Browse > Article
http://dx.doi.org/10.4014/jmb.1903.03054

Lactobacillus casei Zhang Prevents Jejunal Epithelial Damage to Early-Weaned Piglets Induced by Escherichia coli K88 via Regulation of Intestinal Mucosal Integrity, Tight Junction Proteins and Immune Factor Expression  

Wang, Yuying (College of Veterinary Medicine, China Agricultural University)
Yan, Xue (State Key Laboratory of Direct-Fed Microbial Engineering, Beijing DaBeiNong Science and Technology Group Co., Ltd. (DBN))
Zhang, Weiwei (College of Veterinary Medicine, China Agricultural University)
Liu, Yuanyuan (State Key Laboratory of Direct-Fed Microbial Engineering, Beijing DaBeiNong Science and Technology Group Co., Ltd. (DBN))
Han, Deping (College of Veterinary Medicine, China Agricultural University)
Teng, Kedao (College of Veterinary Medicine, China Agricultural University)
Ma, Yunfei (College of Veterinary Medicine, China Agricultural University)
Publication Information
Journal of Microbiology and Biotechnology / v.29, no.6, 2019 , pp. 863-876 More about this Journal
Abstract
Farm animals such as piglets are often affected by environmental stress, which can disturb the gut ecosystem. Antibiotics were commonly used to prevent diarrhea in weaned piglets, but this was banned by the European Union due to the development of antibiotic resistance. However, the use of probiotics instead of antibiotics may reduce the risk posed by pathogenic microorganisms and reduce the incidence of gastrointestinal diseases. Therefore, this study was conducted to investigate the effects of Lactobacillus casei Zhang on the mechanical barrier and immune function of early-weaned piglets infected using Escherichia coli K88 based on histomorphology and immunology. Fourteen-day-old weaned piglets were divided into a control group and experimental groups that were fed L. casei Zhang and infected with E. coli K88 with or without prefeeding and/or postfeeding of L. casei Zhang. The L. casei Zhang dose used was $10^7CFU/g$ diet. Jejunum segments were obtained before histological, immunohistochemical, and western blot analyses were performed. In addition, the relative mRNA expression of toll receptors and cytokines was measured. Piglets fed L. casei Zhang showed significantly increased jejunum villus height, villus height-crypt depth ratio, muscle thickness, and expression of proliferating cell nuclear antigen and tight junction proteins ZO-1 and occludin. The use of L. casei Zhang effectively reduced intestinal inflammation after infection. We found that L. casei Zhang feeding prevented the jejunum damage induced by E. coli K88, suggesting that it may be a potential alternative to antibiotics for preventing diarrhea in early-weaned piglets.
Keywords
Lactobacillus casei Zhang; jejunum of weaned piglets; mechanical barrier; Toll-like receptor; cytokine;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Bron PA, Kleerebezem M, Brummer RJ, Cani PD. 2017. Can probiotics modulate human disease by impacting intestinal barrier function? Br. J. Nutr. 117: 93-107.   DOI
2 Nemcova R, Bomba A, Gancarcikova S, Reiffova K, Guba P, Koscova J, et al. 2007. Effects of the administration of lactobacilli, maltodextrins and fructooligosaccharides upon the adhesion of E. coli O8: K88 to the intestinal mucosa and organic acid levels in the gut contents of piglets. Vet. Res. Commun. 31: 791-800.   DOI
3 Zhang H , Meng H B L, W ang JG, Sun TS, Xu J , Wang L P, et al. 2006. Research on the potential probiotic characteristics of L. casei Zhang isolated from traditional fermented sour milk in Inner Mongolia, China Dairy Industry 34: 4-10.
4 Zhang H, Zhang QJ, Ren GQ, Bao QH., 2007. The protective effect of Lactobacillus on challenged mice and its influence on intestinal flora. Microbiology Bulletin 34: 447-45.
