Diets high in fermentable protein and fibre alter tight junction protein composition with minor effects on barrier function in piglet colon

British Journal of Nutrition

Volumn 111, Issue 6, 2014, Pages 1040-1049

  Richter, Jan F ^a,b   Pieper, Robert ^c   Zakrzewski, Silke S ^b   Günzel, Dorothee ^b   Schulzke, Joerg D ^b   Van Kessel, Andrew G ^d  

^a FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c FREIE UNIVERSITÄT BERLIN   (Germany)

^d UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

Epithelial barrier; Fermentable fibre; Fermentable protein; Macromolecule passage; Tight junctions

Indexed keywords

CLAUDIN 1; CLAUDIN 2; CLAUDIN 3; CLAUDIN 4; HORSERADISH PEROXIDASE; OCCLUDIN; SODIUM CHANNEL; TIGHT JUNCTION PROTEIN; TRICELLULIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOTINYLATION; COLON MUCOSA; CONTROLLED STUDY; DIETARY FIBER; ELECTROCHEMICAL IMPEDANCE SPECTROSCOPY; MOLECULAR WEIGHT; NONHUMAN; OXIDATIVE STRESS; PERMEABILITY BARRIER; PIGLET; PROTEIN ANALYSIS; PROTEIN CONTENT; PROTEIN DIET; PROTEIN EXPRESSION; SODIUM TRANSPORT; ANIMAL; ANIMAL DISEASE; CHEMISTRY; COLON; DIET; FEMALE; FERMENTATION; INTESTINE ABSORPTION; INTESTINE MUCOSA; MALE; PHYSIOLOGY; PROTEIN INTAKE; SWINE;

ARMORACIA RUSTICANA;

ANIMALS; COLON; DIET; DIETARY FIBER; DIETARY PROTEINS; FEMALE; FERMENTATION; INTESTINAL ABSORPTION; INTESTINAL MUCOSA; MALE; SUS SCROFA; TIGHT JUNCTION PROTEINS;

EID: 84899671209     PISSN: 00071145     EISSN: 14752662     Source Type: Journal    
DOI: 10.1017/S0007114513003498     Document Type: Article

References (52)

