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Regulation and identity of intracellular calcium stores involved in membrane cross talk in the early distal tubule of the frog kidney

¹School of Biomedical Sciences, Worsley Building, University of Leeds, Leeds, West Yorkshire LS2 9NQ; and ²Department of Biomedical Science, The University of Sheffield, Western Bank, Sheffield S10 2TN, United Kingdom

Submitted 18 July 2003 ; accepted in final form 9 February 2004

The early distal tubule (EDT) of the frog nephron, similar to the thick ascending limb in mammals, mediates the transepithelial absorption of NaCl. The continued absorption of NaCl in the face of varying Na⁺ load is maintained by coordination of the activity of ion-transporting proteins in the apical and basolateral membranes, so-called pump-leak coupling. Previous studies identified intracellular Ca²⁺, originating from an intracellular Ca²⁺ store, as playing a key role in pump-leak coupling in the EDT (Cooper GJ, Fowler MR, and Hunter M. Pflügers Arch 442: 243–247, 2001). The purpose of the experiments described in this paper was to identify the intracellular Ca²⁺ storage pools in the renal diluting segment. Store Ca²⁺ movements were monitored by the fluorescence of mag-fura 2 in permeabilized segments of frog EDTs. The presence of both ATP and Ca²⁺ was required to maintain store Ca²⁺ content. Removal of either of these substrates resulted in a passive leak of Ca²⁺ from the stores. The uptake of Ca²⁺ into the store was sensitive to the SERCA inhibitor 2,5-di(tert-butyl) hydroquinone, whereas Ca²⁺ release from the store was stimulated by IP₃ but not cADPR. Store Ca²⁺ was insensitive to the mitochondrial ATP synthase inhibitor oligomycin, and, under conditions that energized _m, the complex 1 inhibitor rotenone and the protonophore FCCP. Ionomycin was able to mobilize store Ca²⁺ following exposure to IP₃. These results suggest that the endoplasmic reticulum is a dominant Ca²⁺ store in the frog EDT. A second pool, sensitive to ionomycin but not IP₃, may overlap with the IP₃-sensitve pool. The data also rule out any contribution by mitochondria to EDT Ca²⁺ cycling.

pump-leak coupling; permeability

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