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Title: A Novel Secreted Protein, MYR1, Is Central to Toxoplasma ’s Manipulation of Host Cells

Abstract

ABSTRACT The intracellular protozoanToxoplasma gondiidramatically reprograms the transcriptome of host cells it infects, including substantially up-regulating the host oncogene c-myc. By applying a flow cytometry-based selection to infected mouse cells expressing green fluorescent protein fused to c-Myc (c-Myc–GFP), we isolated mutant tachyzoites defective in this host c-Myc up-regulation. Whole-genome sequencing of three such mutants led to the identification ofMYR1(Mycregulation1;TGGT1_254470) as essential for c-Myc induction. MYR1 is a secreted protein that requires TgASP5 to be cleaved into two stable portions, both of which are ultimately found within the parasitophorous vacuole and at the parasitophorous vacuole membrane. Deletion ofMYR1revealed that in addition to its requirement for c-Myc up-regulation, the MYR1 protein is needed for the ability ofToxoplasmatachyzoites to modulate several other important host pathways, including those mediated by the dense granule effectors GRA16 and GRA24. This result, combined with its location at the parasitophorous vacuole membrane, suggested that MYR1 might be a component of the machinery that translocatesToxoplasmaeffectors from the parasitophorous vacuole into the host cytosol. Support for this possibility was obtained by showing that transit of GRA24 to the host nucleus is indeed MYR1-dependent. As predicted by this pleiotropic phenotype, parasites deficient inMYR1were found to be severely attenuated in a mousemore » model of infection. We conclude, therefore, that MYR1 is a novel protein that plays a critical role in howToxoplasmadelivers effector proteins to the infected host cell and that this is crucial to virulence. IMPORTANCEToxoplasma gondiiis an important human pathogen and a model for the study of intracellular parasitism. Infection of the host cell withToxoplasmatachyzoites involves the introduction of protein effectors, including many that are initially secreted into the parasitophorous vacuole but must ultimately translocate to the host cell cytosol to function. The work reported here identified a novel protein that is required for this translocation. These results give new insight into a very unusual cell biology process as well as providing a potential handle on a pathway that is necessary for virulence and, therefore, a new potential target for chemotherapy.« less

