Toxoplasma membrane inositol phospholipid binding protein TgREMIND is essential for secretory organelle function and host infection

Apicomplexan parasites possess specialized secretory organelles called rhoptries, micronemes, and dense granules that play a vital role in host infection. In this study, we demonstrate that TgREMIND, a protein found in Toxoplasma gondii, is necessary for the biogenesis of rhoptries and dense granule...

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Published inCell reports (Cambridge) Vol. 43; no. 1; p. 113601
Main Authors Houngue, Rodrigue, Sangaré, Lamba Omar, Alayi, Tchilabalo Dilezitoko, Dieng, Aissatou, Bitard-Feildel, Tristan, Boulogne, Claire, Slomianny, Christian, Atindehou, Cynthia Menonve, Fanou, Lucie Ayi, Hathout, Yetrib, Callebaut, Isabelle, Tomavo, Stanislas
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 23.01.2024
Elsevier
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Online AccessGet full text
ISSN2211-1247
2639-1856
2211-1247
DOI10.1016/j.celrep.2023.113601

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Abstract Apicomplexan parasites possess specialized secretory organelles called rhoptries, micronemes, and dense granules that play a vital role in host infection. In this study, we demonstrate that TgREMIND, a protein found in Toxoplasma gondii, is necessary for the biogenesis of rhoptries and dense granules. TgREMIND contains a Fes-CIP4 homology-Bin/Amphiphysin/Rvs (F-BAR) domain, which binds to membrane phospholipids, as well as a novel uncharacterized domain that we have named REMIND (regulator of membrane-interacting domain). Both the F-BAR domain and the REMIND are crucial for TgREMIND functions. When TgREMIND is depleted, there is a significant decrease in the abundance of dense granules and abnormal transparency of rhoptries, leading to a reduction in protein secretion from these organelles. The absence of TgREMIND inhibits host invasion and parasite dissemination, demonstrating that TgREMIND is essential for the proper function of critical secretory organelles required for successful infection by Toxoplasma. [Display omitted] •TgREMIND is a membrane-associated protein binding to PIP2 lipids•Both F-BAR domain and REMIND of TgREMIND are required for PIP2 binding•TgREMIND is essential for the biogenesis of rhoptries and dense granules in Toxoplasma•Inactivation of TgREMIND abolished Toxoplasma host cell invasion and dissemination In this study, Houngue et al. describe an essential role for the uncharacterized protein named TgREMIND, for regulator of membrane-interacting domain, in the biogenesis of rhoptries and dense granules, two secretory organelles that contain virulence factors released during and after Toxoplasma cell invasion.
AbstractList Apicomplexan parasites possess specialized secretory organelles called rhoptries, micronemes, and dense granules that play a vital role in host infection. In this study, we demonstrate that TgREMIND, a protein found in Toxoplasma gondii, is necessary for the biogenesis of rhoptries and dense granules. TgREMIND contains a Fes-CIP4 homology-Bin/Amphiphysin/Rvs (F-BAR) domain, which binds to membrane phospholipids, as well as a novel uncharacterized domain that we have named REMIND (regulator of membrane-interacting domain). Both the F-BAR domain and the REMIND are crucial for TgREMIND functions. When TgREMIND is depleted, there is a significant decrease in the abundance of dense granules and abnormal transparency of rhoptries, leading to a reduction in protein secretion from these organelles. The absence of TgREMIND inhibits host invasion and parasite dissemination, demonstrating that TgREMIND is essential for the proper function of critical secretory organelles required for successful infection by Toxoplasma.
Apicomplexan parasites possess specialized secretory organelles called rhoptries, micronemes, and dense granules that play a vital role in host infection. In this study, we demonstrate that TgREMIND, a protein found in Toxoplasma gondii, is necessary for the biogenesis of rhoptries and dense granules. TgREMIND contains a Fes-CIP4 homology-Bin/Amphiphysin/Rvs (F-BAR) domain, which binds to membrane phospholipids, as well as a novel uncharacterized domain that we have named REMIND (regulator of membrane-interacting domain). Both the F-BAR domain and the REMIND are crucial for TgREMIND functions. When TgREMIND is depleted, there is a significant decrease in the abundance of dense granules and abnormal transparency of rhoptries, leading to a reduction in protein secretion from these organelles. The absence of TgREMIND inhibits host invasion and parasite dissemination, demonstrating that TgREMIND is essential for the proper function of critical secretory organelles required for successful infection by Toxoplasma.Apicomplexan parasites possess specialized secretory organelles called rhoptries, micronemes, and dense granules that play a vital role in host infection. In this study, we demonstrate that TgREMIND, a protein found in Toxoplasma gondii, is necessary for the biogenesis of rhoptries and dense granules. TgREMIND contains a Fes-CIP4 homology-Bin/Amphiphysin/Rvs (F-BAR) domain, which binds to membrane phospholipids, as well as a novel uncharacterized domain that we have named REMIND (regulator of membrane-interacting domain). Both the F-BAR domain and the REMIND are crucial for TgREMIND functions. When TgREMIND is depleted, there is a significant decrease in the abundance of dense granules and abnormal transparency of rhoptries, leading to a reduction in protein secretion from these organelles. The absence of TgREMIND inhibits host invasion and parasite dissemination, demonstrating that TgREMIND is essential for the proper function of critical secretory organelles required for successful infection by Toxoplasma.
