Toxoplasma gondii virulence factor ROP1 reduces parasite susceptibility to murine and human innate immune restriction

Toxoplasma gondii is an intracellular parasite that can infect many host species and is a cause of significant human morbidity worldwide. T . gondii secretes a diverse array of effector proteins into the host cell which are critical for infection. The vast majority of these secreted proteins have no...

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Published inPLoS pathogens Vol. 18; no. 12; p. e1011021
Main Authors Butterworth, Simon, Torelli, Francesca, Lockyer, Eloise J., Wagener, Jeanette, Song, Ok-Ryul, Broncel, Malgorzata, Russell, Matt R. G., Moreira-Souza, Aline Cristina A., Young, Joanna C., Treeck, Moritz
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 07.12.2022
Public Library of Science (PLoS)
Subjects
Animals
Biology and Life Sciences
Carrier Proteins
CRISPR
Development and progression
Genes
Genomes
Genotype & phenotype
Health aspects
Humans
Immunity, Innate
Infections
Innate immunity
Macrophages
Medicine and Health Sciences
Mice
Mitochondrial Proteins - metabolism
Morbidity
Morphology
Parasite resistance
Parasites
Physiological aspects
Plasmids
Proteins
Protozoan Proteins - metabolism
Research and Analysis Methods
Rhoptry protein
Toxoplasma
Toxoplasma gondii
Toxoplasmosis
Virulence
Virulence (Microbiology)
Virulence Factors
United Kingdom
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Abstract Toxoplasma gondii is an intracellular parasite that can infect many host species and is a cause of significant human morbidity worldwide. T . gondii secretes a diverse array of effector proteins into the host cell which are critical for infection. The vast majority of these secreted proteins have no predicted functional domains and remain uncharacterised. Here, we carried out a pooled CRISPR knockout screen in the T . gondii Prugniaud strain in vivo to identify secreted proteins that contribute to parasite immune evasion in the host. We demonstrate that ROP1, the first-identified rhoptry protein of T . gondii , is essential for virulence and has a previously unrecognised role in parasite resistance to interferon gamma-mediated innate immune restriction. This function is conserved in the highly virulent RH strain of T . gondii and contributes to parasite growth in both murine and human macrophages. While ROP1 affects the morphology of rhoptries, from where the protein is secreted, it does not affect rhoptry secretion. Finally, we show that ROP1 co-immunoprecipitates with the host cell protein C1QBP, an emerging regulator of innate immune signaling. In summary, we identify putative in vivo virulence factors in the T . gondii Prugniaud strain and show that ROP1 is an important and previously overlooked effector protein that counteracts both murine and human innate immunity.
AbstractList Toxoplasma gondii is an intracellular parasite that can infect many host species and is a cause of significant human morbidity worldwide. T. gondii secretes a diverse array of effector proteins into the host cell which are critical for infection. The vast majority of these secreted proteins have no predicted functional domains and remain uncharacterised. Here, we carried out a pooled CRISPR knockout screen in the T. gondii Prugniaud strain in vivo to identify secreted proteins that contribute to parasite immune evasion in the host. We demonstrate that ROP1, the first-identified rhoptry protein of T. gondii, is essential for virulence and has a previously unrecognised role in parasite resistance to interferon gamma-mediated innate immune restriction. This function is conserved in the highly virulent RH strain of T. gondii and contributes to parasite growth in both murine and human macrophages. While ROP1 affects the morphology of rhoptries, from where the protein is secreted, it does not affect rhoptry secretion. Finally, we show that ROP1 co-immunoprecipitates with the host cell protein C1QBP, an emerging regulator of innate immune signaling. In summary, we identify putative in vivo virulence factors in the T. gondii Prugniaud strain and show that ROP1 is an important and previously overlooked effector protein that counteracts both murine and human innate immunity.