5 Zhao HM., Huang XY, Zuo ZQ, Pan QH., Ao MY, Zhou F, et al. 2013.Probiotics increase T regulatory cells and reduce severity of experimental colitis in mice. World J. Gastroenterol. 19: 742-749.   DOI
6 Matsumoto S, Hara T, Hori T, Mitsuyama K, Nagaoka M, Tomiyasu N, et al. 2005. Probiotic Lactobacillus induced improvement in murine chronic inflammatory bowel disease is associated with the down regulation of proinflammatory cytokines in lamina propria mononuclear cells. Cli. Exp. Immunol. 140: 417-426.   DOI
7 Fujiwara M, Kaneko T, Iwana H, Taketomo N, Tsunoo H, Kanno J, et al. 2003. Okayasu I. Inhibitory effects of Bifidobacterium longum on experimental ulcerative colitis induced in mice by synthetic dextran sulfate sodium. Digestion 67: 90-95.   DOI
8 Osman N, Adawi D, Ahrne S, Jeppsson B, Molin G, 2004. Modulation of the effect of dextran sulfate sodium-induced acute colitis by the administration of different probiotic strains of Lactobacillus and Bifidobacterium. Dig. Dis. Sci. 49: 320-327.   DOI
9 Pluske JR, Hampson, DJ, Williams IH. 1997. Factors influencing the structure and function of the small intestine in the weaned pig: a review. Livest. Prod. Sci. 51: 215-236.   DOI
10 Chichlowski M, Croom WJ, Edens FW, MacBride BW, Qiu R, Chiang CC, et al. 2007. Microarchitecture and spatial relationship between bacteria and ileal, cecal, and colonic epithelium in chicks fed a direct-fed microbial, PrimaLac, and Salinomycin. Poult. Sci. 86: 1121-1132.   DOI
11 Samanya M, Yamauchi K, 2002. Histological alterations of intestinal villi in chickens fed dried Bacillus subtilis var natto. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 133: 95-104.   DOI
12 Mailand N, Gibbs-Seymour I, Bekker-Jensen S. 2013. Regulation of PCNA-protein interactions for genome stability. Nat. Rev. Mol. Cell Biol. 14: 269-82.   DOI
13 Nusrat A, Turner JR., Madara JL,. 2000. Regulation of tight junctions by extracellular stimuli: nutrients, cytokines, and immune cells. Am. J. Physiol. Gastrointest. Liver Physiol. 279: G851-G857.   DOI
14 Fasano A. 2011. Zonulin and its regulation of intestinal barrier function: the biological door to inflammation, autoimmunity, and cancer. Physiol. Rev. 91: 151-175.   DOI
15 Khailova L, Dvorak K, Arganbright KM, Halpern MD, Kinouchi T, Yajima M, et al. 2009. Bifidobacterium bifidum improves intestinal integrity in a rat model of necrotizing enterocolitis. Am. J. Physiol.Gastrointest. Liver Physiol. 297: G940-949.   DOI
16 Lalles JP, Bosi P, Smidt H, Stokes CR. 2007. Weaning-a challenge to gut physiologists. Livest. Sci. 108: 82-93.   DOI
17 Parassol N, Freitas M, Thoreux K, Dalmasso G, Bourdet-Sicard R, Rampal P, 2005. Lactobacillus casei DN-114 001 inhibits the increase in paracellular permeability of enteropathogenic Escherichia coli-infected T84 cells. Res. Microbiol. 156: 256-262.   DOI
18 Resta-Lenert, S, Barrett KE. 2003. Live probiotics protect intestinal epithelial cells from the effects of infection with enteroinvasive Escherichia coli (EIEC). Gut 52: 988-997.   DOI
19 Lim KH, Staudt LM. 2013. Toll-like receptor signaling. Cold Spring Harb. Perspect. Biol. 5: a011247.   DOI
20 Halas D, Heo JM, Hansen CF, Kim JC, Hampson DJ, Mullan BP, et al. 2007. Organic acids, prebiotics and protein level as dietary tools to control the weaning transition and reduce post-weaning diarrhoea in piglets. CAB Rev. Perspectives Agric. Vet. Sci. Nutr. Nat. Res. 79: 13.
