Toxicological Research

Korean Society of Toxicology & Korea Environmental Mutagen Society (한국독성학회)
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A Probiotic Preparation Alleviates Atopic Dermatitis-Like Skin Lesions in Murine Models

  • Received : 2015.07.03
  • Accepted : 2015.08.13
  • Published : 2016.04.15
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Abstract

Atopic dermatitis (AD) is a chronic inflammatory skin disease with a complex etiology that encompasses immunologic responses. AD is frequently associated with elevated immunoglobulin (Ig) E levels, and common environmental factors contribute to its pathogenesis. Several recent studies have documented the role of specific lactic acid bacteria in the treatment and prevention of AD in humans and mice. In this study, the efficacy of Duolac ATP, a probiotic preparation, was determined in a mouse model with AD-like skin lesions. Alterations in the cytokine levels and histological staining suggested the alleviation of AD. The in vivo test showed that T helper (Th)2 cytokines, IgE, interleukin (IL)-4, and IL-5, were significantly downregulated, whereas Th1 cytokines, IL-12p40 and interferon (IFN)-${\gamma}$, were upregulated in all groups of mice treated with Duolac ATP compared to that observed in the group of mice treated with 1-chloro-2,4-dinitrobenzene (DNCB) alone. Moreover, the scratch score decreased in all mice treated with Duolac ATP. Staining of the dorsal area of the mice in each group with hematoxylin and eosin and toluidine blue further confirmed the alleviation of AD in mice orally treated with Duolac ATP. These results suggest that Duolac ATP inhibits the development of AD-like skin lesions in NC/Nga mice by suppressing the Th2 cell response and increasing the Th1 cell response. Thus, Duolac ATP is beneficial and effective for the treatment of AD-like skin lesions.

