Skip to main content Accessibility help

Three-Dimensional Ultrastructure of the Ring Stage of Plasmodium falciparum: Evidence for Export Pathways

  • Lawrence Howard Bannister (a1), John Mervyn Hopkins (a1) (a2), Gabriele Margos (a1) (a2), Anton Richard Dluzewski (a1) (a2) and Graham Howard Mitchell (a2)...


The three-dimensional structure of the Plasmodium falciparum ring stage has been explored by reconstruction from serial sections and stereoscopic examination of tilted sections. The ring-like light microscopic appearance is related to the shape and contents of the biconcave discoidal parasite at this stage, its thick perimeter containing most of the ribosomes and its thin center containing smooth membrane organelles. The shapes of rings vary between flat and curved cuplike forms. The rough endoplasmic reticulum is a branched network continuous with the nuclear envelope. Evidence for a simple Golgi complex is seen in the presence on the outer nuclear envelope of a locus of coated vesicle budding associated with a single membranous cisterna or cluster of smooth vesicles. In middle and late stage rings this complex migrates along an extension of the nuclear envelope continuous with the rough endoplasmic reticulum. Evidence is also presented for a mechanism of exporting membrane from the parasite into the parasitophorous vacuole membrane and beyond into the red blood cell, by means of double-membraned vesicle-based exocytosis.


Corresponding author

Corresponding author. E-mail:


Hide All


Adisa, A., Rug, M., Foley, M., & Tilley, L. (2002). Characterisation of a delta-COP homologue in the malaria parasite, Plasmodium falciparum. Mol Biochem Parasitol 123, 1121.
Aikawa, M., Huff, C.G., & Sprinz, H. (1967). Comparative feeding mechanisms of avian and primate malarial parasites. Mil Med 131, 969983.
Bannister, L.H., Hopkins, J.M., Fowler, R.E., Krishna, S., & Mitchell, G.H. (2000). Ultrastructure of rhoptry development in Plasmodium falciparum erythrocytic merozoites. Parasitology 121, 273287.
Bannister, L.H., Hopkins, J.M., Fowler, R.E., Krishna, S., & Mitchell, G.H. (2001). A brief illustrated guide to the ultrastructure of Plasmodium falciparum asexual blood stages. Parasitol Today 16, 427433.
Cooke, B.M., Mohandas, N., & Coppel, R.L. (2001). The malaria-infected red blood cell: Structural and functional changes. Adv Parasitol 50, 186.
Deng, W. & Baker, D.A. (2002). A novel cyclic GMP-dependent protein kinase is expressed in the ring stage of the Plasmodium falciparum life cycle. Mol Microbiol 44, 11411151.
el-Shoura, S.M. & al-Amari, O.M. (1993). Falciparum malaria in naturally infected human patients: I. Ultrastructural differences between malaria pigments in intraerythrocytic asexual and sexual forms. J Morphol 215, 201206.
Fujioka, H. & Aikawa, M. (2002). Structure and life cycle. In Chemical Immunology, Vol. 80, Malaria Immunology, Perlmann, P. & Troye-Blomberg, M. (Eds.), pp. 126. Basel: Karger.
Garnham, P.C.C. (1966). Malaria Parasites and Other Haemosporidia. Oxford: Blackwell.
Hager, K.M., Striepen, B., Tilney, L.G., & Roos, D. (1999). The nuclear envelope serves as an intermediary between the ER and Golgi complex in the intracellular parasite Toxoplasma gondii. J Cell Sci 112, 26312638.
Haldar, K. (1998). Intracellular trafficking in Plasmodium-infected erythrocytes. Curr Opin Microbiol 1, 466471.
Hibbs, A.R. & Saul, A.J. (1994). Plasmodium falciparum: Highly mobile small vesicles in the malaria-infected red blood cell cytoplasm. Exp Parasitol 79, 260269.
Hopkins, J.M., Fowler, R.E., Krishna, S., Wilson, I., Mitchell, G.H., & Bannister, L.H. (1999). The plastid in Plasmodium falciparum asexual blood stages: A three-dimensional ultrastructural analysis. Protista 150, 283295.
Langreth, S.G., Jensen, J.B., Reese, R.T., & Trager, W. (1978). Fine structure of human malaria in vitro. J Protozool 25, 443452.
Meis, J.F.G.M., Jap, P.H.K., Verhave, J.P., & Meuwissen, J.H.E.T. (1983). Ultrastructural studies of a vesicle system associated with endoplasmic reticulum in exo-erythrocytic forms of Plasmodium berghei. J Protozool 30, 111114.
Pouvelle, B., Buffet, P.A., Lepolard, C., Scherf, A., & Gysin, J. (2000). Cytoadhesion of Plasmodium falciparum ring-stage-infected erythrocytes. Nat. Med 6, 12641268.
Prensier, G. & Slomianny, C. (1986). The karyotype of Plasmodium falciparum determined by ultrastructural serial sectioning and 3D reconstruction. J Parasitol 72, 731736.
Slomianny, C. (1990). Three-dimensional reconstruction of the feeding process of the malaria parasite. Blood Cells 16, 369378.
Slomianny, C. & Prensier, G. (1986). Application of the serial sectioning and tridimensional reconstruction techniques to the morphological study of the Plasmodium falciparum mitochondrion. J Parasitol 72, 595598.
Slomianny, C., Prensier, G., & Charet, P. (1985a). Comparative ultrastructural study on hemoglobin degradation by Plasmodium berghei in relation to maturity of the host cell. J Protozool 32, 15.
Slomianny, C., Prensier, G., & Charet, P. (1985b). Ingestion of erythrocytic stroma by Plasmodium chabaudi trophozoites: Ultrastructural study by serial sectioning and 3-dimensional reconstruction. Parasitology 90, 579588.
Spielmann, T. & Beck, H.P. (2000). Analysis of stage-specific transcription in Plasmodium falciparum reveals a set of genes exclusively transcribed in ring stage parasites. Mol Biochem Parasitol 111, 453458.
Van Wye, J., Ghori, N., Webster, P., Mitschler, R.R., Elmendorf, H.G., & Haldar, K. (1996). Identification and localization of rab6, separation of rab6 from ERD2 and implications for an ‘unstacked’ Golgi, in Plasmodium falciparum. Mol Biochem Parasitol 83, 107120.
Yayon, A., Timberg, R., Friedman, S., & Ginsburg, H. (1984). Effects of chloroquine on the feeding mechanism of the intraerythrocytic human malarial parasite Plasmodium falciparum. J Protozool 31, 367372.



Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed