Biology subjects

Veenstra, J. A.

Publications and source records attributed to Veenstra, J. A..

13 recordsLinked to original sources

bioRxiv2024

Elimination of the neuroparsin neuroendocrine cells in Drosophila virilis using the UAS-Gal4 system shows that neuroparsin is not important for reproduction in this species.

Neuroparsin is a common insect neurohormone produced in large neuroendocrine cells in the brain and is important in mosquito reproduction. Although it is present in many flies including many Drosophila species, it was lost from D. melanogaster and a few closely related species. Three different lines of transgenic D. virilis were produced: One that expresses the yeast transcription factor gal4 under the control of the neuroparsin promoter (NP-gal4), while others codes for proteins under the control of the gal4 promoter, either enhanced green fluorescent protein (UAS-eGFP) or the D. virilis ortholog of reaper, an apoptosis inducing protein (UAS-rpr). Crosses between UAS-eGFP and NP-gal4 revealed that expression of NP-gal4 was correct. Crosses between UAS-rpr and NP-gal4 completely eliminated the neuroparsin neuroendocrine cells, but were without effect on reproduction.

neuroscience↗

bioRxiv2024

Neuropeptides from a praying mantis: What the loss of pyrokinins and tryptopyrokinins suggests about the endocrine functions of these peptides

BackgroundNeuropeptides play important roles in insects, but in many cases their functions remain obscure. Comparative neuropeptidome analyses may provide clues to what these functions might be. Praying mantises are predators and close relatives of cockroaches that are scavengers. Cockroach neuropeptidomes are well established, but little is known about mantis neuropeptides. The recently published genome assembly of the praying mantis Tenodera sinensis makes it possble to change that. MethodsThe genome assembly from T. sinensis was analyzed for the presence of genes coding neuropeptides. For comparison publicly available short read archives from this and other mantis species were also examined for the presence and expression of neuropeptides. ResultsAs a rule the neuropeptidomes of the Mantodea and Blattodea are almost identical; praying mantises and cockroaches use very similar neuropeptides. However, there is one surprising exception. Praying mantises lack the receptors for pyrokinins, including those for the tryptopyrokinins. No typical pyrokinin genes were found, but some species do have a tryptopyrokinin gene, in others this has also been lost and in one species it is a speudogene. For most praying mantises there is no information where tryptopyrokinin is expressed, but in Deroplatys truncata it is in the thorax and thus not in the suboesophageal ganglion as in other insects. In the genomic short read archives of two species - out 52 - sequences were found for a tryptopyrokinin specific receptor. The phylogenetic position of those two species implies that the receptor gene was independently lost on multiple occasions. The loss of the tryptopyrokinin gene also happened more than once. DiscussionThe multiple independent losses of the pyrokinin receptors in mantises suggests that these receptors are irrelevant in praying mantises. This is very surprising, since expression of tryptopyrokinin is very strongly conserved in two neuroendocrine cells in the suboeosphageal ganglion. In those species for which this is known, the expression of its receptor is in the salivary gland. As a neuroendocrine. tryptopyrokinin is unlikely to acutely regulate salivation, which in other insects is regulated by well characterized neurons. If the action of tryptopyrokinin were to prime the salivary gland for subsequent salivation, it would make perfect sense for a praying mantis to loose this capacity, as they can not anticipate when they will catch their next prey. Priming the salivary gland hours before it is actually needed would be energetically costly. The other pyrokinins are known to facilitate feeding and may in a similar fashion prime muscles needed for moving to the food source and digesting it. This hypothesis provides a good explanation as to why praying mantises do not need pyrokinins and also what the function of these ubiquitous arthropod neuropeptides may be.

zoology↗

bioRxiv2024

Drosophila Glue Expulsion and Spreading Behavior is Modulated by Neuropeptidergic Mip-SPR Signaling from a Descending Command Neuron

