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MEMBRANE TRANSPORTERS, ION CHANNELS, AND PUMPS

Interactions between Na⁺ channels and Na⁺-HCO₃^– cotransporters in the freshwater fish gill MR cell: a model for transepithelial Na⁺ uptake

Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada

Submitted 2 December 2005 ; accepted in final form 24 September 2006

Isolated mitochondria-rich (MR) cells from the rainbow trout gill epithelium were subjected to intracellular pH (pH_i) imaging with the pH-sensitive dye BCECF-AM. MR cells were categorized into two distinct functional subtypes based on their ability to recover pH_i from an NH₄Cl-induced acidification in the absence of Na⁺. An apparent link between resting pH_i and Na⁺-independent pH_i recovery was made. We observed a unique pH_i acidification event that was induced by extracellular Na⁺ addition. This further classified the mixed MR cell population into two functional subtypes: the majority of cells (77%) demonstrated the Na⁺-induced pH_i acidification, whereas the minority (23%) demonstrated an alkalinization of pH_i under the same circumstances. The focus of this study was placed on the Na⁺-induced acidification and pharmacological analysis via the use of amiloride and phenamil, which revealed that Na⁺ uptake was responsible for the intracellular acidification. Further experiments revealed that pH_i acidification could be abolished when Na⁺ was allowed entry into the cell, but the activity of an electrogenic Na⁺-HCO₃^– cotransporter (NBC) was inhibited by DIDS. The electrogenic NBC activity was supported by a DIDS-sensitive, Na⁺-induced membrane potential depolarization as observed via imaging of the voltage-sensitive dye bis-oxonol. We also demonstrated NBC immunoreactivity via Western blotting and immunohistochemistry in gill tissue. We propose a model for transepithelial Na⁺ uptake occurring via an apical Na⁺ channel linked to a basolateral, electrogenic NBC in one subpopulation of MR cells.

epithelial sodium channels; sodium-induced acidification; amiloride; phenamil; DIDS; acid-base; peanut lectin agglutinin binding; membrane potential; BCECF-AM; bis-oxonol; ion uptake

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