Short-term adaptation of the ruminal epithelium involves abrupt changes in sodium and short-chain fatty acid transport

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 307, Issue 7, 2014, Pages R802-R816

  Schurmann, Brittney L ^a   Walpole, Matthew E ^a   Górka, Pawel ^a,b   Ching, John C H ^b   Loewen, Matthew E ^b   Penner, Gregory B ^a,c  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

^b UNIVERSITY OF AGRICULTURE IN KRAKOW   (Poland)

^c UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

dietary adaptation; rumen epithelium; short chain fatty acid; Ussing chamber

Indexed keywords

ACETIC ACID; BUTYRIC ACID; INTERLEUKIN 1BETA; MANNITOL; SHORT CHAIN FATTY ACID; TOLL LIKE RECEPTOR 2; SODIUM; VOLATILE FATTY ACID;

ANIMAL EXPERIMENT; ARTICLE; BARLEY; BODY WEIGHT; CONTROLLED STUDY; DIET THERAPY; EPITHELIUM; FATTY ACID TRANSPORT; GENE EXPRESSION; HAY; HOLSTEIN CATTLE; NONHUMAN; PH MEASUREMENT; RUMINAL EPITHELIUM; SHORT CHAIN FATTY ACID TRANSPORT; SIGNAL TRANSDUCTION; SODIUM TRANSPORT; STOMACH ABSORPTION; ADAPTATION; ANALYSIS; ANIMAL; ANIMAL FOOD; BOVINAE; DIET; DIET SUPPLEMENTATION; METABOLISM; PHYSIOLOGY; RUMINANT STOMACH; TIME; TRANSPORT AT THE CELLULAR LEVEL; VETERINARY;

ADAPTATION, PHYSIOLOGICAL; ANIMAL FEED; ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; BIOLOGICAL TRANSPORT; CATTLE; DIET; DIETARY SUPPLEMENTS; EPITHELIUM; FATTY ACIDS, VOLATILE; RUMEN; SODIUM; TIME FACTORS;

EID: 84907676179     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00035.2014     Document Type: Article

References (64)

