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Research article

Clinical Microbiology and Biomedical Sciences

Immunomodulatory and Anti-Allergic Effects of Orally Administered Lactobacillus Species in Ovalbumin-Sensitized Mice

Jeongmin Lee 1, 2, Jieun Bang 1 and Hee-Jong Woo 1*

1Laboratory of Immunology, College of Veterinary Medicine, Seoul National University, Seoul 151-742, Korea, 2Division of Zoonoses, Center for Immunology and Pathology, National Institute of Health, Korea Centers for Disease Control and Prevention, Cheongwon-gun, Chungcheongbuk-do 363-951, Korea

Received: November 28, 2012; Accepted: January 8, 2013

J. Microbiol. Biotechnol. 2013; 23(5): 724-730

Published May 25, 2013 https://doi.org/10.4014/jmb.1211.11079

Copyright © The Korean Society for Microbiology and Biotechnology.

Abstract

We investigated the effects of orally administered probiotic bacteria (Lactobacillus species) as allergic immune modulators in ovalbumin (OVA)-sensitized mice. BALB/c mice were intraperitoneally injected with OVA twice at a 2-week interval for allergy sensitization. The mice were then orally administered Lactobacillus casei YIT9029 (L1), L. casei HY7201 (L2), L. brevis HY7401 (L3), or L. plantarum HY20301 (L4) every 2 days for 3 weeks. Total IgE levels significantly decreased in sera of L3-administered mice but increased in the other groups. OVA-specific IgE levels decreased slightly in sera of mice administered L1, L3, and L4 but increased significantly in L2-administered mice. In passive cutaneous anaphylaxis (PCA) using sera from administered mice, only the L3-administered group showed reaction inhibition. High expression of TLR-2 with interferon (IFN)-γ stimulation on peripheral blood mononuclear cells occurred in L3- or L4-administered mice. Th1 cytokines, including IFN-γ and interleukin (IL)- 12, increased in splenocytes of L3-administered mice; however, IL-4 decreased in L1- and L4-administered groups; IL-5 decreased in all experimental groups. IL-6 decreased in the L3-administered group; and IL-10 decreased in L1-, L2-, and L3-administered groups. L3 induced antiallergic effects by increasing Th1 cytokines, decreasing Th2 cytokines, and inhibiting the PCA reaction, whereas L2 administration increased allergic effects.

