Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-23T05:13:20.888Z Has data issue: false hasContentIssue false
  • English
  • Français

Effect of ammonia on Na+ transport across isolated rumen epithelium of sheep is diet dependent

Published online by Cambridge University Press:  09 March 2007

Khalid Abdoun ,
Katarina Wolf ,
Gisela Arndt  and
Holger Martens
Khalid Abdoun
Affiliation:
Department of Physiology, Faculty of Veterinary Sciences, University of Khartoum, Khartoum, Sudan
Katarina Wolf
Affiliation:
Institute of Veterinary Physiology, Free University of Berlin, Oertzenweg 19b, 14163 Berlin, Germany
Gisela Arndt
Affiliation:
Department of Biometrics and Statistics, Free University of Berlin, Berlin, Germany
Holger Martens*
Affiliation:
Institute of Veterinary Physiology, Free University of Berlin, Oertzenweg 19b, 14163 Berlin, Germany
*
*Corresponding author: Dr H. Martens, fax +49 30 8386 2610, email [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

The cellular uptake of ammonia affects the intracellular pH (pHi) of polar and non-polar cells. A predominant uptake of NH3 and its intra-cellular protonation tend to alkalinise the cytoplasm, whereas a predominant uptake of NH4+ acidifies the cytoplasm by reversing this reaction. Hence, the well-known absorption of ammonia across the rumen epithelium probably causes a change in the pHi. The magnitude and direction of this change in pHi (acid or alkaline) depends on the relative transport rates of NH3 and NH4+. Consequently, the intra-cellular availability of protons will influence the activity of the Na+-H+ exchanger, which could affect transepithelial Na+ transport. The aim of the present study has been to test this possible interaction between ruminal ammonia concentrations and Na+ transport. The term ammonia is used to designate the sum of the protonated (NH4+) and unprotonated (NH3) forms. Isolated ruminal epithelium of sheep was investigated by using the Ussing-chamber technique in vitro. The present results indicate that ammonia inhibits Na+ transport across the rumen epithelium of hay-fed sheep, probably by binding intracellular protons and thus inhibiting Na+-H+ exchange. By contrast, ammonia stimulates Na+ transport in concentrate-fed and urea-fed sheep, which develop an adaptation mechanism in the form of an increased metabolism of ammonia in the rumen mucosa and/or an increased permeability of rumen epithelium to the charged ammonium ion (NH4+). Intracellular dissociation of NH4+ increases the availability of protons, which stimulate Na+ –H+ exchange. This positive effect of ruminal ammonia on Na+ absorption may significantly contribute to the regulation of osmotic pressure of the ruminal fluid, because intraruminal ammonia concentrations up to 40 mmol/l have been reported.

Keywords

RumenSheepNa+ transportAmmonia
Type
Research Article
Information
British Journal of Nutrition , Volume 90 , Issue 4 , October 2003 , pp. 751 - 758
Copyright
Copyright © The Nutrition Society 2003

