Food Science of Animal Resources (한국축산식품학회지)

Korean Society for Food Science of Animal Resources (한국축산식품학회)
권호 표지
DOI QR코드

DOI QR Code

Immuno-Modulatory Effects of Bacteriocin-Producing Pediococcus pentosaceus JWS 939 in Mice

  • Choi, Hyun-Jong (College of Veterinary Medicine and Research Institute of Veterinary Medicine, Chungbuk National University) ;
  • Kim, Ji-Ye (College of Veterinary Medicine and Research Institute of Veterinary Medicine, Chungbuk National University) ;
  • Shin, Myeong-Su (College of Veterinary Medicine and Research Institute of Veterinary Medicine, Chungbuk National University) ;
  • Lee, Sang-Myeong (Division of Biotechnology, College of Environmental & Bioresource Sciences, Chonbuk National University) ;
  • Lee, Wan-Kyu (College of Veterinary Medicine and Research Institute of Veterinary Medicine, Chungbuk National University)
  • Received : 2011.08.09
  • Accepted : 2011.10.10
  • Published : 2011.10.31
Download PDF
⟨ Previous Next ⟩

Abstract

Pediococcus pentosaceus JWS 939 (JWS 939) is a nonpathogenic bacteriocin-producing probiotic isolated from the duck intestine. This study assessed the immunomodulatory effects of JWS 939 and compared them with those of Lactobacillus rhamnosus GG (LGG), a well-known immune enhancer. The immune-enhancing effects of JWS 939 were measured by measuring the production of nitric oxide (NO) and cytokines in C57BL/6 mouse peritoneal macrophages. In addition, to assess the immune enhancement abilities of JWS 939, in vivo, a Listeria monocytogenes challenge mice model was used. The results showed that heat-killed JWS 939 induced more NO and interleukin (IL)-$1{\beta}$ production in mouse peritoneal macrophages than in LGG, and that oral administration of viable JWS 939 in mice increased more NO, IL-$1{\beta}$, and tumor necrosis factor (TNF)-${\alpha}$ level than in LGG in serum upon L. monocytogenes challenge. In addition, mice fed with JWS 939 had a longer survival time after lethal challenge with L. monocytogenes, and these effects were stronger than those induced by LGG. Collectively, P. pentosaceus JWS 939 is a remarkable strain that, by releasing bacteriocin and enhancing host immune responses, may have potential as a duck feed additive to suppress pathogens.

