Browse > Article
http://dx.doi.org/10.4014/jmb.1512.12002

Lactic Acid Bacteria Improves Peyer's Patch Cell-Mediated Immunoglobulin A and Tight-Junction Expression in a Destructed Gut Microbial Environment  

Kim, Sung Hwan (R&BD Center, Korea Yakult Co. Ltd.)
Jeung, Woonhee (R&BD Center, Korea Yakult Co. Ltd.)
Choi, Il-Dong (R&BD Center, Korea Yakult Co. Ltd.)
Jeong, Ji-Woong (R&BD Center, Korea Yakult Co. Ltd.)
Lee, Dong Eun (R&BD Center, Korea Yakult Co. Ltd.)
Huh, Chul-Sung (College of Agriculture and Life Sciences, Seoul National University)
Kim, Geun-Bae (Department of Animal Science and Technology, Chung-Ang University)
Hong, Seong Soo (Division of Gastroenterology, Vievisnamuh Hospital)
Shim, Jae-Jung (R&BD Center, Korea Yakult Co. Ltd.)
Lee, Jung Lyoul (R&BD Center, Korea Yakult Co. Ltd.)
Sim, Jae-Hun (R&BD Center, Korea Yakult Co. Ltd.)
Ahn, Young-Tae (R&BD Center, Korea Yakult Co. Ltd.)
Publication Information
Journal of Microbiology and Biotechnology / v.26, no.6, 2016 , pp. 1035-1045 More about this Journal
Abstract
To evaluate the effects of lactic acid bacteria (LAB) on Peyer's patch cells, mice were treated with a high dose of kanamycin to disturb the gut microbial environment. The overarching goal was to explore the potential of LAB for use as a dietary probiotic that buffers the negative consequences of antibiotic treatment. In vitro, LAB stimulated the production of immunoglobulin A (IgA) from isolated Peyer's patch cells. Inflammation-related genes (TNF-α, IL-1β, and IL-8) were up-regulated in Caco-2 cells stimulated with lipopolysaccharide (LPS), while tight-junction-related genes (ZO-1 and occludin) were down-regulated; the effects of LPS on inflammatory gene and tight-junction gene expression were reversed by treatment with LAB. Mice treated with a high dose of kanamycin showed increased serum IgE levels and decreases in serum IgA and fecal IgA levels; the number of Peyer's patch cells decreased with kanamycin treatment. However, subsequent LAB treatment was effective in reducing the serum IgE level and recovering the serum IgA and fecal IgA levels, as well as the number of Peyer's patch cells. In addition, ZO-1 and occludin mRNA levels were up-regulated in the ileum tissues of mice receiving LAB treatment. Lactic acid bacteria can enhance the intestinal immune system by improving the integrity of the intestinal barrier and increasing the production of IgA in Peyer's patches. Lactic acid bacteria should be considered a potential probiotic candidate for improving intestinal immunity, particularly in mitigating the negative consequences of antibiotic use.
Keywords
Lactic acid bacteria; Peyer's patch; Caco-2 cells; IgA; tight junction; kanamycin;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Lim BO, Lee SH, Park DK, Choue RW. 2003. Effect of dietary pectin on the production of immunoglobulins and cytokines by mesenteric lymph node lymphocytes in mouse colitis induced with dextran sulfate sodium. Biosci. Biotechnol. Biochem. 67: 1706-1712.   DOI
2 Liu Z, Li N, Neu J. 2005. Tight junctions, leaky intestines, and pediatric diseases. Acta Paediatr. 94: 386-393.   DOI
3 Rey J, Garin N, Spertini F, Corthesy B. 2004. Targeting of secretory IgA to Peyer’s patch dendritic and T cells after transport by intestinal M cells. J. Immunol. 172: 3026-3033.   DOI
4 Penders J, Stobberingh EE, van den Brandt PA, Thijs C. 2007. The role of the intestinal microbiota in the development of atopic disorders. Allergy 62: 1223-1236.   DOI
5 Perdigon G, Medina M, Vintini E, Valdez JC. 2000. Intestinal pathway of internalization of lactic acid bacteria and gut mucosal immunostimulation. Int. J. Immunopathol. Pharmacol. 13: 141-150.
