A high-grain diet causes massive disruption of ruminal epithelial tight junctions in goats

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 305, Issue 3, 2013, Pages

  Liu, Jun Hua ^a   Xu, Ting Ting ^a   Liu, Yu Jie ^a   Zhu, Wei Yun ^a   Mao, Sheng Yong ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

Author keywords

High grain diet; Inflammation; Lipopolysaccharide; Rumen epithelium; Tight junction protein

Indexed keywords

CLAUDIN 4; GAMMA INTERFERON; LIPOPOLYSACCHARIDE; MESSENGER RNA; OCCLUDIN; PROTEIN ZO1; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DIETARY INTAKE; GOAT; GRAIN; IMMUNOFLUORESCENCE; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REAL TIME POLYMERASE CHAIN REACTION; RNA ANALYSIS; RUMINANT STOMACH; SCANNING ELECTRON MICROSCOPY; STOMACH EPITHELIUM; TIGHT JUNCTION; TISSUE DISTRIBUTION; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING;

HIGH-GRAIN DIET; INFLAMMATION; LIPOPOLYSACCHARIDE; RUMEN EPITHELIUM; TIGHT JUNCTION PROTEIN;

ANIMALS; BLOTTING, WESTERN; BODY FLUIDS; CEREALS; CLAUDINS; CYTOKINES; DIET; DNA PRIMERS; DNA, COMPLEMENTARY; EPITHELIUM; FLUORESCENT ANTIBODY TECHNIQUE; GOATS; HOMEOSTASIS; HYDROGEN-ION CONCENTRATION; LIPOPOLYSACCHARIDES; MALE; OCCLUDIN; REAL-TIME POLYMERASE CHAIN REACTION; RNA; RUMEN; TIGHT JUNCTIONS; ZONULA OCCLUDENS-1 PROTEIN;

EID: 84881013813     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00068.2013     Document Type: Article

References (42)

