Nitric oxide contributes to high-salt perception in a blood-sucking insect model

Agustina Cano,Diego Anfossi,Romina B Barrozo,Gina Pontes,Valeria Sfara

doi:10.1038/s41598-017-15861-0

Abstract

In all organisms, salts produce either appetitive or aversive responses depending on the concentration. While low-salt concentration in food elicits positive responses to ingest, high-salt triggers aversion. Still the mechanisms involved in this dual behavior have just started to be uncovered in some organisms. In Rhodnius prolixus, using pharmacological and behavioral assays, we demonstrated that upon high-salt detection in food a nitric oxide (NO) dependent cascade is activated. This activation involves a soluble guanylate cyclase (sGC) and the production of cyclic guanosine monophosphate (cGMP). Thus, appetitive responses to low-salt diets turn to aversion whenever this cascade is activated. Conversely, insects feed over aversive high-salt solutions when it is blocked by reducing NO levels or by affecting the sGC activity. The activation of NO/sGC/cGMP cascade commands the avoidance feeding behavior in R. prolixus. Investigations in other insect species should examine the possibility that high-salt aversion is mediated by NO/sSG/cGMP signaling.

Highlights

The taste sense helps animals to evaluate the quality of food, favoring the ingestion of nutrients and avoiding the consumption of harmful or toxic compounds
Knowing that taste detection of low-salt concentration in artificial diets triggers feeding in R. prolixus, we propose that whenever salt concentration rises beyond a threshold of tolerance, a nitric oxide (NO)/soluble guanylate cyclase (sGC)/cyclic guanosine monophosphate (cGMP) pathway is activated in taste receptor cells
We investigated the effect of the administration of a NO donor (SNAC), a sGC inhibitor (1H-[1,2,4]oxadiazolo[4,3-a] quinoxalin-1-one, ODQ) or a cGMP analogue (8-bromoguanosine 3′,5′-cyclic monophosphate, 8-Br-cGMP) on the feeding behavior of insects offered with a low-NaCl feeding solution

Summary

Introduction

The taste sense helps animals to evaluate the quality of food, favoring the ingestion of nutrients and avoiding the consumption of harmful or toxic compounds. The detection of low-salt concentrations in food generally trigger feeding acceptance while high-salt concentrations are generally rejected[2,3,4]. Mammals and insects, two separate taste pathways have been proposed for salt sensing: an appetitive (tuned to low salt detection) vs an aversive pathway (for high salt detection). Detection of low-salt concentrations in mammals is mediated by taste receptor cells expressing ENaC receptors[2], and in insects by ppk[11], ppk[19] and IR76a receptors[3,4]. High-salt sensing in mammals seems not involve dedicated taste receptor cells but instead through the recruitment of two populations of cells tuned to detect bitter and sour[15]. Topical application of a NO donor (S-nitroso-N-acetylcysteine, SNAC) over kissing bugs’ antennae significantly decreased the feeding response over a living host[24]

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Conclusion