Disruption of the RNA exosome reveals the hidden face of the malaria parasite transcriptome

References

• World malaria report. Geneva: World Health Organization; November 2017. ISBN: 978 92 4 156552 3. Available from: http://www.who.int/malaria/publications/world-malaria-report-2017/report/en/.2017
   Google Scholar
• Duraisingh MT, Horn D. Epigenetic regulation of virulence gene expression in parasitic protozoa. Cell Host Microbe. 2016;19:629–640.
   PubMed Web of Science ®Google Scholar
• Rai R, Zhu L, Chen H, et al. Genome-wide analysis in Plasmodium falciparum reveals early and late phases of RNA polymerase II occupancy during the infectious cycle. BMC Genomics. 2014;15:959.
   PubMed Web of Science ®Google Scholar
• Vembar SS, Droll D, Scherf A. Translational regulation in blood stages of the malaria parasite Plasmodium spp.: systems-wide studies pave the way. Wiley Interdiscip Rev RNA. 2016;7:772–792.
   PubMed Web of Science ®Google Scholar
• Mair GR, Braks JA, Garver LS, et al. Regulation of sexual development of Plasmodium by translational repression. Science. 2016;313:667–669.
   Google Scholar
• Zhang Q, Siegel TN, Martins RM, et al. Exonuclease-mediated degradation of nascent RNA silences genes linked to severe malaria. Nature. 2014;513:431–435.
   PubMed Web of Science ®Google Scholar
• Siegel TN, Hon CC, Zhang Q, et al. Strand-specific RNA-Seq reveals widespread and developmentally regulated transcription of natural antisense transcripts in Plasmodium falciparum. BMC Genomics. 2014;15:150.
   PubMed Web of Science ®Google Scholar
• Filarsky M, Fraschka SA, Niederwieser I, et al. GDV1 induces sexual commitment of malaria parasites by antagonizing HP1-dependent gene silencing. Science. 2018;359:1259–1263.
   PubMed Web of Science ®Google Scholar
• Houseley J, Tollervey D. The many pathways of RNA degradation. Cell. 2009;136:763–776.
   PubMed Web of Science ®Google Scholar
• Januszyk K, Lima CD. The eukaryotic RNA exosome. Curr Opin Struct Biol. 2014;24:132–140.
   PubMed Web of Science ®Google Scholar
• Kilchert C, Wittmann S, Vasiljeva L. The regulation and functions of the nuclear RNA exosome complex. Nat Rev Mol Cell Biol. 2016;17:227–239.
   PubMed Web of Science ®Google Scholar
• Vanacova S, Stefl R. The exosome and RNA quality control in the nucleus. EMBO Rep. 2007;8:651–657.
   PubMed Web of Science ®Google Scholar
• Liu Q, Greimann JC, Lima CD. Reconstitution, activities, and structure of the eukaryotic RNA exosome. Cell. 2006;127:1223–1237.
   PubMed Web of Science ®Google Scholar
• Meola N, Domanski M, Karadoulama E, et al. Identification of a nuclear exosome decay pathway for processed transcripts. Mol Cell. 2016;64:520–533.
   PubMed Web of Science ®Google Scholar
• Halbach F, Reichelt P, Rode M, et al. The yeast ski complex: crystal structure and RNA channeling to the exosome complex. Cell. 2013;154:814–826.
   PubMed Web of Science ®Google Scholar
• Schneider C, Tollervey D. Threading the barrel of the RNA exosome. Trends Biochem Sci. 2013;38:485–493.
   PubMed Web of Science ®Google Scholar
• Lykke-Andersen S, Tomecki R, Jensen TH, et al. The eukaryotic RNA exosome: same scaffold but variable catalytic subunits. RNA Biol. 2011;8:61–66.
   PubMed Web of Science ®Google Scholar
• Estévez AM, Lehner B, Sanderson CM, et al. The roles of intersubunit interactions in exosome stability. J Biol Chem. 2003;278:34943–34951.
   PubMed Web of Science ®Google Scholar
• Szczepińska T, Kalisiak K, Tomecki R, et al. DIS3 shapes the RNA polymerase II transcriptome in humans by degrading a variety of unwanted transcripts. Genome Res. 2015;25:1622–1633.
   PubMed Web of Science ®Google Scholar
• Jensen TH. RNA exosome. New York (NY): Landes Bioscience and Springer Science+Business Media, LLC; 2010.
   Google Scholar
• Williams CW, Elmendorf HG. Identification and analysis of the RNA degrading complexes and machinery of Giardia lamblia using an in silico approach. BMC Genomics. 2011;12:586.
