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Research article

Microbial Cell Biology

Different Immune Regulatory Potential of Lactobacillus plantarum and Lactobacillus sakei Isolated from Kimchi

Yi-Fan Hong 1, 2, Hangeun Kim 1, 3, Hye Rim Kim 1, Min Geun Gim 1 and Dae Kyun Chung 1, 2, 3*

1Graduate School of Biotechnology and Institute of Life Science and Resources, Kyung Hee University, Yongin 446-701, Republic of Korea , 2Skin Biotechnology Center, Kyung Hee University, Yongin 449-701, Republic of Korea, 3RNA Inc., #308 College of Life Science, Kyung Hee University, Yongin 449-701, Republic of Korea

Received: June 23, 2014; Accepted: August 4, 2014

J. Microbiol. Biotechnol. 2014; 24(12): 1629-1635

Published December 28, 2014 https://doi.org/10.4014/jmb.1406.06062

Copyright © The Korean Society for Microbiology and Biotechnology.

Abstract

It is known that lactic acid bacteria (LAB) have many beneficial health effects, including antioxidative activity and immune regulation. In this study, the immune regulatory effects of Lactobacillus sakei and Lactobacillus plantarum, which are found in different types of kimchi, were evaluated. L. sakei and its lipoteichoic acid (LTA) have greater immune stimulating potential in IL-12, IFN-γ, and TNF-α production as compared with L. plantarum in an in vitro condition. On the other hand, L. plantarum is assumed to repress the Th1 immune response in murine experiments. After being injected with LPS, L. plantarum-fed mice maintained a healthier state, and the level of TNF-α in their blood was lower than in other bacterial strainfed mice and in the LPS-only control mice. Additionally, IL-12 production was significantly decreased and the production of IL-4 was greatly increased in the splenocytes from L. plantarum-fed mice. Further experiments revealed that the pre-injection of purified LTA from L. plantarum (pLTA), L. sakei (sLTA), and S. aureus (aLTA) decreased TNF-α and IL-4 production in LPS-injected mice. Mouse IL-12, however, was significantly increased by aLTA pre-injection. In conclusion, the L. sakei and L. plantarum strains have immune regulation effects, but the effects differ in cytokine production and the regulatory effects of the Th1/Th2 immune response.

Keywords

Lactobacillus plantarum, Lactobacillus sakei, Kimchi, Cytokine, lipoteichoic acid, Immune regulation

