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Research article

References

  1. Okada H, Kuhn C, Feillet H, Bach JF. 2010. The ‘hygiene hypothesis’ for autoimmune and allergic diseases: an update. Clin. Exp. Immunol. 160: 1-9.
    Pubmed PMC CrossRef
  2. Strachan DP. 1989. Hay fever, hygiene, and household size. Brit. Med. J. 299: 1259-1260.
    Pubmed PMC CrossRef
  3. Fahy JV. 2015. Type 2 inflammation in asthma - present in most, absent in many. Nat. Rev. Immunol. 15: 57-65.
    Pubmed PMC CrossRef
  4. Kaiko GE, Horvat JC, Beagley KW, Hansbro P M. 2 008. Immunological decision-making: how does the immune system decide to mount a helper T-cell response? Immunology 123:326-338.
    Pubmed PMC CrossRef
  5. Kay AB. 2001. Allergy and allergic diseases. First of two parts. N. Engl. J . Med. 344: 30-37.
    Pubmed CrossRef
  6. Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R. 2012. Diversity, stability and resilience of the human gut microbiota. Nature 489: 220-230.
    Pubmed PMC CrossRef
  7. Vieira AT, Teixeira MM, Martins FS. 2013. The role of probiotics and prebiotics in inducing gut immunity. Front. Immunol. 4: 445.
    Pubmed PMC CrossRef
  8. Jung JY, Lee SH, Kim JM, Park MS, Bae JW, Hahn Y, et al. 2011. Metagenomic analysis of kimchi, a traditional Korean fermented food. Appl. Environ. Microbiol. 77: 2264-2274.
    Pubmed PMC CrossRef
  9. Kang H , Myung E J, Ahn KS, Eom HJ, Han N S, Kim YB, et al. 2009. Induction of Th1 cytokines by Leuconostoc mesenteroides subsp. mesenteroides (KCTC 3100) under Th2type conditions and the requirement of NF-kappaB and p38/JNK. Cytokine 46: 283-289.
    Pubmed CrossRef
  10. Kang H, Oh YJ, Ahn KS, Eom HJ, Han N, Kim YB, Sohn NW. 2009. Leuconostoc citreum HJ-P4 (KACC 91035) regulates immunoglobulin E in an ovalbumin-induced allergy model and induces interleukin-12 through nuclear factor-kappa B and p38/c-Jun N-terminal kinases signaling in macrophages. Microbiol. Immunol. 53: 331-339.
    Pubmed CrossRef
  11. Kang H, Moon JS, Lee MG, Han NS. 2016. Immunomodulatory effects of Leuconostoc citreum EFEL2061 isolated from kimchi, a traditional Korean food, on the Th2 type-dominant immune response in vitro and in vivo. J Funct. Foods 20: 79-87.
    CrossRef
  12. Ha D, Cha D, Han S. 1994. Identification of bacteriocinproducing lactic acid bacteria from kimchi and partial characterization of their bacteriocin. J. Microbiol. Biotechnol. 4: 305-315.
  13. Moon GS, Kang CH, Pyun YR, Kim WJ. 2004. Isolation, identification, and characterization of a bacteriocin-producing Enterococcus sp. from kimchi and its application to kimchi fermentation. J. Microbiol. Biotechnol. 14: 924-931.
  14. Miettinen M, Matikainen S, Vuopio-Varkila J, Pirhonen J, Varkila K, Kurimoto M, Julkunen I. 1998. Lactobacilli and streptococci induce interleukin-12 (IL-12), IL-18, and gamma interferon production in human peripheral blood mononuclear cells. Infect. Immun. 66: 6058-6062.
    Pubmed PMC
  15. Mansour NM, Heine H, Abdou SM, Shenana ME, Zakaria MK, El-Diwany A. 2014. Isolation of Enterococcus faecium NM113, Enterococcus faecium NM213 and Lactobacillus casei NM512 as novel probiotics with immunomodulatory properties. Microbiol. Immunol. 58: 559-569.
    Pubmed CrossRef
  16. Noben-Trauth N, Hu-Li J , Paul W E. 2 000. C onventional, naive CD4+ T cells provide an initial source of IL-4 during Th2 differentiation. J. Immunol. 165: 3620-3625.
    Pubmed CrossRef
  17. Gould HJ, Sutton BJ. 2008. IgE in allergy and asthma today. Nat. Rev. Immunol. 8: 205-217.
    Pubmed CrossRef
  18. Shang XZ, Armstrong J, Yang GY, Volk A, Li J, Griswold DE, et al. 2004. Regulation of antigen-specific versus by-stander IgE production after antigen sensitization. Cell. Immunol. 229: 106-116.
    Pubmed CrossRef
  19. Pene J, Rousset F, Briere F, Chretien I, Bonnefoy JY, Spits H, et al. 1988. IgE production by normal human lymphocytes is induced by interleukin 4 and suppressed by interferons gamma and alpha and prostaglandin E2. Proc. Natl. Acad. Sci. USA 85: 6880-6884.
    Pubmed PMC CrossRef
  20. Karimi K, Inman MD, Bienenstock J, Forsythe P. 2009. Lactobacillus reuteri-induced regulatory T cells protect against an allergic airway response in mice. Am. J. Respir. Crit. Care Med. 179: 186-193.
    Pubmed CrossRef
  21. Feleszko W, Jaworska J, Rha RD, Steinhausen S, Avagyan A, Jaudszus A, et al. 2007. 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 37: 498-505.
    Pubmed CrossRef
  22. Kwon HK, Lee CG, So JS, Chae CS, Hwang J S, Sahoo A, et al. 2010. Generation of regulatory dendritic cells and CD4+Foxp3+ T cells by probiotics administration suppresses immune disorders. Proc. Natl. Acad. Sci. USA 107: 2159-2164.
    Pubmed PMC CrossRef
  23. Yoshida T, Fujiwara W, Enomoto M, Nakayama S, Matsuda H, Sugiyama H, et al. 2013. An increased number of CD4+CD25+ cells induced by an oral administration of Lactobacillus plantarum NRIC0380 are involved in antiallergic activity. Int. Arch. Allergy Immunol. 162: 283-289.
    Pubmed CrossRef
  24. Ozdemir C, Akdis M, Akdis CA. 2009. T regulatory cells and their counterparts: masters of immune regulation. Clin. Exp. Allergy 39: 626-639.
    Pubmed CrossRef
  25. Ling EM, Smith T , Nguyen XD, Pridgeon C, D allman M , Arbery J, et al. 2004. Relation of CD4+CD25+ regulatory Tcell suppression of allergen-driven T-cell activation to atopic status and expression of allergic disease. Lancet 363: 608-615.
    CrossRef

