Sodium Butyrate Improves High-Concentrate-Diet-Induced Impairment of Ruminal Epithelium Barrier Function in Goats

Journal of Agricultural and Food Chemistry

Volumn 66, Issue 33, 2018, Pages 8729-8736

  Zhang, Kai ^a,b   Meng, Meijuan ^a   Gao, Lipeng ^a   Tu, Yuanlu ^a   Bai, Yunfeng ^a  

^a INSTITUTE OF PLANT PROTECTION   (China)

^b AGRO ENVIRONMENTAL PROTECTION INSTITUTE   (China)

Author keywords

goat; rumen epithelium; sodium butyrate; subacute rumen acidosis; tight junction proteins

Indexed keywords

ALKYLATION; ENZYMES; NUCLEIC ACIDS; SODIUM;

BARRIER FUNCTIONS; CONCENTRATE DIET; DNA METHYLATION; MITOGEN ACTIVATED PROTEIN KINASE; MRNA EXPRESSION; PHOSPHORYLATED PROTEINS; PROTEIN EXPRESSIONS; PROTEIN KINASE C;

ISOMERS;

BUTYRIC ACID; CLAUDIN 1; OCCLUDIN; PROTEIN KINASE C;

ACIDOSIS; ANALYSIS; ANIMAL; ANIMAL FOOD; CHEMISTRY; DNA METHYLATION; EPITHELIUM; GENETICS; GOAT; GOAT DISEASE; MALE; METABOLISM; PH; RUMEN; TIGHT JUNCTION; VETERINARY MEDICINE;

ACIDOSIS; ANIMAL FEED; ANIMALS; BUTYRIC ACID; CLAUDIN-1; DNA METHYLATION; EPITHELIUM; GOAT DISEASES; GOATS; HYDROGEN-ION CONCENTRATION; MALE; OCCLUDIN; PROTEIN KINASE C; RUMEN; TIGHT JUNCTIONS;

EID: 85050090602     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/acs.jafc.8b03108     Document Type: Article

References (57)

