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Luminal hyperosmolarity decreases Na transport and impairs barrier function of sheep rumen epithelium

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Abstract

The effects of luminal hyperosmolarity on Na and Cl transport were studied in rumen epithelium of sheep. An increase of luminal osmotic pressure with mannitol (350 and 450 mosm/l) caused a significant increase of tissue conductance, G T, which is linearly correlated with flux rates of 51Cr-EDTA and indicates an increase of passive permeability. Studies with microelectrodes revealed, that an increase of the osmotic pressure caused a significant increase of the conductance of the shunt pathway from 1.23±0.10 (control) to 1.92±0.14 mS cm−2 (450 mosm/l) without a change of fractional resistance. Hyperosmolarity significantly increased J sm and reduced J net Na. The effect of hyperosmolarity on J ms Na is explained by two independent and opposed effects: increase of passive permeability and inhibition of the Na+/H+ exchanger. Hypertonic buffer solution induced a decrease of the intracellular pH (pHi) of isolated ruminal cells, which is consistent with an inhibition of Na+/H+ exchange, probably isoform NHE-3, because NHE-3-mRNA was detectable in rumen epithelium. These data are in contrast to previous reports and reveal a disturbed Na transport and an impaired barrier function of the rumen epithelium, which predisposes translocation of rumen endotoxins and penetration of bacteria.

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Abbreviations

I sc :

Short circuit current in μeq cm−2 h−1

J ms :

Mucosal to serosal flux in μeq cm−2 h−1

J sm :

Serosal to mucosal flux in μeq cm−2 h−1

J net :

Jms −Jsm in μeq cm−2 h−1

NHE:

Na+/H+ exchanger

NHERF:

Na+/H+ exchanger regulatory factor

G :

Conductance in mS cm−2

G T :

Conductance of the epithelium

G a,b,p :

Conductance of the apical, basolateral membrane or the paracellular pathway

G c :

Conductance of the epithelial cell

ROP:

Ruminal osmotic pressure in mosm/l

hyperROP:

Hypertonic ruminal osmotic pressure

SCFA:

Short chain fatty acids

PDt :

Transepithelial potential difference in mV

PDa :

Potential difference of the apical membrane in mV

fRa :

Fractional resistance = ΔPDa/ΔPDt)

REL:

Resistance of the (micro)electrode in Ohm

R t :

Resistance of the epithelium in cm2

R a :

Resistance of the apical membrane in Ω cm2

R b :

Resistance of the basolateral membrane in Ω cm2

R p :

Resistance of the paracellular pathway in Ω cm2

REC:

Rumen epithelial cells

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Acknowledgements

we gratefully acknowledge the expert technical assistance of Katharina Wolf and the valuable assistance of Sophie Heipertz. Thanks to Dr. H.-J. Lang (HMR-Germany GmbH, Frankfurt a. Main, Germany) for kindly providing us with HOE 694 and S3226. This study was supported by the Schaumann Foundation (scholarship Almut Böttcher, and M. Freyer) and the Margarete-Markus-Charity.

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Authors and Affiliations

  1. Department of Veterinary Physiology, Faculty of Veterinary Medicine, Free University of Berlin, Oertzenweg 19b, 14163, Berlin, Germany

    Markus Freyer, Sabine Leclercq, Benjamin Etschmann, Ulrike Lodemann, Almut Böttcher & Holger Martens

  2. Forschungsinstitut für die Biologie landwirtschaftlicher Nutztiere–FBN, Forschungsbereich Ernährungsphysiologie “Oskar Kellner”, Wilhelm-Stahl-Allee 2, 18196, Dummerstorf, Germany

    Monika Schweigel

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  1. Monika Schweigel
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Correspondence to Holger Martens.

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Communicated by G. Heldmaier

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Schweigel, M., Freyer, M., Leclercq, S. et al. Luminal hyperosmolarity decreases Na transport and impairs barrier function of sheep rumen epithelium. J Comp Physiol B 175, 575–591 (2005). https://doi.org/10.1007/s00360-005-0021-3

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  • DOI: https://doi.org/10.1007/s00360-005-0021-3

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