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Am J Physiol Gastrointest Liver Physiol 284: G68-G74, 2003; doi:10.1152/ajpgi.00113.2002
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Vol. 284, Issue 1, G68-G74, January 2003

Regulation of atrial natriuretic peptide secretion by cholinergic and PACAP neurons of the gastric antrum

William R. Gower Jr.1,3,5,6, John R. Dietz4,6, Robert W. McCuen9, Peter J. Fabri2,5, Ethan A. Lerner7, and Mitchell L. Schubert8,9

1 Laboratory and 2 Surgery Services, James A. Haley Veterans Administration Hospital; Departments of 3 Biochemistry and Molecular Biology, 4 Physiology and Biophysics, and 5 Surgery, University of South Florida; and 6 University of South Florida Cardiac Hormone Center, Tampa, Florida 33612; 7 Department of Dermatology, Harvard Medical School, Charlestown, Massachusetts 02129; and 8 Department of Medicine, Medical College of Virginia/Virginia Commonwealth University, and 9 McGuire Veterans Administration Hospital, Richmond, Virginia 23249

Atrial natriuretic peptide (ANP) released from enterochromaffin cells helps regulate antral somatostatin secretion, but the mechanisms regulating ANP secretion are not known. We superfused rat antral segments with selective neural agonists/antagonists to identify the neural pathways regulating ANP secretion. The nicotinic agonist 1,1-dimethyl-4-phenylpiperazinium (DMPP) stimulated ANP secretion; the effect was abolished by hexamethonium but doubled by atropine. Atropine's effect implied that DMPP activated concomitantly cholinergic neurons that inhibit and noncholinergic neurons that stimulate ANP secretion, the latter effect predominating. Methacholine inhibited ANP secretion. Neither bombesin nor vasoactive intestinal polypeptide stimulated ANP secretion, whereas pituitary adenylate cyclase-activating polypeptide (PACAP)-27, PACAP-38, and maxadilan [PACAP type 1 (PAC1) agonist] each stimulated ANP secretion. The PAC1 antagonist M65 1) abolished PACAP-27/38-stimulated ANP secretion; 2) inhibited basal ANP secretion by 28 ± 5%, implying that endogenous PACAP stimulates ANP secretion; and 3) converted the ANP response to DMPP from 109 ± 21% above to 40 ± 5% below basal, unmasking the cholinergic component and indicating that DMPP activated PACAP neurons that stimulate ANP secretion. Combined atropine and M65 restored DMPP-stimulated ANP secretion to basal levels. ANP secretion in the antrum is thus regulated by intramural cholinergic and PACAP neurons; cholinergic neurons inhibit and PACAP neurons stimulate ANP secretion.

stomach; methacholine; 1,1-dimethyl-4-phenylpiperazinium; atropine; enterochromaffin; hormone; peptide; enteric nervous system; pituitary adenylate cyclase-activating peptide


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