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References

  1. Adams CA. 2010. The probiotic paradox: live and dead cells are biological response modifiers. Nutr. Res. Rev. 23: 37-46.
    Pubmed CrossRef
  2. Amrouche T, Boutin Y, Prioult G, Fliss I. 2006. Effects of bifidobacterial cytoplasm, cell wall and exopolysaccharide on mouse lymphocyte proliferation and cytokine production. Int. Dairy J. 16: 70-80.
    CrossRef
  3. Bogdan C. 2001. Nitric oxide and the immune response. Nat. Immunol. 2: 907-916.
    Pubmed CrossRef
  4. Chung HK. 1993. The physiological characteristics and immunological functions of lactic acid bacteria from kimchi. Kimchi Sci. Ind. 2: 23-28.
  5. Crome SQ, W ang AY, L evings M K. 2009. Translational mini-review series on Th17 cells: function and regulation of human T helper 17 cells in health and disease. Clin. Exp. Immunol. 159: 109-119.
    Pubmed PMC CrossRef
  6. de Oliveira SF, das Neves SP, de Melo CML, Teixeira EH, de Sousa CB, Pereira VAR, et al. 2011. Immunostimulatory activity of ConBr: a focus on splenocyte proliferation and proliferative cytokine secretion. Cell Tissue Res. 346: 237-244.
    Pubmed CrossRef
  7. de Petrino SF, de Jorrrat MEBB, Meson O, Perdigon G. 1995. Protective ability of certain lactic acid bacteria against an infection with Candida albicans in a mouse immunosuppression model by corticoid. Food Agric. Immnol. 7: 365-373.
    CrossRef
  8. de Vries MC, Vaughan EE, Kleerebezem M, de Vos WM. 2006. Lactobacillus plantarum - survival, functional and potential probiotic properties in the human intestinal tract. Int. Dairy J. 16: 1018-1028.
    CrossRef
  9. Ding AH, Nathan CF, Stuehr DJ. 1988. Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal-macrophages: comparison of activating cytokines and evidence for independent production. J. Immunol. 141: 2407-2412.
    Pubmed
  10. Erickson KL, Hubbard NE. 2000. Probiotic immunomodulation in health and disease. J. Nutr. 130: 403S-409S.
    Pubmed
  11. Gill HS. 1998. Stimulation of the immune system by lactic cultures. Int. Dairy J. 8: 535-544.
    CrossRef
  12. Gill HS, Rutherfurd KJ, Prasad J, Gopal PK. 2000. Enhancement of natural and acquired immunity by Lactobacillus rhamnosus (HN001), Lactobacillus acidophilus (HN017) and Bifidobacterium lactis (HN019). Br. J. Nutr. 83: 167-176.
    Pubmed CrossRef
  13. Gilliland SE, Morelli L, Reid G. 2001. Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. Paper presented at the Joint FAO/WHO expert consultation on evaluation of health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria, Córdoba, Argentina.
  14. Hasegawa H, Kan T. 2008. Immunity for longevity and lactic acid bacteria: the effect of nanometric particles of lactic acid bacteria on Th1 cell induction. New Food Ind. 50:1-8.
  15. Hessle C, Andersson B, Wold AE. 2000. Gram-positive bacteria are potent inducers of monocytic interleukin-12 (IL12) while gram-negative bacteria preferentially stimulate IL10 production. Infect. Immun. 68: 3581-3586.
    Pubmed PMC CrossRef
  16. Hong YF, Kim H, Kim HR, Gim MG, Chung DK. 2014. Different immune regulatory potential of Lactobacillus plantarum and Lactobacillus sakei isolated from kimchi. J. Microbiol. Biotechnol. 24: 1629-1635.
    Pubmed CrossRef
  17. Hur HJ, Lee KW, Lee HJ. 2004. Production of nitric oxide, tumor necrosis factor-α and interleukin-6 by RAW 264.7 macrophage cells treated with lactic acid bacteria isolated from kimchi. Biofactors 21: 123-125.
    Pubmed CrossRef
  18. Kaburagi T, Yamano T, Fukushima Y, Yoshino H, Mito N, Sato K. 2007. Effect of Lactobacillus johnsonii La1 on immune function and serum albumin in aged and malnourished aged mice. Nutrition 23: 342-350.
    Pubmed CrossRef
  19. 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
  20. Kan T, Ohwaki M. 2014. Lactobacillus having ability to induce IL-12 production, and method for culturing same. WO Patent, 2014/088183.
  21. Kanasugi H, Hasegawa T, Goto Y, Ohtsuka H, Makimura S, Yamamoto T. 1997. Single administration of enterococcal preparation (FK-23) augments non-specific immune responses in healthy dogs. Int. J. Immunopharmacol. 19: 655-659.
    CrossRef
