Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Heat-Killed Lactobacillus plantarum KCTC 13314BP Enhances Phagocytic Activity and Immunomodulatory Effects via Activation of MAPK and STAT3 Pathways

  • Jeong, Minju (Department of Agricultural Biotechnology, Seoul National University) ;
  • Kim, Jae Hwan (Department of Agricultural Biotechnology, Seoul National University) ;
  • Yang, Hee (Department of Agricultural Biotechnology, Seoul National University) ;
  • Kang, Shin Dal (Research Institute of Food and Biotechnology, SPC Group) ;
  • Song, Seongbong (Research Institute of Food and Biotechnology, SPC Group) ;
  • Lee, Deukbuhm (Research Institute of Food and Biotechnology, SPC Group) ;
  • Lee, Ji Su (Division of Bioengineering, Incheon National University) ;
  • Park, Jung Han Yoon (Research Institute of Agriculture and Life Sciences, Seoul National University) ;
  • Byun, Sanguine (Division of Bioengineering, Incheon National University) ;
  • Lee, Ki Won (Department of Agricultural Biotechnology, Seoul National University)
  • Received : 2019.05.30
  • Accepted : 2019.06.13
  • Published : 2019.08.28
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Abstract

Identification of novel probiotic strains is of great interest in the field of functional foods. Specific strains of heat-killed bacteria have been reported to exert immunomodulatory effects. Herein, we investigated the immune-stimulatory function of heat-killed Lactobacillus plantarum KCTC 13314BP (LBP). Treatment with LBP significantly increased the production of $TNF-{\alpha}$ and IL-6 by macrophages. More importantly, LBP was able to enhance the phagocytic activity of macrophages against bacterial particles. Activation of p38, JNK, ERK, $NF-{\kappa}B$, and STAT3 was involved in the immunomodulatory function of LBP. LBP treatment significantly increased production of $TNF-{\alpha}$ by bone marrow-derived macrophages and splenocytes, further confirming the immunostimulatory effect of LBP in primary immune cells. Interestingly, the immunomodulatory effects of LBP were much stronger than those of Lactobacillus rhamnosus GG, a well-known probiotic strain. These results indicate that LBP can be a promising immune-enhancing functional food agent.