Keywords

allergy, oral administration, probiotics, Lactobacillus

References

  1. Borchers, A. T., C. Selmi, F. J. Meyers, C. L. Keen, and M. E. Gershwin. 2009. Probiotics and immunity. J. Gastroenterol. 44:26-46.
    Pubmed CrossRef
  2. Frossard, C. P. and P. A. Eigenmann. 2008. The role of IL-10 in preventing food-induced anaphylaxis. Expert Opin. Biol. Ther. 8: 1309-1317.
    Pubmed CrossRef
  3. Fujiwara, D., S. Inoue, H. Wakabayashi, and T. Fujii. 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.
    Pubmed CrossRef
  4. Fuller, R. 1989. Probiotics in man and animals. J. Appl. Bacteriol. 66: 365-378.
    Pubmed CrossRef
  5. Gajewski, T. F., E. Goldwasser, and F. W. Fitch. 1988. Antiproliferative effect of IFN-gamma in immune regulation. II. IFN-gamma inhibits the proliferation of murine bone marrow cells stimulated with IL-3, IL-4, or granulocyte-macrophage colony-stimulating factor. J. Immunol. 141: 2635-2642.
    Pubmed
  6. Gill, H. and J. Prasad. 2008. Probiotics, immunomodulation, and health benefits. Adv. Exp. Med. Biol. 606: 423-454.
    Pubmed CrossRef
  7. Huang, J., Y. Zhong, W. Cai, H. Zhang, W. Tang, and B. Chen. 2010. The effects of probiotics supplementation timing on an ovalbumin-sensitized rat model. FEMS Immunol. Med. Microbiol. 60: 132-141.
    Pubmed CrossRef
  8. Kaisho, T. and S. Akira. 2006. Toll-like receptor function and signaling. J. Allergy Clin. Immunol. 117: 979-987; quiz 988.
    Pubmed CrossRef
  9. Kim, H., K. Kwack, D. Y. Kim, and G. E. Ji. 2005. Oral probiotic bacterial administration suppressed allergic responses in an ovalbumin-induced allergy mouse model. FEMS Immunol. Med. Microbiol. 45: 259-267.
    Pubmed CrossRef
  10. Kim, H., S. Y. Lee, and G. E. Ji. 2005. Timing of Bifidobacterium administration influences the development of allergy to ovalbumin in mice. Biotechnol. Lett. 27: 1361-1367.
    Pubmed CrossRef
  11. Kim, J. Y., Y. O. Choi, and G. E. Ji. 2008. Effect of oral probiotics (Bifidobacterium lactis AD011 and Lactobacillus acidophilus AD031) administration on ovalbumin-induced food allergy mouse model. J. Microbiol. Biotechnol. 18: 1393-1400.
    Pubmed
  12. Kindt, T. J., R. A. Goldsby, B. A. Osborne, and J. Kuby. 2007. Kuby immunology, pp. xxii, 574, A-531, G-512, AN-527, I527, 6th Ed. W. H. Freeman, New York.
  13. Kubota, E., T. Joh, S. Tanida, M. Sasaki, H. Kataoka, K. Watanabe, et al. 2005. Oral vaccination against Helicobacter pylori with recombinant cholera toxin B-subunit. Helicobacter 10: 345-352.
    Pubmed CrossRef
  14. Kwak, C., B. C. Jeong, J. H. Ku, H. H. Kim, J. J. Lee, C. S. Huh, Y. J. Baek, et al. 2006. Prevention of nephrolithiasis by Lactobacillus in stone-forming rats: A preliminary study. Urol. Res. 34: 265-270.
    Pubmed CrossRef
  15. Lee, H. S., S. Y. Han, E. A. Bae, C. S. Huh, Y. T. Ahn, J. H. Lee, et al. 2008. Lactic acid bacteria inhibit proinflammatory cytokine expression and bacterial glycosaminoglycan degradation activity in dextran sulfate sodium-induced colitic mice. Int. Immunopharmacol. 8: 574-580.
    Pubmed CrossRef
  16. Lee, J. and H. J. Woo. 2010. Antigenicity of partial fragments of recombinant Pasteurella multocida toxin. J. Microbiol. Biotechnol. 20: 1756-1763.
    Pubmed
  17. Lewkowich, I. P., J. D. Rempel, and K. T. HayGlass. 2004. In vivo IgE levels in exogenous antigen stimulated responses:Measurement of total IgE as a valid, simple surrogate for Agspecific IgE. J. Immunol. Methods 286: 123-132.
    Pubmed CrossRef