1. De Preter V, Hamer HM, Windey K, et al. (2011) The impact of pre- and/or probiotics on human colonic metabolism: does it affect human health? Mol Nutr Food Res 55, 46-57.
2. Heo JM, Opapeju FO, Pluske JR, et al. (2013) Gastrointestinal health and function in weaned pigs: a review of feeding strategies to control post-weaning diarrhoea without using in-feed antimicrobial compounds. J Anim Physiol Anim Nutr (Berl) 97, 207-237.
3. Kau AL, Ahern PP, Griffin NW, et al. (2011) Human nutrition, the gut microbiome and the immune system. Nature 474, 327-336.
4. Blaut M & Clavel T (2007) Metabolic diversity of the intestinal microbiota: implications for health and disease. J Nutr 137, 751-755.
5. Lupton JR (2004) Microbial degradation products influence colon cancer risk: the butyrate controversy. J Nutr 134, 479-482.
6. Ball RO & Aherne FX (1987) Influence of dietary nutrient density, level of feed intake and weaning age on young pigs. II. Apparent nutrient digestibility and incidence and severity of diarrhea. Can J Anim Sci 67, 1105-1115.
7. Macfarlane S & Macfarlane GT (2006) Composition and metabolic activities of bacterial biofilms colonizing food residues in the human gut. Appl Environ Microbiol 72, 6204-6211.
8. Russell WR, Gratz SW, Duncan SH, et al. (2011) High-protein, reduced-carbohydrate weight-loss diets promote metabolite profiles likely to be detrimental to colonic health. Am J Clin Nutr 93, 1062-1072.
9. McGarr SE, Ridlon JM & Hylemon PB (2005) Diet, anaerobic bacterial metabolism, and colon cancer - a review of the literature. J Clin Gastroenterol 39, 98-109.
10. Maslowski KM, Vieira AT, Ng A, et al. (2009) Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 29, 1282-1286.
11. Bordin M, D'Atri F, Guillemot L, et al. (2004) Histone deacetylase inhibitors up-regulate the expression of tight junction proteins. Mol Cancer Res 2, 692-701.
12. +channels. Biochem Biophys Res Commun 382, 280-285.
13. Zeissig S, Fromm A, Mankertz J, et al. (2007) Butyrate induces intestinal sodium absorption via Sp3-mediated transcriptional up-regulation of epithelial sodium channels. Gastroenterology 132, 236-248.
14. + absorption defends from paracellular back-leakage by claudin-8 upregulation. Biochem Biophys Res Commun 378, 45-50.
15. Capaldo CT & Nusrat A (2009) Cytokine regulation of tight junctions. Biochim Biophys Acta 1788, 864-871.
16. Turner JR (2009) Intestinal mucosal barrier function in health and disease. Nat Rev Immunol 9, 799-809.
17. Weber CR, Nalle SC, Tretiakova M, et al. (2008) Claudin-1 and claudin-2 expression is elevated in inflammatory bowel disease and may contribute to early neoplastic transformation. Lab Invest 88, 1110-1120.
18. Prasad S, Mingrino R, Kaukinen K, et al. (2005) Inflammatory processes have differential effects on claudins 2, 3 and 4 in colonic epithelial cells. Lab Invest 85, 1139-1162.
19. Elkouby-Naor L & Ben-Yosef T (2010) Functions of claudin tight junction proteins and their complex interactions in various physiological systems. Int Rev Cell Mol Biol 279, 1-32.
20. Hermes RG, Molist F, Ywazaki M, et al. (2009) Effect of dietary level of protein and fiber on the productive performance and health status of piglets. J Anim Sci 87, 3569-3577.
21. Htoo JK, Araiza BA, Sauer WC, et al. (2007) Effect of dietary protein content on ileal amino acid digestibility, growth performance, and formation of microbial metabolites in ileal and cecal digesta of early-weaned pigs. J Anim Sci 85, 3303-3312.
22. Jeaurond EA, Rademacher M, Pluske JR, et al. (2008) Impact of feeding fermentable proteins and carbohydrates on growth performance, gut health and gastrointestinal function of newly weaned pigs. Can J Anim Sci 88, 271-281.
23. Bikker P, Dirkzwager A, Fledderus J, et al. (2006) The effect of dietary protein and fermentable carbohydrates levels on growth performance and intestinal characteristics in newly weaned piglets. J Anim Sci 84, 3337-3345.
24. Pieper R, Bindelle J, Rossnagel B, et al. (2009) Effect of carbohydrate composition in barley and oat cultivars on microbial ecophysiology and the proliferation of Salmonella enterica in an in vitro model of the porcine gastrointestinal tract. Appl Environ Microbiol 75, 7000-7016.
25. Metzler-Zebeli BU, Hooda S, Pieper R, et al. (2010) Nonstarch polysaccharides modulate bacterial microbiota, pathways for butyrate production, and abundance of pathogenic Escherichia coli in the pig gastrointestinal tract. Appl Environ Microbiol 76, 3692-3701.