At the end of their growth phase, Drosophila larvae remodel their bodies, firmly glue themselves to a substrate, and harden their cuticle in preparation for metamorphosis. This process is termed pupariation and it is triggered by a surge in the steroid hormone ecdysone. Substrate attachment is achieved by a recently-described pupariation subprogram called glue expulsion and spreading behavior (GSB). An epidermis-to-CNS Dilp8-Lgr3 relaxin signaling event that occurs downstream of ecdysone after pupariation initiation is critical for unlocking progression of the pupariation motor program towards GSB, but the factors and circuits acting downstream of Lgr3 signaling remain unknown. Here, we screened for such factors using cell type-specific RNA interference (RNAi) and behavioral monitoring. We identify Myoinhibiting peptide (Mip) and its highly conserved neuronal receptor, Sex peptide receptor (SPR), as a critical neuropeptidergic signaling pathway required to trigger and modulate multiple action components of GSB. In addition, we find that Mip is specifically required in a pair of descending neurons, whose optogenetic activation at a specific competence window triggers GSB-like behavior and whose neurogenetic silencing completely abrogates GSB without overtly affecting other pupariation components. This strongly suggests that these descending Mip neurons are developmentally-regulated GSB command neurons. Dissection of the GSB action components via muscle calcium-level monitoring coupled with cell-type specific RNAi indicates that Mip acts on multiple SPR-positive neuronal populations, which collectively define and pattern the sequence and timing of GSB actions. Hence, we have identified a pair of descending command neurons that utilize both synaptic transmission and neuropeptidergic signaling to trigger and modulate a complex innate behavior in Drosophila. Our results advance our molecular and cellular understanding of pupariation control, reveal the complexity of glue expulsion and spreading behavior control, provide insight into conserved aspects of Mip-SPR signaling in animals, and contribute to the understanding of how multi-step innate behaviors are coordinated in time and with other developmental processes through command neurons and neuropeptidergic signaling.

neuroscience↗

bioRxiv2023

Pigment-Dispersing Factor is present in circadian clock neurons of pea aphids and may mediate photoperiodic signaling to insulin-producing cells

The neuropeptide Pigment-Dispersing Factor (PDF) plays a pivotal role in the circadian clock of most Ecdysozoa and is additionally involved in the timing of seasonal responses of several photoperiodic species. The pea aphid, Acyrthosiphon pisum, is a paradigmatic photoperiodic species with an annual life cycle tightly coupled to the seasonal changes in day length. Nevertheless, PDF could not be identified in A. pisum so far. In the present study, we identified a PDF-coding gene that has undergone significant changes in the otherwise highly conserved insect C-terminal amino acid sequence. A newly generated aphid-specific PDF antibody stained four neurons in each hemisphere of the aphid brain that co-express the clock protein Period and have projections to the pars lateralis that are highly plastic and change their appearance in a daily and seasonal manner, resembling those of the fruit fly PDF neurons. Most intriguingly, the PDF terminals overlap with dendrites of the insulin-like peptide (ILP) positive neurosecretory cells in the pars intercerebralis and with putative terminals of Cryptochrome (CRY) positive clock neurons. Since ILP has been previously shown to be crucial for seasonal adaptations and CRY might serve as a circadian photoreceptor vital for measuring day length, our results suggest that PDF plays a critical role in aphid seasonal timing.

cell biology↗

bioRxiv2023

Differential expression of some termite neuropeptides and insulin/IGF-related hormones and their plausible functions in growth, reproduction and caste determination

BackgroundInsulin-like growth factor (IGF) and other Insulin-like peptides (ilps) are important hormones regulating growth and development in animals. Whereas most animals have a single female and male adult phenotype, in some insect species the same genome may lead to different final forms. Perhaps the best known example is the honeybee where females can either develop into queens or workers. More extreme forms of such polyphenism occur in termites, where queens, kings, workers and soldiers coexist. Both juvenile hormone and insulin-like peptides are known to regulate growth and reproduction as well as polyphenism. In termites the role of juvenile hormone in reproduction and the induction of the soldier caste is well known, but the role of IGF and other ilps in these processes remains largely unknown. Here the various termite ilps are identified and hypotheses regarding their functions suggested. MethodsGenome assemblies and transcriptome short read archives (SRAs) were used to identify insulin-like peptides and neuropeptides in termites and to determine their expression in different species, tissues and castes. Results and DiscussionTermites have seven different ilps, i.e. gonadulin, IGF and an ortholog of Drosophila insulin-like peptide 7 (dilp7), which are commonly present in insects, and four smaller peptides, that have collectively been called short IGF-related peptides (sirps) and individually atirpin, birpin, cirpin and brovirpin. Gonadulin is lost from the higher termites which have however amplified the brovirpin gene, of which they often have two or three paralogs. Based on differential expression of these genes it seems likely that IGF is a growth hormone and atirpin an autocrine tissue factor that is released when a tissue faces metabolic stress. Birpin seems to be responsible for growth and in the absence of juvenile hormone this may lead to reproductive adults or, when juvenile hormone is present, to soldiers. Brovirpin is expressed both by the brain and the ovary and likely stimulates vitellogenesis, while the function of cirpin is less clear.

zoology↗

bioRxiv2022

Different neuroendocrine cell types in the pars intercerebralis of Periplaneta americana produce their own specific IGF-related peptides

