Intraerythrocytic development of Plasmodium knowlesi: structure, temperature- and Ca2+-response of the host and parasite membranes

Abstract

Thin-sectioning and freeze-etching electron microscopy were applied to explore the structure and the temperature- and Ca2+-response of the different host and parasite membranes during intraerythrocytic development of Plasmodium knowlesi in Macaca mulatta. The plasma membrane of uninfected erythrocytes is temperature- and Ca2+-responsive: chilling to 4 degrees C and exposure to 5 mM Ca2+ induces a slight decrease in IMP-frequency and the emergence of small IMP-devoid patches on P-faces. On parasite infection, the erythrocyte membrane becomes modified as indicated by an enhanced temperature-response and the appearance of caveolae, ca. 70-90 nm in diameter. The frequency of these caveolae is increased in schizont-infected erythrocytes. Moreover, electron dense plaques, ca. 40 nm in width, appear just beneath the erythrocyte membrane in late trophozoites and schizonts, thus indicating a further modification of the host cell membrane during parasite development. The membrane of the parasitophorous vacuole, derived from the host plasma membrane, dramatically reduces the IMP-frequency especially on the P-face upon parasite infection. This leads to an apparent reversal of the IMP-distribution persisting throughout the whole infection cycle. The parasite plasma membrane forms local compaction domains with the nuclear envelope in ca. 30% of the ring-stages and trophozoites, which disappear in late trophozoites and schizonts. Moreover, the IMP-frequency on plasma membrane fracture faces almost doubles during parasite development. Chilling induces a decrease in the IMP-frequency on P-faces of the plasma membrane. Surprisingly, however, the parasite plasma membrane and the vacuolar membrane respond to externally applied Ca2+ with almost a doubling of the IMP-frequency. The different parasite endomembranes also undergo characteristic changes during parasite development.