Effects of Ex Vivo Infection with ETEC on Jejunal Barrier Properties and Cytokine Expression in Probiotic-Supplemented Pigs

Digestive Diseases and Sciences

Volumn 62, Issue 4, 2017, Pages 922-933

  Lodemann, Ulrike ^a   Amasheh, Salah ^a   Radloff, Judith ^a   Kern, Martina ^a   Bethe, Astrid ^a   Wieler, Lothar H ^a,b   Pieper, Robert ^a   Zentek, Jürgen ^a   Aschenbach, Jörg R ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b ROBERT KOCH INSTITUTE   (Germany)

Author keywords

Cytokine; Enterotoxigenic Escherichia coli; Intestine; Pig; Probiotic; Tight junction

Indexed keywords

CLAUDIN 1; CLAUDIN 2; CLAUDIN 3; CLAUDIN 4; CLAUDIN 7; FLUORESCEIN; GLUCOSE; INTERLEUKIN 8; MESSENGER RNA; PROBIOTIC AGENT; PROSTAGLANDIN E2; TIGHT JUNCTION PROTEIN; TUMOR NECROSIS FACTOR; CYTOKINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; CYTOKINE RELEASE; DIET SUPPLEMENTATION; ENTEROTOXIGENIC ESCHERICHIA COLI; ESCHERICHIA COLI INFECTION; EX VIVO STUDY; INTESTINE MUCOSA; JEJUNUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SHORT CIRCUIT CURRENT; SMALL INTESTINE EPITHELIUM; TRANSEPITHELIAL RESISTANCE; ANIMAL; ANIMAL FOOD; BIOSYNTHESIS; DIET THERAPY; DRUG EFFECTS; ESCHERICHIA COLI INFECTIONS; FEMALE; GENE EXPRESSION; GENETICS; MALE; METABOLISM; MICROBIOLOGY; PIG; PREGNANCY; RANDOMIZATION;

ANIMAL FEED; ANIMALS; CYTOKINES; ENTEROTOXIGENIC ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; FEMALE; GENE EXPRESSION; INTESTINAL MUCOSA; JEJUNUM; MALE; PREGNANCY; PROBIOTICS; RANDOM ALLOCATION; SWINE;

EID: 85006489022     PISSN: 01632116     EISSN: 15732568     Source Type: Journal    
DOI: 10.1007/s10620-016-4413-x     Document Type: Article

References (58)

