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Alleviation of Atopic Dermatitis through Probiotic and Mixed-probiotic Treatments in an Atopic Dermatitis Model

  • Received : 2011.03.10
  • Accepted : 2011.06.27
  • Published : 2011.06.30

Abstract

The use of lactic-acid bacteria (LAB) is effective for preventing and curing immune disorders by activating the immune system in the digestive tract and the consequent immune response in the blood. In this study, LAB and mixed LABs were used in an atopic dermatitis (AD) mouse model. Alleviation of AD was observed based on the change in cytokine level and immunohistochemical staining. An ex vivo test showed that immunoglobulin-E and interleukin (IL)-4 levels were significantly lower in all groups treated with LAB than in the group treated with only 1-chloro-2,4-dinitrobenzene. Results of an in vivo test based on the ex vivo results showed that the scratch score decreased in all groups treated with the LAB and particularly decreased in the group treated with mixed LABs. Additionally, the T helper (Th) 1 cytokines interferon-gamma and IL-12p40 were upregulated by the LAB and mixed-LABs, whereas levels of the Th2 cytokine IL-4 were downregulated in a mouse model of AD-like skin lesions. Furthermore, hematoxylin & eosin and immunohistochemical staining of the dorsal area of the mice in each group showed that AD improved in the LAB-treated groups. These results suggest that LAB and mixed LABs inhibit the development of AD in NC/Nga mice by suppressing the Th2 cell response and increasing the Th1 cell response. Our results indicate that mixed LABs are better than LAB for treating AD-like skin lesions.

