Ultrastructural and Functional Analysis of a Novel Extra-Axonemal Structure in Parasitic Trichomonads

Autores
Cóceres, Verónica Mabel; Iriarte, Lucrecia Soledad; Miranda Magalhães, Abigail; Santos de Andrade, Thiago André; de Miguel, Natalia; Pereira-Neves, Antonio
Año de publicación
2021
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Trichomonas vaginalis and Tritrichomonas foetus are extracellular flagellated parasites that inhabit humans and other mammals, respectively. In addition to motility, flagella act in a variety of biological processes in different cell types, and extra-axonemal structures (EASs) have been described as fibrillar structures that provide mechanical support and act as metabolic, homeostatic, and sensory platforms in many organisms. It has been assumed that T. vaginalis and T. foetus do not have EASs. However, here, we used complementary electron microscopy techniques to reveal the ultrastructure of EASs in both parasites. Such EASs are thin filaments (3–5 nm diameter) running longitudinally along the axonemes and surrounded by the flagellar membrane, forming prominent flagellar swellings. We observed that the formation of EAS increases after parasite adhesion on the host cells, fibronectin, and precationized surfaces. A high number of rosettes, clusters of intramembrane particles that have been proposed as sensorial structures, and microvesicles protruding from the membrane were observed in the EASs. Our observations demonstrate that T. vaginalis and T. foetus can connect to themselves by EASs present in flagella. The protein VPS32, a member of the ESCRT-III complex crucial for diverse membrane remodeling events, the pinching off and release of microvesicles, was found in the surface as well as in microvesicles protruding from EASs. Moreover, we demonstrated that the formation of EAS also increases in parasites overexpressing VPS32 and that T. vaginalis-VPS32 parasites showed greater motility in semisolid agar. These results provide valuable data about the role of the flagellar EASs in the cell-to-cell communication and pathogenesis of these extracellular parasites.
Fil: Cóceres, Verónica Mabel. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas "Dr. Raúl Alfonsín" (sede Chascomús). Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas "Dr. Raúl Alfonsín" (sede Chascomús); Argentina
Fil: Iriarte, Lucrecia Soledad. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas "Dr. Raúl Alfonsín" (sede Chascomús). Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas "Dr. Raúl Alfonsín" (sede Chascomús); Argentina
Fil: Miranda Magalhães, Abigail. Instituto Aggeu Magalhães, Fiocruz, Recife; Brasil
Fil: Santos de Andrade, Thiago André. Instituto Aggeu Magalhães, Fiocruz, Recife; Brasil
Fil: de Miguel, Natalia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas "Dr. Raúl Alfonsín" (sede Chascomús). Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas "Dr. Raúl Alfonsín" (sede Chascomús); Argentina
Fil: Pereira-Neves, Antonio. Instituto Aggeu Magalhães, Fiocruz, Recife; Brasil
Materia
CELL ATTACHMENT
ELECTRON MICROSCOPY
FLAGELLA
PARASITE–HOST CELL INTERACTION
TRICHOMONAS VAGINALIS
TRITRICHOMONAS FOETUS
VPS32
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/164968
Acceder
id CONICETDig_cbb70bf0f481d80c724430237965fcaf
oai_identifier_str oai:ri.conicet.gov.ar:11336/164968
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Ultrastructural and Functional Analysis of a Novel Extra-Axonemal Structure in Parasitic TrichomonadsCóceres, Verónica MabelIriarte, Lucrecia SoledadMiranda Magalhães, AbigailSantos de Andrade, Thiago Andréde Miguel, NataliaPereira-Neves, AntonioCELL ATTACHMENTELECTRON MICROSCOPYFLAGELLAPARASITE–HOST CELL INTERACTIONTRICHOMONAS VAGINALISTRITRICHOMONAS FOETUSVPS32https://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Trichomonas vaginalis and Tritrichomonas foetus are extracellular flagellated parasites that inhabit humans and other mammals, respectively. In addition to motility, flagella act in a variety of biological processes in different cell types, and extra-axonemal structures (EASs) have been described as fibrillar structures that provide mechanical support and act as metabolic, homeostatic, and sensory platforms in many organisms. It has been assumed that T. vaginalis and T. foetus do not have EASs. However, here, we used complementary electron microscopy techniques to reveal the ultrastructure of EASs in both parasites. Such EASs are thin filaments (3–5 nm diameter) running longitudinally along the axonemes and surrounded by the flagellar membrane, forming prominent flagellar swellings. We observed that the formation of EAS increases after parasite adhesion on the host cells, fibronectin, and precationized surfaces. A high number of rosettes, clusters of intramembrane particles that have been proposed as sensorial structures, and microvesicles protruding from the membrane were observed in the EASs. Our observations demonstrate that T. vaginalis and T. foetus can connect to themselves by EASs present in flagella. The protein VPS32, a member of the ESCRT-III complex crucial for diverse membrane remodeling events, the pinching off and release of microvesicles, was found in the surface as well as in microvesicles protruding from EASs. Moreover, we demonstrated that the formation of EAS also increases in parasites overexpressing VPS32 and that T. vaginalis-VPS32 parasites showed greater motility in semisolid agar. These results provide valuable data about the role of the flagellar EASs in the cell-to-cell communication and pathogenesis of these extracellular parasites.Fil: Cóceres, Verónica Mabel. