Brain-midgut cross-talk and autocrine metabolastat via the sNPF/CCAP negative feed-back loop in the American cockroach, Periplaneta americana

Abstract

Immunohistochemical reactivities against short neuropeptide F (sNPF-ir) and crustacean cardioactive peptide (CCAP-ir) were detected in both the brain-subesophageal ganglion (Br-SOG) and midgut epithelial cells of the male American cockroach, Periplaneta americana. Four weeks of starvation increased the number of sNPF-ir cells and decreased the CCAP-ir cells in the Br-SOG, whereas refeeding reversed these effects. The contents of sNPF in the Br-SOG, midgut and hemolymph titer decreased in response to an injection of CCAP into the hemocoel of normally fed male cockroaches, while CCAP titers/contents decreased in response to an injection of sNPF. The results of a double-labeling experiment demonstrated that sNPF-ir co-existed in CCAP-ir cells in the pars intercerebralis (PI), dorsolateral region of protocerebrum (DL), deutocerebrum (De) and SOG. sNPF-ir and CCAP-ir were also colocalized in the midgut. sNPF and CCAP are neuropeptides and midgut factors that interact with each other. Since the two peptides are known to be secreted by identical cells that affect each other, this constitutes autocrine negative feedback regulation for a quick response to food accessibility/inaccessibility. These peptides not only constitute the switch in the digestive mechanism but also couple digestive adaptation with behavior. A CCAP injection suppressed locomotor activity when cockroaches were starved, whereas sNPF activated it when they were fed.

Adipokinetic hormones control amylase activity in the cockroach (Periplaneta americana) gut

“…Especially, the effect of CCAP deserves attention, since it has been shown in locusts that this neuropeptide stimulates in vitro release of AKH from corpora cardiaca (Veelaert et al, 1997). Further, it has also been proved that CCAP elevates the amylase activity in the midgut of P. americana (Sakai et al, 2004) and that it occurs even in epithelial cells (apart from the brain-suboesophageal ganglion) of the same organ (Mikani et al, 2015). Later on the same group (Sakai et al, 2006) proved that incubation of cockroach midgut in the CCAP presence significantly increased amylase activity within 2-3 h after the hormonal application.…”

Distribution of Short Neuropeptide F-like Immunohistochemical Reactivity in the Brain and Midgut of the Terrestrial Isopod, <i>Armadillidium vulgare</i> (Latreille)

“…Mikani [22] showed that sNPF as both a neuropeptide and a midgut factor that suppresses α-amylase, protease and lipase activities during starvation this demonstrates an intricate interplay between the brain and midgut to regulate digestive activities. This finding indicated that enzyme activities were downregulated by sNPF [21,22].…”

“…Veenstra and Lambrou [38] isolated a large amount of sNPF from the midgut of P. americana. Changes in peptide content in paraneuronal cells are correlated with the state of digestion of insects [21,50]. The number of sNPF-ir paraneuronal cells increased during 4 weeks of starvation and decreased after 3 h of refeeding [22].This suggests that the nutritional input was sensed by the midgut and CCAP is released to the hemocoel that stimulate the secretion of CCAP from the brain, constituting a large feed-forward loop.…”

“…This diverse population of sNPF-expressing neurons and paraneurons suggests that sNPF may serve multiple functions both in the CNS as neurotransmitter and the gut as a circulating hormone and paracrine factor [19,20]. Mikani [21] demonstrated that sNPF functioned as both a neuropeptide and midgut factor to suppress α-amylase, protease and lipase activities during starvation in the American cockroach Periplaneta americana. They have demonstrated an interactive loop betaeen the midgut and brain via two antagonistic neuropeptides, CCAP and sNPF.…”

Effect of caffeic acid on feeding, α-amylase and protease activities and allatostatin—A content of Egyptian cotton leafworm, <i>Spodoptera littoralis</i> (Lepidoptera: Noctuidae)—

“…Competitive ELISA was performed as previously described. 19) Briefly, after dissection of the midgut in TBS, homogenization, and centrifugation (4000×g, 4°C, 15 min), the supernatant was used as an assay sample. After coupling synthetic AST-6 and to BSA with dimethyl suberimidate (Sigma-Aldrich, USA) and preparing an AST-A-BSA conjugate, the plates were coated with AST-6-BSA (0.6 µg/mL per well) in 0.05 M sodium carbonatebicarbonate buffer (pH 9.0).…”