Opposite effects of 5-HT/AKH and octopamine on the crop contractions in adult Drosophila melanogaster: Evidence of a double brain-gut serotonergic circuitry

Abstract

This study showed that in adult Drosophila melanogaster, the type of sugar—either present within the crop lumen or in the bathing solution of the crop—had no effect on crop muscle contraction. What is important, however, is the volume within the crop lumen. Electrophysiological recordings demonstrated that exogenous applications of serotonin on crop muscles increases both the amplitude and the frequency of crop contraction rate, while adipokinetic hormone mainly enhances the crop contraction frequency. Conversely, octopamine virtually silenced the overall crop activity. The present study reports for the first time an analysis of serotonin effects along the gut-brain axis in adult D. melanogaster. Injection of serotonin into the brain between the interocellar area shows that brain applications of serotonin decrease the frequency of crop activity. Based on our results, we propose that there are two different, opposite pathways for crop motility control governed by serotonin: excitatory when added in the abdomen (i.e., directly bathing the crop) and inhibitory when supplied within the brain (i.e., by injection). Finally, our results point to a double brain-gut serotonergic circuitry suggesting that not only the brain can affect gut functions, but the gut can also affect the central nervous system. On the basis of our results, and data in the literature, a possible mechanism for these two discrete serotonergic functions is suggested.

Physiological characterization and regulation of the contractile properties of the mosquito ventral diverticulum (crop)

“…The present study demonstrated that the crop of adult female A. aegypti spontaneously contracts in vitro at a rate of ~6 contractions per min; which is noticeably lower than corresponding rates (15–90 contractions per min) in P. regina , M. domestica, and D. melanogaster (Haselton et al 2006; Kaminski et al 2002; Liscia et al 2012; Solari et al 2017, 2013; Stoffolano et al 2014b; Stoffolano et al 2013). Whether the lower spontaneous contraction rate in female mosquitoes is adaptive to their hematophagous life style remains to be determined.…”

“…Similarly, 5-HT stimulates crop contractions in P. reginia and D. melanogaster (Liscia et al 2012; Solari et al 2017). The effects of 5-HT on the isolated mosquito crop in vitro suggest that in vivo the contractile activity of the crop can potentially be regulated by changes in hemolymph 5-HT levels and/or the release of 5-HT from 5-HT-immunoreactive neurons that innervate the crop of A. aegypti (Moffett and Moffett, 2005).…”

“…We cannot rule out that 5-HT also binds to a 5-HT 2 -like receptor in the mosquito crop that would signal via inositol triphosphate (IP 3 ) and diacylglycerol. In the crop of D. melanogaster , transcriptomic and pharmacological evidence supports the presence of a 5-HT 2 -like receptor (Chintapalli et al 2007; Robinson et al 2013; Solari et al 2017), but in the crop of P. regina physiological evidence for a 5-HT-activated IP3 pathway is lacking (Liscia et al 2012). Additional molecular and pharmacological studies of the mosquito crop will be necessary to further elucidate the 5-HT signaling pathway.…”

“…5-HT is a biogenic amine that stimulates crop contractions in P. regina and D. melanogaster (Liscia et al, 2012; Solari et al, 2017). 8-Bromo-cAMP is a membrane-permeable analog of cAMP used to elevate intracellular concentrations of cAMP (e.g., Goino et al 2014).…”

“…Moreover, the volume of liquid within the crop influences the contraction rates in both P. regina and M. domestica (Holling, 1976; Stoffolano et al 2014b). Neuropeptides, such as adipokinetic hormone (AKH), dromyosuppressin (DMS), drosulfakinin, and FMRFamide, and biogenic amines, such as serotonin (5-hydroxytryptamine, 5-HT) and octopamine, modulate crop contraction rates in P. regina and/or D. melanogaster (Duttlinger et al 2002; Liscia et al 2012; Palmer et al 2007; Solari et al 2017; Stoffolano et al 2013; Stoffolano et al 2014a). Notably, nerves associated with the crop contain DMS, FMRFamide, insulin-like peptide, 5-HT, and AKH, suggesting the potential for direct neural control of crop contractions (Cao and Brown, 2001; Duttlinger et al 2002; Haselton et al 2004; Lee and Park, 2004; Liu et al 2011; McCormick and Nichols, 1993).…”