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas "Dr. Raúl Alfonsín" (sede Chascomús). Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas "Dr. Raúl Alfonsín" (sede Chascomús); ArgentinaFil: Iriarte, Lucrecia Soledad. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas "Dr. Raúl Alfonsín" (sede Chascomús). Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas "Dr. Raúl Alfonsín" (sede Chascomús); ArgentinaFil: Miranda Magalhães, Abigail. Instituto Aggeu Magalhães, Fiocruz, Recife; BrasilFil: Santos de Andrade, Thiago André. Instituto Aggeu Magalhães, Fiocruz, Recife; BrasilFil: de Miguel, Natalia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas "Dr. Raúl Alfonsín" (sede Chascomús). Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas "Dr. Raúl Alfonsín" (sede Chascomús); ArgentinaFil: Pereira-Neves, Antonio. Instituto Aggeu Magalhães, Fiocruz, Recife; BrasilFrontiers Media2021-11info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/164968Cóceres, Verónica Mabel; Iriarte, Lucrecia Soledad; Miranda Magalhães, Abigail; Santos de Andrade, Thiago André; de Miguel, Natalia; et al.; Ultrastructural and Functional Analysis of a Novel Extra-Axonemal Structure in Parasitic Trichomonads; Frontiers Media; Frontiers in Cellular and Infection Microbiology; 11; 75185; 11-2021; 1-212235-2988CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://www.frontiersin.org/articles/10.3389/fcimb.2021.757185/fullinfo:eu-repo/semantics/altIdentifier/doi/10.3389/fcimb.2021.757185info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2026-04-28T12:44:47Zoai:ri.conicet.gov.ar:11336/164968instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982026-04-28 12:44:47.637CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Ultrastructural and Functional Analysis of a Novel Extra-Axonemal Structure in Parasitic Trichomonads
title Ultrastructural and Functional Analysis of a Novel Extra-Axonemal Structure in Parasitic Trichomonads
spellingShingle Ultrastructural and Functional Analysis of a Novel Extra-Axonemal Structure in Parasitic Trichomonads
Cóceres, Verónica Mabel
CELL ATTACHMENT
ELECTRON MICROSCOPY
FLAGELLA
PARASITE–HOST CELL INTERACTION
TRICHOMONAS VAGINALIS
TRITRICHOMONAS FOETUS
VPS32
title_short Ultrastructural and Functional Analysis of a Novel Extra-Axonemal Structure in Parasitic Trichomonads
title_full Ultrastructural and Functional Analysis of a Novel Extra-Axonemal Structure in Parasitic Trichomonads
title_fullStr Ultrastructural and Functional Analysis of a Novel Extra-Axonemal Structure in Parasitic Trichomonads
title_full_unstemmed Ultrastructural and Functional Analysis of a Novel Extra-Axonemal Structure in Parasitic Trichomonads
title_sort Ultrastructural and Functional Analysis of a Novel Extra-Axonemal Structure in Parasitic Trichomonads
dc.creator.none.fl_str_mv Cóceres, Verónica Mabel
Iriarte, Lucrecia Soledad
Miranda Magalhães, Abigail
Santos de Andrade, Thiago André
de Miguel, Natalia
Pereira-Neves, Antonio
author Cóceres, Verónica Mabel
author_facet Cóceres, Verónica Mabel
Iriarte, Lucrecia Soledad
Miranda Magalhães, Abigail
Santos de Andrade, Thiago André
de Miguel, Natalia
Pereira-Neves, Antonio
author_role author
author2 Iriarte, Lucrecia Soledad
Miranda Magalhães, Abigail
Santos de Andrade, Thiago André
de Miguel, Natalia
Pereira-Neves, Antonio
author2_role author
author
author
author
author
dc.subject.none.fl_str_mv CELL ATTACHMENT
ELECTRON MICROSCOPY
FLAGELLA
PARASITE–HOST CELL INTERACTION
TRICHOMONAS VAGINALIS
TRITRICHOMONAS FOETUS
VPS32
topic CELL ATTACHMENT
ELECTRON MICROSCOPY
FLAGELLA
PARASITE–HOST CELL INTERACTION
TRICHOMONAS VAGINALIS
TRITRICHOMONAS FOETUS
VPS32
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Trichomonas vaginalis and Tritrichomonas foetus are extracellular flagellated parasites that inhabit humans and other mammals, respectively. In addition to motility, flagella act in a variety of biological processes in different cell types, and extra-axonemal structures (EASs) have been described as fibrillar structures that provide mechanical support and act as metabolic, homeostatic, and sensory platforms in many organisms. It has been assumed that T. vaginalis and T. foetus do not have EASs. However, here, we used complementary electron microscopy techniques to reveal the ultrastructure of EASs in both parasites. Such EASs are thin filaments (3–5 nm diameter) running longitudinally along the axonemes and surrounded by the flagellar membrane, forming prominent flagellar swellings. We observed that the formation of EAS increases after parasite adhesion on the host cells, fibronectin, and precationized surfaces. A high number of rosettes, clusters of intramembrane particles that have been proposed as sensorial structures, and microvesicles protruding from the membrane were observed in the EASs. Our observations demonstrate that T. vaginalis and T. foetus can connect to themselves by EASs present in flagella. The protein VPS32, a member of the ESCRT-III complex crucial for diverse membrane remodeling events, the pinching off and release of microvesicles, was found in the surface as well as in microvesicles protruding from EASs. Moreover, we demonstrated that the formation of EAS also increases in parasites overexpressing VPS32 and that T. vaginalis-VPS32 parasites showed greater motility in semisolid agar. These results provide valuable data about the role of the flagellar EASs in the cell-to-cell communication and pathogenesis of these extracellular parasites.