Toxoplasma gondii is an intracellular parasite that can infect many host species and is a cause of significant human morbidity worldwide. T . gondii secretes a diverse array of effector proteins into the host cell which are critical for infection. The vast majority of these secreted proteins have no predicted functional domains and remain uncharacterised. Here, we carried out a pooled CRISPR knockout screen in the T . gondii Prugniaud strain in vivo to identify secreted proteins that contribute to parasite immune evasion in the host. We demonstrate that ROP1, the first-identified rhoptry protein of T . gondii , is essential for virulence and has a previously unrecognised role in parasite resistance to interferon gamma-mediated innate immune restriction. This function is conserved in the highly virulent RH strain of T . gondii and contributes to parasite growth in both murine and human macrophages. While ROP1 affects the morphology of rhoptries, from where the protein is secreted, it does not affect rhoptry secretion. Finally, we show that ROP1 co-immunoprecipitates with the host cell protein C1QBP, an emerging regulator of innate immune signaling. In summary, we identify putative in vivo virulence factors in the T . gondii Prugniaud strain and show that ROP1 is an important and previously overlooked effector protein that counteracts both murine and human innate immunity. Toxoplasma gondii is a single-celled eukaryotic pathogen that can infect many different species, including mice and humans. T . gondii secretes a large number of proteins into host cells that it infects, although the majority of these proteins are not well studied. We have carried out a knockout screen to identify T . gondii genes that are important for the parasite to survive during infection of a mouse. One of the genes we identified encodes the parasite protein ROP1, which was shown 30 years ago to be secreted into the host cell, but whose function remains unknown. We show that deletion of ROP1 causes an otherwise lethal infection to be efficiently cleared by the host immune system. ROP1 is important for T . gondii to evade the cell autonomous immune responses of both human and murine cells, which is usual as the key mechanisms that control intracellular pathogens differ between humans and mice. ROP1 may interact with the host protein C1QBP, indicating the direction of future work to establish a mechanistic link to immune evasion.
Toxoplasma gondii is an intracellular parasite that can infect many host species and is a cause of significant human morbidity worldwide. T. gondii secretes a diverse array of effector proteins into the host cell which are critical for infection. The vast majority of these secreted proteins have no predicted functional domains and remain uncharacterised. Here, we carried out a pooled CRISPR knockout screen in the T. gondii Prugniaud strain in vivo to identify secreted proteins that contribute to parasite immune evasion in the host. We demonstrate that ROP1, the first-identified rhoptry protein of T. gondii, is essential for virulence and has a previously unrecognised role in parasite resistance to interferon gamma-mediated innate immune restriction. This function is conserved in the highly virulent RH strain of T. gondii and contributes to parasite growth in both murine and human macrophages. While ROP1 affects the morphology of rhoptries, from where the protein is secreted, it does not affect rhoptry secretion. Finally, we show that ROP1 co-immunoprecipitates with the host cell protein C1QBP, an emerging regulator of innate immune signaling. In summary, we identify putative in vivo virulence factors in the T. gondii Prugniaud strain and show that ROP1 is an important and previously overlooked effector protein that counteracts both murine and human innate immunity.Toxoplasma gondii is an intracellular parasite that can infect many host species and is a cause of significant human morbidity worldwide. T. gondii secretes a diverse array of effector proteins into the host cell which are critical for infection. The vast majority of these secreted proteins have no predicted functional domains and remain uncharacterised. Here, we carried out a pooled CRISPR knockout screen in the T. gondii Prugniaud strain in vivo to identify secreted proteins that contribute to parasite immune evasion in the host. We demonstrate that ROP1, the first-identified rhoptry protein of T. gondii, is essential for virulence and has a previously unrecognised role in parasite resistance to interferon gamma-mediated innate immune restriction. This function is conserved in the highly virulent RH strain of T. gondii and contributes to parasite growth in both murine and human macrophages. While ROP1 affects the morphology of rhoptries, from where the protein is secreted, it does not affect rhoptry secretion. Finally, we show that ROP1 co-immunoprecipitates with the host cell protein C1QBP, an emerging regulator of innate immune signaling. In summary, we identify putative in vivo virulence factors in the T. gondii Prugniaud strain and show that ROP1 is an important and previously overlooked effector protein that counteracts both murine and human innate immunity.
Toxoplasma gondii is an intracellular parasite that can infect many host species and is a cause of significant human morbidity worldwide. T . gondii secretes a diverse array of effector proteins into the host cell which are critical for infection. The vast majority of these secreted proteins have no predicted functional domains and remain uncharacterised. Here, we carried out a pooled CRISPR knockout screen in the T . gondii Prugniaud strain in vivo to identify secreted proteins that contribute to parasite immune evasion in the host. We demonstrate that ROP1, the first-identified rhoptry protein of T . gondii , is essential for virulence and has a previously unrecognised role in parasite resistance to interferon gamma-mediated innate immune restriction. This function is conserved in the highly virulent RH strain of T . gondii and contributes to parasite growth in both murine and human macrophages. While ROP1 affects the morphology of rhoptries, from where the protein is secreted, it does not affect rhoptry secretion. Finally, we show that ROP1 co-immunoprecipitates with the host cell protein C1QBP, an emerging regulator of innate immune signaling. In summary, we identify putative in vivo virulence factors in the T . gondii Prugniaud strain and show that ROP1 is an important and previously overlooked effector protein that counteracts both murine and human innate immunity.
Audience Academic
Author Wagener, Jeanette
Broncel, Malgorzata
Moreira-Souza, Aline Cristina A.
Lockyer, Eloise J.
Russell, Matt R. G.
Song, Ok-Ryul
Torelli, Francesca
Young, Joanna C.
