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How the venom from the ectoparasitoid wasp Nasonia vitripennis exhibits anti-inflammatory properties on mammalian cell lines

Ellen Danneels (UGent) , Sarah Gerlo (UGent) , Karen Heyninck (UGent) , Kathleen Van Craenenbroeck (UGent) , Karolien De Bosscher (UGent) , Guy Haegeman (UGent) and Dirk de Graaf (UGent)
(2014) PLOS ONE. 9(5).
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Abstract
With more than 150,000 species, parasitoids are a large group of hymenopteran insects that inject venom into and then lay their eggs in or on other insects, eventually killing the hosts. Their venoms have evolved into different mechanisms for manipulating host immunity, physiology and behavior in such a way that enhance development of the parasitoid young. The venom from the ectoparasitoid Nasonia vitripennis inhibits the immune system in its host organism in order to protect their offspring from elimination. Since the major innate immune pathways in insects, the Toll and Imd pathways, are homologous to the NF-kappa B pathway in mammals, we were interested in whether a similar immune suppression seen in insects could be elicited in a mammalian cell system. A well characterized NF-kappa B reporter gene assay in fibrosarcoma cells showed a dose-dependent inhibition of NF-kappa B signaling caused by the venom. In line with this NF-kappa B inhibitory action, N. vitripennis venom dampened the expression of IL-6, a prototypical proinflammatory cytokine, from LPS-treated macrophages. The venom also inhibited the expression of two NF-kappa B target genes, I kappa B alpha and A20, that act in a negative feedback loop to prevent excessive NF-kappa B activity. Surprisingly, we did not detect any effect of the venom on the early events in the canonical NF-kappa B activation pathway, leading to NF-kappa B nuclear translocation, which was unaltered in venom-treated cells. The MAP kinases ERK, p38 and JNK are other crucial regulators of immune responses. We observed that venom treatment did not affect p38 and ERK activation, but induced a prolonged JNK activation. In summary, our data indicate that venom from N. vitripennis inhibits NF-kappa B signaling in mammalian cells. We identify venom-induced up regulation of the glucocorticoid receptor-regulated GILZ as a most likely molecular mediator for this inhibition.
Keywords
NF-KAPPA-B, SARCOPHAGA-BULLATA, ACTIVATED PROTEIN-KINASE, CULTURED INSECT CELLS, PAIN-RELATED BEHAVIORS, FLESH FLY, WALKER HYMENOPTERA, IMMUNE-RESPONSE, TRANSCRIPTION FACTORS, GENE-EXPRESSION

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MLA
Danneels, Ellen, et al. “How the Venom from the Ectoparasitoid Wasp Nasonia Vitripennis Exhibits Anti-Inflammatory Properties on Mammalian Cell Lines.” PLOS ONE, vol. 9, no. 5, 2014, doi:10.1371/journal.pone.0096825.
APA
Danneels, E., Gerlo, S., Heyninck, K., Van Craenenbroeck, K., De Bosscher, K., Haegeman, G., & de Graaf, D. (2014). How the venom from the ectoparasitoid wasp Nasonia vitripennis exhibits anti-inflammatory properties on mammalian cell lines. PLOS ONE, 9(5). https://doi.org/10.1371/journal.pone.0096825
Chicago author-date
Danneels, Ellen, Sarah Gerlo, Karen Heyninck, Kathleen Van Craenenbroeck, Karolien De Bosscher, Guy Haegeman, and Dirk de Graaf. 2014. “How the Venom from the Ectoparasitoid Wasp Nasonia Vitripennis Exhibits Anti-Inflammatory Properties on Mammalian Cell Lines.” PLOS ONE 9 (5). https://doi.org/10.1371/journal.pone.0096825.
Chicago author-date (all authors)
Danneels, Ellen, Sarah Gerlo, Karen Heyninck, Kathleen Van Craenenbroeck, Karolien De Bosscher, Guy Haegeman, and Dirk de Graaf. 2014. “How the Venom from the Ectoparasitoid Wasp Nasonia Vitripennis Exhibits Anti-Inflammatory Properties on Mammalian Cell Lines.” PLOS ONE 9 (5). doi:10.1371/journal.pone.0096825.
Vancouver
1.
Danneels E, Gerlo S, Heyninck K, Van Craenenbroeck K, De Bosscher K, Haegeman G, et al. How the venom from the ectoparasitoid wasp Nasonia vitripennis exhibits anti-inflammatory properties on mammalian cell lines. PLOS ONE. 2014;9(5).
IEEE
[1]
E. Danneels et al., “How the venom from the ectoparasitoid wasp Nasonia vitripennis exhibits anti-inflammatory properties on mammalian cell lines,” PLOS ONE, vol. 9, no. 5, 2014.
@article{5720607,
  abstract     = {{With more than 150,000 species, parasitoids are a large group of hymenopteran insects that inject venom into and then lay their eggs in or on other insects, eventually killing the hosts. Their venoms have evolved into different mechanisms for manipulating host immunity, physiology and behavior in such a way that enhance development of the parasitoid young. The venom from the ectoparasitoid Nasonia vitripennis inhibits the immune system in its host organism in order to protect their offspring from elimination. Since the major innate immune pathways in insects, the Toll and Imd pathways, are homologous to the NF-kappa B pathway in mammals, we were interested in whether a similar immune suppression seen in insects could be elicited in a mammalian cell system. A well characterized NF-kappa B reporter gene assay in fibrosarcoma cells showed a dose-dependent inhibition of NF-kappa B signaling caused by the venom. In line with this NF-kappa B inhibitory action, N. vitripennis venom dampened the expression of IL-6, a prototypical proinflammatory cytokine, from LPS-treated macrophages. The venom also inhibited the expression of two NF-kappa B target genes, I kappa B alpha and A20, that act in a negative feedback loop to prevent excessive NF-kappa B activity. Surprisingly, we did not detect any effect of the venom on the early events in the canonical NF-kappa B activation pathway, leading to NF-kappa B nuclear translocation, which was unaltered in venom-treated cells. The MAP kinases ERK, p38 and JNK are other crucial regulators of immune responses. We observed that venom treatment did not affect p38 and ERK activation, but induced a prolonged JNK activation. In summary, our data indicate that venom from N. vitripennis inhibits NF-kappa B signaling in mammalian cells. We identify venom-induced up regulation of the glucocorticoid receptor-regulated GILZ as a most likely molecular mediator for this inhibition.}},
  articleno    = {{e96825}},
  author       = {{Danneels, Ellen and Gerlo, Sarah and Heyninck, Karen and Van Craenenbroeck, Kathleen and De Bosscher, Karolien and Haegeman, Guy and de Graaf, Dirk}},
  issn         = {{1932-6203}},
  journal      = {{PLOS ONE}},
  keywords     = {{NF-KAPPA-B,SARCOPHAGA-BULLATA,ACTIVATED PROTEIN-KINASE,CULTURED INSECT CELLS,PAIN-RELATED BEHAVIORS,FLESH FLY,WALKER HYMENOPTERA,IMMUNE-RESPONSE,TRANSCRIPTION FACTORS,GENE-EXPRESSION}},
  language     = {{eng}},
  number       = {{5}},
  pages        = {{13}},
  title        = {{How the venom from the ectoparasitoid wasp Nasonia vitripennis exhibits anti-inflammatory properties on mammalian cell lines}},
  url          = {{http://doi.org/10.1371/journal.pone.0096825}},
  volume       = {{9}},
  year         = {{2014}},
}

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