Skip to main content

Advertisement

SpringerLink
Log in

High-Intensity Swimming Exercise Increases Dust Mite Extract and 1-Chloro-2,4-Dinitrobenzene-Derived Atopic Dermatitis in BALB/c Mice

  • Published:
Inflammation Aims and scope Submit manuscript

Abstract

The aim of this study was to investigate the effect of high-intensity swimming exercise (HISE) on atopic dermatitis (AD). For the study, we established an AD model in BALB/c mice by repeated local exposure of house dust mite extract (Dermatophagoides farinae extract, DFE) and 1-chloro-2,4-dinitrobenzene (CDNB) to the ears. After HISE for 4 weeks, epidermal thickness, mast cell infiltration, serum immunoglobulin E (IgE), and histamine were measured. In addition, the gene expression of interleukin (IL)-5 and IL-31 in the ears was assayed. HISE increased DFE/CDNB-induced AD symptoms based on ear thickness, histopathological analysis, and serum IgE level. Moreover, HISE exercise stimulated mast cell infiltration into the ear, elevation of serum histamine, and DFE/CDNB-induced expression of IL-5 and IL-31 in the ears in the AD model. Taken together, our results indicate the possibility that HISE-induced stress gives rise to AD symptoms through the stimulation of IgE level by increasing IL-5 and IL-31 production.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

REFERENCES

  1. Benedetto, A.D., R. Agnihothri, L.Y. McGirt, L.G. Bankova, and L.A. Beck. 2009. Atopic dermatitis: a disease caused by innate immune defects? Journal of Investigative Dermatology 129: 14–30.

    Article  PubMed  Google Scholar 

  2. Incorvaia, C., F. Frati, N. Verna, S. D’Alò, A. Motolese, and S. Pucci. 2008. Allergy and the skin. Clinical and Experimental Immunology 1: S27–S29.

    Article  Google Scholar 

  3. Boguniewicz, M., and D.Y.M. Leung. 2010. Recent insights into atopic dermatitis and implications for management of infectious complications. Journal of Allergy and Clinical Immunology 125: 4–13.

    Article  PubMed Central  PubMed  Google Scholar 

  4. Finkelman, F.D., J.A. Boyce, D. Vercelli, and M.E. Rothenber. 2010. Key advances in mechanisms of asthma, allergy, and immunology in 2009. Journal of Allergy and Clinical Immunology 125: 312–318.

    Article  CAS  PubMed  Google Scholar 

  5. Novak, N., S. Koch, J.P. Allam, and T. Bieber. 2010. Dendritic cells: bridging innate and adaptive immunity in atopic dermatitis. Journal of Allergy and Clinical Immunology 125: 50–59.

    Article  CAS  PubMed  Google Scholar 

  6. Leung, D.Y.M., M. Boguniewicz, M.D. Howell, I. Nomura, and Q.A. Hamid. 2004. New insights into atopic dermatitis. Journal of Clinical Investigation 113: 651–657.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  7. Novak, N., T. Bieber, and D.Y.M. Leung. 2003. Immune mechanisms leading to atopic dermatitis. Journal of Allergy and Clinical Immunology 112: S128–S139.

    Article  CAS  PubMed  Google Scholar 

  8. He, R., M.K. Oyoshi, H. Jin, and R.S. Geha. 2007. Epicutaneous antigen exposure induces a Th17 response that drives airway inflammation after inhalation challenge. Proceedings of the National Academy of Sciences 104: 15817–15822.

    Article  CAS  Google Scholar 

  9. Bilsborough, J., D.Y. Leung, M. Maurer, M. Howell, M. Boguniewicz, and L. Yao. 2006. IL-31 is associated with cutaneous lymphocyte antigen-positive skin homing T cells in patients with atopic dermatitis. Journal of Allergy and Clinical Immunology 117: 418–425.

