Key role of short-chain fatty acids in epithelial barrier failure during ruminal acidosis

Journal of Dairy Science

Volumn 100, Issue 8, 2017, Pages 6662-6675

  Meissner, Svenja ^a   Hagen, Franziska ^a   Deiner, Carolin ^a   Günzel, Dorothee ^b   Greco, Gabriele ^a   Shen, Zanming ^c   Aschenbach, Jörg R ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c NANJING AGRICULTURAL UNIVERSITY   (China)

Author keywords

ruminal epithelium; short chain fatty acid; subacute ruminal acidosis; tight junction

Indexed keywords

VOLATILE FATTY ACID;

ACIDOSIS; ANIMAL; CHEMISTRY; EPITHELIUM; METABOLISM; PATHOPHYSIOLOGY; PH; PHYSIOLOGY; RUMEN; SHEEP; SHEEP DISEASE; STOMACH DISEASE; VETERINARY;

ACIDOSIS; ANIMALS; EPITHELIUM; FATTY ACIDS, VOLATILE; HYDROGEN-ION CONCENTRATION; RUMEN; SHEEP; SHEEP DISEASES; STOMACH DISEASES;

EID: 85019591896     PISSN: 00220302     EISSN: 15253198     Source Type: Journal    
DOI: 10.3168/jds.2016-12262     Document Type: Article

References (57)