21 Heo JM, Opapeju FO, Pluske JR, Kim JC, Hampson DJ, Nyachoti CM. 2013.Gastrointestinal health and function in weaned pigs: a review of feeding strategies to control postweaning diarrhoea without using in-feed antimicrobial compounds. J. Anim. Physiol. Anim. Nutr. 97: 207-237.   DOI
22 McDermott PF, Walker RD, White DG. 2003. Antimicrobials: modes of action and mechanisms of resistance. Int. J. Toxicol. 22: 135-143.   DOI
23 Kemper N. 2008. Veterinary antibiotics in the aquatic and terrestrial environment. Ecol. Indic. 8: 1-13.   DOI
24 Yanju C. 2012. Effects of probiotics on TLR2, TLR4 expression and NF-${\kappa}B$ activity in intestinal mucosa of rats with experimental colitis. J. Gastroenterol. Hepatol. 21: 760-763.
25 Shimazu T, Villena J, Tohno M, Fujie H, Hosoya S, Shimosato T. et al. 2012. Immunobiotic Lactobacillus jensenii elicits anti-inflammatory activity in porcine intestinal epithelial cells by modulating negative regulators of the Toll-like receptor signaling pathway. Infect. Immun. 80: 276-288.   DOI
26 Villena J, Suzuki R, Fujie H, Chiba E, Takahashi T, Tomosada Y, et al. 2012. Immunobiotic Lactobacillus jensenii modulates the Toll-like receptor 4-induced inflammatory response via negative regulation in porcine antigenpresenting cells. Clin. Vaccine Immunol. 19: 1038-1053.   DOI
27 Deng J, Li Y, Zhang J, Yang Q. 2013. Co-administration of Bacillus subtilis RJGP16 and Lactobacillus salivarius B1 strongly enhances the intestinal mucosal immunity of piglets. Res. Vet. Sci. 94: 62-68.   DOI
28 Castillo NA, Perdigon G, de LeBlanc AM. 2011. Oral administration of a probiotic Lactobacillu modulates cytokine production and TLR expression improving the immune response against Salmonella enterica serovar Typhimurium infection in mice. BMC Microbiol. 11: 177.   DOI
29 Galdeano CM, Perdigon G. 2006. The probiotic bacterium Lactobacillus casei induces activation of the gut mucosal immune system through innate immunity. Clin. Vaccine Immunol. 13: 219-226.   DOI
30 Yang X, Fu Y, Liu J, Ren HY. 2013. Impact of probiotics on toll-like receptor 4 expression in an experimental model of ulcerative colitis. J. Huazhong Univ. Sci. Technol. Med. Sci. 33: 661-665.   DOI
31 Saraiva M, O'Garra A. 2010. The regulation of IL-10 production by immune cells. Nat. Rev. Immunol. 10: 170-181.   DOI
32 Katz Y, Nadiv O, Rapoport MJ, Loos M. 2000. IL-17 regulates gene expression and protein synthesis of the complement system, C3 and factor B, in skin fibroblasts. Clin. Exp. Immunol. 120: 22-29.   DOI
33 Zelova H, Hosek J. 2013. TNF-${\alpha}$ signalling and inflammation: interactions between old acquaintances. Inflamm. Res. 62: 641-651.   DOI
34 Dong C, Flavell RA. 2001. Th1 and Th2 cells. Curr. Opin. Hematol. 8: 47-51.   DOI
35 Dieleman LA, Goerres MS, Arends A, Sprengers D, Torrice C, Hoentjen F, et al. 2003. Lactobacillus GG prevents recurrence of colitis in HLA-B27 transgenic rats after antibiotic treatment. Gut 52: 370-376.   DOI
36 Tuo Y, Zhang QJ, Chu FL, Merritt J, Bilige M, Sun,TS, et al. 2008. Immunological evaluation of Lactobacillus casei Zhang: a newly isolated strain from koumiss in Inner Mongolia, China. BMC Immunol. 9: 68   DOI