6 Perdigon G, Vintini E, Alvarez S, Medina M, Medici M. 1999. Study of the possible mechanisms involved in the mucosal immune system activation by lactic acid bacteria. J. Dairy Sci. 82: 1108-1114.   DOI
7 Kraehenbuhl JP, Neutra MR. 2000. Epithelial M cells: differentiation and function. Annu. Rev. Cell Dev. Biol. 16: 301-332.   DOI
8 Maes M, Leunis JC. 2008 Normalization of leaky gut in chronic fatigue syndrome (CFS) is accompanied by a clinical improvement: effects of age, duration of illness and the translocation of LPS from gram-negative bacteria. Neuroendocrinol. Lett. 29: 902-910.
9 Macpherson AJ, Gatto D, Sainsbury E, Harriman GR, Hengartner H, Zinkernagel RM. 2000. A primitive T cell-independent mechanism of intestinal mucosal IgA responses to commensal bacteria. Science 288: 2222-2226.   DOI
10 Macpherson AJ, Hunziker L, McCoy K, Lamarre A. 2001. IgA responses in the intestinal mucosa against pathogenic and non-pathogenic microorganisms. Microbes Infect. 3: 1021-1035.   DOI
11 Thitaram SN, Siragusa GR, Hinton A. 2005. Bifidobacterium-selective isolation and enumeration from chicken caeca by a modified oligosaccharide antibiotic-selective agar medium. Lett. Appl. Microbiol. 41: 355-360.   DOI
12 Sudo N, Yu XN, Aiba Y, Oyama N, Sonoda J, Koga Y, Kubo C. 2002. An oral introduction of intestinal bacteria prevents the development of a long-term Th2-skewed immunological memory induced by neonatal antibiotic treatment in mice. Clin. Exp. Allergy 32: 1112-1116.   DOI
13 Vaarala O, Atkinson MA, Neu J. 2008. The “perfect storm” for type 1 diabetes: the complex interplay between intestinal microbiota, gut permeability, and mucosal immunity. Diabetes 57: 2555-2562.   DOI
14 Takahashi T, Nakagawa E, Nara T, Yajima T, Kuwata T. 1998. Effects of orally ingested Bifidobacterium longum on the mucosal IgA response of mice to dietary antigens. Biosci. Biotechnol. Biochem. 62: 10-15.   DOI
15 Ubeda C, Pamer EG. 2012. Antibiotics, microbiota, and immune defense. Trends Immunol. 33: 459-466.   DOI
16 Vanderploeg R, Panaccione R, Ghosh S, Rioux K. 2010. Influences of intestinal bacteria in human inflammatory bowel disease. Infect. Dis. Clin. North Am. 24: 977-993.   DOI
17 Van Itallie CM, Anderson JM. 2006. Claudins and epithelial paracellular transport. Annu. Rev. Physiol. 68: 403-429.   DOI
18 Sekirov I, Russell SL, Antunes LC, Finlay BB. 2010. Gut microbiota in health and disease. Physiol. Rev. 90: 859-904.   DOI
19 Rupnik M, Wilcox MH, Gerding DN. 2009. Clostridium difficile infection: new developments in epidemiology and pathogenesis. Nat. Rev. Microbiol. 7: 526-536.   DOI
20 Sandek A, Rauchhaus M, Anker SD, von Haehling S. 2008. The emerging role of the gut in chronic heart failure. Curr. Opin. Clin. Nutr. Metab. Care 11: 632-639.   DOI
21 Silbart LK, Keren DF. 1989. Reduction of intestinal carcinogen absorption by carcinogen-specific secretory immunity. Science 243: 1462-1464.   DOI
