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The Journal of Experimental Biology 206, 233-243 (2003)
doi: 10.1242/jeb.00066

The dependence of electrical transport pathways in Malpighian tubules on ATP

Daniel S. Wu and Klaus W. Beyenbach^*

Department of Biomedical Sciences, VRT 8014, Cornell University, Ithaca, NY 14853, USA

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

Accepted 10 October 2002

The relationship between the intracellular ATP concentration [ATP]_i and the electrical properties of principal cells was investigated in Malpighian tubules of the yellow fever mosquito, Aedes aegypti. Under control conditions, [ATP]_i was 0.91 mmol l^-1, the input resistance of the principal cell (R_pc) was 334.1 k, and the basolateral membrane was marked by a large K⁺-conductance and a membrane voltage (V_bl) of -75.8 mV. Peritubular cyanide (CN, 0.3 mmol l^-1) reduced [ATP]_i to 0.08 mmol l^-1 in less than 2 min; however, V_bl dropped to -8 mV and R_pc increased to 3150.8 k in 8 min, while the K⁺-conductance of the basolateral membrane disappeared. Upon washout of CN, V_bl and R_pc returned to control values within 2 min, and the basolateral membrane recovered its K⁺-conductance. The recovery of normal [ATP]_i took 15 min. Dose-dependence and EC₅₀ values for the CN-inhibition of V_bl and the increase in R_pc were strikingly similar (184.0 µmol l^-1 and 164.4 µmol l^-1). Similar effects of metabolic inhibition were observed with dinitrophenol (DNP), but the EC₅₀ values were 50.3 µmol l^-1 and 71.7 µmol l^-1 for the effects on V_bl and R_pc, respectively. Barium, a blocker of K⁺-channels, significantly hyperpolarized V_bl to -89.1 mV and increased R_pc to 769.4 k under control conditions, but had no effects during metabolic inhibition. These results illustrate a temporal relationship between [ATP]_i and electrogenic and conductive transport pathways in principal cells that is consistent with the role of ATP as an integrator of transport steps at apical and basolateral membranes of the cell. When [ATP]_i drops to levels that are 10% of control, the V-type H⁺-ATPase is inhibited, preventing the extrusion of K⁺ to the tubule lumen. At the same time, basolateral membrane K⁺-channels close, preventing the entry of K⁺ from the hemolymph. Intracellular K⁺ homeostasis is thus protected during metabolic inhibition, allowing the cell to re-establish K⁺ transport when ATP is synthesized again.

Key words: Malphigian tubule, ATP, yellow fever mosquito, Aedes aegypti, metabolism, electrogenic transport, electroconductive transport

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