Journal of Microbiology and Biotechnology

  • 제32권2호
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  • Pages.205-211
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  • 2022
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  • 1017-7825(pISSN)
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  • 1738-8872(eISSN)
한국미생물·생명공학회 (The Korean Society for Microbiology and Biotechnology)
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Protective Effects of a Novel Lactobacillus brevis Strain with Probiotic Characteristics against Staphylococcus aureus Lipoteichoic Acid-Induced Intestinal Inflammatory Response

  • Kim, Won-Ju (Department of Food Science and Biotechnology of Animal Resources, Konkuk University) ;
  • Hyun, Jun-Hyun (Department of Food Science and Biotechnology of Animal Resources, Konkuk University) ;
  • Lee, Na-Kyoung (Department of Food Science and Biotechnology of Animal Resources, Konkuk University) ;
  • Paik, Hyun-Dong (Department of Food Science and Biotechnology of Animal Resources, Konkuk University)
  • 투고 : 2021.10.21
  • 심사 : 2021.11.04
  • 발행 : 2022.02.28
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초록

Probiotics can effectively modulate host immune responses and prevent gastrointestinal diseases. The objective of this study was to investigate the probiotic characteristics of Lactobacillus brevis KU15152 isolated from kimchi and its protective potential against intestinal inflammation induced by Staphylococcus aureus lipoteichoic acid (aLTA). L. brevis KU15152 exhibited a high survival rate in artificial gastric and bile environments. Additionally, the adhesion capability of the strain to HT-29 cells was higher than that of L. rhamnosus GG. L. brevis KU15152 did not produce harmful enzymes, such as β-glucuronidase, indicating that it could be used as a potential probiotic. The anti-inflammatory potential of L. brevis KU15152 was determined in HT-29 cells. Treatment with L. brevis KU15152 suppressed the production of interleukin-8 without inducing significant cytotoxicity. The downregulatory effects of L. brevis KU15152 were involved in the suppression of nuclear factor-kappa B activation mediated by the extracellular signal-regulated kinase and Akt signaling pathways. Collectively, these data suggest that L. brevis KU15152 can be used in developing therapeutic and prophylactic products to manage and treat aLTA-induced intestinal damage.

키워드

과제정보

This work was supported by the Korea Institute of Planning and Evaluation for Technology in Food, Agriculture and Forestry (IPET) through the High Value-added Food Technology Development Program, funded by the Ministry of Agriculture, Food and Rural Affairs (MAFRA) (#321035-5).