References

  1. Adlerberth I, Ahrne S, Johansson ML, Molin G, Hanson LA, Wold AE. 1996. A mannose-specific adherence mechanism in Lactobacillus plantarum c onferring binding to the human colonic cell line HT-29. Appl. Environ. Microbiol. 62: 2244-2251.
    Pubmed
  2. Adlerberth I, Hanson LA, Svanborg C, Svennerholm AM, Nordgren S, Wold AE. 1995. Adhesins of Escherichia coli associated with extra-intestinal pathogenicity confer binding to colonic epithelial cells. Microb. Pathog. 18: 373-385.
    Pubmed CrossRef
  3. Borchers AT, Keen CL, Gershwin ME. 2002. The influence of yogurt/Lactobacillus on the innate and acquired immune response. Clin. Rev. Allergy Immunol. 22: 207-230.
    Pubmed CrossRef
  4. Cho YR, Chang JY, Chang HC. 2007. Production of gammaaminobutyric acid (GABA) by Lactobacillus buchneri isolated from kimchi and its neuroprotective effect on neuronal cells. J. Microbiol. Biotechnol. 17: 104-109.
    Pubmed
  5. D'Elios M, Del Prete G. 1998. Th1/Th2 balance in human disease. Transplant Proc. 30: 2373-2377.
    CrossRef
  6. de Oliveira VM, Manfio GP, da Costa Coutinho HL, KeijzerWolters AC, van Elsas JD. 2006. A ribosomal RNA gene intergenic spacer based PCR and DGGE fingerprinting method for the analysis of specific rhizobial communities in soil. J. Microbiol. Methods 64: 366-379.
    Pubmed CrossRef
  7. Duguid JP. 1959. Fimbriae and adhesive properties in Klebsiella strains. J. Gen. Microbiol. 21: 271-286.
    Pubmed CrossRef
  8. Engvall E, Perlmann P. 1972. Enzyme-linked immunosorbent assay, ELISA. III. Quantitation of specific antibodies by enzyme-labeled anti-immunoglobulin in antigen-coated tubes. J. Immunol. 109: 129-135.
    Pubmed
  9. Finegold SM, Attebery HR, Sutter VL. 1974. Effect of diet on human faecal flora: comparison of Japanese and American diets. Am. J. Clin. Nutr. 27: 1546-1569.
  10. Grangette C, Nutten S, Palumbo E, Morath S, Hermann C, Dewulf J, et al. 2005. Enhanced antiinflammatory capacity of a Lactobacillus plantarum mutant synthesizing modified teichoic acids. Proc. Natl. Acad. Sci. USA 102: 10321-10326.
    Pubmed CrossRef
  11. Gustafsson BE. 1959. Light weight stainless steel systems for rearing germfree animals. Ann. NY Acad. Sci. 78: 17-28.
    Pubmed CrossRef
  12. Han SH, Kim JH, Martin M, Michalek SM, Nahm MH. 2003. Pneumococcal lipoteichoic acid (LTA) is not as potent as staphylococcal LTA in stimulating Toll-like receptor 2. Infect. Immun. 71: 5541-5548.
    Pubmed CrossRef
  13. Herías MV, Midtvedt T, Hanson LA, Wold AE. 1995. Role of Escherichia coli P fimbriae in intestinal colonization in gnotobiotic rats. Infect. Immun. 63: 4781-4789.
    Pubmed
  14. Isolauri E, Sütas Y, Kankaanpää P, Arvilommi H, Salminen S. 2001. Probiotics: effects on immunity. Am. J. Clin. Nutr. 73(2 Suppl): 444S-450S.
    Pubmed
  15. Johansson ML, Molin G, Jeppsson B, Nobaek S, Ahrné S, Bengmark S. 1993. Administration of different Lactobacillus strains in fermented oatmeal soup: in vivo colonization of human intestinal mucosa and effect on the indigenous flora. Appl. Environ. Microbiol. 59: 15-20.
    Pubmed
  16. Kaila M, Isolauri E, Soppi E, Virtanen E, Laine S, Arvilommi H. 1992. Enhancement of the circulating antibody secreting cell response in human diarrhea by a human Lactobacillus strain. Pediatr. Res. 32: 141-144.
    Pubmed CrossRef
  17. Kandler O, Weiss N. 1986. Regular, non-sporing, gram positive rods. Bergey's Manual Syst. Bacteriol. 2: 1208-1234.
  18. Kim HG, Gim MG, Kim JY, Hwang HJ, Ham MS, Lee JM, et al. 2007. Lipoteichoic acid from Lactobacillus plantarum elicits both the production of interleukin-23p19 and suppression of pathogen mediated interleukin-10 in THP-1 cells. FEMS Immunol. Med. Microbiol. 49: 205-214.
    Pubmed CrossRef
  19. Kim HG, Kim NR, Gim MG, Lee JM, Lee SY, Ko MY, et al. 2008. Lipoteichoic Acid Isolated from Lactobacillus plantarum Inhibits Lipopolysaccharide-Induced TNF-alpha Production in THP-1 Cells and Endotoxin Shock in Mice. J. Immunol. 180: 2553-2561.
    Pubmed CrossRef
  20. Kim M, Chun J. 2005. Bacterial community structure in kimchi, a Korean fermented vegetable food, as revealed by 16S rRNA gene analysis. Int. J. Food Microbiol. 103: 91-96.
    Pubmed CrossRef
  21. Lee KH, Park JY, Jeong SJ, Kwon GH, Lee HJ, Chang HC, et al. 2007. Characterization of paraplantaricin C7, a novel bacteriocin produced by Lactobacillus paraplantarum C7 isolated from kimchi. J. Microbiol. Biotechnol. 17:287-296.
    Pubmed
  22. Madsen K. 2006. Probiotics and the immune response. J. Clin. Gastroenterol. 40: 232-234.
    Pubmed CrossRef
  23. Mao Y, Nobaek S, Kasravi B, Adawi D, Stenram U, Molin G, Jeppsson B. 1996. The effects of Lactobacillus strains, and oat fiber on methotrexate-induced enterocolitis in rats. Gastroenterology 111: 334-344.
    Pubmed CrossRef
  24. Molin G, Jeppsson B, Johansson ML, Ahrné S, Nobaek S, Ståhl M, Bengmark S. 1993. Numerical taxonomy of Lactobacillus spp. associated with healthy and diseased mucosa of the human intestines. J. Appl. Bacteriol. 74: 314323.
    CrossRef
  25. O’Hagan DT, MacKichan ML, Singh M. 2001. Recent developments in adjuvants for vaccines against infectious diseases. Biomol. Eng. 18: 69-85.
    CrossRef
  26. Ouwehand AC, Salminen S, Isolauri E. 2002. Probiotics: an overview of beneficial effects. Antonie Van Leeuwenhoek 82:279-289.
    Pubmed CrossRef
  27. Perdigón G, Alvarez S, Pesce de Ruiz Holgado A. 1991. Immunoadjuvant activity of oral Lactobacillus casei: influence of dose on the secretory immune response and protective capacity in intestinal infections. J. Dairy Res. 58: 485-496.
    Pubmed CrossRef
  28. Sacchi CT, Whitney AM, Mayer LW, Morey R, Steigerwalt A, Boras A, et al. 2002. Sequencing of 16S rRNA gene: a rapid tool for identification of Bacillus anthracis. Emerg. Infect. Dis. 8: 1117-1123.
    Pubmed CrossRef
  29. Sato Y, Akiyama H, Suganuma H, Watanabe T, Nagaoka MH, Inakuma T, et al. 2004. The feeding of beta-carotene down-reg ulates s erum I gE levels a nd i nhibits the type I allergic response in mice. Biol. Pharm. Bull. 27: 978-984.
    Pubmed CrossRef
  30. Telemo E, Karlsson M, Dahlman-Höglund A, Dahlgren U, Lundin S. 1997. Oral tolerance in experimental animals. Int. Arch. Allergy Immunol. 113: 219-223.
    Pubmed CrossRef
  31. Wadolkowski EA, Laux DC, Cohen PS. 1988. Colonization of the streptomycin-treated mouse large intestine by a human fecal Escherichia coli strain: role of adhesion to mucosal receptors. Infect. Immun. 56: 1036-1043.
    Pubmed
  32. Wold AE, Thorssén M, Hull S, Edén CS. 1988. Attachment of Escherichia coli via mannose- or Galα1–4Galβ-containing receptors to human colonic epithelial cells. Infect. Immun. 56:2531-2537.
    Pubmed

