Genome-wide RIP-Chip analysis of translational repressor-bound mRNAs in the Plasmodium gametocyte

Handle URI:
http://hdl.handle.net/10754/337000
Title:
Genome-wide RIP-Chip analysis of translational repressor-bound mRNAs in the Plasmodium gametocyte
Authors:
Guerreiro, Ana; Deligianni, Elena; Santos, Jorge M; Silva, Patricia AGC; Louis, Christos; Pain, Arnab ( 0000-0002-1755-2819 ) ; Janse, Chris J; Franke-Fayard, Blandine; Carret, Celine K; Siden-Kiamos, Inga; Mair, Gunnar R
Abstract:
Background Following fertilization, the early proteomes of metazoans are defined by the translation of stored but repressed transcripts; further embryonic development relies on de novo transcription of the zygotic genome. During sexual development of Plasmodium berghei, a rodent model for human malaria species including P. falciparum, the stability of repressed mRNAs requires the translational repressors DOZI and CITH. When these repressors are absent, Plasmodium zygote development and transmission to the mosquito vector is halted, as hundreds of transcripts become destabilized. However, which mRNAs are direct targets of these RNA binding proteins, and thus subject to translational repression, is unknown. Results We identify the maternal mRNA contribution to post-fertilization development of P. berghei using RNA immunoprecipitation and microarray analysis. We find that 731 mRNAs, approximately 50% of the transcriptome, are associated with DOZI and CITH, allowing zygote development to proceed in the absence of RNA polymerase II transcription. Using GFP-tagging, we validate the repression phenotype of selected genes and identify mRNAs relying on the 5′ untranslated region for translational control. Gene deletion reveals a novel protein located in the ookinete crystalloid with an essential function for sporozoite development. Conclusions Our study details for the first time the P. berghei maternal repressome. This mRNA population provides the developing ookinete with coding potential for key molecules required for life-cycle progression, and that are likely to be critical for the transmission of the malaria parasite from the rodent and the human host to the mosquito vector.
KAUST Department:
Pathogen Genomics Laboratory; Computational Bioscience Research Center (CBRC)
Citation:
Genome-wide RIP-Chip analysis of translational repressor-bound mRNAs in the Plasmodium gametocyte 2014, 15 (11) Genome Biology
Publisher:
Springer Nature
Journal:
Genome Biology
Issue Date:
3-Nov-2014
DOI:
10.1186/s13059-014-0493-0
Type:
Article
ISSN:
1465-6906
Additional Links:
http://genomebiology.com/2014/15/11/493
Appears in Collections:
Articles; Computational Bioscience Research Center (CBRC)

Full metadata record

DC FieldValue Language
dc.contributor.authorGuerreiro, Anaen
dc.contributor.authorDeligianni, Elenaen
dc.contributor.authorSantos, Jorge Men
dc.contributor.authorSilva, Patricia AGCen
dc.contributor.authorLouis, Christosen
dc.contributor.authorPain, Arnaben
dc.contributor.authorJanse, Chris Jen
dc.contributor.authorFranke-Fayard, Blandineen
dc.contributor.authorCarret, Celine Ken
dc.contributor.authorSiden-Kiamos, Ingaen
dc.contributor.authorMair, Gunnar Ren
dc.date.accessioned2014-12-10T06:26:52Z-
dc.date.available2014-12-10T06:26:52Z-
dc.date.issued2014-11-03en
dc.identifier.citationGenome-wide RIP-Chip analysis of translational repressor-bound mRNAs in the Plasmodium gametocyte 2014, 15 (11) Genome Biologyen
dc.identifier.issn1465-6906en
dc.identifier.doi10.1186/s13059-014-0493-0en
dc.identifier.urihttp://hdl.handle.net/10754/337000en
dc.description.abstractBackground Following fertilization, the early proteomes of metazoans are defined by the translation of stored but repressed transcripts; further embryonic development relies on de novo transcription of the zygotic genome. During sexual development of Plasmodium berghei, a rodent model for human malaria species including P. falciparum, the stability of repressed mRNAs requires the translational repressors DOZI and CITH. When these repressors are absent, Plasmodium zygote development and transmission to the mosquito vector is halted, as hundreds of transcripts become destabilized. However, which mRNAs are direct targets of these RNA binding proteins, and thus subject to translational repression, is unknown. Results We identify the maternal mRNA contribution to post-fertilization development of P. berghei using RNA immunoprecipitation and microarray analysis. We find that 731 mRNAs, approximately 50% of the transcriptome, are associated with DOZI and CITH, allowing zygote development to proceed in the absence of RNA polymerase II transcription. Using GFP-tagging, we validate the repression phenotype of selected genes and identify mRNAs relying on the 5′ untranslated region for translational control. Gene deletion reveals a novel protein located in the ookinete crystalloid with an essential function for sporozoite development. Conclusions Our study details for the first time the P. berghei maternal repressome. This mRNA population provides the developing ookinete with coding potential for key molecules required for life-cycle progression, and that are likely to be critical for the transmission of the malaria parasite from the rodent and the human host to the mosquito vector.en
dc.language.isoenen
dc.publisherSpringer Natureen
dc.relation.urlhttp://genomebiology.com/2014/15/11/493en
dc.rightsThis 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.en
dc.titleGenome-wide RIP-Chip analysis of translational repressor-bound mRNAs in the Plasmodium gametocyteen
dc.typeArticleen
dc.contributor.departmentPathogen Genomics Laboratoryen
dc.contributor.departmentComputational Bioscience Research Center (CBRC)en
dc.identifier.journalGenome Biologyen
dc.eprint.versionPublisher's Version/PDFen
dc.contributor.institutionInstituto de Medicina Molecular, Faculdade de Medicina da Universidade de Lisboa, Av. Prof. Egas Moniz, Lisbon, 1649-028, Portugalen
dc.contributor.institutionInstitute of Molecular Biology and Biotechnology (IMBB), Foundation of Research and Technology (FORTH), N. Plastira 100, Heraklio 71110, Crete P.C., Greeceen
dc.contributor.institutionDepartment of Parasitology, Leiden University Medical Centre, Leiden, The Netherlandsen
dc.contributor.institutionParasitology, Department of Infectious Diseases, University of Heidelberg Medical School, Im Neuenheimer Feld 324, Heidelberg, 69120, Germanyen
dc.contributor.affiliationKing Abdullah University of Science and Technology (KAUST)en
kaust.authorPain, Arnaben
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