Hostname: page-component-848d4c4894-xm8r8 Total loading time: 0 Render date: 2024-07-05T01:15:55.513Z Has data issue: false hasContentIssue false

Crystalloid body, refractile body and virus-like particles in Apicomplexa: what is in there?

Published online by Cambridge University Press:  05 January 2012

LEANDRO LEMGRUBER*
Affiliation:
Department of Infectious Diseases, Parasitology, University of Heidelberg Medical School, Heidelberg, Germany
PIETRO LUPETTI
Affiliation:
Department of Evolutionary Biology, University of Siena, Italy
*
*Corresponding author: Department of Infectious Diseases, Parasitology, Im Neuenheimer Feld 324, 69120 Heidelberg, Germany. Tel: +49 6221 567818. Fax: +49 6221 566543. E-mail: [email protected]

Summary

The phylum of Apicomplexa comprises parasitic protozoa that share distinctive features such as the apical complex, the apicoplast, specialized cytoskeletal components and secretory organelles. Other unique cytoplasmic inclusions sharing similar features have been described in some representatives of Apicomplexa, although under different denominations. These are the crystalloid body, present for example in Cryptosporidium, Plasmodium and Cystoisospora; the refractile body in Eimeria and Lankesterella; and virus-like particles, also present in Eimeria and Cryptosporidium. Yet, the specific role of these cytoplasmic inclusions in the cell cycle of these protozoa is still unknown. Here, we discuss their morphology, possible inter-relatedness and speculate upon their function to bring these organelles back to the attention of the scientific community and promote new interest towards original research on these elusive structures.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2012

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

Abrahamsen, M. S., Johnson, R. R., Jutila, M. A., Speer, C. A. and White, M. W. (1994). Eimeria bovis expression of a related group of refractile body-associated proteins during schizogony. Experimental Parasitology 78, 331335.CrossRefGoogle ScholarPubMed
Alderete, J. F., Demes, P., Gombosova, A., Valent, M., Yánoska, A., Fabusová, H., Kasmala, L., Garza, G. E. and Metcalfe, E. (1987). Phenotypes and protein/epitope phenotypic variation among fresh isolates of Trichomonas vaginalis. Infection and Immunity 55, 10371041.CrossRefGoogle ScholarPubMed
Augustine, P. C. (1999). Reduced invasion of cultured cells pretreated with a monoclonal antibody elicited against refractile body antigens of avian coccidial sporozoites. Journal of Eukaryotic Microbiology 46, 254258.CrossRefGoogle ScholarPubMed
Augustine, P. C. (2001). Invasion of different cell types of sporozoites of Eimeria species and effects of monoclonal antibody 1209-C2 on invasion of cells by sporozoites of several apicomplexan parasites. Journal of Eukaryotic Microbiology 48, 177181.CrossRefGoogle ScholarPubMed
Azevedo, C. (2001). Fine structure of sporogonic stages of Goussia clupearum (Apicomplexa: Eimeriidae) in the liver of infected fish (Belone belone L.), using light and electron microscopy. Parasitology Research 87, 326330.CrossRefGoogle Scholar
Benchimol, M., Monteiro, S. P., Chang, T. H. and Alderete, J. F. (2002). Virus in Trichomonas – an ultrastructural study. Parasitoligy International 51, 293298.CrossRefGoogle ScholarPubMed
Beyer, T., Scholtyseck, E. and Entzeroth, E. (1983). Fine structure of the merozoite of a haemogregarine from the testis of a lizard. Zeitschrift für Parasitenkunde 69, 439445.CrossRefGoogle Scholar
