Two Novel Tachykinin-Related Neuropeptides in the Echiuroid Worm, Urechis unicinctus

doi:10.1006/bbrc.1993.1373

Biochemical and Biophysical Research Communications

Volume 192, Issue 1, 15 April 1993, Pages 1-6

https://doi.org/10.1006/bbrc.1993.1373 Get rights and content

Abstract

Two novel neuropeptides, urechistachykinin I (H-Leu-Arg-Gln-Ser-Gln-Phe-Val-Gly-Ser-Arg-NH₂) and urechistachykinin II (H-Ala-Ala-Gly-Met-Gly-Phe-Phe-Gly-Ala-Arg-NH₂), were isolated from the ventral nerve cords of the echiuroid worm, Urechis unicinctus. These peptides showed a contractile action on the inner circular body-wall muscle of the animal. Their amino acid sequences were found to be significantly homologous with those of the vertebrate and insect tachykinins. The urechistachykinins potentiated spontaneous rhythmic contractions of the cockroach hindgut.

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Cited by (36)

Characterization of a tachykinin signalling system in the bivalve mollusc Crassostrea gigas
2018, General and Comparative Endocrinology
Citation Excerpt :
In bilateria, TKs have been shown to participate in the control of the activity of a wide array of peripheral organs and tissues. In vitro studies on organ preparations of protostome species suggest that TK signalling plays a role in the regulation of gut activity and visceral and skeletal muscle contractions (Palamiuc et al., 2017; Schoofs et al., 1990; Schoofs et al., 1990; Ikeda et al., 1993). Deficient TK functioning contributes to multiple disease processes in humans (Steinhoff et al., 2014).
Although tachykinin-like neuropeptides have been identified in molluscs more than two decades ago, knowledge on their function and signalling has so far remained largely elusive. We developed a cell-based assay to address the functionality of the tachykinin G-protein coupled receptor (Cragi-TKR) in the oyster Crassostrea gigas. The oyster tachykinin neuropeptides that are derived from the tachykinin precursor gene Cragi-TK activate the Cragi-TKR in nanomolar concentrations. Receptor activation is sensitive to Ala-substitution of critical Cragi-TK amino acid residues. The Cragi-TKR gene is expressed in a variety of tissues, albeit at higher levels in the visceral ganglia (VG) of the nervous system. Fluctuations of Cragi-TKR expression is in line with a role for TK signalling in C. gigas reproduction. The expression level of the Cragi-TK gene in the VG depends on the nutritional status of the oyster, suggesting a role for TK signalling in the complex regulation of feeding in C. gigas.
Biostable multi-Aib analogs of tachykinin-related peptides demonstrate potent oral aphicidal activity in the pea aphid Acyrthosiphon pisum (Hemiptera: Aphidae)
2011, Peptides
Citation Excerpt :
The tachykinin-related peptides (TRPs; also designated ‘insectatachykinins’) are multifunctional neuropeptides found in several arthropod and invertebrate groups [4,13,18,22,26,28,29,42,44,45,68,69,70].
The tachykinin-related peptides (TRPs) are multifunctional neuropeptides found in a variety of arthropod species, including the pea aphid Acyrthosiphon pisum (Hemiptera: Aphidae). Two new biostable TRP analogs containing multiple, sterically hindered Aib residues were synthesized and found to exhibit significantly enhanced resistance to hydrolysis by angiotensin converting enzyme and neprilysin, membrane-bound enzymes that degrade and inactivate natural TRPs. The two biostable analogs were also found to retain significant myostimulatory activity in an isolated cockroach hindgut preparation, the bioassay used to isolate and identify the first members of the TRP family. Indeed one of the analogs (Leuma-TRP-Aib-1) matched the potency and efficacy of the natural, parent TRP peptide in this myotropic bioassay. The two biostable TRP analogs were further fed in solutions of artificial diet to the pea aphid over a period of 3 days and evaluated for antifeedant and aphicidal activity and compared with the effect of treatment with three natural, unmodified TRPs. The two biostable multi-Aib TRP analogs were observed to elicit aphicidal effects within the first 24 h. In contrast natural, unmodified TRPs, including two that are native to the pea aphid, demonstrated little or no activity. The most active analog, double-Aib analog Leuma-TRP-Aib-1 (pEA[Aib]SGFL[Aib]VR-NH₂), featured aphicidal activity calculated at an LC₅₀ of 0.0083 nmol/μl (0.0087 μg/μl) and an LT₅₀ of 1.4 days, matching or exceeding the potency of commercially available aphicides. The mechanism of this activity has yet to be established. The aphicidal activity of the biostable TRP analogs may result from disruption of digestive processes by interfering with gut motility patterns and/or with fluid cycling in the gut; processes shown to be regulated by the TRPs in other insects. These active TRP analogs and/or second generation analogs offer potential as environmentally friendly pest aphid control agents.
Tachykinin-related peptides and their receptors in invertebrates: A current view
2010, Peptides