37 Alexopoulos C, Georgoulakis IE, Tzivara A, Kyriakis CS, Govaris A, Kyriakis SC. 2004. Fiel evaluation of the effect of a probiotic-containing Bacillus licheniformis and Bacillus subtilis spores on the health status, performance, and carcass quality of grower and finisher pigs. J. Vet. Med. Series A 51: 306-312.   DOI
38 Konstantinov SR, Smidt H, Akkermans AD, Casini L, Trevisi P, Mazzoni M, et al. 2008. Feeding of Lactobacillus sobrius reduces Escherichia coli F4 levels in the gut and promotes growth of infected piglets. FEMS Microbiol. Ecol. 66: 599-607.   DOI
39 Modesto M, D'Aimmo MR, Stefanini I, Trevisi P, Filippi SD, Casini L, et al. 2009. A novel strategy to select Bifidobacterium strains and prebiotics as natural growth promoters in newly weaned pigs. Livest. Sci. 122: 248-258.   DOI
40 Wu RN, Wang LP, Wang JC, Li HP, Menghe B, Wu JR, et al. 2009. Isolation and preliminary probiotic selection of Lactobacilli from koumiss in Inner Mongolia. J. Basic Microbiol. 49: 1-9.   DOI
41 Rescigno M. 2011.The intestinal epithelial barrier in the control of homeostasis and immunity. Trends Immunol. 32: 256-264.   DOI
42 Sun Y, Kim SW. 2017. Intestinal challenge with enterotoxigenic Escherichia coli in pigs, and nutritional intervention to prevent postweaning diarrhea. Anim. Nutr. 3: 322-330.   DOI
43 Bron PA, van Baarlen P, Kleerebezem M. 2011. Emerging molecular insights into the interaction between probiotics and the host intestinal mucosa. Nat. Rev. Microbiol. 10: 66-78.   DOI
44 Wan LY, Chen ZJ, Shah NP, El-Nezami H. 2016. Modulation of intestinal epithelial defense responses by probiotic bacteria. Crit. Rev. Food Sci. Nutr. 56: 2628-2641.   DOI
45 Tezuka H., Abe Y, Iwata M., Takeuchi H., Ishikawa H., Matsushita M, et al. 2007. Regulation of IgA production by naturally occurring TNF/iNOS-producing dendritic cells. Nature 448: 929-933.   DOI
46 Ya T, Zhang Q, Chu F, Merritt J, Bilige M, Sun T, et al. 2008. Immunological evaluation of Lactobacillus casei Zhang: a newly isolated strain from koumiss in Inner Mongolia, China. BMC Immunol. 9: 68.   DOI
47 Gill HS. 2003. Probiotics to enhance anti-infective defences in the gastrointestinal tract. Best Pract. Res. Clin. Gastroenterol. 17: 755-773.   DOI
48 Fagarasan S, Kawamoto S, Kanagawa O, Suzuki K. 2009. Adaptive immune regulation in the gut: T cell-dependent and T cell-independent IgA synthesis. Annu. Rev. Immunol. 28: 243-273.   DOI
49 Ogawa M, Shimizu K, Nomoto K, Takahashi M, Watanuki M, Tanaka R, et al. 2001. Protective effect of Lactobacillus casei strain Shirota on Shiga toxin-producing Escherichia coli O157:H7 infection in infant rabbits. Infect. Immun. 69: 1101-1108.   DOI
50 Martins FS, S ilva AA, V ieira AT, B arbosa FH, Arantes RM, Teixeira MM, et al. 2009. Comparative study of Bifidobacterium animalis, Escherichia coli, Lactobacillus casei and Saccharomyces boulardii probiotic properties. Arch. Microbiol. 191: 623-630.   DOI
51 Shu Q, Gill HS. 2001. A dietary probiotic (Bifidobacterium lactis HN019) reduces the severity of Escherichia coli O157:H7 infection in mice. Med. Microbiol. Immunol. 189: 147-152.   DOI
52 Shandilya UK, Sharma A, Kapila R, Kansal VK. 2016. Probiotic Dahi containing Lactobacillus acidophilus and Bifidobacterium bifidum modulates immunoglobulin levels and cytokines expression in whey proteins sensitised mice. J. Sci. Food Agric. 96: 3180-3187.   DOI