1. Lanata CF, Fischer-Walker CL, Olascoaga AC, Torres CX, Aryee MJ, Black RE. Global causes of diarrheal disease mortality in children <5 years of age: a systematic review. PLoS One. 2013;8:e72788.
2. Goswami PS, Friendship RM, Gyles CL, Poppe C, Boerlin P. Preliminary investigations of the distribution of Escherichia coli O149 in sows, piglets, and their environment. Can J Vet Res. 2011;75:57–60.
3. Miller BG, Newby TJ, Stokes CR, Bourne FJ. Influence of diet on postweaning malabsorption and diarrhoea in the pig. Res Vet Sci. 1984;36:187–193.
4. Read LT, Hahn RW, Thompson CC, Bauer DL, Norton EB, Clements JD. Simultaneous exposure to Escherichia coli heat-labile and heat-stable enterotoxins increases fluid secretion and alters cyclic nucleotide and cytokine production by intestinal epithelial cells. Infect Immun. 2014;82:5308–5316.
5. Madec F, Bridoux N, Bounaix S, et al. Experimental models of porcine post-weaning colibacillosis and their relationship to post-weaning diarrhoea and digestive disorders as encountered in the field. Vet Microbiol. 2000;72:295–310.
6. Wieler LH, Ilieff A, Herbst W, et al. Prevalence of enteropathogens in suckling and weaned piglets with diarrhoea in southern Germany. J Vet Med B Infect Dis Vet Public Health. 2001;48:151–159.
7. Shimizu M, Terashima T. Appearance of enterotoxigenic Escherichia coli in piglets with diarrhea in connection with feed changes. Microbiol Immunol. 1982;26:467–477.
8. Tzipori S, Chandler D, Smith M, Makin T, Hennessy D. Factors contributing to postweaning diarrhoea in a large intensive piggery. Aust Vet J. 1980;56:274–278.
9. Pineiro M, Stanton C. Probiotic bacteria: legislative framework—requirements to evidence basis. J Nutr. 2007;137:850S–853S.
10. Kiarie E, Bhandari S, Scott M, Krause DO, Nyachoti CM. Growth performance and gastrointestinal microbial ecology responses of piglets receiving Saccharomyces cerevisiae fermentation products after an oral challenge with Escherichia coli (K88). J Anim Sci. 2011;89:1062–1078.
11. Li XQ, Zhu YH, Zhang HF, et al. Risks associated with high-dose Lactobacillus rhamnosus in an Escherichia coli model of piglet diarrhoea: intestinal microbiota and immune imbalances. PLoS One. 2012;7:e40666.
12. Yang KM, Jiang ZY, Zheng CT, Wang L, Yang XF. Effect of Lactobacillus plantarum on diarrhea and intestinal barrier function of young piglets challenged with enterotoxigenic Escherichia coli K88. J Anim Sci. 2014;92:1496–1503.
13. Schroeder B, Duncker S, Barth S, et al. Preventive effects of the probiotic Escherichia coli strain Nissle 1917 on acute secretory diarrhea in a pig model of intestinal infection. Dig Dis Sci. 2006;51:724–731. doi:10.1007/s10620-006-3198-8
14. Roselli M, Finamore A, Britti MS, et al. The novel porcine Lactobacillus sobrius strain protects intestinal cells from enterotoxigenic Escherichia coli K88 infection and prevents membrane barrier damage. J Nutr. 2007;137:2709–2716.
15. Buydens P, Debeuckelaere S. Efficacy of SF 68 in the treatment of acute diarrhea. A placebo-controlled trial. Scand J Gastroenterol. 1996;31:887–891.
16. Wunderlich PF, Braun L, Fumagalli I, et al. Double-blind report on the efficacy of lactic acid-producing Enterococcus SF68 in the prevention of antibiotic-associated diarrhoea and in the treatment of acute diarrhoea. J Int Med Res. 1989;17:333–338.
17. Scharek L, Guth J, Reiter K, et al. Influence of a probiotic Enterococcus faecium strain on development of the immune system of sows and piglets. Vet Immunol Immunopathol. 2005;105:151–161.
18. Taras D, Vahjen W, Macha M, Simon O. Performance, diarrhea incidence, and occurrence of Escherichia coli virulence genes during long-term administration of a probiotic Enterococcus faecium strain to sows and piglets. J Anim Sci. 2006;84:608–617.
19. Zeyner A, Boldt E. Effects of a probiotic Enterococcus faecium strain supplemented from birth to weaning on diarrhoea patterns and performance of piglets. J Anim Physiol Anim Nutr (Berl). 2006;90:25–31.
