Abstract
BackgroundTaenia pisiformis is one of the most common intestinal parasites in canines, and leads to serious economic losses in the rabbit breeding industry. Exosome-like vesicles from parasites play crucial roles in host-parasite interactions by transferring cargo from parasites to host cells and by modulating host immunological response through inducing production of host-derived cytokines. Nevertheless, the mechanism by which exosome-like vesicles from T. pisiformis cysticercus regulate the macrophage immune response remains unknown.MethodsUsing ultracentrifugation, we isolated exosome-like vesicles from excretory/secretory products (ESP) of T. pisiformis cysticercus. The morphology and size of purified vesicles were confirmed by transmission electron microscopy (TEM) and nanoparticle tracking analysis (NTA). The components of proteins and miRNAs within these vesicles were identified by proteomic analysis and high-throughput small RNA sequencing. The biological function of targets of exosomal miRNAs was predicted by Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis. Moreover, the expression of Th1- and Th2-type immune response associated cytokines in RAW264.7 macrophages were evaluated by qPCR and ELISA. We found that exosome-like vesicles were typical cup-shaped vesicles with diameters from 30 to 150 nm. A total of 87 proteins were identified by proteomic analysis, including proteins prominently associated with exosome-like vesicles biogenesis and vesicle trafficking. 41 known miRNAs and 18 novel miRNAs were identified in the exosome-like vesicles. Eleven selected miRNAs, including 7 known miRNAs (miR-71-5p, miR-10a-5p, miR-let-7-5p, miR-745-3p, miR-219-5p, miR-124-3p and miR-4989-3p) and 4 novel miRNAs (novel-mir-3, novel-mir-7, novel-mir-8 and novel-mir-11) were validated to exist in metacestiodes and exosome-like vesicles of T. pisiformis cysticercus by qPCR. The functions of most targets of exosomal miRNAs were mainly associated with signal transduction and the immune system. Additionally, T. pisiformis cysticercus-derived vesicles induced the production of IL-4, IL-6, IL-10, IL-13 and Arg-1, but downregulated the expression of IL-12, IFN-γ and iNOS in RAW264.7 macrophages.ConclusionsWe demonstrated that proteins and miRNAs enclosed within exosome-like vesicles from T. pisiformis cysticercus have immunomodulatory functions. Furthermore, exosome-like vesicles were shown to induce the macrophage Th2-type immune response in vitro. Our study suggests that exosome-like vesicles play an important role in the interaction between cysticerci and their hosts.
Highlights
Taenia pisiformis is one of the most common intestinal parasites in canines, and leads to serious eco‐ nomic losses in the rabbit breeding industry
We demonstrated that proteins and miRNAs enclosed within exosome-like vesicles from T. pisiformis cysticercus have immunomodulatory functions
Size and morphological analysis of T. pisiformis cysticercus‐derived exosome‐like vesicles To confirm the presence of exosome-like vesicles isolated from the culture medium of T. pisiformis cysticercus, the pellets obtained from sequential centrifugation were subjected to transmission electron micros‐ copy (TEM) and nanoparticle tracking analysis (NTA) analysis
Summary
Taenia pisiformis is one of the most common intestinal parasites in canines, and leads to serious eco‐ nomic losses in the rabbit breeding industry. The mechanism by which exosome-like vesicles from T. pisiformis cysticercus regulate the macrophage immune response remains unknown. A common intestinal tapeworm in canines and felines, is widely distributed around the world [1, 2]. Cysticercus pisiformis, the larval stage of T. pisiformis, causes considerable economic losses to the rabbit breeding industry [3]. Infection in the definitive host may occur when they consume lagomorph internal organs infected with T. pisiformis cysticercus. Rabbits infected with T. pisiformis have a weakened immunologic resistance and are susceptible to secondary infections with other pathogens, which may cause host digestive disorders, growth retardation, a decrease in feed conversion, reduction of proliferation, and even death [5]
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