1. Krause, K. M.; Oetzel, G. R. Understanding and preventing subacute ruminal acidosis in dairy herds: A review. Anim. Feed Sci. Technol. 2006, 126, 215-236, 10.1016/j.anifeedsci.2005.08.004
2. Chang, G. J.; Zhuang, S.; Seyfert, H. M.; Zhang, K.; Xu, T. L.; Jin, D.; Guo, J. F.; Shen, X. Z. Hepatic TLR4 signaling is activated by LPS from digestive tract during SARA, and epigenetic mechanisms contribute to enforced TLR4 expression. Oncotarget 2015, 6 (36), 38578-38590, 10.18632/oncotarget.6161
3. Plaizier, J.; Krause, D.; Gozho, G.; McBride, B. Subacute ruminal acidosis in dairy cows: The physiological causes, incidence and consequences. Vet. J. 2008, 176, 21-31, 10.1016/j.tvjl.2007.12.016
4. Martens, H.; Krutzfeld, T.; Wolf, K. Sodium transport across the isolated epithelium of sheep omasum is influenced by luminal ammonia. J. Vet. Med., A 2004, 51, 46-51, 10.1111/j.1439-0442.2004.00609.x
5. Khafipour, E.; Krause, D. O.; Plaizier, J. C. Alfalfa pellet-induced subacute ruminal acidosis in dairy cows increases bacterial endotoxin in the rumen without causing inflammation. J. Dairy Sci. 2009, 92, 1712-1724, 10.3168/jds.2008-1656
6. Plaizier, J.; Khafipour, E.; Li, S.; Gozho, G.; Krause, D. Subacute ruminal acidosis (SARA), endotoxins and health consequences. Anim. Feed Sci. Technol. 2012, 172, 9-21, 10.1016/j.anifeedsci.2011.12.004
7. Nagaraja, T. G.; Titgemeyer, E. C. Ruminal acidosis in beef cattle: The current microbiological and nutritional outlook. J. Dairy Sci. 2007, 90, E17-E38, 10.3168/jds.2006-478
8. Gozho, G. N.; Krause, D. O.; Plaizier, J. C. Ruminal lipopolysaccharide concentration and inflammatory response during grain-induced subacute ruminal acidosis in dairy cows. J. Dairy Sci. 2007, 90, 856-866, 10.3168/jds.S0022-0302(07)71569-2
9. Gareau, M. G.; Silva, M. A.; Perdue, M. H. Pathophysiological mechanisms of stress-induced intestinal damage. Curr. Mol. Med. 2008, 8, 274-281, 10.2174/156652408784533760
10. Steele, M. A.; Croom, J.; Kahler, M.; Al-Zahal, O.; Hook, S. E.; Plaizier, K.; McBride, B. W. Bovine rumen epithelium undergoes rapid structural adaptations during grain-induced subacute ruminal acidosis. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2011, 300, R1515-R1523, 10.1152/ajpregu.00120.2010
11. Liu, J. H.; Xu, T. T.; Liu, Y. J.; Zhu, W. Y.; Mao, S. Y. A high-grain diet causes massive disruption of ruminal epithelial tight junctions in goats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2013, 305, R232-R241, 10.1152/ajpregu.00068.2013
12. Gassler, N.; Rohr, C.; Schneider, A.; Kartenbeck, J.; Bach, A.; Obermüller, N.; Otto, H. F.; Autschbach, F. Inflammatory bowel disease is associated with changes of enterocytic junctions. Am. J. Physiol. Gastrointest. Liver Physiol. 2001, 281, G216-G228, 10.1152/ajpgi.2001.281.1.G216
13. Heller, F.; Florian, P.; Bojarski, C.; Richter, J.; Christ, M.; Hillenbrand, B.; Mankertz, J.; Gitter, A. H.; Burgel, N.; Fromm, M.; Zeitz, M.; Fuss, I.; Strober, W.; Schulzke, J. D. Interleukin-13 is the key effector Th2 cytokine in ulcerative colitis that affects epithelial tight junctions, apoptosis, and cell restitution. Gastroenterology 2005, 129, 550-564, 10.1053/j.gastro.2005.05.002
14. Poritz, L. S.; Harris, L. R.; Kelly, A. A.; Koltun, W. A. Increase in the tight junction protein claudin-1 in intestinal inflammation. Dig. Dis. Sci. 2011, 56, 2802-2809, 10.1007/s10620-011-1688-9
