A Glycosylphosphatidylinositol-Anchored Carbonic Anhydrase-Related Protein of <named-content content-type="genus-species">Toxoplasma gondii</named-content> Is Important for Rhoptry Biogenesis and Virulence

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 othe...

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Autores principales:	Nathan M. Chasen, Beejan Asady, Leandro Lemgruber, Rossiane C. Vommaro, Jessica C. Kissinger, Isabelle Coppens, Silvia N. J. Moreno
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	carbonic anhydrase infectivity Toxoplasma gondii glycosylphosphatidylinositols organelle structure rhoptry Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/60ddfb8fd73a43078878e276965dd038
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spelling	oai:doaj.org-article:60ddfb8fd73a43078878e276965dd0382021-11-15T15:21:47ZA Glycosylphosphatidylinositol-Anchored Carbonic Anhydrase-Related Protein of <named-content content-type="genus-species">Toxoplasma gondii</named-content> Is Important for Rhoptry Biogenesis and Virulence10.1128/mSphere.00027-172379-5042https://doaj.org/article/60ddfb8fd73a43078878e276965dd0382017-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00027-17https://doaj.org/toc/2379-5042ABSTRACT 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.Nathan M. ChasenBeejan AsadyLeandro LemgruberRossiane C. VommaroJessica C. KissingerIsabelle CoppensSilvia N. J. MorenoAmerican Society for Microbiologyarticlecarbonic anhydraseinfectivityToxoplasma gondiiglycosylphosphatidylinositolsorganelle structurerhoptryMicrobiologyQR1-502ENmSphere, Vol 2, Iss 3 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	carbonic anhydrase infectivity Toxoplasma gondii glycosylphosphatidylinositols organelle structure rhoptry Microbiology QR1-502
spellingShingle	carbonic anhydrase infectivity Toxoplasma gondii glycosylphosphatidylinositols organelle structure rhoptry Microbiology QR1-502 Nathan M. Chasen Beejan Asady Leandro Lemgruber Rossiane C. Vommaro Jessica C. Kissinger Isabelle Coppens Silvia N. J. Moreno A Glycosylphosphatidylinositol-Anchored Carbonic Anhydrase-Related Protein of <named-content content-type="genus-species">Toxoplasma gondii</named-content> Is Important for Rhoptry Biogenesis and Virulence
description	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.
format	article
author	Nathan M. Chasen Beejan Asady Leandro Lemgruber Rossiane C. Vommaro Jessica C. Kissinger Isabelle Coppens Silvia N. J. Moreno
author_facet	Nathan M. Chasen Beejan Asady Leandro Lemgruber Rossiane C. Vommaro Jessica C. Kissinger Isabelle Coppens Silvia N. J. Moreno
author_sort	Nathan M. Chasen
title	A Glycosylphosphatidylinositol-Anchored Carbonic Anhydrase-Related Protein of <named-content content-type="genus-species">Toxoplasma gondii</named-content> Is Important for Rhoptry Biogenesis and Virulence
title_short	A Glycosylphosphatidylinositol-Anchored Carbonic Anhydrase-Related Protein of <named-content content-type="genus-species">Toxoplasma gondii</named-content> Is Important for Rhoptry Biogenesis and Virulence
title_full	A Glycosylphosphatidylinositol-Anchored Carbonic Anhydrase-Related Protein of <named-content content-type="genus-species">Toxoplasma gondii</named-content> Is Important for Rhoptry Biogenesis and Virulence
title_fullStr	A Glycosylphosphatidylinositol-Anchored Carbonic Anhydrase-Related Protein of <named-content content-type="genus-species">Toxoplasma gondii</named-content> Is Important for Rhoptry Biogenesis and Virulence
title_full_unstemmed	A Glycosylphosphatidylinositol-Anchored Carbonic Anhydrase-Related Protein of <named-content content-type="genus-species">Toxoplasma gondii</named-content> Is Important for Rhoptry Biogenesis and Virulence
title_sort	glycosylphosphatidylinositol-anchored carbonic anhydrase-related protein of <named-content content-type="genus-species">toxoplasma gondii</named-content> is important for rhoptry biogenesis and virulence
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/60ddfb8fd73a43078878e276965dd038
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A Glycosylphosphatidylinositol-Anchored Carbonic Anhydrase-Related Protein of <named-content content-type="genus-species">Toxoplasma gondii</named-content> Is Important for Rhoptry Biogenesis and Virulence

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