References

Abdoun, K & Martens, H (1999) Effect of ammonia on Na transport across the ruminal epithelium of sheep in vitro. Proc Soc Nutr Physiol 8, 87 Abstr.Google Scholar
Aronson, PS, Nee, J & Suhm, MA (1982) Modifier role of internal H+ in activating the Na+-H+ exchanger in renal microvillus membrane vesicles. Nature 299, 161–163.CrossRefGoogle Scholar
Baldwin, RL (1999) The proliferative actions of insulin, insulin-like growth factor-I, epidermal growth factor, butyrate and propionate on ruminal epithelial cells in vitro. Small Rum Res 32, 261–278.CrossRefGoogle Scholar
Bennink, MR, Tayler, RT, Ward, GM & Johnson, DE (1978) Ionic milieu of bovine and ovine rumen as affected by diet. J Dairy Sci 61, 315–323.CrossRefGoogle ScholarPubMed
Bödeker, D & Kemkowski, J (1996) Participation of NH4+ in total ammonia absorption across the rumen epithelium of sheep (Ovis aries). Comp Biochem Physiol A Physiol 114, 305–310.CrossRefGoogle ScholarPubMed
Bödeker, D, Shen, Y, Kemkowski, J & Höller, H (1992) Influence of short-chain fatty acids on ammonia absorption across the rumen wall of sheep. Exp Physiol 77, 369–376.CrossRefGoogle Scholar
Bödeker, D, Winkler, A & Höller, H (1990) Ammonia absorption from the isolated reticulo-rumen in sheep. Exp Physiol 75, 587–595.CrossRefGoogle Scholar
Burckhardt, BC & Frömter, E (1992) Pathways of NH3/NH4+ permeation across Xenopus laevis oocyte cell membrane. Eur J Physiol 420, 83–86.CrossRefGoogle ScholarPubMed
Care, AD, Brown, RC, Farrar, AR & Pickard, DW (1984) Magnesium absorption from the digestive tract of sheep. Q J Exp Physiol 69, 577–587.CrossRefGoogle ScholarPubMed
Carter, RR & Grovum, LW (1990) A review of the physiological significance of hypertonic body fluid on feed intake and ruminal function: Salivation, motility and microbes. J Anim Sci 68, 2811–2832.CrossRefGoogle ScholarPubMed
Dirksen, G, Liebich, HG, Brosi, G, Hagemeister, H & Mayer, E (1984) Morphologie der Pansenschleimhaut und Fettsäurere-sorption beim Rind – Bedeutende Faktoren für Gesundheit und Leistung (Morphology of the rumen mucosa and fatty acid absorption in cattle – important factors for health and production). Zentralbl Veterinärmed A 31, 414–430.CrossRefGoogle ScholarPubMed
Dobson, A, Sellers, AF & Gatewood, VH (1976) Absorption and exchange of water across rumen epithelium. Am J Physiol 231, 1588–1594.CrossRefGoogle ScholarPubMed
Gäbel, G, Galfi, P, Neogrady, S & Martens, H (1996) Characterisation of Na+/H+ exchange in sheep rumen epithelial cells kept in primary culture. Zentralbl Veterinärmed A 43, 365–375.CrossRefGoogle ScholarPubMed
Gäbel, G & Martens, H (1986) The effect of ammonia on magnesium metabolism in sheep. J Anim Physiol Anim Nutr 55, 278–287.CrossRefGoogle Scholar
Gäbel, G, Martens, H, Suendermann, M & Galfi, P (1987) The effect of diet, intraruminal pH and osmolarity on sodium, chloride and magnesium absorption from the temporarily isolated and washed reticulo-rumen of the sheep. Q J Exp Physiol 118A, 367–374.Google Scholar
Head, MJ & Rook, JA (1955) Hypomagnesaemia in dairy cattle and its possible relationship to ruminal ammonia production. Nature 176, 262–263.CrossRefGoogle ScholarPubMed
Heitzmann, D, Warth, R, Bleich, M, Henger, A, Nitschke, R & Greger, R (2000) Regulation of the Na+ 2Cl- K+ cotransporter in isolated rat colon crypts. Eur J Physiol 439, 378–384.Google ScholarPubMed
Hoshino, S, Sarumaru, K & Morimoto, K (1966) Ammonia anabolism in ruminants. J Dairy Sci 49, 1523–1528.CrossRefGoogle Scholar
