Acetylcholine and Malpighian tubules of the kissing bug, Rhodnius prolixus: Evidence for expression of the non-neuronal cholinergic system and a diuretic action of acetylcholine

Acetylcholine (ACh) and its signaling pathways are expressed in peripheral tissues in mammals, leading to the concept of a non-neuronal cholinergic signaling system. This non-neuronal ACh is now known to participate as an autocrine/paracrine in many processes, including transport of ions and water, immunity, and reproduction. Non-neuronal cholinergic signaling in insects has only recently been explored, with transcriptome analyses disclosing the presence of transcripts for pivotal components of the cholinergic system in non-neuronal tissues, including Malpighian tubules (MTs), ovaries, hemocytes, and fat body. A recent transcriptome analysis of MTs of the Chagas disease vector Rhodnius prolixus revealed the presence of transcripts for muscarinic ACh receptors and for acetylcholinesterase, raising the possibility that non-neuronal ACh may play a role in the control of MTs. Here we provide evidence for a non-neuronal ACh signaling pathway in MTs of R. prolixus. Transcripts for ACh signaling are expressed, and ACh is capable of stimulating small increases in secretion by isolated MTs (small, relative to the true diuretic neurohormones in R. prolixus). The effects of ACh are mimicked by carbachol and pilocarpine, with atropine inhibiting ACh- and pilocarpine-stimulated secretion. Blood gorging alters expression of transcripts for ACh signaling. We discuss the physiological relevance for ACh since MTs are much more than diuresis; they play major roles in immunity, detoxification, and in tolerance to overall stress. Perhaps ACh is a signaling component of these essential functions that might require an increase in secretion rate by MTs that is separate from the well described rapid post-prandial diuresis.