   PubMed Web of Science ®Google Scholar
• Zuo Y, Vincent HA, Zhang J, et al. Structural basis for processivity and single-strand specificity of RNase II. Mol Cell. 2006;24:149–156.
   PubMed Web of Science ®Google Scholar
• Jones ML, Das S, Belda H, et al. A versatile strategy for rapid conditional genome engineering using loxP sites in a small synthetic intron in Plasmodium falciparum. Sci Rep. 2016;6:21800.
   PubMed Web of Science ®Google Scholar
• Knuepfer E, Napiorkowska M, van Ooij C, et al. Generating conditional gene knockouts in Plasmodium - a toolkit to produce stable DiCre recombinase-expressing parasite lines using CRISPR/Cas9. Sci Rep. 2017;7:3881.
   PubMed Web of Science ®Google Scholar
• Gardner MJ, Hall N, Fung E, et al. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature. 2002;419:498–511.
   PubMed Web of Science ®Google Scholar
• Calderwood MS, Gannoun-Zaki L, Wellems TE, et al. Plasmodium falciparum var genes are regulated by two regions with separate promoters, one upstream of the coding region and a second within the intron. J Biol Chem. 2003;278:34125–34132.
   PubMed Web of Science ®Google Scholar
• Amit-Avraham I, Pozner G, Eshar S, et al. Antisense long noncoding RNAs regulate var gene activation in the malaria parasite Plasmodium falciparum. Proc Natl Acad Sci USA. 2015;112:E982–91.
   PubMed Web of Science ®Google Scholar
• Jiang L, Mu J, Zhang Q, et al. PfSETvs methylation of histone H3K36 represses virulence genes in Plasmodium falciparum. Nature. 2013;499:223–227.
   PubMed Web of Science ®Google Scholar
• Painter HJ, Chung NC, Sebastian A, et al. Genome-wide real-time in vivo transcriptional dynamics during Plasmodium falciparum blood-stage development. Nat Commun. 2018;9:2656.
   PubMed Web of Science ®Google Scholar
• Shock JL, Fischer KF, DeRisi JL. Whole-genome analysis of mRNA decay in Plasmodium falciparum reveals a global lengthening of mRNA half-life during the intra-erythrocytic development cycle. Genome Biol. 2007;8:R134.
   PubMed Web of Science ®Google Scholar
• Zhang L, Wan Y, Huang G, et al. The exosome controls alternative splicing by mediating the gene expression and assembly of the spliceosome complex. Sci Rep. 2015;5:13403.
   PubMed Web of Science ®Google Scholar
• Ghorbal M, Gorman M, Macpherson CR, et al. Genome editing in the human malaria parasite Plasmodium falciparum using the CRISPR-Cas9 system. Nat Biotechnol. 2014;32:819–821.
   PubMed Web of Science ®Google Scholar
• Zhang Q, Huang Y, Zhang Y, et al. A critical role of perinuclear filamentous actin in spatial repositioning and mutually exclusive expression of virulence genes in malaria parasites. Cell Host Microbe. 2011;10:451–463.
   PubMed Web of Science ®Google Scholar
• Collins CR, Das S, Wong EH, et al. Robust inducible Cre recombinase activity in the human malaria parasite Plasmodium falciparum enables efficient gene deletion within a single asexual erythrocytic growth cycle. Mol Microbiol. 2013;88:687–701.
   PubMed Web of Science ®Google Scholar
• Cox J, Hein MY, Luber CA, et al. Accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction, termed MaxLFQ. Mol Cell Proteomics. 2014;13:2513–2526.
   PubMed Web of Science ®Google Scholar
• Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25:1754–1760.
   PubMed Web of Science ®Google Scholar
• Li H, Handsaker B, Wysoker A, et al. The sequence alignment/map format and SAMtools. Bioinformatics. 2009;25:2078–2079.
   PubMed Web of Science ®Google Scholar
• Anders S, Pyl PT, Huber W. HTSeq–a Python framework to work with high-throughput sequencing data. Bioinformatics. 2015;31:166–169.
   PubMed Web of Science ®Google Scholar
• Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26:139–140.
   PubMed Web of Science ®Google Scholar
• Ramírez F, Ryan DP, Grüning B, et al. deepTools2: a next generation web server for deep-sequencing data analysis. Nucleic Acids Res. 2016;44:W160–65.
   PubMed Web of Science ®Google Scholar
• Thorvaldsdóttir H, Robinson JT, Mesirov JP. Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform. 2012;14:178–192.
   PubMed Web of Science ®Google Scholar