15. Matter, K.; Balda, M. S. Occludin and the functions of tight junctions. International Review of Cytology; Elsevier: Amsterdam, Netherlands, 1998; Vol. 186, pp 117-146, 10.1016/S0074-7696(08)61052-9.
16. Feldman, G. J.; Mullin, J. M.; Ryan, M. P. Occludin: Structure, function and regulation. Adv. Drug Delivery Rev. 2005, 57, 883-917, 10.1016/j.addr.2005.01.009
17. Saitou, M.; Furuse, M.; Sasaki, H.; Schulzke, J. D.; Fromm, M.; Takano, H.; Noda, T.; Tsukita, S. Complex phenotype of mice lacking occludin, a component of tight junction strands. Mol. Biol. Cell 2000, 11, 4131-4142, 10.1091/mbc.11.12.4131
18. McCarthy, K. M.; Skare, I. B.; Stankewich, M. C.; Furuse, M.; Tsukita, S.; Rogers, R. A.; Lynch, R. D.; Schneeberger, E. E. Occludin is a functional component of the tight junction. J. Cell Sci. 1996, 109, 2287-2298
19. Balda, M. S.; Matter, K. Tight junctions and the regulation of gene expression. Biochim. Biophys. Acta, Biomembr. 2009, 1788, 761-767, 10.1016/j.bbamem.2008.11.024
20. Balda, M. S.; Flores-Maldonado, C.; Cereijido, M.; Matter, K. Multiple domains of occludin are involved in the regulation of paracellular permeability. J. Cell. Biochem. 2000, 78, 85-96, 10.1002/(SICI)1097-4644(20000701)78:1<85::AID-JCB8>3.0.CO;2-F
21. Yu, A. L.; McCarthy, K. M.; Francis, S. A.; McCormack, J. M.; Lai, J.; Rogers, R. A.; Lynch, R. D.; Schneeberger, E. E. Knock down of occludin expression leads to diverse phenotypic alterations in epithelial cells. Am. J. Physiol. Cell Physiol. 2005, 288, C1231-C1241, 10.1152/ajpcell.00581.2004
22. Furuse, M.; Fujita, K.; Hiiragi, T.; Fujimoto, K.; Tsukita, S. Claudin-1 and -2: Novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin. J. Cell Biol. 1998, 141, 1539-1550, 10.1083/jcb.141.7.1539
23. Inai, T.; Kobayashi, J.; Shibata, Y. Claudin-1 contributes to the epithelial barrier function in MDCK cells. Eur. J. Cell Biol. 1999, 78, 849-855, 10.1016/S0171-9335(99)80086-7
24. Furuse, M.; Furuse, K.; Sasaki, H.; Tsukita, S. Conversion of zonulae occludentes from tight to leaky strand type by introducing claudin-2 into Madin-Darby canine kidney I cells. J. Cell Biol. 2001, 153, 263-272, 10.1083/jcb.153.2.263
25. Tsukita, S.; Furuse, M.; Itoh, M. Multifunctional strands in tight junctions. Nat. Rev. Mol. Cell Biol. 2001, 2, 285-293, 10.1038/35067088
26. Bazzoni, G.; Martinez-Estrada, O. M.; Orsenigo, F.; Cordenonsi, M.; Citi, S.; Dejana, E. Interaction of junctional adhesion molecule with the tight junction components ZO-1, cingulin, and occludin. J. Biol. Chem. 2000, 275, 20520-20526, 10.1074/jbc.M905251199
27. Clarke, H.; Marano, C. W.; Peralta, S. A.; Mullin, J. M. Modification of tight junction function by protein kinase C isoforms. Adv. Drug Delivery Rev. 2000, 41, 283-301, 10.1016/S0169-409X(00)00047-8
28. Naydenov, N. G.; Hopkins, A. M.; Ivanov, A. I. c-Jun N-terminal kinase mediates disassembly of apical junctions in model intestinal epithelia. Cell Cycle 2009, 8, 2110-2121, 10.4161/cc.8.13.8928
29. Lee, M. H.; Koria, P.; Qu, J.; Andreadis, S. T. JNK phosphorylates beta-catenin and regulates adherens junctions. FASEB J. 2009, 23, 3874-3883, 10.1096/fj.08-117804
30. Kida, Y.; Shimizu, T.; Kuwano, K. Sodium butyrate up-regulates cathelicidin gene expression via activator protein-1 and histone acetylation at the promoter region in a human lung epithelial cell line, EBC-1. Mol. Immunol. 2006, 43 (12), 1972-1981, 10.1016/j.molimm.2005.11.014
