DOI QR코드

DOI QR Code

Effects of Bifidobacterium Strains Treated with Gastrointestinal Enzymes on Cytokine Induction in RAW 264.7 Macrophage Cells

  • Kim, Dong-Woon (Swine Science Division, National Institute of Animal Science, RDA) ;
  • Cho, Sung-Back (Swine Science Division, National Institute of Animal Science, RDA) ;
  • Jung, Hyun-Jung (Swine Science Division, National Institute of Animal Science, RDA) ;
  • Lee, Sung-Dae (Swine Science Division, National Institute of Animal Science, RDA) ;
  • Kim, Sang-Ho (Swine Science Division, National Institute of Animal Science, RDA) ;
  • Cho, Kyu-Ho (Swine Science Division, National Institute of Animal Science, RDA) ;
  • Kang, Seog-Jin (Swine Science Division, National Institute of Animal Science, RDA) ;
  • Kim, In-Cheul (Swine Science Division, National Institute of Animal Science, RDA)
  • Received : 2010.07.08
  • Accepted : 2010.09.21
  • Published : 2010.10.31

Abstract

The objective of the current study was to compare the abilities of undigested and enzymatically digested bifidobacteria to induce nitric oxide and cytokine release in RAW 264.7 macrophage cells. Nine different Bifidobacterium strains derived from herbivorous animals were digested with pepsin and then pancreatin, and the precipitates and supernatants were acquired via centrifugation. The RAW 264.7 cells were incubated with whole cells, the precipitate, or the supernatant, and the macrophage culture supernatants were analyzed with respect to the induction of nitric oxide and cytokines. Pronounced increases in the production of nitric oxide, interleukin (IL)-$1{\beta}$, IL-6, IL-12, and tumor necrosis factor-$\alpha$ (TNF-$\alpha$) were observed when cultured with whole cells and the precipitates. It is noteworthy that the precipitates in most of the Bifidobacterium strains evidenced a trend toward superior IL-12 release compared with whole cells. The results showed that both whole cells and digested Bifidobacterium sp. are effective at stimulating RAW 264.7 cells to induce the production of nitric oxide and cytokines. The pepsin-pancreatin system used in the current study may be useful in unraveling the mechanism by which ingested lactic acid bacteria modulate the induction of macrophage mediators at the cellular level.