  22. Kato I, Tanaka K, Yokokura T. 1999. Lactic acid bacterium potently induces the production of interleukin-12 and interferon-γ by mouse splenocytes. Int. J. Immunopharmacol. 21: 121-131.
    CrossRef
  23. Kidd P. 2003. Th1/Th2 balance: the hypothesis, its limitations, and implications for health and disease. Altern. Med. Rev. 8:223-246.
    Pubmed
  24. Kim HY, Yang JO, Ji GE. 2005. Effect of bifidobacteria on production of allergy-related cytokines from mouse spleen cells. J. Microbiol. Biotechnol. 15: 265-268.
  25. Kimura A, Kishimoto T. 2010. IL-6: regulator of Treg/Th17 balance. Eur. J. Immunol. 40: 1830-1835.
    Pubmed CrossRef
  26. Korn T, Bettelli E, O ukka M , Kuchroo VK. 2009. IL-17 and Th17 cells. Annu. Rev. Immunol. 27: 485-517.
    Pubmed CrossRef
  27. Lee HA, Bong YJ, Kim H, Jeong JK, Kim HY, Lee KW, et al. 2015. Effect of nanometric Lactobacillus plantarum in kimchi on dextran sulfate sodium-induced colitis in mice. J. Med. Food 18: 1073-1080.
    Pubmed CrossRef
  28. Lee HA, Kim H, Lee KW, Park KY. 2015. Dead nano-sized Lactobacillus plantarum inhibits azoxymethane/dextran sulfate sodium-induced colon cancer in Balb/c mice. J. Med. Food 18: 1400-1405.
    Pubmed CrossRef
  29. Makino S, Ikegami S, Kano H, Sashihara T, Sugano H, Horiuchi H, et al. 2006. Immunomodulatory effects of polysaccharides produced by Lactobacillus delbrueckii ssp. bulgaricus OLL1073R-1. J. Dairy Sci. 89: 2873-2881.
    CrossRef
  30. Matsuguchi T, Takagi A, Matsuzaki T, Nagaoka M, Ishikawa K, Yokokura T, et al. 2003. Lipoteichoic acids from Lactobacillus strains elicit strong tumor necrosis factor α-inducing activities in macrophages through Toll-like receptor 2. Clin. Diagn. Lab. Immunol. 10: 259-266.
    CrossRef
  31. Matsuzaki T, C hin J. 2000. Modulating immune r esponses with probiotic bacteria. Immunol. Cell Biol. 78: 67-73.
    Pubmed CrossRef
  32. Miura NN, Ohno N, Aketagawa J, Tamura H, Tanaka S, Yadomae T. 1996. Blood clearance of (1→3)-β-D-glucan in MRL lpr/lpr mice. FEMS Immunol. Med. Microbiol. 13: 51-57.
    CrossRef
  33. Mullié C, Yazourh A, Thibault H, Odou MF, Singer E, Kalach N, et al. 2004. Increased poliovirus-specific intestinal antibody response coincides with promotion of Bifidobacterium longum-infantis and Bifidobacterium breve in infants: a randomized, double-blind, placebo-controlled trial. Pediatr. Res. 56: 791-795.
    Pubmed CrossRef
  34. Murosaki S, Yamamoto Y, Ito K, Inokuchi T, Kusaka H, Ikeda H, et al. 1998. Heat-killed Lactobacillus plantarum L-137 suppresses naturally fed antigen-specific IgE production by stimulation of IL-12 production in mice. J. Allergy Clin. Immunol. 102: 57-64.
    CrossRef
  35. Rousset F, Garcia E, Defrance T, Peronne C, Vezzio N, Hsu DH, et al. 1992. Interleukin 10 is a potent growth and differentiation factor for activated human B lymphocytes. Proc. Natl. Acad. Sci. USA 89: 1890-1893.
    Pubmed PMC CrossRef
  36. Sakai Y, Tsukahara T, Bukawa W, Matsubara N, Ushida K. 2006. Cell preparation of Enterococcus faecalis strain EC-12 prevents vancomycin-resistant enterococci colonization in the cecum of newly hatched chicks. Poult. Sci. 85: 273-277.
    Pubmed CrossRef
  37. Seo JH, Lee H. 2007. Characteristics and immunomodulating activity of lactic acid bacteria for the potential probiotics. Korean J. Food Sci. Technol. 39: 681-687.
  38. Sharma R, Tiku AB. 2016. Emodin inhibits splenocyte proliferation and inflammation by modulating cytokine responses in a mouse model system. J. Immunotoxicol. 13: 2026.
    Pubmed CrossRef
  39. Sun Y, Sun T, Wang F, Zhang J, Li C, Chen X, et al. 2013. A polysaccharide from the fungi of Huaier exhibits anti-tumor potential and immunomodulatory effects. Carbohydr. Polym. 92: 577-582.
    Pubmed CrossRef
  40. Trinchieri G. 1994. Interleukin-12: a cytokine produced by antigen-presenting cells with immunoregulatory functions in the generation of T-helper cells type 1 and cytotoxic lymphocytes. Blood 84: 4008-4027.
    Pubmed
  41. Wagn er RD, Pierson C, Warner T, Dohnalek M, Hilty M, Balish E. 2000. Probiotic effects of feeding heat-killed Lactobacillus acidophilus and Lactobacillus casei to Candida albicans-colonized immunodeficient mice. J. Food Prot. 63: 638-644.

