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First published online April 8, 2004
Journal of Experimental Biology 207, 1655-1663 (2004)
Published by The Company of Biologists 2004
doi: 10.1242/jeb.00932

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Mechanisms of K⁺ transport across basolateral membranes of principal cells in Malpighian tubules of the yellow fever mosquito, Aedes aegypti

Brett N. Scott, Ming-Jiun Yu, Lenora W. Lee and Klaus W. Beyenbach^*

Department of Biomedical Sciences, Cornell University, Ithaca, NY 14853, USA

^* Author for correspondence (e-mail: kwb1{at}cornell.edu)

Accepted 12 February 2004

The mechanisms of K⁺ entry from the hemolymph into principal cells of Malpighian tubules were investigated in the yellow fever mosquito, Aedes aegypti. The K⁺ channel blocker Ba²⁺ (5 mmol l^–1) significantly decreased transepithelial (TEP) fluid secretion (V_s) from 0.84 nl min^–1 to 0.37 nl min^–1 and decreased the K⁺ concentration in secreted fluid from 119.0 mmol l^–1 to 54.3 mmol l^–1 with no change in the Cl^– concentration. Even though the Na⁺ concentration increased significantly from 116.8 mmol l^–1 to 144.6 mmol l^–1, rates of TEP ion secretion significantly decreased for all three ions. In addition, Ba²⁺ had the following significant electrophysiological effects: it depolarized the TEP voltage (V_t) from 19.4 mV to 17.2 mV, increased the TEP resistance (R_t) from 6.4 kcm to 6.9 kcm, hyperpolarized the basolateral membrane voltage of principal cells (V_bl) from –75.2 mV to –88.2 mV and increased the cell input resistance from 363.7 k to 516.3 k. These effects of Ba²⁺ reflect the block of K⁺ channels that, apparently, are also permeable to Na⁺. Bumetanide (100 µmol l^–1) had no effect on TEP fluid secretion and electrical resistance but significantly decreased TEP K⁺ secretion, consistent with the inhibition of electroneutral Na⁺/K⁺/2Cl^– cotransport. TEP Na⁺ secretion significantly increased because other Na⁺ entry pathways remained active. Bumetanide plus Ba²⁺ completely inhibited TEP electrolyte and fluid secretion, with fast and slow kinetics reflecting the Ba²⁺ block of basolateral membrane K⁺ channels and the inhibition of Na⁺/K⁺/2Cl^– cotransport, respectively. The single and combined effects of Ba²⁺ and bumetanide suggest that (1) K⁺ channels and Na⁺/K⁺/2Cl^– cotransport are the primary mechanisms for bringing K⁺ into cells, (2) K⁺ channels mediate a significant Na⁺ influx, (3) Na⁺ has as many as four entry pathways and (4) the mechanisms of TEP K⁺ and Na⁺ secretion are coupled such that complete block of TEP K⁺ renders the epithelium unable to secrete Na⁺.

Key words: transepithelial Na⁺ secretion, transepithelial K⁺ secretion, transepithelial Cl^– secretion, barium block, K⁺ channel, bumetanide, Na⁺/K⁺/2Cl^– cotransport, basolateral membrane voltage, cell input resistance, transepithelial voltage, transepithelial resistance

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