20. Martens H, Gabel G, Strozyk H. The effect of potassium and the transmural potential difference on magnesium transport across an isolated preparation of sheep rumen epithelium. Q J Exp Physiol. 1987;72:181–188.
21. Klingspor S, Martens H, Caushi D, Twardziok S, Aschenbach JR, Lodemann U. Characterization of the effects of Enterococcus faecium on intestinal epithelial transport properties in piglets. J Anim Sci. 2013;91:1707–1718.
22. Klingspor S, Bondzio A, Martens H, et al. Enterococcus faecium NCIMB 10415 modulates epithelial integrity, heat shock protein, and proinflammatory cytokine response in intestinal cells. Mediators Inflamm. 2015;2015:304149.
23. Lalles JP, Bosi P, Smidt H, Stokes CR. Weaning—a challenge to gut physiologists. Livest Sci. 2007;108:82–93.
24. Rezzola S, Belleri M, Gariano G, et al. In vitro and ex vivo retina angiogenesis assays. Angiogenesis. 2014;17:429–442.
25. Schuller S, Chong Y, Lewin J, Kenny B, Frankel G, Phillips AD. Tir phosphorylation and Nck/N-WASP recruitment by enteropathogenic and enterohaemorrhagic Escherichia coli during ex vivo colonization of human intestinal mucosa is different to cell culture models. Cell Microbiol. 2007;9:1352–1364.
26. Gao Y, Han F, Huang X, Rong Y, Yi H, Wang Y. 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. 2013;91:5614–5625.
27. Egberts HJ, de Groot EC, van Dijk JE, Vellenga L, Mouwen JM. Tight junctional structure and permeability of porcine jejunum after enterotoxic Escherichia coli infection. Res Vet Sci. 1993;55:10–14.
28. McLamb BL, Gibson AJ, Overman EL, Stahl C, Moeser AJ. Early weaning stress in pigs impairs innate mucosal immune responses to enterotoxigenic E. coli challenge and exacerbates intestinal injury and clinical disease. PLoS One. 2013;8:e59838.
29. Awad WA, Hess C, Khayal B, Aschenbach JR, Hess M. In vitro exposure to Escherichia coli decreases ion conductance in the jejunal epithelium of broiler chickens. PLoS One. 2014;9:e92156.
30. Tanimoto Y, Arikawa K, Nishikawa Y. Effect of diffusely adherent Escherichia coli strains isolated from diarrhoeal patients and healthy carriers on IL-8 secretion and tight junction barrier integrity of Caco-2 cells. Vet Immunol Immunopathol. 2013;152:183–188.
31. Awad WA, Aschenbach JR, Khayal B, Hess C, Hess M. Intestinal epithelial responses to Salmonella enterica serovar Enteritidis: effects on intestinal permeability and ion transport. Poult Sci. 2012;91:2949–2957.
32. Krug SM, Schulzke JD, Fromm M. Tight junction, selective permeability, and related diseases. Semin Cell Dev Biol. 2014;36:166–176.
33. Rahner C, Mitic LL, Anderson JM. Heterogeneity in expression and subcellular localization of claudins 2, 3, 4, and 5 in the rat liver, pancreas, and gut. Gastroenterology. 2001;120:411–422.
34. Pasternak JA, Kent-Dennis C, Van Kessel AG, Wilson HL. Claudin-4 undergoes age-dependent change in cellular localization on pig jejunal villous epithelial cells, independent of bacterial colonization. Mediators Inflamm. 2015;2015:263629.
35. Markov AG, Aschenbach JR, Amasheh S. Claudin clusters as determinants of epithelial barrier function. IUBMB Life. 2015;67:29–35.
36. Van Itallie CM, Fanning AS, Anderson JM. Reversal of charge selectivity in cation or anion-selective epithelial lines by expression of different claudins. Am J Physiol Renal Physiol. 2003;285:F1078–F1084.
37. Mitic LL, Unger VM, Anderson JM. Expression, solubilization, and biochemical characterization of the tight junction transmembrane protein claudin-4. Protein Sci. 2003;12:218–227.
38. Goswami P, Das P, Verma AK, et al. Are alterations of tight junctions at molecular and ultrastructural level different in duodenal biopsies of patients with celiac disease and Crohn’s disease? Virchows Arch. 2014;465:521–530.
