Inflammasome sensor NLRP1 controls rat macrophage susceptibility to Toxoplasma gondii.

Toxoplasma gondii is an intracellular parasite that infects a wide range of warm-blooded species. Rats vary in their susceptibility to this parasite. The Toxo1 locus conferring Toxoplasma resistance in rats was previously mapped to a region of chromosome 10 containing Nlrp1. This gene encodes an inf...

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Main Authors: Kimberly M Cirelli, Gezahegn Gorfu, Musa A Hassan, Morton Printz, Devorah Crown, Stephen H Leppla, Michael E Grigg, Jeroen P J Saeij, Mahtab Moayeri
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2014-03-01
Series:PLoS Pathogens
Online Access:https://doi.org/10.1371/journal.ppat.1003927
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author Kimberly M Cirelli
Gezahegn Gorfu
Musa A Hassan
Morton Printz
Devorah Crown
Stephen H Leppla
Michael E Grigg
Jeroen P J Saeij
Mahtab Moayeri
author_facet Kimberly M Cirelli
Gezahegn Gorfu
Musa A Hassan
Morton Printz
Devorah Crown
Stephen H Leppla
Michael E Grigg
Jeroen P J Saeij
Mahtab Moayeri
author_sort Kimberly M Cirelli
collection DOAJ
description Toxoplasma gondii is an intracellular parasite that infects a wide range of warm-blooded species. Rats vary in their susceptibility to this parasite. The Toxo1 locus conferring Toxoplasma resistance in rats was previously mapped to a region of chromosome 10 containing Nlrp1. This gene encodes an inflammasome sensor controlling macrophage sensitivity to anthrax lethal toxin (LT) induced rapid cell death (pyroptosis). We show here that rat strain differences in Toxoplasma infected macrophage sensitivity to pyroptosis, IL-1β/IL-18 processing, and inhibition of parasite proliferation are perfectly correlated with NLRP1 sequence, while inversely correlated with sensitivity to anthrax LT-induced cell death. Using recombinant inbred rats, SNP analyses and whole transcriptome gene expression studies, we narrowed the candidate genes for control of Toxoplasma-mediated rat macrophage pyroptosis to four genes, one of which was Nlrp1. Knockdown of Nlrp1 in pyroptosis-sensitive macrophages resulted in higher parasite replication and protection from cell death. Reciprocally, overexpression of the NLRP1 variant from Toxoplasma-sensitive macrophages in pyroptosis-resistant cells led to sensitization of these resistant macrophages. Our findings reveal Toxoplasma as a novel activator of the NLRP1 inflammasome in rat macrophages.
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spelling doaj-art-08ffeadd52ba4b23a88d6edb3374c7932025-08-20T02:34:09ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742014-03-01103e100392710.1371/journal.ppat.1003927Inflammasome sensor NLRP1 controls rat macrophage susceptibility to Toxoplasma gondii.Kimberly M CirelliGezahegn GorfuMusa A HassanMorton PrintzDevorah CrownStephen H LepplaMichael E GriggJeroen P J SaeijMahtab MoayeriToxoplasma gondii is an intracellular parasite that infects a wide range of warm-blooded species. Rats vary in their susceptibility to this parasite. The Toxo1 locus conferring Toxoplasma resistance in rats was previously mapped to a region of chromosome 10 containing Nlrp1. This gene encodes an inflammasome sensor controlling macrophage sensitivity to anthrax lethal toxin (LT) induced rapid cell death (pyroptosis). We show here that rat strain differences in Toxoplasma infected macrophage sensitivity to pyroptosis, IL-1β/IL-18 processing, and inhibition of parasite proliferation are perfectly correlated with NLRP1 sequence, while inversely correlated with sensitivity to anthrax LT-induced cell death. Using recombinant inbred rats, SNP analyses and whole transcriptome gene expression studies, we narrowed the candidate genes for control of Toxoplasma-mediated rat macrophage pyroptosis to four genes, one of which was Nlrp1. Knockdown of Nlrp1 in pyroptosis-sensitive macrophages resulted in higher parasite replication and protection from cell death. Reciprocally, overexpression of the NLRP1 variant from Toxoplasma-sensitive macrophages in pyroptosis-resistant cells led to sensitization of these resistant macrophages. Our findings reveal Toxoplasma as a novel activator of the NLRP1 inflammasome in rat macrophages.https://doi.org/10.1371/journal.ppat.1003927
spellingShingle Kimberly M Cirelli
Gezahegn Gorfu
Musa A Hassan
Morton Printz
Devorah Crown
Stephen H Leppla
Michael E Grigg
Jeroen P J Saeij
Mahtab Moayeri
Inflammasome sensor NLRP1 controls rat macrophage susceptibility to Toxoplasma gondii.
PLoS Pathogens
title Inflammasome sensor NLRP1 controls rat macrophage susceptibility to Toxoplasma gondii.
title_full Inflammasome sensor NLRP1 controls rat macrophage susceptibility to Toxoplasma gondii.
title_fullStr Inflammasome sensor NLRP1 controls rat macrophage susceptibility to Toxoplasma gondii.
title_full_unstemmed Inflammasome sensor NLRP1 controls rat macrophage susceptibility to Toxoplasma gondii.
title_short Inflammasome sensor NLRP1 controls rat macrophage susceptibility to Toxoplasma gondii.
title_sort inflammasome sensor nlrp1 controls rat macrophage susceptibility to toxoplasma gondii
url https://doi.org/10.1371/journal.ppat.1003927
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