Allergy, Asthma & Immunology Research

The Korean Academy of Asthma, Allergy and Clinical Immunology (대한천식알레르기학회)
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Asthma Prevention by Lactobacillus Rhamnosus in a Mouse Model is Associated With $CD4^+CD25^+Foxp3^+$ T Cells

  • Jang, Seong-Ok (Asan Institute for Life Sciences, University of Ulsan College of Medicine) ;
  • Kim, Ha-Jung (Asan Institute for Life Sciences, University of Ulsan College of Medicine) ;
  • Kim, Young-Joon (Asan Institute for Life Sciences, University of Ulsan College of Medicine) ;
  • Kang, Mi-Jin (Asan Institute for Life Sciences, University of Ulsan College of Medicine) ;
  • Kwon, Ji-Won (Department of Pediatrics, Childhood Asthma Atopy Center, Asan Medical Center, University of Ulsan College of Medicine) ;
  • Seo, Ju-Hee (Department of Pediatrics, Childhood Asthma Atopy Center, Asan Medical Center, University of Ulsan College of Medicine) ;
  • Kim, Hyung-Young (Department of Pediatrics, Childhood Asthma Atopy Center, Asan Medical Center, University of Ulsan College of Medicine) ;
  • Kim, Byoung-Ju (Department of Pediatrics, Inje University Haeundae Paik Hospital) ;
  • Yu, Jin-Ho (Department of Pediatrics, Childhood Asthma Atopy Center, Asan Medical Center, University of Ulsan College of Medicine) ;
  • Hong, Soo-Jong (Department of Pediatrics, Childhood Asthma Atopy Center, Asan Medical Center, University of Ulsan College of Medicine)
  • Published : 2012.05.01
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Abstract

Purpose: Probiotic bacteria can induce immune regulation or immune tolerance in allergic diseases. The underlying mechanisms have been recently investigated, but are still unclear. The aim of this study was to evaluate the protective effects of the probiotic Lactobacillus rhamnosus (Lcr35) in a mouse model of asthma and to identify its mechanism of action. Methods: Lcr35 was administered daily by the oral route at a dosage of $1{\times}10^9$ CFU/mouse in BALB/c mice for 7 days before the first sensitization. Clinical parameters and regulatory T (Treg) cells were examined. The role of $CD4^+CD25^+Foxp3^+$ Treg cells was analyzed using a Treg cell-depleting anti-CD25 monoclonal antibody (mAb). Results: Airway hyperresponsiveness, total IgE production, pulmonary eosinophilic inflammation, and splenic lymphocyte proliferation were suppressed after Lcr35 treatment. Th1 (IFN-${\gamma}$) and Th2 (IL-4, IL-5, and IL-13) cytokines in the serum were suppressed, and the percentage of $CD4^+CD25^+Foxp3^+$ Treg cells in the spleen was significantly increased in the Lcr35 treatment group. Anti-CD25 mAb administration abolished the protective effects of Lcr35, indicating that $CD4^+CD25^+Foxp3^+$ Treg cells are essential in mediating the activity of Lcr35. Conclusions: Oral administration of Lcr35 attenuated the features of allergic asthma in a mouse model and induced immune regulation by a $CD4^+CD25^+Foxp3^+$ Treg cell-mediated mechanism.

