; Rodet, K.; Benetière, J.; Schmitt, A.-M.; Aries, M.-F.; Bérard, F.; Rozières, A.; Nicolas, J.-F. Skin-Infiltrating CD8+ T Cells Initiate Atopic Dermatitis Lesions1. J. Immunol. 2007, 178, 5571–5577. [Google Scholar] [CrossRef]
- Antweiler, R.C.; Taylor, H.E. Evaluation of Statistical Treatments of Left-Censored Environmental Data using Coincident Uncensored Data Sets: I. Summary Statistics. Environ. Sci. Technol. 2008, 42, 3732–3738. [Google Scholar] [CrossRef]
- Dapic, I.; Jakasa, I.; Yau, N.L.H.; Kezic, S.; Kammeyer, A. Evaluation of an HPLC Method for the Determination of Natural Moisturizing Factors in the Human Stratum Corneum. Anal. Lett. 2013, 46, 2133–2144. [Google Scholar] [CrossRef]
- Breternitz, M.; Flach, M.; Präßler, J.; Elsner, P.; Fluhr, J.W. Acute barrier disruption by adhesive tapes is influenced by pressure, time and anatomical location: Integrity and cohesion assessed by sequential tape stripping; a randomized, controlled study. Br. J. Dermatol. 2007, 156, 231–240. [Google Scholar] [CrossRef]
- Clausen, M.-L.; Slotved, H.-C.; Krogfelt, K.A.; Agner, T. Tape Stripping Technique for Stratum Corneum Protein Analysis. Sci. Rep. 2016, 6, 19918. [Google Scholar] [CrossRef]
- Clausen, M.-L.; Jungersted, J.M.; Andersen, P.S.; Slotved, H.-C.; Krogfelt, K.A.; Agner, T. Human β-defensin-2 as a marker for disease severity and skin barrier properties in atopic dermatitis. Br. J. Dermatol. 2013, 169, 587–593. [Google Scholar] [CrossRef] [PubMed]
- Røpke, M.A.; Mekulova, A.; Pipper, C.; Eisen, M.; Pender, K.; Spee, P.; Kezic, S. Non-invasive assessment of soluble skin surface biomarkers in atopic dermatitis patients—Effect of treatment. Skin Res. Technol. 2021, 27, 715–722. [Google Scholar] [CrossRef] [PubMed]
- De Jongh, C.M.; Verberk, M.M.; Spiekstra, S.W.; Gibbs, S.; Kezic, S. Cytokines at different stratum corneum levels in normal and sodium lauryl sulphate-irritated skin. Skin Res. Technol. 2007, 13, 390–398. [Google Scholar] [CrossRef] [PubMed]
- Clausen, M.-L.; Slotved, H.-C.; Krogfelt, K.A.; Agner, T. Measurements of AMPs in stratum corneum of atopic dermatitis and healthy skin–tape stripping technique. Sci. Rep. 2018, 8, 1666. [Google Scholar] [CrossRef] [PubMed]
- Kim, S.-W.; Kim, J.-H. Establishing an experimental model for canine atopic dermatitis through epicutaneous application of Dermatophagoides farinae. Front. Vet. Sci. 2022, 9, 1015915. [Google Scholar] [CrossRef]
- Marsella, R.; Olivry, T.; Maeda, S. Cellular and cytokine kinetics after epicutaneous allergen challenge (atopy patch testing) with house dust mites in high-IgE beagles. Vet. Dermatol. 2006, 17, 111–120. [Google Scholar] [CrossRef]
- Pucheu-Haston, C.M.; Shuster, D.; Olivry, T.; Brianceau, P.; Lockwood, P.; McClanahan, T.; Malefyt, R.d.W.; Mattson, J.D.; Hammerberg, B. A canine model of cutaneous late-phase reactions: Prednisolone inhibition of cellular and cytokine responses. Immunology 2006, 117, 177–187. [Google Scholar] [CrossRef]
- McCandless, E.E.; Rugg, C.A.; Fici, G.J.; Messamore, J.E.; Aleo, M.M.; Gonzales, A.J. Allergen-induced production of IL-31 by canine Th2 cells and identification of immune, skin, and neuronal target cells. Vet. Immunol. Immunopathol. 2014, 157, 42–48. [Google Scholar] [CrossRef]
- Schlotter, Y.M.; Rutten, V.P.M.G.; Riemers, F.M.; Knol, E.F.; Willemse, T. Lesional skin in atopic dogs shows a mixed Type-1 and Type-2 immune responsiveness. Vet. Immunol. Immunopathol. 2011, 143, 20–26. [Google Scholar] [CrossRef]
- Maeda, S.; Fujiwara, S.; Omori, K.; Kawano, K.; Kurata, K.; Masuda, K.; Ohno, K.; Tsujimoto, H. Lesional expression of thymus and activation-regulated chemokine in canine atopic dermatitis. Vet. Immunol. Immunopathol. 2002, 88, 79–87. [Google Scholar] [CrossRef]