1. Al-Sadi R Khatib K Guo S Ye D Youssef M Ma T. Occludin regulates macromolecule flux across the intestinal epithelial tight junction barrier. Am J Physiol Gastrointest Liver Physiol 300: G1054-G1064 2011.
2. Aschenbach JR Penner GB Stumpff F Gabel G. Ruminant Nutrition Symposium: Role of fermentation acid absorption in the regulation of ruminal pH. J Anim Sci 89: 1092-1107 2011.
3. Chen X Oshima T Shan J Fukui H Watari J Miwa H. Bile salts disrupt human esophageal squamous epithelial barrier function by modulating tight junction proteins. Am J Physiol Gastrointest Liver Physiol 303: G199-G208 2012.
4. Chen X Oshima T Tomita T Fukui H Watari J Matsumoto T Miwa H. Acidic bile salts modulate the squamous epithelial barrier function by modulating tight junction proteins. Am J Physiol Gastrointest Liver Physiol 301: G203-G209 2011.
5. Chin AC Flynn AN Fedwick JP Buret AG. The role of caspase-3 in lipopolysaccharide-mediated disruption of intestinal epithelial tight junctions. Can J Physiol Pharmacol 84: 1043-1050 2006.
6. Chomczynski P Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162: 156-159 1987.
7. Emmanuel DGV Madsen KL Churchill TA Dunn SM Ametaj BN. Acidosis and lipopolysaccharide from Escherichia coli B: 055 cause hyperpermeability of rumen and colon tissues. J. Dairy Sci. 90: 5552-5557 2007.
8. Fanning AS Anderson JM. PDZ domains and the formation of protein networks at the plasma membrane. Curr Top Microbiol 228: 209-233 1998.
9. Gaebel G Bell M Martens H. The effect of low mucosal Ph on sodium and chloride movement across the isolated rumen mucosa of sheep. Q J Exp Physiol 74: 35-44 1989.
10. Gassler N Rohr C Schneider A Kartenbeck J Bach A Overmuller N Otto HF Autschbach F. Inflammatory bowel disease is associated with changes of enterocytic junctions. Am J Physiol Gastrointest Liver Physiol 281: G216-G228 2001.
11. Gonzalez-Mariscal L Tapia R Chamorro D. Crosstalk of tight junction components with signaling pathways. Biochim Biophys Acta 1778: 729-756 2008.
12. Graham C Simmons NL. Functional organization of the bovine rumen epithelium. Am J Physiol Regul Integr Comp Physiol 288: R173-R181 2005.
13. Han XN Fink MP Yang RK Delude RL. Increased iNOS activity is essential for intestinal epithelial tight junction dysfunction in endotoxemic mice. Shock 21: 261-270 2004.
14. Heiskala M Peterson PA Yang Y. The roles of claudin superfamily proteins in paracellular transport. Traffic 2: 93-98 2001.
15. Heller F Florian P Bojarski C Richter J Christ M Hillenbrand B Mankertz J Gitter AH Burgel N Fromm M Zeitz M Fuss I Strober W Schulzke JD. Interleukin-13 is the key effector Th2 cytokine in ulcerative colitis that affects epithelial tight junctions apoptosis and cell restitution. Gastroenterology 129: 550-564 2005.
16. John LJ Fromm M Schulzke JD. Epithelial barriers in intestinal inflammation. Antioxid Redox Signal 15: 1255-1270 2011.
17. Khafipour E Krause DO Plaizier JC. Alfalfa pellet-induced subacute ruminal acidosis in dairy cows increases bacterial endotoxin in the rumen without causing inflammation. J Dairy Sci 92: 1712-1724 2009.
18. Khafipour E Krause DO Plaizier JC. A grain-based subacute ruminal acidosis challenge causes translocation of lipopolysaccharide and triggers inflammation. J Dairy Sci 92: 1060-1070 2009.
19. Klevenhusen F Hollmann M Podstatzky-Lichtenstein L Krametter-Frotscher R Aschenbach JR Zebeli Q. Feeding barley grain-rich diets altered electrophysiological properties and permeability of the ruminal wall in a goat model. J Dairy Sci 96: 2293-302 2013.
20. Lodemann U Martens H. Effects of diet and osmotic pressure on Na transport and tissue conductance of sheep isolated rumen epithelium. Exp Physiol 91: 539-550 2006.
21. Ma TY Iwamoto GK Hoa NT Akotia V Pedram A Boivin MA Said HM. TNF-induced increase in intestinal epithelial tight junction permeability requires NFB activation. Am J Physiol Gastrointest Liver Physiol 286: G367-G376 2004.
22. Mazzon E Cuzzocrea S. Role of TNFin ileum tight junction alteration in mouse model of restraint stress. Am J Physiol Gastrointest Liver Physiol 294: G1268-G1280 2008.
23. Nagaraja TG Chengappa MM. Liver abscesses in feedlot cattle: A review. J. Anim. Sci. 76: 287-298 1998.
24. Odongo NE AlZahal O Lindinger MI Duffield TF Valdes EV Terrell SP McBride BW. Effects of mild heat stress and grain challenge on acid-base balance and rumen tissue histology in lambs. J. Anim. Sci. 84: 447-455 2006.
25. Oshima T Koseki J Chen X Matsumoto T Miwa H. Acid modulates the squamous epithelial barrier function by modulating the localization of claudins in the superficial layers. Lab Invest 92: 22-31 2012.
26. Penner GB Oba M Gabel G Aschenbach JR. A single mild episode of subacute ruminal acidosis does not affect ruminal barrier function in the short term. J Dairy Sci 93: 4838-4845 2010.
27. Penner GB Steele MA Aschenbach JR McBride BW. Ruminant Nutrition Symposium: Molecular adaptation of ruminal epithelia to highly fermentable diets. J Anim Sci 89: 1108-1119 2011.
28. Plaizier JC Khafipour E Li S Gozho GN Krause DO. Subacute ruminal acidosis (SARA) endotoxins and health consequences. Anim Feed Sci Tech 172: 9-21 2012.
29. Plaizier JC Krause DO Gozho GN McBride BW. Subacute ruminal acidosis in dairy cows: the physiological causes incidence and consequences. Vet J 176: 21-31 2008.
30. Poritz LS Harris LR 3rd Kelly AA Koltun WA. Increase in the tight junction protein claudin-1 in intestinal inflammation. Dig Dis Sci 56: 2802-2809 2011.
31. Qin WL. Determination of rumen volatile fatty acids by means of gas chromatography. J Nanjing Agric Coll 4: 110-116 1982.
32. Raleigh DR Boe DM Yu D Weber CR Marchiando AM Bradford EM Wang Y Wu L Schneeberger EE Shen L Turner JR. Occludin S408 phosphorylation regulates tight junction protein interactions and barrier function. J Cell Biol 193: 565-582 2011.
33. Schulzke JD Fromm M. Tight junctions: molecular structure meets function. Ann N Y Acad Sci 1165: 1-6 2009.
34. Schweigel M Freyer M Leclercq S Etschmann B Lodemann U Bottcher A Martens H. Luminal hyperosmolarity decreases Na transport and impairs barrier function of sheep rumen epithelium. J Comp Physiol B 175: 575-591 2005.
35. Steele MA. An increase in dietary non-structural carbohydrates alters the structure and metabolism of the rumen epithelium in lambs. Can J Anim Sci 92: 123-130 2012.
36. Steele MA AlZahal O Hook SE Croom J McBride BW. Ruminal acidosis and the rapid onset of ruminal parakeratosis in a mature dairy cow: a case report. Acta Vet Scan 51: 2009.
37. Steele MA Croom J Kahler M AlZahal O Hook SE Plaizier K McBride BW. Bovine rumen epithelium undergoes rapid structural adaptations during grain-induced subacute ruminal acidosis. Am J Physiol Regul Integr Comp Physiol 300: R1515-R1523 2011.
38. Stumpff F Georgi MI Mundhenk L Rabbani I Fromm M Martens H Gunzel D. Sheep rumen and omasum primary cultures and source epithelia: barrier function aligns with expression of tight junction proteins. J Exp Biol 214: 2871-2882 2011.
39. Turner JR. Intestinal mucosal barrier function in health and disease. Nat Rev Immunol 9: 799-809 2009.
40. Wang A Gu Z Heid B Akers RM Jiang H. Identification and characterization of the bovine G protein-coupled receptor GPR41 and GPR43 genes. J Dairy Sci 92: 2696-2705 2009.
41. Watson CJ Hoare CJ Garrod DR Carlson GL Warhurst G. Interferonselectively increases epithelial permeability to large molecules by activating different populations of paracellular pores. J Cell Sci 118: 5221-5230 2005.
42. Zeissig S Burgel N Gunzel D Richter J Mankertz J Wahnschaffe U Kroesen AJ Zeitz M Fromm M Schulzke JD. Changes in expression and distribution of claudin 2 5 and 8 lead to discontinuous tight junctions and barrier dysfunction in active Crohn's disease. Gut 56: 61-72 2007.