  18. Masood, M. I., M. I. Qadir, J. H. Shirazi, and I. U. Khan. 2011. Beneficial effects of lactic acid bacteria on human beings. Crit. Rev. Microbiol. 37: 91-98.
    Pubmed CrossRef
  19. Matsuzaki, T., R. Yamazaki, S. Hashimoto, and T. Yokokura. 1998. The effect of oral feeding of Lactobacillus casei strain Shirota on immunoglobulin E production in mice. J. Dairy Sci. 81: 48-53.
    CrossRef
  20. Nonaka, Y., T. Izumo, F. Izumi, T. Maekawa, H. Shibata, A. Nakano, et al. 2008. Antiallergic effects of Lactobacillus pentosus strain S-PT84 mediated by modulation of Th1/Th2 immunobalance and induction of IL-10 production. Int. Arch. Allergy Immunol. 145: 249-257.
    Pubmed CrossRef
  21. Ohno, H., S. Tsunemine, Y. Isa, M. Shimakawa, and H. Yamamura. 2005. Oral administration of Bifidobacterium bifidum G9-1 suppresses total and antigen specific immunoglobulin E production in mice. Biol. Pharm. Bull. 28: 1462-1466.
    Pubmed CrossRef
  22. Okudaira, H., T. Suzuki, and T. Ogita. 1980. A study of the rat passive cutaneous anaphylaxis (PCA) reaction for the assay of mouse IgE antibody. J. Immunol. Methods 33: 369-377.
    CrossRef
  23. Patel, M., D. Xu, P. Kewin, B. Choo-Kang, C. McSharry, N. C. Thomson, et al. 2005. TLR2 agonist ameliorates established allergic airway inflammation by promoting Th1 response and not via regulatory T cells. J. Immunol. 174: 7558-7563.
    Pubmed
  24. Pene, J., F. Rousset, F. Briere, I. Chretien, J. Wideman, J. Y. Bonnefoy, et al. 1988. Interleukin 5 enhances interleukin 4induced IgE production by normal human B cells. The role of soluble CD23 antigen. Eur. J. Immunol. 18: 929-935.
    Pubmed CrossRef
  25. Peng, S., J. Y. Lin, and M. Y. Lin. 2007. Antiallergic effect of milk fermented with lactic acid bacteria in a murine animal model. J. Agric. Food Chem. 55: 5092-5096.
    Pubmed CrossRef
  26. Powrie, F. and R. L. Coffman. 1993. Cytokine regulation of Tcell function: Potential for therapeutic intervention. Immunol. Today 14: 270-274.
    CrossRef
  27. Segawa, S., Y. Nakakita, Y. Takata, Y. Wakita, T. Kaneko, H. Kaneda, et al. 2008. 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. 121: 1-10.
    Pubmed CrossRef
  28. Seiskari, T., A. Kondrashova, H. Viskari, M. Kaila, A. M. Haapala, J. Aittoniemi, et al. 2007. Allergic sensitization and microbial load - a comparison between Finland and Russian Karelia. Clin. Exp. Immunol. 148: 47-52.
    Pubmed PMC CrossRef
  29. Shek, L. P. and B. W. Lee. 2006. Food allergy in Asia. Curr. Opin. Allergy Clin. Immunol. 6: 197-201.
    Pubmed CrossRef
  30. Sokol, C. L., G. M. Barton, A. G. Farr, and R. Medzhitov. 2008. A mechanism for the initiation of allergen-induced T helper type 2 responses. Nat. Immunol. 9: 310-318.
    Pubmed CrossRef
  31. Taylor, R. C., P. Richmond, and J. W. Upham. 2006. Toll-like receptor 2 ligands inhibit TH2 responses to mite allergen. J. Allergy Clin. Immunol. 117: 1148-1154.
    Pubmed CrossRef
  32. Temblay, J. N., E. Bertelli, J. L. Arques, M. Regoli, and C. Nicoletti. 2007. Production of IL-12 by Peyer patch-dendritic cells is critical for the resistance to food allergy. J. Allergy Clin. Immunol. 120: 659-665.
    Pubmed CrossRef
  33. Torii, A., S. Torii, S. Fujiwara, H. Tanaka, N. Inagaki, and H. Nagai. 2007. Lactobacillus acidophilus strain L-92 regulates the production of Th1 cytokine as well as Th2 cytokines. Allergol. Int. 56: 293-301.
    Pubmed CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2013; 23(5): 724-730

