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References

  1. Gruver AL, Hudson LL, Sempowski GD. 2007. Immunosenescence of ageing. J. Pathol. 211: 144-156.
    Pubmed PMC CrossRef
  2. Castle SC. 2000. Clinical relevance of age-related immune dysfunction. Clin. Infect. Dis. 31: 578-585.
    Pubmed CrossRef
  3. Busse PJ, Mathur SK. 2010. Age-related changes in immune function: effect on airway inflammation. J. Allergy Clin. Immunol. 126: 690-699.
    Pubmed PMC CrossRef
  4. Gill HS, Rutherfurd KJ, Cross ML, Gopal PK. 2001. Enhancement of immunity in the elderly by dietary supplementation with the probiotic Bifidobacterium lactis HN019. Am. J. Clin. Nutr. 74: 833-839.
    Pubmed
  5. Yamada K, Tokunaga Y, Ikeda A, Ohkura K, Kaku-Ohkura S, Mamiya S, et al. 2003. Effect of dietary fiber on the lipid metabolism and immune function of aged Sprague-Dawley rats. Biosci. Biotechnol. Biochem. 67: 429-433.
    Pubmed CrossRef
  6. Meydani SN, Han SN, Wu D. 2005. Vitamin E and immune response in the aged: molecular mechanisms and clinical implications. Immunol. Rev. 205: 269-284.
    Pubmed CrossRef
  7. Fuller R. 1989. Probiotics in man and animals. J. Appl. Bacteriol. 66: 365-378.
    Pubmed CrossRef
  8. Ashraf R, Shah NP. 2014. Immune system stimulation by probiotic microorganisms. Crit. Rev. Food Sci. Nutr. 54: 938-956.
    Pubmed CrossRef
  9. Rolfe RD. 2000. The role of probiotic cultures in the control of gastrointestinal health. J. Nutr. 130: 396S-402S.
    Pubmed
  10. Pae M, Meydani SN, Wu D. 2012. The role of nutrition in enhancing immunity in aging. Aging Dis. 3: 91-129.
    Pubmed
  11. Duncan SH, Flint HJ. 2013. Probiotics and prebiotics and health in ageing populations. Maturitas 75: 44-50.
    Pubmed CrossRef
  12. Bjorkroth KJ, Schillinger U, Geisen R, Weiss N, Hoste B, Holzapfel WH, et al. 2002. Taxonomic study of Weissella confusa and description of Weissella cibaria sp. nov., detected in food and clinical samples. Int. J. Syst. Evol. Microbiol. 52: 141-148.
    Pubmed CrossRef
  13. Kang MS, Lim HS, Kim SM, Lee HC, Oh JS. 2011. Effect of Weissella cibaria on Fusobacterium nucleatum-induced interleukin-6 and interleukin-8 production in KB cells. J. Bacteriol. Virol. 41: 10.
    CrossRef
  14. Ahn SB, Park HE, Lee SM, Kim SY, Shon MY, Lee WK. 2013. Characteristics and immuno-modulatory effects of Weissella cibaria JW15 isolated from kimchi, Korea traditional fermented food, for probiotic use. J. Biomed. Res. 14: 206-212.
    CrossRef
  15. Choi HJ, Shin MS, Lee SM, Lee WK. 2012. Immunomodulatory properties of Enterococcus faecium JWS 833 isolated from duck intestinal tract and suppression of Listeria monocytogenes infection. Microbiol. Immunol. 56: 613-620.
    Pubmed CrossRef
  16. Jang SE, Joh EH, Ahn YT, Huh CS, Han MJ, Kim DH. 2013. Lactobacillus casei HY7213 ameliorates cyclophosphamideinduced immunosuppression in mice by activating NK, cytotoxic T cells and macrophages. Immunopharm. Immunotoxicol. 35: 396-402.
    Pubmed CrossRef
  17. 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
  18. Seo DW, Cho YI, Gu S, Kim DH, Park JH, Yi YJ, et al. 2016. A hot water extract of Aralia cordata activates bone marrowderived macrophages via a myeloid differentiation protein 88-dependent pathway and protects mice from bacterial infection. Microbiol. Immunol. 60: 343-355.
    Pubmed CrossRef
  19. Park HE, Lee WK. 2017. Immunomodulatory effects of mixed Weissella cibaria JW15 with water extract of black soybean and burdock on Listeria monocytogenes infection in mice. J. Biomed. Transl. Res. 18: 1-6.
  20. Hori Y, Perkins EH, Halsall MK. 1973. Decline in phytohemagglutinin responsiveness of spleen cells from aging mice. Proc. Soc. Exp. Biol. Med. 144: 48-53.
    Pubmed CrossRef
  21. Cyster JG. 1999. Chemokines and cell migration in secondary lymphoid organs. Science 286: 2098-2102.
    Pubmed CrossRef
  22. Le Couteur DG, Tay SS, Solon-Biet S, Bertolino P, McMahon AC, Cogger VC, et al. 2015. The influence of macronutrients on splanchnic and hepatic lymphocytes in aging mice. J. Gerontol. A Biol. Sci. Med. Sci. 70: 1499-1507.
    Pubmed CrossRef
  23. Kaushal D, Kansal VK. 2012. Probiotic Dahi containing Lactobacillus acidophilus and Bifidobacterium bifidum alleviates age-inflicted oxidative stress and improves expression of biomarkers of ageing in mice. Mol. Biol. Rep. 39: 1791-1799.
    Pubmed CrossRef
  24. Beli E, Duriancik DM, Clinthorne JF, Lee T, Kim S, Gardner EM. 2014. Natural killer cell development and maturation in aged mice. Mech. Ageing Dev. 135: 33-40.
    Pubmed PMC CrossRef
  25. Kared H, Camous X, Larbi A. 2014. T cells and their cytokines in persistent stimulation of the immune system. Curr. Opin. Immunol. 29: 79-85.
    Pubmed CrossRef
  26. Sharma R, Kapila R, Dass G, Kapila S. 2014. Improvement in Th1/Th2 immune homeostasis, antioxidative status and resistance to pathogenic E. coli on consumption of probiotic Lactobacillus rhamnosus fermented milk in aging mice. Age 36: 9686.
    Pubmed PMC CrossRef
  27. Fu YR, Yi ZJ, Pei JL, Guan S. 2010. Effects of Bifidobacterium bifidum on adaptive immune senescence in aging mice. Microbiol. Immunol. 54: 578-583.
    CrossRef
  28. Shaw AC, Joshi S , Greenwood H, P anda A, Lord JM. 2 010. Aging of the innate immune system. Curr. Opin. Immunol. 22: 507-513.
    Pubmed PMC CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2017; 27(12): 2094-2103