Keywords

References

  1. Aversa, G., Punnonen, J., Cocks, B. G., de Waal Malefyt, R., Vega, F., Jr., Zurawski, S. M., Zurawski, G., and de Vries, J. E. (1993) An interleukin 4 (IL-4) mutant protein inhibits both IL-4 or IL-13-induced human immunoglobulin G4 (IgG4) and IgE synthesis and B cell proliferation: support for a common component shared by IL-4 and IL-13 receptors. J. Exp. Med. 178, 2213-2218. https://doi.org/10.1084/jem.178.6.2213
  2. Brouwer, M. L., Wolt-Plompen, S. A., Dubois, A. E., van der Heide, S., Jansen, D. F., Hoijer, M. A., Kauffman, H. F., and Duiverman, E. J. (2006) No effects of probiotics on atopic dermatitis in infancy: a randomized placebo-controlled trial. Clin. Exp. Allergy 36, 899-906. https://doi.org/10.1111/j.1365-2222.2006.02513.x
  3. Choi, K. O., Nguyen, H. H., and Kwak, H. S. (2010) The role of the immune system in the use of probiotic lactic acid bacteria in preventing and treating allergic diseases. Korean J. Food Sci. Ani. Resour. 30, 1-12. https://doi.org/10.5851/kosfa.2010.30.1.1
  4. Ferrick, D. A., Schrenzel, M. D., Mulvania, T., Hsieh, B., Ferlin, W. G., and Lepper, H. (1995) Differential production of interferon-gamma and interleukin-4 in response to Th1-and Th2-stimulating pathogens by gamma delta T cells in vivo. Nature 373, 255-257. https://doi.org/10.1038/373255a0
  5. Folster-Holst, R., Muller, F., Schnopp, N., Abeck, D., Kreiselmaier, I., Lenz, T., von Ruden, U., Schrezenmeir, J., Christophers, E., and Weichenthal, M. (2006) Prospective, randomized controlled trial on Lactobacillus rhamnosus in infants with moderate to severe atopic dermatitis. Br. J. Dermatol. 155, 1256-1261. https://doi.org/10.1111/j.1365-2133.2006.07558.x
  6. Gunther, C., Bello-Fernandez, C., Kopp, T., Kund, J., Carballido- Perrig, N., Hinteregger, S., Fassl, S., Schwarzler, C., Lametschwandtner, G., Stingl, G., Biedermann, T., and Carballido, J. M. (2005) CCL18 is expressed in atopic dermatitis and mediates skin homing of human memory T cells. J. Immunol. 174, 1723-1728. https://doi.org/10.4049/jimmunol.174.3.1723
  7. Hiroi, J., Sengoku, T., Morita, K., Kishi, S., Sato, S., Ogawa, T., Tsudzuki, M., Matsuda, H., Wada, A., and Esaki, K., (1998) Effect of tacrolimus hydrate (FK506) ointment on spontaneous dermatitis in NC/Nga mice. Jpn. J. Pharmacol. 76, 175-183. https://doi.org/10.1254/jjp.76.175
  8. Homey, B., Steinhoff, M., Ruzicka, T., and Leung, D. Y. (2006) Cytokines and chemokines orchestrate atopic skin inflammation. J. Allergy Clin. Immunol. 118, 178-189. https://doi.org/10.1016/j.jaci.2006.03.047
  9. Kalliomaki, M., Salminen, S., Arvilommi, H., Kero, P., Koskinen, P., and Isolauri, E. (2001) Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trial. Lancet 357, 1076-1079. https://doi.org/10.1016/S0140-6736(00)04259-8
  10. Kay, A. B., Ying, S., Varney, V., Gaga, M., Durham, S. R., Moqbel, R., Wardlaw, A. J., and Hamid, Q. (1991) Messenger RNA expression of the cytokine gene cluster, interleukin 3 (IL-3), IL-4, IL-5, and granulocyte/macrophage colonystimulating factor, in allergen-induced late-phase cutaneous reactions in atopic subjects. J. Exp. Med. 173, 775-778. https://doi.org/10.1084/jem.173.3.775
  11. Ker, J. and Hartert, T. V. (2009) The atopic march: what's the evidence? Ann. Allergy Asthma. Immunol. 103, 282-289. https://doi.org/10.1016/S1081-1206(10)60526-1
  12. Kim, J. Y., Kwon, J. H., Ahn, S. H., Lee, S. I., Han, Y. S., Choi, Y. O., Lee, S. Y., Ahn, K. M., and Ji, G. E. (2010) Effect of probiotic mix (Bifidobacterium bifidum, Bifidobacterium lactis, Lactobacillus acidophilus) in the primary prevention of eczema: a double-blind, randomized, placebocontrolled trial. Pediatr Allergy Immunol. 21, e386-393. https://doi.org/10.1111/j.1399-3038.2009.00958.x
  13. Lester, M. R., Hofer, M. F., Gately, M., Trumble, A., and Leung, D. Y. (1995) Down-regulating effects of IL-4 and IL- 10 on the IFN-gamma response in atopic dermatitis. J. Immunol. 154, 6174-6181.
  14. Leung, D.Y. and Bieber, T. (2003) Atopic dermatitis. Lancet 361, 151-160. https://doi.org/10.1016/S0140-6736(03)12193-9
  15. Maeda, S. and Yanagihara, Y. (2001) Inflammatory cytokines (IL-4, IL-5 and IL-13). Nippon Rinsho 59, 1894-1899.
  16. Mancini, A. J., Kaulback K., and Chamlin S. L. (2008) The socioeconomic impact of atopic dermatitis in the United States: a systematic review. Pediatr. Dermatol. 25, 1-6.
  17. 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 dermatitislike skin lesion with IgE hyperproduction in NC/Nga mice. Int. Immunol. 9, 461-466. https://doi.org/10.1093/intimm/9.3.461
  18. Ohmen, J. D., Hanifin, J. M., Nickoloff, B. J., Rea, T. H., Wyzykowski, R., Kim, J., Jullien, D., McHugh, T., Nassif, A. S., and Chan, S. C. (1995) Overexpression of IL-10 in atopic dermatitis. Contrasting cytokine patterns with delayed-type hypersensitivity reactions. J. Immunol. 154, 1956-1963.
  19. Pivarcsi, A., Gombert, M., Dieu-Nosjean, M. C., Lauerma, A., Kubitza, R., Meller, S., Rieker, J., Muller, A., Da Cunha, L., Haahtela, A., Sonkoly, E., Fridman, W. H., Alenius, H., Kemeny, L., Ruzicka, T., Zlotnik, A., and Homey, B. (2004) CC chemokine ligand 18, an atopic dermatitis-associated and dendritic cell-derived chemokine, is regulated by staphylococcal products and allergen exposure. J. Immunol. 173, 5810-5817. https://doi.org/10.4049/jimmunol.173.9.5810
  20. Rosenfeldt, V., Benfeldt, E., Nielsen, S. D., Michaelsen, K. F., Jeppesen, D. L., Valerius, N. H., and Paerregaard A. (2003) Effect of probiotic Lactobacillus strains in children with atopic dermatitis. J. Allergy Clin. Immunol. 111, 389-395. https://doi.org/10.1067/mai.2003.389
  21. Rousset, F., Robert, J., Andary, M., Bonnin, J. P., Souillet, G., Chretien, I., Briere, F., Pene, J., and de Vries, J. E. (1991) Shifts in interleukin-4 and interferon-gamma production by T cells of patients with elevated serum IgE levels and the modulatory effects of these lymphokines on spontaneous IgE synthesis. J. Allergy Clin. Immunol. 87, 58-69. https://doi.org/10.1016/0091-6749(91)90213-8
  22. 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
  23. Taylor, A. L., Dunstan, J. A., and Prescott, S. L. (2007) Probiotic supplementation for the first 6 months of life fails to reduce the risk of atopic dermatitis and increases the risk of allergen sensitization in high-risk children: a randomized controlled trial. J. Allergy Clin. Immunol. 119, 184-191. https://doi.org/10.1016/j.jaci.2006.08.036
  24. Tazawa, T., Sugiura, H., Sugiura, Y., and Uehara, M. (2004) Relative importance of IL-4 and IL-13 in lesional skin of atopic dermatitis. Arch. Dermatol. Res. 295, 459-464. https://doi.org/10.1007/s00403-004-0455-6
  25. van der Kleij, H. P., Kraneveld, A. D., van Houwelingen A. H., Kool, M., Weitenberg, A. C., Redegeld, F. A., and Nijkamp, F. P. (2004) Murine model for non-IgE-mediated asthma. Inflammation 28, 115-125. https://doi.org/10.1023/B:IFLA.0000039557.33267.65
  26. 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
  27. Viljanen, M., Pohjavuori, E., Haahtela, T., Korpela, R., Kuitunen, M., Sarnesto, A., Vaarala, O., and Savilahti, E. (2005) Induction of inflammation as a possible mechanism of probiotic effect in atopic eczema-dermatitis syndrome. J. Allergy Clin. Immunol. 115, 1254-1259. https://doi.org/10.1016/j.jaci.2005.03.047
  28. Wakabayashi, H., Nariai C., Takemura F., Nakao W., and Fujiwara, D. (2008) Dietary supplementation with lactic acid bacteria attenuates the development of atopic-dermatitis-like skin lesions in NC/Nga mice in a strain-dependent manner. Int. Arch. Allergy Immunol. 145, 141-151. https://doi.org/10.1159/000108139

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