1. Andrews, F.M., Buchanan, B.R., Smith, S.H., Elliott, S.B., Saxton, A.M., In vitro effects of hydrochloric acid and various concentrations of acetic, propionic, butyric, or valeric acids on bioelectric properties of equine gastric squamous mucosa. Am. J. Vet. Res. 67 (2006), 1873–1882 10.2460/ajvr.67.11.1873 17078749.
2. Argenzio, R.A., Eisemann, J., Mechanisms of acid injury in porcine gastroesophageal mucosa. Am. J. Vet. Res. 57 (1996), 564–573 8712526.
3. Aschenbach, J.R., Bilk, S., Tadesse, G., Stumpff, F., Gäbel, G., Bicarbonate-dependent and bicarbonate-independent mechanisms contribute to nondiffusive uptake of acetate in the ruminal epithelium of sheep. Am. J. Physiol. Gastrointest. Liver Physiol. 296 (2009), G1098–G1107 10.1152/ajpgi.90442.2008 19264953.
4. Aschenbach, J.R., Gäbel, G., Effect and absorption of histamine in sheep rumen: Significance of acidotic epithelial damage. J. Anim. Sci. 78 (2000), 464–470 10709939.
5. Aschenbach, J.R., Kristensen, N.B., Donkin, S.S., Hammon, H.M., Penner, G.B., Gluconeogenesis in dairy cows: The secret of making sweet milk from sour dough. IUBMB Life 62 (2010), 869–877 10.1002/iub.400 21171012.
6. Aschenbach, J.R., Penner, G.B., Stumpff, F., Gäbel, G., Ruminant Nutrition Symposium: Role of fermentation acid absorption in the regulation of ruminal pH. J. Anim. Sci. 89 (2011), 1092–1107 10.2527/jas.2010-3301 20952531.
7. Balda, M.S., Matter, K., Epithelial cell adhesion and the regulation of gene expression. Trends Cell Biol. 13 (2003), 310–318 12791297.
8. Bergman, E.N., Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiol. Rev. 70 (1990), 567–590 2181501.
9. Brandner, J.M., Tight junctions and tight junction proteins in mammalian epidermis. Eur. J. Pharm. Biopharm. 72 (2009), 289–294 10.1016/j.ejpb.2008.08.007 18775491.
10. Bugaut, M., Occurrence, absorption and metabolism of short chain fatty acids in the digestive tract of mammals. Comp. Biochem. Physiol. B 86 (1987), 439–472 3297476.
11. Ding, L., Lu, Z., Foreman, O., Tatum, R., Lu, Q., Renegar, R., Cao, J., Chen, Y.H., Inflammation and disruption of the mucosal architecture in claudin-7-deficient mice. Gastroenterology 142 (2012), 305–315 10.1053/j.gastro.2011.10.025 22044670.
12. Furuse, M., Hata, M., Furuse, K., Yoshida, Y., Haratake, A., Sugitani, Y., Noda, T., Kubo, A., Tsukita, S., Claudin-based tight junctions are crucial for the mammalian epidermal barrier: A lesson from claudin-1-deficient mice. J. Cell Biol. 156 (2002), 1099–1111 11889141.
13. 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 (1989), 35–44 2717703.
14. Georgi, M.I., Rosendahl, J., Ernst, F., Günzel, D., Aschenbach, J.R., Martens, H., Stumpff, F., Epithelia of the ovine and bovine forestomach express basolateral maxi-anion channels permeable to the anions of short-chain fatty acids. Pflugers Arch. 466 (2014), 1689–1712 10.1007/s00424-013-1386-x 24240698.
15. Gozho, G.N., Plaizier, J.C., Krause, D.O., Kennedy, A.D., Wittenberg, K.M., Subacute ruminal acidosis induces ruminal lipopolysaccharide endotoxin release and triggers an inflammatory response. J. Dairy Sci. 88 (2005), 1399–1403 10.3168/jds.S0022-0302(05)72807-1 15778308.
16. Graham, C., Simmons, N.L., Functional organization of the bovine rumen epithelium. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288 (2005), R173–R181 10.1152/ajpregu.00425.2004 15319221.
17. Gutknecht, J., Proton/hydroxide conductance through phospholipid bilayer membranes: Effects of phytanic acid. Biochim. Biophys. Acta 898 (1987), 97–108 3030426.
18. 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 129 (2005), 550–564 10.1016/j.gastro.2005.05.002 16083712.
19. Hirst, B.H., The gastric mucosal barrier. Schultz, S.G., Forte, J.G., Rauner, B.B., (eds.) Handbook of Physiology: A Critical, Comprehensive Presentation of Physiological Knowledge and Concepts. Section 6: The Gastrointestinal System. Vol. 3: Salivary, Gastric, Pancreatic, and Hepatobiliary Secretion, 1989, Am. Physiol. Soc., Bethesda, MA, 279–308.