Published online December 28, 2017 https://doi.org/10.4014/jmb.1708.08016

Copyright © The Korean Society for Microbiology and Biotechnology.

Immunomodulatory Potential of Weissella cibaria in Aged C57BL/6J Mice

Ho-Eun Park 1, Kyung-Won Kang 2, Bum-Seok Kim 3, Sang-Myeong Lee 2 and Wan-Kyu Lee 1*

1Veterinary Medical Center and College of Veterinary Medicine, Chungbuk National University, Cheongju 28644, Republic of Korea, 2College of Environmental and Bioresource Sciences, Chonbuk National University, Iksan 54596, Republic of Korea, 3College of Veterinary Medicine, Chonbuk National University, Iksan 54596, Republic of Korea

Received: August 9, 2017; Accepted: September 17, 2017

Abstract

Aging is associated with distinct changes in immune cells and a decline in immune function,
leading to increased susceptibility to infection and reduced responses to vaccination. Certain
strains of lactic acid bacteria exert beneficial effects on the immune system. Previously, we
reported that Weissella cibaria JW15 isolated from kimchi possesses immune stimulatory
activity in vitro. In the present study, we further investigated whether oral administration of
JW15 improves immune function in aged mice. Eighteen-month-old female mice were
administered JW15 daily at low (JW15-L; 1 × 108 CFU/mouse) or high dosage (JW15-H;
1 × 109 CFU/mouse), or with Lactobacillus rhamnosus GG (LGG) using oral gavage. Twomonth-
old female mice were included as healthy young mice. After 4 weeks, the mice were
euthanized and immune profiles were analyzed using whole blood and spleen. In complete
blood count analysis, the numbers of white and red blood cells were significantly increased in
the JW15-L group compared with those in the old mouse (OM) control group. In addition,
administration of either JW15 of LGG resulted in higher numbers of splenocytes in
comparison with the OM group. Furthermore, proliferative potentials were higher in all
probiotic groups than OM. Cytokines such as IFN-γ and IL-6 were secreted at higher levels in
splenocytes isolated from JW15-fed mice than in OM control mice. Similarly, mRNA
expression of various cytokines was altered in the JW15 groups. Collectively, these results
suggest that JW15 supplementation induces immunomodulatory effects in aged mice and
indicate JW15 as a potential probiotic strain to improve immune function in aged animals.

Keywords: Weissella cibaria JW15, probiotics, aged mice, immunomodulatory effects

