The Venom of the Ectoparasitoid Wasp Pachycrepoideus vindemiae (Hymenoptera: Pteromalidae) Induces Apoptosis of Drosophila melanogaster Hemocytes

Abstract

The pupal ectoparasitoid Pachycrepoideus vindemiae injects venom into its fly hosts prior to oviposition. We have shown that this venom causes immune suppression in Drosophila melanogaster pupa but the mechanism involved remained unclear. Here, we show using transgenic D. melanogaster with fluorescent hemocytes that the in vivo number of plasmatocytes and lamellocytes decreases after envenomation while it has a limited effect on crystal cells. After in vitro incubation with venom, the cytoskeleton of plasmatocytes underwent rearrangement with actin aggregation around the internal vacuoles, which increased with incubation time and venom concentration. The venom also decreased the lamellocytes adhesion capacity and induced nucleus fragmentation. Electron microscopy observation revealed that the shape of the nucleus and mitochondria became irregular after in vivo incubation with venom and confirmed the increased vacuolization with the formation of autophagosomes-like structures. Almost all venom-treated hemocytes became positive for TUNEL assays, indicating massive induced apoptosis. In support, the caspase inhibitor Z-VAD-FMK attenuated the venom-induced morphological changes suggesting an involvement of caspases. Our data indicate that P. vindemiae venom inhibits D. melanogaster host immunity by inducing strong apoptosis in hemocytes. These assays will help identify the individual venom component(s) responsible and the precise mechanism(s)/pathway(s) involved.

Prostaglandin A2 induces apoptosis in three cell lines derived from the fall armyworm, Spodoptera frugiperda

“…Similarly, a parasitoid venom can inhibit host immunity by inducing hemocyte apoptosis. Venom injected from the ectoparasitoid wasp, Pachycrepoideus vindemiae , leads to reduced numbers of plasmatocytes and to reduced lamellocyte adhesion in Drosophila melanogastser hemocytes (Wan et al, 2020). The authors used TUNEL assays to document large‐scale venom‐induced apoptosis.…”

Extracellular Vesicles from Bothrops jararaca Venom Are Diverse in Structure and Protein Composition and Interact with Mammalian Cells

“…On the other hand, Ado is immunosuppressive when immune cells express P1 receptors [117][118][119][120]129], which may be related to the long-term effects of snakebites [24][25][26][27][28]. In accordance with this, a strong immune suppressive function is well characterized in EVs from wasp venoms [48,54,55].…”

“…The parasitoid wasp venom suppresses the Drosophila immune system, facilitating wasp offspring development and survival [48,53,141,142]. Notably, the macrophage-like immune cells of Drosophila internalize the wasp venom EVs that circulate in the hemolymph, which leads to the destruction of the phagolysosomal compartments and cause their death by apoptosis [54,55]. Based on the CD73 + PDE + phenotype found in Bj-EVs, we expect that the vesicles can modulate macrophages and other immune cells in vivo.…”

“…Many pathogens vs. host recipient cells crosstalk result in the modulation of pathogen adhesion and infectivity, allowing the transference of toxic molecules and virulence factors, increasing pathogen survival and immune system escape [39,46,47,51,52]. For example, in Drosophila, EVs from the parasitoid wasp venom suppress immune cells, increasing the wasp's offspring survival and parasitism success [48,[53][54][55].…”

Haemocyte‐mediated immunity in insects: Cells, processes and associated components in the fight against pathogens and parasites

“…Similarly, the infection of the silkworm, Bombyx mori , with Serratia marcescens and Porphyromonas gingivalis leads to caspase activation in the immune cells and suppression of insect immunity [210,211]. The venom of parasitoids contains cytotoxic proteins that are capable of inducing apoptosis in host hemocytes [212]. Apoptosis, however, can have an active role in the host immune response by helping the insect cope with the immune challenge.…”