Article

Research article

J. Microbiol. Biotechnol. 2017; 27(6): 1071-1077

Published online June 28, 2017 https://doi.org/10.4014/jmb.1611.11020

Copyright © The Korean Society for Microbiology and Biotechnology.

Enterococcus faecium FC-K Derived from Kimchi Is a Probiotic Strain That Shows Anti-Allergic Activity

Man-Kwang Rho 1, Young-Eun Kim 1, Hyun-In Rho 2, Tae-Rahk Kim 3, Yoon-Bum Kim 4, Won-Kyung Sung 4, Taw-Woo Kim 2, Dae-Ok Kim 1 and Hee Kang 2*

1Department of Food Science and Biotechnology, College of Life Sciences, Kyung Hee University, Yongin 17104, Republic of Korea, 2Graduate School of East-West Medical Science, Kyung Hee University, Yongin 17104, Republic of Korea, 3Cellbion Co., Ltd, Sungnam 13605, Republic of Korea, 4Department of Oriental Dermatology, College of Korean Medicine, Kyung Hee University, Seoul 02447, Republic of Korea

Received: November 7, 2016; Accepted: March 15, 2017

Abstract

A rise in the occurrence of allergic diseases is attributed to the dysregulated balance of type 1/type
2 immunity, where type 2 T-helper (Th2) cells predominate over type 1 T-helper (Th1) cells,
leading to an abnormally increased production of IgE in response to unharmful antigens.
Kimchi, a traditional Korean fermented food, is a rich source of beneficial lactic acid bacteria.
In this study, we investigated the ability of Enterococcus faecium FC-K derived from kimchi to
induce type I immunity in the presence of Th2 polarizing conditions in vitro and in vivo.
Stimulation of mouse peritoneal macrophages with E. faecium FC-K induced the production of
tumor necrosis factor alpha, interleukin (IL)-6, and IL-12. Under the in vitro Th2 conditions in
which splenic T cells were activated in the presence of IL-4, E. faecium FC-K enhanced the
ability of T cells to produce interferon (IFN)-γ. Using the ovalbumin (OVA)-induced allergy
model, male BALB/c mice receiving E. faecium FC-K reduced the serum level of total IgE, but
not that of OVA-specific IgE. Furthermore, the population of activated splenic B cells during
OVA immunization was decreased in E. faecium FC-K-treated mice, accounting for a reduction
of total IgE in the serum. Restimulating splenocytes from OVA-immunized mice with OVA ex
vivo resulted in an increased production of IFN-γ, with no effect on IL-4, in E. faecium FC-Ktreated
mice. These observations provide the evidence that E. faecium FC-K can be a beneficial
probiotic strain that can modulate the Th2-mediated pathologic response.