31. Gorka, P.; Kowalski, Z. M.; Pietrzak, P.; Kotunia, A.; Kiljanczyk, R.; Flaga, J.; Holst, J. J.; Guilloteau, P.; Zabielski, R. Effect of sodium butyrate supplementation in milk replacer and starter diet on rumen development in calves. J. Physiol. Pharmacol. 2009, 60 (3), 47-53
32. Guilloteau, P.; Zabielski, R.; David, J. C.; Blum, J. W.; Morisset, J. A.; Biernat, M.; Woliński, J.; Laubitz, D.; Hamon, Y. Sodium-butyrate as a growth promoter in milk replacer formula for young calves. J. Dairy Sci. 2009, 92 (3), 1038-1049, 10.3168/jds.2008-1213
33. Khan, S.; Jena, G. B. Protective role of sodium butyrate, a HDAC inhibitor on beta-cell proliferation, function and glucose homeostasis through modulation of p38/ERK MAPK and apoptotic pathways: Study in juvenile diabetic rat. Chem.-Biol. Interact. 2014, 213, 1-12, 10.1016/j.cbi.2014.02.001
34. Aguirre, T. A.; Rosa, M.; Guterres, S. S.; Pohlmann, A. R.; Coulter, I.; Brayden, D. J. Investigation of coco-glucoside as a novel intestinal permeation enhancer in rat models. Eur. J. Pharm. Biopharm. 2014, 88, 856-865, 10.1016/j.ejpb.2014.10.013
35. Wu, X.; Vallance, B. A.; Boyer, L.; Bergstrom, K. S.; Walker, J.; Madsen, K.; O'Kusky, J. R.; Buchan, A. M.; Jacobson, K. Saccharomyces boulardii ameliorates Citrobacter rodentium-induced colitis through actions on bacterial virulence factors. Am. J. Physiol. Gastrointest. Liver Physiol 2008, 294, G295-G306, 10.1152/ajpgi.00173.2007
36. Livak, K. J.; Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative pcr and the 2-δδct method. Methods 2001, 25 (4), 402-408, 10.1006/meth.2001.1262
37. Bock, C.; Reither, S.; Mikeska, T.; Paulsen, M.; Walter, J.; Lengauer, T. BiQ Analyzer: Visualization and quality control for DNA methylation data from bisulfite sequencing. Bioinformatics 2005, 21 (21), 4067-4068, 10.1093/bioinformatics/bti652
38. Hnasko, T. S.; Hnasko, R. M. The Western Blot. Methods Mol. Biol. 2015, 1318, 87-96, 10.1007/978-1-4939-2742-5-9
39. Emmanuel, D. G.; Dunn, S. M.; Ametaj, B. N. Feeding high proportions of barley grain stimulates an inflammatory response in dairy cows. J. Dairy Sci. 2008, 91, 606-614, 10.3168/jds.2007-0256
40. Castrillo, C.; Mota, M.; Van Laar, H.; Martín-Tereso, J.; Gimeno, A.; Fondevila, M.; Guada, J. A. Effect of compound feed pelleting and die diameter on rumen fermentation in beef cattle fed high concentrate diets. Anim. Feed Sci. Technol. 2013, 180, 34-43, 10.1016/j.anifeedsci.2013.01.004
41. Penner, G. B.; Steele, M. A.; Aschenbach, J. R.; McBride, B. W. Ruminant nutrition symposium: Molecular adaptation of ruminal epithelia to highly fermentable diets. J. Anim. Sci. 2011, 89, 1108-1119, 10.2527/jas.2010-3378
42. Klevenhusen, F.; Hollmann, M.; Podstatzky-Lichtenstein, L.; Krametter-Frotscher, R.; Aschenbach, J. R.; Zebeli, Q. Feeding barley grain-rich diets altered electrophysiological properties and permeability of the ruminal wall in a goat model. J. Dairy Sci. 2013, 96, 2293-2302, 10.3168/jds.2012-6187
43. Penner, G. B.; Oba, M.; Gabel, G.; Aschenbach, J. R. A single mild episode of subacute ruminal acidosis does not affect ruminal barrier function in the short term. J. Dairy Sci. 2010, 93, 4838-4845, 10.3168/jds.2010-3406
44. Roth, M. J.; Abnet, C. C.; Hu, N.; Wang, Q.-H.; Wei, W.-Q.; Green, L.; D'Alelio, M.; Qiao, Y.-L.; Dawsey, S. M.; Taylor, P. R.; Woodson, K. p16, MGMT, RARβ2, CLDN3, CRBP and MT1G gene methylation in esophageal squamous cell carcinoma and its precursor lesions. Oncol. Rep. 2006, 15, 1591-1597, 10.3892/or.15.6.1591
