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Budding pouches and associated bubbles: 3D visualization of exo-membrane structures in plasmodium falciparum gametocytes

Plasmodium falciparum gametocytes have unique morphology, metabolism, and protein expression profiles in their asexual stages of development. In addition to the striking changes in their appearance, a wide variety of “exo-membrane structures” are newly formed in the gametocyte stage. Little is known...

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Detalles Bibliográficos
Autores principales: Hayakawa, Eri Saki H., Wayama, Marina, Tokumasu, Fuyuki, Ohno, Nobuhiko, Matsumoto, Mami, Usukura, Jiro
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9441640/
https://www.ncbi.nlm.nih.gov/pubmed/36072224
http://dx.doi.org/10.3389/fcimb.2022.962495
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author Hayakawa, Eri Saki H.
Wayama, Marina
Tokumasu, Fuyuki
Ohno, Nobuhiko
Matsumoto, Mami
Usukura, Jiro
author_facet Hayakawa, Eri Saki H.
Wayama, Marina
Tokumasu, Fuyuki
Ohno, Nobuhiko
Matsumoto, Mami
Usukura, Jiro
author_sort Hayakawa, Eri Saki H.
collection PubMed
description Plasmodium falciparum gametocytes have unique morphology, metabolism, and protein expression profiles in their asexual stages of development. In addition to the striking changes in their appearance, a wide variety of “exo-membrane structures” are newly formed in the gametocyte stage. Little is known about their function, localization, or three-dimensional structural information, and only some structural data, typically two-dimensional, have been reported using conventional electron microscopy or fluorescence microscopy. For better visualization of intracellular organelle and exo-membrane structures, we previously established an unroofing technique to directly observe Maurer’s clefts (MCs) in asexual parasitized erythrocytes by removing the top part of the cell’s membrane followed by transmission electron microscopy. We found that MCs have numerous tethers connecting themselves to the host erythrocyte membrane skeletons. In this study, we investigated the intracellular structures of gametocytes using unroofing-TEM, Serial Block Face scanning electron microscopy, and fluorescence microscopy to unveil the exo-membrane structures in gametocytes. Our data showed “balloon/pouch”-like objects budding from the parasitophorous vacuole membrane (PVM) in gametocytes, and some balloons included multiple layers of other balloons. Furthermore, numerous bubbles appeared on the inner surface of the erythrocyte membrane or PVM; these were similar to MC-like membranes but were smaller than asexual MCs. Our study demonstrated P. falciparum reforms exo-membranes in erythrocytes to meet stage-specific biological activities during their sexual development.
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spelling pubmed-94416402022-09-06 Budding pouches and associated bubbles: 3D visualization of exo-membrane structures in plasmodium falciparum gametocytes Hayakawa, Eri Saki H. Wayama, Marina Tokumasu, Fuyuki Ohno, Nobuhiko Matsumoto, Mami Usukura, Jiro Front Cell Infect Microbiol Cellular and Infection Microbiology Plasmodium falciparum gametocytes have unique morphology, metabolism, and protein expression profiles in their asexual stages of development. In addition to the striking changes in their appearance, a wide variety of “exo-membrane structures” are newly formed in the gametocyte stage. Little is known about their function, localization, or three-dimensional structural information, and only some structural data, typically two-dimensional, have been reported using conventional electron microscopy or fluorescence microscopy. For better visualization of intracellular organelle and exo-membrane structures, we previously established an unroofing technique to directly observe Maurer’s clefts (MCs) in asexual parasitized erythrocytes by removing the top part of the cell’s membrane followed by transmission electron microscopy. We found that MCs have numerous tethers connecting themselves to the host erythrocyte membrane skeletons. In this study, we investigated the intracellular structures of gametocytes using unroofing-TEM, Serial Block Face scanning electron microscopy, and fluorescence microscopy to unveil the exo-membrane structures in gametocytes. Our data showed “balloon/pouch”-like objects budding from the parasitophorous vacuole membrane (PVM) in gametocytes, and some balloons included multiple layers of other balloons. Furthermore, numerous bubbles appeared on the inner surface of the erythrocyte membrane or PVM; these were similar to MC-like membranes but were smaller than asexual MCs. Our study demonstrated P. falciparum reforms exo-membranes in erythrocytes to meet stage-specific biological activities during their sexual development. Frontiers Media S.A. 2022-08-22 /pmc/articles/PMC9441640/ /pubmed/36072224 http://dx.doi.org/10.3389/fcimb.2022.962495 Text en Copyright © 2022 Hayakawa, Wayama, Tokumasu, Ohno, Matsumoto and Usukura https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cellular and Infection Microbiology
Hayakawa, Eri Saki H.
Wayama, Marina
Tokumasu, Fuyuki
Ohno, Nobuhiko
Matsumoto, Mami
Usukura, Jiro
Budding pouches and associated bubbles: 3D visualization of exo-membrane structures in plasmodium falciparum gametocytes
title Budding pouches and associated bubbles: 3D visualization of exo-membrane structures in plasmodium falciparum gametocytes
title_full Budding pouches and associated bubbles: 3D visualization of exo-membrane structures in plasmodium falciparum gametocytes
title_fullStr Budding pouches and associated bubbles: 3D visualization of exo-membrane structures in plasmodium falciparum gametocytes
title_full_unstemmed Budding pouches and associated bubbles: 3D visualization of exo-membrane structures in plasmodium falciparum gametocytes
title_short Budding pouches and associated bubbles: 3D visualization of exo-membrane structures in plasmodium falciparum gametocytes
title_sort budding pouches and associated bubbles: 3d visualization of exo-membrane structures in plasmodium falciparum gametocytes
topic Cellular and Infection Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9441640/
https://www.ncbi.nlm.nih.gov/pubmed/36072224
http://dx.doi.org/10.3389/fcimb.2022.962495
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