Treeck, Moritz
Butterworth, Simon
AuthorAffiliation 2 High-Throughput Screening Science Technology Platform, The Francis Crick Institute, London, United Kingdom
4 Electron Microscopy Science Technology Platform, The Francis Crick Institute, London, United Kingdom
Universitat Bern, SWITZERLAND
3 Proteomics Science Technology Platform, The Francis Crick Institute, London, United Kingdom
1 Signalling In Apicomplexan Parasites Laboratory, The Francis Crick Institute, London, United Kingdom
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/36476844$$D View this record in MEDLINE/PubMed
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Cites_doi 10.4049/jimmunol.175.7.4706
10.3389/fcimb.2019.00103
10.1093/nar/gky1106
10.3389/fimmu.2018.02073
10.1128/EC.00297-10
10.1096/fj.201901416RR
10.1128/mBio.01117-13
10.1128/iai.51.3.760-764.1986
10.1093/emboj/20.12.3132
10.1128/JVI.79.16.10807-10820.2005
10.1186/gb-2010-11-10-r106
10.1021/pr101065j
10.1111/j.1550-7408.1992.tb04844.x
10.1038/nature05395
10.1038/s41541-022-00518-5
10.1073/pnas.1515966112
10.1016/j.mib.2017.10.021
10.1371/journal.pbio.1001845
10.1128/mSphere.00183-17
10.1016/j.chom.2019.09.008
10.1534/genetics.115.186270
10.1016/0166-6851(95)02487-5
10.1126/science.3128869
10.1038/nmeth.2089
10.1038/nbt.1511
10.1016/j.cell.2016.08.019
10.1073/pnas.96.7.3572
10.1073/pnas.0811029106
10.1016/0166-6851(92)90239-G
10.7554/eLife.50598
10.1016/j.chom.2011.04.015
10.4049/jimmunol.2100392
10.1073/pnas.1015980108
10.1093/nar/gkab929
10.1038/nrmicro1800
10.1016/j.ijpara.2006.03.003
10.15252/embj.2018100926
10.1093/nar/gks774
10.1371/journal.pbio.1001358
10.1099/0022-1317-79-7-1677
10.1016/j.chom.2020.09.011
10.1128/mBio.00260-21
10.1016/j.chom.2010.11.005
10.1093/emboj/18.4.1014
10.1128/IAI.01339-13
10.1371/journal.ppat.1002992
10.1371/journal.pgen.1005434
10.1128/IAI.01170-13
10.1128/JVI.77.23.12875-12880.2003
10.1038/s41467-019-11855-w
10.1128/EC.00358-08
10.1074/jbc.272.39.24363
10.1074/jbc.271.24.14010
10.1073/pnas.1904637116
10.1371/journal.ppat.1000288
10.1126/science.1133690
10.1371/journal.ppat.1002784
10.1038/s41467-020-18991-8
10.1073/pnas.1015338108
10.1038/nmeth.3901
10.1126/science.1133643
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– notice: 2022 Butterworth et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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License Copyright: © 2022 Butterworth et al. 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 credited.
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References RG Donald (ppat.1011021.ref058) 1996; 271
M Yagi (ppat.1011021.ref041) 2012; 40
SK Matta (ppat.1011021.ref052) 2019; 116
AJ Shastri (ppat.1011021.ref021) 2014; 82
PN Ossorio (ppat.1011021.ref049) 1992; 50
Y Suzuki (ppat.1011021.ref051) 1988; 240
H Bando (ppat.1011021.ref047) 2018; 9
JC Boothroyd (ppat.1011021.ref031) 2008; 6
SK Petersen-Mahrt (ppat.1011021.ref040) 1999; 18
KDC Jensen (ppat.1011021.ref050) 2011; 9
CA Schneider (ppat.1011021.ref063) 2012; 9
S Håkansson (ppat.1011021.ref053) 2001; 20
JP Saeij (ppat.1011021.ref034) 2017; 40
AM Cygan (ppat.1011021.ref025)
JPJ Saeij (ppat.1011021.ref032) 2007; 445
J-L Wang (ppat.1011021.ref014) 2020; 34
S Tyanova (ppat.1011021.ref066) 2016; 13
BA Fox (ppat.1011021.ref013) 2019
H Jiao (ppat.1011021.ref037) 2015
K Barylyuk (ppat.1011021.ref017) 2020; 28
B Amos (ppat.1011021.ref068) 2022; 50
ML Blank (ppat.1011021.ref045) 2021
J Young (ppat.1011021.ref015) 2019; 10
S Anders (ppat.1011021.ref062) 2010; 11
Y Adomako-Ankomah (ppat.1011021.ref043) 2016; 203