References

  1. Gruver AL, Hudson LL, Sempowski GD. 2007. Immunosenescence of ageing. J. Pathol. 211: 144-156.
    Pubmed KoreaMed CrossRef
  2. Castle SC. 2000. Clinical relevance of age-related immune dysfunction. Clin. Infect. Dis. 31: 578-585.
    Pubmed CrossRef
  3. Busse PJ, Mathur SK. 2010. Age-related changes in immune function: effect on airway inflammation. J. Allergy Clin. Immunol. 126: 690-699.
    Pubmed KoreaMed CrossRef
  4. Gill HS, Rutherfurd KJ, Cross ML, Gopal PK. 2001. Enhancement of immunity in the elderly by dietary supplementation with the probiotic Bifidobacterium lactis HN019. Am. J. Clin. Nutr. 74: 833-839.
    Pubmed
  5. Yamada K, Tokunaga Y, Ikeda A, Ohkura K, Kaku-Ohkura S, Mamiya S, et al. 2003. Effect of dietary fiber on the lipid metabolism and immune function of aged Sprague-Dawley rats. Biosci. Biotechnol. Biochem. 67: 429-433.
    Pubmed CrossRef
  6. Meydani SN, Han SN, Wu D. 2005. Vitamin E and immune response in the aged: molecular mechanisms and clinical implications. Immunol. Rev. 205: 269-284.
    Pubmed CrossRef
  7. Fuller R. 1989. Probiotics in man and animals. J. Appl. Bacteriol. 66: 365-378.
    Pubmed CrossRef
  8. Ashraf R, Shah NP. 2014. Immune system stimulation by probiotic microorganisms. Crit. Rev. Food Sci. Nutr. 54: 938-956.
    Pubmed CrossRef
  9. Rolfe RD. 2000. The role of probiotic cultures in the control of gastrointestinal health. J. Nutr. 130: 396S-402S.
    Pubmed
  10. Pae M, Meydani SN, Wu D. 2012. The role of nutrition in enhancing immunity in aging. Aging Dis. 3: 91-129.
    Pubmed
  11. Duncan SH, Flint HJ. 2013. Probiotics and prebiotics and health in ageing populations. Maturitas 75: 44-50.
    Pubmed CrossRef
  12. Bjorkroth KJ, Schillinger U, Geisen R, Weiss N, Hoste B, Holzapfel WH, et al. 2002. Taxonomic study of Weissella confusa and description of Weissella cibaria sp. nov., detected in food and clinical samples. Int. J. Syst. Evol. Microbiol. 52: 141-148.
    Pubmed CrossRef
  13. Kang MS, Lim HS, Kim SM, Lee HC, Oh JS. 2011. Effect of Weissella cibaria on Fusobacterium nucleatum-induced interleukin-6 and interleukin-8 production in KB cells. J. Bacteriol. Virol. 41: 10.
    CrossRef
  14. Ahn SB, Park HE, Lee SM, Kim SY, Shon MY, Lee WK. 2013. Characteristics and immuno-modulatory effects of Weissella cibaria JW15 isolated from kimchi, Korea traditional fermented food, for probiotic use. J. Biomed. Res. 14: 206-212.
    CrossRef
  15. Choi HJ, Shin MS, Lee SM, Lee WK. 2012. Immunomodulatory properties of Enterococcus faecium JWS 833 isolated from duck intestinal tract and suppression of Listeria monocytogenes infection. Microbiol. Immunol. 56: 613-620.
