Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Probiotic and Antioxidant Properties of Novel Lactobacillus brevis KCCM 12203P Isolated from Kimchi and Evaluation of Immune-Stimulating Activities of Its Heat-Killed Cells in RAW 264.7 Cells

  • Song, Myung Wook (Department of Food Science and Biotechnology of Animal Resources, Konkuk University) ;
  • Jang, Hye Ji (Department of Food Science and Biotechnology of Animal Resources, Konkuk University) ;
  • Kim, Kee-Tae (Food Biotechnology Research Institute, Konkuk University) ;
  • Paik, Hyun-Dong (Department of Food Science and Biotechnology of Animal Resources, Konkuk University)
  • Received : 2019.07.31
  • Accepted : 2019.09.25
  • Published : 2019.12.28
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Abstract

The purpose of this study was to determine the probiotic properties of Lactobacillus brevis KCCM 12203P isolated from the Korean traditional food kimchi and to evaluate the antioxidative activity and immune-stimulating potential of its heat-killed cells to improve their bio-functional activities. Lactobacillus rhamnosus GG, which is a representative commercial probiotic, was used as a comparative sample. Regarding probiotic properties, L. brevis KCCM 12203P was resistant to 0.3% pepsin with a pH of 2.5 for 3 h and 0.3% oxgall solution for 24 h, having approximately a 99% survival rate. It also showed strong adhesion activity (6.84%) onto HT-29 cells and did not produce β-glucuronidase but produced high quantities of leucine arylamidase, valine arylamidase, β-galactosidase, and N-acetyl-β-glucosaminidase. For antioxidant activity, it appeared that viable cells had higher radical scavenging activity in the 2,2-diphenyl-1-picryl-hydrazyl (DPPH) assay, while in the 2-azinobis-(3-ethylbenzothiazoline-6-sulfonic acid (ABTS) assay, heat-killed cells had higher antioxidant activity. Additionally, L. brevis KCCM 12203P showed higher lipid oxidation inhibition ability than L. rhamnosus GG; however, there was no significant difference (p < 0.05) between heat-killed cells and control cells. Furthermore, heat-killed L. brevis KCCM 12203P activated RAW 264.7 macrophage cells without cytotoxicity at a concentration lower than 108 CFU/ml and promoted higher gene expression levels of inducible nitric oxide synthase, interleukin-1β, and interleukin-6 than L. rhamnosus GG. These results suggest that novel L. brevis KCCM 12203P could be used as a probiotic or applied to functional food processing and pharmaceutical fields for immunocompromised people.

