Nuclear, Cytosolic, and Surface-Localized Poly(A)-Binding Proteins of <named-content content-type="genus-species">Plasmodium yoelii</named-content>

ABSTRACT Malaria is a devastating illness that causes approximately 500,000 deaths annually. The malaria-causing parasite (Plasmodium genus) uses the process of translational repression to regulate its growth, development, and transmission. As poly(A)-binding proteins (PABP) have been identified as...

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Autores principales:	Allen M. Minns, Kevin J. Hart, Suriyasri Subramanian, Susan Hafenstein, Scott E. Lindner
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	PABP Plasmodium RNA metabolism electron microscopy poly(A)-binding protein surface proteins Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/07d6645df6f944e78e80f1221d522353
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spelling	oai:doaj.org-article:07d6645df6f944e78e80f1221d5223532021-11-15T15:22:01ZNuclear, Cytosolic, and Surface-Localized Poly(A)-Binding Proteins of <named-content content-type="genus-species">Plasmodium yoelii</named-content>10.1128/mSphere.00435-172379-5042https://doaj.org/article/07d6645df6f944e78e80f1221d5223532018-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00435-17https://doaj.org/toc/2379-5042ABSTRACT Malaria is a devastating illness that causes approximately 500,000 deaths annually. The malaria-causing parasite (Plasmodium genus) uses the process of translational repression to regulate its growth, development, and transmission. As poly(A)-binding proteins (PABP) have been identified as critical components of RNA metabolism and translational repression in model eukaryotes and in Plasmodium, we have identified and investigated two PABPs in Plasmodium yoelii, PyPABP1 and PyPABP2. In contrast to most single-celled eukaryotes, Plasmodium closely resembles metazoans and encodes both a nuclear PABP and a cytosolic PABP; here, we provide multiple lines of evidence in support of this observation. The conserved domain architectures of PyPABP1 and PyPABP2 resemble those of yeast and metazoans, while multiple independent binding assays demonstrated their ability to bind very strongly and specifically to poly(A) sequences. Interestingly, we also observed that purified PyPABP1 forms homopolymeric chains despite exhaustive RNase treatment in vitro. Finally, we show by indirect immunofluorescence assays (IFAs) that PyPABP1 and PyPABP2 are cytoplasm- and nucleus-associated PABPs during the blood stages of the life cycle. Surprisingly, however, PyPABP1 was instead observed to also be localized on the surface of transmitted salivary gland sporozoites and to be deposited in trails when parasites glide on a substrate. This is the third RNA-binding protein verified to be found on the sporozoite surface, and the data may point to an unappreciated RNA-centered interface between the host and parasite. IMPORTANCE Malaria remains one of the great global health problems. The parasite that causes malaria (Plasmodium genus) relies upon exquisite control of its transmission between vertebrate hosts and mosquitoes. One crucial way that it does so is by proactively producing mRNAs needed to establish the new infection but by silencing and storing them until they are needed. One key protein in this process of translational repression in model eukaryotes is poly(A)-binding protein (PABP). Here we have shown that Plasmodium yoelii utilizes both a nuclear PABP and a cytosolic PABP, both of which bind specifically to polyadenylated RNA sequences. Moreover, we find that the cytosolic PABP forms chains in vitro, consistent with its appreciated role in coating the poly(A) tails of mRNA. Finally, we have also verified that, surprisingly, the cytosolic PABP is found on the surface of Plasmodium sporozoites. Taking the data together, we propose that Plasmodium utilizes a more metazoan-like strategy for RNA metabolism using specialized PABPs.Allen M. MinnsKevin J. HartSuriyasri SubramanianSusan HafensteinScott E. LindnerAmerican Society for MicrobiologyarticlePABPPlasmodiumRNA metabolismelectron microscopypoly(A)-binding proteinsurface proteinsMicrobiologyQR1-502ENmSphere, Vol 3, Iss 1 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	PABP Plasmodium RNA metabolism electron microscopy poly(A)-binding protein surface proteins Microbiology QR1-502