26. Heo JM, Kim JC, Hansen CF, et al. (2009) Feeding a diet with decreased protein content reduces indices of protein fermentation and the incidence of postweaning diarrhea in weaned pigs challenged with an enterotoxigenic strain of Escherichia coli. J Anim Sci 87, 2833-2843.
27. Pieper R, Kröger S, Richter JF, et al. (2012) Fermentable fiber ameliorates fermentable protein-induced changes in microbial ecology, but not the mucosal response, in the colon of piglets. J Nutr 142, 661-667.
28. th revised ed. Washington, DC: National Academy Press.
29. -secretion in epithelial monolayers of mucus-forming human colon cells. Am J Physiol 261, 574-582.
30. Günzel D, Zakrzewski SS, Schmid T, et al. (2012) From TER to trans- and paracellular resistance: lessons from impedance spectroscopy. Ann N Y Acad Sci 1257, 142-151.
31. Barmeyer C, Amasheh S, Tavalali S, et al. (2004) IL-1beta and TNFalpha regulate sodium absorption in rat distal colon. Biochem Biophys Res Commun 317, 500-507.
32. Günzel D, Stuiver M, Kausalya PJ, et al. (2009) Claudin-10 exists in six alternatively spliced isoforms that exhibit distinct localization and function. J Cell Sci 122, 1507-1151.
33. Rasband WS (1997-2013) Image J. Bethesda, MD: US National Institutes of Health. http://imagej.nih.gov/ij/(accessed January 2011).
34. Krug SM, Amasheh S, Richter JF, et al. (2009) Tricellulin forms a barrier to macromolecules intricellular tight junctions without affecting ion permeability. Mol Biol Cell 20, 3713-3724.
35. von Bonsdorff CH, Fuller SD & Simons K (1985) Apical and basolateral endocytosis in Madin-Darby canine kidney (MDCK) cells grown on nitrocellulose filters. EMBO J 4, 2781-2792.
36. Heyman M, Ducroc R, Desjeux JF, et al. (1982) Horseradish peroxidase transport across adult rabbit jejunum in vitro. Am J Physiol 242, G558-G564.
37. Amasheh S, Meiri N, Gitter AH, et al. (2002) Claudin-2 expression induces cation-selective channels in tight junctions of epithelial cells. J Cell Sci 115, 4969-4976.
38. Yu AS, Enck AH, Lencer WI, et al. (2003) Claudin-8 expression in Madin-Darby canine kidney cells augments the paracellular barrier to cation permeation. J Biol Chem 278, 17350-17359.
39. Barmeyer C, Harren M, Schmitz H, et al. (2004) Mechanisms of diarrhea in the interleukin-2-deficient mouse model of colonic inflammation. Am J Physiol Gastrointest Liver Physiol 286, 244-252.
40. Schumann M, Winter S, Wichner K, et al. (2012) CCR7 deficiency causes diarrhea associated with altered ion transport in colonocytes in the absence of overt colitis. Mucosal Immunol 5, 377-387.
41. Bergann T, Zeissig S, Fromm A, et al. (2009) Glucocorticoids and tumor necrosis factor-alpha synergize to induce absorption by the epithelial sodium channel in the colon. Gastroenterology 136, 933-942.
42. Günzel D & Fromm M (2012) Claudins and other tight junction proteins. Compr Physiol 2, 1819-1852.
43. Shen L, Weber CR, Raleigh DR, et al. (2011) Tight junction pore and leak pathways: a dynamic duo. Annu Rev Physiol 73, 283-309.
44. Plöger S, Stumpff F, Penner GB, et al. (2012) Microbial butyrate and its role for barrier function in the gastrointestinal tract. Ann N Y Acad Sci 1258, 52-59.
45. Schmitz H, Fromm M, Bentzel CJ, et al. (1999) Tumor necrosis factor-alpha (TNFalpha) regulates the epithelial barrier in the human intestinal cell line HT-29/B6. J Cell Sci 112, 137-146.
46. Turksen K & Troy TC (2011) Junctions gone bad: claudins and loss of the barrier in cancer. Biochim Biophys Acta 1816, 73-79.
47. Feldman GJ, Mullin JM & Ryan MP (2005) Occludin: structure, function and regulation. Adv Drug Deliv Rev 57, 883-917.
48. Cummins PM (2012) Occludin: one protein, many forms. Mol Cell Biol 32, 242-250.
49. Blasig IE, Bellmann C, Cording J, et al. (2011) Occludin protein family: oxidative stress and reducing conditions. Antioxid Redox Signal 15, 1195-1219.
50. Raleigh DR, Boe DM, Yu D, et al. (2011) Occludin S408 phosphorylation regulates tight junction protein interactions and barrier function. J Cell Biol 193, 565-582.
51. Bojarski C, Weiske J, Schöneberg T, et al. (2004) The specific fates of tight junction proteins in apoptotic epithelial cells. J Cell Sci 117, 2097-2107.
52. Nieto MA (2011) The ins and outs of the epithelial to mesenchymal transition in health and disease. Annu Rev Cell Dev Biol 27, 347-376.