BgTEP: an antiprotease involved in innate immune sensing in Biomphalaria glabrata

Abstract

Insect Thioester-containing protein (iTEP) is the most recently defined group among the TEP superfamily. TEPs are key components of the immune system, and iTEPs from flies and mosquitoes were shown to be major immune weapons. Initially characterised from insects, TEP genes homologous to iTEP were further described from several other invertebrates including arthropods, cniderians and mollusks albeit with few functional characterisations. In the freshwater snail Biomphalaria glabrata, a vector of the schistosomiasis disease, the presence of a TEP protein (BgTEP) was previously described in a well-defined immune complex involving snail lectins (FREP) and schistosome parasite mucins (SmPoMuc).To investigate the potential role of BgTEP in the immune response of the snail, we first characterised its genomic organisation and its predicted protein structure. A phylogenetic analysis clustered BgTEP in a well-conserved subgroup of mollusk TEP. We then investigated the BgTEP expression profile in different snail tissues, and followed immune challenges using different kinds of intruders during infection kinetics. Results revealed that BgTEP is particularly expressed in hemocytes, the immune-specialised cells in invertebrates, and is secreted into the hemolymph. Transcriptomic results further evidenced an intruder-dependent differential expression pattern of BgTEP whilst interactome experiments showed that BgTEP is capable of binding to the surface of different microbes and parasite either in its full length form or in processed forms.Through this work, we report the first characterisation of a snail TEP. Our study also reveals that BgTEP may display an unexpected functional dual-role. In addition to its previously characterised anti-protease activity, we demonstrate that BgTEP can bind to the intruder surface membrane, which supports a likely opsonin role.

The immunobiological interplay between Pseudosuccinea columella resistant/susceptible snails with Fasciola hepatica: Hemocytes in the spotlight

“…While the functional role of blast-like cells remains unclear, perhaps these results indicate a potential stem-cell capacity in P. columella, considering that blast-like cells in molluscs from other taxa (caenogastropoda and bivalves) were proposed to be an immature stem cell-like developmental stage Iakovleva, 2008, Wang et al, 2012). Alternatively, blast-like cells have been also associated with crucial roles in pathogen interaction during infection through the production of molecular signals (Cima et al, 2000, Travers et al, 2008, Portet et al, 2018.…”

Molecular characterisation of immunological memory following homologous or heterologous challenges in the schistosomiasis vector snail, Biomphalaria glabrata

“…Finally, thioester-containing proteins (TEP) are complement-like proteins that act as opsonin, promoting phagocytosis, or lysis and sometimes even melanisation, in invertebrates (Le Clec'h et al, 2016), andarthropods (Blandin andLevashina, 2004;Buresova et al, 2011;Volohonsky et al, 2017) and appear to also participate in primary cellular immune response and encapsulation in Biomphalaria glabrata snails (Mitta et al, 2012;Mone et al, 2010;Portet et al, 2018a). Following immunological memory acquisition in Biomphalaria, the cellular immune encapsulation response shifts to a humoral response (Pinaud et al, 2016) and is associated with the down-regulation of TEP in the homologous challenge RNAseq data 15 days after the primo-infection (Figs.…”