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Multimodal analysis of Plasmodium knowlesi-infected erythrocytes reveals large invaginations, swelling of the host cell, and rheological defects.
- Source :
-
Cellular microbiology [Cell Microbiol] 2019 May; Vol. 21 (5), pp. e13005. Date of Electronic Publication: 2019 Feb 11. - Publication Year :
- 2019
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Abstract
- The simian parasite Plasmodium knowlesi causes severe and fatal malaria infections in humans, but the process of host cell remodelling that underpins the pathology of this zoonotic parasite is only poorly understood. We have used serial block-face scanning electron microscopy to explore the topography of P. knowlesi-infected red blood cells (RBCs) at different stages of asexual development. The parasite elaborates large flattened cisternae (Sinton Mulligan's clefts) and tubular vesicles in the host cell cytoplasm, as well as parasitophorous vacuole membrane bulges and blebs, and caveolar structures at the RBC membrane. Large invaginations of host RBC cytoplasm are formed early in development, both from classical cytostomal structures and from larger stabilised pores. Although degradation of haemoglobin is observed in multiple disconnected digestive vacuoles, the persistence of large invaginations during development suggests inefficient consumption of the host cell cytoplasm. The parasite eventually occupies ~40% of the host RBC volume, inducing a 20% increase in volume of the host RBC and an 11% decrease in the surface area to volume ratio, which collectively decreases the ability of the P. knowlesi-infected RBCs to enter small capillaries of a human erythrocyte microchannel analyser. Ektacytometry reveals a markedly decreased deformability, whereas correlative light microscopy/scanning electron microscopy and python-based skeleton analysis (Skan) reveal modifications to the surface of infected RBCs that underpin these physical changes. We show that P. knowlesi-infected RBCs are refractory to treatment with sorbitol lysis but are hypersensitive to hypotonic lysis. The observed physical changes in the host RBCs may underpin the pathology observed in patients infected with P. knowlesi.<br /> (© 2019 The Authors. Cellular Microbiology Published by John Wiley & Sons Ltd.)
- Subjects :
- Cytoplasm metabolism
Cytoplasm ultrastructure
Erythrocyte Membrane ultrastructure
Erythrocytes cytology
Erythrocytes ultrastructure
Hemoglobins metabolism
Host-Parasite Interactions
Humans
Merozoites ultrastructure
Microscopy, Electron, Scanning
Osmotic Pressure
Plasmodium falciparum growth & development
Plasmodium falciparum pathogenicity
Plasmodium knowlesi growth & development
Plasmodium knowlesi pathogenicity
Schizonts ultrastructure
Trophozoites ultrastructure
Vacuoles metabolism
Vacuoles ultrastructure
Erythrocyte Membrane metabolism
Erythrocytes parasitology
Plasmodium knowlesi ultrastructure
Subjects
Details
- Language :
- English
- ISSN :
- 1462-5822
- Volume :
- 21
- Issue :
- 5
- Database :
- MEDLINE
- Journal :
- Cellular microbiology
- Publication Type :
- Academic Journal
- Accession number :
- 30634201
- Full Text :
- https://doi.org/10.1111/cmi.13005