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Article

Research article

J. Microbiol. Biotechnol. 2014; 24(12): 1629-1635

Published online December 28, 2014 https://doi.org/10.4014/jmb.1406.06062

Copyright © The Korean Society for Microbiology and Biotechnology.

Different Immune Regulatory Potential of Lactobacillus plantarum and Lactobacillus sakei Isolated from Kimchi

Yi-Fan Hong 1, 2, Hangeun Kim 1, 3, Hye Rim Kim 1, Min Geun Gim 1 and Dae Kyun Chung 1, 2, 3*

1Graduate School of Biotechnology and Institute of Life Science and Resources, Kyung Hee University, Yongin 446-701, Republic of Korea , 2Skin Biotechnology Center, Kyung Hee University, Yongin 449-701, Republic of Korea, 3RNA Inc., #308 College of Life Science, Kyung Hee University, Yongin 449-701, Republic of Korea

Received: June 23, 2014; Accepted: August 4, 2014

Abstract

It is known that lactic acid bacteria (LAB) have many beneficial health effects, including antioxidative
activity and immune regulation. In this study, the immune regulatory effects of
Lactobacillus sakei and Lactobacillus plantarum, which are found in different types of kimchi,
were evaluated. L. sakei and its lipoteichoic acid (LTA) have greater immune stimulating
potential in IL-12, IFN-γ, and TNF-α production as compared with L. plantarum in an in vitro
condition. On the other hand, L. plantarum is assumed to repress the Th1 immune response in
murine experiments. After being injected with LPS, L. plantarum-fed mice maintained a
healthier state, and the level of TNF-α in their blood was lower than in other bacterial strainfed
mice and in the LPS-only control mice. Additionally, IL-12 production was significantly
decreased and the production of IL-4 was greatly increased in the splenocytes from
L. plantarum-fed mice. Further experiments revealed that the pre-injection of purified LTA
from L. plantarum (pLTA), L. sakei (sLTA), and S. aureus (aLTA) decreased TNF-α and IL-4
production in LPS-injected mice. Mouse IL-12, however, was significantly increased by aLTA
pre-injection. In conclusion, the L. sakei and L. plantarum strains have immune regulation
effects, but the effects differ in cytokine production and the regulatory effects of the Th1/Th2
immune response.