Of the nine genes of the American cockroach, Periplaneta americana, coding for peptides related to insulin and insulin-like growth factor, seven show significant expression in the central nervous system as demonstrated by the polymerase chain reaction on reverse transcribed RNA. In situ hybridisation shows that five of those are expressed by cells in the pars intercerebralis. Antisera raised to the predicted peptides show that these cells are neuroendocrine in nature and project to the corpora cardiaca. Interestingly, there are at least three cell types that each express different genes. This contrasts with Drosophila where a single cell type expresses a number of genes expressing several such peptides. Whereas in Drosophila the neuroendocrine cells producing insulin-like peptides also express sulfakinins, the arthropod orthologs of gastrin and cholecystokinin, in Periplaneta the sulfakinins are produced by different cells. Other neuropeptides known to be produced by the pars intercerebralis in Periplaneta and other insect species, such as the CRF-like diuretic hormone, neuroparsin, leucokinin or myosuppressin, neither colocalize with an insulin-related peptide. The separate cellular localization of these peptides and the existence of multiple insulin receptors in this species implies a more complex regulation by insulin and IGF-related peptides in cockroaches than in the fruit fly.

zoology↗

bioRxiv2021

Identification of cells expressing Calcitonins A and B, PDF and ACP in Locusta migratoria using cross-reacting antisera and in situ hybridization

This work was initiated because an old publication suggested that electrocoagulation of four paraldehyde fuchsin positive cells in the brain of Locusta migratoria might produce a diuretic hormone, the identity of which remains unknown, since none of the antisera to the various putative Locusta diuretic hormones recognizes these cells. The paraldehyde fuchsin positive staining suggests a peptide with a disulfide bridge and the recently identified Locusta calcitonins have both a disulfide bridge and are structurally similar to calcitonin-like diuretic hormone. In situ hybridization and antisera raised to calcitonin-A and -B were used to show were these peptides are expressed in Locusta. Calcitonin-A is produced by neurons and neuroendocrine cells that were previously shown to be immunoreactive to an antiserum to pigment dispersing factor (PDF). The apparent PDF-immunoreactivity in these neurons and neuroendocrine cells is due to crossreactivity with the calcitonin-A precursor. As confirmed by both an PDF-precursor specific antiserum and in situ hybridisation, those calcitonin-A expressing cells do not express PDF. Calcitonin B is expressed by numerous enteroendocrine cells in the midgut as well as the midgut caeca. A guinea pig antiserum to calcitonin A seemed quite specific as it recognized only the calcitonin A expressing cells. However, rabbit antisera to calcitonin-A and-B both crossreacted with neuroendocrine cells in the brain that produce ACP, this is almost certainly due to the common C-terminal dipeptide SPamide that is shared between Locusta calcitonin-A, calcitonin-B and ACP.

neuroscience↗

bioRxiv2021

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

BackgroundSome 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, 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 how insulin might be related to this trio of irps. MethodologyGenes encoding irps as well as their putative receptors were identified in genomes and transcriptomes from echinoderms and hemichordates. ResultsA similar triplet of genes coding for irps is also found 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 than 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, it seems to suggest that 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. ConclusionThe 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.

zoology↗

bioRxiv2020

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

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.

zoology↗

bioRxiv2020

Arthropod ILGF, Relaxin and Gonadulin, putative orthologs of Drosophila insulin-like peptides 6, 7 and 8, likely originated from an ancient gene triplication

