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J Biol Chem, Vol. 274, Issue 16, 10927-10935, April 16, 1999

Cyclic GMP-dependent Protein Kinase Activates Cloned BK_Ca Channels Expressed in Mammalian Cells by Direct Phosphorylation at Serine 1072

From the Department of Physiology and Cell Biology, University of Nevada School of Medicine, Reno, Nevada 89557

NO-induced activation of cGMP-dependent protein kinase (PKG) increases the open probability of large conductance Ca²⁺-activated K⁺ channels and results in smooth muscle relaxation. However, the molecular mechanism of channel regulation by the NO-PKG pathway has not been determined on cloned channels. The present study was designed to clarify PKG-mediated modulation of channels at the molecular level. The cDNA encoding the -subunit of the large conductance Ca²⁺-activated K⁺ channel, cslo-, was expressed in HEK293 cells. Whole cell and single channel characteristics of cslo- exhibited functional features of native large conductance Ca²⁺-activated K⁺ channels in smooth muscle cells. The NO-donor sodium nitroprusside increased outward current 2.3-fold in whole cell recordings. In cell-attached patches, sodium nitroprusside increased the channel open probability (NPo) of cslo- channels 3.3-fold without affecting unitary conductance. The stimulatory effect of sodium nitroprusside was inhibited by the PKG-inhibitor KT5823. Direct application of PKG-I to the cytosolic surface of inside-out patches increased NPo 3.2-fold only in the presence of ATP and cGMP without affecting unitary conductance. A point mutation of cslo- in which Ser-1072 (the only optimal consensus sequence for PKG phosphorylation) was replaced by Ala abolished the PKG effect on NPo in inside-out patches and the effect of SNP in cell attached patches. These results indicate that PKG activates cslo- by direct phosphorylation at serine 1072.

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