MS Behnke (ppat.1011021.ref006) 2011; 108
MS Behnke (ppat.1011021.ref012) 2015; 11
M Wu (ppat.1011021.ref022) 2022; 7
D Soldati (ppat.1011021.ref023) 1995; 74
BA Fox (ppat.1011021.ref020) 2016; 7
M-H Huynh (ppat.1011021.ref059) 2009; 8
JPJ Saeij (ppat.1011021.ref004) 2006; 314
A Hunt (ppat.1011021.ref026) 2019; 8
YO Zhao (ppat.1011021.ref027) 2009; 5
G Gorfu (ppat.1011021.ref028) 2014; 5
DA Matthews (ppat.1011021.ref057) 1998; 79
MC Fleckenstein (ppat.1011021.ref009) 2012; 10
SE Ewald (ppat.1011021.ref030) 2014; 82
AK Haldar (ppat.1011021.ref035) 2015; 112
JD Schwartzman (ppat.1011021.ref048) 1986; 51
K Song (ppat.1011021.ref054) 2021
SM Sidik (ppat.1011021.ref018) 2016; 166
J Cox (ppat.1011021.ref064) 2008; 26
MS Behnke (ppat.1011021.ref010) 2012; 8
LD Saffer (ppat.1011021.ref024) 1992; 39
T Muta (ppat.1011021.ref046) 1997; 272
J Cox (ppat.1011021.ref065) 2011; 10
JP Dubey (ppat.1011021.ref001) 2014
ML Reese (ppat.1011021.ref008) 2011; 108
D. Beatch Martin (ppat.1011021.ref055) 2005; 79
Y Wang (ppat.1011021.ref019) 2020; 11
MW Panas (ppat.1011021.ref033) 2019
S Lainé (ppat.1011021.ref056) 2003; 77
E-M Frickel (ppat.1011021.ref003) 2021; 218
BA Fox (ppat.1011021.ref060) 2011; 10
SN Waggoner (ppat.1011021.ref039) 2005; 175
SJ Fentress (ppat.1011021.ref007) 2010; 8
L Pernas (ppat.1011021.ref042) 2014; 12
D Fisch (ppat.1011021.ref029) 2019; 38
TS Lima (ppat.1011021.ref002) 2019; 9
S Taylor (ppat.1011021.ref005) 2006; 314
C Su (ppat.1011021.ref061) 2006; 36
J Jiang (ppat.1011021.ref036) 1999; 96
W Niedelman (ppat.1011021.ref011) 2012; 8
FD Kelly (ppat.1011021.ref044) 2017; 2
L Xu (ppat.1011021.ref038) 2009; 106
LO Sangaré (ppat.1011021.ref016) 2019; 26
Y Perez-Riverol (ppat.1011021.ref067) 2019; 47
References_xml – start-page: 1
  volume-title: Toxoplasma Gondii (Second Edition)
  year: 2014
  ident: ppat.1011021.ref001
– volume: 175
  start-page: 4706
  year: 2005
  ident: ppat.1011021.ref039
  article-title: gC1q receptor ligation selectively down-regulates human IL-12 production through activation of the phosphoinositide 3-kinase pathway
  publication-title: J Immunol
  doi: 10.4049/jimmunol.175.7.4706
– volume: 9
  start-page: 103
  year: 2019
  ident: ppat.1011021.ref002
  article-title: Mechanisms of Human Innate Immune Evasion by Toxoplasma gondii
  publication-title: Front Cell Infect Microbiol
  doi: 10.3389/fcimb.2019.00103
– volume: 47
  start-page: D442
  year: 2019
  ident: ppat.1011021.ref067
  article-title: The PRIDE database and related tools and resources in 2019: improving support for quantification data
  publication-title: Nucleic Acids Res
  doi: 10.1093/nar/gky1106
– volume: 9
  start-page: 2073
  year: 2018
  ident: ppat.1011021.ref047
  article-title: Toxoplasma Effector TgIST Targets Host IDO1 to Antagonize the IFN-γ-Induced Anti-parasitic Response in Human Cells.
  publication-title: Front Immunol
  doi: 10.3389/fimmu.2018.02073
– volume: 10
  start-page: 1193
  year: 2011
  ident: ppat.1011021.ref060
  article-title: Type II Toxoplasma gondii KU80 knockout strains enable functional analysis of genes required for cyst development and latent infection
  publication-title: Eukaryot Cell
  doi: 10.1128/EC.00297-10
– volume: 34
  start-page: 3165
  year: 2020
  ident: ppat.1011021.ref014
  article-title: Novel roles of dense granule protein 12 (GRA12) in Toxoplasma gondii infection.
  publication-title: FASEB J
  doi: 10.1096/fj.201901416RR
– volume: 5
  year: 2014
  ident: ppat.1011021.ref028
  article-title: Dual role for inflammasome sensors NLRP1 and NLRP3 in murine resistance to Toxoplasma gondii.