Members of the tachykinin peptide family have been well conserved during evolution and are mainly expressed in the central nervous system and in the intestine of both vertebrates and invertebrates. In these animals, they act as multifunctional messengers that exert their biological effects by specifically interacting with a subfamily of structurally related G protein-coupled receptors. Despite the identification of multiple tachykinin-related peptides (TKRPs) in species belonging to the insects, crustaceans, mollusks and echiuroid worms, only five invertebrate receptors harboring profound sequence similarities to mammalian receptors for tachykinins have been functionally characterized to date. Three of these have been cloned from dipteran insect species, i.e. NKD (neurokinin receptor from Drosophila), DTKR (Drosophila tachykinin receptor) and STKR (tachykinin-related peptide receptor from the stable fly, Stomoxys calcitrans). In addition, two receptors from non-insect species, present in echiuroid worms and mollusks, respectively have been identified as well. In this brief review, we will survey some recent findings and insights into the signaling properties of invertebrate tachykinin-related peptides via their respective receptors. In this context, we will also point out the necessity to take into account differences in signaling mechanisms induced by distinct TKRP isoforms in insects.
Antimicrobial effect and membrane-active mechanism of Urechistachykinins, neuropeptides derived from Urechis unicinctus
2008, FEBS Letters
We investigated the antimicrobial effects of Urechistachykinins I and II (UI and UII) and their modes of action. UI and UII showed antimicrobial activities without a hemolytic effect. To investigate the mechanism(s) of UI and UII, cellular localization was examined. Confocal microscopy results showed that peptides were located in the cell envelope. To elucidate the physical changes of membrane induced by UI and UII in Candida albicans, flow cytometry analyses were performed by using bis-(1,3-dibutylbarbituric acid) trimethine oxonol, and changes in membrane dynamics were assessed using 1,6-diphenyl-1,3,5-hexatriene. The results suggest that UI and UII may exert their antimicrobial effect by disrupting the cell membranes.
Insect Neuropeptide and Peptide Hormone Receptors: Current Knowledge and Future Directions
2005, Vitamins and Hormones
Citation Excerpt :
In insects, immunoreactivity to vertebrate tachykinins was demonstrated multiple times, but the identification of the first tachykinin‐related peptides (TRPs, also designated as “insectatachykinins”) occurred in 1990 (Schoofs et al., 1990). After this initial discovery of the locustatachykinins (derived from Locusta migratoria), the number of known TRPs rapidly increased, with family members found in many other arthropod species and even in other invertebrate phyla, such as mollusks (Anastasi and Erspamer, 1962; Fujisawa et al., 1994; Kanda et al., 2003; Satake et al., 2003) and echiuroid worms (Ikeda et al., 1993; Kawada et al., 2000). With the exception of tachykinin‐like peptides from Aedes and Stomoxys, all known insect TRPs possess the C‐terminal consensus sequence FX1GX2Ra (Nässel, 1999; Vanden Broeck et al., 1999).
Peptides form a very versatile class of extracellular messenger molecules that function as chemical communication signals between the cells of an organism. Molecular diversity is created at different levels of the peptide synthesis scheme. Peptide messengers exert their biological functions via specific signal‐transducing membrane receptors. The evolutionary origin of several peptide precursor and receptor gene families precedes the divergence of the important animal Phyla. In this chapter, current knowledge is reviewed with respect to the analysis of peptide receptors from insects, incorporating many recent data that result from the sequencing of different insect genomes. Therefore, detailed information is provided on six different peptide receptor families belonging to two distinct receptor categories (i.e., the heptahelical and the single transmembrane receptors). In addition, the remaining problems, the emerging concepts, and the future prospects in this area of research are discussed.
Functional analysis of synthetic insectatachykinin analogs on recombinant neurokinin receptor expressing cell lines
2002, Peptides
The activity of a series of synthetic tachykinin-like peptide analogs was studied by means of microscopic calcium imaging on recombinant neurokinin receptor expressing cell lines. A C-terminal pentapeptide (FTGMRa) is sufficient for activation of the stomoxytachykinin receptor (STKR) expressed in Schneider 2 cells. Replacement of amino acid residues at the position of the conserved phenylalanine (F) or arginine (R) residues by alanine (A) results in inactive peptides (when tested at 1 μM), whereas A-replacements at other positions do not abolish the biological activity of the resulting insectatachykinin-like analogs. Calcium imaging was also employed to compare the activity of C-terminally substituted tachykinin analogs on three different neurokinin receptors. The results indicate that the major pharmacological and evolutionary difference between tachykinin-related agonists for insect (STKR) and human (NK1 and NK2) receptors resides in the C-terminal amino acid residues (R versus M). A single C-terminal amino acid change can turn an STKR-agonist into an NK-agonist and vice versa.

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Regular ArticleTwo Novel Tachykinin-Related Neuropeptides in the Echiuroid Worm, Urechis unicinctus

Abstract

Regular Article
Two Novel Tachykinin-Related Neuropeptides in the Echiuroid Worm, Urechis unicinctus