Boulard, Y., Paperna, I., Petit, G. and Landau, I. (2001). Ultrastructure of developmental stages of Hemolivia stellata (Apicomplexa: Haemogregarinidae) in the cane toad Bufo marinus and its vector tick Amblyomma rotondatum. Parasitology Research 87, 598604.CrossRefGoogle ScholarPubMed
Carruthers, V. B. and Tomley, F. M. (2008). Microneme proteins in apicomplexans. Subcellular Biochemistry 47, 3345.CrossRefGoogle ScholarPubMed
Carter, V., Shimizu, S., Arai, M. and Dessens, J. T. (2008). PbSR is synthesized in macrogametocytes and involved in formation of the malaria crystalloids. Molecular Microbiology 68, 15601569.CrossRefGoogle ScholarPubMed
Cesbron-Delauw, M. F., Gendrin, C., Travier, L., Ruffiot, P. and Mercier, C. (2008). Apicomplexan in mammalian cells: Trafficking to the parasitophorous vacuole. Traffic 9, 657664.CrossRefGoogle Scholar
Claudianos, C., Dessens, J. T., Trueman, H. E., Arai, M., Mendoza, J., Butcher, G. A., Crompton, T. and Sinden, R. E. (2002). A malaria scavenger receptor-like protein essential for parasite development. Molecular Microbiology 45, 14731484.CrossRefGoogle ScholarPubMed
Ctrnacta, V., Ault, J. G., Stejskal, F. and Keithly, J. S. (2006). Localization of pyruvate:NADP+ oxidoreductase in sporozoites of Cryptosporidium parvum. Journal of Eukaryotic Microbiology 53, 225331.CrossRefGoogle ScholarPubMed
Danforth, H. D. and Augustine, P. C. (1989). Eimeria tenella: use of a monoclonal antibody in determining the intracellular fate of the refractile body organelles and the effect on in vitro development. Experimental Parasitology 68, 17.CrossRefGoogle ScholarPubMed
de Venevelles, P., Chich, J. F., Faigle, W., Loew, D., Labbé, M., Girard-Misguich, F. and Péry, P. (2004). Towards a reference map of Eimeria tenella sporozoite proteins by two-dimensional electrophoresis and mass spectrometry. International Journal for Parasitology 34, 1321–1231.CrossRefGoogle ScholarPubMed
de Venevelles, P., Chich, J. F., Faigle, W., Lombard, B., Loew, D., Péry, P. and Labbé, M. (2006). Study of proteins associated with the Eimeria tenella refractile body by a proteomic approach. International Journal for Parasitology 36, 13991407.CrossRefGoogle ScholarPubMed
del Cacho, E., Gallego, M., Montes, C., López-Bernad, F., Quílez, J. and Sánchez-Acedo, C. (2001). Eimeria necatrix virus: intracellular localisation of viral particles and proteins. International Journal for Parasitology 31, 12691274.CrossRefGoogle ScholarPubMed
Dessens, J. T., Sinde, R. E. and Claudianos, C. (2004). LCCL proteins of apicomplexan parasites. Trends in Parasitology 20, 102108.CrossRefGoogle ScholarPubMed
Dessens, J. T., Saeed, S., Tremp, A. Z. and Carter, V. (2011). Malaria crystalloids: sprecialized structures for parasite transmission? Trends in Parasitology 27, 106110.CrossRefGoogle ScholarPubMed
Desser, S. S. (1993). The Haemogregarinidae and Lankesterellidae. In Parasitic Protozoa vol. 4 (ed. Kreler, J. P.), pp. 133245. Academic Press, Inc., San Diego, CA, USA.Google Scholar
Dowling, S. C., Perryman, L. E. and Jasmer, D. P. (1996). A Babesia bovis 225-kilodalton spherical-body protein: localization to the cytoplasmic face of infected erythrocytes after merozoite invasion. Infection and Immunity 64, 26182626.CrossRefGoogle Scholar
Dubremetz, J. F. (2007). Rhoptries are major players in Toxoplasma gondii invasion and host cell interaction. Cellular Microbiology 9, 841848.CrossRefGoogle ScholarPubMed
