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Epithelia of the ovine and bovine forestomach express basolateral maxi-anion channels permeable to the anions of short-chain fatty acids

  • Ion channels, receptors and transporters
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Abstract

It has long been established that the absorption of short-chain fatty acids (SCFA) across epithelia stimulates sodium proton exchange. The apically released protons are not available as countercations for the basolateral efflux of SCFA anions and a suitable transport model is lacking. Patch clamp and microelectrode techniques were used to characterize an anion conductance expressed by cultured cells of the sheep and bovine rumen and the sheep omasum and to localize the conductance in the intact tissue. Cells were filled with a Na-gluconate solution and superfused with sodium salts of acetate, propionate, butyrate, or lactate. Reversal potential rose and whole cell current at +100 mV decreased with the size of the anion. Anion-induced currents could be blocked by diisothiocyanato-stilbene-2,2′-disulfonic acid (DIDS), NPPB (200 μmol l−1), or pCMB (1 mmol l−1). In patches of bovine ruminal cells, single channels were observed with a conductance for chloride (327 ± 11 pS), acetate (115 ± 8 pS), propionate (102 ± 10 pS), butyrate (81 ± 2 pS), and gluconate (44 ± 3 pS). Channels expressed by sheep rumen and omasum were similar. Microelectrode experiments suggest basolateral localization. In conclusion, forestomach epithelia express basolateral maxi-anion channels with a permeability sequence of chloride > acetate > propionate > butyrate. SCFA absorption may resemble functionally coupled transport of NaCl, with the Na+/K+-ATPase driving the basolateral efflux of the anion through a channel. Since protons are apically extruded, the model accurately predicts that influx of buffers with saliva is essential for the pH homeostasis of the ruminant forestomach.

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Acknowledgments

The expert technical assistance of Gisela Manz and Susanne Trappe is gratefully acknowledged. This study was generously supported by the Margarete Markus Charity and by the Schaumann Foundation.

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  1. Institute of Veterinary Physiology, Department of Veterinary Medicine, Freie Universität Berlin, Oertzenweg 19b, 14163, Berlin, Germany

    Maria I. Georgi, Julia Rosendahl, Franziska Ernst, Jörg R. Aschenbach, Holger Martens & Friederike Stumpff

  2. Institute of Clinical Physiology, Charité Berlin, Campus Benjamin Franklin, Berlin, Germany

    Dorothee Günzel

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  1. Maria I. Georgi
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Georgi, M.I., Rosendahl, J., Ernst, F. et al. Epithelia of the ovine and bovine forestomach express basolateral maxi-anion channels permeable to the anions of short-chain fatty acids. Pflugers Arch - Eur J Physiol 466, 1689–1712 (2014). https://doi.org/10.1007/s00424-013-1386-x

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