Keywords

References

  1. Boudoulas KD, Triposkiadis F, Stefanadis C, Boudoulas H. 2017. The endlessness evolution of medicine, continuous increase in life expectancy and constant role of the physician. Hellenic J. Cardiol. 58: 322-330. https://doi.org/10.1016/j.hjc.2017.05.001
  2. Ziemer CJ, Gibson GR. 1998. An overview of probiotics, prebiotics and synbiotics in the functional food concept: perspectives and future strategies. Int. Dairy J. 8: 473-479. https://doi.org/10.1016/S0958-6946(98)00071-5
  3. Sommer F, Bäckhed F. 2013. The gut microbiota - masters of host development and physiology. Nat. Rev. Microbiol. 11: 227-238. https://doi.org/10.1038/nrmicro2974
  4. Gamallat Y, Ren X, Walana W, Meyiah A, Xinxiu R, Zhu Y, et al. 2019. Probiotic Lactobacillus rhamnosus modulates the gut microbiome composition attenuates preneoplastic colorectal Aberrant crypt foci. J. Funct. Foods 53: 146-156. https://doi.org/10.1016/j.jff.2018.12.018
  5. Wu Q, Shah NP. 2018. Restoration of GABA production machinery in Lactobacillus brevis by accessible carbohydrates, anaerobiosis and early acidification. Food Microbiol. 69: 151-158. https://doi.org/10.1016/j.fm.2017.08.006
  6. Yang X, Zhou J, Fan L, Qin Z, Chen Q, Zhao L. 2018. Antioxidant properties of a vegetable-fruit beverage fermented with two Lactobacillus plantarum strains. Food Sci. Biotechnol. 27: 1719-1726. https://doi.org/10.1007/s10068-018-0411-4
  7. Daliri EB, Lee BH, Park BJ, Kim SH, Oh DH. 2018. Antihypertensive peptides from whey proteins fermented by lactic acid bacteria. Food Sci. Biotechnol. 27: 1781-1789. https://doi.org/10.1007/s10068-018-0423-0
  8. Koh WY, Utra U, Ahmad R, Rather IA, Park YH. 2018. Evaluation of probiotic potential and anti-hyperglycemic properties of a novel Lactobacillus strain isolated from water kefir grains. Food Sci. Biotechnol. 27: 1369-1376. https://doi.org/10.1007/s10068-018-0360-y
  9. Lv X, Miao L, Ma H, Bai F, Lin Y, Sun M, et al. 2018. Purification, characterization and action mechanism of plantaricin JY22, a novel bacteriocin against Bacillus cereus produced by Lactobacillus plantarum JY22 from golden carp intestine. Food Sci. Biotechnol. 27: 695-703. https://doi.org/10.1007/s10068-017-0280-2
  10. Cruz Rodrigues VC, Silva LGS Simabuco FM, Venema K, Antunes AEC. 2019. Survival, metabolic status and cellular morphology of probiotics in dairy products and dietary supplement after simulated digestion. J. Funct. Foods 55: 126-134. https://doi.org/10.1016/j.jff.2019.01.046
  11. Ou CC, Lin SL, Tsai JJ, Lin MY. 2011. Heat-killed lactic acid bacteria enhance immunomodulatory potential by skewing the immune response toward Th1 polarization. J. Food Sci. 76: 260-267. https://doi.org/10.1111/j.1750-3841.2011.02161.x
  12. 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. https://doi.org/10.1016/S0192-0561(97)00109-4
  13. 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. https://doi.org/10.1093/ps/85.2.273
  14. Sashihara T, Sueki N, Ikegami S. 2006. An analysis of the effectiveness of heat-killed lactic acid bacteria in alleviating allergic diseases. J. Dairy Sci. 89: 2846-2855. https://doi.org/10.3168/jds.S0022-0302(06)72557-7
  15. Kamiya T, Wang L, Forsythe P, Goettsche G, Mao Y, Wang Y, et al. 2006. Inhibitory effects of Lactobacillus reuteri on visceral pain induced by colorectal distension in Sprague-Dawley rats. Gut 55: 191-196. https://doi.org/10.1136/gut.2005.070987
  16. Lee NK, H an KJ, S on S H, E om S J, Lee S K, Paik HD. 2015. Multifunctional effect of probiotic Lactococcus lactis KC24 isolated from kimchi. LWT-Food Sci. Technol. 64: 1036-1041. https://doi.org/10.1016/j.lwt.2015.07.019
  17. Yang SJ, Lee JE, Lim SM, Kim YJ, LEE NK, Paik HD. 2019. Antioxidant and immune-enhancing effects of probiotic Lactobacillus plantarum 200655 isolated from kimchi. Food Sci. Biotechnol. 28: 491-499. https://doi.org/10.1007/s10068-018-0473-3
  18. Jang HJ, Song MW, Lee NK, Paik HD. 2018. Antioxidant effects of live and heat-killed probiotic Lactobacillus plantarum Ln1 isolated from kimchi. J. Food Sci. Technol. 55: 3174-3180. https://doi.org/10.1007/s13197-018-3245-4
  19. Kachouri F, Ksontini H, Kraiem M, Setti K, Mechmeche M, Hamdi M. 2015. Involvement of antioxidant activity of Lactobacillus plantarum on functional properties of olive phenolic compounds. J. Food Sci. Technol. 52: 7924-7933. https://doi.org/10.1007/s13197-015-1912-2
  20. Jeon EB, Son SH, Jeewanthi RKC, Lee NK, Paik HD. 2016. Characterization of Lactobacillus plantarum Lb41, an isolate from kimchi and its application as a probiotic in cottage cheese. Food Sci. Biotechnol. 25: 1129-1133. https://doi.org/10.1007/s10068-016-0181-9