  publication-title: MBio
  doi: 10.1128/mBio.01117-13
– volume: 51
  start-page: 760
  year: 1986
  ident: ppat.1011021.ref048
  article-title: Inhibition of a penetration-enhancing factor of Toxoplasma gondii by monoclonal antibodies specific for rhoptries
  publication-title: Infect Immun
  doi: 10.1128/iai.51.3.760-764.1986
– volume: 20
  start-page: 3132
  year: 2001
  ident: ppat.1011021.ref053
  article-title: Toxoplasma evacuoles: a two-step process of secretion and fusion forms the parasitophorous vacuole
  publication-title: EMBO J
  doi: 10.1093/emboj/20.12.3132
– volume: 79
  start-page: 10807
  year: 2005
  ident: ppat.1011021.ref055
  article-title: Interactions between Rubella Virus Capsid and Host Protein p32 Are Important for Virus Replication
  publication-title: J Virol
  doi: 10.1128/JVI.79.16.10807-10820.2005
– volume: 11
  start-page: R106
  year: 2010
  ident: ppat.1011021.ref062
  article-title: Differential expression analysis for sequence count data
  publication-title: Genome Biol
  doi: 10.1186/gb-2010-11-10-r106
– volume: 10
  start-page: 1794
  year: 2011
  ident: ppat.1011021.ref065
  article-title: Andromeda: a peptide search engine integrated into the MaxQuant environment
  publication-title: J Proteome Res
  doi: 10.1021/pr101065j
– volume: 39
  start-page: 526
  year: 1992
  ident: ppat.1011021.ref024
  article-title: Localization of a Toxoplasma gondii rhoptry protein by immunoelectron microscopy during and after host cell penetration
  publication-title: J Protozool
  doi: 10.1111/j.1550-7408.1992.tb04844.x
– start-page: 118
  year: 2021
  ident: ppat.1011021.ref045
  article-title: Toxoplasma gondii association with host mitochondria requires key mitochondrial protein import machinery
  publication-title: Proc Natl Acad Sci U S A
– volume: 445
  start-page: 324
  year: 2007
  ident: ppat.1011021.ref032
  article-title: Toxoplasma co-opts host gene expression by injection of a polymorphic kinase homologue
  publication-title: Nature
  doi: 10.1038/nature05395
– volume: 7
  start-page: 98
  year: 2022
  ident: ppat.1011021.ref022
  article-title: Live-attenuated ME49Δcdpk3 strain of Toxoplasma gondii protects against acute and chronic toxoplasmosis.
  publication-title: NPJ Vaccines.
  doi: 10.1038/s41541-022-00518-5
– volume: 112
  start-page: E5628
  year: 2015
  ident: ppat.1011021.ref035
  article-title: Ubiquitin systems mark pathogen-containing vacuoles as targets for host defense by guanylate binding proteins
  publication-title: Proc Natl Acad Sci U S A
  doi: 10.1073/pnas.1515966112
– volume: 40
  start-page: 72
  year: 2017
  ident: ppat.1011021.ref034
  article-title: Exposing Toxoplasma gondii hiding inside the vacuole: a role for GBPs, autophagy and host cell death
  publication-title: Curr Opin Microbiol
  doi: 10.1016/j.mib.2017.10.021
– volume: 218
  year: 2021
  ident: ppat.1011021.ref003
  article-title: Lessons from Toxoplasma: Host responses that mediate parasite control and the microbial effectors that subvert them
  publication-title: J Exp Med
– volume: 12
  start-page: e1001845
  year: 2014
  ident: ppat.1011021.ref042
  article-title: Toxoplasma effector MAF1 mediates recruitment of host mitochondria and impacts the host response
  publication-title: PLoS Biol
  doi: 10.1371/journal.pbio.1001845
– volume: 2
  year: 2017
  ident: ppat.1011021.ref044
  article-title: Toxoplasma gondii MAF1b Binds the Host Cell MIB Complex To Mediate Mitochondrial Association.
  publication-title: mSphere
  doi: 10.1128/mSphere.00183-17
– volume: 26
  start-page: 478
  year: 2019
  ident: ppat.1011021.ref016
  article-title: In Vivo CRISPR Screen Identifies TgWIP as a Toxoplasma Modulator of Dendritic Cell Migration.
  publication-title: Cell Host Microbe
  doi: 10.1016/j.chom.2019.09.008
– volume: 203
  start-page: 283
  year: 2016
  ident: ppat.1011021.ref043
  article-title: Host Mitochondrial Association Evolved in the Human Parasite Toxoplasma gondii via Neofunctionalization of a Gene Duplicate
  publication-title: Genetics
  doi: 10.1534/genetics.115.186270
– volume: 7
  year: 2016
  ident: ppat.1011021.ref020
  article-title: The Toxoplasma gondii Rhoptry Kinome Is Essential for Chronic Infection.
