Screening of antifeedant activity in brain extracts led to the identification of sulfakinin as a satiety promoter in the German cockroach (original) (raw)
Related papers
Peptides, 2013
The insect sulfakinins (SKs) constitute a family of neuropeptides that display both structural and functional similarities to the mammalian hormones gastrin and cholecystokinin (CCK). As a multifunctional neuropeptide, SKs are involved in muscle contractions as well as food intake regulation in many insects. In the red flour beetle Tribolium castaneum, the action on food intake by a series of synthetic SK analogs and one putative antagonist was investigated by injection in beetle adults. The most remarkable result was that both sulfated and non-sulfated SKs [FDDY(SO 3 H)GHMRFamide] inhibited food intake by about 70%. Strong activity observed for SK analogs featuring a residue that mimics the acidic nature of Tyr(SO 3 H) but lack the phenyl ring of Tyr, indicate that aromaticity is not a critical characteristic for this position of the peptide. SK demonstrated considerable tolerance to Ser and Ala substitution in position 8 (basic Arg), as analogs featuring these uncharged substitutions retained almost all of the food intake inhibitory activity. Also, the Phe in position 1 could be replaced by Ser without complete loss of activity. Conversely, substitution of Met by Nle in position 3 led to inactive compounds. Finally, the Caenorhabditis elegans sulfated neuropeptide-like protein-12 (NLP-12), that shares some sequence similarities with the SKs but features a Gln-Phe-amide rather than an Arg-Phe-amide at the C-terminus, elicited increased food intake in T. castaneum, which may indicate an antagonist activity. Co-injection NLP-12 with nsSK blocked the food intake inhibitory effects of nsSK. (G. Smagghe). As hormones, SKs require certain receptors. Sulfakinin recep-38 tors (SK-Rs) were predicted and cloned in Drosophila melanogaster, 39 based on their sequence similarity to the CCK receptors, and 40 designated as DSK-R1 and DSK-R2 [15,18]. In the red flour bee-41 tle Tribolium castaneum, two SK-Rs were predicted based on the 42 genome sequence [14]. These receptors were identified as G 43 protein-coupled receptors. 44 Studies on function reported that SKs influence the frequency 45 and amplitude of foregut and hindgut visceral muscle contractions 46 [26,28,33,36]. Similar to the satiety effect of gastrin/CCK in mam-47 mals, insect SKs significantly inhibited food intake in the locust 48 Schistocerca gregaria [46], the cockroach Blattella germanica [19] 49 and in the cricket Gryllus bimaculatus [22]. In the blow fly Phormia 50 regina, carbohydrate ingestion was decreased by feeding SK [6]. In 51 addition, SKs stimulate release of the digestive enzyme ␣-amylase 52 in the red palm weevil Rhynchophorus ferrugineus [24] and the 53 coconut pest Opisina arenosella [13]. 54 The insect SKs share a conserved C-terminus (DYGHMRFamide) 55 among various species [5,8,22]. Two SK peptides exist in many 56 0196-9781/$ -see front matter PEP 68869 1-6 2 N. Yu et al. / Peptides xxx (2012) xxx-xxx insects, which were designated as SK I and SK II, differing in the N-57 terminal sequences. Previous studies showed that the sulfated Tyr 58 is required for the activities of SKs [18,19,46]. In Drosophila, a 3000-59 fold higher concentration of the nonsulfated sulfakinin (nsDSK) 60 than the sulfated sulfakinin (sDSK) was required to stimulate the SK 61 receptor (DSK-R1) as expressed in mammalian cells [18]. In addi-62 tion, sDSK and nsDSK were reported to display different activities 63 in odor preference and locomotion or in different tissues or stages, 64 phenomena which indicate that distinct mechanisms may underlie 65 the effect of SKs [33,34]. Thus, studies on the SK activity related to 235 Tyr is not necessary for this activity. In the American cockroach 236 Periplaneta americana, both sulfated and nonsulfated SKs (Lem-237 SKs) were detected in the corpora cardiac/corpora allata complexes, 238 providing evidence that the two forms of SK naturally co-exist in 239 insects [39]. Previous studies on food intake suggested that the 240 sulfate moiety is critical for this modulatory activity, which is oppo-241 site to the case in T. castaneum. In the desert locust, S. gregaria, 242 nsLom-SK had no effect on food intake [46]. Maestro et al. reported 243 that in B. germanica, the sLem-SK-II and sPea-SK could inhibit food 244 intake at low concentrations, while the nonsulfated peptides were 245 inactive even at higher concentrations [19]. In addition, the nsDSK 246 was 3000-fold less potent than the sDSK to activate DSK-R1 in D. 247 melanogaster [18]. Nevertheless, nsSK activities were also reported 248 in Drosophila, mainly focusing on myoactivity, odor preference and 249 Please cite this article in press as: Yu N, et al. Analogs of sulfakinin-related peptides demonstrate reduction in food intake in the red flour beetle, Tribolium castaneum, while putative antagonists increase consumption. Peptides (2012), http://dx.
