Strain-Dependent Host Transcriptional Responses to Toxoplasma Infection Are Largely Conserved in Mammalian and Avian Hosts

Strain-Dependent Host Transcriptional Responses to Toxoplasma Infection Are Largely Conserved in Mammalian and Avian Hosts

Toxoplasma gondii has a remarkable ability to infect an enormous variety of mammalian and avian species. Given this, it is surprising that three strains (Types I/II/III) account for the majority of isolates from Europe/North America. The selective pressures that have driven the emergence of these pa...

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Main Authors: Ong, Yi-Ching, Boyle, Jon P., Boothroyd, John C.
Format: Online
Language:English
Published: Public Library of Science 2011
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3192797/
id pubmed-3192797
recordtype oai_dc
spelling pubmed-31927972011-10-21 Strain-Dependent Host Transcriptional Responses to Toxoplasma Infection Are Largely Conserved in Mammalian and Avian Hosts Ong, Yi-Ching Boyle, Jon P. Boothroyd, John C. Research Article Toxoplasma gondii has a remarkable ability to infect an enormous variety of mammalian and avian species. Given this, it is surprising that three strains (Types I/II/III) account for the majority of isolates from Europe/North America. The selective pressures that have driven the emergence of these particular strains, however, remain enigmatic. We hypothesized that strain selection might be partially driven by adaptation of strains for mammalian versus avian hosts. To test this, we examine in vitro, strain-dependent host responses in fibroblasts of a representative avian host, the chicken (Gallus gallus). Using gene expression profiling of infected chicken embryonic fibroblasts and pathway analysis to assess host response, we show here that chicken cells respond with distinct transcriptional profiles upon infection with Type II versus III strains that are reminiscent of profiles observed in mammalian cells. To identify the parasite drivers of these differences, chicken fibroblasts were infected with individual F1 progeny of a Type II x III cross and host gene expression was assessed for each by microarray. QTL mapping of transcriptional differences suggested, and deletion strains confirmed, that, as in mammalian cells, the polymorphic rhoptry kinase ROP16 is the major driver of strain-specific responses. We originally hypothesized that comparing avian versus mammalian host response might reveal an inversion in parasite strain-dependent phenotypes; specifically, for polymorphic effectors like ROP16, we hypothesized that the allele with most activity in mammalian cells might be less active in avian cells. Instead, we found that activity of ROP16 alleles appears to be conserved across host species; moreover, additional parasite loci that were previously mapped for strain-specific effects on mammalian response showed similar strain-specific effects in chicken cells. These results indicate that if different hosts select for different parasite genotypes, the selection operates downstream of the signaling occurring during the beginning of the host's immune response. Public Library of Science 2011-10-13 /pmc/articles/PMC3192797/ /pubmed/22022607 http://dx.doi.org/10.1371/journal.pone.0026369 Text en Ong et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
repository_type Open Access Journal
institution_category Foreign Institution
institution US National Center for Biotechnology Information
building NCBI PubMed
collection Online Access
language English
format Online
author Ong, Yi-Ching
Boyle, Jon P.
Boothroyd, John C.
spellingShingle Ong, Yi-Ching
Boyle, Jon P.
Boothroyd, John C.
Strain-Dependent Host Transcriptional Responses to Toxoplasma Infection Are Largely Conserved in Mammalian and Avian Hosts
author_facet Ong, Yi-Ching
Boyle, Jon P.
Boothroyd, John C.
author_sort Ong, Yi-Ching
title Strain-Dependent Host Transcriptional Responses to Toxoplasma Infection Are Largely Conserved in Mammalian and Avian Hosts
title_short Strain-Dependent Host Transcriptional Responses to Toxoplasma Infection Are Largely Conserved in Mammalian and Avian Hosts
title_full Strain-Dependent Host Transcriptional Responses to Toxoplasma Infection Are Largely Conserved in Mammalian and Avian Hosts
title_fullStr Strain-Dependent Host Transcriptional Responses to Toxoplasma Infection Are Largely Conserved in Mammalian and Avian Hosts
title_full_unstemmed Strain-Dependent Host Transcriptional Responses to Toxoplasma Infection Are Largely Conserved in Mammalian and Avian Hosts
title_sort strain-dependent host transcriptional responses to toxoplasma infection are largely conserved in mammalian and avian hosts
description Toxoplasma gondii has a remarkable ability to infect an enormous variety of mammalian and avian species. Given this, it is surprising that three strains (Types I/II/III) account for the majority of isolates from Europe/North America. The selective pressures that have driven the emergence of these particular strains, however, remain enigmatic. We hypothesized that strain selection might be partially driven by adaptation of strains for mammalian versus avian hosts. To test this, we examine in vitro, strain-dependent host responses in fibroblasts of a representative avian host, the chicken (Gallus gallus). Using gene expression profiling of infected chicken embryonic fibroblasts and pathway analysis to assess host response, we show here that chicken cells respond with distinct transcriptional profiles upon infection with Type II versus III strains that are reminiscent of profiles observed in mammalian cells. To identify the parasite drivers of these differences, chicken fibroblasts were infected with individual F1 progeny of a Type II x III cross and host gene expression was assessed for each by microarray. QTL mapping of transcriptional differences suggested, and deletion strains confirmed, that, as in mammalian cells, the polymorphic rhoptry kinase ROP16 is the major driver of strain-specific responses. We originally hypothesized that comparing avian versus mammalian host response might reveal an inversion in parasite strain-dependent phenotypes; specifically, for polymorphic effectors like ROP16, we hypothesized that the allele with most activity in mammalian cells might be less active in avian cells. Instead, we found that activity of ROP16 alleles appears to be conserved across host species; moreover, additional parasite loci that were previously mapped for strain-specific effects on mammalian response showed similar strain-specific effects in chicken cells. These results indicate that if different hosts select for different parasite genotypes, the selection operates downstream of the signaling occurring during the beginning of the host's immune response.
publisher Public Library of Science
publishDate 2011
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3192797/
_version_ 1611480644904288256

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