참고문헌

  1. Conlon MA, Bird AR. 2015. The impact of diet and lifestyle on gut microbiota and human health. Nutrients 7: 17-44. https://doi.org/10.3390/nu7010017
  2. Mendes V, Galvao I, Vieira AT. 2019. Mechanisms by which the gut microbiota influences cytokine production and modulates host inflammatory responses. J. Interferon Cytokine Res. 39: 393-409. https://doi.org/10.1089/jir.2019.0011
  3. Issac Ginsburg. 2002. Role of lipoteichoic acid in infection and inflammation. Lancet Infect. Dis. 2: 171-179. https://doi.org/10.1016/S1473-3099(02)00226-8
  4. Jeong JH, Jang S, Jung BJ, Jang KS, Kim BG, Chung DK, et al. 2015. Differential immunue-stimulatory effects of LTAs from different lactic acid bacteria via MAPK signaling pathway in RAW 264.7 cells. Immunobiol. 220: 460-466. https://doi.org/10.1016/j.imbio.2014.11.002
  5. Shokryazdan P, Sieo CC, Kalavathy R, Liang JB, Alitheen NB, Faseleh Jahromi M, et al. 2014. Probiotic potential of Lactobacillus strains with antimicrobial activity against some human pathogenic strains. Biomed. Res. Int. 2014: 927268-927216.
  6. Jiang Y, Li L, Sun H, Shan Y, Liu Y, Li L, et al. 2016. Induction of cytokines via NF-κB and p38 MAP kinase signaling pathways associated with the immunomodulation by Lactobacillus plantarum NDC 75017 in vitro and in vivo. J. Func. Foods 20: 215-225. https://doi.org/10.1016/j.jff.2015.10.027
  7. Gupta T, Kaur H, Kapila S, Kapila R. 2021. Lactobacillus fermentum (MTCC-5898) alleviates Escherichia coli-induced inflammatory responses in intestinal epithelial cells by modulating immune genes and NF-κB signaling. J. Appl. Microbiol. https://doi: 10.1111/jam.15153.
  8. Li X, Hu D, Tian Y, Song Y, Hou Y, Sun L, et al. 2020. Protective effects of a novel Lactobacillus rhamnosus strain with probiotic characteristics against lipopolysaccharide-induced intestinal inflammation in vitro and in vivo. Food Funct. 11: 5799. https://doi.org/10.1039/D0FO00308E
  9. Song MW, Chung Y, Kim KT, Hong WS, Chang HJ, Paik HD. 2020. Probiotic characteristics of Lactobacillus brevis B13-2 isolated from kimchi and investigation of antioxidant and immune-modulating abilities of its heat-killed cells. LWT-Food Sci. Technol. 128: 109452. https://doi.org/10.1016/j.lwt.2020.109452
  10. Yu HS, Lee NK, Choi AJ, Choe JS, Bae CH, Paik HD. 2019. Antagonistic and antioxidant effect of probiotic Weissella cibaria JW15. Food Sci. Biotechnol. 28: 851-855. https://doi.org/10.1007/s10068-018-0519-6
  11. Kim KT, Yang SJ, Paik HD. 2021. Probiotic properties of novel probiotic Levilactobacillus brevis KU15147 isolated from radish kimchi and its antioxidant and immune-enhancing activities. Food Sci. Biotechnol. 30: 257-265. https://doi.org/10.1007/s10068-020-00853-0
  12. Yu HS, Lee NK, Choi AJ, Choe JS, Bae CH, Paik HD. 2019. Anti-inflammatory potential of probiotic strain Weissella cibaria JW15 isolated from kimchi through regulation of NF-κB and MAPKs pathways in LPS-induced RAW 264.7 cells. J. Microbiol. Biotechnol. 29: 1022-1032. https://doi.org/10.4014/jmb.1903.03014
  13. Kim H, Kim HS, Park WJ, Chung DK. 2015. Inhibitory effect of Lactobacillus plantarum extracts on HT-29 colon cancer cell apoptosis induced by Staphylococcus aureus and its alpha-toxin. J. Microbiol. Biotechnol. 25: 1849-1855. https://doi.org/10.4014/jmb.1504.04047
  14. Li SC, Hsu WF, Chang JS, Shih CK. 2019. Combination of Lactobacillus acidophilus and Bifidobacterium animalis subsp. lactis shows a stronger anti-inflammatory effect than individual strains in HT-29 cells. Nutrients 11: 969. https://doi.org/10.3390/nu11050969
  15. Jang HJ, Lee NK, Paik HD. 2019. Probiotic characterization of Lactobacillus brevis KU15153 showing antimicrobial and antioxidant effect isolated from kimchi. Food Sci. Biotechnol. 28: 1521-1528. https://doi.org/10.1007/s10068-019-00576-x
  16. Yu HS, Jang HJ, Lee NK, Paik HD. 2019. Evaluation of the probiotic characteristics and prophylactic potential of Weissella cibaria strains isolated from kimchi. LWT-Food Sci. Technol. 112:108229. https://doi.org/10.1016/j.lwt.2019.05.127
  17. Kim WJ, Yu HS, Bae WY, Ko KY, Chang KH, Lee NK, et al. 2021. Chrysanthemum indicum suppresses adipogenesis by inhibiting mitotic clonal expansion in 3T3-L1 preadipocytes. J. Food Biochem. 45: e13896.
  18. Yu HS, Kim WJ, Bae WY, Lee NK, Paik HD. 2020. Inula britannica inhibits adipogenesis of 3T3-L1 preadipocytes via modulation of mitotic clonal expansion involving ERK 1/2 and Akt signaling pathways. Nutrients 12: 3037. https://doi.org/10.3390/nu12103037
  19. Yang SJ, Kim KT, Kim TY, Paik HD. 2020. Probiotic properties and antioxidant activities of Pediococcus pentosaceus SC28 and Levilactobacillus brevis KU15151 in fermented black gamju. Foods 9: 1154. https://doi.org/10.3390/foods9091154
