Lactobacillus Plantarum Surface Layer Adhesive Protein Protects Intestinal Epithelial Cells Against Tight Junction Injury Induced by Enteropathogenic Escherichia Coli

Overview

Journal Mol Biol Rep

Specialty Molecular Biology

Date 2010 Nov 19

PMID 21086172

Citations 22

Authors

Zhihua Liu

Tongyi Shen

Peng Zhang

Yanlei Ma

Huanlong Qin

Affiliations

Soon will be listed here.

Abstract

Lactobacillus plantarum (LP) has previously been used for the treatment and prevention of intestinal disorders and disease. However, the role of the LP surface layer adhesive protein (SLAP) in inhibition of epithelial cell disruption is not fully understood. The aim of the present study was to investigate the protective effects of purified SLAP on Caco-2 cells infected with enteropathogenic Escherichia coli (EPEC). The role of ERK in LP-mediated inhibition of tight junction (TJ) injury was also evaluated in order to determine the molecular mechanisms underlying the protective effects of LP in epithelial cells. SLAP was extracted and purified from LP cells using a porcine stomach mucin-Sepharose 4B column. SLAP-mediated inhibition of bacterial adhesion was measured using a competition-based adhesion assay. Expression of TJ-associated proteins, maintenance of TJ structure, and levels of extracellular signal regulated kinase (ERK) and ERK phosphorylation were assessed in SLAP-treated cells by a combination of real-time PCR, western blotting, and immunofluorescence microscopy. Cell permeability was analyzed by measurement of trans-epithelial electrical resistance (TER) and dextran permeability. The effect of SLAP on levels of apoptosis in epithelial cells was assessed by flow cytometry. Results from these experiments revealed that treatment with SLAP decreased the level of adhesion of EPEC to Caco-2 cells. SLAP treatment also enhanced expression of TJ proteins at both the mRNA and protein levels and affected F-actin distribution. Although ERK levels remained unchanged, ERK phosphorylation was increased by SLAP treatment. Caco-2 cells treated with SLAP exhibited increased TER and decreased macromolecular permeability, which was accompanied by a decrease in the level of apoptosis. Together, these results suggest that LP-produced SLAP protects intestinal epithelial cells from EPEC-induced injury, likely through a mechanism involving ERK activation.

Citing Articles

Postbiotics in colorectal cancer: intervention mechanisms and perspectives.

Xie W, Zhong Y, Li X, Kang Y, Peng Q, Ying H Front Microbiol. 2024; 15:1360225.

PMID: 38450163 PMC: 10914944. DOI: 10.3389/fmicb.2024.1360225.

Mechanisms and applications of probiotics in prevention and treatment of swine diseases.

Zhang Y, Zhang Y, Liu F, Mao Y, Zhang Y, Zeng H Porcine Health Manag. 2023; 9(1):5.

PMID: 36740713 PMC: 9901120. DOI: 10.1186/s40813-022-00295-6.

Emerging role of protein modification in inflammatory bowel disease.

Wang G, Yuan J, Luo J, Ocansey D, Zhang X, Qian H J Zhejiang Univ Sci B. 2022; 23(3):173-188.

PMID: 35261214 PMC: 8913920. DOI: 10.1631/jzus.B2100114.

Precision Postbiotics and Mental Health: the Management of Post-COVID-19 Complications.

Pandey M, Bhati A, Priya K, Sharma K, Singhal B Probiotics Antimicrob Proteins. 2021; 14(3):426-448.

PMID: 34806151 PMC: 8606251. DOI: 10.1007/s12602-021-09875-4.

Early supplementation with Lactobacillus plantarum in liquid diet modulates intestinal innate immunity through toll-like receptor 4-mediated mitogen-activated protein kinase signaling pathways in young piglets challenged with Escherichia coli K88.

Yang K, Zhu C, Wang L, Cao S, Yang X, Gao K J Anim Sci. 2021; 99(6).

PMID: 33928383 PMC: 8212570. DOI: 10.1093/jas/skab128.

References

Rosseland C, Wierod L, Oksvold M, Werner H, Ostvold A, Thoresen G . Cytoplasmic retention of peroxide-activated ERK provides survival in primary cultures of rat hepatocytes. Hepatology. 2005; 42(1):200-7. DOI: 10.1002/hep.20762. View

Johnson-Henry K, Hagen K, Gordonpour M, Tompkins T, Sherman P . Surface-layer protein extracts from Lactobacillus helveticus inhibit enterohaemorrhagic Escherichia coli O157:H7 adhesion to epithelial cells. Cell Microbiol. 2006; 9(2):356-67. DOI: 10.1111/j.1462-5822.2006.00791.x. View

Liu Z, Ma Y, He Y, Zhang P, Zhou Y, Qin H . Tamoxifen reverses the multi-drug-resistance of an established human cholangiocarcinoma cell line in combined chemotherapeutics. Mol Biol Rep. 2010; 38(3):1769-75. DOI: 10.1007/s11033-010-0291-z. View

Kaper J, Nataro J, Mobley H . Pathogenic Escherichia coli. Nat Rev Microbiol. 2004; 2(2):123-40. DOI: 10.1038/nrmicro818. View

