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Am J Physiol Gastrointest Liver Physiol 278: G974-G980, 2000;
0193-1857/00 $5.00
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Vol. 278, Issue 6, G974-G980, June 2000

Gi-1/Gi-2-dependent signaling by single-transmembrane natriuretic peptide clearance receptor

K. S. Murthy, B.-Q. Teng, H. Zhou, J.-G. Jin, J. R. Grider, and G. M. Makhlouf

Departments of Physiology and Medicine, Medical College of Virginia, Virginia Commonwealth University, Richmond, Virginia 23298-0711

Single-transmembrane natriuretic peptide clearance receptor (NPR-C), which is devoid of a cytoplasmic guanylyl cyclase domain, interacts with pertussis toxin (PTx)-sensitive G proteins to activate endothelial nitric oxide synthase (eNOS) expressed in gastrointestinal smooth muscle cells. We examined the ability of NPR-C to activate other effector enzymes in eNOS-deficient tenia coli smooth muscle cells; these cells expressed NPR-C and NPR-B but not NPR-A. Atrial natriuretic peptide (ANP), the selective NPR-C ligand cANP-(4-23), and vasoactive intestinal peptide (VIP) inhibited 125I-ANP and 125I-VIP binding to muscle membranes in a pattern indicating high-affinity binding to NPR-C. Interaction of VIP with NPR-C was confirmed by its ability to inhibit 125I-ANP binding to membranes of NPR-C-transfected COS-1 cells. In tenia muscle cells, all ligands selectively activated Gi-1 and Gi-2; VIP also activated Gs via VIP2 receptors. All ligands stimulated phosphoinositide hydrolysis, which was inhibited by ANP-(1-11), PTx, and antibodies to phospholipase C-beta 3 (PLC-beta 3) and Gbeta . cANP-(4-23) contracted tenia muscle cells; contraction was blocked by U-73122 and PTx and by antibodies to PLC-beta 3 and Gbeta in intact and permeabilized muscle cells, respectively. VIP and ANP contracted muscle cells only after inhibition of cAMP- and cGMP-dependent protein kinases. ANP and cANP-(4-23) inhibited forskolin-stimulated cAMP in a PTx-sensitive fashion. We conclude that NPR-C is coupled to activation of PLC-beta 3 via beta gamma -subunits of Gi-1 and Gi-2 and to inhibition of adenylyl cyclase via alpha -subunits.

G protein; smooth muscle; vasoactive intestinal peptide; signal transduction; phosphoinositide metabolism; phospholipase C


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