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Article

Research article

J. Microbiol. Biotechnol. 2016; 26(3): 469-476

Published online March 28, 2016 https://doi.org/10.4014/jmb.1511.11001

Copyright © The Korean Society for Microbiology and Biotechnology.

Dead Lactobacillus plantarum Stimulates and Skews Immune Responses toward T helper 1 and 17 Polarizations in RAW 264.7 Cells and Mouse Splenocytes

Hyun Ah Lee 1, 2, Hyunung Kim 3, Kwang-Won Lee 2 and Kun-Young Park 1*

1Kimchi Research Institute, Pusan National University, Busan 46241, Republic of Korea, 2Department of Biotechnology, College of Life Science and Biotechnology, Korea University, Seoul 02841, Republic of Korea, 3Biogenics Korea Co., Ltd., Seoul 06125, Republic of Korea

Received: November 2, 2015; Accepted: December 15, 2015

Abstract

This study was undertaken to evaluate the immunomodulatory effect of dead nano-sized
Lactobacillus plantarum (nLp) in RAW 264.7 cells and murine primary splenocytes. nLp is a
dead, shrunken, processed form of L. plantarum nF1 isolated from kimchi (a traditional Korean
fermented cabbage) and is less than 1 μm in size. It was found that nLp treatment stimulated
nitric oxide (NO) production more in RAW 264.7 macrophages than pure live L. plantarum
(pLp), and that the stimulatory properties were probably largely derived from its cell wall. In
addition, nLp induced murine splenocyte proliferation more so than pLp; in particular, a high
dose of nLp (1.0 × 1011 CFU/ml) stimulated proliferation as much as lipopolysaccharide at
2 μg/ml. Moreover, according to our cytokine profile results in splenocytes, nLp treatment
promoted Th1 (TNF-α, IL-12 p70) responses rather than Th2 (IL-4, IL-5) responses and also
increased Th17 (IL-6, IL-17A) responses. Thus, nLp stimulated NO release in RAW 264.7 cells
and induced splenocyte proliferation more so than pLp and stimulated Th1 and Th17 cytokine
production. These findings suggested that dead nLp has potential use as a functional food
ingredient to improve the immune response, and especially as a means of inducing Th1/Th17
immune responses.

Keywords: Dead nano-sized Lactobacillus plantarum, nitric oxide, RAW 264.7 macrophages, splenocyte, Th1/Th2/Th17 cytokine