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References

  1. Leung, D.Y. and Bieber, T. (2003) Atopic dermatitis. Lancet., 361, 151-160. https://doi.org/10.1016/S0140-6736(03)12193-9
  2. Morar, N., Willis-Owen, S.A., Moffatt, M.F. and Cookson, W.O. (2006) The genetics of atopic dermatitis. J. Allergy Clin. Immunol., 118, 24-34. https://doi.org/10.1016/j.jaci.2006.03.037
  3. Sicherer, S.H. and Leung, D.Y. (2009) Advances in allergic skin disease, anaphylaxis, and hypersensitivity reactions to foods, drugs, and insects in 2008. J. Allergy Clin. Immunol., 123, 319-327. https://doi.org/10.1016/j.jaci.2008.12.025
  4. Fujiwara, D., Inoue, S., Wakabayashi, H. and Fujii, T. (2004) The anti-allergic effects of lactic acid bacteria are strain dependent and mediated by effects on both Th1/Th2 cytokine expression and balance. Int. Arch. Allergy Immunol., 135, 205-215. https://doi.org/10.1159/000081305
  5. Wahlgren, C.F. (1999) Itch and atopic dermatitis: an overview. J. Dermatol., 26, 770-779. https://doi.org/10.1111/j.1346-8138.1999.tb02090.x
  6. Hengge, U.R., Ruzicka, T., Schwartz, R.A. and Cork, M.J. (2006) Adverse effects of topical glucocorticosteroids. J. Am. Acad. Dermatol., 54, 1-15. https://doi.org/10.1016/j.jaad.2005.01.010
  7. Woodfolk, J.A. (2007) T-cell responses to allergens. J. Allergy Clin. Immunol., 119, 280-294. https://doi.org/10.1016/j.jaci.2006.11.008
  8. Abbas, A.K., Murphy, K.M. and Sher, A. (1996) Functional diversity of helper T lymphocytes. Nature, 383, 787-793. https://doi.org/10.1038/383787a0
  9. Klewicka, E., Cukrowska, B., Libudzisz, Z., Slizewska, K. and Motyl, I. (2011) Changes in gut microbiota in children with atopic dermatitis administered the bacteria Lactobacillus casei DN--114001. Pol. J. Microbiol., 60, 329-333. https://doi.org/10.1099/jmm.0.019703-0
  10. Habu, Y., Seki, S., Takayama, E., Ohkawa, T., Koike, Y., Ami, K., Majima, T. and Hiraide, H. (2001) The mechanism of a defective IFN-gamma response to bacterial toxins in an atopic dermatitis model, NC/Nga mice, and the therapeutic effect of IFN-gamma, IL-12, or IL-18 on dermatitis. J. Immunol., 166, 5439-5447. https://doi.org/10.4049/jimmunol.166.9.5439
  11. Mercenier, A., Pavan, S. and Pot, B. (2003) Probiotics as biotherapeutic agents: present knowledge and future prospects. Curr. Pharm. Des., 9, 175-191. https://doi.org/10.2174/1381612033392224
  12. van Buul-Offers, S.C., Smink, J.J., Gresnigt, R., Hamers, N., Koedam, J. and Karperien, M. (2005) Thyroid hormone, but not parathyroid hormone, partially restores glucocorticoidinduced growth retardation. Pediatr. Nephrol., 20, 335-341. https://doi.org/10.1007/s00467-004-1690-y
  13. Rapaport, M.J. and Lebwohl, M. (2003) Corticosteroid addiction and withdrawal in the atopic: the red burning skin syndrome. Clin. Dermatol., 21, 201-214. https://doi.org/10.1016/S0738-081X(02)00365-6
  14. Gupta, A.K. and Chow, M. (2003) Pimecrolimus: a review. J. Eur. Acad. Dermatol. Venereol., 17, 493-503. https://doi.org/10.1046/j.1468-3083.2003.00692.x
  15. Mainardi, T., Kapoor, S. and Bielory, L. (2009) Complementary and alternative medicine: herbs, phytochemicals and vitamins and their immunologic effects. J. Allergy Clin. Immunol., 123, 283-294. https://doi.org/10.1016/j.jaci.2008.12.023
  16. Klovekorn, W., Tepe, A. and Danesch, U. (2007) A randomized, double-blind, vehicle-controlled, half-side comparison with a herbal ointment containing Mahonia aquifolium, Viola tricolor and Centella asiatica for the treatment of mild-to-moderate atopic dermatitis. Int. J. Clin. Pharmacol. Ther., 45, 583-591. https://doi.org/10.5414/CPP45583
  17. Donsky, H. and Clarke, D. (2007) Relieva, a Mahonia aquifolium extract for the treatment of adult patients with atopic dermatitis. Am. J. Ther., 14, 442-446. https://doi.org/10.1097/MJT.0b013e31814002c1