spellingShingle	PABP Plasmodium RNA metabolism electron microscopy poly(A)-binding protein surface proteins Microbiology QR1-502 Allen M. Minns Kevin J. Hart Suriyasri Subramanian Susan Hafenstein Scott E. Lindner Nuclear, Cytosolic, and Surface-Localized Poly(A)-Binding Proteins of <named-content content-type="genus-species">Plasmodium yoelii</named-content>
description	ABSTRACT Malaria is a devastating illness that causes approximately 500,000 deaths annually. The malaria-causing parasite (Plasmodium genus) uses the process of translational repression to regulate its growth, development, and transmission. As poly(A)-binding proteins (PABP) have been identified as critical components of RNA metabolism and translational repression in model eukaryotes and in Plasmodium, we have identified and investigated two PABPs in Plasmodium yoelii, PyPABP1 and PyPABP2. In contrast to most single-celled eukaryotes, Plasmodium closely resembles metazoans and encodes both a nuclear PABP and a cytosolic PABP; here, we provide multiple lines of evidence in support of this observation. The conserved domain architectures of PyPABP1 and PyPABP2 resemble those of yeast and metazoans, while multiple independent binding assays demonstrated their ability to bind very strongly and specifically to poly(A) sequences. Interestingly, we also observed that purified PyPABP1 forms homopolymeric chains despite exhaustive RNase treatment in vitro. Finally, we show by indirect immunofluorescence assays (IFAs) that PyPABP1 and PyPABP2 are cytoplasm- and nucleus-associated PABPs during the blood stages of the life cycle. Surprisingly, however, PyPABP1 was instead observed to also be localized on the surface of transmitted salivary gland sporozoites and to be deposited in trails when parasites glide on a substrate. This is the third RNA-binding protein verified to be found on the sporozoite surface, and the data may point to an unappreciated RNA-centered interface between the host and parasite. IMPORTANCE Malaria remains one of the great global health problems. The parasite that causes malaria (Plasmodium genus) relies upon exquisite control of its transmission between vertebrate hosts and mosquitoes. One crucial way that it does so is by proactively producing mRNAs needed to establish the new infection but by silencing and storing them until they are needed. One key protein in this process of translational repression in model eukaryotes is poly(A)-binding protein (PABP). Here we have shown that Plasmodium yoelii utilizes both a nuclear PABP and a cytosolic PABP, both of which bind specifically to polyadenylated RNA sequences. Moreover, we find that the cytosolic PABP forms chains in vitro, consistent with its appreciated role in coating the poly(A) tails of mRNA. Finally, we have also verified that, surprisingly, the cytosolic PABP is found on the surface of Plasmodium sporozoites. Taking the data together, we propose that Plasmodium utilizes a more metazoan-like strategy for RNA metabolism using specialized PABPs.
format	article
author	Allen M. Minns Kevin J. Hart Suriyasri Subramanian Susan Hafenstein Scott E. Lindner
author_facet	Allen M. Minns Kevin J. Hart Suriyasri Subramanian Susan Hafenstein Scott E. Lindner
author_sort	Allen M. Minns
title	Nuclear, Cytosolic, and Surface-Localized Poly(A)-Binding Proteins of <named-content content-type="genus-species">Plasmodium yoelii</named-content>
title_short	Nuclear, Cytosolic, and Surface-Localized Poly(A)-Binding Proteins of <named-content content-type="genus-species">Plasmodium yoelii</named-content>
title_full	Nuclear, Cytosolic, and Surface-Localized Poly(A)-Binding Proteins of <named-content content-type="genus-species">Plasmodium yoelii</named-content>
title_fullStr	Nuclear, Cytosolic, and Surface-Localized Poly(A)-Binding Proteins of <named-content content-type="genus-species">Plasmodium yoelii</named-content>
title_full_unstemmed	Nuclear, Cytosolic, and Surface-Localized Poly(A)-Binding Proteins of <named-content content-type="genus-species">Plasmodium yoelii</named-content>
title_sort	nuclear, cytosolic, and surface-localized poly(a)-binding proteins of <named-content content-type="genus-species">plasmodium yoelii</named-content>
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/07d6645df6f944e78e80f1221d522353
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Nuclear, Cytosolic, and Surface-Localized Poly(A)-Binding Proteins of <named-content content-type="genus-species">Plasmodium yoelii</named-content>

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