Nicotinic signaling stimulates glucagon secretion in mouse and human pancreatic α-cells

Diabetes. 2024 Oct 30:db230809. doi: 10.2337/db23-0809. Online ahead of print.

Abstract

Smoking is widely regarded as a risk factor for type 2 diabetes, as nicotine contributes to insulin resistance by desensitizing the insulin receptors in muscle, liver, or fat. Little is known, however, about the immediate regulation of islet hormonal output by nicotine, an agonist of ionotropic cholinergic receptors. We investigated this by imaging cytosolic Ca2+ dynamics in mouse and human islets using confocal microscopy and measuring glucagon secretion in response to the alkaloid from isolated mouse islets. Nicotine acutely stimulated cytosolic Ca2+ in glucagon-secreting α-cells but not in insulin-secreting β-cells. The 2.8±0.5-fold (p<0.05) increase in the Ca2+, observed in >70% of α-cells, correlated well with a 2.5±0.3-fold stimulation of glucagon secretion. Nicotine-induced elevation of cytosolic Ca2+ relied on the influx from the extracellular compartment rather than the release of the cation from intracellular depots. Metabotropic cholinergic signaling, monitored at the level of intracellular diacylglycerol, was limited to 69% of α-cells vs 94% of β-cells. We conclude that parasympathetic regulation of pancreatic islet hormone release utilizes different signaling pathways in β- (metabotropic) and α-cells (metabotropic and ionotropic), resulting in the finetuning of the ACh-induced glucagon exocytosis. Sustained nicotinic stimulation is, therefore, likely to attenuate insulin sensitivity by increasing glucagon release.