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Schistosoma mansoni Eggs Modulate the Timing of Granuloma Formation to Promote Transmission.

ABSTRACT: Schistosome eggs provoke the formation of granulomas, organized immune aggregates, around them. For the host, the granulomatous response can be both protective and pathological. Granulomas are also postulated to facilitate egg extrusion through the gut lumen, a necessary step for parasite transmission. We used zebrafish larvae to visualize the granulomatous response to Schistosomamansoni eggs and inert egg-sized beads. Mature eggs rapidly recruit macrophages, which form granulomas within days. Beads also induce granulomas rapidly, through a foreign body response. Strikingly, immature eggs do not recruit macrophages, revealing that the eggshell is immunologically inert. Our findings suggest that the eggshell inhibits foreign body granuloma formation long enough for the miracidium to mature. Then parasite antigens secreted through the eggshell trigger granulomas that facilitate egg extrusion into the environment. In support of this model, we find that only mature S. mansoni eggs are shed into the feces of mice and humans.

SUBMITTER: Takaki KK

PROVIDER: S-EPMC7815046 | biostudies-literature | 2021 Jan

REPOSITORIES: biostudies-literature

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Schistosoma mansoni Eggs Modulate the Timing of Granuloma Formation to Promote Transmission.

Takaki Kevin K KK Rinaldi Gabriel G Berriman Matthew M Pagán Antonio J AJ Ramakrishnan Lalita L

Cell host & microbe 20201028 1

Schistosome eggs provoke the formation of granulomas, organized immune aggregates, around them. For the host, the granulomatous response can be both protective and pathological. Granulomas are also postulated to facilitate egg extrusion through the gut lumen, a necessary step for parasite transmission. We used zebrafish larvae to visualize the granulomatous response to Schistosomamansoni eggs and inert egg-sized beads. Mature eggs rapidly recruit macrophages, which form granulomas within days. B ...[more]

PMID: 33120115

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Project description:Protein variation in blood-dwelling schistosome worms generated by differential splicing of micro-exon gene transcripts. The infective schistosome cercaria develops from an undifferentiated germ ball within the daughter sporocyst in the molluscan host, during which considerable morphological development and synthesis of proteins essential for infection occurs. The free-living, non-feeding cercaria is notable for its swimming and host location behaviour. On contact with host skin it rapidly penetrates, replaces its tegument surface membranes, and begins body remodelling, before crossing the dermis to exit the skin via a blood vessel. Such a ‘violent’ transition from snail to fresh water to mammalian host should be accompanied by remarkable changes in the patterns of gene expression. All gene models from version E of the S. mansoni genome (www.GeneDB.org) were incorporated into a 350K feature Roche-NimbleGen, high-density oligonucleotide array. From a map-ordered list, every 13th 50mer was chosen as a probe. Double-stranded cDNA from three biological replicates each of germ balls, cercariae, and day 3 schistosomula was hybridised to the array without amplification. Statistical analysis was carried out using programmes from the Bioconductor suite (Gentleman et al. 2004 Genome Biol 5(10):R80). More than 1000 loci were shown to be differentially expressed in each of the comparisons between the three life cycle stages. Gene ontology (GO) analysis was then carried out to discover the categories enriched in each stage. In addition custom categories based on biological function (e.g. stress response) or parasite tissue (e.g. tegument) were analysed. Three biological replicates each of germ balls, cercariae, day 3 in vitro cultured schistosomula, and eggs were used. No technical replicates were included. This is the first genome-wide microarray platform for S. mansoni. It was used to investigate the gene expression patterns of the above lifecycle stages. The first three are the stages before, during and after penetration of mammalian host skin.

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Schistosoma mansoni Eggs Modulate the Timing of Granuloma Formation to Promote Transmission.

Publications

Schistosoma mansoni Eggs Modulate the Timing of Granuloma Formation to Promote Transmission.

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