Dataset Information

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

ABSTRACT: 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 pathways of energy metabolism that power motility, a feature that facilitates gamete encounter and fertilization, is unknown. To gain more insight into male gamete, we performed the first proteomic analysis of purified Plasmodium berghei microgametes. We recovered 615 proteins, which include all male gamete proteins described thus far. Amongst the most abundant proteins were the 11 enzymes of the glycolytic pathway. We localized the hexose transporter to the gamete plasma membrane and show that microgamete motility can be suppressed effectively by inhibitors of this transporter, and of the glycolytic pathway. Taken together, these results suggest that glycolysis is the exclusive source of energy for microgamete motility. Considering that this proteome provides a unique platform for the understanding of the original features of the male gamete, we discuss not only the mitochondria-independent energy metabolism but also flagellar structure and intra-flagellar transport-independent assembly, another divergent feature of these cells.

INSTRUMENT(S): LTQ Orbitrap

ORGANISM(S): Plasmodium Sp. Pbt9

TISSUE(S): Blood Cell, Blood Plasma

DISEASE(S): Malaria

SUBMITTER: Ceereena Ubaida Mohien

LAB HEAD: Arthur M. Talman

PROVIDER: PXD001163 | Pride | 2014-08-18

REPOSITORIES: pride

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Dataset's files

Source:

			Action	DRS
	GametesRep1.peparml.pep.xml	Pepxml
	GametesRep2.peparml.pep.xml	Pepxml
	GametesRep3.peparml.pep.xml	Pepxml
	Gametes_rep1_01.mzXML	Mzxml
	Gametes_rep1_02.mzXML	Mzxml

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Publications

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

Talman Arthur M AM Prieto Judith H JH Marques Sara S Ubaida-Mohien Ceereena C Lawniczak Mara M Wass Mark N MN Xu Tao T Frank Roland R Ecker Andrea A Stanway Rebecca S RS Krishna Sanjeev S Sternberg Michael J E MJ Christophides Georges K GK Graham David R DR Dinglasan Rhoel R RR Dinglasan Rhoel R RR Yates John R JR Sinden Robert E RE

Malaria journal 20140813

<h4>Background</h4>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.<h4>Methods</h4>Plasmodium berghei microgametes were purified and analysed by w ...[more]

PMID: 25124718

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Project description:The transmission of the malaria parasite between mosquitoes and mammals requires translational repression to ensure that only the proper proteins are expressed at the right time, while still allowing the parasite to prepare the mRNAs it will need for the next developmental stage. With relatively few known specific transcription factors (ApiAP2 family) that may specifically initiate gene transcription, Plasmodium parasites also regulate the stability and turnover of transcripts to provide more comprehensive gene regulation. The CAF1/CCR4/NOT complex has been shown in model organisms to be important for not only mRNA degradation, but also translational control through its deadenylases CAF1 and CCR4. However, few proteins that impose translational repression in Plasmodium sexual stages are known, and those that are characterized primarily affect female gametocytes. Therefore, we have characterized two deadenylases and have uncovered their roles in transmission. We have identified and characterized CCR4-1, which we show plays a role in activating male gametocytes, stabilizing transcripts in gametocytes, and regulating host-to-vector transmission. We find that when ccr4-1 is genetically deleted, there is a loss in the coordination of male gametocyte activation and a reduction in the ability of the parasite to productively infect the mosquito, which is independent of its effect upon male activation. Comparative RNA-seq shows that the deletion of ccr4-1 affects many transcripts that are translationally repressed in females, are related to male gamete function, and/or are important for early mosquito stage development. In contrast, we found that genetic deletion of the major deadenylase Caf1 is lethal. However, we observed that expression of only the N-terminal Caf1 domain is permissive, yet prevents proper complex assembly and phenocopies the ccr4-1 deletion. We therefore conclude that the general and transmission-specialized deadenylases of the CAF1/CCR4/NOT complex play critical and intertwined roles in parasite growth and transmission.