- Olivry, T.; Dean, G.A.; Tompkins, M.B.; Dow, J.L.; Moore, P.F. Toward a canine model of atopic dermatitis: Amplification of cytokine-gene transcripts in the skin of atopic dogs. Exp. Dermatol. 1999, 8, 204–211. [Google Scholar] [CrossRef] [PubMed]
- Nuttall, T.J.; Knight, P.A.; McAleese, S.M.; Lamb, J.R.; Hill, P.B. Expression of Th1, Th2 and immunosuppressive cytokine gene transcripts in canine atopic dermatitis. Clin. Exp. Allergy 2002, 32, 789–795. [Google Scholar] [CrossRef] [PubMed]
- Nuttall, T.J.; Knight, P.A.; McAleese, S.M.; Lamb, J.R.; Hill, P.B. T-helper 1, T-helper 2 and immunosuppressive cytokines in canine atopic dermatitis. Vet. Immunol. Immunopathol. 2002, 87, 379–384. [Google Scholar] [CrossRef] [PubMed]
- Asahina, R.; Nishida, H.; Kamishina, H.; Maeda, S. Expression of IL-33 in chronic lesional skin of canine atopic dermatitis. Vet. Dermatol. 2018, 29, 246-e91. [Google Scholar] [CrossRef]
- Klukowska-Rötzler, J.; Chervet, L.; Müller, E.J.; Roosje, P.; Marti, E.; Janda, J. Expression of thymic stromal lymphopoietin in canine atopic dermatitis. Vet. Dermatol. 2013, 24, 54-e14. [Google Scholar] [CrossRef]
- Mineshige, T.; Kamiie, J.; Sugahara, G.; Shirota, K. A study on periostin involvement in the pathophysiology of canine atopic skin. J. Vet. Med. Sci. 2018, 80, 103–111. [Google Scholar] [CrossRef]
- Chaudhary, S.K.; Singh, S.K.; Kumari, P.; Kanwal, S.; Soman, S.P.; Choudhury, S.; Garg, S.K. Alterations in circulating concentrations of IL-17, IL-31 and total IgE in dogs with atopic dermatitis. Vet. Dermatol. 2019, 30, 383-e114. [Google Scholar] [CrossRef]
- Marsella, R.; Ahrens, K.; Sanford, R. Investigation of the correlation of serum IL-31 with severity of dermatitis in an experimental model of canine atopic dermatitis using beagle dogs. Vet. Dermatol. 2018, 29, 69-e28. [Google Scholar] [CrossRef]
- Furue, M.; Yamamura, K.; Kido-Nakahara, M.; Nakahara, T.; Fukui, Y. Emerging role of interleukin-31 and interleukin-31 receptor in pruritus in atopic dermatitis. Allergy 2018, 73, 29–36. [Google Scholar] [CrossRef]
- Verde, M.T.; Villanueva-Saz, S.; Loste, A.; Marteles, D.; Pereboom, D.; Conde, T.; Fernández, A. Comparison of circulating CD4+, CD8+ lymphocytes and cytokine profiles between dogs with atopic dermatitis and healthy dogs. Res. Vet. Sci. 2022, 145, 13–20. [Google Scholar] [CrossRef]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Mosca, M.; Milhau, N.; Legain, M.; Idée, A.; Langon, X.; Pin, D. Use of D-Squame® as a Minimally Invasive Technique to Evaluate Skin Immune Response Biomarkers in Canine Atopic Dermatitis. Vet. Sci. 2025, 12, 4. https://doi.org/10.3390/vetsci12010004
Mosca M, Milhau N, Legain M, Idée A, Langon X, Pin D. Use of D-Squame® as a Minimally Invasive Technique to Evaluate Skin Immune Response Biomarkers in Canine Atopic Dermatitis. Veterinary Sciences. 2025; 12(1):4. https://doi.org/10.3390/vetsci12010004
Chicago/Turabian StyleMosca, Marion, Nadège Milhau, Mélanie Legain, Adrien Idée, Xavier Langon, and Didier Pin. 2025. "Use of D-Squame® as a Minimally Invasive Technique to Evaluate Skin Immune Response Biomarkers in Canine Atopic Dermatitis" Veterinary Sciences 12, no. 1: 4. https://doi.org/10.3390/vetsci12010004
APA StyleMosca, M., Milhau, N., Legain, M., Idée, A., Langon, X., & Pin, D. (2025). Use of D-Squame® as a Minimally Invasive Technique to Evaluate Skin Immune Response Biomarkers in Canine Atopic Dermatitis. Veterinary Sciences, 12(1), 4. https://doi.org/10.3390/vetsci12010004