Authors:
 [1];  [2];  [2];  [3];  [2];  [2];  [4];  [4];  [3];  [2]
+ Show Author Affiliations
  1. Stanford Univ. School of Medicine, CA (United States); Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
  2. Stanford Univ. School of Medicine, CA (United States)
  3. Univ. of California, Santa Cruz, CA (United States)
  4. Washington Univ., St. Louis, MO (United States)
Publication Date:
Research Org.:
Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)
Sponsoring Org.:
USDOE; National Institutes of Health (NIH)
OSTI Identifier:
1259517
Alternate Identifier(s):
OSTI ID: 1420295
Report Number(s):
LLNL-JRNL-736669
Journal ID: ISSN 2150-7511
Grant/Contract Number:  
R21-AI112962; RO1-AI73756; T32-AI007328; P01-35HG000205; T32-AI007290; F31-AI120649; K08AI102946-01; S10RR025518-01; P30-NS069375; AC52-07NA27344
Resource Type:
Accepted Manuscript
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Name: mBio (Online); Journal Volume: 7; Journal Issue: 1; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES; 59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Franco, Magdalena, Panas, Michael W., Marino, Nicole D., Lee, Mei-Chong Wendy, Buchholz, Kerry R., Kelly, Felice D., Bednarski, Jeffrey J., Sleckman, Barry P., Pourmand, Nader, and Boothroyd, John C. A Novel Secreted Protein, MYR1, Is Central to Toxoplasma ’s Manipulation of Host Cells. United States: N. p., 2016. Web. doi:10.1128/mbio.02231-15.
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Franco, Magdalena, Panas, Michael W., Marino, Nicole D., Lee, Mei-Chong Wendy, Buchholz, Kerry R., Kelly, Felice D., Bednarski, Jeffrey J., Sleckman, Barry P., Pourmand, Nader, & Boothroyd, John C. A Novel Secreted Protein, MYR1, Is Central to Toxoplasma ’s Manipulation of Host Cells. United States. https://doi.org/10.1128/mbio.02231-15
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Franco, Magdalena, Panas, Michael W., Marino, Nicole D., Lee, Mei-Chong Wendy, Buchholz, Kerry R., Kelly, Felice D., Bednarski, Jeffrey J., Sleckman, Barry P., Pourmand, Nader, and Boothroyd, John C. Tue . "A Novel Secreted Protein, MYR1, Is Central to Toxoplasma ’s Manipulation of Host Cells". United States. https://doi.org/10.1128/mbio.02231-15. https://www.osti.gov/servlets/purl/1259517.
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@article{osti_1259517,
title = {A Novel Secreted Protein, MYR1, Is Central to Toxoplasma ’s Manipulation of Host Cells},
author = {Franco, Magdalena and Panas, Michael W. and Marino, Nicole D. and Lee, Mei-Chong Wendy and Buchholz, Kerry R. and Kelly, Felice D. and Bednarski, Jeffrey J. and Sleckman, Barry P. and Pourmand, Nader and Boothroyd, John C.},
abstractNote = {ABSTRACT The intracellular protozoanToxoplasma gondiidramatically reprograms the transcriptome of host cells it infects, including substantially up-regulating the host oncogene c-myc. By applying a flow cytometry-based selection to infected mouse cells expressing green fluorescent protein fused to c-Myc (c-Myc–GFP), we isolated mutant tachyzoites defective in this host c-Myc up-regulation. Whole-genome sequencing of three such mutants led to the identification ofMYR1(Mycregulation1;TGGT1_254470) as essential for c-Myc induction. MYR1 is a secreted protein that requires TgASP5 to be cleaved into two stable portions, both of which are ultimately found within the parasitophorous vacuole and at the parasitophorous vacuole membrane. Deletion ofMYR1revealed that in addition to its requirement for c-Myc up-regulation, the MYR1 protein is needed for the ability ofToxoplasmatachyzoites to modulate several other important host pathways, including those mediated by the dense granule effectors GRA16 and GRA24. This result, combined with its location at the parasitophorous vacuole membrane, suggested that MYR1 might be a component of the machinery that translocatesToxoplasmaeffectors from the parasitophorous vacuole into the host cytosol. Support for this possibility was obtained by showing that transit of GRA24 to the host nucleus is indeed MYR1-dependent. As predicted by this pleiotropic phenotype, parasites deficient inMYR1were found to be severely attenuated in a mouse model of infection. We conclude, therefore, that MYR1 is a novel protein that plays a critical role in howToxoplasmadelivers effector proteins to the infected host cell and that this is crucial to virulence. IMPORTANCEToxoplasma gondiiis an important human pathogen and a model for the study of intracellular parasitism. Infection of the host cell withToxoplasmatachyzoites involves the introduction of protein effectors, including many that are initially secreted into the parasitophorous vacuole but must ultimately translocate to the host cell cytosol to function. The work reported here identified a novel protein that is required for this translocation. These results give new insight into a very unusual cell biology process as well as providing a potential handle on a pathway that is necessary for virulence and, therefore, a new potential target for chemotherapy.},
doi = {10.1128/mbio.02231-15},
journal = {mBio (Online)},
number = 1,
volume = 7,
place = {United States},
year = {Tue Feb 02 00:00:00 EST 2016},
month = {Tue Feb 02 00:00:00 EST 2016}
}
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Journal Article:
Free Publicly Available Full Text
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https://doi.org/10.1128/mbio.02231-15
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Cited by: 97 works
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Figures / Tables:

FIG 1 FIG 1: Genetic screen to isolate Toxoplasma mutants that fail to induce c-Myc. (A) Flow cytometry histogram of BMMs expressing c-Myc–GFP infected with Toxoplasma wild-type tachyzoites (RH) or Neospora tachyzoites or mock-infected. The gate was set on highly infected cells. The y axis shows relative cell count for each populationmore » (normalized to mode), and the x axis shows green fluorescence intensity. (B) Selection of mutants that fail to induce c-Myc. BMM c-Myc–GFP reporter cells were infected with a mutagenized population of RH tachyzoites and sorted for low GFP fluorescence. This was repeated until a homogeneous population was obtained that induced low GFP fluorescence. The GFP fluorescence profiles for the mutagenized population after 3, 5, and 7 rounds of selection are shown. (Histograms for first two sorts were similar to the one for sort 3 and were omitted.) The profiles for cells infected with wild-type RH and Neospora tachyzoites are shown for comparison. The x and y axes are as described for panel A.« less
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journal, April 2014