Keywords: Lactobacillus plantarum, Lactobacillus sakei, Kimchi, Cytokine, lipoteichoic acid, Immune regulation

References

  1. Adlerberth I, Ahrne S, Johansson ML, Molin G, Hanson LA, Wold AE. 1996. A mannose-specific adherence mechanism in Lactobacillus plantarum c onferring binding to the human colonic cell line HT-29. Appl. Environ. Microbiol. 62: 2244-2251.
    Pubmed
  2. Adlerberth I, Hanson LA, Svanborg C, Svennerholm AM, Nordgren S, Wold AE. 1995. Adhesins of Escherichia coli associated with extra-intestinal pathogenicity confer binding to colonic epithelial cells. Microb. Pathog. 18: 373-385.
    Pubmed CrossRef
  3. Borchers AT, Keen CL, Gershwin ME. 2002. The influence of yogurt/Lactobacillus on the innate and acquired immune response. Clin. Rev. Allergy Immunol. 22: 207-230.
    Pubmed CrossRef
  4. Cho YR, Chang JY, Chang HC. 2007. Production of gammaaminobutyric acid (GABA) by Lactobacillus buchneri isolated from kimchi and its neuroprotective effect on neuronal cells. J. Microbiol. Biotechnol. 17: 104-109.
    Pubmed
  5. D'Elios M, Del Prete G. 1998. Th1/Th2 balance in human disease. Transplant Proc. 30: 2373-2377.
    CrossRef
  6. de Oliveira VM, Manfio GP, da Costa Coutinho HL, KeijzerWolters AC, van Elsas JD. 2006. A ribosomal RNA gene intergenic spacer based PCR and DGGE fingerprinting method for the analysis of specific rhizobial communities in soil. J. Microbiol. Methods 64: 366-379.
    Pubmed CrossRef
  7. Duguid JP. 1959. Fimbriae and adhesive properties in Klebsiella strains. J. Gen. Microbiol. 21: 271-286.
    Pubmed CrossRef
  8. Engvall E, Perlmann P. 1972. Enzyme-linked immunosorbent assay, ELISA. III. Quantitation of specific antibodies by enzyme-labeled anti-immunoglobulin in antigen-coated tubes. J. Immunol. 109: 129-135.
    Pubmed
  9. Finegold SM, Attebery HR, Sutter VL. 1974. Effect of diet on human faecal flora: comparison of Japanese and American diets. Am. J. Clin. Nutr. 27: 1546-1569.
  10. Grangette C, Nutten S, Palumbo E, Morath S, Hermann C, Dewulf J, et al. 2005. Enhanced antiinflammatory capacity of a Lactobacillus plantarum mutant synthesizing modified teichoic acids. Proc. Natl. Acad. Sci. USA 102: 10321-10326.
    Pubmed CrossRef
  11. Gustafsson BE. 1959. Light weight stainless steel systems for rearing germfree animals. Ann. NY Acad. Sci. 78: 17-28.
    Pubmed CrossRef
  12. Han SH, Kim JH, Martin M, Michalek SM, Nahm MH. 2003. Pneumococcal lipoteichoic acid (LTA) is not as potent as staphylococcal LTA in stimulating Toll-like receptor 2. Infect. Immun. 71: 5541-5548.
    Pubmed CrossRef
  13. Herías MV, Midtvedt T, Hanson LA, Wold AE. 1995. Role of Escherichia coli P fimbriae in intestinal colonization in gnotobiotic rats. Infect. Immun. 63: 4781-4789.
    Pubmed
  14. Isolauri E, Sütas Y, Kankaanpää P, Arvilommi H, Salminen S. 2001. Probiotics: effects on immunity. Am. J. Clin. Nutr. 73(2 Suppl): 444S-450S.
    Pubmed
  15. Johansson ML, Molin G, Jeppsson B, Nobaek S, Ahrné S, Bengmark S. 1993. Administration of different Lactobacillus strains in fermented oatmeal soup: in vivo colonization of human intestinal mucosa and effect on the indigenous flora. Appl. Environ. Microbiol. 59: 15-20.
    Pubmed
  16. Kaila M, Isolauri E, Soppi E, Virtanen E, Laine S, Arvilommi H. 1992. Enhancement of the circulating antibody secreting cell response in human diarrhea by a human Lactobacillus strain. Pediatr. Res. 32: 141-144.
