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The dopamine transporter (DAT) terminates dopamine (DA) neurotransmission by reuptake of DA into presynaptic neurons. Regulation of DA uptake by D₂ dopamine receptors (D₂R) has been reported. The high affinity of DA and other DAT substrates for the D₂R, however, has complicated investigation of the intracellular mechanisms mediating this effect. The present studies used the fluorescent DAT substrate, 4-[4-(diethylamino)-styryl]-N-methylpyridinium iodide (ASP⁺) with live cell imaging techniques to identify the role of two D₂R-linked signaling pathways, extracellular signal-regulated kinases 1 and 2 (ERK1/2), and phosphoinositide 3 kinase (PI3K) in mediating D₂R regulation of DAT. Addition of the D₂/D₃ receptor agonist quinpirole (0.1–10 μM) to human embryonic kidney cells coexpressing human DAT and D₂ receptor (short splice variant, D_2SR) induced a rapid, concentration-dependent and pertussis …