  publication-title: MBio
– year: 2019
  ident: ppat.1011021.ref033
  article-title: Translocation of Dense Granule Effectors across the Parasitophorous Vacuole Membrane in Toxoplasma- Infected Cells Requires the Activity of ROP17, a Rhoptry Protein Kinase.
  publication-title: mSphere
– volume: 74
  start-page: 87
  year: 1995
  ident: ppat.1011021.ref023
  article-title: Complementation of a Toxoplasma gondii ROP1 knock-out mutant using phleomycin selection
  publication-title: Mol Biochem Parasitol
  doi: 10.1016/0166-6851(95)02487-5
– volume: 240
  start-page: 516
  year: 1988
  ident: ppat.1011021.ref051
  article-title: Interferon-gamma: the major mediator of resistance against Toxoplasma gondii
  publication-title: Science
  doi: 10.1126/science.3128869
– volume: 9
  start-page: 671
  year: 2012
  ident: ppat.1011021.ref063
  article-title: NIH Image to ImageJ: 25 years of image analysis.
  publication-title: Nat Methods.
  doi: 10.1038/nmeth.2089
– volume: 26
  start-page: 1367
  year: 2008
  ident: ppat.1011021.ref064
  article-title: MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification
  publication-title: Nat Biotechnol
  doi: 10.1038/nbt.1511
– volume: 166
  start-page: 1423
  year: 2016
  ident: ppat.1011021.ref018
  article-title: A Genome-wide CRISPR Screen in Toxoplasma Identifies Essential Apicomplexan Genes
  publication-title: Cell
  doi: 10.1016/j.cell.2016.08.019
– volume: 96
  start-page: 3572
  year: 1999
  ident: ppat.1011021.ref036
  article-title: Crystal structure of human p32, a doughnut-shaped acidic mitochondrial matrix protein
  publication-title: Proc Natl Acad Sci U S A
  doi: 10.1073/pnas.96.7.3572
– year: 2015
  ident: ppat.1011021.ref037
  article-title: Chaperone-like protein p32 regulates ULK1 stability and autophagy
  publication-title: Cell Death Differ
– volume: 106
  start-page: 1530
  year: 2009
  ident: ppat.1011021.ref038
  article-title: Inhibition of RIG-I and MDA5-dependent antiviral response by gC1qR at mitochondria
  publication-title: Proc Natl Acad Sci U S A
  doi: 10.1073/pnas.0811029106
– volume: 50
  start-page: 1
  year: 1992
  ident: ppat.1011021.ref049
  article-title: A Toxoplasma gondii rhoptry protein associated with host cell penetration has unusual charge asymmetry
  publication-title: Mol Biochem Parasitol
  doi: 10.1016/0166-6851(92)90239-G
– volume: 8
  year: 2019
  ident: ppat.1011021.ref026
  article-title: Differential requirements for cyclase-associated protein (CAP) in actin-dependent processes of Toxoplasma gondii.
  publication-title: Elife
  doi: 10.7554/eLife.50598
– volume: 9
  start-page: 472
  year: 2011
  ident: ppat.1011021.ref050
  article-title: Toxoplasma polymorphic effectors determine macrophage polarization and intestinal inflammation
  publication-title: Cell Host Microbe
  doi: 10.1016/j.chom.2011.04.015
– year: 2019
  ident: ppat.1011021.ref013
  article-title: Toxoplasma gondiiParasitophorous Vacuole Membrane-Associated Dense Granule Proteins Orchestrate Chronic Infection and GRA12 Underpins Resistance to Host Gamma Interferon.