  21. Chang C K, W ang S C, C hiu CK, Chen S Y, C hen ZT, Duh PD. 2015. Effect of lactic acid bacteria isolated from fermented mustard on immunopotentiating activity. Asian Pac. J. Prop. Biomed. 5: 281-286. https://doi.org/10.1016/S2221-1691(15)30346-4
  22. S on SH, Jeon HL, Yang S J, S im MH, Kim Y J, Lee NK, et al. 2018. Probiotic lactic acid bacteria isolated from traditional Korean fermented foods based on ${\beta}$-glucosidase activity. Food Sci. Biotechnol. 27: 123-129. https://doi.org/10.1007/s10068-017-0212-1
  23. Park YU, Kim MD, Jung DH, Seo DH, Jung JH, Park JG, et al. 2015. Probiotic properties of lactic acid bacteria isolated from Korean rice wine Makgeolli. Food Sci. Biotechnol. 24: 1761-1766. https://doi.org/10.1007/s10068-015-0229-2
  24. Kleeman EG, Klaenhammer TR. 1982. Adherence of Lactobacillus species to human fetal intestinal cells. J. Dairy Sci. 65: 2063-2069. https://doi.org/10.3168/jds.s0022-0302(82)82462-4
  25. Devi SM, Kurrey NK, Halami PM. 2018. In vitro antiinflammatory activity among probiotic Lactobacillus species isolated from fermented foods. J. Funct. Foods 47: 19-27. https://doi.org/10.1016/j.jff.2018.05.036
  26. Duary RK, Rajput YS, Batish VK, Grover S. 2011. Assessing the adhesion of putative indigenous probiotic lactobacilli to human colonic epithelial cells. Indian J. Med. Res. 134: 664-671. https://doi.org/10.4103/0971-5916.90992
  27. Monteagudo-Mera A, Rodriguez-Aparico L, Rua J, Martínez- Blanco H, Navasa N, Garcia-Armesto MR, et al. 2012. In vitro evaluation of physiological probiotic properties of different lactic acid bacteria strains of dairy and human origin. J. Funct. Foods 4: 531-541. https://doi.org/10.1016/j.jff.2012.02.014
  28. Lee NK, Kim SY, Han KJ, Eom SJ, Paik HD. 2014. Probiotic potential of Lactobacillus strains with anti-allergic effects from kimchi for yogurt starters. LWT-Food Sci. Technol. 58: 130-134. https://doi.org/10.1016/j.lwt.2014.02.028
  29. Mroczynska M, Libudzisz Z. 2010. Beta-glucuronidase and beta-glucosidase activity of Lactobacillus and Enterococcus isolated from human feces. Pol. J. Microbiol. 59: 265-269. https://doi.org/10.33073/pjm-2010-040
  30. Lin MY, Yen CL. 1999. Antioxidative ability of lactic acid bacteria. J. Agric. Food. Chem. 47: 1460-1466. https://doi.org/10.1021/jf981149l
  31. Schaich KM, Tian X, Xie J. 2015. Reprint of "Hurdles and pitfalls in measuring antioxidant efficacy: a critical evaluation of ABTS, DPPH, and ORAC assays". J. Funct. Foods 18: 782-796. https://doi.org/10.1016/j.jff.2015.05.024
  32. Amaretti A, di Nunzio M, Pompei A, Raimondi S, Rossi M, Bordoni A. 2013. Antioxidant properties of potentially probiotic bacteria: in vitro and in vivo activities. Appl. Microbiol. Biotechnol. 97: 809-817. https://doi.org/10.1007/s00253-012-4241-7
  33. Rajoka MSR, Mehwish HM, Siddiq M, Haoin Z, Zhu J, Yan L, et al. 2017. Identification, characterization, and probiotic potential of Lactobacillus rhamnosus isolated from human milk. LWT-Food Sci. Technol. 84: 271-280. https://doi.org/10.1016/j.lwt.2017.05.055
  34. Davis CD, Milner JA. 2009. Gastrointestinal microflora, food components and colon cancer prevention. J. Nutr. Btochem. 20: 743-752. https://doi.org/10.1016/j.jnutbio.2009.06.001
  35. Bogdan C. 2001. Nitric oxide and the immune response. Nat. Immunol. 2: 907-916. https://doi.org/10.1038/ni1001-907
  36. Park HE, Lee WK. 2018. Immune enhancing effects of Weissella cibaria JW15 on BALB/c mice immunosuppressed by cyclophosphamide. J. Funct. Foods 49: 518-525. https://doi.org/10.1016/j.jff.2018.09.003
  37. Mikkelsen K, Stojanovska L, Prakash M, Apostolopoulos V. 2017. The effects of vitamin B on the immune/cytokine network and their involvement in depression. Maturitas 96: 58-71. https://doi.org/10.1016/j.maturitas.2016.11.012
  38. Tang C, Sun J, Liu J, Jin C, Wu X, Zhang X, et al. 2019. Immune-enhancing effects of polysaccharides from purple sweet potato. Int. J. Biol. Macromol. 123: 923-930. https://doi.org/10.1016/j.ijbiomac.2018.11.187
  39. Choi EJ, Iwasa M, Han KI, Kim WJ, Tang Y, Han WC, et al. 2016. Effect of Enterococcus faecalis EF-2001 on experimentally induced atopic eczema in mice. Food Sci. Biotechnol. 25: 1087- 1093. https://doi.org/10.1007/s10068-016-0175-7
  40. Lin WH, Yu B, Lin CK, Hwang WZ, Tsen HY. 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
  41. Kim JH, L i J, H an S K, Qin P , Kim J, P ark Y, et al. 2016. Characterization of macrophage-activating lactic acid bacteria isolated from Mukeunji. Food Sci. Biotechnol. 25: 595-599. https://doi.org/10.1007/s10068-016-0083-x
  42. Jeong JH, Jang S, Jung BJ, Jang KS, Kim BG, Chung DK, et al. 2015. Differential immune-stimulatory effects of LTAs from different lactic acid bacteria via MAPK signaling pathway in RAW 264.7 cells. Immunobiology 220: 460-466. https://doi.org/10.1016/j.imbio.2014.11.002

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