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Electrogenic Cl− secretion does not occur in the ileum of the Australian common brushtail possum, Trichosurus vulpecula, due to low levels of expression of the NaK2Cl cotransporter, NKCC1

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Abstract

The colon of the brushtail possum does not have an electrogenic secretory response. Given the functional significance of electrogenic Cl− secretion in the intestine of eutherian mammals, we have investigated the secretory response in the small intestine of this marsupial. In the Ussing chamber cAMP-dependent secretagogues stimulated a sustained increase in ileal short-circuit current (Isc), whereas Ca2+-dependent secretagogues induced a transient increase. Both the responses were inhibited by mucosal addition of the anion channel blocker 5-nitro-2-(3-phenylpropylamino) benzoic acid (100 μmol l−1), consistent with an anion secretory response. However, the responses were not inhibited by serosal bumetanide (10 μmol l−1) and were independent of bath Cl−, indicating that the stimulated ileal Isc does not involve electrogenic Cl− secretion driven by the NaK2Cl cotransporter, NKCC1. Consistent with this, there were low levels of NKCC1 expression in the ileal epithelium. In particular, NKCC1 expression in the ileal crypt cells was comparable to that of the villous cells. This differs from eutherian mammals where high levels of NKCC1 expression in the ileal crypt cells are associated with their role in Cl− secretion. The cAMP- and Ca2+-dependent secretory responses were inhibited by the removal of HCO3 − suggesting that these responses were due to electrogenic HCO3 − secretion. We conclude that the ileum of the possum does not secrete Cl− due to low levels of NKCC1 expression. It does however appear to secrete HCO3 −. These results are further significant examples of differences in the transport function of the possum intestinal epithelium compared with eutherian mammals.

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Acknowledgments

We thank Sonya Mathieson for excellent technical assistance and Euan Thompson for the collection and maintenance of the possums. This work was supported by a University of Otago Research Grant, and grants from the Foundation for Research Science and Technology, the Animal Health Board Inc., and the National Centre for Possum Biocontrol.

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Authors and Affiliations

  1. Department of Physiology, School of Medical Sciences, University of Otago, PO Box 913, Dunedin, 9054, New Zealand

    Natalie Harfoot, Mike Gill & A. Grant Butt

  2. Invermay Agricultural Centre, AgResearch, Private Bag 50034, Mosgiel, 9024, New Zealand

    Ray C. Bartolo, Kristy Demmers & Bernie McLeod

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  1. Ray C. Bartolo
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  2. Natalie Harfoot
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  3. Mike Gill
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Correspondence to A. Grant Butt.

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Communicated by I. D. Hume.

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Bartolo, R.C., Harfoot, N., Gill, M. et al. Electrogenic Cl− secretion does not occur in the ileum of the Australian common brushtail possum, Trichosurus vulpecula, due to low levels of expression of the NaK2Cl cotransporter, NKCC1. J Comp Physiol B 179, 997–1010 (2009). https://doi.org/10.1007/s00360-009-0379-8

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