Sulfakinins reduce food intake in the desert locust, Schistocerca gregaria
Journal of Insect Physiology, 2000
In vertebrates, the peptides cholecystokinin (CCK), neuropeptide Y, galanin, and bombesin are known to be involved in the control of food intake. We report here that insect sulfakinins, peptides which display substantial sequence similarities with the vertebrate gastrin/CCK peptide family, significantly inhibit food uptake in fifth instar nymphs of the locust, Schistocerca gregaria. Upon injection of Lom-sulfakinin, a neuropeptide present in the corpus cardiacum of locusts, food intake was significantly reduced in a dose-dependent manner within a fixed 20 min time period. The induced effect ranged from 13% inhibition (10 pmol of injected peptide) to over 50% inhibition at 1 nmol. Other naturally occurring sulfakinins from different insect species also elicited this satiety effect. Analogous to the satiety effect of CCK in vertebrates, the sulfate group is required for activity. No effect on the palptip resistance was found after injection with sulfakinin. Therefore it seems unlikly that sulfakinins reduce food intake by decreasing the sensitivity of the taste receptors.
Insect Biochemistry and Molecular Biology, 2015
Sulfakinin (SK) is a sulfated insect neuropeptide that is best known for its function as a satiety factor. It displays structural and functional similarities with the vertebrate peptides gastrin and cholecystokinin. Peptidomic studies in multiple insects, crustaceans and arachnids have revealed the widespread occurrence of SK in the arthropod phylum. Multiple studies in hemi-and holometabolous insects revealed the pleiotropic nature of this neuropeptide: in addition to its activity as a satiety factor, SK was also reported to affect muscle contraction, digestive enzyme release, odor preference, aggression and metabolism. However, the main site of action seems to be the digestive system of insects. In this study, we have investigated whether SK can intervene in the control of nutrient uptake and digestion in the migratory locust (Locusta migratoria). We provide evidence that sulfakinin reduces food uptake in this species. Furthermore, we discovered that SK has very pronounced effects on the main digestive enzyme secreting parts of the locust gut. It effectively reduced digestive enzyme secretion from both the midgut and gastric caeca. SK injection also elicited a reduction in absorbance and proteolytic activity of the gastric caeca contents. The characteristic sulfation of the tyrosine residue is crucial for the observed effects on digestive enzyme secretion. In an attempt to provide potential leads for the development of peptidomimetic compounds based on SK, we also tested two mimetic analogs of the natural peptide ligand in the digestive enzyme secretion assay. These analogs were able to mimic the effect of the natural SK, but their effects were milder. The results of this study provide new insights into the action of SK on the digestive system in (hemimetabolous) insects.