Apicomplexan parasites possess specialized secretory organelles called rhoptries, micronemes, and dense granules that play a vital role in host infection. In this study, we demonstrate that TgREMIND, a protein found in Toxoplasma gondii, is necessary for the biogenesis of rhoptries and dense granules. TgREMIND contains a Fes-CIP4 homology-Bin/Amphiphysin/Rvs (F-BAR) domain, which binds to membrane phospholipids, as well as a novel uncharacterized domain that we have named REMIND (regulator of membrane-interacting domain). Both the F-BAR domain and the REMIND are crucial for TgREMIND functions. When TgREMIND is depleted, there is a significant decrease in the abundance of dense granules and abnormal transparency of rhoptries, leading to a reduction in protein secretion from these organelles. The absence of TgREMIND inhibits host invasion and parasite dissemination, demonstrating that TgREMIND is essential for the proper function of critical secretory organelles required for successful infection by Toxoplasma
Apicomplexan parasites possess specialized secretory organelles called rhoptries, micronemes, and dense granules that play a vital role in host infection. In this study, we demonstrate that TgREMIND, a protein found in Toxoplasma gondii, is necessary for the biogenesis of rhoptries and dense granules. TgREMIND contains a Fes-CIP4 homology-Bin/Amphiphysin/Rvs (F-BAR) domain, which binds to membrane phospholipids, as well as a novel uncharacterized domain that we have named REMIND (regulator of membrane-interacting domain). Both the F-BAR domain and the REMIND are crucial for TgREMIND functions. When TgREMIND is depleted, there is a significant decrease in the abundance of dense granules and abnormal transparency of rhoptries, leading to a reduction in protein secretion from these organelles. The absence of TgREMIND inhibits host invasion and parasite dissemination, demonstrating that TgREMIND is essential for the proper function of critical secretory organelles required for successful infection by Toxoplasma. [Display omitted] •TgREMIND is a membrane-associated protein binding to PIP2 lipids•Both F-BAR domain and REMIND of TgREMIND are required for PIP2 binding•TgREMIND is essential for the biogenesis of rhoptries and dense granules in Toxoplasma•Inactivation of TgREMIND abolished Toxoplasma host cell invasion and dissemination In this study, Houngue et al. describe an essential role for the uncharacterized protein named TgREMIND, for regulator of membrane-interacting domain, in the biogenesis of rhoptries and dense granules, two secretory organelles that contain virulence factors released during and after Toxoplasma cell invasion.
ArticleNumber 113601
Author Bitard-Feildel, Tristan
Boulogne, Claire
Fanou, Lucie Ayi
Sangaré, Lamba Omar
Atindehou, Cynthia Menonve
Tomavo, Stanislas
Alayi, Tchilabalo Dilezitoko
Dieng, Aissatou
Houngue, Rodrigue
Hathout, Yetrib
Slomianny, Christian
Callebaut, Isabelle
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  givenname: Lamba Omar
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  givenname: Claire
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  surname: Slomianny
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  organization: University of Lille, Laboratory of Cell Physiology, INSERM U 1003, 59655 Villeneuve d'Ascq, France
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  fullname: Atindehou, Cynthia Menonve
  organization: Université d’Abomey Calavi, Laboratoire de Biochimie et de Biologie Moléculaire, Faculté des Sciences et Technologies, Cotonou, Bénin
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  givenname: Lucie Ayi
  surname: Fanou
  fullname: Fanou, Lucie Ayi
  organization: Université d’Abomey Calavi, Laboratoire de Biochimie et de Biologie Moléculaire, Faculté des Sciences et Technologies, Cotonou, Bénin
– sequence: 10
  givenname: Yetrib
  surname: Hathout
  fullname: Hathout, Yetrib
  organization: Department of Pharmaceutical Science, School of Pharmacy and Pharmaceutical Sciences, Binghamton University−SUNY, Johnson City, NY 13790, USA
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  surname: Callebaut
  fullname: Callebaut, Isabelle
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  givenname: Stanislas
  surname: Tomavo
  fullname: Tomavo, Stanislas
  email: stanislas.tomavo@gmail.com
  organization: Université Paris Saclay, CNRS UMR 9198-CEA, Institute for Integrative Biology of the Cell (I2BC), 91190 Gif sur Yvette, France
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Issue 1
Keywords Toxoplasma gondii
membrane lipid binding
TgREMIND protein
REMIND domain
F-BAR-containing protein
CP: Microbiology
apicomplexan parasites
lineage-specific organelles
host cell infection
Language English
License This is an open access article under the CC BY-NC-ND license.
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Snippet Apicomplexan parasites possess specialized secretory organelles called rhoptries, micronemes, and dense granules that play a vital role in host infection. In...
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SubjectTerms Animals
apicomplexan parasites
CP: Microbiology
F-BAR-containing protein
host cell infection
Life Sciences
lineage-specific organelles
membrane lipid binding
Membrane Proteins - metabolism
Microbiology and Parasitology
Organelles - metabolism
Parasites - metabolism
Parasitology
Phosphatidylinositols - metabolism
Protozoan Proteins - metabolism
REMIND domain
TgREMIND protein
Toxoplasma - metabolism
Toxoplasma gondii
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Title Toxoplasma membrane inositol phospholipid binding protein TgREMIND is essential for secretory organelle function and host infection
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https://www.ncbi.nlm.nih.gov/pubmed/38157297
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https://doi.org/10.1016/j.celrep.2023.113601
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