Kikeri, D, Sun, A, Zeidel, ML & Hebert, SC (1992) Cellular NH4+/ K+ transport pathways in mouse medullary thick limb of Henle. J Gen Physiol 99, 435–461.CrossRefGoogle ScholarPubMed
Leonhard-Marek, S, Marek, M & Martens, H (1998) Effect of transmural potential difference on Mg transport across rumen epithelium from different breeds of sheep. J Agric Sci 130, 241–247.CrossRefGoogle Scholar
McLaren, GA, Anderson, GC, Martin, WG & Cooper, WK (1961) Fixation of ammonia nitrogen by rumen mucosa. J Anim Sci 20, 942–943.Google Scholar
Martens, H, Gäbel, G & Strozyk, H (1987) The effect of potassium and the transmural potential difference on magnesium transport across an isolated preparation of sheep rumen epithelium. Q J Exp Physiol 72, 181–188.CrossRefGoogle ScholarPubMed
Martens, H, Gäbel, G & Strozyk, B (1991) Mechanism of electrically silent Na+ and Cl- transport across the rumen epithelium of sheep. Exp Physiol 76, 103–114.CrossRefGoogle ScholarPubMed
Martens, H, Kudritzki, J, Wolf, K & Schweigel, M (2001) No evidence for active peptide transport in forestomach epithelia of sheep. J Anim Physiol Anim Nutr 85, 314–324.CrossRefGoogle ScholarPubMed
Martens, H & Rayssiguier, Y (1980) Magnesium metabolism and hypomagnesaemia. In Digestive Physiology and Metabolism in Ruminants, pp. 447–466 [Ruckebusch, Y and Thivend, P, editors]. Lancaster, UK: MTP Press Ltd.CrossRefGoogle Scholar
Martens, H & Schweigel, M (2000) Grass tetany and other hypomagnesaemias. In Veterinary Clinics of North America: Food Animal Practice: Metabolic Disorders of Ruminants, Vol. 16, pp. 339–368 [Herdt, T, editor]. Philadelphia, PA: Saunders.Google Scholar
Morris, JG & Payne, E (1970) Ammonia and urea toxicoses in sheep and their relation to dietary nitrogen intake. J Agric Sci 74, 259–271.CrossRefGoogle Scholar
Müller, F, Aschenbach, JR & Gäbel, G (2000) Role of Na+/H+exchange and HCO3- transport in [pHi]recovery from intra-cellular acid load in cultured epithelial cells of sheep rumen. J Comp Physiol B 170, 337–343.Google Scholar
Musch, MW, Bookstein, C, Xie, Y, Sellin, JH & Chang, EB (2001) SCFA increase intestinal Na absorption by induction of NHE3 in rat colon and human intestinal C2/bbe cells. Am J Physiol 280, G687–G693.Google ScholarPubMed
Nagaraja, TN & Brookes, N (1998) Intracellular acidification induced by passive and active transport of ammonium ions in astrocytes. Am J Physiol 274, C883–C891.CrossRefGoogle ScholarPubMed
Nocek, JE, Herbein, JH & Polan, CE (1980) Influence of ration physical form, ruminal degradable nitrogen and age on rumen epithelial propionate and acetate transport and some enzymatic activities. J Nutr 110, 2355–2364.CrossRefGoogle ScholarPubMed
Remond, D, Chaise, JP, Delval, E & Poncet, C (1993) Net transfer of urea and ammonia across the ruminal wall of sheep. J Anim Sci 71, 2785–2792.CrossRefGoogle ScholarPubMed
Sakata, T & Tamate, H (1978) Rumen epithelial cell proliferation accelerated by rapid increase in intraruminal butyrate. J Dairy Sci 61, 1109–1113.CrossRefGoogle ScholarPubMed
Schweigel, M, Vormann, H & Martens, H (2000) Mechanisms of Mg2+ transport cultured epithelial cells. Am J Physiol 278, G400–G408.Google Scholar
Warner, ACI & Stacy, BD (1977) Influence of ruminal and plasma osmotic pressure on salivary secretion in sheep. Q J Exp Physiol 62, 133–141.CrossRefGoogle ScholarPubMed
Zanming, S, Seifert, H-M, Löhrke, B, et al. (2002) Effects of diet on rumen papillae development is mediated by IGF-1. Proc Soc Nutr Physiol 11, 29 Abstr.Google Scholar