Molecular pathways shared between host-parasitoid interaction in insect and other animals: The case of teratocyte extracellular enolase

Molecular pathways shared between host-parasitoid interaction in insect and other animals: The case of teratocyte extracellular enolase Introduction: Enolase is an ubiquitous metalloenzyme involved in the glycolytic pathway. Interestingly it appears also as a multifunctional protein. Enolases anchored on the outer surface of the plasma membrane are involved in tissue invasion mechanisms by the activation of Plasminogen. Methods: To determine the Enolase localization and its capacity to bind and activate the plasminogen, experiments of immunogold labeling, indirect immunofluorescence staining, co-localization, binding and activation in vitro assay, Duolink in situ Proximity Ligation Assay (PLA) and dot blotting assay were carried out. Furthermore the Enolase ability to degrade extracellular matrix was in vitro evaluated by a Matrix digestion assay. Results/Conclusion: We have identified an extracellular Enolase (Ae-ENO) produced by teratocytes, embryonic cells of the insect parasitoid Aphidius ervi (Hymenoptera, Braconidae). For the first time we demonstrate that Ae-ENO, although lacking a signal peptide, accumulates in cytoplasmic vesicles oriented towards the cell membrane. Ae-ENO binds and activates a plasminogen-like molecule inducing digestion of the host tissue and thereby ensuring successful parasitism. The results support the hypothesis of the existence of plasminogen-like proteins in invertebrates and their activation through mechanisms involving the surface enolase/fibrinolytic system that until now seemed to be exclusively found in vertebrates, and that is conserved across species. These findings also suggest that Ae-ENO is a novel and unique example of gene sharing in insects.