References

  1. Adams CA. 2010. The probiotic paradox: live and dead cells are biological response modifiers. Nutr. Res. Rev. 23: 37-46.
    Pubmed CrossRef
  2. Amrouche T, Boutin Y, Prioult G, Fliss I. 2006. Effects of bifidobacterial cytoplasm, cell wall and exopolysaccharide on mouse lymphocyte proliferation and cytokine production. Int. Dairy J. 16: 70-80.
    CrossRef
  3. Bogdan C. 2001. Nitric oxide and the immune response. Nat. Immunol. 2: 907-916.
    Pubmed CrossRef
  4. Chung HK. 1993. The physiological characteristics and immunological functions of lactic acid bacteria from kimchi. Kimchi Sci. Ind. 2: 23-28.
  5. Crome SQ, W ang AY, L evings M K. 2009. Translational mini-review series on Th17 cells: function and regulation of human T helper 17 cells in health and disease. Clin. Exp. Immunol. 159: 109-119.
    Pubmed KoreaMed CrossRef
  6. de Oliveira SF, das Neves SP, de Melo CML, Teixeira EH, de Sousa CB, Pereira VAR, et al. 2011. Immunostimulatory activity of ConBr: a focus on splenocyte proliferation and proliferative cytokine secretion. Cell Tissue Res. 346: 237-244.
    Pubmed CrossRef
  7. de Petrino SF, de Jorrrat MEBB, Meson O, Perdigon G. 1995. Protective ability of certain lactic acid bacteria against an infection with Candida albicans in a mouse immunosuppression model by corticoid. Food Agric. Immnol. 7: 365-373.
    CrossRef
  8. de Vries MC, Vaughan EE, Kleerebezem M, de Vos WM. 2006. Lactobacillus plantarum - survival, functional and potential probiotic properties in the human intestinal tract. Int. Dairy J. 16: 1018-1028.
    CrossRef
  9. Ding AH, Nathan CF, Stuehr DJ. 1988. Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal-macrophages: comparison of activating cytokines and evidence for independent production. J. Immunol. 141: 2407-2412.
    Pubmed
  10. Erickson KL, Hubbard NE. 2000. Probiotic immunomodulation in health and disease. J. Nutr. 130: 403S-409S.
    Pubmed
  11. Gill HS. 1998. Stimulation of the immune system by lactic cultures. Int. Dairy J. 8: 535-544.
    CrossRef
  12. Gill HS, Rutherfurd KJ, Prasad J, Gopal PK. 2000. Enhancement of natural and acquired immunity by Lactobacillus rhamnosus (HN001), Lactobacillus acidophilus (HN017) and Bifidobacterium lactis (HN019). Br. J. Nutr. 83: 167-176.
    Pubmed CrossRef
  13. Gilliland SE, Morelli L, Reid G. 2001. Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. Paper presented at the Joint FAO/WHO expert consultation on evaluation of health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria, Córdoba, Argentina.
  14. Hasegawa H, Kan T. 2008. Immunity for longevity and lactic acid bacteria: the effect of nanometric particles of lactic acid bacteria on Th1 cell induction. New Food Ind. 50:1-8.
  15. Hessle C, Andersson B, Wold AE. 2000. Gram-positive bacteria are potent inducers of monocytic interleukin-12 (IL12) while gram-negative bacteria preferentially stimulate IL10 production. Infect. Immun. 68: 3581-3586.
    Pubmed KoreaMed CrossRef
  16. Hong YF, Kim H, Kim HR, Gim MG, Chung DK. 2014. Different immune regulatory potential of Lactobacillus plantarum and Lactobacillus sakei isolated from kimchi. J. Microbiol. Biotechnol. 24: 1629-1635.
    Pubmed CrossRef
  17. Hur HJ, Lee KW, Lee HJ. 2004. Production of nitric oxide, tumor necrosis factor-α and interleukin-6 by RAW 264.7 macrophage cells treated with lactic acid bacteria isolated from kimchi. Biofactors 21: 123-125.
    Pubmed CrossRef
  18. Kaburagi T, Yamano T, Fukushima Y, Yoshino H, Mito N, Sato K. 2007. Effect of Lactobacillus johnsonii La1 on immune function and serum albumin in aged and malnourished aged mice. Nutrition 23: 342-350.
    Pubmed CrossRef
  19. 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
  20. Kan T, Ohwaki M. 2014. Lactobacillus having ability to induce IL-12 production, and method for culturing same. WO Patent, 2014/088183.
  21. Kanasugi H, Hasegawa T, Goto Y, Ohtsuka H, Makimura S, Yamamoto T. 1997. Single administration of enterococcal preparation (FK-23) augments non-specific immune responses in healthy dogs. Int. J. Immunopharmacol. 19: 655-659.
    CrossRef
