Arthropod IGF, relaxin and gonadulin, putative orthologs of <i>Drosophila</i> insulin-like peptides 6, 7 and 8, likely originated from an ancient gene triplication

Veenstra, Jan A.

doi:10.7717/peerj.9534

Cited by 40 publications

(89 citation statements)

References 70 publications

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“…In the dilp8 mutant the effects might reflect the loss of action of endogeneous DILP8 on its receptor. However, it is possible that the ectopic DILP8 may act not only on the GPCR Lgr3, but also on the insulin receptor, dInR (a receptor tyrosine kinase), similar to the other Drosophila relaxin-like peptide, DILP7 (53,54). It was actually shown that dInR could be captured by DILP8 in a ligand capture assay, suggesting that DILP8 is able bind to both Lgr3 and dInR (13).…”

Section: Functional Roles Of Dilp8 Signalingmentioning

confidence: 99%

Drosophila Insulin-Like Peptide 8 (DILP8) in Ovarian Follicle Cells Regulates Ovulation and Metabolism

Liao

Nässel

2020

Front. Endocrinol.

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In Drosophila melanogaster eight insulin-like peptides (DILP1-8) are encoded on separate genes. These DILPs are characterized by unique spatial and temporal expression patterns during the lifecycle. Whereas, functions of several of the DILPs have been extensively investigated at different developmental stages, the role of DILP8 signaling is primarily known from larvae and pupae where it couples organ growth and developmental transitions. In adult female flies, a study showed that a specific set of neurons that express the DILP8 receptor, Lgr3, is involved in regulation of reproductive behavior. Here, we further investigated the expression of dilp8/DILP8 and Lgr3 in adult female flies and the functional role of DILP8 signaling. The only site where we found both dilp8 expression and DILP8 immunolabeling was in follicle cells around mature eggs. Lgr3 expression was detected in numerous neurons in the brain and ventral nerve cord, a small set of peripheral neurons innervating the abdominal heart, as well as in a set of follicle cells close to the oviduct. Ovulation was affected in dilp8 mutants as well as after dilp8-RNAi using dilp8 and follicle cell Gal4 drivers. More eggs were retained in the ovaries and fewer were laid, indicating that DILP8 is important for ovulation. Our data suggest that DILP8 signals locally to Lgr3 expressing follicle cells as well as systemically to Lgr3 expressing efferent neurons in abdominal ganglia that innervate oviduct muscle. Thus, DILP8 may act at two targets to regulate ovulation: follicle cell rupture and oviduct contractions. Furthermore, we could show that manipulations of dilp8 expression affect starvation resistance suggesting effects on metabolism. Possibly this reflects a feedback signaling between ovaries and the CNS that ensures nutrients for ovary development. In summary, it seems that DILP8 signaling in regulation of reproduction is an ancient function, conserved in relaxin signaling in mammals.

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Section: Functional Roles Of Dilp8 Signalingmentioning

confidence: 99%

Drosophila Insulin-Like Peptide 8 (DILP8) in Ovarian Follicle Cells Regulates Ovulation and Metabolism

Liao

Nässel

2020

Front. Endocrinol.

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“…Methods employed in bioinformatics have been described in detail in a previous manuscript (Veenstra, 2020). For the expression of SIFamide, SMYamide and their putative receptors in Periplaneta the followoing transcriptome short read archives (SRAs) were analyzed: DRR014884, DRR014885, DRR014886, DRR014887, DRR014888, DRR014889, SRR921630, SRR5286150, SRR5286151, SRR5286152, SRR5286153, SRR5286154, SRR1184457, SRR1184458, SRR1322009, SRR2994649, SRR2994650, SRR3056857, SRR3056858, SRR3089536, SRR3089537, SRR3089538, SRR3289663, SRR3289684, SRR3289687, SRR5097509, SRR5097510, SRR5097511, SRR5097512, SRR5097513, SRR5097514, SRR5097515 and SRR5097516.…”

Section: Methodsmentioning

confidence: 99%

“…Coding sequences for SIFamide and SMYamide precursors as well as those for putative SIFamide receptors were deduced from transcriptome and genome data as described (Veenstra, 2020). All these sequences are listed in the supplementary spreadsheet.…”

Section: Methodsmentioning

confidence: 99%

The neuropeptide SMYamide, a SIFamide paralog, is expressed by salivary gland innervating neurons in the American cockroach and likely functions as a hormone

Veenstra

2020

Preprint

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The SMYamide genes are paralogs of the SIFamide genes and code for neuropeptides that are structurally similar to SIFamide. In the American cockroach, Periplanea americana, the SMYamide gene is specifically expressed in the SN2 neurons that innervate the salivary glands and are known to produce action potentials during feeding. The innervation of the salivary glands by the SN2 neurons is such that one has to expect that on activation of these neurons significant amounts of SMYamide will be released into the hemolymph, thus suggesting that SMYamide also functions as a hormone. In the Periplaneta genome there are two putative SIFamide receptors and these are both expressed not only in the central nervous system and the salivary gland, but also in the gonads and other peripheral tissues. This reinforces the hypothesis that SMYamide also has an endocrine function in this species.

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“…The genomes were downloaded from https://www.ncbi.nlm.nih.gov/genome. For many of these species there are also significant amounts of RNAseq data and these were analyzed using the sratoolkit (https://trace.ncbi.nlm.nih.gov/Traces/sra/sra.cgi?view=software ) in combination with Trinity (Grabherr et al, 2011) using methods described in detail elsewhere (Veenstra, 2020b). Some protein sequences were found in the NCBI database, but several of them contain errors or are incomplete.…”

Section: Sequence Analysismentioning

confidence: 99%

“…This raises the interesting question as how this apparent jump from one type of receptor to another may have come about. In cockroaches, termites and stick insects three different irp genes, gonadulin, arthropod insulin-like growth factor (aIGF) and arthropod relaxin, are located next to one another in the genome and thus likely originated from a local gene triplication (Veenstra, 2020b). To avoid confusion with the vertebrate relaxins and related peptides, the arthropod relaxins will be referred to as Drosophila ilp7 (dilp7) in this manuscript.…”

Section: Introductionmentioning

confidence: 99%

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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Arthropod IGF, relaxin and gonadulin, putative orthologs of Drosophila insulin-like peptides 6, 7 and 8, likely originated from an ancient gene triplication

Cited by 40 publications

References 70 publications

Drosophila Insulin-Like Peptide 8 (DILP8) in Ovarian Follicle Cells Regulates Ovulation and Metabolism

Drosophila Insulin-Like Peptide 8 (DILP8) in Ovarian Follicle Cells Regulates Ovulation and Metabolism

The neuropeptide SMYamide, a SIFamide paralog, is expressed by salivary gland innervating neurons in the American cockroach and likely functions as a hormone

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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