Liong M . Safety of probiotics: translocation and infection. Nutr Rev. 2008; 66(4):192-202. DOI: 10.1111/j.1753-4887.2008.00024.x. View

Rioux K, Madsen K, Fedorak R . The role of enteric microflora in inflammatory bowel disease: human and animal studies with probiotics and prebiotics. Gastroenterol Clin North Am. 2005; 34(3):465-82, ix. DOI: 10.1016/j.gtc.2005.05.005. View

Whelan K, Myers C . Safety of probiotics in patients receiving nutritional support: a systematic review of case reports, randomized controlled trials, and nonrandomized trials. Am J Clin Nutr. 2010; 91(3):687-703. DOI: 10.3945/ajcn.2009.28759. View

Chaturvedi L, Gayer C, Marsh H, Basson M . Repetitive deformation activates Src-independent FAK-dependent ERK motogenic signals in human Caco-2 intestinal epithelial cells. Am J Physiol Cell Physiol. 2008; 294(6):C1350-61. PMC: 3971650. DOI: 10.1152/ajpcell.00027.2008. View

Zhang J, Owen C, Sanders M, Turner J, Basson M . The motogenic effects of cyclic mechanical strain on intestinal epithelial monolayer wound closure are matrix dependent. Gastroenterology. 2006; 131(4):1179-89. DOI: 10.1053/j.gastro.2006.08.007. View

10.

Gareau M, Jury J, MacQueen G, Sherman P, Perdue M . Probiotic treatment of rat pups normalises corticosterone release and ameliorates colonic dysfunction induced by maternal separation. Gut. 2007; 56(11):1522-8. PMC: 2095679. DOI: 10.1136/gut.2006.117176. View

11.

Qin H, Zhang Z, Hang X, Jiang Y . L. plantarum prevents enteroinvasive Escherichia coli-induced tight junction proteins changes in intestinal epithelial cells. BMC Microbiol. 2009; 9:63. PMC: 2674056. DOI: 10.1186/1471-2180-9-63. View

12.

Chaturvedi L, Marsh H, Shang X, Zheng Y, Basson M . Repetitive deformation activates focal adhesion kinase and ERK mitogenic signals in human Caco-2 intestinal epithelial cells through Src and Rac1. J Biol Chem. 2006; 282(1):14-28. DOI: 10.1074/jbc.M605817200. View

13.

Gopal P, Prasad J, Smart J, Gill H . In vitro adherence properties of Lactobacillus rhamnosus DR20 and Bifidobacterium lactis DR10 strains and their antagonistic activity against an enterotoxigenic Escherichia coli. Int J Food Microbiol. 2001; 67(3):207-16. DOI: 10.1016/s0168-1605(01)00440-8. View

14.

Prisciandaro L, Geier M, Butler R, Cummins A, Howarth G . Probiotics and their derivatives as treatments for inflammatory bowel disease. Inflamm Bowel Dis. 2009; 15(12):1906-14. DOI: 10.1002/ibd.20938. View

15.

Johnson-Henry K, Donato K, Shen-Tu G, Gordanpour M, Sherman P . Lactobacillus rhamnosus strain GG prevents enterohemorrhagic Escherichia coli O157:H7-induced changes in epithelial barrier function. Infect Immun. 2008; 76(4):1340-8. PMC: 2292865. DOI: 10.1128/IAI.00778-07. View

16.

Apostolou E, Kirjavainen P, Saxelin M, Rautelin H, Valtonen V, Salminen S . Good adhesion properties of probiotics: a potential risk for bacteremia?. FEMS Immunol Med Microbiol. 2001; 31(1):35-9. DOI: 10.1111/j.1574-695X.2001.tb01583.x. View

17.

Hayes M, Ross R, Fitzgerald G, Hill C, Stanton C . Casein-derived antimicrobial peptides generated by Lactobacillus acidophilus DPC6026. Appl Environ Microbiol. 2006; 72(3):2260-4. PMC: 1393211. DOI: 10.1128/AEM.72.3.2260-2264.2006. View

18.

Francius G, Alsteens D, Dupres V, Lebeer S, De Keersmaecker S, Vanderleyden J . Stretching polysaccharides on live cells using single molecule force spectroscopy. Nat Protoc. 2009; 4(6):939-46. DOI: 10.1038/nprot.2009.65. View

19.

Granato D, Bergonzelli G, Pridmore R, Marvin L, Rouvet M, Corthesy-Theulaz I . Cell surface-associated elongation factor Tu mediates the attachment of Lactobacillus johnsonii NCC533 (La1) to human intestinal cells and mucins. Infect Immun. 2004; 72(4):2160-9. PMC: 375183. DOI: 10.1128/IAI.72.4.2160-2169.2004. View

20.

Bousvaros A, Guandalini S, Baldassano R, Botelho C, Evans J, Ferry G . A randomized, double-blind trial of Lactobacillus GG versus placebo in addition to standard maintenance therapy for children with Crohn's disease. Inflamm Bowel Dis. 2005; 11(9):833-9. DOI: 10.1097/01.mib.0000175905.00212.2c. View