    Pubmed CrossRef
  17. Kandler O, Weiss N. 1986. Regular, non-sporing, gram positive rods. Bergey's Manual Syst. Bacteriol. 2: 1208-1234.
  18. Kim HG, Gim MG, Kim JY, Hwang HJ, Ham MS, Lee JM, et al. 2007. Lipoteichoic acid from Lactobacillus plantarum elicits both the production of interleukin-23p19 and suppression of pathogen mediated interleukin-10 in THP-1 cells. FEMS Immunol. Med. Microbiol. 49: 205-214.
    Pubmed CrossRef
  19. Kim HG, Kim NR, Gim MG, Lee JM, Lee SY, Ko MY, et al. 2008. Lipoteichoic Acid Isolated from Lactobacillus plantarum Inhibits Lipopolysaccharide-Induced TNF-alpha Production in THP-1 Cells and Endotoxin Shock in Mice. J. Immunol. 180: 2553-2561.
    Pubmed CrossRef
  20. Kim M, Chun J. 2005. Bacterial community structure in kimchi, a Korean fermented vegetable food, as revealed by 16S rRNA gene analysis. Int. J. Food Microbiol. 103: 91-96.
    Pubmed CrossRef
  21. Lee KH, Park JY, Jeong SJ, Kwon GH, Lee HJ, Chang HC, et al. 2007. Characterization of paraplantaricin C7, a novel bacteriocin produced by Lactobacillus paraplantarum C7 isolated from kimchi. J. Microbiol. Biotechnol. 17:287-296.
    Pubmed
  22. Madsen K. 2006. Probiotics and the immune response. J. Clin. Gastroenterol. 40: 232-234.
    Pubmed CrossRef
  23. Mao Y, Nobaek S, Kasravi B, Adawi D, Stenram U, Molin G, Jeppsson B. 1996. The effects of Lactobacillus strains, and oat fiber on methotrexate-induced enterocolitis in rats. Gastroenterology 111: 334-344.
    Pubmed CrossRef
  24. Molin G, Jeppsson B, Johansson ML, Ahrné S, Nobaek S, Ståhl M, Bengmark S. 1993. Numerical taxonomy of Lactobacillus spp. associated with healthy and diseased mucosa of the human intestines. J. Appl. Bacteriol. 74: 314323.
    CrossRef
  25. O’Hagan DT, MacKichan ML, Singh M. 2001. Recent developments in adjuvants for vaccines against infectious diseases. Biomol. Eng. 18: 69-85.
    CrossRef
  26. Ouwehand AC, Salminen S, Isolauri E. 2002. Probiotics: an overview of beneficial effects. Antonie Van Leeuwenhoek 82:279-289.
    Pubmed CrossRef
  27. Perdigón G, Alvarez S, Pesce de Ruiz Holgado A. 1991. Immunoadjuvant activity of oral Lactobacillus casei: influence of dose on the secretory immune response and protective capacity in intestinal infections. J. Dairy Res. 58: 485-496.
    Pubmed CrossRef
  28. Sacchi CT, Whitney AM, Mayer LW, Morey R, Steigerwalt A, Boras A, et al. 2002. Sequencing of 16S rRNA gene: a rapid tool for identification of Bacillus anthracis. Emerg. Infect. Dis. 8: 1117-1123.
    Pubmed CrossRef
  29. Sato Y, Akiyama H, Suganuma H, Watanabe T, Nagaoka MH, Inakuma T, et al. 2004. The feeding of beta-carotene down-reg ulates s erum I gE levels a nd i nhibits the type I allergic response in mice. Biol. Pharm. Bull. 27: 978-984.
    Pubmed CrossRef
  30. Telemo E, Karlsson M, Dahlman-Höglund A, Dahlgren U, Lundin S. 1997. Oral tolerance in experimental animals. Int. Arch. Allergy Immunol. 113: 219-223.
    Pubmed CrossRef
  31. Wadolkowski EA, Laux DC, Cohen PS. 1988. Colonization of the streptomycin-treated mouse large intestine by a human fecal Escherichia coli strain: role of adhesion to mucosal receptors. Infect. Immun. 56: 1036-1043.
    Pubmed
  32. Wold AE, Thorssén M, Hull S, Edén CS. 1988. Attachment of Escherichia coli via mannose- or Galα1–4Galβ-containing receptors to human colonic epithelial cells. Infect. Immun. 56:2531-2537.
    Pubmed