1. Abreu MT. Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function. Nat Rev Immunol 10: 131-144, 2010.
2. Al-Sadi RM, Ma TY. IL-1fj causes an increase in intestinal epithelial tight junction permeability. J Immunol (Baltimore, Md: 1950) 178: 4641-4649, 2007.
3. + exchanger (NHE1) in breast cancer metastasis. Cancer Res 73: 1259-1264, 2013.
4. Aschenbach JR, Bilk S, Tadesse G, Stumpff F, Gabel G. Bicarbonate-dependent and bicarbonate-independent mechanisms contribute to nondif-fusive uptake of acetate in the ruminal epithelium of sheep. Am J Physiol Gastrointest Liver Physiol 296: G1098-G1107, 2009.
5. Aschenbach JR, Gabel G. Effect and absorption of histamine in sheep rumen: significance of acidotic epithelial damage. J Anim Sci 78: 464-470, 2000.
6. Aschenbach JR, Penner GB, Stumpff F, Gabel G. Ruminant nutrition symposium: Role of fermentation acid absorption in the regulation of ruminal pH. J Animal Sci 89: 1092-1107, 2011.
7. Bannink A, France J, Lopez S, Gerrits WJJ, Kebreab E, Tamminga S, Dijkstra J. Modelling the implications of feeding strategy on rumen fermentation and functioning of the rumen wall. Animal Feed Sci Technol 143: 3-26, 2008.
8. Bergman EN. Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiol Rev 70: 567-590, 1990.
9. Brown AJ, Goldsworthy SM, Barnes AA, Eilert MM, Tcheang L, Daniels D, Muir AI, Wigglesworth MJ, Kinghorn I, Fraser NJ, Pike NB, Strum JC, Steplewski KM, Murdock PR, Holder JC, Marshall FH, Szekeres PG, Wilson S, Ignar DM, Foord SM, Wise A, Dowell SJ. The orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short-chain carboxylic acids. J Biol Chem 278: 11312-11319, 2003.
10. Carretta MD, Conejeros I, Hidalgo MA, Burgos RA. Propionate induces the release of granules from bovine neutrophils. J Dairy Sci 96: 2507-2520, 2013.
11. Charavaryamath C, Fries P, Gomis S, Bell C, Doig K, Guan LL, Potter A, Napper S, Griebel PJ. Mucosal changes in a long-term bovine intestinal segment model following removal of ingesta and microflora. Gut Microbes 2: 134-144, 2011.
12. Chen Y, Oba M, Guan LL. Variation of bacterial communities and expression of Toll-like receptor genes in the rumen of steers differing in susceptibility to subacute ruminal acidosis. Vet Microbiol 159: 451-459, 2012.
13. Dengler F, Rackwitz R, Benesch F, Pfannkuche H, Gabel G. Bicarbonate-dependent transport of acetate and butyrate across the basolateral membrane of sheep rumen epithelium. Acta Physiol (Oxf) 210: 403-413, 2013.
14. Dijkstra J, Boer H, Van Bruchem J, Bruining M, Tamminga S. Absorption of volatile fatty acids from the rumen of lactating dairy cows as influenced by volatile fatty acid concentration, pH and rumen liquid volume. Br J Nutr 69: 385-396, 1993.
15. Dinarello CA. Biologic basis for interleukin-1 in disease. Blood 87: 2095-2147, 1996.
16. Dirksen GLH; Mayer K. Adaptive changes of the ruminal mucosa and functional and clinical significance. Bovine Pract 20: 116-120, 1985.
17. Etschmann B, Suplie A, Martens H. Change of ruminal sodium transport in sheep during dietary adaptation. Arch Animal Nutr 63: 26-38, 2009.
18. Firth SM, Baxter RC. Cellular actions of the insulin-like growth factor binding proteins. Endocr Rev 23: 824-854, 2002.
19. Gäbel G, Aschenbach JR, Muller F. Transfer of energy substrates across the ruminal epithelium: implications and limitations. Animal Health Res Rev 3: 15-30, 2002.
20. Gäbel G, Bestmann M, Martens H. [Influences of diet, short-chain fatty acids, lactate and chloride on bicarbonate movement across the reticulo-rumen wall of sheep]. Zentralblatt fur Veterinarmedizin Reihe A 38: 523-529, 1991.
21. +, Cl∼- and short-chain fatty acids across sheep ruminal epithelium. Exp Physiol 84: 333-345, 1999.
22. Gäbel G, Marek M, Martens H. [Influence of food deprivation on SCFA and electrolyte transport across sheep reticulorumen]. Zentralbl Veteri-narmed A 40: 339-344, 1993.
23. + and Cl∼- absorption in isolated sheep rumen mucosa. J Comp Physiol B 161: 419-426, 1991.
24. Gäbel 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.
25. Gäbel G, Martens H, Suendermann M, Galfi P. The effect of diet, intraruminal pH and osmolarity on sodium, chloride and magnesium absorption from the temporarily isolated and washed reticulo-rumen of sheep. Q J Exp Physiol 72: 501-511, 1987.
26. Graham C, Gatherar I, Haslam I, Glanville M, Simmons NL. Expression and localization of monocarboxylate transporters and sodium/proton exchangers in bovine rumen epithelium. Am J Physiol Regul Integr Comp Physiol 292: R997-R1007, 2007.
27. Graham C, Simmons NL. Functional organization of the bovine rumen epithelium. Am J Physiol Regul Integr Comp Physiol 288: R173-R181, 2005.
28. Khorasani GR, Okine EK, Kennelly JJ. Forage source alters nutrient supply to the intestine without influencing milk yield. J Dairy Sci 79: 862-872, 1996.
29. 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: 2293-2302, 2013.
30. + absorption across the rumen epithelium of goat and sheep. Am J Physiol Gastrointest Liver Physiol 291: G246-G252, 2006.
31. Liu JH, Xu TT, Liu YJ, Zhu WY, Mao SY. A high-grain diet causes massive disruption of ruminal epithelial tight junctions in goats. Am J Physiol Regul Integr Comp Physiol 305: R232-R241, 2013.
32. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402-408, 2001.
33. + transport and tissue conductance of sheep isolated rumen epithelium. Exp Physiol 91: 539-550, 2006.
34. Malhi M, Gui H, Yao L, Aschenbach JR, Gabel G, Shen Z. Increased papillae growth and enhanced short-chain fatty acid absorption in the rumen of goats are associated with transient increases in cyclin D1 expression after ruminal butyrate infusion. J Dairy Sci 96: 7603-7616, 2013.
