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Research Article | Host-Microbe Biology

The Toxoplasma gondii Active Serine Hydrolase 4 Regulates Parasite Division and Intravacuolar Parasite Architecture

Ian T. Foe, Ouma Onguka, Katherine Amberg-Johnson, Rikki M. Garner, Neri Amara, Wandy Beatty, Ellen Yeh, Matthew Bogyo
Ira J. Blader, Editor
Ian T. Foe
aDepartment of Pathology, Stanford University School of Medicine, Stanford, California, USA
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Ouma Onguka
aDepartment of Pathology, Stanford University School of Medicine, Stanford, California, USA
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Katherine Amberg-Johnson
bMicrobiology and Immunology, Stanford University School of Medicine, Stanford, California, USA
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Rikki M. Garner
cBiophysics Program, Stanford University School of Medicine, Stanford, California, USA
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Neri Amara
aDepartment of Pathology, Stanford University School of Medicine, Stanford, California, USA
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Wandy Beatty
dDepartment of Molecular Microbiology, Washington University School of Medicine, Saint Louis, Missouri, USA
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Ellen Yeh
aDepartment of Pathology, Stanford University School of Medicine, Stanford, California, USA
bMicrobiology and Immunology, Stanford University School of Medicine, Stanford, California, USA
eDepartment of Biochemistry, Stanford University School of Medicine, Stanford, California, USA
fChan Zuckerburg Biohub, San Francisco, California, USA
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Matthew Bogyo
aDepartment of Pathology, Stanford University School of Medicine, Stanford, California, USA
bMicrobiology and Immunology, Stanford University School of Medicine, Stanford, California, USA
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Ira J. Blader
University at Buffalo
Roles: Editor
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DOI: 10.1128/mSphere.00393-18
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This article has a correction. Please see:

  • Erratum for Foe et al., “The Toxoplasma gondii Active Serine Hydrolase 4 Regulates Parasite Division and Intravacuolar Parasite Architecture”
    - October 10, 2018

ABSTRACT

Hydrolase are enzymes that regulate diverse biological processes, including posttranslational protein modifications. Recent work identified four active serine hydrolases (ASHs) in Toxoplasma gondii as candidate depalmitoylases. However, only TgPPT1 (ASH1) has been confirmed to remove palmitate from proteins. ASH4 (TgME49_264290) was reported to be refractory to genetic disruption. We demonstrate that recombinant ASH4 is an esterase that processes short acyl esters but not palmitoyl thioesters. Genetic disruption of ASH4 causes defects in cell division and premature scission of parasites from residual bodies. These defects lead to the presence of vacuoles with a disordered intravacuolar architecture, with parasites arranged in pairs around multiple residual bodies. Importantly, we found that the deletion of ASH4 correlates with a defect in radial dispersion from host cells after egress. This defect in dispersion of parasites is a general phenomenon that is observed for disordered vacuoles that occur at low frequency in wild-type parasites, suggesting a possible general link between intravacuolar organization and dispersion after egress.

IMPORTANCE This work defines the function of an enzyme in the obligate intracellular parasite Toxoplasma gondii. We show that this previously uncharacterized enzyme is critical for aspects of cellular division by the parasite and that loss of this enzyme leads to parasites with cell division defects and which also are disorganized inside their vacuoles. This leads to defects in the ability of the parasite to disseminate from the site of an infection and may have a significant impact on the parasite's overall infectivity of a host organism.

  • Copyright © 2018 Foe et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

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The Toxoplasma gondii Active Serine Hydrolase 4 Regulates Parasite Division and Intravacuolar Parasite Architecture
Ian T. Foe, Ouma Onguka, Katherine Amberg-Johnson, Rikki M. Garner, Neri Amara, Wandy Beatty, Ellen Yeh, Matthew Bogyo
mSphere Sep 2018, 3 (5) e00393-18; DOI: 10.1128/mSphere.00393-18

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The Toxoplasma gondii Active Serine Hydrolase 4 Regulates Parasite Division and Intravacuolar Parasite Architecture
Ian T. Foe, Ouma Onguka, Katherine Amberg-Johnson, Rikki M. Garner, Neri Amara, Wandy Beatty, Ellen Yeh, Matthew Bogyo
mSphere Sep 2018, 3 (5) e00393-18; DOI: 10.1128/mSphere.00393-18
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KEYWORDS

ASH proteins
serine hydrolase
cell division
intravacuolar organization

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