45. 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 2011, 300, G1054-G1064, 10.1152/ajpgi.00055.2011
46. Raleigh, D. R.; Boe, D. M.; Yu, D.; Weber, C. R.; Marchiando, A. M.; Bradford, E. M.; Wang, Y.; Wu, L.; Schneeberger, E. E.; Shen, L.; Turner, J. R. Occludin S408 phosphorylation regulates tight junction protein interactions and barrier function. J. Cell Biol. 2011, 193, 565-582, 10.1083/jcb.201010065
47. Kenichi, T.; Takashi, K.; Norimasa, S.; Tetsuo, H. Role of tight junctions in signal transduction: An update. EXCLI J. 2014, 13, 1145-1162
48. Seth, A.; Sheth, P.; Elias, B. C.; Rao, R. Protein phosphatases 2A and 1 interact with occludin and negatively regulate the assembly of tight junctions in the CACO-2 cell monolayer. J. Biol. Chem. 2007, 282, 11487-11498, 10.1074/jbc.M610597200
49. Banan, A.; Zhang, L. J.; Shaikh, M.; Fields, J. Z.; Choudhary, S.; Forsyth, C. B.; Farhadi, A.; Keshavarzian, A. θ Isoform of protein kinase C alters barrier function in intestinal epithelium through modulation of distinct claudin isotypes: A novel mechanism for regulation of permeability. J. Pharmacol. Exp. Ther. 2005, 313, 962-982
50. Clarke, H.; Ginanni, N.; Laughlin, K. V.; Smith, J. B.; Pettit, G. R.; Mullin, J. M. The transient increase of tight junction permeability induced by bryostatin 1 correlates with rapid downregulation of protein kinase C-α. Exp. Cell Res. 2000, 261, 239-249, 10.1006/excr.2000.5035
51. Li, D.; Mrsny, R. J. Oncogenic Raf-1 disrupts epithelial tight junctions via downregulation of occludin. J. Cell Biol. 2000, 148, 791-800, 10.1083/jcb.148.4.791
52. Kojima, T.; Yamamoto, T.; Murata, M.; Chiba, H.; Kokai, Y.; Sawada, N. Regulation of the blood-biliary barrier: Interaction between gap and tight junctions in hepatocytes. Med. Electron Microsc. 2003, 36, 157-164, 10.1007/s00795-003-0220-5
53. Yamamoto, T.; Kojima, T.; Murata, M.; Takano, K.; Go, M.; Hatakeyama, N.; Chiba, H.; Sawada, N. p38 MAP-kinase regulates function of gap and tight junctions during regeneration of rat hepatocytes. J. Hepatol. 2005, 42, 707-718, 10.1016/j.jhep.2004.12.033
54. Saadat, I.; Higashi, H.; Obuse, C.; Umeda, M.; Murata-Kamiya, N.; Saito, Y.; Lu, H.; Ohnishi, N.; Azuma, T.; Suzuki, A.; Ohno, S.; Hatakeyama, M. Helicobacter pylori CagA targets PAR1/MARK kinase to disrupt epithelial cell polarity. Nature 2007, 447, 330-333, 10.1038/nature05765
55. Carrozzino, F.; Pugnale, P.; Féraille, E.; Montesano, R. Inhibition of basal p38 or JNK activity enhances epithelial barrier function through differential modulation of claudin expression. Am. J. Physiol. Cell Physiol. 2009, 297, C775-787, 10.1152/ajpcell.00084.2009
56. Kojima, T.; Fuchimoto, J.; Yamaguchi, H.; Ito, T.; Takasawa, A.; Ninomiya, T.; Kikuchi, S.; Ogasawara, N.; Ohkuni, T.; Masaki, T.; Hirata, K.; Himi, T.; Sawada, N. c-Jun N-terminal kinase is largely involved in the regulation of tricellular tight junctions via tricellulin in human pancreatic duct epithelial cells. J. Cell. Physiol. 2010, 225, 720-733, 10.1002/jcp.22273
57. Guo, J.; Chang, G.; Zhang, K.; Xu, L.; Jin, D.; Bilal, M. S.; Shen, X. Rumen-derived lipopolysaccharide provoked inflammatory injury in the liver of dairy cows fed a high-concentrate diet. Oncotarget. 2017, 8 (29), 46769-46780, 10.18632/oncotarget.18151