Enterotoxigenic Escherichia coli infection induces tight junction proteins expression in mice

Document Type : Full paper (Original article)

Authors

College of Animal Science and Technology, Hunan Agricultural University, Changsha, Hunan 410128, China

Abstract

Enterotoxigenic Escherichia coli (ETEC) causes diarrhea in travelers, young children and piglets, but the precise pathogenesis of ETEC induced diarrhea is not fully known. Recent investigations have shown that tight junction (TJ) proteins and aquaporin 3 (AQP 3) are contributing factors in bacterial diarrhea. In this study, using immunoblotting and immunohistochemistry analyses, we found that ETEC increases the protein abundance of TJ proteins (occludin, claudin-1, zonula occludens-1) in mice. Enterotoxigenic Escherichia coli induced the expression of TJ proteins in mice through pathways by involving myosin light chain kinase (MLCK)-myosin II regulatory light chain (MLC20) pathways; however, ETEC has little effect on the activation of the phosphatidylinositol 3-kinase (PI3K)-Akt pathway. Enterotoxigenic Escherichia coli infection has little effect on the protein abundance of AQP 3. Collectively, ETEC infection affects the abundance of intestinal TJ protein, which suggests the importance of TJ proteins in ETEC induced diarrhea.

Keywords

References

Allen, KP; Randolph, MM and Fleckenstein, JM (2006). Importance of heat-labile enterotoxin in colonization of the adult mouse small intestine by human enterotoxigenic Escherichia coli strains. Infect. Immun., 74: 869-875.
Barreau, F and Hugot, JP (2014). Intestinal barrier dysfunction triggered by invasive bacteria. Curr. Opin. Microbiol., 17: 91-98.
Berberov, EM; Zhou, Y; Francis, DH; Scott, MA; Kachman, SD and Moxley, RA (2004). Relative importance of heat-labile enterotoxin in the causation of severe diarrheal disease in the gnotobiotic piglet model by a strain of enterotoxigenic Escherichia coli that produces multiple enterotoxins. Infect. Immun., 72: 3914-3924.
Celli, J; Olivier, M and Finlay, BB (2001). Enteropathogenic Escherichia coli mediates antiphagocytosis through the inhibition of PI 3-kinase-dependent pathways. EMBO J., 20: 1245-1258.
Chen, X; Huan, H; Wan, T; Wang, L; Gao, S and Jiao, X (2014). Antigenic determinants analysis and detection of virulence factors in F18 fimbriae Escherichia coli strains isolated from pigs. Wei Sheng Wu Xue Bao. 54: 236-242.
Edelblum, KL and Turner, JR (2009). The tight junction in inflammatory disease: communication breakdown. Curr. Opin. Pharmacol., 9: 715-720.
Egberts, HJ; de Groot, EC; van Dijk, JE; Vellenga, L and Mouwen, JM (1993). Tight junctional structure and permeability of porcine jejunum after enterotoxic Escherichia coli infection. Res. Vet. Sci., 55: 10-14.
Gao, Y; Han, F; Huang, X; Rong, Y; Yi, H and Wang, Y (2013). Changes in gut microbial populations, intestinal morphology, expression of tight junction proteins, and cytokine production between two pig breeds after challenge with Escherichia coli K88: a comparative study. J. Anim. Sci., 91: 5614-5625.
Guignot, J; Chaplais, C; Coconnier-Polter, MH and Servin, AL (2007). The secreted autotransporter toxin, Sat, functions as a virulence factor in Afa/Dr diffusely adhering Escherichia coli by promoting lesions in tight junction of polarized epithelial cells. Cell Microbiol., 9: 204-221.
Guttman, JA; Li, Y; Wickham, ME; Deng, W; Vogl, AW and Finlay, BB (2006). Attaching and effacing pathogen-induced tight junction disruption in vivo. Cell Microbiol., 8: 634-645.
Guttman, JA; Samji, FN; Li, Y; Deng, W; Lin, A and Finlay, BB (2007). Aquaporins contribute to diarrhoea caused by attaching and effacing bacterial pathogens. Cell Microbiol., 9: 131-141.
Johnson, AM; Kaushik, RS and Hardwidge, PR (2010). Disruption of transepithelial resistance by enterotoxigenic Escherichia coli. Vet. Microbiol., 141: 115-119.
Kim, CY and Kim, KH (2014). Curcumin prevents leptin-induced tight junction dysfunction in intestinal Caco-2 BBe cells. J. Nutr. Biochem., 25: 26-35.
Kohler, H; Sakaguchi, T; Hurley, BP; Kase, BA; Reinecker, HC and McCormick, BA (2007). Salmonella enterica serovar Typhimurium regulates intercellular junction proteins and facilitates transepithelial neutrophil and bacterial passage. Am. J. Physiol. Gastrointest. Liver Physiol., 293: G178-187.
