Dataset Information

Stings on wings: venom proteomics and tissue transcriptomics of the lesser banded hornet, Vespa affinis

ABSTRACT: The project aims at unraveling the venom repertoire of the lesser banded hornet (Vespa affinis) and investigate the regimes of natural selection underpinning their venom evolution. The study also sheds light on the clinical repercussions of the V. affinis venom.

INSTRUMENT(S): Orbitrap Fusion

ORGANISM(S): Vespa Affinis

TISSUE(S): Venom

SUBMITTER: Kartik Sunagar

LAB HEAD: Dr Kartik Sunagar

PROVIDER: PXD037171 | Pride | 2023-03-10

REPOSITORIES: pride

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Publications

Stings on wings: Proteotranscriptomic and biochemical profiling of the lesser banded hornet (<i>Vespa affinis</i>) venom.

Sunagar Kartik K Khochare Suyog S Jaglan Anurag A Senthil Samyuktha S Suranse Vivek V

Frontiers in molecular biosciences 20221219

Distinct animal lineages have convergently recruited venoms as weaponry for prey capture, anti-predator defence, conspecific competition, or a combination thereof. Most studies, however, have been primarily confined to a narrow taxonomic breadth. The venoms of cone snails, snakes, spiders and scorpions remain particularly well-investigated. Much less explored are the venoms of wasps (Order: Hymenoptera) that are infamous for causing excruciating and throbbing pain, justifying their apex position ...[more]

PMID: 36601583

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Project description:Spider venoms are a unique source of bioactive peptides displaying remarkable structural stability and potent neuroactivity. Phoneutria nigriventer, often referred to as Brazilian wandering spider, banana spider or “armed” spider, is endemic from South America and amongst the most dangerous venomous spiders in the world. Envenomation accidents with P. nigriventer often occur in Brazil with approximately 4,000 cases per year and which symptoms include priapism, hypertension, blurred vision, sweating, and vomiting, amongst others. Besides its clinical relevance, P. nigriventer venom comprises promising peptide drug leads providing therapeutic effects in a range of disease models. In this study, we further explored the neuroactivity and molecular diversity of the venom from P. nigriventer using fractionation-guided high-throughput cellular assays coupled to proteomics analysis and multi-pharmacology activity to broaden the knowledge and therapeutic potential of this venom, as well as a proof-of-concept for an investigative pipeline to study spider-venom derived neuroactive peptides. We applied ion channel assays in a neuroblastoma cell line to investigate modulation of voltage-gated sodium and calcium channels, and nicotinic acetylcholine α7 receptor. We then investigated the venom components using mass spectrometry to identify peptide masses and sequences associated to the observed neuromodulations. Our findings showed this venom is highly complex compared to other neurotoxin-rich venoms and comprises potent modulators of voltage-gated sodium and calcium channels which were classified into 4 families of neuroactive peptides based on their activities and structures. In addition to the reported P. nigriventer neuroactive peptides, we identified at least 27 novel cysteine-rich venom peptides in which neuroactivities are still to be elucidated in voltage-gated ion channels and other potential targets. Our findings provide a new basis for studying non-explored bioactivities of known and novel neuroactive components in P. nigriventer venom, and further supports the successful application of our discovery pipeline for identifying ion channel-targeting venom peptides with potential to become drug leads with diverse exploratory and therapeutic applications.

Project description:Background The generalist dipteran pupal parasitoid Nasonia vitripennis injects 79 venom peptides into the host before egg laying. This venom induces several important changes in the host, including developmental arrest, immunosuppression, and alterations to normal metabolism. It is hoped that diverse and potent bioactivities of N. vitripennis venom provide an opportunity for the design of novel acting drugs. However, currently very little is known about the individual functions of N. vitripennis venom peptides and less than half can be bioinformatically annotated. The paucity of annotation information complicates the design of studies that seek to better understand the potential mechanisms underlying the envenomation response. Although the RNA interference system of N. vitripennis provides an opportunity to functionally characterise venom encoding genes, with 79 candidates this represents a daunting task. For this reason we were interested in determining the expression levels of venom encoding genes in the venom gland, such that this information could be used to rank candidate venoms. To do this we carried out deep sequencing of the transcriptome of the venom gland and neighbouring ovary tissue and used RNA-seq to measure expression from the 79 venom encoding genes. The generation of a specific venom gland transcriptome dataset also provides further opportunities to investigate novel features of this highly specialised organ. Results High throughput sequencing and RNA-seq revealed that the highest expressed venom encoding gene in the venom gland was a serine protease called Nasvi2EG007167, which has previously been implicated in the apoptotic activity of N. vitripennis venom. As expected the RNA-seq confirmed that the N. vitripennis venom encoding genes are almost exclusively expressed in the venom gland relative to the neighbouring ovary tissue. Novel peptides appear to perform key roles in N. vitripennis venom function as only four of the highest 15 expressed venom encoding genes are bioinformatically annotationed. The high throughput sequencing data also provided evidence for the existence of an additional 471 novel genes in the Nasonia genome that are expressed in the venom gland and ovary. Finally, metagenomic analysis of venom gland transcripts identified viral transcripts that may play an important part in the N. vitripennis venom function. Conclusions The expression level information provided here for the 79 venom encoding genes provides an unbiased dataset that can be used by the N. vitripennis community to identify high value candidates for further functional characterisation. These candidates represent bioactive peptides that have value in drug development pipelines.

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