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Proteomic analysis of the Plasmodium male gamete reveals the key role for glycolysis in flagellar motility

BACKGROUND: Gametogenesis and fertilization play crucial roles in malaria transmission. While male gametes are thought to be amongst the simplest eukaryotic cells and are proven targets of transmission blocking immunity, little is known about their molecular organization. For example, the pathway of...

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Autores principales: Talman, Arthur M, Prieto, Judith H, Marques, Sara, Ubaida-Mohien, Ceereena, Lawniczak, Mara, Wass, Mark N, Xu, Tao, Frank, Roland, Ecker, Andrea, Stanway, Rebecca S, Krishna, Sanjeev, Sternberg, Michael JE, Christophides, Georges K, Graham, David R, Dinglasan, Rhoel R, Yates, John R, Sinden, Robert E
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4150949/
https://www.ncbi.nlm.nih.gov/pubmed/25124718
http://dx.doi.org/10.1186/1475-2875-13-315
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author Talman, Arthur M
Prieto, Judith H
Marques, Sara
Ubaida-Mohien, Ceereena
Lawniczak, Mara
Wass, Mark N
Xu, Tao
Frank, Roland
Ecker, Andrea
Stanway, Rebecca S
Krishna, Sanjeev
Sternberg, Michael JE
Christophides, Georges K
Graham, David R
Dinglasan, Rhoel R
Yates, John R
Sinden, Robert E
author_facet Talman, Arthur M
Prieto, Judith H
Marques, Sara
Ubaida-Mohien, Ceereena
Lawniczak, Mara
Wass, Mark N
Xu, Tao
Frank, Roland
Ecker, Andrea
Stanway, Rebecca S
Krishna, Sanjeev
Sternberg, Michael JE
Christophides, Georges K
Graham, David R
Dinglasan, Rhoel R
Yates, John R
Sinden, Robert E
author_sort Talman, Arthur M
collection PubMed
description BACKGROUND: Gametogenesis and fertilization play crucial roles in malaria transmission. While male gametes are thought to be amongst the simplest eukaryotic cells and are proven targets of transmission blocking immunity, little is known about their molecular organization. For example, the pathway of energy metabolism that power motility, a feature that facilitates gamete encounter and fertilization, is unknown. METHODS: Plasmodium berghei microgametes were purified and analysed by whole-cell proteomic analysis for the first time. Data are available via ProteomeXchange with identifier PXD001163. RESULTS: 615 proteins were recovered, they included all male gamete proteins described thus far. Amongst them were the 11 enzymes of the glycolytic pathway. The hexose transporter was localized to the gamete plasma membrane and it was shown that microgamete motility can be suppressed effectively by inhibitors of this transporter and of the glycolytic pathway. CONCLUSIONS: This study describes the first whole-cell proteomic analysis of the malaria male gamete. It identifies glycolysis as the likely exclusive source of energy for flagellar beat, and provides new insights in original features of Plasmodium flagellar organization. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1475-2875-13-315) contains supplementary material, which is available to authorized users.
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spelling pubmed-41509492014-09-03 Proteomic analysis of the Plasmodium male gamete reveals the key role for glycolysis in flagellar motility Talman, Arthur M Prieto, Judith H Marques, Sara Ubaida-Mohien, Ceereena Lawniczak, Mara Wass, Mark N Xu, Tao Frank, Roland Ecker, Andrea Stanway, Rebecca S Krishna, Sanjeev Sternberg, Michael JE Christophides, Georges K Graham, David R Dinglasan, Rhoel R Yates, John R Sinden, Robert E Malar J Research BACKGROUND: Gametogenesis and fertilization play crucial roles in malaria transmission. While male gametes are thought to be amongst the simplest eukaryotic cells and are proven targets of transmission blocking immunity, little is known about their molecular organization. For example, the pathway of energy metabolism that power motility, a feature that facilitates gamete encounter and fertilization, is unknown. METHODS: Plasmodium berghei microgametes were purified and analysed by whole-cell proteomic analysis for the first time. Data are available via ProteomeXchange with identifier PXD001163. RESULTS: 615 proteins were recovered, they included all male gamete proteins described thus far. Amongst them were the 11 enzymes of the glycolytic pathway. The hexose transporter was localized to the gamete plasma membrane and it was shown that microgamete motility can be suppressed effectively by inhibitors of this transporter and of the glycolytic pathway. CONCLUSIONS: This study describes the first whole-cell proteomic analysis of the malaria male gamete. It identifies glycolysis as the likely exclusive source of energy for flagellar beat, and provides new insights in original features of Plasmodium flagellar organization. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1475-2875-13-315) contains supplementary material, which is available to authorized users. BioMed Central 2014-08-13 /pmc/articles/PMC4150949/ /pubmed/25124718 http://dx.doi.org/10.1186/1475-2875-13-315 Text en © Talman et al.; licensee BioMed Central Ltd. 2014 This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Talman, Arthur M
Prieto, Judith H
Marques, Sara
Ubaida-Mohien, Ceereena
Lawniczak, Mara
Wass, Mark N
Xu, Tao
Frank, Roland
Ecker, Andrea
Stanway, Rebecca S
Krishna, Sanjeev
Sternberg, Michael JE
Christophides, Georges K
Graham, David R
Dinglasan, Rhoel R
Yates, John R
Sinden, Robert E
Proteomic analysis of the Plasmodium male gamete reveals the key role for glycolysis in flagellar motility
title Proteomic analysis of the Plasmodium male gamete reveals the key role for glycolysis in flagellar motility
title_full Proteomic analysis of the Plasmodium male gamete reveals the key role for glycolysis in flagellar motility
title_fullStr Proteomic analysis of the Plasmodium male gamete reveals the key role for glycolysis in flagellar motility
title_full_unstemmed Proteomic analysis of the Plasmodium male gamete reveals the key role for glycolysis in flagellar motility
title_short Proteomic analysis of the Plasmodium male gamete reveals the key role for glycolysis in flagellar motility
title_sort proteomic analysis of the plasmodium male gamete reveals the key role for glycolysis in flagellar motility
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4150949/
https://www.ncbi.nlm.nih.gov/pubmed/25124718
http://dx.doi.org/10.1186/1475-2875-13-315
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