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Dynamic protein modification of the malaria parasite Plasmodium falciparum and the infected erythrocytes

ABSTRACT: Plasmodium falciparum, a lethal protozoan, undergoes a complex extra- and intraerythrocytic development cycle that requires intricate and flexible regulatory mechanisms in order to facilitate reproduction and maintain the parasite’s resistance to environmental stress. Protein post-translational modifications (PTMs) are essential processes following protein biogenesis that allow proteins to fulfill their diverse biological functions. Here, we present comprehensive PTMomic profiling of both P. falciparum and its erythrocytic host cells during the 48 hours after infection. Fine mappings of each protein in both P. falciparum and the infected red blood cells (pRBCs) were accomplished. More than two-thirds of the parasite and its host cell proteins underwent extensive and dynamic modification throughout the erythrocytic developmental stage of the malarial parasite. Apart from the finding that PTMs actively regulated P. falciparum gene activation and silencing, the key molecules involved in the host-parasite interaction and pathogenesis were essentially modified. The establishment of an atlas of PTMomes of P. falciparum and its host erythrocytes will promote a deeper understanding of the parasite biology and will provide a basis for the search for novel antimalarials.

INSTRUMENT(S): Q Exactive Plus

ORGANISM(S): Plasmodium Falciparum Homo Sapiens (human)

SUBMITTER: Jianhua Wang

LAB HEAD: Qijun Chen

PROVIDER: PXD017503 | Pride | 2020-11-09

REPOSITORIES: Pride

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Project description:The human malaria parasite Plasmodium falciparum has a complex and multi-stage life cycle that requires extensive immune escape, invasion of human liver and blood cells, and transmission through the female Anopholes mosquito. To date, the regulatory elements orchestrating these critical parasite processes remain largely unknown. However, there is mounting evidence across a broad range of species that intergenic long non-coding RNA (lncRNA) and antisense RNA can regulate chromatin state and gene expression. To pursue such functional roles for lncRNAs in P. falciparum, we performed deep, strand-specific RNA sequencing of fifteen non-polyA-selected blood stage samples, and assembled and characterized the properties of 660 intergenic lncRNAs, 474 antisense RNAs, and 1381 circular RNAs (circRNAs). We further validated the non-canonical splice junctions of seven P. falciparum circRNAs, an emerging class of non-coding RNA with regulatory potential and unexplored functional significance in P. falciparum. Our comprehensive analysis of P. falciparum lncRNAs indicates a functional role for these transcripts; P. falciparum intergenic lncRNAs and antisense RNAs are developmentally regulated in a similar periodic fashion to annotated transcripts, and sense-antisense pair expression is significantly anti-correlated. Notable outliers include intergenic lncRNAs that strongly peak in expression during parasite invasion, such as the telomere-associated lncRNA-TARE family, antisense transcripts that drop in expression during parasite invasion, and a highly correlated, multi-exonic, antisense counterpart to P. falciparum Gametocyte Developmental Protein 1 (PfGDV1). Taken together, our results present over two thousand P. falciparum intergenic lncRNA, antisense, and circRNA candidates and highlight promising P. falciparum lncRNAs for future investigation. We harvested fifteen blood stage samples from two biological replicate time-courses. The first time-course comprised of eleven samples that finely map temporal changes during P. falciparum blood stage development. We harvested samples over 56 hours, at roughly 4-hour time intervals, from a tightly synchronized P. falciparum 3D7 parasite population. As the asexual blood stage is an approximately 48-hour cycle, this time-course allowed us to profile gene expression during RBC rupture and parasite invasion. The second time-course comprised of four samples harvested in synchronous P. falciparum 3D7 parasites approximately four hours before and after the ring to trophozoite and trophozoite to schizont morphological stage transitions, which occur during the blood stage at 24 hours post invasion (hpi) and 36 hpi, respectively.

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Dynamic protein modification of the malaria parasite Plasmodium falciparum and the infected erythrocytes

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