Virulence in Mice of a Toxoplasma gondii Type II Isolate Does Not Correlate With the Outcome of Experimental Infection in Pregnant Sheep

Toxoplasma gondii is an apicomplexan parasite that infects almost all warm-blooded animals. Little is known about how the parasite virulence in mice extrapolates to other relevant hosts. In the current study, in vitro phenotype and in vivo behavior in mice and sheep of a type II T. gondii isolate (T...

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Main Authors: Roberto Sánchez-Sánchez, Ignacio Ferre, Javier Regidor-Cerrillo, Daniel Gutiérrez-Expósito, Luis Miguel Ferrer, Noive Arteche-Villasol, Javier Moreno-Gonzalo, Joachim Müller, Adriana Aguado-Martínez, Valentín Pérez, Andrew Hemphill, Luis Miguel Ortega-Mora, Julio Benavides
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-01-01
Series:Frontiers in Cellular and Infection Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fcimb.2018.00436/full
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author Roberto Sánchez-Sánchez
Ignacio Ferre
Javier Regidor-Cerrillo
Daniel Gutiérrez-Expósito
Luis Miguel Ferrer
Noive Arteche-Villasol
Javier Moreno-Gonzalo
Joachim Müller
Adriana Aguado-Martínez
Valentín Pérez
Andrew Hemphill
Luis Miguel Ortega-Mora
Julio Benavides
author_facet Roberto Sánchez-Sánchez
Ignacio Ferre
Javier Regidor-Cerrillo
Daniel Gutiérrez-Expósito
Luis Miguel Ferrer
Noive Arteche-Villasol
Javier Moreno-Gonzalo
Joachim Müller
Adriana Aguado-Martínez
Valentín Pérez
Andrew Hemphill
Luis Miguel Ortega-Mora
Julio Benavides
author_sort Roberto Sánchez-Sánchez
collection DOAJ
description Toxoplasma gondii is an apicomplexan parasite that infects almost all warm-blooded animals. Little is known about how the parasite virulence in mice extrapolates to other relevant hosts. In the current study, in vitro phenotype and in vivo behavior in mice and sheep of a type II T. gondii isolate (TgShSp1) were compared with the reference type II T. gondii isolate (TgME49). The results of in vitro assays and the intraperitoneal inoculation of tachyzoites in mice indicated an enhanced virulence for the laboratory isolate, TgME49, compared to the recently obtained TgShSp1 isolate. TgShSp1 proliferated at a slower rate and had delayed lysis plaque formation compared to TgME49, but it formed more cyst-like structures in vitro. No mortality was observed in adult mice after infection with 1–105 tachyzoites intraperitoneally or with 25–2,000 oocysts orally of TgShSp1. In sheep orally challenged with oocysts, TgME49 infection resulted in sporadically higher rectal temperatures and higher parasite load in cotyledons from ewes that gave birth and brain tissues of the respective lambs, but no differences between these two isolates were found on fetal/lamb mortality or lesions and number of T. gondii-positive lambs. The congenital infection after challenge at mid-pregnancy with TgShSp1, measured as offspring mortality and vertical transmission, was different depending on the challenged host. In mice, mortality in 50% of the pups was observed when a dam was challenged with a high oocyst dose (500 TgShSp1 oocysts), whereas in sheep infected with the same dose of oocysts, mortality occurred in all fetuses. Likewise, mortality of 9 and 27% of the pups was observed in mice after infection with 100 and 25 TgShSp1 oocysts, respectively, while in sheep, infection with 50 and 10 TgShSp1 oocysts triggered mortality in 68 and 66% of the fetuses/lambs. Differences in vertical transmission in the surviving offspring were only found with the lower oocyst doses (100% after infection with 10 TgShSp1 oocysts in sheep and only 37% in mice after infection with 25 TgShSp1 oocysts). In conclusion, virulence in mice of T. gondii type II isolates may not be a good indicator to predict the outcome of infection in pregnant sheep.
