Genome-wide RNAi selection identifies a regulator of transmission stage-enriched gene families and cell-type differentiation in Trypanosoma brucei

Trypanosoma brucei, causing African sleeping-sickness, exploits quorum-sensing (QS) to generate the 'stumpy forms' necessary for the parasite's transmission to tsetse-flies. These quiescent cells are generated by differentiation in the bloodstream from proliferative slender forms. Usi...

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Published inPLoS pathogens Vol. 13; no. 3; p. e1006279
Main Authors Rico, Eva, Ivens, Alasdair, Glover, Lucy, Horn, David, Matthews, Keith R
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 23.03.2017
Public Library of Science (PLoS)
Subjects
Animals
Biology
Biology and life sciences
Cell cycle
Cell Differentiation
Cell Differentiation - genetics
Cell fate
Differentiation (biology)
Disease Models, Animal
Disease transmission
Enrichment
Evolution
Female
Flies
Flow Cytometry
Gene expression
Gene Expression Regulation
Gene Expression Regulation - genetics
Gene families
Genetic aspects
Genome-Wide Association Study
Genomes
Immunoblotting
Immunology
Infections
Life Sciences
Mammals
Medicine and Health Sciences
Messenger RNA
Mice
Midgut
Parasites
Proteins
Protozoa
Protozoan Proteins
Protozoan Proteins - biosynthesis
Protozoan Proteins - genetics
Repressors
RNA Interference
RNA-Binding Proteins
RNA-Binding Proteins - biosynthesis
RNA-Binding Proteins - genetics
RNA-mediated interference
Transcription
Transfection
Tropism
Trypanosoma brucei
Trypanosoma brucei brucei
Trypanosoma congolense
Trypanosoma vivax
Trypanosome
Trypanosomiasis, African
Trypanosomiasis, African - genetics
Trypanosomiasis, African - transmission
Scotland
Edinburgh Scotland
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Abstract Trypanosoma brucei, causing African sleeping-sickness, exploits quorum-sensing (QS) to generate the 'stumpy forms' necessary for the parasite's transmission to tsetse-flies. These quiescent cells are generated by differentiation in the bloodstream from proliferative slender forms. Using genome-wide RNAi selection we screened for repressors of transmission stage-enriched mRNAs in slender forms, using the stumpy-elevated ESAG9 transcript as a model. This identified REG9.1, whose RNAi-silencing alleviated ESAG9 repression in slender forms and tsetse-midgut procyclic forms. Interestingly, trypanosome surface protein Family 5 and Family 7 mRNAs were also elevated, which, like ESAG9, are T. brucei specific and stumpy-enriched. We suggest these contribute to the distinct transmission biology and vector tropism of T. brucei from other African trypanosome species. As well as surface family regulation, REG9.1-depletion generated QS-independent development to stumpy forms in vivo, whereas REG9.1 overexpression in bloodstream forms potentiated spontaneous differentiation to procyclic forms in the absence of an external signal. Combined, this identifies REG9.1 as a regulator of developmental cell fate, controlling the expression of Trypanosoma brucei-specific molecules elevated during transmission.
AbstractList Trypanosoma brucei, causing African sleeping-sickness, exploits quorum-sensing (QS) to generate the 'stumpy forms' necessary for the parasite's transmission to tsetse-flies. These quiescent cells are generated by differentiation in the bloodstream from proliferative slender forms. Using genome-wide RNAi selection we screened for repressors of transmission stage-enriched mRNAs in slender forms, using the stumpy-elevated ESAG9 transcript as a model. This identified REG9.1, whose RNAi-silencing alleviated ESAG9 repression in slender forms and tsetse-midgut procyclic forms. Interestingly, trypanosome surface protein Family 5 and Family 7 mRNAs were also elevated, which, like ESAG9, are T. brucei specific and stumpy-enriched. We suggest these contribute to the distinct transmission biology and vector tropism of T. brucei from other African trypanosome species. As well as surface family regulation, REG9.1-depletion generated QS-independent development to stumpy forms in vivo, whereas REG9.1 overexpression in bloodstream forms potentiated spontaneous differentiation to procyclic forms in the absence of an external signal. Combined, this identifies REG9.1 as a regulator of developmental cell fate, controlling the expression of Trypanosoma brucei-specific molecules elevated during transmission.
Trypanosoma brucei , causing African sleeping-sickness, exploits quorum-sensing (QS) to generate the ‘stumpy forms’ necessary for the parasite’s transmission to tsetse-flies. These quiescent cells are generated by differentiation in the bloodstream from proliferative slender forms. Using genome-wide RNAi selection we screened for repressors of transmission stage-enriched mRNAs in slender forms, using the stumpy-elevated ESAG9 transcript as a model. This identified REG9 . 1 , whose RNAi-silencing alleviated ESAG9 repression in slender forms and tsetse-midgut procyclic forms. Interestingly, trypanosome surface protein Family 5 and Family 7 mRNAs were also elevated, which, like ESAG9 , are T . brucei specific and stumpy-enriched. We suggest these contribute to the distinct transmission biology and vector tropism of T . brucei from other African trypanosome species. As well as surface family regulation, REG9 . 1 -depletion generated QS-independent development to stumpy forms in vivo , whereas REG9 . 1 overexpression in bloodstream forms potentiated spontaneous differentiation to procyclic forms in the absence of an external signal. Combined, this identifies REG9 . 1 as a regulator of developmental cell fate, controlling the expression of Trypanosoma brucei -specific molecules elevated during transmission. African trypanosomes cause important disease of humans and livestock in sub Saharan Africa and are transmitted by tsetse flies. In preparation for transmission, Trypanosoma brucei uses quorum sensing to generate ‘stumpy forms’ that are arrested and express a distinct subset of genes to the ‘slender forms’ that proliferate to establish the parasitaemia in the bloodstream. This necessitates that stumpy-enriched transcripts are repressed in slender forms, although the molecular control of this is unknown. Here, we have developed a genome-wide selectional strategy to isolate repressors of stumpy-enriched genes, and successfully identified a novel regulatory molecule, termed REG9.1. Silencing of REG9.1 alleviates the repression of the previously characterised stumpy-enriched ESAG9 gene family, and also two novel predicted surface protein families that are specific to Trypansoma brucei but absent from other African trypanosome species. REG9.1 silencing also drives density-independent differentiation to stumpy forms, whereas its ectopic expression in bloodstream forms potentiates differentiation to tsetse midgut procyclic forms in the absence of an external signal. REG9.1 is therefore identified as a novel developmental regulator whose action may contribute to the species-specific transmission biology of Trypanosoma brucei , which differs from that of either Trypanosoma congolense or Trypanosoma vivax .