35. Muller F, Huber K, Pfannkuche H, Aschenbach JR, Breves G, Gabel G. Transport of ketone bodies and lactate in the sheep ruminal epithelium by monocarboxylate transporter 1. Am J Physiol Gastrointest Liver Physiol 283: G1139-G1146, 2002.
36. National Research Council. Nutrient Requirements of Beef Cattle: Seventh Revised Edition: Update 2000. Washington, DC: National Academies Press, 2000.
37. Oh DY, Lagakos WS. The role of G-protein-coupled receptors in mediating the effect of fatty acids on inflammation and insulin sensitivity. Curr Opin Clin Nutr Metab Care 14: 322-327, 2011.
38. Owens FN, Secrist DS, Hill WJ, Gill DR. Acidosis in cattle: a review. J Anim Sci 76: 275-286, 1998.
39. Penner GB, Aschenbach JR, Gabel G, Oba M. Technical note: Evaluation of a continuous ruminal pH measurement system for use in noncan-nulated small ruminants. J Anim Sci 87: 2363-2366, 2009.
40. Penner GB, Aschenbach JR, 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: 1714-1720, 2009.
41. 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.
42. 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.
43. Penner GB, Taniguchi M, Guan LL, Beauchemin KA, Oba M. Effect of dietary forage to concentrate ratio on volatile fatty acid absorption and the expression of genes related to volatile fatty acid absorption and metabolism in ruminal tissue. J Dairy Sci 92: 2767-2781, 2009.
44. Rabbani I, Siegling-Vlitakis C, Noci B, Martens H. Evidence for NHE3-mediated Na transport in sheep and bovine forestomach. Am J Physiol Regul Integr Comp Physiol 301: R313-R319, 2011.
45. Rojen BA, Poulsen SB, Theil PK, Fenton RA, Kristensen NB. Effects of dietary nitrogen concentration on messenger RNA expression and protein abundance of urea transporter-B and aquaporins in ruminal papillae from lactating Holstein cows. J Dairy Sci 94: 2587-2591, 2011.
46. Schlau N, Guan LL, Oba M. The relationship between rumen acidosis resistance and expression of genes involved in regulation of intracellular pH and butyrate metabolism of ruminal epithelial cells in steers. J Dairy Sci 95: 5866-5875, 2012.
47. Schwaiger T, Beauchemin KA, Penner GB. The duration of time that beef cattle are fed a high-grain diet affects the recovery from a bout of ruminal acidosis: dry matter intake and ruminal fermentation. J Anim Sci 91: 5729-5742, 2013.
48. Schwaiger T, Beauchemin KA, Penner GB. Duration of time that beef cattle are fed a high-grain diet affects the recovery from a bout of ruminal acidosis: short-chain fatty acid and lactate absorption, saliva production, and blood metabolites. J Anim Sci 91: 5743-5753, 2013.
49. 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.
50. Sehested J, Diernaes L, Laverty G, Møller PD, Skadhauge E. Methodological and functional aspects of the isolated bovine rumen epithelium in Ussing chamber flux studies. Acta Agric Scand A 46: 76-86, 1996.
51. Sehested J, Diernaes L, Moller PD, Skadhauge E. Ruminal transport and metabolism of short-chain fatty acids (SCFA) in vitro: effect of SCFA chain length and pH. Comp Biochem Physiol A 123: 359-368, 1999.
52. Sehested J, Diernaes L, Moller PD, Skadhauge E. Transport of butyrate across the isolated bovine rumen epithelium—interaction with sodium, chloride and bicarbonate. Comp Biochem Physiol A 123: 399-408, 1999.
53. + transport across rumen epithelium of hay-fed sheep is acutely stimulated by the peptide IGF-1 in vitro. Exp Physiol 97: 497-505, 2012.
54. Shen Z, Seyfert HM, Lohrke B, Schneider F, Zitnan R, Chudy A, Kuhla S, Hammon HM, Blum JW, Martens H, Hagemeister H, Voigt J. An energy-rich diet causes rumen papillae proliferation associated with more IGF type 1 receptors and increased plasma IGF-1 concentrations in young goats. J Nutr 134: 11-17, 2004.
55. 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.
56. Steele MA, Dionissopoulos L, AlZahal O, Doelman J, McBride BW. Rumen epithelial adaptation to ruminal acidosis in lactating cattle involves the coordinated expression of insulin-like growth factor-binding proteins and a cholesterolgenic enzyme. J Dairy Sci 95: 318-327, 2012.
57. Stumpff F, Martens H, Bilk S, Aschenbach JR, Gabel G. Cultured ruminal epithelial cells express a large-conductance channel permeable to chloride, bicarbonate, and acetate. Pflügers Arch 457: 1003-1022, 2009.
58. Vasconcelos JT, Galyean ML. Nutritional recommendations of feedlot consulting nutritionists: the 2007 Texas Tech University survey. J Anim Sci 85: 2772-2781, 2007.
59. Waldron MR, Schrick FN, Quigley JD, Klotz JL, Saxton AM, Heit-mann RN. Volatile fatty acid metabolism by epithelial cells isolated from different areas of the ewe rumen. J Anim Sci 80: 270-278, 2002.
60. 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.
61. Wang YH, Xu M, Wang FN, Yu ZP, Yao JH, Zan LS, Yang FX. Effect of dietary starch on rumen and small intestine morphology and digesta pH in goats. Livestock Sci 122: 48-52, 2009.
62. Wilson DJ, Mutsvangwa T, Penner GB. Supplemental butyrate does not enhance the absorptive or barrier functions of the isolated ovine ruminal epithelia. J Anim Sci 90: 3153-3161, 2012.
63. + exchanger isoform 1 and 3 messenger RNA in rumen epithelium of goat. J Anim Sci 90: 307-317, 2012.
64. Zhang S, Albornoz RI, Aschenbach JR, Barreda DR, Penner GB. Short-term feed restriction impairs the absorptive function of the reticulo-rumen and total tract barrier function in beef cattle. J Anim Sci 91: 1685-1695, 2013.