Identification of the short neuropeptide F precursor in the desert locust: Evidence for an inhibitory role of sNPF in the control of feeding

Dillen, Senne; Verdonck, Rik; Zels, Sven; Wielendaele, Pieter Van; Broeck, Jozef Vanden

doi:10.1016/j.peptides.2013.09.018

Cited by 42 publications

(47 citation statements)

References 34 publications

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“…The influence of sNPF on feeding behavior and growth is well described [109][110][111], but numerous other roles have been reported [86,112]. We detected short NPF-2 (SPSLRLRFa), one of the four predicted sNPF neuropeptides, in the brain, TG, and CC-CA.…”

Section: Short Neuropeptide Fmentioning

confidence: 63%

Peptidomics of Neuropeptidergic Tissues of the Tsetse FlyGlossina morsitans morsitans

Caers

Boonen

Abbeele³

et al. 2015

J. Am. Soc. Mass Spectrom.

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Abstract. Neuropeptides and peptide hormones are essential signaling molecules that regulate nearly all physiological processes. The recent release of the tsetse fly genome allowed the construction of a detailed in silico neuropeptide database (International Glossina Genome Consortium, Science 344, 380-386 (2014)), as well as an in-depth mass spectrometric analysis of the most important neuropeptidergic tissues of this medically and economically important insect species. Mass spectrometric confirmation of predicted peptides is a vital step in the functional characterization of neuropeptides, as in vivo peptides can be modified, cleaved, or even mispredicted. Using a nanoscale reversed phase liquid chromatography coupled to a Q Exactive Orbitrap mass spectrometer, we detected 51 putative bioactive neuropeptides encoded by 19 precursors: adipokinetic hormone (AKH) I and II, allatostatin A and B, capability/ pyrokinin (capa/PK), corazonin, calcitonin-like diuretic hormone (CT/DH), FMRFamide, hugin, leucokinin, myosuppressin, natalisin, neuropeptide-like precursor (NPLP) 1, orcokinin, pigment dispersing factor (PDF), RYamide, SIFamide, short neuropeptide F (sNPF) and tachykinin. In addition, propeptides, truncated and spacer peptides derived from seven additional precursors were found, and include the precursors of allatostatin C, crustacean cardioactive peptide, corticotropin releasing factor-like diuretic hormone (CRF/DH), ecdysis triggering hormone (ETH), ion transport peptide (ITP), neuropeptide F, and proctolin, respectively. The majority of the identified neuropeptides are present in the central nervous system, with only a limited number of peptides in the corpora cardiaca-corpora allata and midgut. Owing to the large number of identified peptides, this study can be used as a reference for comparative studies in other insects.

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Section: Short Neuropeptide Fmentioning

confidence: 63%

Peptidomics of Neuropeptidergic Tissues of the Tsetse FlyGlossina morsitans morsitans

Caers

Boonen

Abbeele³

et al. 2015

J. Am. Soc. Mass Spectrom.

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“…Similarly, an inverse relation of sNPF signaling and feeding behavior was also observed in the desert locust. Injection of sNPF peptides decreases food uptake while knock down of sNPF prepropeptide and sNPFR genes stimulates it [27] , [28] . Some of these generalizations, however, are made on the basis of transcript levels alone, and not peptide and/or receptor protein, so caution is needed when interpreting them.…”

Section: Introductionmentioning

confidence: 99%

The Red Imported Fire Ant (Solenopsis invicta Buren) Kept Y not F: Predicted sNPY Endogenous Ligands Deorphanize the Short NPF (sNPF) Receptor

Bajracharya

Pietrantonio

2014

PLoS ONE

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Neuropeptides and their receptors play vital roles in controlling the physiology and behavior of animals. Short neuropeptide F (sNPF) signaling regulates several physiological processes in insects such as feeding, locomotion, circadian rhythm and reproduction, among others. Previously, the red imported fire ant (Solenopsis invicta) sNPF receptor (S. invicta sNPFR), a G protein-coupled receptor, was immunolocalized in queen and worker brain and queen ovaries. Differential distribution patterns of S. invicta sNPFR protein in fire ant worker brain were associated both with worker subcastes and with presence or absence of brood in the colony. However, the cognate ligand for this sNPFR has not been characterized and attempts to deorphanize the receptor with sNPF peptides from other insect species which ended in the canonical sequence LRLRFamide, failed. Receptor deorphanization is an important step to understand the neuropeptide receptor downstream signaling cascade. We cloned the full length cDNA of the putative S. invicta sNPF prepropeptide and identified the putative “sNPF” ligand within its sequence. The peptide ends with an amidated Tyr residue whereas in other insect species sNPFs have an amidated Phe or Trp residue at the C-terminus. We stably expressed the HA-tagged S. invicta sNPFR in CHO-K1 cells. Two S. invicta sNPFs differing at their N-terminus were synthesized that equally activated the sNPFR, SLRSALAAGHLRYa (EC50 = 3.2 nM) and SALAAGHLRYa (EC50 = 8.6 nM). Both peptides decreased the intracellular cAMP concentration, indicating signaling through the Gαi-subunit. The receptor was not activated by sNPF peptides from other insect species, honey bee long NPF (NPY) or mammalian PYY. Further, a synthesized peptide otherwise identical to the fire ant sequence but in which the C-terminal amidated amino acid residue ‘Y’ was switched to ‘F’, failed to activate the sNPFR. This discovery will now allow us to investigate the function of sNPY and its cognate receptor in fire ant biology.

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“…Short neuropeptide F (sNPF) has been shown to modulate feeding behavior in a wide variety of insect species. While this peptide stimulates feeding and food-searching behavior in Drosophila melanogaster (Hong et al 2012) and Apis mellifera (Hummon et al 2006), an opposite effect has recently been demonstrated in the desert locust, Schistocerca gregaria (Dillen et al 2014) and P. americana (Mikani et al 2012). In D.melanogaster, sNPF-ir cells were detected in both the nervous system and and the epithelium of midgut (Brown et al 1999).…”

Section: Discussionmentioning

confidence: 98%

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

2015

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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.

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Identification of the short neuropeptide F precursor in the desert locust: Evidence for an inhibitory role of sNPF in the control of feeding

Cited by 42 publications

References 34 publications

Peptidomics of Neuropeptidergic Tissues of the Tsetse FlyGlossina morsitans morsitans

Peptidomics of Neuropeptidergic Tissues of the Tsetse FlyGlossina morsitans morsitans

The Red Imported Fire Ant (Solenopsis invicta Buren) Kept Y not F: Predicted sNPY Endogenous Ligands Deorphanize the Short NPF (sNPF) Receptor

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

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