Discrete escape responses are generated by neuropeptide-mediated circuit logic

Imambocus, Bibi Nusreen; Wittich, Annika; Tenedini, Federico; Zhou, Fangmin; Hu, Chun; Sauter, Kathrin; Varela, Ednilson Mascarenhas; Herédia, Fabiana; Casimiro, Andreia P.; Macedo, André; Yang, Chung-Hui; Schlegel, Philipp; Pankratz, Michael J.; Miguel-Aliaga, Irene; Gontijo, Alisson M.; Cardona, Albert; Soba, Peter

doi:10.1101/2020.09.22.307033

Cited by 4 publications

(4 citation statements)

References 86 publications

(103 reference statements)

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“…Another LGR identified (Pt-GPCR-A33) clustered with relaxin receptor (LGR4,type C1 LGR). Recent experimental evidence from D. melanogaster suggests LGR4 activated by dilp7, which has also been called relaxin ( Imambocus et al., 2020 ). In insects, relaxin influences lipid synthesis and regulates egg laying decisions ( Semaniuk et al., 2018 ; Yang et al., 2008 ).…”

Section: Resultsmentioning

confidence: 99%

Identification and characterization of expression profiles of neuropeptides and their GPCRs in the swimming crab, Portunus trituberculatus

Wang

et al. 2021

PeerJ

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Neuropeptides and their G protein-coupled receptors (GPCRs) regulate multiple physiological processes. Currently, little is known about the identity of native neuropeptides and their receptors in Portunus trituberculatus. This study employed RNA-sequencing and reverse transcription-polymerase chain reaction (RT-PCR) techniques to identify neuropeptides and their receptors that might be involved in regulation of reproductive processes of P. trituberculatus. In the central nervous system transcriptome data, 47 neuropeptide transcripts were identified. In further analyses, the tissue expression profile of 32 putative neuropeptide-encoding transcripts was estimated. Results showed that the 32 transcripts were expressed in the central nervous system and 23 of them were expressed in the ovary. A total of 47 GPCR-encoding transcripts belonging to two classes were identified, including 39 encoding GPCR-A family and eight encoding GPCR-B family. In addition, we assessed the tissue expression profile of 33 GPCRs (27 GPCR-As and six GPCR-Bs) transcripts. These GPCRs were found to be widely expressed in different tissues. Similar to the expression profiles of neuropeptides, 20 of these putative GPCR-encoding transcripts were also detected in the ovary. This is the first study to establish the identify of neuropeptides and their GPCRs in P. trituberculatus, and provide information for further investigations into the effect of neuropeptides on the physiology and behavior of decapod crustaceans.

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Section: Resultsmentioning

confidence: 99%

Identification and characterization of expression profiles of neuropeptides and their GPCRs in the swimming crab, Portunus trituberculatus

Wang

et al. 2021

PeerJ

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“…One of the irps, aIGF, is known to use an insulin RTK, while gonadulin acts through insect LGR3 ( Vallejo et al, 2015 ; Garelli et al, 2015 ; Colombani et al, 2015 ). Bioinformatic evidence suggested that dilp7 must be the ligand for insect LGR4, and this has now been confirmed experimentally in Drosophila ( Veenstra, Rombauts & Grbić, 2012 ; Imambocus et al, 2020 ), but dilp7 may also activate an RTK ( Linneweber et al, 2014 ). This suggests that the archtype arthropod IGF-related peptide acted through both an RTK and an LGR and that after a likely gene triplication, some of the ligands may have lost one of the two original receptors.…”

Section: Introductionmentioning

confidence: 82%

Ambulacrarian insulin-related peptides and their putative receptors suggest how insulin and similar peptides may have evolved from insulin-like growth factor

Veenstra

2021

PeerJ

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Background Some insulin/IGF-related peptides (irps) stimulate a receptor tyrosine kinase (RTK) that transfers the extracellular hormonal signal into an intracellular response. Other irps, such as relaxin, do not use an RTK, but a G-protein coupled receptor (GPCR). This is unusual since evolutionarily related hormones typically either use the same or paralogous receptors. In arthropods three different irps, i.e. arthropod IGF, gonadulin and Drosophila insulin-like peptide 7 (dilp7), likely evolved from a gene triplication, as in several species genes encoding these three peptides are located next to one another on the same chromosomal fragment. These arthropod irps have homologs in vertebrates, suggesting that the initial gene triplication was perhaps already present in the last common ancestor of deuterostomes and protostomes. It would be interesting to know whether this is indeed so and how insulin might be related to this trio of irps. Methodology Genes encoding irps as well as their putative receptors were identified in genomes and transcriptomes from echinoderms and hemichordates. Results A similar triplet of genes coding for irps also occurs in some ambulacrarians. Two of these are orthologs of arthropod IGF and dilp7 and the third is likely a gonadulin ortholog. In echinoderms, two novel irps emerged, gonad stimulating substance (GSS) and multinsulin, likely from gene duplications of the IGF and dilp7-like genes respectively. The structures of GSS diverged considerably from IGF, which would suggest they use different receptors from IGF, but no novel irp receptors evolved. If IGF and GSS use different receptors, and the evolution of GSS from a gene duplication of IGF is not associated with the appearance of a novel receptor, while irps are known to use two different types of receptors, the ancestor of GSS and IGF might have acted on both types of receptors while one or both of its descendants act on only one. There are three ambulacrarian GPCRs that have amino acid sequences suggestive of being irp GPCRs, two of these are orthologs of the gonadulin and dilp7 receptors. This suggests that the third might be an IGF receptor, and that by deduction, GSS only acts on the RTK. The evolution of GSS from IGF may represent a pattern, where IGF gene duplications lead to novel genes coding for shorter peptides that activate an RTK. It is likely this is how insulin and the insect neuroendocrine irps evolved independently from IGF. Conclusion The local gene triplication described from arthropods that yielded three genes encoding irps was already present in the last common ancestor of protostomes and deuterostomes. It seems plausible that irps, such as those produced by neuroendocrine cells in the brain of insects and echinoderm GSS evolved independently from IGF and, thus, are not true orthologs, but the result of convergent evolution.