    Article  CAS  PubMed  Google Scholar 

  10. Orita, K., K. Hiramoto, R. Inoue, E.F. Sato, H. Kobayashi, M. Ishii, and M. Inoue. 2010. Strong exercise stress exacerbates dermatitis in atopic model mice, NC/Nga mice, while proper exercise reduces it. Experimental Dermatology 19: 1067–1072.

    Article  CAS  PubMed  Google Scholar 

  11. Kuphal, K.E., E.E. Fibuch, and B.K. Taylor. 2007. Extended swimming exercise reduces inflammatory and peripheral neuropathic pain in rodents. Journal of Pain 8: 989–997.

    Article  PubMed  Google Scholar 

  12. Mazzardo-Martins, L., D.F. Martins, R. Marcon, U.D. Santos, B. Speckhann, V.M. Gadotti, A.R. Sigwalt, L.G.A. Guglielmo, and A.R.S. Santos. 2010. High-intensity extended swimming exercise reduces pain-related behavior in mice: involvement of endogenous opioids and the serotonergic system. Journal of Pain 1: 1384–1393.

    Article  Google Scholar 

  13. Choi, E.J., S. Lee, H.H. Kim, T. Singh, J.K. Choi, H.G. Choi, W.M. Suh, S.H. Lee, and S.H. Kim. 2011. Generation of regulatory dendritic cells and CD4+Foxp3+ T cells by probiotics administration suppresses immune disorders. Journal of Ethnopharmacology 137: 802–807.

    Article  PubMed  Google Scholar 

  14. Kim, S.H., S. Lee, K. Suk, H. Bark, C.D. Jun, D.K. Kim, C.H. Choi, and T. Yoshimura. 2007. Discoidin domain receptor 1 mediates collagen-induced nitric oxide production in J774A.1 murine macrophages. Free Radical Biology & Medicine 42: 343–352.

    Article  Google Scholar 

  15. Kim, S.H., C.D. Jun, K. Suk, B.J. Choi, H. Lim, S. Park, S.H. Lee, H.Y. Shin, D.K. Kim, and T.Y. Shin. 2006. Gallic acid inhibits histamine release and pro-inflammatory cytokine production in mast cells. Toxicological Sciences 91: 123–131.

    Article  CAS  PubMed  Google Scholar 

  16. Hammerberg, B., T. Olivry, and S.M. Orton. 2001. Skin mast cell histamine release following stem cell factor and high-affinity immunoglobulin E receptor cross-linking in dogs with atopic dermatitis. Veterinary Dermatology 12: 339–346.

    Article  CAS  PubMed  Google Scholar 

  17. Cooper, C.E., N.B. Vollaard, T. Choueiri, and M.T. Wilson. 2002. Exercise, free radicals and oxidative stress. Biochemical Society Transactions 30: 280–285.

    Article  CAS  PubMed  Google Scholar 

  18. American Diabetes Association. 1993. Exercise and NIDDM. Diabetes Care 16: 54–58.

    Google Scholar 

  19. Sen, C.K. 1999. Glutathione homeostasis in response to exercise training and nutritional supplements. Molecular and Cellular Biochemistry 196: 31–42.

    Article  CAS  PubMed  Google Scholar 

  20. Sen, C.K., and L. Packer. 2000. Thiol homeostasis and supplements in physical exercise. The American Journal of Clinical Nutrition 72: S653–S669.

    Google Scholar 

  21. Hiramoto, K., H. Kobayashi, A. Sekiyama, F.E. Sato, D. Tsuruta, and M. Ishii. 2013. Mild exercise suppresses exacerbation of dermatitis by increasing cleavage of the β-endorphin from proopiomelanocortin in NC/Nga mice. Journal of Clinical Biochemistry and Nutrition 52: 58–63.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  22. Nakazawa, M., N. Sugi, H. Kawaguchi, N. Ishii, H. Nakajima, and M. Minami. 1997. Predominance of type 2 cytokine-producing CD4+ and CD8+ cells in patients with atopic dermatitis. Journal of Allergy and Clinical Immunology 99: 673–682.

