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Research Article | Host-Microbe Biology

A Glycosylphosphatidylinositol-Anchored Carbonic Anhydrase-Related Protein of Toxoplasma gondii Is Important for Rhoptry Biogenesis and Virulence

Nathan M. Chasen, Beejan Asady, Leandro Lemgruber, Rossiane C. Vommaro, Jessica C. Kissinger, Isabelle Coppens, Silvia N. J. Moreno
William J. Sullivan Jr., Editor
Nathan M. Chasen
aCenter for Tropical and Emerging Global Diseases, University of Georgia, Athens, Georgia, USA
bDepartment of Infectious Diseases, University of Georgia, Athens, Georgia, USA
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Beejan Asady
aCenter for Tropical and Emerging Global Diseases, University of Georgia, Athens, Georgia, USA
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Leandro Lemgruber
cInstituto Nacional de Metrologia, Inmetro-RJ, UFRJ, Rio de Janeiro, Brazil
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Rossiane C. Vommaro
dInstituto de Biofísica Carlos Chagas Filho, UFRJ, Rio de Janeiro, Brazil
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Jessica C. Kissinger
aCenter for Tropical and Emerging Global Diseases, University of Georgia, Athens, Georgia, USA
eDepartment of Genetics, University of Georgia, Athens, Georgia, USA
fInstitute of Bioinformatics, University of Georgia, Athens, Georgia, USA
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Isabelle Coppens
gDepartment of Molecular Microbiology and Immunology, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, USA
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Silvia N. J. Moreno
aCenter for Tropical and Emerging Global Diseases, University of Georgia, Athens, Georgia, USA
hDepartment of Cellular Biology, University of Georgia, Athens, Georgia, USA
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William J. Sullivan Jr.
Indiana University School of Medicine
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DOI: 10.1128/mSphere.00027-17
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ABSTRACT

Carbonic anhydrase-related proteins (CARPs) have previously been described as catalytically inactive proteins closely related to α-carbonic anhydrases (α-CAs). These CARPs are found in animals (both vertebrates and invertebrates) and viruses as either independent proteins or domains of other proteins. We report here the identification of a new CARP (TgCA_RP) in the unicellular organism Toxoplasma gondii that is related to the recently described η-class CA found in Plasmodium falciparum. TgCA_RP is posttranslationally modified at its C terminus with a glycosylphosphatidylinositol anchor that is important for its localization in intracellular tachyzoites. The protein localizes throughout the rhoptry bulbs of mature tachyzoites and to the outer membrane of nascent rhoptries in dividing tachyzoites, as demonstrated by immunofluorescence and immunoelectron microscopy using specific antibodies. T. gondii mutant tachyzoites lacking TgCA_RP display a growth and invasion phenotype in vitro and have atypical rhoptry morphology. The mutants also exhibit reduced virulence in a mouse model. Our results show that TgCA_RP plays an important role in the biogenesis of rhoptries.

IMPORTANCE Toxoplasma gondii is an intracellular pathogen that infects humans and animals. The pathogenesis of T. gondii is linked to its lytic cycle, which starts when tachyzoites invade host cells and secrete proteins from specialized organelles. Once inside the host cell, the parasite creates a parasitophorous vacuole (PV) where it divides. Rhoptries are specialized secretory organelles that contain proteins, many of which are secreted during invasion. These proteins have important roles not only during the initial interaction between parasite and host but also in the formation of the PV and in the modification of the host cell. We report here the identification of a new T. gondii carbonic anhydrase-related protein (TgCA_RP), which localizes to rhoptries of mature tachyzoites. TgCA_RP is important for the morphology of rhoptries and for invasion and growth of parasites. TgCA_RP is also critical for parasite virulence. We propose that TgCA_RP plays a role in the biogenesis of rhoptries.

  • Copyright © 2017 Chasen 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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A Glycosylphosphatidylinositol-Anchored Carbonic Anhydrase-Related Protein of Toxoplasma gondii Is Important for Rhoptry Biogenesis and Virulence
Nathan M. Chasen, Beejan Asady, Leandro Lemgruber, Rossiane C. Vommaro, Jessica C. Kissinger, Isabelle Coppens, Silvia N. J. Moreno
mSphere May 2017, 2 (3) e00027-17; DOI: 10.1128/mSphere.00027-17

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A Glycosylphosphatidylinositol-Anchored Carbonic Anhydrase-Related Protein of Toxoplasma gondii Is Important for Rhoptry Biogenesis and Virulence
Nathan M. Chasen, Beejan Asady, Leandro Lemgruber, Rossiane C. Vommaro, Jessica C. Kissinger, Isabelle Coppens, Silvia N. J. Moreno
mSphere May 2017, 2 (3) e00027-17; DOI: 10.1128/mSphere.00027-17
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KEYWORDS

carbonic anhydrase
infectivity
Toxoplasma gondii
glycosylphosphatidylinositols
organelle structure
rhoptry

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