Suppression of inflammatory genes expression in the injured host intestinal wall during Mesocestoides vogae tetrathyridium larvae migration.

Mesocestoides vogae is a cestode parasite of the family Mesocestoididae (order Cyclophyllidea). Its larvae, tetrathyridium, are approximately 1 mm long and 300 μm wide and infect a wide range of host species including humans. Tetrathyridium migrate through the intestinal wall to invade the peritonea...

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Main Authors: Kei Hayashi, Rinako Sugisawa, Taizo Saito, Toshiyasu Matsui, Yuji Taniguchi, Tatiana Batanova, Tokuma Yanai, Jun Matsumoto, Katsuya Kitoh, Yasuhiro Takashima
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2020-10-01
Series:PLoS Neglected Tropical Diseases
Online Access:https://doi.org/10.1371/journal.pntd.0008685
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author Kei Hayashi
Rinako Sugisawa
Taizo Saito
Toshiyasu Matsui
Yuji Taniguchi
Tatiana Batanova
Tokuma Yanai
Jun Matsumoto
Katsuya Kitoh
Yasuhiro Takashima
author_facet Kei Hayashi
Rinako Sugisawa
Taizo Saito
Toshiyasu Matsui
Yuji Taniguchi
Tatiana Batanova
Tokuma Yanai
Jun Matsumoto
Katsuya Kitoh
Yasuhiro Takashima
author_sort Kei Hayashi
collection DOAJ
description Mesocestoides vogae is a cestode parasite of the family Mesocestoididae (order Cyclophyllidea). Its larvae, tetrathyridium, are approximately 1 mm long and 300 μm wide and infect a wide range of host species including humans. Tetrathyridium migrate through the intestinal wall to invade the peritoneal cavity. Despite intestinal penetration by such a large-sized parasite, symptomatic intestinal disorders are not common during the migration period. In this study, the dynamics of tetrathyridia migration and their pathogenicity towards intestinal tissues were examined in mice infected orally with these parasites. Most tetrathyridia were found to migrate through the intestinal wall, moving into the peritoneal cavity or liver 24 to 48 hours after the oral infections. Next, the pathogenicity of tetrathyridium in the intestinal wall was histopathologically evaluated, and tissue injury from tetrathyridium migration was confirmed. Inflammatory foci were observed as tetrathyridium migration tracks from 48 hours after oral infection; however, the number of inflammatory foci had decreased by half more than 48 hours later. Therefore, we examined the gene expression levels of the macrophage driving cytokine, IL-1β, and the eosinophil recruiting chemokine, CCL11, by quantitative reverse-transcriptase PCR. The expression levels of these genes in the infected group were significantly lower than those of the non-infected group at 48 hours post-infection. Although the immunomodulating ability of the excretory-secretory products released from tetrathyridium has been previously shown by in vitro assays, the significance of this ability in their lifecycle has remained unclear. In this study, we discovered that tetrathyridium causes temporal inflammation in the intestinal wall during penetration and large-scale migration in this organ, but tetrathyridium simultaneously suppresses the host's inflammatory gene expression, might to be a strategy that reduces inflammatory responses and increases survival of the parasite.
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spelling doaj.art-9d7240c012454c39b822b583295b52032022-12-21T21:32:15ZengPublic Library of Science (PLoS)PLoS Neglected Tropical Diseases1935-27271935-27352020-10-011410e000868510.1371/journal.pntd.0008685Suppression of inflammatory genes expression in the injured host intestinal wall during Mesocestoides vogae tetrathyridium larvae migration.Kei HayashiRinako SugisawaTaizo SaitoToshiyasu MatsuiYuji TaniguchiTatiana BatanovaTokuma YanaiJun MatsumotoKatsuya KitohYasuhiro TakashimaMesocestoides vogae is a cestode parasite of the family Mesocestoididae (order Cyclophyllidea). Its larvae, tetrathyridium, are approximately 1 mm long and 300 μm wide and infect a wide range of host species including humans. Tetrathyridium migrate through the intestinal wall to invade the peritoneal cavity. Despite intestinal penetration by such a large-sized parasite, symptomatic intestinal disorders are not common during the migration period. In this study, the dynamics of tetrathyridia migration and their pathogenicity towards intestinal tissues were examined in mice infected orally with these parasites. Most tetrathyridia were found to migrate through the intestinal wall, moving into the peritoneal cavity or liver 24 to 48 hours after the oral infections. Next, the pathogenicity of tetrathyridium in the intestinal wall was histopathologically evaluated, and tissue injury from tetrathyridium migration was confirmed. Inflammatory foci were observed as tetrathyridium migration tracks from 48 hours after oral infection; however, the number of inflammatory foci had decreased by half more than 48 hours later. Therefore, we examined the gene expression levels of the macrophage driving cytokine, IL-1β, and the eosinophil recruiting chemokine, CCL11, by quantitative reverse-transcriptase PCR. The expression levels of these genes in the infected group were significantly lower than those of the non-infected group at 48 hours post-infection. Although the immunomodulating ability of the excretory-secretory products released from tetrathyridium has been previously shown by in vitro assays, the significance of this ability in their lifecycle has remained unclear. In this study, we discovered that tetrathyridium causes temporal inflammation in the intestinal wall during penetration and large-scale migration in this organ, but tetrathyridium simultaneously suppresses the host's inflammatory gene expression, might to be a strategy that reduces inflammatory responses and increases survival of the parasite.https://doi.org/10.1371/journal.pntd.0008685
spellingShingle Kei Hayashi
Rinako Sugisawa
Taizo Saito
Toshiyasu Matsui
Yuji Taniguchi
Tatiana Batanova
Tokuma Yanai
Jun Matsumoto
Katsuya Kitoh
Yasuhiro Takashima
Suppression of inflammatory genes expression in the injured host intestinal wall during Mesocestoides vogae tetrathyridium larvae migration.
PLoS Neglected Tropical Diseases
title Suppression of inflammatory genes expression in the injured host intestinal wall during Mesocestoides vogae tetrathyridium larvae migration.
title_full Suppression of inflammatory genes expression in the injured host intestinal wall during Mesocestoides vogae tetrathyridium larvae migration.
title_fullStr Suppression of inflammatory genes expression in the injured host intestinal wall during Mesocestoides vogae tetrathyridium larvae migration.
title_full_unstemmed Suppression of inflammatory genes expression in the injured host intestinal wall during Mesocestoides vogae tetrathyridium larvae migration.
title_short Suppression of inflammatory genes expression in the injured host intestinal wall during Mesocestoides vogae tetrathyridium larvae migration.
title_sort suppression of inflammatory genes expression in the injured host intestinal wall during mesocestoides vogae tetrathyridium larvae migration
url https://doi.org/10.1371/journal.pntd.0008685
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