2003
Allatostatins of the YXFGLamide group were discovered in cockroaches through their capacity to inhibit juvenile hormone biosynthesis. Here, we assess the occurrence of preproallatostatin (preproAST) mRNA in the brain and midgut of adult females of the cockroach Blattella germanica, and estimate brain and midgut preproAST mRNA levels during the first reproductive cycle. Reverse transcription polymerase chain reaction (RT-PCR) shows that brain preproAST mRNA levels increase slightly during the gonadotrophic cycle, and remain high during ootheca transport. In the midgut, preproAST mRNA levels decline around the middle of the gonadotrophic cycle. The pattern of allatostatin expression in gut tissues suggests that these peptides play roles related to feeding and nutrition. Our results have shown that synthetic allatostatins inhibit hindgut motility and activate midgut a-amylase secretion. In addition, injected allatostatins inhibit food consumption, which might be connected to the above activities. D
Tissue and Cell, 1997
We describe the distribution of sulfakinin-like neuropeptides in the central and sympathetic nervous system of the American cockroach Periplaneta americana (L.) (Blattodea) and the field cricket Teleogryllus commodus (Walker) (Orthoptera), using an antisulfakinin primary antibody and confocal laser scanning microscopy. We conclude that, in the cockroach, sulfakinin-like material is produced in ten pairs of anterior cells in the pars intercerebralis, as well as two pairs of medial and one major pair of lateral posterior brain cells. This contrasts with findings in other insects, including the cricket, where only the posterior cell groups express sulfakinin-immunoreactive material. Extensive arborization of dendrites containing sulfakinin-like peptides occurs within the neuropile of both species, suggesting a neurotransmitter/ neuromodulator function. In the cockroach, there is clear evidence of direct distribution of sulfakinin-like peptides along axons to the foregut tissue, and a plexus of retrocerebral nerves is likely to serve as a neurohaemal release site. Neurohaemal release into the dorsal aorta is also postulated. Sulfakininimmunoreactive axons do not innervate the hindgut in either cockroaches or crickets. Sulfakinin may function as a gut myotropin in the Blattodea, in addition to functioning as a neurotransmitter within the central nervous system. This latter function appears to be general across insect orders, while the neurohaemal distribution and myotropic activity are restricted to the Blattodea.
Peptidergic control of food intake and digestion in insects1
Canadian Journal of Zoology
Like all heterotrophic organisms, insects require a strict control of food intake and efficient digestion of food into nutrients to maintain homeostasis and to fulfill physiological tasks. Feeding and digestion are steered by both external and internal signals that are transduced by a multitude of regulatory factors, delivered either by neurons innervating the gut or mouthparts, or by midgut endocrine cells. The present review gives an overview of peptide regulators known to control feeding and digestion in insects. We describe the discovery and functional role in these processes for insect allatoregulatory peptides, diuretic hormones, FMRFamide-related peptides, (short) neuropeptide F, proctolin, saliva production stimulating peptides, kinins, and tachykinins. These peptides control either gut myoactivity, food intake, and (or) release of digestive enzymes. Some peptides exert their action at multiple levels, possibly having a biological function that depends on their site of deliv...