Fil: Cóceres, Verónica Mabel. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas "Dr. Raúl Alfonsín" (sede Chascomús). Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas "Dr. Raúl Alfonsín" (sede Chascomús); Argentina
Fil: Iriarte, Lucrecia Soledad. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas "Dr. Raúl Alfonsín" (sede Chascomús). Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas "Dr. Raúl Alfonsín" (sede Chascomús); Argentina
Fil: Miranda Magalhães, Abigail. Instituto Aggeu Magalhães, Fiocruz, Recife; Brasil
Fil: Santos de Andrade, Thiago André. Instituto Aggeu Magalhães, Fiocruz, Recife; Brasil
Fil: de Miguel, Natalia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas "Dr. Raúl Alfonsín" (sede Chascomús). Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. Instituto de Investigaciones Biotecnológicas "Dr. Raúl Alfonsín" (sede Chascomús); Argentina
Fil: Pereira-Neves, Antonio. Instituto Aggeu Magalhães, Fiocruz, Recife; Brasil
description Trichomonas vaginalis and Tritrichomonas foetus are extracellular flagellated parasites that inhabit humans and other mammals, respectively. In addition to motility, flagella act in a variety of biological processes in different cell types, and extra-axonemal structures (EASs) have been described as fibrillar structures that provide mechanical support and act as metabolic, homeostatic, and sensory platforms in many organisms. It has been assumed that T. vaginalis and T. foetus do not have EASs. However, here, we used complementary electron microscopy techniques to reveal the ultrastructure of EASs in both parasites. Such EASs are thin filaments (3–5 nm diameter) running longitudinally along the axonemes and surrounded by the flagellar membrane, forming prominent flagellar swellings. We observed that the formation of EAS increases after parasite adhesion on the host cells, fibronectin, and precationized surfaces. A high number of rosettes, clusters of intramembrane particles that have been proposed as sensorial structures, and microvesicles protruding from the membrane were observed in the EASs. Our observations demonstrate that T. vaginalis and T. foetus can connect to themselves by EASs present in flagella. The protein VPS32, a member of the ESCRT-III complex crucial for diverse membrane remodeling events, the pinching off and release of microvesicles, was found in the surface as well as in microvesicles protruding from EASs. Moreover, we demonstrated that the formation of EAS also increases in parasites overexpressing VPS32 and that T. vaginalis-VPS32 parasites showed greater motility in semisolid agar. These results provide valuable data about the role of the flagellar EASs in the cell-to-cell communication and pathogenesis of these extracellular parasites.
publishDate 2021
dc.date.none.fl_str_mv 2021-11
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/164968
Cóceres, Verónica Mabel; Iriarte, Lucrecia Soledad; Miranda Magalhães, Abigail; Santos de Andrade, Thiago André; de Miguel, Natalia; et al.; Ultrastructural and Functional Analysis of a Novel Extra-Axonemal Structure in Parasitic Trichomonads; Frontiers Media; Frontiers in Cellular and Infection Microbiology; 11; 75185; 11-2021; 1-21
2235-2988
CONICET Digital
CONICET
url http://hdl.handle.net/11336/164968
identifier_str_mv Cóceres, Verónica Mabel; Iriarte, Lucrecia Soledad; Miranda Magalhães, Abigail; Santos de Andrade, Thiago André; de Miguel, Natalia; et al.; Ultrastructural and Functional Analysis of a Novel Extra-Axonemal Structure in Parasitic Trichomonads; Frontiers Media; Frontiers in Cellular and Infection Microbiology; 11; 75185; 11-2021; 1-21
2235-2988
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/https://www.frontiersin.org/articles/10.3389/fcimb.2021.757185/full
info:eu-repo/semantics/altIdentifier/doi/10.3389/fcimb.2021.757185
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Frontiers Media
publisher.none.fl_str_mv Frontiers Media
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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score 13.039539

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