Comparative ribosome profiling uncovers a dominant role for translational control in Toxoplasma gondii

Abstract Background The lytic cycle of the protozoan parasite Toxoplasma gondii, which involves a brief sojourn in the extracellular space, is characterized by defined transcriptional profiles. For an obligate intracellular parasite that is shielded from the cytosolic host immune factors by a parasi...

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Main Authors: Musa A. Hassan, Juan J. Vasquez, Chew Guo-Liang, Markus Meissner, T. Nicolai Siegel
Format: Article
Language:English
Published: BMC 2017-12-01
Series:BMC Genomics
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12864-017-4362-6
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spelling doaj-53802098d15f41d5820641442029b9482020-11-24T21:13:29ZengBMCBMC Genomics1471-21642017-12-0118111210.1186/s12864-017-4362-6Comparative ribosome profiling uncovers a dominant role for translational control in Toxoplasma gondiiMusa A. Hassan0Juan J. Vasquez1Chew Guo-Liang2Markus Meissner3T. Nicolai Siegel4Division of Infection and Immunity, The Roslin Institute, University of EdinburghResearch Centre for Infectious Diseases, University of WuerzburgComputational Biology Program, Basic Sciences and Public Health Sciences Division, Fred Hutchinson Cancer Research CentreWellcome Centre for Molecular Parasitology, University of GlasgowResearch Centre for Infectious Diseases, University of WuerzburgAbstract Background The lytic cycle of the protozoan parasite Toxoplasma gondii, which involves a brief sojourn in the extracellular space, is characterized by defined transcriptional profiles. For an obligate intracellular parasite that is shielded from the cytosolic host immune factors by a parasitophorous vacuole, the brief entry into the extracellular space is likely to exert enormous stress. Due to its role in cellular stress response, we hypothesize that translational control plays an important role in regulating gene expression in Toxoplasma during the lytic cycle. Unlike transcriptional profiles, insights into genome-wide translational profiles of Toxoplasma gondii are lacking. Methods We have performed genome-wide ribosome profiling, coupled with high throughput RNA sequencing, in intracellular and extracellular Toxoplasma gondii parasites to investigate translational control during the lytic cycle. Results Although differences in transcript abundance were mostly mirrored at the translational level, we observed significant differences in the abundance of ribosome footprints between the two parasite stages. Furthermore, our data suggest that mRNA translation in the parasite is potentially regulated by mRNA secondary structure and upstream open reading frames. Conclusion We show that most of the Toxoplasma genes that are dysregulated during the lytic cycle are translationally regulated.http://link.springer.com/article/10.1186/s12864-017-4362-6Ribosome profilingRNA-sequencingTranslation efficiencyToxoplasma gondiiApicomplexan
collection DOAJ
language English
format Article
sources DOAJ
author Musa A. Hassan
Juan J. Vasquez
Chew Guo-Liang
Markus Meissner
T. Nicolai Siegel
spellingShingle Musa A. Hassan
Juan J. Vasquez
Chew Guo-Liang
Markus Meissner
T. Nicolai Siegel
Comparative ribosome profiling uncovers a dominant role for translational control in Toxoplasma gondii
BMC Genomics
Ribosome profiling
RNA-sequencing
Translation efficiency
Toxoplasma gondii
Apicomplexan
author_facet Musa A. Hassan
Juan J. Vasquez
Chew Guo-Liang
Markus Meissner
T. Nicolai Siegel
author_sort Musa A. Hassan
title Comparative ribosome profiling uncovers a dominant role for translational control in Toxoplasma gondii
title_short Comparative ribosome profiling uncovers a dominant role for translational control in Toxoplasma gondii
title_full Comparative ribosome profiling uncovers a dominant role for translational control in Toxoplasma gondii
title_fullStr Comparative ribosome profiling uncovers a dominant role for translational control in Toxoplasma gondii
title_full_unstemmed Comparative ribosome profiling uncovers a dominant role for translational control in Toxoplasma gondii
title_sort comparative ribosome profiling uncovers a dominant role for translational control in toxoplasma gondii
publisher BMC
series BMC Genomics
issn 1471-2164
publishDate 2017-12-01
description Abstract Background The lytic cycle of the protozoan parasite Toxoplasma gondii, which involves a brief sojourn in the extracellular space, is characterized by defined transcriptional profiles. For an obligate intracellular parasite that is shielded from the cytosolic host immune factors by a parasitophorous vacuole, the brief entry into the extracellular space is likely to exert enormous stress. Due to its role in cellular stress response, we hypothesize that translational control plays an important role in regulating gene expression in Toxoplasma during the lytic cycle. Unlike transcriptional profiles, insights into genome-wide translational profiles of Toxoplasma gondii are lacking. Methods We have performed genome-wide ribosome profiling, coupled with high throughput RNA sequencing, in intracellular and extracellular Toxoplasma gondii parasites to investigate translational control during the lytic cycle. Results Although differences in transcript abundance were mostly mirrored at the translational level, we observed significant differences in the abundance of ribosome footprints between the two parasite stages. Furthermore, our data suggest that mRNA translation in the parasite is potentially regulated by mRNA secondary structure and upstream open reading frames. Conclusion We show that most of the Toxoplasma genes that are dysregulated during the lytic cycle are translationally regulated.
topic Ribosome profiling
RNA-sequencing
Translation efficiency
Toxoplasma gondii
Apicomplexan
url http://link.springer.com/article/10.1186/s12864-017-4362-6
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AT chewguoliang comparativeribosomeprofilinguncoversadominantrolefortranslationalcontrolintoxoplasmagondii
AT markusmeissner comparativeribosomeprofilinguncoversadominantrolefortranslationalcontrolintoxoplasmagondii
AT tnicolaisiegel comparativeribosomeprofilinguncoversadominantrolefortranslationalcontrolintoxoplasmagondii
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