22 Song HJ, Shim KN, Jung SA, Choi HJ, Lee MA, Ryu KH, et al. 2008. Antibiotic-associated diarrhea: candidate organisms other than Clostridium difficile. Korean J. Intern. Med. 23: 9-15.   DOI
23 Stokes CR, Soothill JF, Turner MW. 1975. Immune exclusion is a function of IgA. Nature 255: 745-746.   DOI
24 Hart A, Kamm MA. 2002. Review article: mechanisms of initiation and perpetuation of gut inflammation by stress. Aliment. Pharmacol. Ther. 16: 2017-2028.   DOI
25 Fuller R. 1989. Probiotics in man and animals. J. Appl. Bacteriol. 66: 365-378.   DOI
26 Feldman GJ, Mullin JM, Ryan MP. 2005. Occludin: structure, function and regulation. Adv. Drug Deliver. Rev. 57: 883-917.   DOI
27 Guttman JA, Samji FN, Li Y, Vogl AW, Finlay BB. 2006. Evidence that tight junctions are disrupted due to intimate bacterial contact and not inflammation during attaching and effacing pathogen infection in vivo. Infect. Immun. 74: 6075-6084.   DOI
28 Hosono A, Lee J, Ametani A, Natsume M, Hirayama M, Adachi T, Kaminogawa S. 1997. Characterization of a water-soluble polysaccharide fraction with immunopotentiating activity from Bifidobacterium adolescentis M101-4. Biosci. Biotechnol. Biochem. 61: 312-316.   DOI
29 Cunningham-Rundles C. 2001. Physiology of IgA and IgA deficiency. J. Clin. Immunol. 21: 303-309.   DOI
30 Farquhar MG, Palade GE. 1963. Junctional complexes in various epithelia. J. Cell Biol. 17: 375-412.   DOI
31 Naomi O, Nobuyuki S, Hiroshi S, Chiharu K. 2001. Antibiotic use during infancy promotes a shift in the Th1/Th2 balance toward Th2-dominant immunity in mice. J. Allergy Clin. Immunol. 107: 153-159.   DOI
32 Young VB, Schmidt TM. 2004. Antibiotic-associated diarrhea accompanied by large-scale alterations in the composition of the fecal microbiota. J. Clin. Microbiol. 42: 1203-1206.   DOI
33 Makino H, Kushiro A, Ishikawa E, Kubota H, Gawad A, Sakai T, et al. 2013. Mother-to-infant transmission of intestinal bifidobacterial strains has an impact on the early development of vaginally delivered infant’s microbiota. PLoS One 8: e78331.   DOI
34 Manichanh C, Rigottier-Gois L, Bonnaud E, Gloux K, Pelletier E, Frangeul L, et al. 2006. Reduced diversity of faecal microbiota in Crohn’s disease revealed by a metagenomic approach. Gut 55: 205-211.   DOI
35 Matsumoto M, Ishige A, Yazawa Y, Kondo M, Muramatsu K, Watanabe K. 2012. Promotion of intestinal peristalsis by Bifidobacterium spp. capable of hydrolysing sennosides in mice. PLoS One 7: e31700.   DOI
36 McGhee JR, Mestecky J, Dertzbaugh MT, Eldridge JH, Hirasawa M, Kiyono H. 1992. The mucosal immune system: from fundamental concepts to vaccine development. Vaccine 10: 75-88.   DOI
37 Maes M. 2008. The cytokine hypothesis of depression: inflammation, oxidative & nitrosative stress (IO&NS) and leaky gut as new targets for adjunctive treatments in depression. Neuroendocrinol. Lett. 29: 287-291.