    Article  CAS  PubMed  Google Scholar 

  23. Beck, L.A., M. Boguniewicz, T. Hata, L.C. Schneider, J. Hanifin, R. Gallo, A.S. Paller, S. Lieff, J. Reese, D. Zaccaro, H. Milgrom, K.C. Barnes, and D.Y.M. Leung. 2009. Phenotype of atopic dermatitis subjects with a history of eczema herpeticum. Journal of Allergy and Clinical Immunology 124: 260–269.

    Article  PubMed Central  PubMed  Google Scholar 

  24. Salt, B.H., M. Boguniewicz, and D.Y. Leung. 2007. Severe refractory atopic dermatitis in adults is highly atopic. Journal of Allergy and Clinical Immunology 119: 508–509.

    Article  PubMed  Google Scholar 

  25. Kang, J.S., W.K. Yoon, M.H. Han, H. Lee, C.W. Lee, K.H. Lee, S.B. Han, K. Lee, K.H. Yang, S.K. Park, and H.M. Kim. 2008. Inhibition of atopic dermatitis by topical application of silymarin in NC/Nga mice. International Immunopharmacology 8: 1475–1480.

    Article  CAS  PubMed  Google Scholar 

  26. Matsuoka, H., N. Maki, S. Yoshida, M. Arai, J. Wang, Y. Oikawa, T. Ikeda, N. Hirota, H. Nakagawa, and A. Ishii. 2003. A mouse model of the atopic eczema/dermatitis syndrome by repeated application of a crude extract of house-dust mite dermatophagoides farina. Allergy 58: 139–145.

    Article  CAS  PubMed  Google Scholar 

  27. Bradding, P., J.A. Roberts, K.M. Britten, S. Montefort, R. Djukanovic, R. Mueller, C.H. Heusser, P.H. Howarth, and S.T. Holgate. 1994. Interleukin-4, -5, and -6 and tumor necrosis factor-alpha in normal and asthmatic airways: evidence for the human mast cell as a source of these cytokines. American Journal of Respiratory Cell and Molecular Biology 10: 471–480.

    Article  CAS  PubMed  Google Scholar 

  28. Shen, H.H., S.I. Ochkur, M.P. McGarry, J.R. Crosby, E.M. Hines, M.T. Borchers, H. Wang, T.L. Biechelle, K.R. O’Neill, T.L. Ansay, D.C. Colbert, S.A. Cormier, J.P. Justice, N.A. Lee, and J.J. Lee. 2003. A causative relationship exists between eosinophils and the development of allergic pulmonary pathologies in the mouse. Journal of Immunology 170: 3296–3305.

    Article  CAS  Google Scholar 

  29. Lee, G.R., and R.A. Flavell. 2004. Transgenic mice which overproduce Th2 cytokines develop spontaneous atopic dermatitis and asthma. International Immunology 16: 1155–1160.

    Article  CAS  PubMed  Google Scholar 

  30. Simon, D., S. Von Gunten, S. Borelli, L.R. Braathen, and H.U. Simon. 2003. The interleukin-13 production by peripheral blood T cells from atopic dermatitis patients does not require CD2 costimulation. International Archives of Allergy and Immunology 132: 148–155.

    Article  CAS  PubMed  Google Scholar 

  31. Jeong, C.W., K.S. Ahn, N.K. Rho, Y.D. Park, D.Y. Lee, J.H. Lee, E.S. Lee, and J.M. Yang. 2003. Differential in vivo cytokine mRNA expression in lesional skin of intrinsic vs. extrinsic atopic dermatitis patients using semiquantitative RT-PCR. Clinical and Experimental Allergy 33: 1717–1724.