Regulatory Peptides, 2004
The feeding pattern of the adult female of Blattella germanica peaks in the middle of the vitellogenic cycle. Following the hypothesis that a factor inhibiting gut peristalsis also inhibits food intake and is involved in the regulation of feeding, we searched for the most powerful myoinhibitory peptide in brain extracts from B. germanica females collected after the peak within the feeding cycle. Through HPLC purification and sequence analysis, we obtained the peptide leucomyosuppressin (LMS): pQDVDHVFLRFamide. LMS elicited a powerful myoinhibitory effect on B. germanica foregut and hindgut, with ED 50 values around 10 À 10 M. In addition, it inhibited food intake in vivo in a dose-dependent manner at doses between 5 and 50 Ag. The study of the distribution of ingested food in the foregut, midgut and hindgut of B. germanica females treated with LMS showed that food accumulates in the foregut, which may be due to the myoinhibitory effects of the peptide. We propose that this accumulation inhibits food intake because of the persistence of the signals from gut stretch receptors. D
Effects of myoinhibitory peptides on food intake in the German cockroach
Physiological Entomology, 2006
Insect myoinhibitory peptides were discovered through their inhibitory activity on visceral muscle contraction. The present study tests the antimyotropic gut properties of three galanin-related myoinhibitory peptides (Mas-MIP II: GWQDLNSAW-NH2; Grb-AST-B1: GWQDLNGGW-NH 2 ; and Grb-AST-B3: AWRDLSGGW-NH2) in adult females of the cockroach Blattella germanica (L.) (Dictyoptera, Blattellidae). The three peptides elicit a strong inhibitory effect on both foregut and hindgut contractions, with ID 50 values in all the cases within the nanomolar range. In addition, the modulatory effects of these three peptides on food intake are studied on previously starved female cockroaches. The results show that Grb-AST-B3 is the most active peptide, inhibiting food intake by 60-80% at doses between 15 and 50 mg, followed by Grb-AST-B1 (45% inhibition of food intake at the 50 mg dose), whereas Mas-MIP II is inactive even at the 50 mg dose. The differences between the three peptides may be due to a differential effect of their structure on activity or to a differential degradation. These results show that myomodulatory gut activity in vitro and antifeeding effects do not always correlate.
Peptides, 2012
Immunohistochemical reactivity against short neuropeptide F (sNPF) was observed in the brain-corpus cardiacum and midgut paraneurons of the American cockroach, Periplaneta americana. Four weeks of starvation increased the number of sNPF-ir cells in the midgut epithelium but the refeeding decreased the number in 3 h. Dramatic rises in sNPF contents in the midgut epithelium and hemolymph of roaches starved for 4 weeks were confirmed by ELISA. Starvation for 4 weeks reduced ␣-amylase, protease and lipase activities in the midgut of P. americana but refeeding restored these to high levels. Co-incubation of dissected midgut with sNPF at physiological concentrations inhibited ␣-amylase, protease and lipase activities. sNPF injection into the hemocoel led to a decrease in ␣-amylase, protease and lipase activities, whereas PBS injection had no effects. The injection of d-(+)-trehalose and l-proline into the hemocoel of decapitated adult male cockroaches that had been starved for 4 weeks had no effect on these digestive enzymes. However, injection into the hemocoel of head-intact starved cockroaches stimulated digestive activity. Injection of d-(+)-trehalose and l-proline into the lumen of decapitated cockroaches that had been starved for 4 weeks increased enzymes activities and suppressed sNPF in the midgut. Our data indicate that sNPF from the midgut paraneurons suppresses ␣-amylase, protease and lipase activities during starvation. Injection of d-(+)-trehalose/l-proline into the hemocoel of head-intact starved cockroach decreased the hemolymph sNPF content, which suggests that sNPF could be one of the brain factors, demonstrating brain-midgut interplay in the regulation of digestive activities and possibly nutritionassociated behavioral modifications.
Peptides, 2014
Insects acquire essential nutrients from their food to support a diverse range of biological processes such as development and reproduction. An important role in the food intake regulation is attributed to the neurohormone sulfakinin signaling pathway. Sulfakinins (SKs) elicit satiety together with sulfakinin receptors (SKRs). In this project, the gene coding a second putative SKR, namely skr2, was cloned, characterized and functionally studied in the red flour beetle Tribolium castaneum, with the purpose to understand its role in food intake regulation. The gene skr2 encoded a seven-transmembrane SKR2 protein with 420 amino acids and is evolutionarily close to the two SKRs in Drosophila. A distribution analysis by means of quantitative real-time PCR revealed a tissue-and stage-specific expression pattern with skr2 being dominantly expressed in head, and in the pupal and adult stages. Besides, its expression in gut was notable. With use of dsRNA of skr2, larval food intake was stimulated in an injection RNAi assay. Based on the data obtained, skr2 is considered as an indispensable component in the regulation of food intake in T. castaneum.