38 Oboki K, Ohno T, Saito H, Nakae S. 2008. Th17 and allergy. Allergol. Int. 57: 121-134.   DOI
39 McGuckin MA, Eri R, Simms LA, Florin TH, Radford-Smith G. 2009. Intestinal barrier dysfunction in inflammatory bowel diseases. Inflamm. Bowel Dis. 15: 100-113.   DOI
40 Mullin J, Valenzano M, Verrecchio J, Kothari R. 2002. Age-and diet-related increase in transepithelial colon permeability of Fischer 344 rats. Dig. Dis. Sci. 47: 2262-2270.   DOI
41 Oyama N, Sudo N, Sogawa H, Kubo C. 2001. Antibiotic use during infancy promotes a shift in the T(H)1/T(H)2 balance toward T(H)2-dominant immunity in mice. J. Allergy Clin. Immunol. 107: 153-159.   DOI
42 Orban JI, Patterson JA. 2000. Modification of the phosphoketolase assay for rapid identification of bifidobacteria. J. Microbiol. Methods 40: 221-224.   DOI
43 Bazzoni G, Dejana E. 2004. Endothelial cell-to-cell junctions: molecular organization and role in vascular homeostasis. Physiol. Rev. 84: 869-901.   DOI
44 Al-Sadi RM, Ma TY. 2007. IL-1b causes an increase in epithelial tight junction permeability. Intest. J. Immunol. 178: 4641-4649.
45 Abbas AK. 1996. Die and let live: eliminating dangerous lymphocytes. Cell 84: 655-657.   DOI
46 Andre C, Lambert R, Bazin H, Heremans JF. 1974. Interference of oral immunization with the intestinal absorption of heterologous albumin. Eur. J. Immunol. 4: 701-704.   DOI
47 Angrisano T, Pero R, Peluso S, Keller S, Sacchetti S, Bruni CB, et al. 2010. LPS-induced IL-8 activation in human intestinal epithelial cells is accompanied by specific histone H3 acetylation and methylation changes. BMC Microbiol. 10: 172-180.   DOI
48 Barbara G. 2006. Mucosal barrier defects in irritable bowel syndrome: who left the door open? Am. J. Gastroenterol. 101: 1295-1298.   DOI
49 Boullier S, Tanguy M, Kadaoui KA, Caubet C, Sansonetti P, Corthesy B. 2009. Secretory IgA-mediated neutralization of Shigella flexneri prevents intestinal tissue destruction by down-regulating inflammatory circuits. J. Immunol. 183: 5879-5885.   DOI
50 Bruewer M, Samarin S, Nusrat A. 2006. Inflammatory bowel disease and the apical junctional complex. Ann. NY Acad. Sci. 1072: 242-252.   DOI
51 Yan F, Polk DB. 2010. Probiotics: progress toward novel therapies for intestinal diseases. Curr. Opin. Gastroenterol. 26: 95-101.   DOI
52 Van Itallie CM, Anderson JM. 1997. Occludin confers adhesiveness when expressed in fibroblasts. J. Cell Sci. 110: 1113-1121.
53 Wachtel M, Bolliger MF, Ishihara H, Frei K, Bluethmann H, Gloor SM. 2001. Down-regulation of occludin expression in astrocytes by tumour necrosis factor (TNF) is mediated via TNF type-1 receptor and nuclear factor-κB activation. J. Neurochem. 78: 155-162.   DOI
54 Yamada K, Tokunaga Y, Ikeda A, Ohkura K, Kaku-Ohkura S, Mamiya S, et al. 2003. Effect of dietary fiber on the lipid metabolism and immune function of aged Sprague-Dawley rats. Biosci. Biotechnol. Biochem. 67: 429-433.   DOI
55 Wilcox MH. 2003. Gastrointestinal disorders and the critically ill. Clostridium difficile infection and pseudomembranous colitis. Best Pract. Res. Clin. Gastroenterol. 17: 475-493.   DOI
56 Schiffrin EJ, Brassart D, Servin AL, Rochat F, Donnet-Hughes A. 1997. Immune modulation of blood leukocytes in humans by lactic acid bacteria: criteria for strain selection. Am. J. Clin. Nutr. 66: 515S-520S.   DOI