Keywords

References

  1. Adams, D. O., and Hamilton, T. A. (1987) Molecular transductional mechanisms by which Interferon-$\gamma$ and other signals regulate macrophage development. Immunol. Rev. 97, 5-27. https://doi.org/10.1111/j.1600-065X.1987.tb00514.x
  2. Amrouche, T., Boutin, Y., Prioult, G., and Fliss, I. (2006) Effects of bifidobacterial cytoplasm, cell wall and exopolysaccharide on mouse lymphocyte proliferation and cytokine production. Int. Dairy J. 16, 70-80. https://doi.org/10.1016/j.idairyj.2005.01.008
  3. Arai, K., Lee, F., Miyajima, A., Miyatake, S., Arai, N., and Yokota, T. (1990) Cytokines: coordinators of immune and inflammatory responses. Ann. Rev. Biochem. 59, 783-836. https://doi.org/10.1146/annurev.bi.59.070190.004031
  4. Beagley, K. W., Eldridge, J. H., Lee, F., Kiyono, H., Everson, M. P., and Koopman, W. J. (1989) Interleukins and Immunoglobulin A synthesis: Human and murine intereukin-6 induce high rate Immunoglobulin A secretion in Immunoglobulin A-committed B cells. J. Exp. Med. 169, 2133-48. https://doi.org/10.1084/jem.169.6.2133
  5. Boisen, S. and Fernandez, J. A. (1995) Prediction of the apparent ileal digestibility of protein and amino acids in feedstuffs and feed mixtures for pigs by in vitro analyses. Anim. Feed Sci. Techno. 51, 29-43. https://doi.org/10.1016/0377-8401(94)00686-4
  6. Clark, P. A., and Martin, J. H. (1994) Selection of bifidobacteria for use as dietary adjuncts in cultured dairy foods: III-Tolerance to simulated bile concentrations of human small intestines. Cult. Dairy Prod. J. 29, 18-21.
  7. Ding, A. H., Nathan, C. F., and Stuehr, D. J. (1988) Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. J. Immunol. 141, 2407-2412.
  8. Dong, W., Azcona-Olivera, J. L., Brooks, K. H., Linz, J. E., and Pestka, J. J. (1994) Elevated gene expression and production of interleukins 2, 4, 5, and 6 during exposure to vomitoxin(deoxynivalenol) and cycloheximide in the EL-4 thymoma. Toxicol. Appl. Pharmacol. 127, 282-290. https://doi.org/10.1006/taap.1994.1163
  9. Fukushima, Y., Kawata, Y., Mizumachi, K., Kurisaki, J., and Mitsuoka, T. (1999) Effect of bifidobacteria feeding on fecal flora and production of immunoglobulins in lactating mouse. Int. J. Food Microbiol. 46, 193-197. https://doi.org/10.1016/S0168-1605(98)00183-4
  10. Fuller, R. (1991) Probiotics in human medicine. Gut 32, 439-442. https://doi.org/10.1136/gut.32.4.439
  11. Gilliland, S. E. (1990) Health and nutritional benefits from lactic acid bacteria. Fed. Eur. Microbial. Rev. 87, 175-188. https://doi.org/10.1111/j.1574-6968.1990.tb04887.x
  12. Hatcher, G. E., and Lambrecht, R. S. (1993) Augmentation of macrophage phagocytic activity by cell-free extracts of selected lactic acid-producing bacteria. J. Dairy Sci. 76, 2485-2492. https://doi.org/10.3168/jds.S0022-0302(93)77583-9
  13. Hosono, A., Lee, J., Ametani, A., Natsume, M., Hirayama, M., Adachi, T., and Kaminogawa, S. (1997) Characterization of a Water-soluble Polysaccharide Fraction with Immunopotentiating Actvity from Bifidobacterium adolescentis M101-4. Biosci. Biotech. Biothem. 61, 312-316. https://doi.org/10.1271/bbb.61.312
  14. Kang, K. Y., Park, S. H., and Choe, T. B. (1994) Immunostimulation effect of cell wall components isolated from Lactobacillus plantarum. J. Microbiol. Biotechnol. 4, 195-199.
  15. Kimoto, H., Mizumachi, K., Okamoto, T., and Kurisaki, J. (2004) New Lactococcus strain with immunomodulatory activity: enhancement of Th1-type immune response. Microbiol. Immunol. 48, 75-82. https://doi.org/10.1111/j.1348-0421.2004.tb03490.x
  16. Kirjavainen, P. V., El-Nezami, H. S., Salminen, S. J., Ahokas, J. T., and Wright, P. F. (1999) The effect of orally administered viable probiotic and dairy lactobacilli on mouse lymphocyte proliferation. FEMS Immunol. Med. Microbiol. 26, 131-135. https://doi.org/10.1111/j.1574-695X.1999.tb01380.x