Keywords: Enterococcus faecium, kimchi, T cells, allergy, IgE

References

  1. Okada H, Kuhn C, Feillet H, Bach JF. 2010. The ‘hygiene hypothesis’ for autoimmune and allergic diseases: an update. Clin. Exp. Immunol. 160: 1-9.
    Pubmed KoreaMed CrossRef
  2. Strachan DP. 1989. Hay fever, hygiene, and household size. Brit. Med. J. 299: 1259-1260.
    Pubmed KoreaMed CrossRef
  3. Fahy JV. 2015. Type 2 inflammation in asthma - present in most, absent in many. Nat. Rev. Immunol. 15: 57-65.
    Pubmed KoreaMed CrossRef
  4. Kaiko GE, Horvat JC, Beagley KW, Hansbro P M. 2 008. Immunological decision-making: how does the immune system decide to mount a helper T-cell response? Immunology 123:326-338.
    Pubmed KoreaMed CrossRef
  5. Kay AB. 2001. Allergy and allergic diseases. First of two parts. N. Engl. J . Med. 344: 30-37.
    Pubmed CrossRef
  6. Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R. 2012. Diversity, stability and resilience of the human gut microbiota. Nature 489: 220-230.
    Pubmed KoreaMed CrossRef
  7. Vieira AT, Teixeira MM, Martins FS. 2013. The role of probiotics and prebiotics in inducing gut immunity. Front. Immunol. 4: 445.
    Pubmed KoreaMed CrossRef
  8. Jung JY, Lee SH, Kim JM, Park MS, Bae JW, Hahn Y, et al. 2011. Metagenomic analysis of kimchi, a traditional Korean fermented food. Appl. Environ. Microbiol. 77: 2264-2274.
    Pubmed KoreaMed CrossRef
  9. Kang H , Myung E J, Ahn KS, Eom HJ, Han N S, Kim YB, et al. 2009. Induction of Th1 cytokines by Leuconostoc mesenteroides subsp. mesenteroides (KCTC 3100) under Th2type conditions and the requirement of NF-kappaB and p38/JNK. Cytokine 46: 283-289.
    Pubmed CrossRef
  10. Kang H, Oh YJ, Ahn KS, Eom HJ, Han N, Kim YB, Sohn NW. 2009. Leuconostoc citreum HJ-P4 (KACC 91035) regulates immunoglobulin E in an ovalbumin-induced allergy model and induces interleukin-12 through nuclear factor-kappa B and p38/c-Jun N-terminal kinases signaling in macrophages. Microbiol. Immunol. 53: 331-339.
    Pubmed CrossRef
  11. Kang H, Moon JS, Lee MG, Han NS. 2016. Immunomodulatory effects of Leuconostoc citreum EFEL2061 isolated from kimchi, a traditional Korean food, on the Th2 type-dominant immune response in vitro and in vivo. J Funct. Foods 20: 79-87.
    CrossRef
  12. Ha D, Cha D, Han S. 1994. Identification of bacteriocinproducing lactic acid bacteria from kimchi and partial characterization of their bacteriocin. J. Microbiol. Biotechnol. 4: 305-315.
  13. Moon GS, Kang CH, Pyun YR, Kim WJ. 2004. Isolation, identification, and characterization of a bacteriocin-producing Enterococcus sp. from kimchi and its application to kimchi fermentation. J. Microbiol. Biotechnol. 14: 924-931.