Audience Academic
Author Glover, Lucy
Horn, David
Rico, Eva
Matthews, Keith R
Ivens, Alasdair
AuthorAffiliation Yale School of Public Health, UNITED STATES
1 Centre for Immunity, Infection and Evolution, Institute for Immunology and Infection Research, School of Biological Sciences, University of Edinburgh, Edinburgh, Scotland, United Kingdom
2 The Wellcome Trust Centre for Anti-Infectives Research, School of Life Sciences, University of Dundee, Dundee, Scotland, United Kingdom
AuthorAffiliation_xml – name: Yale School of Public Health, UNITED STATES
– name: 1 Centre for Immunity, Infection and Evolution, Institute for Immunology and Infection Research, School of Biological Sciences, University of Edinburgh, Edinburgh, Scotland, United Kingdom
– name: 2 The Wellcome Trust Centre for Anti-Infectives Research, School of Life Sciences, University of Dundee, Dundee, Scotland, United Kingdom
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  givenname: Eva
  surname: Rico
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ContentType Journal Article
Copyright COPYRIGHT 2017 Public Library of Science
2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: . PLoS Pathog 13(3): e1006279. https://doi.org/10.1371/journal.ppat.1006279
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2017 Rico et al 2017 Rico et al
2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: . PLoS Pathog 13(3): e1006279. https://doi.org/10.1371/journal.ppat.1006279
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– notice: 2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: . PLoS Pathog 13(3): e1006279. https://doi.org/10.1371/journal.ppat.1006279
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– notice: 2017 Rico et al 2017 Rico et al
– notice: 2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: . PLoS Pathog 13(3): e1006279. https://doi.org/10.1371/journal.ppat.1006279
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PMCID: PMC5380359
Conceptualization: KRM ER DH AI LG.Data curation: AI.Formal analysis: AI ER KRM.Funding acquisition: KRM DH.Investigation: ER AI LG.Methodology: KRM ER DH AI LG.Project administration: KRM.Resources: KRM ER DH AI LG.Software: AI.Supervision: KRM DH.Validation: KRM.Visualization: KRM ER AI.Writing – original draft: KRM ER DH AI LG.Writing – review & editing: KRM ER DH AI LG.
Current address: Department of Parasites and Insect Vectors, Institut Pasteur, Paris, France
The authors have declared that no competing interests exist.
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SSID ssj0041316
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Snippet Trypanosoma brucei, causing African sleeping-sickness, exploits quorum-sensing (QS) to generate the 'stumpy forms' necessary for the parasite's transmission to...
Trypanosoma brucei, causing African sleeping-sickness, exploits quorum-sensing (QS) to generate the ‘stumpy forms’ necessary for the parasite’s transmission to...
Trypanosoma brucei , causing African sleeping-sickness, exploits quorum-sensing (QS) to generate the ‘stumpy forms’ necessary for the parasite’s transmission...
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StartPage e1006279
SubjectTerms Animals
Biology
Biology and life sciences
Cell cycle
Cell Differentiation
Cell Differentiation - genetics
Cell fate
Differentiation (biology)
Disease Models, Animal
Disease transmission
Enrichment
Evolution
Female
Flies
Flow Cytometry
Gene expression
Gene Expression Regulation
Gene Expression Regulation - genetics
Gene families
Genetic aspects
Genome-Wide Association Study
Genomes
Immunoblotting
Immunology
Infections
Life Sciences
Mammals
Medicine and Health Sciences
Messenger RNA
Mice
Midgut
Parasites
Proteins
Protozoa
Protozoan Proteins
Protozoan Proteins - biosynthesis
Protozoan Proteins - genetics
Repressors
RNA Interference
RNA-Binding Proteins
RNA-Binding Proteins - biosynthesis
RNA-Binding Proteins - genetics
RNA-mediated interference
Transcription
Transfection
Tropism
Trypanosoma brucei
Trypanosoma brucei brucei
Trypanosoma congolense
Trypanosoma vivax
Trypanosome
Trypanosomiasis, African
Trypanosomiasis, African - genetics
Trypanosomiasis, African - transmission
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Title Genome-wide RNAi selection identifies a regulator of transmission stage-enriched gene families and cell-type differentiation in Trypanosoma brucei
URI https://www.ncbi.nlm.nih.gov/pubmed/28334017
https://www.proquest.com/docview/1900162988
https://search.proquest.com/docview/1881263117
https://pasteur.hal.science/pasteur-03107156
https://pubmed.ncbi.nlm.nih.gov/PMC5380359
https://doaj.org/article/3bde0ca8595f4e2eb5d06968a93c27ad
http://dx.doi.org/10.1371/journal.ppat.1006279
Volume 13
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