Keywords

References

  1. Marteau P. Probiotics, prebiotics, synbiotics: ecological treatment for inflammatory bowel disease? Gut 2006;55:1692-1693. https://doi.org/10.1136/gut.2004.051458
  2. Kwon HK, Lee CG, So JS, Chae CS, Hwang JS, Sahoo A, Nam JH, Rhee JH, Hwang KC, Im SH. Generation of regulatory dendritic cells and CD4+Foxp3+ T cells by probiotics administration suppresses immune disorders. Proc Natl Acad Sci U S A 2010;107:2159-2164. https://doi.org/10.1073/pnas.0904055107
  3. Macpherson AJ, Uhr T. Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science 2004;303:1662-1665. https://doi.org/10.1126/science.1091334
  4. Huang FP, Platt N, Wykes M, Major JR, Powell TJ, Jenkins CD, MacPherson GG. A discrete subpopulation of dendritic cells transports apoptotic intestinal epithelial cells to T cell areas of mesenteric lymph nodes. J Exp Med 2000;191:435-444. https://doi.org/10.1084/jem.191.3.435
  5. Feleszko W, Jaworska J, Rha RD, Steinhausen S, Avagyan A, Jaudszus A, Ahrens B, Groneberg DA, Wahn U, Hamelmann E. Probiotic-induced suppression of allergic sensitization and airway inflammation is associated with an increase of T regulatory-dependent mechanisms in a murine model of asthma. Clin Exp Allergy 2007;37:498-505. https://doi.org/10.1111/j.1365-2222.2006.02629.x
  6. Hong HJ, Kim E, Cho D, Kim TS. Differential suppression of heat-killed lactobacilli isolated from kimchi, a Korean traditional food, on airway hyper-responsiveness in mice. J Clin Immunol 2010;30:449-458. https://doi.org/10.1007/s10875-010-9375-8
  7. Yu J, Jang SO, Kim BJ, Song YH, Kwon JW, Kang MJ, Choi WA, Jung HD, Hong SJ. The effects of Lactobacillus rhamnosus on the prevention of asthma in a murine model. Allergy Asthma Immunol Res 2010;2:199-205. https://doi.org/10.4168/aair.2010.2.3.199
  8. Kalliomaki M, Salminen S, Arvilommi H, Kero P, Koskinen P, Isolauri E. Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trial. Lancet 2001;357:1076-1079. https://doi.org/10.1016/S0140-6736(00)04259-8
  9. Helin T, Haahtela S, Haahtela T. No effect of oral treatment with an intestinal bacterial strain, Lactobacillus rhamnosus (ATCC 53103), on birch-pollen allergy: a placebo-controlled double-blind study. Allergy 2002;57:243-246. https://doi.org/10.1034/j.1398-9995.2002.1s3299.x
  10. Shida K, Takahashi R, Iwadate E, Takamizawa K, Yasui H, Sato T, Habu S, Hachimura S, Kaminogawa S. Lactobacillus casei strain Shirota suppresses serum immunoglobulin E and immunoglobulin G1 responses and systemic anaphylaxis in a food allergy model. Clin Exp Allergy 2002;32:563-570. https://doi.org/10.1046/j.0954-7894.2002.01354.x
  11. Pochard P, Gosset P, Grangette C, Andre C, Tonnel AB, Pestel J, Mercenier A. Lactic acid bacteria inhibit Th2 cytokine production by mononuclear cells from allergic patients. J Allergy Clin Immunol 2002;110:617-623. https://doi.org/10.1067/mai.2002.128528
  12. Smits HH, Engering A, van der Kleij D, de Jong EC, Schipper K, van Capel TM, Zaat BA, Yazdanbakhsh M, Wierenga EA, van Kooyk Y, Kapsenberg ML. Selective probiotic bacteria induce IL-10-producing regulatory T cells in vitro by modulating dendritic cell function through dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin. J Allergy Clin Immunol 2005;115:1260-1267. https://doi.org/10.1016/j.jaci.2005.03.036
  13. Tournoy KG, Kips JC, Schou C, Pauwels RA. Airway eosinophilia is not a requirement for allergen-induced airway hyperresponsiveness. Clin Exp Allergy 2000;30:79-85. https://doi.org/10.1046/j.1365-2222.2000.00772.x
  14. Borchers AT, Selmi C, Meyers FJ, Keen CL, Gershwin ME. Probiotics and immunity. J Gastroenterol 2009;44:26-46. https://doi.org/10.1007/s00535-008-2296-0
  15. Torii A, Torii S, Fujiwara S, Tanaka H, Inagaki N, Nagai H. Lactobacillus acidophilus strain L-92 regulates the production of Th1 cytokine as well as Th2 cytokines. Allergol Int 2007;56:293-301. https://doi.org/10.2332/allergolint.O-06-459
  16. Segawa S, Nakakita Y, Takata Y, Wakita Y, Kaneko T, Kaneda H, Watari J, Yasui H. Effect of oral administration of heat-killed Lactobacillus brevis SBC8803 on total and ovalbumin-specific immunoglobulin E production through the improvement of Th1/Th2 balance. Int J Food Microbiol 2008;121:1-10. https://doi.org/10.1016/j.ijfoodmicro.2007.10.004
  17. Mastrangeli G, Corinti S, Butteroni C, Afferni C, Bonura A, Boirivant M, Colombo P, Di Felice G. Effects of live and inactivated VSL#3 probiotic preparations in the modulation of in vitro and in vivo allergen-induced Th2 responses. Int Arch Allergy Immunol 2009;150:133-143. https://doi.org/10.1159/000218116
  18. Kearley J, Barker JE, Robinson DS, Lloyd CM. Resolution of airway inflammation and hyperreactivity after in vivo transfer of CD4+ CD25+ regulatory T cells is interleukin 10 dependent. J Exp Med 2005;202:1539-1547. https://doi.org/10.1084/jem.20051166
  19. Kearley J, Robinson DS, Lloyd CM. CD4+CD25+ regulatory T cells reverse established allergic airway inflammation and prevent airway remodeling. J Allergy Clin Immunol 2008;122:617-624.e6. https://doi.org/10.1016/j.jaci.2008.05.048
  20. McHugh RS, Shevach EM. Cutting edge: depletion of CD4+CD25+ regulatory T cells is necessary, but not sufficient, for induction of organ-specific autoimmune disease. J Immunol 2002;168:5979-5983. https://doi.org/10.4049/jimmunol.168.12.5979
  21. Kohm AP, Williams JS, Miller SD. Cutting edge: ligation of the glucocorticoid-induced TNF receptor enhances autoreactive CD4+ T cell activation and experimental autoimmune encephalomyelitis. J Immunol 2004;172:4686-4690. https://doi.org/10.4049/jimmunol.172.8.4686
  22. Kohm AP, Williams JS, Bickford AL, McMahon JS, Chatenoud L, Bach JF, Bluestone JA, Miller SD. Treatment with nonmitogenic anti-CD3 monoclonal antibody induces CD4+ T cell unresponsiveness and functional reversal of established experimental autoimmune encephalomyelitis. J Immunol 2005;174:4525-4534. https://doi.org/10.4049/jimmunol.174.8.4525
  23. Kohm AP, McMahon JS, Podojil JR, Begolka WS, DeGutes M, Kasprowicz DJ, Ziegler SF, Miller SD. Cutting Edge: Anti-CD25 monoclonal antibody injection results in the functional inactivation, not depletion, of CD4+CD25+ T regulatory cells. J Immunol 2006;176:3301-3305. https://doi.org/10.4049/jimmunol.176.6.3301

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