  14. Miettinen M, Matikainen S, Vuopio-Varkila J, Pirhonen J, Varkila K, Kurimoto M, Julkunen I. 1998. Lactobacilli and streptococci induce interleukin-12 (IL-12), IL-18, and gamma interferon production in human peripheral blood mononuclear cells. Infect. Immun. 66: 6058-6062.
    Pubmed KoreaMed
  15. Mansour NM, Heine H, Abdou SM, Shenana ME, Zakaria MK, El-Diwany A. 2014. Isolation of Enterococcus faecium NM113, Enterococcus faecium NM213 and Lactobacillus casei NM512 as novel probiotics with immunomodulatory properties. Microbiol. Immunol. 58: 559-569.
    Pubmed CrossRef
  16. Noben-Trauth N, Hu-Li J , Paul W E. 2 000. C onventional, naive CD4+ T cells provide an initial source of IL-4 during Th2 differentiation. J. Immunol. 165: 3620-3625.
    Pubmed CrossRef
  17. Gould HJ, Sutton BJ. 2008. IgE in allergy and asthma today. Nat. Rev. Immunol. 8: 205-217.
    Pubmed CrossRef
  18. Shang XZ, Armstrong J, Yang GY, Volk A, Li J, Griswold DE, et al. 2004. Regulation of antigen-specific versus by-stander IgE production after antigen sensitization. Cell. Immunol. 229: 106-116.
    Pubmed CrossRef
  19. Pene J, Rousset F, Briere F, Chretien I, Bonnefoy JY, Spits H, et al. 1988. IgE production by normal human lymphocytes is induced by interleukin 4 and suppressed by interferons gamma and alpha and prostaglandin E2. Proc. Natl. Acad. Sci. USA 85: 6880-6884.
    Pubmed KoreaMed CrossRef
  20. Karimi K, Inman MD, Bienenstock J, Forsythe P. 2009. Lactobacillus reuteri-induced regulatory T cells protect against an allergic airway response in mice. Am. J. Respir. Crit. Care Med. 179: 186-193.
    Pubmed CrossRef
  21. Feleszko W, Jaworska J, Rha RD, Steinhausen S, Avagyan A, Jaudszus A, et al. 2007. 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 37: 498-505.
    Pubmed CrossRef
  22. Kwon HK, Lee CG, So JS, Chae CS, Hwang J S, Sahoo A, et al. 2010. Generation of regulatory dendritic cells and CD4+Foxp3+ T cells by probiotics administration suppresses immune disorders. Proc. Natl. Acad. Sci. USA 107: 2159-2164.
    Pubmed KoreaMed CrossRef
  23. Yoshida T, Fujiwara W, Enomoto M, Nakayama S, Matsuda H, Sugiyama H, et al. 2013. An increased number of CD4+CD25+ cells induced by an oral administration of Lactobacillus plantarum NRIC0380 are involved in antiallergic activity. Int. Arch. Allergy Immunol. 162: 283-289.
    Pubmed CrossRef
  24. Ozdemir C, Akdis M, Akdis CA. 2009. T regulatory cells and their counterparts: masters of immune regulation. Clin. Exp. Allergy 39: 626-639.
    Pubmed CrossRef
  25. Ling EM, Smith T , Nguyen XD, Pridgeon C, D allman M , Arbery J, et al. 2004. Relation of CD4+CD25+ regulatory Tcell suppression of allergen-driven T-cell activation to atopic status and expression of allergic disease. Lancet 363: 608-615.
    CrossRef