  22. Kato I, Tanaka K, Yokokura T. 1999. Lactic acid bacterium potently induces the production of interleukin-12 and interferon-γ by mouse splenocytes. Int. J. Immunopharmacol. 21: 121-131.
    CrossRef
  23. Kidd P. 2003. Th1/Th2 balance: the hypothesis, its limitations, and implications for health and disease. Altern. Med. Rev. 8:223-246.
    Pubmed
  24. Kim HY, Yang JO, Ji GE. 2005. Effect of bifidobacteria on production of allergy-related cytokines from mouse spleen cells. J. Microbiol. Biotechnol. 15: 265-268.
  25. Kimura A, Kishimoto T. 2010. IL-6: regulator of Treg/Th17 balance. Eur. J. Immunol. 40: 1830-1835.
    Pubmed CrossRef
  26. Korn T, Bettelli E, O ukka M , Kuchroo VK. 2009. IL-17 and Th17 cells. Annu. Rev. Immunol. 27: 485-517.
    Pubmed CrossRef
  27. Lee HA, Bong YJ, Kim H, Jeong JK, Kim HY, Lee KW, et al. 2015. Effect of nanometric Lactobacillus plantarum in kimchi on dextran sulfate sodium-induced colitis in mice. J. Med. Food 18: 1073-1080.
    Pubmed CrossRef
  28. Lee HA, Kim H, Lee KW, Park KY. 2015. Dead nano-sized Lactobacillus plantarum inhibits azoxymethane/dextran sulfate sodium-induced colon cancer in Balb/c mice. J. Med. Food 18: 1400-1405.
    Pubmed CrossRef
  29. Makino S, Ikegami S, Kano H, Sashihara T, Sugano H, Horiuchi H, et al. 2006. Immunomodulatory effects of polysaccharides produced by Lactobacillus delbrueckii ssp. bulgaricus OLL1073R-1. J. Dairy Sci. 89: 2873-2881.
    CrossRef
  30. Matsuguchi T, Takagi A, Matsuzaki T, Nagaoka M, Ishikawa K, Yokokura T, et al. 2003. Lipoteichoic acids from Lactobacillus strains elicit strong tumor necrosis factor α-inducing activities in macrophages through Toll-like receptor 2. Clin. Diagn. Lab. Immunol. 10: 259-266.
    CrossRef
  31. Matsuzaki T, C hin J. 2000. Modulating immune r esponses with probiotic bacteria. Immunol. Cell Biol. 78: 67-73.
    Pubmed CrossRef
  32. Miura NN, Ohno N, Aketagawa J, Tamura H, Tanaka S, Yadomae T. 1996. Blood clearance of (1→3)-β-D-glucan in MRL lpr/lpr mice. FEMS Immunol. Med. Microbiol. 13: 51-57.
    CrossRef
  33. Mullié C, Yazourh A, Thibault H, Odou MF, Singer E, Kalach N, et al. 2004. Increased poliovirus-specific intestinal antibody response coincides with promotion of Bifidobacterium longum-infantis and Bifidobacterium breve in infants: a randomized, double-blind, placebo-controlled trial. Pediatr. Res. 56: 791-795.
    Pubmed CrossRef
  34. Murosaki S, Yamamoto Y, Ito K, Inokuchi T, Kusaka H, Ikeda H, et al. 1998. Heat-killed Lactobacillus plantarum L-137 suppresses naturally fed antigen-specific IgE production by stimulation of IL-12 production in mice. J. Allergy Clin. Immunol. 102: 57-64.
    CrossRef
  35. Rousset F, Garcia E, Defrance T, Peronne C, Vezzio N, Hsu DH, et al. 1992. Interleukin 10 is a potent growth and differentiation factor for activated human B lymphocytes. Proc. Natl. Acad. Sci. USA 89: 1890-1893.
    Pubmed KoreaMed CrossRef
  36. Sakai Y, Tsukahara T, Bukawa W, Matsubara N, Ushida K. 2006. Cell preparation of Enterococcus faecalis strain EC-12 prevents vancomycin-resistant enterococci colonization in the cecum of newly hatched chicks. Poult. Sci. 85: 273-277.
    Pubmed CrossRef
  37. Seo JH, Lee H. 2007. Characteristics and immunomodulating activity of lactic acid bacteria for the potential probiotics. Korean J. Food Sci. Technol. 39: 681-687.
  38. Sharma R, Tiku AB. 2016. Emodin inhibits splenocyte proliferation and inflammation by modulating cytokine responses in a mouse model system. J. Immunotoxicol. 13: 2026.
    Pubmed CrossRef
  39. Sun Y, Sun T, Wang F, Zhang J, Li C, Chen X, et al. 2013. A polysaccharide from the fungi of Huaier exhibits anti-tumor potential and immunomodulatory effects. Carbohydr. Polym. 92: 577-582.
    Pubmed CrossRef
  40. Trinchieri G. 1994. Interleukin-12: a cytokine produced by antigen-presenting cells with immunoregulatory functions in the generation of T-helper cells type 1 and cytotoxic lymphocytes. Blood 84: 4008-4027.
    Pubmed
  41. Wagn er RD, Pierson C, Warner T, Dohnalek M, Hilty M, Balish E. 2000. Probiotic effects of feeding heat-killed Lactobacillus acidophilus and Lactobacillus casei to Candida albicans-colonized immunodeficient mice. J. Food Prot. 63: 638-644.