  18. Reid, G., Sanders, M.E., Gaskins, H.R., Gibson, G.R., Mercenier, A., Rastall, R., Roberfroid, M., Rowland, I., Cherbut, C. and Klaenhammer, T.R. (2003) New scientific paradigms for probiotics and prebiotics. J. Clin. Gastroenterol., 37, 105-118. https://doi.org/10.1097/00004836-200308000-00004
  19. Vestergaard, C., Yoneyama, H. and Matsushima, K. (2000) The NC/Nga mouse: a model for atopic dermatitis. Mol. Med. Today, 6, 209-210. https://doi.org/10.1016/S1357-4310(00)01683-X
  20. Suto, H., Matsuda, H., Mitsuishi, K., Hira, K., Uchida, T., Unno, T., Ogawa, H. and Ra, C. (1999) NC/Nga mice: a mouse model for atopic dermatitis. Int. Arch. Allergy Immunol., 120 Suppl 1, 70-75. https://doi.org/10.1159/000053599
  21. Cha, Y.S., Seo, J.G., Chung, M.J., Cho, C.W. and Youn, H.J. (2014) A mixed formulation of lactic acid bacteria inhibits trinitrobenzene-sulfonic-acid-induced inflammatory changes of the colon tissue in mice. J. Microbiol. Biotechnol., 24, 1438-1444. https://doi.org/10.4014/jmb.1403.03064
  22. Yesilova, Y., Calka, O., Akdeniz, N. and Berktas, M. (2012) Effect of probiotics on the treatment of children with atopic dermatitis. Ann. Dermatol., 24, 189-193. https://doi.org/10.5021/ad.2012.24.2.189
  23. Matsuda, H., Watanabe, N., Geba, G.P., Sperl, J., Tsudzuki, M., Hiroi, J., Matsumoto, M., Ushio, H., Saito, S., Askenase, P.W. and Ra, C. (1997) Development of atopic dermatitis-like skin lesion with IgE hyperproduction in NC/Nga mice. Int. Immunol., 9, 461-466. https://doi.org/10.1093/intimm/9.3.461
  24. Leung, D.Y. (1997) Atopic dermatitis: immunobiology and treatment with immune modulators. Clin. Exp. Immunol., 107 Suppl 1, 25-30.
  25. Grewe, M., Gyufko, K., Schopf, E. and Krutmann, J. (1994) Lesional expression of interferon-gamma in atopic eczema. Lancet, 343, 25-26. https://doi.org/10.1016/S0140-6736(94)90879-6
  26. Ogawa, T., Hashikawa, S., Asai, Y., Sakamoto, H., Yasuda, K. and Makimura, Y. (2006) A new synbiotic, Lactobacillus casei subsp. casei together with dextran, reduces murine and human allergic reaction. FEMS Immunol. Med. Microbiol., 46, 400-409. https://doi.org/10.1111/j.1574-695X.2006.00046.x
  27. Kohara, Y., Tanabe, K., Matsuoka, K., Kanda, N., Matsuda, H., Karasuyama, H. and Yonekawa, H. (2001) A major determinant quantitative-trait locus responsible for atopic dermatitis-like skin lesions in NC/Nga mice is located on Chromosome 9. Immunogenetics, 53, 15-21. https://doi.org/10.1007/s002510000286
  28. Won, T.J., Kim, B., Song, D.S., Lim, Y.T., Oh, E.S., Lee, D.I., Park, E.S., Min, H., Park, S.Y. and Hwang, K.W. (2011) Modulation of Th1/Th2 balance by Lactobacillus strains isolated from Kimchi via stimulation of macrophage cell line J774A.1 in vitro. J. Food Sci., 76, H55-H61. https://doi.org/10.1111/j.1750-3841.2010.02031.x
  29. Ozcan, E., Notarangelo, L.D. and Geha, R.S. (2008) Primary immune deficiencies with aberrant IgE production. J. Allergy Clin. Immunol., 122, 1054-1062. https://doi.org/10.1016/j.jaci.2008.10.023
  30. Kim, M.S., Hur, Y.G., Kim, W.G., Park, B.W., Ahn, K.S., Kim, J.J. and Bae, H. (2011) Inhibitory effect of Platycodon grandiflorum on T(H)1 and T(H)2 immune responses in a murine model of 2,4-dinitrofluorobenzene-induced atopic dermatitislike skin lesions. Ann. Allergy Asthma Immunol., 106, 54-61. https://doi.org/10.1016/j.anai.2010.10.020
  31. Kim, M.S., Kim, W.G., Chung, H.S., Park, B.W., Ahn, K.S., Kim, J.J. and Bae, H. (2012) Improvement of atopic dermatitis-like skin lesions by Platycodon grandiflorum fermented by Lactobacillus plantarum in NC/Nga mice. Biol. Pharm. Bull., 35, 1222-1229. https://doi.org/10.1248/bpb.b110504
  32. Chapat, L., Chemin, K., Dubois, B., Bourdet-Sicard, R. and Kaiserlian, D. (2004) Lactobacillus casei reduces CD8+ T cell-mediated skin inflammation. Eur. J. Immunol. 34, 2520-2528. https://doi.org/10.1002/eji.200425139

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