Published online May 25, 2013 https://doi.org/10.4014/jmb.1211.11079

Copyright © The Korean Society for Microbiology and Biotechnology.

Immunomodulatory and Anti-Allergic Effects of Orally Administered Lactobacillus Species in Ovalbumin-Sensitized Mice

Jeongmin Lee 1, 2, Jieun Bang 1 and Hee-Jong Woo 1*

1Laboratory of Immunology, College of Veterinary Medicine, Seoul National University, Seoul 151-742, Korea, 2Division of Zoonoses, Center for Immunology and Pathology, National Institute of Health, Korea Centers for Disease Control and Prevention, Cheongwon-gun, Chungcheongbuk-do 363-951, Korea

Received: November 28, 2012; Accepted: January 8, 2013

Abstract

We investigated the effects of orally administered probiotic
bacteria (Lactobacillus species) as allergic immune modulators
in ovalbumin (OVA)-sensitized mice. BALB/c mice were
intraperitoneally injected with OVA twice at a 2-week
interval for allergy sensitization. The mice were then
orally administered Lactobacillus casei YIT9029 (L1), L.
casei HY7201 (L2), L. brevis HY7401 (L3), or L. plantarum
HY20301 (L4) every 2 days for 3 weeks. Total IgE levels
significantly decreased in sera of L3-administered mice
but increased in the other groups. OVA-specific IgE levels
decreased slightly in sera of mice administered L1, L3,
and L4 but increased significantly in L2-administered
mice. In passive cutaneous anaphylaxis (PCA) using sera
from administered mice, only the L3-administered group
showed reaction inhibition. High expression of TLR-2
with interferon (IFN)-γ stimulation on peripheral blood
mononuclear cells occurred in L3- or L4-administered
mice. Th1 cytokines, including IFN-γ and interleukin (IL)-
12, increased in splenocytes of L3-administered mice;
however, IL-4 decreased in L1- and L4-administered groups;
IL-5 decreased in all experimental groups. IL-6 decreased
in the L3-administered group; and IL-10 decreased in
L1-, L2-, and L3-administered groups. L3 induced antiallergic
effects by increasing Th1 cytokines, decreasing
Th2 cytokines, and inhibiting the PCA reaction, whereas
L2 administration increased allergic effects.