  publication-title: mBio
– start-page: 2155
  year: 2021
  ident: ppat.1011021.ref054
  article-title: Leaked Mitochondrial C1QBP Inhibits Activation of the DNA Sensor cGAS
  publication-title: Journal of immunology
  doi: 10.4049/jimmunol.2100392
– volume: 108
  start-page: 9625
  year: 2011
  ident: ppat.1011021.ref008
  article-title: Polymorphic family of injected pseudokinases is paramount in Toxoplasma virulence
  publication-title: Proc Natl Acad Sci U S A
  doi: 10.1073/pnas.1015980108
– volume: 50
  start-page: D898
  year: 2022
  ident: ppat.1011021.ref068
  article-title: VEuPathDB: the eukaryotic pathogen, vector and host bioinformatics resource center
  publication-title: Nucleic Acids Res
  doi: 10.1093/nar/gkab929
– volume: 6
  start-page: 79
  year: 2008
  ident: ppat.1011021.ref031
  article-title: Kiss and spit: the dual roles of Toxoplasma rhoptries
  publication-title: Nat Rev Microbiol
  doi: 10.1038/nrmicro1800
– volume: 36
  start-page: 841
  year: 2006
  ident: ppat.1011021.ref061
  article-title: Genotyping of Toxoplasma gondii by multilocus PCR-RFLP markers: a high resolution and simple method for identification of parasites
  publication-title: Int J Parasitol
  doi: 10.1016/j.ijpara.2006.03.003
– volume: 38
  start-page: e100926
  year: 2019
  ident: ppat.1011021.ref029
  article-title: Human GBP1 is a microbe-specific gatekeeper of macrophage apoptosis and pyroptosis
  publication-title: EMBO J
  doi: 10.15252/embj.2018100926
– volume: 40
  start-page: 9717
  year: 2012
  ident: ppat.1011021.ref041
  article-title: p32/gC1qR is indispensable for fetal development and mitochondrial translation: importance of its RNA-binding ability
  publication-title: Nucleic Acids Res
  doi: 10.1093/nar/gks774
– volume: 10
  start-page: e1001358
  year: 2012
  ident: ppat.1011021.ref009
  article-title: A Toxoplasma gondii pseudokinase inhibits host IRG resistance proteins
  publication-title: PLoS Biol
  doi: 10.1371/journal.pbio.1001358
– volume: 79
  start-page: 1677
  issue: Pt 7
  year: 1998
  ident: ppat.1011021.ref057
  article-title: Adenovirus core protein V interacts with p32—a protein which is associated with both the mitochondria and the nucleus
  publication-title: J Gen Virol
  doi: 10.1099/0022-1317-79-7-1677
– volume: 28
  start-page: 752
  year: 2020
  ident: ppat.1011021.ref017
  article-title: A Comprehensive Subcellular Atlas of the Toxoplasma Proteome via hyperLOPIT Provides Spatial Context for Protein Functions
  publication-title: Cell Host Microbe
  doi: 10.1016/j.chom.2020.09.011
– ident: ppat.1011021.ref025
  article-title: Proximity-labeling reveals novel host and parasite proteins at the Toxoplasma parasitophorous vacuole membrane.
  doi: 10.1128/mBio.00260-21
– volume: 8
  start-page: 484
  year: 2010
  ident: ppat.1011021.ref007
  article-title: Phosphorylation of immunity-related GTPases by a Toxoplasma gondii-secreted kinase promotes macrophage survival and virulence
  publication-title: Cell Host Microbe
  doi: 10.1016/j.chom.2010.11.005
– volume: 18
  start-page: 1014
  year: 1999
  ident: ppat.1011021.ref040
  article-title: The splicing factor-associated protein, p32, regulates RNA splicing by inhibiting ASF/SF2 RNA binding and phosphorylation
  publication-title: EMBO J
  doi: 10.1093/emboj/18.4.1014
– volume: 82
  start-page: 2595
  year: 2014
  ident: ppat.1011021.ref021
  article-title: GRA25 is a novel virulence factor of Toxoplasma gondii and influences the host immune response
  publication-title: Infect Immun
  doi: 10.1128/IAI.01339-13
– volume: 8
  start-page: e1002992
  year: 2012
  ident: ppat.1011021.ref010
  article-title: The polymorphic pseudokinase ROP5 controls virulence in Toxoplasma gondii by regulating the active kinase ROP18.
  publication-title: PLoS Pathog
  doi: 10.1371/journal.ppat.1002992
– volume: 11
  start-page: e1005434
  year: 2015
  ident: ppat.1011021.ref012
  article-title: Rhoptry Proteins ROP5 and ROP18 Are Major Murine Virulence Factors in Genetically Divergent South American Strains of Toxoplasma gondii.
  publication-title: PLoS Genet.
