Abstract
In the Chagas disease vector, Rhodnius prolixus, two diuretic hormones act synergistically to dramatically increase fluid secretion by the Malpighian tubules (MTs) during the rapid diuresis that is initiated upon engorgement of vertebrate blood. One of these diuretic hormones is the biogenic amine, serotonin (5-hydroxytryptamine, 5-HT), which controls a variety of additional activities including cuticle plasticization, salivary gland secretion, anterior midgut absorption, cardioacceleratory activity, and myotropic activities on a number of visceral tissues. To better understand the regulatory mechanisms linked to these various physiological actions of serotonin, we have isolated and characterized a serotonin type 2b receptor in R. prolixus, Rhopr5HTR2b, which shares sequence similarity to the vertebrate serotonin type 2 receptors. Rhopr5HTR2b transcript is enriched in well-recognized physiological targets of serotonin, including the MTs, salivary glands and dorsal vessel (i.e., insect heart). Notably, Rhopr5HTR2b was not enriched in the anterior midgut where serotonin stimulates absorption and elicits myotropic control. Using a heterologous functional receptor assay, we examined Rhopr5HTR2b activation characteristics and its sensitivity to potential agonists, antagonists, and other biogenic amines. Rhopr5HTR2b is dose-dependently activated by serotonin with an EC50 in the nanomolar range. Rhopr5HTR2b is sensitive to alpha-methyl serotonin and is inhibited by a variety of serotonin receptor antagonists, including propranolol, spiperone, ketanserin, mianserin, and cyproheptadine. In contrast, the cardioacceleratory activity of serotonin revealed a unique pharmacological profile, with no significant response induced by alpha-methyl serotonin and insensitivity to ketanserin and mianserin. This distinct agonist/antagonist profile indicates that a separate serotonin receptor type may mediate cardiomodulatory effects controlled by serotonin in R. prolixus.
Highlights
The widespread presence and diverse biological roles of the indoleamine, serotonin (5-hydroxytryptamine, 5-HT), spans protozoans, plants and the vast majority of metazoans, attesting to its evolutionary significance
Cloning and Gene Structure of a R. prolixus 5HTR2b Receptor Using a combined approach involving homology-based in silico screening of the preliminary R. prolixus genome data and PCR-based strategy to confirm and obtain further sequence information over the 5′ and 3′ regions using Rapid Amplification of cDNA Ends (RACE) PCR, we have identified a R. prolixus 5HTR2b (Rhopr5HTR2b) cDNA (Genbank accession KP325472)
Diuresis in R. prolixus is under the control of at least two diuretic hormones, which includes the biogenic amine serotonin and RhoprCRF/DH (Lange et al, 1989; Maddrell et al, 1991; Te Brugge et al, 2011)
Summary
The widespread presence and diverse biological roles of the indoleamine, serotonin (5-hydroxytryptamine, 5-HT), spans protozoans, plants and the vast majority of metazoans, attesting to its evolutionary significance (see Turlejski, 1996). The serotonin receptor, 5HTR3, is a ligand-gated channel whereas all other serotonin receptor classes have been characterized as G-protein coupled receptors (GPCRs) (Millan et al, 2008). Released as both a neurotransmitter and a hormone, the functions of serotonin are extensive, ranging from regulating the mechanics of behaviors like learning, memory, perception, fear and appetite, to mediating a plethora of physiological processes (see Berger et al, 2009; Verlinden et al, 2015). Serotonin is a key modulator of feedingrelated behaviors, including salivation, bite-like movements, pharyngeal peristalsis, and control of blood meal ingestion in a blood-feeding aquatic invertebrate, the medicinal leech, Hirudo medicinalis (Lent and Dickinson, 1987, 1988; Lent et al, 1988)
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