Background Insects have several genes coding for insulin-like peptides and they have been particularly well studied in Drosophila. Some of these hormones function as growth hormones and are produced by the fat body and the brain. These act through a typical insulin receptor tyrosine kinase. Two other Drosophila insulin-like hormones are either known or suspected to act through a G-protein coupled receptor. Although insulin-related peptides are known from other insect species, Drosophila insulin-like peptide 8, one that uses a G-protein coupled receptor, has so far only been identified from Drosophila and other flies. However, its receptor is widespread within arthropods and hence it should have orthologs. Such putative orthologs were recently identified in decapods and have been called gonadulins.Methodology In an effort to identify gonadulins in other arthropods public genome assemblies and short-read archives from insects and other arthropods were explored for the presence of genes and transcripts coding insulin-like peptides and their putative receptors.Results Gonadulins were detected in a number of arthropods. In those species for which transcriptome data from the gonads is available insect gonadulin genes are expressed in the ovaries and at least in some species also in the testes. In some insects differences in gonadulin expression in the ovary between actively reproducing and non-reproducing females differs more than 100-fold. Putative orthologs of Drosophila ilp 6 were also identified. In several non-Dipteran insects these peptides have C-terminally extensions that are alternatively spliced. The predicted peptides have been called arthropod insulin-like growth factors. In cockroaches, termites and stick insects genes coding for the arthropod insulin-like growth factors, gonadulin and relaxin, a third insulin-like peptide, are encoded by genes that are next to one another suggesting that they are the result of a local gene triplication. Such a close chromosomal association was also found for the arthropod insulin-like growth factor and gonadulin genes in spiders. Phylogenetic tree analysis of the typical insulin receptor tyrosine kinases from insects, decapods and chelicerates shows that the insulin signaling pathway evolved differently in these three groups. The G-protein coupled receptors that are related to the Drosophila ilp 8 receptor similarly show significant differences between those groups.Conclusion A local gene triplication in an early ancestor likely yielded three genes coding gonadulin, arthropod insulin-like growth factor and relaxin. Orthologs of these genes are now commonly present in arthropods and almost certainly include the Drosophila insulin-like peptides 6, 7 and 8.Competing Interest StatementThe authors have declared no competing interest.View Full Text

zoology↗

bioRxiv2020

Gonadulins, the fourth type of Insulin-related peptides in Decapods

Insulin and related peptides play important roles in the regulation of growth and reproduction. Until recently three different types of insulin-related peptides had been identified from decapod crustaceans. The identification of two novel insulin-related peptides from Sagmariasus verreauxi and Cherax quadricarinatus by Chandler and colleagues (doi: 10.3390/ijms18091832) suggested that there might a fourth type. Publicly available short read archives show that orthologs of these peptides are commonly present in these animals. Most decapods have two genes coding such peptides, but Penaeus species have likely only one and some palaemonids have three. The peptides they encode have been called gonadulins, as they seem consistently expressed by the gonads. Interestingly, expression levels can vary thousand-fold within ovary and testis of Portunus trituberculatus, where gonadulin 1 is expressed by the testis and gonadulin 2 by the ovary.View Full Text

zoology↗

bioRxiv2019

The hormone neuroparsin seems essential in Lepidoptera but not in domesticated silkworms

The primary sequence of the Arthropod neurohormone neuroparsin is so variable that so far no orthologs from moths and butterflies have been characterized, even though classical neurosecretory stains identify cells that are homologous to those producing this hormone in other insect species. Here Lepidopteran cDNAs showing limited sequence similarity to other insect neuroparsins are described. That these cDNAs do indeed code for authentic neuroparsins was confirmed by in situ hybridization in the wax moth, Galleria mellonella, which labeled the neuroparsin neuroendocrine cells. Although in virtually all genome assemblies from Lepidoptera a neuroparsin gene could be identified, the genome assembly from the silkworm, Bombyx mori, has a neuroparsin gene containing a 16 nucleotide deletion that renders this gene nonfunctional. Although only a small number of all silkworm strains carry this deletion, it suggests that the domestication of the silkworm has rendered the function of this neurohormone dispensable.

evolutionary biology↗

bioRxiv2018

Drosophila insulin-like peptide 1 (DILP1) promotes organismal growth during non-feeding stages

The insulin/IGF-signaling pathway is central in control of nutrient-dependent growth during development, and in adult physiology and longevity. Eight insulin-like peptides (DILP1-8) have been identified in Drosophila and several of these are known to regulate growth, metabolism, reproduction, stress responses and lifespan. However, the functional role of DILP1 is far from understood. Previous work has shown that dilp1/DILP1 is transiently expressed mainly during the non-feeding pupal stage and the first days of adult life. Here we show that mutation of dilp1 diminishes organismal weight during pupal development, whereas overexpression increases it, similar to dilp6 manipulations. No growth effects of dilp1 or dilp6 manipulations were detected during larval development. We next show that dilp1 and dilp6 increase metabolic rate in the late pupa and promote lipids as the primary source of catabolic energy. This lipid mobilization in the pupa is not correlated with transcriptional changes of adipokinetic hormone. The effects of dilp1 manipulations carry over to the adult fly. In newly eclosed flies, survival during starvation is strongly diminished in dilp1 mutants, but not in dilp2 and dilp1-dilp2 double mutants, whereas in older flies only double mutants display reduced starvation resistance. In conclusion, dilp1 and dilp6 promote growth of adult tissues during the non-feeding pupal stage, likely by utilization of stored lipids. This results in larger newly-eclosed flies with reduced stores of pupal-derived nutrients and diminished starvation tolerance and fecundity.

neuroscience↗