  doi: 10.1371/journal.pgen.1005434
– volume: 82
  start-page: 460
  year: 2014
  ident: ppat.1011021.ref030
  article-title: NLRP1 is an inflammasome sensor for Toxoplasma gondii
  publication-title: Infect Immun
  doi: 10.1128/IAI.01170-13
– volume: 77
  start-page: 12875
  year: 2003
  ident: ppat.1011021.ref056
  article-title: In vitro and in vivo interactions between the hepatitis B virus protein P22 and the cellular protein gC1qR
  publication-title: J Virol
  doi: 10.1128/JVI.77.23.12875-12880.2003
– volume: 10
  start-page: 3963
  year: 2019
  ident: ppat.1011021.ref015
  article-title: A CRISPR platform for targeted in vivo screens identifies Toxoplasma gondii virulence factors in mice
  publication-title: Nat Commun
  doi: 10.1038/s41467-019-11855-w
– volume: 8
  start-page: 530
  year: 2009
  ident: ppat.1011021.ref059
  article-title: Tagging of endogenous genes in a Toxoplasma gondii strain lacking Ku80
  publication-title: Eukaryot Cell
  doi: 10.1128/EC.00358-08
– volume: 272
  start-page: 24363
  year: 1997
  ident: ppat.1011021.ref046
  article-title: p32 protein, a splicing factor 2-associated protein, is localized in mitochondrial matrix and is functionally important in maintaining oxidative phosphorylation
  publication-title: J Biol Chem
  doi: 10.1074/jbc.272.39.24363
– volume: 271
  start-page: 14010
  year: 1996
  ident: ppat.1011021.ref058
  article-title: Insertional tagging, cloning, and expression of the Toxoplasma gondii hypoxanthine-xanthine-guanine phosphoribosyltransferase gene. Use as a selectable marker for stable transformation
  publication-title: J Biol Chem
  doi: 10.1074/jbc.271.24.14010
– volume: 116
  start-page: 17480
  year: 2019
  ident: ppat.1011021.ref052
  article-title: Toxoplasma gondii effector TgIST blocks type I interferon signaling to promote infection
  publication-title: Proc Natl Acad Sci U S A
  doi: 10.1073/pnas.1904637116
– volume: 5
  start-page: e1000288
  year: 2009
  ident: ppat.1011021.ref027
  article-title: Disruption of the Toxoplasma gondii parasitophorous vacuole by IFNgamma-inducible immunity-related GTPases (IRG proteins) triggers necrotic cell death.
  publication-title: PLoS Pathog
  doi: 10.1371/journal.ppat.1000288
– volume: 314
  start-page: 1780
  year: 2006
  ident: ppat.1011021.ref004
  article-title: Polymorphic secreted kinases are key virulence factors in toxoplasmosis
  publication-title: Science
  doi: 10.1126/science.1133690
– volume: 8
  start-page: e1002784
  year: 2012
  ident: ppat.1011021.ref011
  article-title: The rhoptry proteins ROP18 and ROP5 mediate Toxoplasma gondii evasion of the murine, but not the human, interferon-gamma response.
  publication-title: PLoS Pathog
  doi: 10.1371/journal.ppat.1002784
– volume: 11
  start-page: 5258
  year: 2020
  ident: ppat.1011021.ref019
  article-title: Genome-wide screens identify Toxoplasma gondii determinants of parasite fitness in IFNγ-activated murine macrophages.
  publication-title: Nat Commun
  doi: 10.1038/s41467-020-18991-8
– volume: 108
  start-page: 9631
  year: 2011
  ident: ppat.1011021.ref006
  article-title: Virulence differences in Toxoplasma mediated by amplification of a family of polymorphic pseudokinases
  publication-title: Proc Natl Acad Sci U S A
  doi: 10.1073/pnas.1015338108
– volume: 13
  start-page: 731
  year: 2016
  ident: ppat.1011021.ref066
  article-title: The Perseus computational platform for comprehensive analysis of (prote) omics data.
  publication-title: Nat Methods
  doi: 10.1038/nmeth.3901
– volume: 314
  start-page: 1776
  year: 2006
  ident: ppat.1011021.ref005
  article-title: A secreted serine-threonine kinase determines virulence in the eukaryotic pathogen Toxoplasma gondii
  publication-title: Science
  doi: 10.1126/science.1133643
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Snippet Toxoplasma gondii is an intracellular parasite that can infect many host species and is a cause of significant human morbidity worldwide. T . gondii secretes a...
Toxoplasma gondii is an intracellular parasite that can infect many host species and is a cause of significant human morbidity worldwide. T. gondii secretes a...
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StartPage e1011021
SubjectTerms Animals
Biology and Life Sciences
Carrier Proteins
CRISPR
Development and progression
Genes
Genomes
Genotype & phenotype
Health aspects
Humans
Immunity, Innate
Infections
Innate immunity
Macrophages
Medicine and Health Sciences
Mice
Mitochondrial Proteins - metabolism
Morbidity
Morphology
Parasite resistance
Parasites
Physiological aspects
Plasmids
Proteins
Protozoan Proteins - metabolism
Research and Analysis Methods
Rhoptry protein
Toxoplasma
Toxoplasma gondii
Toxoplasmosis
Virulence
Virulence (Microbiology)
Virulence Factors
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Title Toxoplasma gondii virulence factor ROP1 reduces parasite susceptibility to murine and human innate immune restriction
URI https://www.ncbi.nlm.nih.gov/pubmed/36476844
https://www.proquest.com/docview/2762698074
https://www.proquest.com/docview/2753302611
https://pubmed.ncbi.nlm.nih.gov/PMC9762571
https://doaj.org/article/1ef7567a322246b68d3ab5f125e50e7c
http://dx.doi.org/10.1371/journal.ppat.1011021
Volume 18
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