Ellis, J. and Revets, H. (1990). Eimeria species which infect the chicken contain virus-like RNA molecules. Parasitology 101, 163169.CrossRefGoogle ScholarPubMed
Fleige, T., Fischer, K., Ferguson, D. J., Gross, U. and Bohne, W. (2007). Carbohydrate metabolism in the Toxoplasma gondii apicoplast: localization of three glycolytic isoenzymes, the single pyruvate dehydrogenase complex, and a plastid phosphate translocator. Eukaryotic Cell 6, 984996.CrossRefGoogle Scholar
Garnham, P. C. C., Bird, R. G. and Baker, J. R. (1962). Electron microscope studies of motile stages of malaria parasites: III. The ookinetes of Haemamoeba and Plasmodium. Transactions of the Royal Society of Tropical Medicine and Hygiene 56, 116120.CrossRefGoogle ScholarPubMed
Garnham, P. C. C., Bird, R. G., Baker, J. R., Desser, S. S., El-Nahal, H. M. S. (1969). Electron microscopic studies on motile stages of malaria parasites: VI. The ookinete of Plasmodium berghei yoelii and its transformation into the early oocyst. Transactions of the Royal Society of Tropical Medicine and Hygiene 63, 187194.CrossRefGoogle ScholarPubMed
Gleeson, M. T. (2000). The plastid in Apicomplexa: what use is it? International Journal for Parasitoligy 30, 10531070.CrossRefGoogle Scholar
Goodman, C. D. and McFadden, G. I. (2007). Fatty acid biosynthesis as a drug target in apicomplexan parasites. Current Drug Targets 8, 1530.CrossRefGoogle ScholarPubMed
Greenspan, P., Mayer, E. P. and Fowler, S. D. (1985). Nile red: a selective fluorescent stain for intracellular lipid droplets. Journal of Cell Biology 100, 965973.CrossRefGoogle ScholarPubMed
Harris, P. K., Yeoh, S., Dluzewski, A. R., O'Donnell, R. A., Withers-Martinez, C., Hackett, F., Bannister, L. H., Mitchell, G. H. and Blackman, M. J. (2005). Molecular identification of a malaria merozoite surface sheddase. PLoS Pathogens 1, 241351.CrossRefGoogle ScholarPubMed
Jasmer, D. P., Reduker, D. W., Perryman, L. E. and McGuire, T. C. (1992). A Babesia bovis 225-kilodalton protein located on the cytoplasmic side of the erythrocyte membrane has sequence similarity with a region of glycogen phosphorylase. Molecular and Biochemical Parasitology 52, 263269.CrossRefGoogle ScholarPubMed
Jean, L., Grosclaude, J., Labbé, M., Tomley, F. and Péry, P. (2000). Differential localisation of an Eimeria tenella aspartyl proteinase during the infection process. International Journal for Parasitology 30, 10991107.CrossRefGoogle ScholarPubMed
Johnston, R. C., Farias, N. A., Gonzales, J. C., Dewes, H., Masuda, A., Termignoni, C., Amako, K. and Ozaki, L. S. (1991). A putative RNA virus in Babesia bovis. Molecular and Biochemical Parasitology 45, 155158.CrossRefGoogle ScholarPubMed
Joiner, K. A. and Roos, D. S. (2002). Secretory traffic in the eukaryotic parasite Toxoplasma gondii: less is more. Journal of Cell Biology 157, 557563.CrossRefGoogle ScholarPubMed
Kawai, S., Igarashi, I., Abgaandorjiin, A., Miyazawa, K., Ikadai, H., Nagasawa, H., Fujisaki, K., Mikami, T., Suzuki, N. and Matsuda, H. (1999). Ultrastructural characteristics of Babesia caballi in equine erythrocytes in vitro. Parasitology Research 85, 794799.CrossRefGoogle ScholarPubMed
Keithly, J. S., Langreth, S. G., Buttle, K. F. and Mannella, C. A. (2005). Electron tomographic and ultrastructural analysis of the Cryptosporidium parvum relict mitochondrion, its associated membranes, and organelles. Journal of Eukaryotic Microbiology 52, 132140.CrossRefGoogle ScholarPubMed