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References

  1. Laskin DL. 2009. Macrophages and inflammatory mediators in chemical toxicity: a battle of forces. Chem. Res. Toxicol. 22: 1376-1385. https://doi.org/10.1021/tx900086v
  2. Gordon S. 2016. Phagocytosis: an immunobiologic process. Immunity 44: 463-475. https://doi.org/10.1016/j.immuni.2016.02.026
  3. Wynn TA, Chawla A, Pollard JW. 2013. Macrophage biology in development, homeostasis and disease. Nature 496: 445-455. https://doi.org/10.1038/nature12034
  4. Aderem A, Underhill DM. 1999. Mechanisms of phagocytosis in macrophages. Annu. Rev. Immunol. 17: 593-623. https://doi.org/10.1146/annurev.immunol.17.1.593
  5. Lloberas J, Valverde-Estrella L, Tur J, Vico T, Celada A. 2016. Mitogen-activated protein kinases and mitogen kinase phosphatase 1: a critical interplay in macrophage biology. Front Mol. Biosci. 3: 28.
  6. Rao KM. 2001. MAP kinase activation in macrophages. J. Leukoc. Biol. 69: 3-10.
  7. Valledor AF, Sanchez-Tillo E, Arpa L, Park JM, Caelles C, Lloberas J, et al. 2008. Selective roles of MAPKs during the macrophage response to IFN-gamma. J. Immunol. 180: 4523-4529. https://doi.org/10.4049/jimmunol.180.7.4523
  8. Baeuerle PA, Henkel T. 1994. Function and activation of NF-kappa B in the immune system. Annu. Rev. Immunol. 12: 141-179. https://doi.org/10.1146/annurev.iy.12.040194.001041
  9. Grimm S, Baeuerle PA. 1993. The inducible transcription factor NF-kappa B: structure-function relationship of its protein subunits. Biochem. J. 290 (Pt 2): 297-308. https://doi.org/10.1042/bj2900297
  10. Ghosh S, May MJ, Kopp EB. 1998. NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses. Annu. Rev. Immunol. 16: 225-260. https://doi.org/10.1146/annurev.immunol.16.1.225
  11. Taverniti V, Guglielmetti S. 2011. The immunomodulatory properties of probiotic microorganisms beyond their viability (ghost probiotics: proposal of paraprobiotic concept). Genes Nutr. 6: 261-274. https://doi.org/10.1007/s12263-011-0218-x
  12. Yesilova Y, Calka O, Akdeniz N, Berktas M. 2012. Effect of probiotics on the treatment of children with atopic dermatitis. Ann. Dermatol. 24: 189-193. https://doi.org/10.5021/ad.2012.24.2.189
  13. Doege K, Grajecki D, Zyriax BC, Detinkina E, Zu Eulenburg C, Buhling KJ. 2012. Impact of maternal supplementation with probiotics during pregnancy on atopic eczema in childhood--a meta-analysis. Br. J. Nutr. 107: 1-6. https://doi.org/10.1017/S0007114511003400
  14. Nation ML, Dunne EM, Joseph SJ, Mensah FK, Sung V, Satzke C, et al. 2017. Impact of Lactobacillus reuteri colonization on gut microbiota, inflammation, and crying time in infant colic. Sci. Rep. 7: 15047. https://doi.org/10.1038/s41598-017-15404-7
  15. Chau K, Lau E, Greenberg S, Jacobson S, Yazdani-Brojeni P, Verma N, et al. 2015. Probiotics for infantile colic: a randomized, double-blind, placebo-controlled trial investigating Lactobacillus reuteri DSM 17938. J. Pediatr. 166: 74-78. https://doi.org/10.1016/j.jpeds.2014.09.020
  16. Kadooka Y, Sato M, Imaizumi K, Ogawa A, Ikuyama K, Akai Y, et al. 2010. Regulation of abdominal adiposity by probiotics (Lactobacillus gasseri SBT2055) in adults with obese tendencies in a randomized controlled trial. Eur. J. Clin. Nutr. 64: 636-643. https://doi.org/10.1038/ejcn.2010.19
  17. Andreasen AS, Larsen N, Pedersen-Skovsgaard T, Berg RM, Moller K, Svendsen KD, et al. 2010. Effects of Lactobacillus acidophilus NCFM on insulin sensitivity and the systemic inflammatory response in human subjects. Br. J. Nutr. 104: 1831-1838. https://doi.org/10.1017/S0007114510002874
  18. Ahmad K, Fatemeh F, Mehri N, Maryam S. 2013. Probiotics for the treatment of pediatric helicobacter pylori infection: a randomized double blind clinical trial. Iran J. Pediatr. 23: 79-84.
  19. Hsieh PS, Tsai YC, Chen YC, Teh SF, Ou CM, King VA. 2012. Eradication of Helicobacter pylori infection by the probiotic strains Lactobacillus johnsonii MH-68 and L. salivarius ssp. salicinius AP-32. Helicobacter 17: 466-477. https://doi.org/10.1111/j.1523-5378.2012.00992.x
  20. Seddik HA, Bendali F, Gancel F, Fliss I, Spano G, Drider D. 2017. Lactobacillus plantarum and Its Probiotic and Food Potentialities. Probiotics Antimicrob. Proteins 9: 111-122. https://doi.org/10.1007/s12602-017-9264-z