    Article  CAS  PubMed  Google Scholar 

  32. Spergel, J.M., E. Mizoguchi, H. Oettgen, A.K. Bhan, and R.S. Geha. 1999. Roles of TH1 and TH2 cytokines in a murine model of allergic dermatitis. Journal of Clinical Investigation 103: 1103–1111.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  33. Brandt, E.B., and U. Sivaprasad. 2011. Th2 cytokines and atopic dermatitis. Journal of Clinical & Cellular Immunology 2: 110–134.

    Article  Google Scholar 

  34. Choi, E.J., S. Lee, J.S. Hwang, S.H. Im, C.D. Jun, H.S. Lee, and S.H. Kim. 2011. DA-9601 suppresses 2,4-dinitrochlorobenzene and dust mite extract-induced atopic dermatitis-like skin lesions. International Immunopharmacology 11: 1260–1264.

    Article  CAS  PubMed  Google Scholar 

  35. Dillon, S.R., C. Sprecher, A. Hammond, J. Bilsborough, M. Rosenfeld-Franklin, S.R. Presnell, H.S. Haugen, M. Maurer, B. Harder, J. Johnston, S. Bort, S. Mudri, J.L. Kuijper, T. Bukowski, P. Shea, D.L. Dong, M. Dasovich, F.J. Grant, L. Lockwood, S.D. Levin, C. LeCiel, K. Waggie, H. Day, S. Topouzis, J. Kramer, R. Kuestner, Z. Chen, D. Foster, J. Parrish-Novak, and J.A. Gross. 2004. Interleukin 31, a cytokine produced by activated T cells, induces dermatitis in mice. Nature Immunology 5: 752–760.

    Article  CAS  PubMed  Google Scholar 

  36. Diveu, C., A.H. Lak-Hal, J. Froger, E. Ravon, L. Grimaud, F. Barbier, J. Hermann, H. Gascan, and S. Chevalier. 2004. Predominant expression of the long isoform of GP130-like (GPL) receptor is required for interleukin-31 signaling. European Cytokine Network 15: 291–302.

    CAS  PubMed  Google Scholar 

  37. Sonkoly, E., A. Muller, A. Lauerma, A. Pivarcsi, H. Soto, L. Kemeny, H. Alenius, M.C. Dieu-Nosjean, S. Meller, J. Rieker, M. Steinhoff, T.K. Hoffmann, T. Ruzicka, A. Zlotnik, and B. Homey. 2006. IL-31: a new link between T cell and pruritus in atopic skin inflammation. American College of Allergy, Asthma and Immunology 2: 411–417.

    Google Scholar 

Download references

ACKNOWLEDGMENTS

This work was supported by the National Research Foundation of Korea Grant funded by the Korean Government (NRF-2012S1A5A8024395) and by the “Cooperative Research Program for Agriculture Science & Technology Development (Project No. 009773)” Rural Development Administration, Republic of Korea.

Author information

Authors and Affiliations

  1. Laboratory of Immunotoxicology, Department of Pharmacology, School of Medicine, Kyungpook National University, Daegu, 700-422, Republic of Korea

    Sang-Hyun Kim

  2. Division of Food Bioscience, College of Biomedical and Health Sciences, Konkuk University, Chungju, 380-701, Republic of Korea

    Eun-Kyung Kim

  3. Korea Nokyong Research Center, Konkuk University, Chungju, 380-701, Republic of Korea

    Eun-Kyung Kim

  4. Division of Sport Science, College of Science and Technology, Konkuk University, Chungju, 380-702, Republic of Korea

    Eun-Ju Choi

Authors
  1. Sang-Hyun Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eun-Kyung Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eun-Ju Choi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Eun-Ju Choi.

Additional information

Sang-Hyun Kim and Eun-Kyung Kim contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kim, SH., Kim, EK. & Choi, EJ. High-Intensity Swimming Exercise Increases Dust Mite Extract and 1-Chloro-2,4-Dinitrobenzene-Derived Atopic Dermatitis in BALB/c Mice. Inflammation 37, 1179–1185 (2014). https://doi.org/10.1007/s10753-014-9843-z

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10753-014-9843-z

KEY WORDS

Search

Navigation