Khramtsov, N. V. and Upton, S. J. (2000). Association of RNA polymerase complexes of the parasitic protozoan Cryptosporidium parvum with virus-like particles: heterogeneous system. Journal of Virology 74, 57885795.CrossRefGoogle ScholarPubMed
Khramtsov, N. V., Woods, K. M., Nesterenko, M. V., Dykstra, C. C. and Upton, S. J. (1997). Virus-like, double-stranded RNAs in the parasitic protozoan Cryptosporidium parvum. Molecular Microbiology 26, 289300.CrossRefGoogle ScholarPubMed
Köhler, S., Delwiche, C., Denny, D., Tilney, L., Webster, P., Wilson, R., Palmer, J. and Roos, D. (1997). A plastid of probable green algal origin in Apicomplexan parasites. Science 275, 14851489.CrossRefGoogle ScholarPubMed
Kopko, S. H., Martin, D. S. and Barta, J. S. (2000). Responses of chickens to a recombinant refractile body antigen of Eimeria tenella administered using various immunizing strategies. Poultry Science 79, 336342.CrossRefGoogle ScholarPubMed
Lal, K., Bromley, E., Oakes, R., Prieto, J. H., Sanderson, S. J., Kurian, D., Hunt, L., Yates, J. R. III, Wastling, J. M., Sinden, R. E. and Tomley, F. M. (2009). Proteomic comparison of four Eimeria tenella life-cycle stages: Unsporulated oocyst, sporulated oocyst, sporozoite and second-generation merozoite. Proteomics 9, 45664576.CrossRefGoogle ScholarPubMed
La Scola, B., Audic, S., Robert, C., Jungang, L., de Lamballerie, X., Drancourt, M., Birtles, R., Claverie, J. M. and Raoult, D. (2003). A giant virus in amoebae. Science 299, 2033.CrossRefGoogle ScholarPubMed
Lee, S. and Fernando, M. A. (2000). Viral double-stranded RNAs of Eimeria spp. of the domestic fowl: analysis of genetic relatedness and divergence among various strains. Parasitology Research 86, 733737.CrossRefGoogle ScholarPubMed
Lindsay, D. S., Dubey, J. P. and Blagburn, B. L. (1997). Biology of Isospora spp. from humans, nonhuman primates, and domestic animals. Clinical Microbiology Reviews 10, 1934.CrossRefGoogle ScholarPubMed
Liu, J., Gluzman, I. Y., Drew, M. E. and Goldberg, D. E. (2005). The role of Plasmodium falciparum food vacuole plasmepsins. Journal of Biological Chemistry 280, 14321437.CrossRefGoogle ScholarPubMed
Lowichik, A., Lanners, H. N., Lowrie, R. C. Jr. and Meiners, N. E. (1993). Gametogenesis and sporogony of Hepatozoon mocassini (Apicomplexa: Adeleina: Hepatozoidae) in an experimental mosquito host, Aedes aegypti. Journal of Eukaryotic Microbiology 40, 287297.CrossRefGoogle Scholar
Marche, S., Roth, C., Manohar, S. K., Dollet, M. and Baltz, T. (1993). RNA virus-like particles in pathogenic plant trypanosomatids. Molecular and Biochemical Parasitology 57, 261268.CrossRefGoogle ScholarPubMed
Mattern, C. F., Diamond, L. S. and Daniel, W. A. (1972). Viruses of Entamoeba histolytica. II. Morphogenesis of the polyhedral particle (ABRM 2 leads to HK-9) leads to HB-301 and the filamentous agent (ABRM) 2 leads to HK-9. Journal of Virology 9, 342358.CrossRefGoogle ScholarPubMed
Mattern, C. F., Hruska, J. F. and Diamond, L. S. (1974). Viruses of Entamoeba histolytica. V. Ultrastructure of the polyhedral virus V301. Journal of Virology 13, 247249.CrossRefGoogle ScholarPubMed
Mazumbar, J., Wilson, E. H., Masek, K., Hunter, C. A. and Striepen, B. (2006). Apicoplast fatty acid synthesis is essential for organelle biogenesis and parasite survival in Toxoplasma gondii. Proceedings of the National Academy of Sciences, USA 103, 1319213197.CrossRefGoogle Scholar
