Ampulexins: A New Family of Peptides in Venom of the Emerald Jewel Wasp, <i>Ampulex compressa</i>

Moore, Eugene; Arvidson, Ryan; Banks, Christopher N.; Urenda, Jean Paul; Duong, Elizabeth; Mohammed, Haroun; Adams, Michael E.

doi:10.1021/acs.biochem.7b00916

Cited by 9 publications

(16 citation statements)

References 47 publications

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“…Although VG and VS differ greatly in expression levels of certain venom transcripts, each has at least some level of expression for the great majority of venom proteins. For example, the ampulexins, among the most abundant venom components, are products primarily of the VS, confirming its functional role as a venom gland-independent contributor to the venom (11). We have demonstrated the acidic nature of A. compressa venom and that VS contents are more acidic than those of the venom gland, i.e.…”

Section: Discussionsupporting

confidence: 54%

“…Six of the 196 differentially expressed proteins are highly expressed in the VS, including four members of the recently described ampulexin family (11), and icarapin, a hymenopteran venom allergen (supplemental Fig. S3A).…”

Section: Resultsmentioning

confidence: 99%

“…Animal Husbandry-A. compressa and P. americana were reared as previously described (11). In brief: Single female wasps were housed with three males in 40 cm (W) ϫ 40 cm (L) ϫ 52 cm (H) plexiglass cages with the views of female wasps in adjacent cages occluded.…”

Section: Methodsmentioning

confidence: 99%

“…Extracellular polysaccharides are involved in many critical functions in the central nervous system, including axonal growth and synapse integrity (53,54). Dopamine and GABA are known to be present in the venom and induce grooming and temporary paralysis, respectively (3,11). To explore how these molecules are synthesized in the venom, we looked for expression of key enzymes in their biosynthesis in the venom apparatus transcriptome.…”

Section: Molecular and Cellular Proteomics 181 105mentioning

confidence: 99%

“…For example, short-term paralysis of prothoracic legs induced by the initial sting into the prothoracic ganglion, is caused by venom components GABA and GABA A receptor agonists ␤-alanine and taurine (10). The vigorous grooming response induced by stings into cephalic ganglia likely result from venom component dopamine (3,11).…”

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confidence: 99%

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Parasitoid Jewel Wasp Mounts Multipronged Neurochemical Attack to Hijack a Host Brain

Arvidson

Kaiser

Lee

et al. 2019

Molecular & Cellular Proteomics

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In BriefProteomic analysis of Ampulex compressa venom reveals a multifaceted attack on the host central nervous system. Rather than inducing paralysis or cytotoxicity, the venom appears to modify endogenous signaling, rendering the host lethargic and compliant. Some peptides and proteins in the venom are in precursor form, only to be processed into fully active form once injected into the pH-neutral host brain. This analysis deepens mechanistic understanding of venom action and points to signaling systems previously unrecognized in regulation of locomotion. Graphical Abstract Highlights• The venom transcriptome and proteome (venome) of Ampulex compressa are reported.• 264 proteins (enzymes, peptides, neurotransmitters) were detected.• The venom contains unprocessed neuropeptide precursors absent mature peptides.• Neuropeptide precursors likely are processed into active form upon envenomation.The parasitoid emerald jewel wasp Ampulex compressa induces a compliant state of hypokinesia in its host, the American cockroach Periplaneta americana through direct envenomation of the central nervous system (CNS). To elucidate the biochemical strategy underlying venominduced hypokinesia, we subjected the venom apparatus and milked venom to RNAseq and proteomics analyses to construct a comprehensive "venome," consisting of 264 proteins. Abundant in the venome are enzymes endogenous to the host brain, including M13 family metalloproteases, phospholipases, adenosine deaminase, hyaluronidase, and neuropeptide precursors. The amphipathic, alpha-helical ampulexins are among the most abundant venom components. Also prominent are members of the Toll/NF-B signaling pathway, including proteases Persephone, Snake, Easter, and the Toll receptor ligand Spä tzle. We find evidence that venom components are processed following envenomation. The acidic (pHϳ4) venom contains unprocessed neuropeptide tachykinin and corazonin precursors and is conspicuously devoid of the corresponding processed, biologically active peptides. Neutralization of venom leads to appearance of mature tachykinin and corazonin, suggesting that the wasp employs precursors as a prolonged time-release strategy within the host brain post-envenomation. Injection of fully processed tachykinin into host cephalic ganglia elicits short-term hypokinesia. Ion channel modifiers and cytolytic toxins are absent in A. compressa venom, which appears to hijack control of the host brain by introducing a "storm" of its own neurochemicals. Our findings deepen understanding of the chemical warfare underlying host-parasitoid interactions and in particular neuromodulatory mechanisms that enable manipulation of host behavior to suit the nutritional needs of opportunistic parasitoid progeny.

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Section: Discussionsupporting

confidence: 54%

Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%