  20. Singh S, Bhatia R, Singh A, Singh P, Kaur R, Khare P, et al. 2018. Probiotic attributes and prevention of LPS-induced pro-inflammatory stress in RAW264.7 macrophages and human intestinal epithelial cell line (Caco-2) by newly isolated Weissella cibaria strains. Food Func. 9: 1254. https://doi.org/10.1039/C7FO00469A
  21. Bao Y, Zhang Y, Zhang Y, Liu Y, Wang S, Dong X, et al. 2010. Screening of potential probiotic properties of Lactobacillus fermentum isolated from traditional dairy products. Food Control 21: 695-701. https://doi.org/10.1016/j.foodcont.2009.10.010
  22. Guo CF, Zhang S, Yuan YH, Yue TL, Li JY. 2015. Comparison of lactobacilli isolated from Chinese suan-tsai and koumiss for their probiotic and functional properties. J. Funct. Foods 12: 294-302. https://doi.org/10.1016/j.jff.2014.11.029
  23. Argyri AA, Zoumpopoulou G, Karatzas KAG, Tsakalidou E, Nychas GJE, Panagou EZ, et al. 2013. Selection of potential probiotic lactic acid bacteria from fermented olives by in vitro tests. Food Microbiol. 33: 282-291. https://doi.org/10.1016/j.fm.2012.10.005
  24. Lee CS, Kim SH. 2020. Anti-inflammatory and anti-osteoporotic potential of Lactobacillus plantarum A41 and L. fermentum SRK414 as probiotics. Probiotics Antimicrob. Proteins 12: 623-634. https://doi.org/10.1007/s12602-019-09577-y
  25. Kim HG, Lee SY, Kim NR, Ko MY, Lee JM, Yi TH, et al. 2008. Inhibitory effects of Lactobacillus plantarum lipoteichoic acid (LTA) on Staphylococcus aureus LTA-induced tumor necrosis factor-alpha production. J. Microbiol. Biotechnol. 18: 1191-1196.
  26. Wang J, Qi L, Wu Z, Mei L, Wang H. 2016. Different effects of lipoteichoic acid from C. butyricum and S. aureus on inflammatory responses of HT-29 cells. Int. J. Biol. 87: 481-487.
  27. Kim H, Jung BJ, Jung JH, Kim JY, Chung SK, Chung DK. 2012. Lactobacillus plantarum lipoteichoic acid alleviates TNF-α-induced inflammation in the HT-29 intestinal epithelial cell line. Mol. Cells 33: 479-486. https://doi.org/10.1007/s10059-012-2266-5
  28. Singh S, Singh AP, Sharma B, Owen LB, Singh RK. 2010. CXCL8 and its cognate receptors in melanoma progression and metastasis. Future Oncol. 6: 111-116. https://doi.org/10.2217/fon.09.128
  29. Hubert-Buron A, Leblond J, Jacquot A, Ducrotte P, Dechelotte P, Coeffier M. 2006. Glutamine pretreatment reduces IL-8 production in human intestinal epithelial cells by limiting IκBα ubiquitination. J. Nutr. 136: 1461-1465. https://doi.org/10.1093/jn/136.6.1461
  30. Buchholz KR, Stephens RS. 2008. The cytosolic pattern recognition receptor NOD1 induces inflammatory interleukin-8 during Chlamydia trachomatis infection. Infect. Immun. 76: 3150-3155. https://doi.org/10.1128/IAI.00104-08
  31. Fernandes AF, Bian Q, Jiang JK, Thomas CJ, Taylor A, Pereira P, et al. 2009. Proteasome inactivation promotes p38 mitogen-activated protein kinase-dependent phosphatidylinositol 3-kinase activation and increases interleukin-8 production in retinal pigment epithelial cells. Mol. Biol. Cell 16: 3690-3699.
  32. Zhu L, Dai LM, Shen H, Gu PQ, Zheng K, Liu YJ, et al. 2019. Qing Chang Hua Shi granule ameliorate inflammation in experimental rats and cell model of ulcerative colitis through MEK/ERK signaling pathway. Biomed. Pharmacother. 116: 108967. https://doi.org/10.1016/j.biopha.2019.108967
  33. Kohno M, Tanimura S, Ozaki K. 2011. Targeting the extracellular signal-regulated kinase pathway in cancer therapy. Biol. Pharm. Bull. 12: 1781-1784. https://doi.org/10.1248/bpb.34.1781
  34. Long X, Ye Y, Zhang L, Liu P, Yu W, Wei F, et al. 2016. IL-8, a novel messenger to cross-link inflammation and tumor EMT via autocrine and paracrine pathways (review). Int. J. Oncol. 48: 5-12. https://doi.org/10.3892/ijo.2015.3234
  35. Son YO, Pratheeshkumar P, Wang L, Fan J, Kim DH, Lee JY, et al. 2013. Reactive oxygen species mediate Cr(VI)-induced carcinogenesis through PI3K/AKT-dependent activation of GSK-3β/β-catenin signaling. Toxicol. Appl. Pharmacol. 271: 239-248. https://doi.org/10.1016/j.taap.2013.04.036
  36. Maurer U, Preiss F, Brauns-Schubert P, Schlicher L, Charvet C. 2014. GSK-3-at the crossroads of cell death and survival. J. Cell. Sci. 127: 1369-1378. https://doi.org/10.1242/jcs.138057
  37. Zhang Y, Zhang Z, Wang H, Cai N, Zhou S, Zhao Y, et al. 2016. Neuroprotective effect of ginsenoside Rg1 prevents cognitive impairment induced by isoflurane anesthesia in aged rats via antioxidant, anti-inflammatory and anti-apoptotic effects mediated by the PI3K/AKT/GSK-3β pathway. Mol. Med. Rep. 14: 2778-2784. https://doi.org/10.3892/mmr.2016.5556