Aphidius ervi Teratocytes Release Enolase and Fatty Acid Binding Protein Through Exosomal Vesicles.

Rosanna Salvia,Annalisa Grimaldi,Heiko Vogel,Sabino A Bufo,Andrea Scala,Carmen Scieuzo,Rossana Girardello,Patrizia Falabella

doi:10.3389/fphys.2019.00715

Abstract

The molecular bases of the host-parasitoid interactions in the biological system Acyrthosiphon pisum (Harris) (Homoptera, Aphididae) and Aphidius ervi (Haliday) (Hymenoptera, Braconidae) have been elucidated allowing the identification of a gamma-glutamyl transpeptidase, the active component of maternal venom secretion, and teratocytes, the embryonic parasitic factors responsible for host physiology regulation after parasitization. Teratocytes, cells deriving from the dissociation of the serosa, the parasitoid embryonic membrane, are responsible for extra-oral digestion of host tissues in order to provide a suitable nutritional environment for the development of parasitoid larvae. Teratocytes rapidly grow in size without undergoing any cell division, synthesize, and release in the host hemolymph two proteins: a fatty acid binding protein (Ae-FABP) and an enolase (Ae-ENO). Ae-FABP is involved in transport of fatty acids deriving from host tissues to the parasitoid larva. Ae-ENO is an extracellular glycolytic enzyme that functions as a plasminogen like receptor inducing its activation to plasmin. Both Ae-FABP and Ae-ENO lack their signal peptides, and they are released in the extracellular environment through an unknown secretion pathway. Here, we investigated the unconventional mechanism by which teratocytes release Ae-FABP and Ae-ENO in the extracellular space. Our results, obtained using immunogold staining coupled with TEM and western blot analyses, show that these two proteins are localized in vesicles released by teratocytes. The specific dimension of these vesicles and the immunodetection of ALIX and HSP70, two exosome markers, strongly support the hypothesis that these vesicles are exosomes.

Highlights

Teratocytes are specialized cells derived from the embryonic serosal membrane dissociation during parasitoid egg hatching in some hymenopteran endoparasitoid species (Dahlman and Vinson, 1993; Hotta et al, 2001; Strand, 2014)
This mechanism seems to be shared by some micro-organisms that use an extracellular enolase to invade host tissues (Chavez-Munguia et al, 2011) and by several parasitic helminths releasing proteins, including enolase, through extracellular vesicles (Marcilla et al, 2012). We demonstrate that these vesicles are exosomes, mediating the extracellular transport of proteins lacking a signal peptide
Teratocytes and Aphidius ervi larva observed in the host hemocoel 5 days after parasitization (B)

Summary

Introduction

Teratocytes are specialized cells derived from the embryonic serosal membrane dissociation during parasitoid egg hatching in some hymenopteran endoparasitoid species (Dahlman and Vinson, 1993; Hotta et al, 2001; Strand, 2014). Teratocytes rapidly grow in size without cell division, become highly polyploid, and release molecules impacting physiology, development, and nutritional suitability of colonized hosts (Dahlman and Vinson, 1993; Dahlman et al, 2003; Beckage and Gelman, 2004; Pennacchio and Strand, 2006). These large cells are characterized by a microvillar cell membrane, abundant endoplasmic reticulum, and numerous mitochondria, indicating that they are metabolically active (Pennacchio et al, 1994; Zhang et al, 1994). The nutritional role of teratocytes is generally mediated by digestion of selected host tissues, which release nutrients in a suitable form for the developing larvae (Falabella et al, 2000, 2009; Nakamatsu et al, 2002; Strand, 2014)

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