39. Das P, Goswami P, Das TK, et al. Comparative tight junction protein expressions in colonic Crohn’s disease, ulcerative colitis, and tuberculosis: a new perspective. Virchows Arch. 2012;460:261–270.
40. Hering NA, Richter JF, Krug SM, et al. Yersinia enterocolitica induces epithelial barrier dysfunction through regional tight junction changes in colonic HT-29/B6 cell monolayers. Lab Invest. 2011;91:310–324.
41. Troeger H, Loddenkemper C, Schneider T, et al. Structural and functional changes of the duodenum in human norovirus infection. Gut. 2009;58:1070–1077.
42. Bruewer M, Luegering A, Kucharzik T, et al. Proinflammatory cytokines disrupt epithelial barrier function by apoptosis-independent mechanisms. J Immunol. 2003;171:6164–6172.
43. Hamada K, Kakigawa N, Sekine S, Shitara Y, Horie T. Disruption of ZO-1/claudin-4 interaction in relation to inflammatory responses in methotrexate-induced intestinal mucositis. Cancer Chemother Pharmacol. 2013;72:757–765.
44. Wells JM, Rossi O, Meijerink M, van Baarlen P. Epithelial crosstalk at the microbiota-mucosal interface. Proc Natl Acad Sci USA. 2011;108:4607–4614.
45. Shaw MH, Reimer T, Kim YG, Nunez G. NOD-like receptors (NLRs): bona fide intracellular microbial sensors. Curr Opin Immunol. 2008;20:377–382.
46. Robertson SJ, Girardin SE. Nod-like receptors in intestinal host defense: controlling pathogens, the microbiota, or both? Curr Opin Gastroenterol. 2013;29:15–22.
47. Strowig T, Henao-Mejia J, Elinav E, Flavell R. Inflammasomes in health and disease. Nature. 2012;481:278–286.
48. Vladimer GI, Marty-Roix R, Ghosh S, Weng D, Lien E. Inflammasomes and host defenses against bacterial infections. Curr Opin Microbiol. 2013;16:23–31.
49. Finamore A, Roselli M, Imbinto A, Seeboth J, Oswald IP, Mengheri E. Lactobacillus amylovorus inhibits the TLR4 inflammatory signaling triggered by enterotoxigenic Escherichia coli via modulation of the negative regulators and involvement of TLR2 in intestinal Caco-2 cells and pig explants. PLoS One. 2014;9:e94891.
50. Zanello G, Berri M, Dupont J, et al. Saccharomyces cerevisiae modulates immune gene expressions and inhibits ETEC-mediated ERK1/2 and p38 signaling pathways in intestinal epithelial cells. PLoS One. 2011;6:e18573.
51. Bruins MJ, Cermak R, Kiers JL, van der Meulen J, van Amelsvoort JM, van Klinken BJ. In vivo and in vitro effects of tea extracts on enterotoxigenic Escherichia coli-induced intestinal fluid loss in animal models. J Pediatr Gastroenterol Nutr. 2006;43:459–469.
52. Hediger MA, Kanai Y, You G, Nussberger S. Mammalian ion-coupled solute transporters. J Physiol. 1995;482:7S–17S.
53. Grondahl ML, Thorboll JE, Hansen MB, Skadhauge E. Regional differences in the effect of cholera toxin and enterotoxigenic Escherichia coli infection on electrolyte and fluid transport in the porcine small intestine. Zentralbl Veterinarmed A. 1998;45:369–381.
54. Hayden UL, Greenberg RN, Carey HV. Role of prostaglandins and enteric nerves in Escherichia coli heat-stable enterotoxin (STa)-induced intestinal secretion in pigs. Am J Vet Res. 1996;57:211–215.
55. Conour JE, Ganessunker D, Tappenden KA, Donovan SM, Gaskins HR. Acidomucin goblet cell expansion induced by parenteral nutrition in the small intestine of piglets. Am J Physiol Gastrointest Liver Physiol. 2002;283:G1185–G1196.
56. Bi J, Song S, Fang L, et al. Porcine reproductive and respiratory syndrome virus induces IL-1beta production depending on TLR4/MyD88 pathway and NLRP3 inflammasome in primary porcine alveolar macrophages. Mediators Inflamm. 2014;2014:403515.
57. Ramsay TG, Caperna TJ. Ontogeny of adipokine expression in neonatal pig adipose tissue. Comp Biochem Physiol B Biochem Mol Biol. 2009;152:72–78.
58. Amoozadeh Y, Dan Q, Xiao J, Waheed F, Szaszi K. Tumor necrosis factor-alpha induces a biphasic change in claudin-2 expression in tubular epithelial cells: role in barrier functions. Am J Physiol Cell Physiol. 2015;309:C38–C50.