Li, N and Neu, J (2009). Glutamine deprivation alters intestinal tight junctions via a PI3-K/Akt mediated pathway in Caco-2 cells. J. Nutr., 139: 710-714.
Lin, N; Xu, LF and Sun, M (2013). The protective effect of trefoil factor 3 on the intestinal tight junction barrier is mediated by toll-like receptor 2 via a PI3K/Akt dependent mechanism. Biochem. Biophys. Res. Commun., 440: 143-149.
Martinez, JJ; Mulvey, MA; Schilling, JD; Pinkner, JS and Hultgren, SJ (2000). Type 1 pilus-mediated bacterial invasion of bladder epithelial cells. EMBO J., 19: 2803-2812.
Mecsas, J; Raupach, B and Falkow, S (1998). The Yersinia Yops inhibit invasion of Listeria, Shigella and Edwardsiella but not Salmonella into epithelial cells. Mol. Microbiol., 28: 1269-1281.
Muza-Moons, MM; Schneeberger, EE and Hecht, GA (2004). Enteropathogenic Escherichia coli infection leads to appearance of aberrant tight junctions strands in the lateral membrane of intestinal epithelial cells. Cell Microbiol., 6: 783-793.
Nataro, JP and Kaper, JB (1998). Diarrheagenic Escherichia coli. Clin. Microbiol. Rev., 11: 142-201.
Ren, W; Chen, S; Yin, J; Duan, J; Li, T; Liu, G; Feng, Z; Tan, B; Yin, Y and Wu, G (2014a). Dietary arginine supplementation of mice alters the microbial population and activates intestinal innate immunity. J. Nutr., 144: 988-995.
Ren, W; Wang, P; Yan, J; Liu, G; Zeng, B; Hussain, T; Peng, C; Yin, J; Tan, B; Li, T; Wei, H; Zhu, G; Reiter, RJ and Yin, Y (2017). Melatonin alleviates weanling stress in mice: involvement of intestinal microbiota. J. Pineal. Res., doi: 10.1111/jpi.12448. [Epub ahead of print].
Ren, W; Yin, J; Wu, M; Liu, G; Yang, G; Xion, Y; Su, D;
Wu, L; Li, T; Chen, S; Duan, J; Yin, Y and Wu, G (2014b). Serum amino acids profile and the beneficial effects of L-arginine or L-glutamine supplementation in dextran sulfate sodium colitis. PLoS One. 9: e88335.
Roselli, M; Finamore, A; Britti, MS; Konstantinov, SR; Smidt, H; de Vos, WM and Mengheri, E (2007). The novel porcine Lactobacillus sobrius strain protects intestinal cells from enterotoxigenic Escherichia coli K88 infection and prevents membrane barrier damage. J. Nutr., 137: 2709-2716.
Roselli, M; Finamore, A; Garaguso, I; Britti, MS and Mengheri, E (2003). Zinc oxide protects cultured enterocytes from the damage induced by Escherichia coli. J. Nutr., 133: 4077-4082.
Rowe, B; Taylor, J and Bettelheim, KA (1970). An investigation of traveller’s diarrhoea. Lancet. 1(7636): 1-5.
Sears, CL and Kaper, JB (1996). Enteric bacterial toxins: mechanisms of action and linkage to intestinal secretion. Microbiol. Rev., 60: 167-215.
Shen, L; Weber, CR; Raleigh, DR; Yu, D and Turner, JR (2011). Tight junction pore and leak pathways: a dynamic duo. Annu. Rev. Physiol., 73: 283-309.
Suzuki, T (2013). Regulation of intestinal epithelial permeability by tight junctions. Cell Mol. Life Sci., 70: 631-659.
Tang, Y; Li, F; Tan, B; Liu, G; Kong, X; Hardwidge, PR and Yin, Y (2014). Enterotoxigenic Escherichia coli infection induces intestinal epithelial cell autophagy. Vet. Microbiol., 171: 160-164.
Umeda, K; Ikenouchi, J; Katahira-Tayama, S; Furuse, K; Sasaki, H; Nakayama, M; Matsui, T; Tsukita, S; Furuse, M and Tsukita, S (2006). ZO-1 and ZO-2 independently determine where claudins are polymerized in tight-junction strand formation. Cell. 126: 741-754.
Uzzau, S and Fasano, A (2000). Cross-talk between enteric pathogens and the intestine. Cell Microbiol., 2: 83-89.
Van Itallie, CM; Holmes, J; Bridges, A; Gookin, JL; Coccaro, MR; Proctor, W; Colegio, OR and Anderson, JM (2008). The density of small tight junction pores varies among cell types and is increased by expression of claudin-2. J. Cell Sci., 121: 298-305.
Wang, G; Gao, F; Zhang, W; Chen, J; Wang, T; Zhang, G and Shen, L (2012). Involvement of aquaporin 3 in Helicobacter pylori-related gastric diseases. PLoS ONE. 7: e49104.
Yang, KM; Jiang, ZY; Zheng, CT; Wang, L and Yang, XF (2014). Effect of Lactobacillus plantarum on diarrhea and intestinal barrier function of young piglets challenged with enterotoxigenic Escherichia coli K88. J. Anim. Sci., 92: 1496-1503.
Yu, Q; Wang, Z and Yang, Q (2012). Lactobacillus amylophilus D14 protects tight junction from enteropathogenic bacteria damage in Caco-2 cells. J. Dairy Sci., 95: 5580-5587.

Files

Share

How to cite

Statistics