    Pubmed CrossRef
  16. Jang SE, Joh EH, Ahn YT, Huh CS, Han MJ, Kim DH. 2013. Lactobacillus casei HY7213 ameliorates cyclophosphamideinduced immunosuppression in mice by activating NK, cytotoxic T cells and macrophages. Immunopharm. Immunotoxicol. 35: 396-402.
    Pubmed CrossRef
  17. 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
  18. Seo DW, Cho YI, Gu S, Kim DH, Park JH, Yi YJ, et al. 2016. A hot water extract of Aralia cordata activates bone marrowderived macrophages via a myeloid differentiation protein 88-dependent pathway and protects mice from bacterial infection. Microbiol. Immunol. 60: 343-355.
    Pubmed CrossRef
  19. Park HE, Lee WK. 2017. Immunomodulatory effects of mixed Weissella cibaria JW15 with water extract of black soybean and burdock on Listeria monocytogenes infection in mice. J. Biomed. Transl. Res. 18: 1-6.
  20. Hori Y, Perkins EH, Halsall MK. 1973. Decline in phytohemagglutinin responsiveness of spleen cells from aging mice. Proc. Soc. Exp. Biol. Med. 144: 48-53.
    Pubmed CrossRef
  21. Cyster JG. 1999. Chemokines and cell migration in secondary lymphoid organs. Science 286: 2098-2102.
    Pubmed CrossRef
  22. Le Couteur DG, Tay SS, Solon-Biet S, Bertolino P, McMahon AC, Cogger VC, et al. 2015. The influence of macronutrients on splanchnic and hepatic lymphocytes in aging mice. J. Gerontol. A Biol. Sci. Med. Sci. 70: 1499-1507.
    Pubmed CrossRef
  23. Kaushal D, Kansal VK. 2012. Probiotic Dahi containing Lactobacillus acidophilus and Bifidobacterium bifidum alleviates age-inflicted oxidative stress and improves expression of biomarkers of ageing in mice. Mol. Biol. Rep. 39: 1791-1799.
    Pubmed CrossRef
  24. Beli E, Duriancik DM, Clinthorne JF, Lee T, Kim S, Gardner EM. 2014. Natural killer cell development and maturation in aged mice. Mech. Ageing Dev. 135: 33-40.
    Pubmed KoreaMed CrossRef
  25. Kared H, Camous X, Larbi A. 2014. T cells and their cytokines in persistent stimulation of the immune system. Curr. Opin. Immunol. 29: 79-85.
    Pubmed CrossRef
  26. Sharma R, Kapila R, Dass G, Kapila S. 2014. Improvement in Th1/Th2 immune homeostasis, antioxidative status and resistance to pathogenic E. coli on consumption of probiotic Lactobacillus rhamnosus fermented milk in aging mice. Age 36: 9686.
    Pubmed KoreaMed CrossRef
  27. Fu YR, Yi ZJ, Pei JL, Guan S. 2010. Effects of Bifidobacterium bifidum on adaptive immune senescence in aging mice. Microbiol. Immunol. 54: 578-583.
    CrossRef
  28. Shaw AC, Joshi S , Greenwood H, P anda A, Lord JM. 2 010. Aging of the innate immune system. Curr. Opin. Immunol. 22: 507-513.
    Pubmed KoreaMed CrossRef