Hostname: page-component-8448b6f56d-t5pn6 Total loading time: 0 Render date: 2024-04-19T00:48:31.625Z Has data issue: false hasContentIssue false

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

Published online by Cambridge University Press:  01 October 2004

Lawrence Howard Bannister
Affiliation:
Department of Anatomy, Cell and Human Biology, Guy's, King's and St. Thomas' School of Biomedical Science, Guy's Hospital, London SE1 1UL, UK
John Mervyn Hopkins
Affiliation:
Department of Anatomy, Cell and Human Biology, Guy's, King's and St. Thomas' School of Biomedical Science, Guy's Hospital, London SE1 1UL, UK Department of Immunobiology, Guy's, King's and St. Thomas' School of Medicine, Guy's Hospital, London SE1 9RT, UK
Gabriele Margos
Affiliation:
Department of Anatomy, Cell and Human Biology, Guy's, King's and St. Thomas' School of Biomedical Science, Guy's Hospital, London SE1 1UL, UK Department of Immunobiology, Guy's, King's and St. Thomas' School of Medicine, Guy's Hospital, London SE1 9RT, UK
Anton Richard Dluzewski
Affiliation:
Department of Anatomy, Cell and Human Biology, Guy's, King's and St. Thomas' School of Biomedical Science, Guy's Hospital, London SE1 1UL, UK Department of Immunobiology, Guy's, King's and St. Thomas' School of Medicine, Guy's Hospital, London SE1 9RT, UK
Graham Howard Mitchell
Affiliation:
Department of Immunobiology, Guy's, King's and St. Thomas' School of Medicine, Guy's Hospital, London SE1 9RT, UK
Get access

Abstract

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.

Type
Feature Articles
Copyright
© 2004 Microscopy Society of America

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

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.Google Scholar
Aikawa, M., Huff, C.G., & Sprinz, H. (1967). Comparative feeding mechanisms of avian and primate malarial parasites. Mil Med 131, 969983.Google Scholar
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.Google Scholar
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.Google Scholar
Cooke, B.M., Mohandas, N., & Coppel, R.L. (2001). The malaria-infected red blood cell: Structural and functional changes. Adv Parasitol 50, 186.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Haldar, K. (1998). Intracellular trafficking in Plasmodium-infected erythrocytes. Curr Opin Microbiol 1, 466471.Google Scholar
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.Google Scholar
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.Google Scholar
Langreth, S.G., Jensen, J.B., Reese, R.T., & Trager, W. (1978). Fine structure of human malaria in vitro. J Protozool 25, 443452.Google Scholar
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.Google Scholar
Pouvelle, B., Buffet, P.A., Lepolard, C., Scherf, A., & Gysin, J. (2000). Cytoadhesion of Plasmodium falciparum ring-stage-infected erythrocytes. Nat. Med 6, 12641268.Google Scholar
Prensier, G. & Slomianny, C. (1986). The karyotype of Plasmodium falciparum determined by ultrastructural serial sectioning and 3D reconstruction. J Parasitol 72, 731736.Google Scholar
Slomianny, C. (1990). Three-dimensional reconstruction of the feeding process of the malaria parasite. Blood Cells 16, 369378.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar