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PfCAP-H is essential for assembly of condensin I complex and karyokinesis during asexual proliferation of Plasmodium falciparum.

ABSTRACT: Condensin I is a pentameric complex that regulates the mitotic chromosome assembly in eukaryotes. The kleisin subunit CAP-H of the condensin I complex acts as a linchpin to maintain the structural integrity and loading of this complex on mitotic chromosomes. This complex is present in all eukaryotes and has recently been identified in Plasmodium spp. However, how this complex is assembled and whether the kleisin subunit is critical for this complex in these parasites is yet to be explored. To examine the role of PfCAP-H during cell division within erythrocytes, we generated an inducible PfCAP-H knockout parasite. We find that PfCAP-H is dynamically expressed during mitosis with the peak expression at the metaphase plate. PfCAP-H interacts with PfCAP-G and is a non-SMC member of the condensin I complex. Notably, the absence of PfCAP-H does not alter the expression of PfCAP-G but affects its localization at the mitotic chromosomes. While mitotic spindle assembly is intact in PfCAP-H deficient parasites, duplicated centrosomes remain clustered over the mass of unsegmented nuclei with failed karyokinesis. This failure leads to the formation of an abnormal nuclear mass, while cytokinesis occurs normally. Altogether, our data suggest that PfCAP-H plays a crucial role in maintaining the structural integrity of the condensin I complex on the mitotic chromosomes and is essential for the asexual development of malarial parasites.

SUBMITTER: Gurung P

PROVIDER: S-EPMC10925219 | biostudies-literature | 2024 Feb

REPOSITORIES: biostudies-literature

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PfCAP-H is essential for assembly of condensin I complex and karyokinesis during asexual proliferation of <i>Plasmodium falciparum</i>.

Gurung Pratima P McGee James P JP Dvorin Jeffrey D JD

bioRxiv : the preprint server for biology 20240229

Condensin I is a pentameric complex that regulates the mitotic chromosome assembly in eukaryotes. The kleisin subunit CAP-H of the condensin I complex acts as a linchpin to maintain the structural integrity and loading of this complex on mitotic chromosomes. This complex is present in all eukaryotes and has recently been identified in <i>Plasmodium spp</i>. However, how this complex is assembled and whether the kleisin subunit is critical for this complex in these parasites is yet to be explored ...[more]

PMID: 38464281

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Project description:The cytoskeleton of Plasmodium parasites is essential for replication, motility, and infectivity. Plasmodium falciparum leverages a family of cytoskeletal proteins known as alveolins to meet these diverse needs. The functional role of individual alveolins in Plasmodium blood stages, however, remains unexplored. Here, we demonstrate that the alveolin PfIMC1g (PF3D7_0525800) is essential for P. falciparum asexual replication. Unlike alveolins studied in mosquito stages, PfIMC1g does not play an important role in determining cell shape. PfIMC1g-deficient parasites exhibit only minor defects during segmentation, with most merozoites being indistinguishable from wild type by super-resolution fluorescence microscopy, ultrastructure expansion microscopy, and electron microscopy. In the current study, we demonstrate that the absence of PfIMC1g leads to parasite death shortly after merozoite internalization into red blood cells (RBCs). PfIMC1g-deficient parasites egress and enter new RBCs but fail to develop into rings and die. We hypothesize that the primary role of PfIMC1g is to maintain structural integrity, protecting parasites from incurring damage during the process of internalization. Along with the dispensability of PfIMC1g for merozoite cell shape, we report new findings about the architecture of Plasmodium alveolins including the localization of PfIMC1e and 1f to the basal complex. IMPORTANCE Infection by the Plasmodium falciparum parasite is responsible for the most severe form of human malaria. The asexual blood stage of the parasite, which occurs inside human red blood cells, is responsible for the symptoms of malaria and is the target of most antimalarial drugs. Plasmodium spp. rely on their highly divergent cytoskeletal structures to scaffold their cell division, sustain the mechanical stress of invasion, and survive in both the human bloodstream and the mosquito. We investigate the function of a class of divergent intermediate filament-like proteins called alveolins in the clinically important blood stage. The functional role of individual alveolins in Plasmodium remains poorly understood due to pleiotropic effects of gene knockouts and redundancy among alveolins. We evaluate the localization and essentiality of the four asexual-stage alveolins and find that PfIMC1g and PfIMC1c are essential. Furthermore, we demonstrate that PfIMC1g is critical for survival of the parasite post-invasion.

Dataset Information

PfCAP-H is essential for assembly of condensin I complex and karyokinesis during asexual proliferation of Plasmodium falciparum.

Publications

PfCAP-H is essential for assembly of condensin I complex and karyokinesis during asexual proliferation of <i>Plasmodium falciparum</i>.

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