Transcriptomic Analysis of Toxoplasma Development Reveals Many Novel Functions and Structures Specific to Sporozoites and Oocysts
journal, February 2012

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journal, January 2012

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RADIA: RNA and DNA Integrated Analysis for Somatic Mutation Detection
text, January 2014

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    Toxoplasma Effectors Targeting Host Signaling and Transcription
    journal, April 2017

    • Hakimi, Mohamed-Ali; Olias, Philipp; Sibley, L. David
    • Clinical Microbiology Reviews, Vol. 30, Issue 3
    • DOI: 10.1128/cmr.00005-17

    In vitro characterization of protein effector export in the bradyzoite stage of Toxoplasma gondii
    journal, January 2020

    Toxoplasma GRA15 Activates the NF-κB Pathway through Interactions with TNF Receptor-Associated Factors
    journal, July 2019

    • Sangaré, Lamba Omar; Yang, Ninghan; Konstantinou, Eleni K.
    • mBio, Vol. 10, Issue 4
    • DOI: 10.1128/mbio.00808-19

    Characterization of a Toxoplasma effector uncovers an alternative GSK3/β-catenin-regulatory pathway of inflammation
    journal, October 2018

    • He, Huan; Brenier-Pinchart, Marie-Pierre; Braun, Laurence
    • eLife, Vol. 7
    • DOI: 10.7554/elife.39887

    Toxoplasma Controls Host Cyclin E Expression through the Use of a Novel MYR1-Dependent Effector Protein, HCE1
    journal, April 2019

    In Vitro Characterization of Protein Effector Export in the Bradyzoite Stage of Toxoplasma gondii
    journal, April 2020

    Naïve CD8 T cell IFNγ responses to a vacuolar antigen are regulated by an inflammasome-independent NLRP3 pathway and Toxoplasma gondii ROP5
    journal, August 2020

    Divergent kinase regulates membrane ultrastructure of the Toxoplasma parasitophorous vacuole
    text, January 2019

    A CRISPR platform for targeted in vivo screens identifies Toxoplasma gondii virulence factors in mice.
    text, January 2020

    Divergent kinase regulates membrane ultrastructure of the Toxoplasma parasitophorous vacuole
    text, January 2019

    A CRISPR platform for targeted in vivo screens identifies Toxoplasma gondii virulence factors in mice
    journal, September 2019

    In Vitro Characterization of Protein Effector Export in the Bradyzoite Stage of Toxoplasma gondii
    journal, April 2020

    Toxoplasma gondii Parasitophorous Vacuole Membrane-Associated Dense Granule Proteins Regulate Maturation of the Cyst Wall
    journal, January 2020

    Recent advances in understanding apicomplexan parasites
    journal, January 2016

    Identification of a novel protein complex essential for effector translocation across the parasitophorous vacuole membrane of Toxoplasma gondii
    journal, January 2018

    Toxoplasma gondii Clp family protein: TgClpB1 plays a crucial role in thermotolerance
    journal, September 2017

    Toxoplasma gondii-Derived Synthetic Peptides Containing B- and T-Cell Epitopes from GRA2 Protein Are Able to Enhance Mice Survival in a Model of Experimental Toxoplasmosis
    journal, June 2016

    • Bastos, Luciana M.; Macêdo, Arlindo G.; Silva, Murilo V.
    • Frontiers in Cellular and Infection Microbiology, Vol. 6
    • DOI: 10.3389/fcimb.2016.00059

    Congenital Transmission of Toxoplasma gondii After Experimental Reinfection With Brazilian Typical Strains in Chronically Infected Sheep
    journal, April 2019

    • Chiebao, Daniela Pontes; Pena, Hilda Fátima; Passarelli, Danielle
    • Frontiers in Veterinary Science, Vol. 6
    • DOI: 10.3389/fvets.2019.00093
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