20. Kirschner, N., Brandner, J.M., Barriers and more: Functions of tight junction proteins in the skin. Ann. N. Y. Acad. Sci. 1257 (2012), 158–166 10.1111/j.1749-6632.2012.06554.x 22671602.
21. Kirschner, N., Houdek, P., Fromm, M., Moll, I., Brandner, J.M., Tight junctions form a barrier in human epidermis. Eur. J. Cell Biol. 89 (2010), 839–842 10.1016/j.ejcb.2010.07.010 20732726.
22. Kirschner, N., Poetzl, C., von den Driesch, P., Wladykowski, E., Moll, I., Behne, M.J., Brandner, J.M., Alteration of tight junction proteins is an early event in psoriasis: Putative involvement of proinflammatory cytokines. Am. J. Pathol. 175 (2009), 1095–1106 10.2353/ajpath.2009.080973 19661441.
23. Kleen, J.L., Hooijer, G.A., Rehage, J., Noordhuizen, J.P., Subacute ruminal acidosis (SARA): A review. J. Vet. Med. A Physiol. Pathol. Clin. Med. 50 (2003), 406–414 14633219.
24. Klevenhusen, F., Hollmann, M., Podstatzky-Lichtenstein, L., Krametter-Frötscher, 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. 96 (2013), 2293–2302 10.3168/jds.2012-6187 23403198.
25. Leonhard-Marek, S., Stumpff, F., Martens, H., Transport of cations and anions across forestomach epithelia: Conclusions from in vitro studies. Animal 4 (2010), 1037–1056 10.1017/S1751731110000261 22444608.
26. 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. 305 (2013), R232–R241 10.1152/ajpregu.00068.2013 23739344.
27. Markov, A.G., Aschenbach, J.R., Amasheh, S., Claudin clusters as determinants of epithelial barrier function. IUBMB Life 67 (2015), 29–35 10.1002/iub.1347 25788154.
28. Martin, B.K., Accumulation of drug anions in gastric mucosal cells. Nature 198 (1963), 896–897.
29. 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. 109 (1996), 2287–2298 8886979.
30. Mineta, K., Yamamoto, Y., Yamazaki, Y., Tanaka, H., Tada, Y., Saito, K., Tamura, A., Igarashi, M., Endo, T., Takeuchi, K., Tsukita, S., Predicted expansion of the claudin multigene family. FEBS Lett. 585 (2011), 606–612 10.1016/j.febslet.2011.01.028 21276448.
31. Miyoshi, M., Usami, M., Ohata, A., Short-chain fatty acids and trichostatin A alter tight junction permeability in human umbilical vein endothelial cells. Nutrition 24 (2008), 1189–1198 10.1016/j.nut.2008.06.012 18723323.
32. Morita, K., Furuse, M., Fujimoto, K., Tsukita, S., Claudin multigene family encoding four-transmembrane domain protein components of tight junction strands. Proc. Natl. Acad. Sci. USA 96 (1999), 511–516 9892664.
33. Nocek, J.E., Bovine acidosis: Implications on laminitis. J. Dairy Sci. 80 (1997), 1005–1028 9178142.
34. Ohata, A., Usami, M., Miyoshi, M., Short-chain fatty acids alter tight junction permeability in intestinal monolayer cells via lipoxygenase activation. Nutrition 21 (2005), 838–847 10.1016/j.nut.2004.12.004 15975492.
35. Owens, F.N., Secrist, D.S., Hill, W.J., Gill, D.R., Acidosis in cattle: A review. J. Anim. Sci. 76 (1998), 275–286 9464909.
36. Peng, L., Li, Z.R., Green, R.S., Holzman, I.R., Lin, J., Butyrate enhances the intestinal barrier by facilitating tight junction assembly via activation of AMP-activated protein kinase in Caco-2 cell monolayers. J. Nutr. 139 (2009), 1619–1625 10.3945/jn.109.104638 19625695.
37. Penner, G.B., Aschenbach, J.R., Gabel, G., Rackwitz, R., Oba, M., Epithelial capacity for apical uptake of short chain fatty acids is a key determinant for intraruminal pH and the susceptibility to subacute ruminal acidosis in sheep. J. Nutr. 139 (2009), 1714–1720 10.3945/jn.109.108506 19640964.
38. Penner, G.B., Beauchemin, K.A., Mutsvangwa, T., Severity of ruminal acidosis in primiparous Holstein cows during the periparturient period. J. Dairy Sci. 90 (2007), 365–375 10.3168/jds.S0022-0302(07)72638-3 17183105.
39. 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. 93 (2010), 4838–4845 10.3168/jds.2010-3406 20855017.
40. 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. 89 (2011), 1108–1119 10.2527/jas.2010-3378 20971890.