Keywords

References

  1. Chanos, P. and Williams, D. R. (2011) Anti-Listeria bacteriocin-producing bacteria from raw ewe's milk in northern Greece. J. Appl. Microbiol. 110, 757-768. https://doi.org/10.1111/j.1365-2672.2010.04932.x
  2. Chiu, H. H., Tsai, C. C., Hsih, H. Y., and Tsen, H. Y. (2008) Screening from pickled vegetables the potential probiotic strains of lactic acid bacteria able to inhibit the Salmonella invasion in mice. J. Appl. Microbiol. 104, 605-612.
  3. Daeschel, M. A. and Klaenhammer, T. R. (1985) Association of a 13.6-megadalton plasmid in Pediococcus pentosaceus with bacteriocin activity. Appl. Environ. Microbiol. 50, 1538-1541.
  4. Derouich-Guergour, D., Brenier-Pinchart, M. P., Ambroise-Thomas, P., and Pelloux, H. (2001) Tumour necrosis factor alpha receptors: role in the physiopathology of protozoan parasite infections. Int. J. Parasitol. 31, 763-769. https://doi.org/10.1016/S0020-7519(01)00194-1
  5. Dinarello, C. A. (1996) Biologic basis for interleukin-1 in disease. Blood 87, 2095-2147.
  6. Edelson, B. T. and Unanue, E. R. (2000) Immunity to Listeria infection. Curr. Opin. Immunol. 12, 425-431. https://doi.org/10.1016/S0952-7915(00)00112-6
  7. Ehrmann, M. A., Kurzak, P., Bauer, J., and Vogel, R. F. (2002) Characterization of lactobacilli towards their use as probiotic adjuncts in poultry. J. Appl. Microbiol. 92, 966-975. https://doi.org/10.1046/j.1365-2672.2002.01608.x
  8. Ghadimi, D., de Vrese, M., Heller, K. J., and Schrezenmeir, J. (2010) Lactic acid bacteria enhance autophagic ability of mononuclear phagocytes by increasing Th1 autophagy-promoting cytokine (IFN-gamma) and nitric oxide (NO) levels and reducing Th2 autophagy-restraining cytokines (IL-4 and IL-13) in response to Mycobacterium tuberculosis antigen. Int. Immunopharmacol. 10, 694-706. https://doi.org/10.1016/j.intimp.2010.03.014
  9. Gill, H. S., Shu, Q., Lin, H., Rutherfurd, K. J., and Cross, M. L. (2001) Protection against translocating Salmonella typhimurium infection in mice by feeding the immuno-enhancing probiotic Lactobacillus rhamnosus strain HN001. Med. Microbiol. Immunol. 190, 97-104.
  10. Grilli, E., Messina, M. R., Catelli, E., Morlacchini, M., and Piva, A. (2009) Pediocin A improves growth performance of broilers challenged with Clostridium perfringens. Poultry Sci. 88, 2152-2158. https://doi.org/10.3382/ps.2009-00160
  11. Haakensen, M., Dobson, C. M., Hill, J. E., and Ziola, B. (2009) Reclassification of Pediococcus dextrinicus (Coster and White 1964) back 1978 (Approved Lists 1980) as Lactobacillus dextrinicus comb. Nov., and emended description of the genus Lactobacillus. Int. J. Syst. Evol. Microbiol. 59, 615-621. https://doi.org/10.1099/ijs.0.65779-0
  12. Igarashi, T. (2010) Study of the relationship between changes in lactic acid bacterial cell components and stimulation of IL-12 production under salt-stressed conditions. Biosci. Biotechnol. Biochem. 74, 2171-2175. https://doi.org/10.1271/bbb.100040
  13. Jonganurakkun, B., Wang, Q., Xu, S. H., Tada, Y., Minamida, K., Yasokawa, D., Sugi, M., Hara, H., and Asano, K. (2008) Pediococcus pentosaceus NB-17 for probiotic use. J. Biosci. Bioeng. 106, 69-73. https://doi.org/10.1263/jbb.106.69
  14. Korhonen, R., Korpela, R., Saxelin, M., Mäki, M., Kankaanranta, H., and Moilanen, E. (2001) Induction of nitric oxide synthesis by probiotic Lactobacillus rhamnosus GG in J774 macrophages and human T84 intestinal epithelial cells. Inflammation 25, 223-232. https://doi.org/10.1023/A:1010971703271
  15. Kosin, B. and Rakshit, S. K. (2006) Microbial and processing criteria for production of probiotics: a review. Food Technol. Biotechnol. 44, 371-379.
  16. Lin, W. H., Yu, B., Lin, C. K., Hwang, W. Z., and Tsen, H. Y. (2007) Immune effect of heat-killed multistrain of Lactobacillus acidophilus against Salmonella typhimurium invasion to mice. J. Appl. Microbiol. 102, 22-31. https://doi.org/10.1111/j.1365-2672.2006.03073.x
  17. Lorsbach, R. B., Murphy, W. J., Lowenstein, C. J., Snyder, S. H., and Russell, S. W. (1993) Expression of the nitric oxide synthase gene in mouse macrophages activated for tumor cell killing. Molecular basis for the synergy between interferon-gamma and lipopolysaccharide. J. Biol. Chem. 268, 1908-1913.