  17. Kitazawa, H., Itoh, T., Tomioka, Y., Mizugaki, H., and Yamaguchi, T. (1999) Induction of Interferon-$\gamma$ and Interleukin- 1$\alpha$ production in macrophages stimulated with phosphopolysaccharide produced by Lactococcus lactis ssp. cremoris. Int. J. Food Microbiol. 31, 99-106.
  18. Link-Amster, H., Rochat, F., Saudan, K. Y., Mignot, O., and Aeschlimann, J. M. (1994) Modulation of a specific humoral immune response and changes in intestinal flora mediated through fermented milk intake. FEMS Immunol. Med. Microbiol. 10, 55-64. https://doi.org/10.1111/j.1574-695X.1994.tb00011.x
  19. Marteau, P., Pochart, P., Bouhnik, Y., Zidi, S., Goderel, I., and Rambaud, J. C. (1992) Survival of Lactobacillus acidophilus and Bifidobacterium sp. in the small intestine following ingestion in fermented milk. A rational basis for the use of probiotics in man. Gastroenterol Clin. Biol. 16, 25-8.
  20. Ouwehand, A. C., Kirjavainen, P. V., Gronlund, M. M., and Salminen, S. J. (1999) Adhesion of probiotic microorganisms to intestinal mucus. Int. Dairy J. 9, 623-630. https://doi.org/10.1016/S0958-6946(99)00132-6
  21. Park, S. Y., Ji, G. E., Ko, Y. T., Hoo, H. K., Ustunol, Z., and Pestka, J. J. (1999) Potentiation of hydrogen peroxide, nitric oxide, and cytokine production in RAW 264.7 macrophage cell 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
  22. Rafter, J. J. (1995) The role of lactic acid bacteria in colon cancer prevention. Scand. J. Gastroenterol. 30, 497-502. https://doi.org/10.3109/00365529509089779
  23. Sakai, T., Hamakawa, M., and Shirai, K. (1996) Protective effects of digested bacterial cell powder on diarrhea in suckling piglets. Agri-Practice. 17, 23-27.
  24. Sanders, M.E. (1993) Effect of consumption of lactic cultures on human health. Adv. Food Nutr. Res. 37, 67-130. https://doi.org/10.1016/S1043-4526(08)60116-3
  25. SAS. (2000) SAS/STAT user's guide. Version 8, SAS Institute Inc., Cary, N. C., USA
  26. Sato, K., Saito, H., Tomioka, H., and Yokokura, T. (1988) Enhancement of host resistance against Listeria Infection by Lactobacillus casei: efficacy of cell wall preparation of Lactobacillus casei. Microbiol. Immunol. 32, 1189-1200. https://doi.org/10.1111/j.1348-0421.1988.tb01483.x
  27. Schleifer, K. H., and Kandler, O. (1972) Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol. Rev. 36, 407-477.
  28. Sekine, K., Kasashima, T., and Hashimoto, Y. (1994) Comparison of the TNF-$\alpha$ level induced by human-derived Bifidobacterium longum and rat-derived Bifidobacterium animalis in mouse peritoneal cells. Bifidobact. Microfl. 13, 79-89. https://doi.org/10.12938/bifidus1982.13.2_79
  29. Sekine, K., Ohta, J., Onishi, M., Tatsuki, T., Shimokawa, Y., Toida, T., Kawashima, T. and Hashimoto, Y. (1995) Analysis of antitumor properties of effector cells stimulated with a cell wall preparation of Bifidobacterium infantis. Biol. Pharm. Bull. 18, 148-153. https://doi.org/10.1248/bpb.18.148
  30. Takahashi, T., Oka, T., Iwana, H., Kuwata, T., and Yamamoto, Y. (1993) Immune response of mice to orally administered lactic acid bacteria. Biosci. Biotech. Biochem. 57, 1557-1560. https://doi.org/10.1271/bbb.57.1557
  31. Takahashi, T., Nakagawa, E., and Nara, T. (1998) Effects of orally ingested Bifidobacterium longum on the mucosal Immunoglobulin A response of mice to dietary antigens. Biosci. Biotech. Biochem. 62, 10-15. https://doi.org/10.1271/bbb.62.10
  32. 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.
  33. 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.
  34. Uemura, J., Kitazawa, H., Kawai, Y., Itoh, T., Oda, M., and Saito, T. (2003) Functional alteration of murine macrophages stimulated with extracellular polysaccharides from Lactobacillus delbrueckii ssp. bulgaricus OLL1073R-1. Food Microbiol. 20, 267-273. https://doi.org/10.1016/S0740-0020(02)00177-6
  35. Vinderola, G., Perdigon, G., Duarte, J., Farnworth, E., and Mater, C. (2006) Effects of the oral administration of the products derived from milk fermentation by kefir microflora on immune stimulation. J. Dairy Res.7, 1-8.