41. Plaizier, J.C., Krause, D.O., Gozho, G.N., McBride, B.W., Subacute ruminal acidosis in dairy cows: The physiological causes, incidence and consequences. Vet. J. 176 (2008), 21–31 10.1016/j.tvjl.2007.12.016 18329918.
42. Plöger, S., Stumpff, F., Penner, G.B., Schulzke, J.D., Gäbel, G., Martens, H., Shen, Z., Günzel, D., Aschenbach, J.R., Microbial butyrate and its role for barrier function in the gastrointestinal tract. Ann. N. Y. Acad. Sci. 1258 (2012), 52–59 10.1111/j.1749-6632.2012.06553.x 22731715.
43. Raleigh, D.R., Marchiando, A.M., Zhang, Y., Shen, L., Sasaki, H., Wang, Y., Long, M., Turner, J.R., Tight junction-associated MARVEL proteins marveld3, tricellulin, and occludin have distinct but overlapping functions. Mol. Biol. Cell 21 (2010), 1200–1213 10.1091/mbc.E09-08-0734 20164257.
44. 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 11 (2000), 4131–4142 11102513.
45. Schulzke, J.D., Ploeger, S., Amasheh, M., Fromm, A., Zeissig, S., Troeger, H., Richter, J., Bojarski, C., Schumann, M., Fromm, M., Epithelial tight junctions in intestinal inflammation. Ann. N. Y. Acad. Sci. 1165 (2009), 294–300 10.1111/j.1749-6632.2009.04062.x 19538319.
46. Steele, M.A., AlZahal, O., Hook, S.E., Croom, J., McBride, B.W., Ruminal acidosis and the rapid onset of ruminal parakeratosis in a mature dairy cow: A case report. Acta Vet. Scand., 51, 2009, 39 10.1186/1751-0147-51-39 19840395.
47. Steele, M.A., Croom, J., Kahler, M., AlZahal, 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. 300 (2011), R1515–R1523 10.1152/ajpregu.00120.2010 21451145.
48. Stumpff, F., Georgi, M.I., Mundhenk, L., Rabbani, I., Fromm, M., Martens, H., Günzel, D., Sheep rumen and omasum primary cultures and source epithelia: Barrier function aligns with expression of tight junction proteins. J. Exp. Biol. 214 (2011), 2871–2882 10.1242/jeb.055582 21832130.
49. Stumpff, F., Martens, H., Bilk, S., Aschenbach, J.R., Gäbel, G., Cultured ruminal epithelial cells express a large-conductance channel permeable to chloride, bicarbonate, and acetate. Pflugers Arch. 457 (2009), 1003–1022 10.1007/s00424-008-0566-6 18716793.
50. Sutton, J.D., Dhanoa, M.S., Morant, S.V., France, J., Napper, D.J., Schuller, E., Rates of production of acetate, propionate, and butyrate in the rumen of lactating dairy cows given normal and low-roughage diets. J. Dairy Sci. 86 (2003), 3620–3633 10.3168/jds.S0022-0302(03)73968-X 14672193.
51. Szemeredy, G., Raul, R., Alterations of the ruminal mucosa and its relation to the hepatic abscesses in bulls fed high energy and low fibre diets. Acta Vet. Acad. Sci. Hung. 26 (1976), 313–324 1032458.
52. Tadepalli, S., Narayanan, S.K., Stewart, G.C., Chengappa, M.M., Nagaraja, T.G., Fusobacterium necrophorum: A ruminal bacterium that invades liver to cause abscesses in cattle. Anaerobe 15 (2009), 36–43 10.1016/j.anaerobe.2008.05.005 18595747.
53. Tanaka, H., Takechi, M., Kiyonari, H., Shioi, G., Tamura, A., Tsukita, S., Intestinal deletion of Claudin-7 enhances paracellular organic solute flux and initiates colonic inflammation in mice. Gut 64 (2015), 1529–1538 10.1136/gutjnl-2014-308419 25691495.
54. Van Itallie, C., Rahner, C., Anderson, J.M., Regulated expression of claudin-4 decreases paracellular conductance through a selective decrease in sodium permeability. J. Clin. Invest. 107 (2001), 1319–1327 10.1172/JCI12464 11375422.
55. Van Itallie, C.M., Anderson, J.M., Claudins and epithelial paracellular transport. Annu. Rev. Physiol. 68 (2006), 403–429 10.1146/annurev.physiol.68.040104.131404 16460278.
56. Zebeli, Q., Aschenbach, J.R., Tafaj, M., Boguhn, J., Ametaj, B.N., Drochner, W., Invited review: Role of physically effective fiber and estimation of dietary fiber adequacy in high-producing dairy cattle. J. Dairy Sci. 95 (2012), 1041–1056 10.3168/jds.2011-4421 22365188.
57. Zeissig, S., Burgel, N., Günzel, D., Richter, J., Mankertz, J., Wahnschaffe, U., Kroesen, A.J., Zeitz, M., Fromm, M., Schulzke, J.D., 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 (2007), 61–72 10.1136/gut.2006.094375 16822808.