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“…One of these, aIGF, is known to use an insulin RTK, while gonadulin acts through insect LGR3 (Vallejo et al, 2015;Garelli et al, 2015;Colombani et al, 2015). Bioinformatic evidence suggested that dilp7 must be the ligand for insect LGR4 and this has now been confirmed experimentally in Drosophila (Veenstra, Rombauts & Grbić, 2012;Imambocus et al, 2020), but dilp7 may also activate an RTK (Linneweber et al, 2014). This suggests that the archtype arthropod IGF-related peptide acted through both an RTK and an LGR and that after a likely gene triplication, some of the ligands may have lost one of the two original receptors.…”

Section: Introductionmentioning

confidence: 85%

Ambulacrarian insulin-related peptides and their putative receptors suggest how insulin and similar peptides may have evolved from Insulin-like Growth Factor

Veenstra

2021

Preprint

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Background: Insulin is evolutionarily related to the insulin-like growth factors (IGFs) and like the latter stimulates a receptor tyrosine kinase (RTK) that transfers the extracellular hormonal signal into an intracellular response. Other hormones related to insulin, such as relaxin, do not use an RTK, but a G-protein coupled receptor (GPCR). This is unusual since evolutionarily related hormones typically either use the same or paralogous receptors. In arthropods three different IGF-related peptides likely evolved from a gene triplication, as in several species genes coding these three peptides are located next to one another on the same chromosomal fragment. Of these three hormones one, an IGF-like hormone, acts through an RTK, while the other two use a GPCR. This suggests that the ancestral IGF-like peptide may have used both types of receptors. These arthropod insulin-like peptides have homologs in vertebrates, which suggests that the initial gene triplication was perhaps already present in the last common ancestor of deuterostomes and protostomes. It would be interesting to know whether this is indeed so and to establish how insulin and other insulin-like peptides might be related to this trio of IGF-related hormones. Methodology: Genes coding insulin and related peptides as well as their putative receptors were identified in genomes and transcriptomes from echinoderms and hemichordates. Results: A similar triplet of genes coding insulin-like peptides is also found in some hemichordates and echinoderms. Two of the three ambulacrarian peptides are orthologs of arthropod IGF and Drosophila insulin-like peptide 7 (dilp7), while the third one looks like an ortholog of the arthropod peptide gonadulin. In echinoderms two novel insulin-like peptides emerged, gonad stimulating substance (GSS) and multinsulin, likely from gene duplications of the IGF and dilp7-like genes respectively. However, no novel receptors for insulin-like peptides evolved. If IGF were to act through both a GPCR and an RTK it would suggest that GSS acts on only one of the two receptors, possibly the RTK. The evolution of GSS from IGF may represent a pattern, where IGF gene duplications lead to novel genes coding shorter peptides that have lost their ability to activate a GPCR. It is likely this is how insulin and the insect neuroendocrine insulin-like peptides evolved independently from IGF. Conclusion: The local gene triplication previously described from arthropods that yielded three genes coding IGF-related peptides was already present in the last common ancestor of protostomes and deuterostomes. It seems plausible that insulin and other insulin-like peptides, such as those produced by neuroendocrine cells in the brain of insects and echinoderm GSS evolved independently from IGF and thus are not true orthologs, but the result of convergent evolution.

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Discrete escape responses are generated by neuropeptide-mediated circuit logic

Cited by 4 publications

References 86 publications

Identification and characterization of expression profiles of neuropeptides and their GPCRs in the swimming crab, Portunus trituberculatus

Identification and characterization of expression profiles of neuropeptides and their GPCRs in the swimming crab, Portunus trituberculatus

Ambulacrarian insulin-related peptides and their putative receptors suggest how insulin and similar peptides may have evolved from insulin-like growth factor

Ambulacrarian insulin-related peptides and their putative receptors suggest how insulin and similar peptides may have evolved from Insulin-like Growth Factor

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