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spelling doaj.art-39c152ab6ae0487a94c768fd8eaed1602022-12-22T03:36:45ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882019-01-01810.3389/fcimb.2018.00436425588Virulence in Mice of a Toxoplasma gondii Type II Isolate Does Not Correlate With the Outcome of Experimental Infection in Pregnant SheepRoberto Sánchez-Sánchez0Ignacio Ferre1Javier Regidor-Cerrillo2Daniel Gutiérrez-Expósito3Luis Miguel Ferrer4Noive Arteche-Villasol5Javier Moreno-Gonzalo6Joachim Müller7Adriana Aguado-Martínez8Valentín Pérez9Andrew Hemphill10Luis Miguel Ortega-Mora11Julio Benavides12SALUVET, Animal Health Department, Faculty of Veterinary Sciences, Complutense University of Madrid, Madrid, SpainSALUVET, Animal Health Department, Faculty of Veterinary Sciences, Complutense University of Madrid, Madrid, SpainSALUVET, Animal Health Department, Faculty of Veterinary Sciences, Complutense University of Madrid, Madrid, SpainInstituto de Ganadería de Montaña (CSIC-Universidad de León), León, SpainDepartamento de Patología Animal, Facultad de Veterinaria, University of Zaragoza, Zaragoza, SpainInstituto de Ganadería de Montaña (CSIC-Universidad de León), León, SpainSALUVET, Animal Health Department, Faculty of Veterinary Sciences, Complutense University of Madrid, Madrid, SpainVetsuisse Faculty, Institute of Parasitology, University of Bern, Bern, SwitzerlandVetsuisse Faculty, Institute of Parasitology, University of Bern, Bern, SwitzerlandInstituto de Ganadería de Montaña (CSIC-Universidad de León), León, SpainVetsuisse Faculty, Institute of Parasitology, University of Bern, Bern, SwitzerlandSALUVET, Animal Health Department, Faculty of Veterinary Sciences, Complutense University of Madrid, Madrid, SpainInstituto de Ganadería de Montaña (CSIC-Universidad de León), León, SpainToxoplasma gondii is an apicomplexan parasite that infects almost all warm-blooded animals. Little is known about how the parasite virulence in mice extrapolates to other relevant hosts. In the current study, in vitro phenotype and in vivo behavior in mice and sheep of a type II T. gondii isolate (TgShSp1) were compared with the reference type II T. gondii isolate (TgME49). The results of in vitro assays and the intraperitoneal inoculation of tachyzoites in mice indicated an enhanced virulence for the laboratory isolate, TgME49, compared to the recently obtained TgShSp1 isolate. TgShSp1 proliferated at a slower rate and had delayed lysis plaque formation compared to TgME49, but it formed more cyst-like structures in vitro. No mortality was observed in adult mice after infection with 1–105 tachyzoites intraperitoneally or with 25–2,000 oocysts orally of TgShSp1. In sheep orally challenged with oocysts, TgME49 infection resulted in sporadically higher rectal temperatures and higher parasite load in cotyledons from ewes that gave birth and brain tissues of the respective lambs, but no differences between these two isolates were found on fetal/lamb mortality or lesions and number of T. gondii-positive lambs. The congenital infection after challenge at mid-pregnancy with TgShSp1, measured as offspring mortality and vertical transmission, was different depending on the challenged host. In mice, mortality in 50% of the pups was observed when a dam was challenged with a high oocyst dose (500 TgShSp1 oocysts), whereas in sheep infected with the same dose of oocysts, mortality occurred in all fetuses. Likewise, mortality of 9 and 27% of the pups was observed in mice after infection with 100 and 25 TgShSp1 oocysts, respectively, while in sheep, infection with 50 and 10 TgShSp1 oocysts triggered mortality in 68 and 66% of the fetuses/lambs. Differences in vertical transmission in the surviving offspring were only found with the lower oocyst doses (100% after infection with 10 TgShSp1 oocysts in sheep and only 37% in mice after infection with 25 TgShSp1 oocysts). In conclusion, virulence in mice of T. gondii type II isolates may not be a good indicator to predict the outcome of infection in pregnant sheep.https://www.frontiersin.org/article/10.3389/fcimb.2018.00436/fullToxoplasma gondiitype IIvirulencephenotypic traitsmicesheep
spellingShingle Roberto Sánchez-Sánchez
Ignacio Ferre
Javier Regidor-Cerrillo
Daniel Gutiérrez-Expósito
Luis Miguel Ferrer
Noive Arteche-Villasol
Javier Moreno-Gonzalo
Joachim Müller
Adriana Aguado-Martínez
Valentín Pérez
Andrew Hemphill
Luis Miguel Ortega-Mora
Julio Benavides
Virulence in Mice of a Toxoplasma gondii Type II Isolate Does Not Correlate With the Outcome of Experimental Infection in Pregnant Sheep
Frontiers in Cellular and Infection Microbiology
Toxoplasma gondii
type II
virulence
phenotypic traits
mice
sheep
title Virulence in Mice of a Toxoplasma gondii Type II Isolate Does Not Correlate With the Outcome of Experimental Infection in Pregnant Sheep
title_full Virulence in Mice of a Toxoplasma gondii Type II Isolate Does Not Correlate With the Outcome of Experimental Infection in Pregnant Sheep
title_fullStr Virulence in Mice of a Toxoplasma gondii Type II Isolate Does Not Correlate With the Outcome of Experimental Infection in Pregnant Sheep
title_full_unstemmed Virulence in Mice of a Toxoplasma gondii Type II Isolate Does Not Correlate With the Outcome of Experimental Infection in Pregnant Sheep
title_short Virulence in Mice of a Toxoplasma gondii Type II Isolate Does Not Correlate With the Outcome of Experimental Infection in Pregnant Sheep
title_sort virulence in mice of a toxoplasma gondii type ii isolate does not correlate with the outcome of experimental infection in pregnant sheep
topic Toxoplasma gondii
type II
virulence
phenotypic traits
mice
sheep
url https://www.frontiersin.org/article/10.3389/fcimb.2018.00436/full
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