Keywords: allergy, oral administration, probiotics, Lactobacillus

References

  1. Borchers, A. T., C. Selmi, F. J. Meyers, C. L. Keen, and M. E. Gershwin. 2009. Probiotics and immunity. J. Gastroenterol. 44:26-46.
    Pubmed CrossRef
  2. Frossard, C. P. and P. A. Eigenmann. 2008. The role of IL-10 in preventing food-induced anaphylaxis. Expert Opin. Biol. Ther. 8: 1309-1317.
    Pubmed CrossRef
  3. Fujiwara, D., S. Inoue, H. Wakabayashi, and T. Fujii. 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.
    Pubmed CrossRef
  4. Fuller, R. 1989. Probiotics in man and animals. J. Appl. Bacteriol. 66: 365-378.
    Pubmed CrossRef
  5. Gajewski, T. F., E. Goldwasser, and F. W. Fitch. 1988. Antiproliferative effect of IFN-gamma in immune regulation. II. IFN-gamma inhibits the proliferation of murine bone marrow cells stimulated with IL-3, IL-4, or granulocyte-macrophage colony-stimulating factor. J. Immunol. 141: 2635-2642.
    Pubmed
  6. Gill, H. and J. Prasad. 2008. Probiotics, immunomodulation, and health benefits. Adv. Exp. Med. Biol. 606: 423-454.
    Pubmed CrossRef
  7. Huang, J., Y. Zhong, W. Cai, H. Zhang, W. Tang, and B. Chen. 2010. The effects of probiotics supplementation timing on an ovalbumin-sensitized rat model. FEMS Immunol. Med. Microbiol. 60: 132-141.
    Pubmed CrossRef
  8. Kaisho, T. and S. Akira. 2006. Toll-like receptor function and signaling. J. Allergy Clin. Immunol. 117: 979-987; quiz 988.
    Pubmed CrossRef
  9. Kim, H., K. Kwack, D. Y. Kim, and G. E. Ji. 2005. Oral probiotic bacterial administration suppressed allergic responses in an ovalbumin-induced allergy mouse model. FEMS Immunol. Med. Microbiol. 45: 259-267.
    Pubmed CrossRef
  10. Kim, H., S. Y. Lee, and G. E. Ji. 2005. Timing of Bifidobacterium administration influences the development of allergy to ovalbumin in mice. Biotechnol. Lett. 27: 1361-1367.
    Pubmed CrossRef
  11. Kim, J. Y., Y. O. Choi, and G. E. Ji. 2008. Effect of oral probiotics (Bifidobacterium lactis AD011 and Lactobacillus acidophilus AD031) administration on ovalbumin-induced food allergy mouse model. J. Microbiol. Biotechnol. 18: 1393-1400.
    Pubmed
  12. Kindt, T. J., R. A. Goldsby, B. A. Osborne, and J. Kuby. 2007. Kuby immunology, pp. xxii, 574, A-531, G-512, AN-527, I527, 6th Ed. W. H. Freeman, New York.
  13. Kubota, E., T. Joh, S. Tanida, M. Sasaki, H. Kataoka, K. Watanabe, et al. 2005. Oral vaccination against Helicobacter pylori with recombinant cholera toxin B-subunit. Helicobacter 10: 345-352.
    Pubmed CrossRef
  14. Kwak, C., B. C. Jeong, J. H. Ku, H. H. Kim, J. J. Lee, C. S. Huh, Y. J. Baek, et al. 2006. Prevention of nephrolithiasis by Lactobacillus in stone-forming rats: A preliminary study. Urol. Res. 34: 265-270.
    Pubmed CrossRef
  15. Lee, H. S., S. Y. Han, E. A. Bae, C. S. Huh, Y. T. Ahn, J. H. Lee, et al. 2008. Lactic acid bacteria inhibit proinflammatory cytokine expression and bacterial glycosaminoglycan degradation activity in dextran sulfate sodium-induced colitic mice. Int. Immunopharmacol. 8: 574-580.
    Pubmed CrossRef
  16. Lee, J. and H. J. Woo. 2010. Antigenicity of partial fragments of recombinant Pasteurella multocida toxin. J. Microbiol. Biotechnol. 20: 1756-1763.
    Pubmed
  17. Lewkowich, I. P., J. D. Rempel, and K. T. HayGlass. 2004. In vivo IgE levels in exogenous antigen stimulated responses:Measurement of total IgE as a valid, simple surrogate for Agspecific IgE. J. Immunol. Methods 286: 123-132.
    Pubmed CrossRef
  18. Masood, M. I., M. I. Qadir, J. H. Shirazi, and I. U. Khan. 2011. Beneficial effects of lactic acid bacteria on human beings. Crit. Rev. Microbiol. 37: 91-98.
    Pubmed CrossRef
  19. Matsuzaki, T., R. Yamazaki, S. Hashimoto, and T. Yokokura. 1998. The effect of oral feeding of Lactobacillus casei strain Shirota on immunoglobulin E production in mice. J. Dairy Sci. 81: 48-53.
    CrossRef
  20. Nonaka, Y., T. Izumo, F. Izumi, T. Maekawa, H. Shibata, A. Nakano, et al. 2008. Antiallergic effects of Lactobacillus pentosus strain S-PT84 mediated by modulation of Th1/Th2 immunobalance and induction of IL-10 production. Int. Arch. Allergy Immunol. 145: 249-257.
    Pubmed CrossRef
  21. Ohno, H., S. Tsunemine, Y. Isa, M. Shimakawa, and H. Yamamura. 2005. Oral administration of Bifidobacterium bifidum G9-1 suppresses total and antigen specific immunoglobulin E production in mice. Biol. Pharm. Bull. 28: 1462-1466.
    Pubmed CrossRef
  22. Okudaira, H., T. Suzuki, and T. Ogita. 1980. A study of the rat passive cutaneous anaphylaxis (PCA) reaction for the assay of mouse IgE antibody. J. Immunol. Methods 33: 369-377.
    CrossRef
  23. Patel, M., D. Xu, P. Kewin, B. Choo-Kang, C. McSharry, N. C. Thomson, et al. 2005. TLR2 agonist ameliorates established allergic airway inflammation by promoting Th1 response and not via regulatory T cells. J. Immunol. 174: 7558-7563.
    Pubmed
  24. Pene, J., F. Rousset, F. Briere, I. Chretien, J. Wideman, J. Y. Bonnefoy, et al. 1988. Interleukin 5 enhances interleukin 4induced IgE production by normal human B cells. The role of soluble CD23 antigen. Eur. J. Immunol. 18: 929-935.
    Pubmed CrossRef
  25. Peng, S., J. Y. Lin, and M. Y. Lin. 2007. Antiallergic effect of milk fermented with lactic acid bacteria in a murine animal model. J. Agric. Food Chem. 55: 5092-5096.
    Pubmed CrossRef
  26. Powrie, F. and R. L. Coffman. 1993. Cytokine regulation of Tcell function: Potential for therapeutic intervention. Immunol. Today 14: 270-274.
    CrossRef
  27. Segawa, S., Y. Nakakita, Y. Takata, Y. Wakita, T. Kaneko, H. Kaneda, et al. 2008. 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. 121: 1-10.
    Pubmed CrossRef
  28. Seiskari, T., A. Kondrashova, H. Viskari, M. Kaila, A. M. Haapala, J. Aittoniemi, et al. 2007. Allergic sensitization and microbial load - a comparison between Finland and Russian Karelia. Clin. Exp. Immunol. 148: 47-52.
    Pubmed KoreaMed CrossRef
  29. Shek, L. P. and B. W. Lee. 2006. Food allergy in Asia. Curr. Opin. Allergy Clin. Immunol. 6: 197-201.
    Pubmed CrossRef
  30. Sokol, C. L., G. M. Barton, A. G. Farr, and R. Medzhitov. 2008. A mechanism for the initiation of allergen-induced T helper type 2 responses. Nat. Immunol. 9: 310-318.
    Pubmed CrossRef
  31. Taylor, R. C., P. Richmond, and J. W. Upham. 2006. Toll-like receptor 2 ligands inhibit TH2 responses to mite allergen. J. Allergy Clin. Immunol. 117: 1148-1154.
    Pubmed CrossRef
  32. Temblay, J. N., E. Bertelli, J. L. Arques, M. Regoli, and C. Nicoletti. 2007. Production of IL-12 by Peyer patch-dendritic cells is critical for the resistance to food allergy. J. Allergy Clin. Immunol. 120: 659-665.
    Pubmed CrossRef
  33. Torii, A., S. Torii, S. Fujiwara, H. Tanaka, N. Inagaki, and H. Nagai. 2007. Lactobacillus acidophilus strain L-92 regulates the production of Th1 cytokine as well as Th2 cytokines. Allergol. Int. 56: 293-301.
    Pubmed CrossRef