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Ontogeny of flow-stimulated potassium secretion in rabbit cortical collecting duct: functional and molecular aspects

¹Division of Pediatric Nephrology, Department of Pediatrics Mount Sinai School of Medicine, New York 10029; ²Division of Nephrology and Hypertension, Department of Medicine, Winthrop University Hospital, Mineola, New York 11501; and ³Renal-Electrolyte Division, Department of Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania 15213

Submitted 19 May 2003 ; accepted in final form 13 June 2003

High urinary flow rates stimulate K secretion in the fully differentiated but not neonatal or weanling rabbit cortical collecting duct (CCD). Both small-conductance secretory K and high-conductance Ca²⁺/stretch-activated maxi-K channels have been identified in the apical membrane of the mature CCD by patch-clamp analysis. We reported that flow-stimulated net K secretion in the adult rabbit CCD is 1) blocked by TEA and charybdotoxin, inhibitors of intermediate- and high-conductance (maxi-K) Ca²⁺-activated K channels, and 2) associated with increases in net Na absorption and intracellular Ca²⁺ concentration ([Ca²⁺]_i). The present study examined whether the absence of flow-stimulated K secretion early in life is due to a 1) limited flow-induced rise in net Na absorption and/or [Ca²⁺]_i and/or 2) paucity of apical maxi-K channels. An approximately sixfold increase in tubular fluid flow rate in CCDs isolated from 4-wk-old rabbits and microperfused in vitro led to an increase in net Na absorption and [Ca²⁺]_i, similar in magnitude to the response observed in 6-wk-old tubules, but it failed to generate an increase in net K secretion. By 5 wk of age, there was a small, but significant, flow-stimulated rise in net K secretion that increased further by 6 wk of life. Luminal perfusion with iberiotoxin blocked the flow stimulation of net K secretion in the adult CCD, confirming the identity of the maxi-K channel in this response. Maxi-K channel -subunit message was consistently detected in single CCDs from animals 4 wk of age by RT-PCR. Indirect immunofluorescence microscopy using antibodies directed against the -subunit revealed apical labeling of intercalated cells in cryosections from animals 5 wk of age; principal cell labeling was generally intracellular and punctate. We speculate that the postnatal appearance of flow-dependent K secretion is determined by the transcriptional/translational regulation of expression of maxi-K channels. Furthermore, our studies suggest a novel function for intercalated cells in mediating flow-stimulated K secretion.

maxi-K channel; iberiotoxin; in vitro microperfusion; intracellular calcium concentration; mechanoregulation; development

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