Tegumental surface modulation in Schistosoma mansoni primary sporocysts in response to ligand binding

Abstract

The clearance of host molecules from the surface of a parasite constitutes a potential immune evasive strategy. The possibility that certain ligands, when bound to the tegument of Schistosoma mansoni primary sporocysts, could induce such a modulating effect was investigated. Live, in vitro cultured primary sporocysts were first treated with either snail host Biomphalaria glabrata plasma, an anti-sporocyst monoclonal antibody (MoAb III-1), or concanavalin A (con A). The capacity of these primary ligands to produce a modulating effect alone, or when subsequently crosslinked by secondary or tertiary ligands, was measured using quantitative fluorescence microscopy. Snail plasma alone, or plasma crosslinked at the sporocyst surface with a mouse anti-plasma MoAb had little or no modulating effect. However, a tertiary level of ligand crosslinking with an anti-mouse IgG antibody produced an average 1.8-fold decrease in surface fluorescence within 1 h post-labelling. The anti-sporocyst MoAb III-1 also required secondary antibody reactivity to induce an average 1.5-fold decrease in MoAb III-1 recognized epitopes. Sporocysts labelled with con A crosslinked by secondary and tertiary ligands showed inconsistent modulation, with a 1.5-fold decrease in fluorescence in one out of three replicates. Overall, however, analysis of combined data revealed no significant effect of tertiary ligand level crosslinkage on modulation of con A-tegumental receptor complexes. In contrast, con A binding alone to tegumental determinants induced a small, but significant, reduction in surface con A complexes. Modulation of ligand-receptor complexes on the sporocyst tegumental membrane appears to be an energy-requiring event, since clearance of surface complexes was inhibited in the presence of sodium azide and/or sodium iodoacetate, or when larvae were incubated at 4 degrees C. It is concluded that alterations in sporocyst tegumental surface components may be triggered by specific (but as yet undefined) signals. Sporocysts are capable of exhibiting different responses depending on the nature of the binding signal and reactive tegumental receptor, and the degree of ligand crosslinkage.

Parasite-Invertebrate Host Immune Interactions

“…As an alternative explanation, they hypothesized that Con A binding may be inducing a modulation of tegumental lectin determinants, thereby providing an altered parasite surface capable of stimulating cytotoxic activation. This notion is supported by the recent finding that Con A binding to sporocysts in vitro induces a time-and energy-dependent modulation of receptor-lectin complexes at the larval surface, apparently through a membrane shedding process (Dunn and Yoshino 1991). Regardless of the mechanism involved, it appears that exogenous lectins can facilitate hemocyte-parasite immune interactions.…”

When Appearance Misleads: The Role of the Entomopathogen Surface in the Relationship with Its Host

“…Several pathogen cytotoxic molecules, either released or on the surface, can interfere with immunocompetent cell functions, inhibiting adhesion, altering cytoskeletal protein assembly, damaging the plasmalemma, and inducing cell death [37]. Molecular disguise, another form of mimicry, is described as the acquisition (sequestering) of molecular components from the host [1,43,44] to form a body coating antigenically related to the host [45][46][47][48][49]. A Strepsiptera (Stichotrema dallatorreanum) implements an alternative disguise mechanism, using the host epidermal tissues to wrap itself in a sort of bag that camouflages the endoparasite, making it immune to the recognition of the insect [50]; this strategy allows the parasite to carry out the necessary trophic exchanges within the host body that are essential for its development and reproduction.…”