  21. Capozzi V, Russo P, Ladero V, Fernandez M, Fiocco D, Alvarez MA, et al. 2012. Biogenic amines degradation by lactobacillus plantarum: toward a potential application in wine. Front Microbiol. 3: 122. https://doi.org/10.3389/fmicb.2012.00122
  22. Arif IA, Bakir MA, Khan HA, Al Farhan AH, Al Homaidan AA, Bahkali AH, et al. 2010. Application of RAPD for molecular characterization of plant species of medicinal value from an arid environment. Genet Mol. Res. 9: 2191-2198. https://doi.org/10.4238/vol9-4gmr848
  23. Kawashima T, Hayashi K, Kosaka A, Kawashima M, Igarashi T, Tsutsui H, et al. 2011. Lactobacillus plantarum strain YU from fermented foods activates Th1 and protective immune responses. Int. Immunopharmacol. 11: 2017-2024. https://doi.org/10.1016/j.intimp.2011.08.013
  24. Kikuchi Y, Kunitoh-Asari A, Hayakawa K, Imai S, Kasuya K, Abe K, et al. 2014. Oral administration of Lactobacillus plantarum strain AYA enhances IgA secretion and provides survival protection against influenza virus infection in mice. PLoS One 9: e86416. https://doi.org/10.1371/journal.pone.0086416
  25. Rigaux P, Daniel C, Hisbergues M, Muraille E, Hols P, Pot B, et al. 2009. Immunomodulatory properties of Lactobacillus plantarum and its use as a recombinant vaccine against mite allergy. Allergy 64: 406-414. https://doi.org/10.1111/j.1398-9995.2008.01825.x
  26. Rizzo A, Losacco A, Carratelli CR, Domenico MD, Bevilacqua N. 2013. Lactobacillus plantarum reduces Streptococcus pyogenes virulence by modulating the IL-17, IL-23 and Tolllike receptor 2/4 expressions in human epithelial cells. Int. Immunopharmacol. 17: 453-461. https://doi.org/10.1016/j.intimp.2013.07.005
  27. Segers ME, Lebeer S. 2014. Towards a better understanding of Lactobacillus rhamnosus GG--host interactions. Microb. Cell Fact. 13 Suppl 1: S7. https://doi.org/10.1186/1475-2859-13-S1-S7
  28. Billack B. 2006. Macrophage activation: role of toll-like receptors, nitricoxide, and nuclear factor kappa B. Am. J. Pharm. Educ. 70: 102. https://doi.org/10.5688/aj7005102
  29. Mosser DM, Edwards JP. 2008. Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 8: 958-969. https://doi.org/10.1038/nri2448
  30. Fong FL, Kirjavainen PV, El-Nezami H. 2016. Immunomodulation of Lactobacillus rhamnosus GG (LGG)-derived soluble factors on antigen-presenting cells of healthy blood donors. Sci. Rep. 6: 22845. https://doi.org/10.1038/srep22845
  31. Fong FLY, Kirjavainen P, Wong VHY, El-Nezami H. 2015. Immunomodulatory effects of Lactobacillus rhamnosus GG on dendritic cells, macrophages and monocytes from healthy donors. J. Functional Foods 13: 71-79. https://doi.org/10.1016/j.jff.2014.12.040
  32. Parameswaran N, Patial S. 2010. Tumor necrosis factoralpha signaling in macrophages. Crit. Rev. Eukaryot Gene Expr. 20: 87-103. https://doi.org/10.1615/CritRevEukarGeneExpr.v20.i2.10
  33. Lee JH, Ahn DU, Paik HD. 2018. In vitro immune-enhancing activity of ovotransferrin from egg white via mapk signaling p athways in RAW 264.7 macrophages. Korean J. Food Sci. Anim. Resour. 38: 1226-1236. https://doi.org/10.5851/kosfa.2018.e56
  34. Rosales C, Uribe-Querol E. 2017. Phagocytosis: a fundamental process in immunity. Biomed. Res. Int. 2017: 9042851.
  35. Butprom S, Phumkhachorn P, Rattanachaikunsopon P. 2013. Effect of Lactobacillus plantarum C014 on innate immune response and disease resistance against Aeromonas hydrophila in hybrid catfish. ScientificWorldJournal. 2013: 392523.
  36. Jang SE, Joh EH, Lee HY, Ahn YT, Lee JH, Huh CS, et al. 2013. Lactobacillus plantarum HY7712 ameliorates cyclophosphamide-induced immunosuppression in mice. J. Microbiol. Biotechnol. 23: 414-421. https://doi.org/10.4014/jmb.1210.10010
  37. Ren D, Li C, Qin Y, Yin R, Du S, Liu H, et al. 2015. Evaluation of immunomodulatory activity of two potential probiotic Lactobacillus strains by in vivo tests. Anaerobe 35: 22-27. https://doi.org/10.1016/j.anaerobe.2015.06.008
  38. Meng Y, Li B, Jin D, Zhan M, Lu J, Huo G. 2018. Immunomodulatory activity of Lactobacillus plantarum KLDS1.0318 in cyclophosphamide-treated mice. Food Nutr. Res. 62: doi: 10.29219.

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