  18. Marin, M. L., Lee, J. H., Murtha, J., Ustunol, Z., and Pestka, J. J. (1997) Differential cytokine production in clonal macrophage and T-cell lines cultured with Bifidobacteria. J. Dairy Sci. 80, 2713-2720. https://doi.org/10.3168/jds.S0022-0302(97)76232-5
  19. Mileti, E., Matteoli, G., Iliev, I. D., and Rescigno, M. (2009) Comparison of the immunomodulatory properties of three probiotic strains of Lactobacilli using complex culture systems: prediction for in vivo efficacy. PLoS One 4, e7056. https://doi.org/10.1371/journal.pone.0007056
  20. Milon, G. (1997) Listeria monocytogenes in laboratory mice: a model of short-term infectious and pathogenic processes controllable by regulated protective immune responses. Immunol. Rev. 158, 37-46. https://doi.org/10.1111/j.1600-065X.1997.tb00990.x
  21. Nes, I. F., Diep, D. B., and Holo, H. (2007) Bacteriocin diversity in Streptococcus and Enterococcus. J. Bacteriol. 189, 1189-1198. https://doi.org/10.1128/JB.01254-06
  22. Nomoto, K., Miake, S., Hashimoto, S., Yokokura, T., Mutai, M., Yoshikai, Y., and Nomoto, K. (1985) Augmentation of host resistance to Listeria monocytogenes infection by Lactobacillus casei. J. Clin. Lab. Immunol. 17, 91-97.
  23. Nonaka, Y., Izumo, T., Izumi, F., Maekawa, T., Shibata, H., Nakano, A., Kishi, A., Akatani, K., and Kiso, Y. (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. https://doi.org/10.1159/000109294
  24. Park, S. Y., Ji, G. E., Ko, Y. T., Jung, H. K., Ustunol, Z., and Pestka, J. J. (1999) Potentiation of hydrogen peroxide, nitric oxide, and cytokine production in RAW 264.7 macrophage cells exposed to human and commercial isolates of Bifidobacterium. Int. J. Food Microbiol. 46, 231-241. https://doi.org/10.1016/S0168-1605(98)00197-4
  25. Puertollano, E., Puertollano, M. A., Cruz-Chamorro, L., Alvarez de Cienfuegos, G., Ruiz-Bravo, A., and de Pablo, M. A. (2008) Orally administered Lactobacillus plantarum reduces pro-inflammatory interleukin secretion in sera from Listeria monocytogenes infected mice. Br. J. Nutr. 99, 819-825.
  26. Saarela, M., Mogensen, G., Fondén, R. Mättö, J., and Mattila-Sandholm, T. (2000) Probiotic bacteria: safety, functional and technological properties. J. Biotechnol. 84, 197-215. https://doi.org/10.1016/S0168-1656(00)00375-8
  27. Schreiber, R. D., Hicks, L. J., Celada, A., Buchmeier, N. A., and Gray, P. W. (1985) Monoclonal antibodies to murine gamma-interferon which differentially modulate macrophage activation and antiviral activity. J. Immunol. 134, 1609-1618.
  28. Shin, M. S., Han, S. K. Ji, A. R., Ham, M. R., Kim, K. S., and Lee, W. K. (2007) Isolation and characteristics of bacteriocin-producing bacteria from the intestine of duck for probiotics. J. Anim. Sci. Technol. 49, 621-632. https://doi.org/10.5187/JAST.2007.49.5.621
  29. Snyder, S. H., and Bredt, D. S. (1992) Biological roles of nitric oxide. Sci. Am. 266, 68-77.
  30. Tejada-Simon, M. V., and Pestka, J. J. (1999) Proinflammatory cytokine and nitric oxide induction in murine macrophages by cell wall and cytoplasmic extracts of lactic acid bacteria. J. Food Prot. 62, 1435-1444.
  31. Tsai, C. C., Liu, T. H., Chen, M. H., Tsai, C. C, and Tsen, H. Y. (2004) Toxicity evaluation for an Enterococcus faecium strain TM39 in vitro and in vivo. Food Chem. Toxicol. 42, 1601-1609. https://doi.org/10.1016/j.fct.2004.05.005
  32. van Furth, R., Cohn, Z. A., Hirsch, J. G., Humphrey, J. H., Spector, W. G., and Langevoort, H. L. (1972) The mononuclear phagocyte system: a new classification of macrophages, monocytes and their precursor cells. Bull. World Health Organ. 46, 845-852.
  33. Wu, C. W., Yin, L. J., and Jiang, S. T. (2004) Purification and characterization of bacteriocin from Pediococcus pentosaceus ACCEL. J. Agric. Food Chem. 52, 1146-1151. https://doi.org/10.1021/jf035100d
  34. Zhang, X., Goncalves, R., and Mosser, D. M. (2008) The isolation and characterization of murine macrophages. Curr. Protoc. Immunol. Chapter 14, Unit 14.1.

Cited by

  1. Pediococcus spp.: An important genus of lactic acid bacteria and pediocin producers vol.35, pp.3, 2017, https://doi.org/10.1016/j.biotechadv.2017.03.004
  2. Selection and immunomodulatory evaluation of lactic acid bacteria suitable for use as canine probiotics vol.55, pp.2, 2015, https://doi.org/10.14405/kjvr.2015.55.2.81
  3. Characteristics and immuno-modulatory effects of Enterococcus faecium JS1-8 isolated from Kimchi vol.15, pp.4, 2014, https://doi.org/10.12729/jbr.2014.15.4.182