Mazur, P. (1984). Freezing of living cells: mechanisms and implications. American Journal of Physiology 247, C125142.CrossRefGoogle ScholarPubMed
Mehlhorn, H. and Markus, M. B. (1976). Electron microscopy of stages of Isospora felis of the cat in the mesenteric lymph node of the mouse. Zeitschrift für Parasitenkunde 51, 1524.CrossRefGoogle ScholarPubMed
Meis, J. F. and Ponnudurai, T. (1987). Ultrastructural studies on the interaction of Plasmodium falciparum ookinetes with the midgut epithelium of Anopheles stephensi mosquitoes. Parasitology Research 73, 500506.CrossRefGoogle ScholarPubMed
Michalski, W. P., Edgar, J. A. and Prowse, S. J. (1992). Mannitol metabolism in Eimeria tenella. International Journal for Parasitology 22, 11571163.CrossRefGoogle ScholarPubMed
Miranda, K., de Souza, W., Plattner, H., Hentschel, J., Kawazoe, U., Fang, J. and Moreno, S. N. (2008). Acidocalcisomes in Apicomplexan parasites. Experimental Parasitology 118, 29.CrossRefGoogle ScholarPubMed
Mitchell, S. M., Zajac, A. M. and Lindsay, D. S. (2009). Development and ultrastructure of Cystoisospora canis Nemeséri, 1959 (syn. Isospora canis) monozoic cysts in two noncanine cell lines. Journal of Parasitology 95, 793798.CrossRefGoogle ScholarPubMed
Molyneux, D. H. (1974). Virus-like particles in Leishmania parasites. Nature, London 249, 588589.CrossRefGoogle ScholarPubMed
Morrissette, N. and Sibley, L. D. (2002). Cytoskeleton of Apicomplexan parasites. Microbiology and Molecular Biology Reviews 66, 2138.CrossRefGoogle ScholarPubMed
Murphy, F. A., Fauquet, C. M., Bishop, D. H. L., Ghabrial, S. A., Jarvis, A. W., Martelli, G. P., Mayo, M. A. and Summers, M. D. (ed.) (1995). Virus Taxonomy, Classification and Nomenclature of Viruses. Sixth Report of the International Committee on Taxonomy of Viruses. Springer-Verlag, Vienna, Austria.Google Scholar
Ong, S. J. and Tai, J. H. (2000). Identification of virus-specific vesicles in Giardia virus-infected Giardia lamblia. Journal of Microbiology and Immunological Infections 33, 913.Google ScholarPubMed
Paperna, I. (1992). Ultrastructural studies on oocysts, sporulation and sporozoites of Schellakia cf. agamae from the intestine of the starred lizard Agama stellio. International Journal for Parasitology 22, 361368.CrossRefGoogle Scholar
Petry, F. and Harris, J. R. (1999). Ultrastructure, fractionation and biochemical analysis of Cryptosporidium parvum sporozoites. International Journal for Parasitology 29, 12491260.CrossRefGoogle ScholarPubMed
Porchet-Henneré, E. (1971). [Fertilization and sporogony of the cocidian Coelotropha durchoni. Optical and electron microscopy study]. Zeitschrift für Parasitenkunde 37, 94125.Google Scholar
Porchet-Henneré, E. and Richard, A. (1971). [Sporogenesis in the cocdian Aggregata eberthi. Electron microscope study]. Journal of Protozoology 18, 614628.CrossRefGoogle ScholarPubMed
Pradel, G., Hayton, K., Aravind, L., Iyer, L. M., Abrahamsen, M. S., Bonawitz, A., Mejia, C. and Templeton, T. J. (2004). A multidomain adhesion protein family expressed in Plasmodium falciparum is essential for transmission to the mosquito. Journal of Experimental Medicine 199, 15331544.CrossRefGoogle Scholar
Raibaud, A., Lupetti, P., Paul, R. E., Mercati, D., Brey, P. T., Sinden, R. E., Heuser, J. E. and Dallai, R. (2001). Cryofracture electron microscopy of the ookinete pellicle of Plasmodium gallinaceum reveals the existence of novel pores in the alveolar membranes. Journal of Structural Biology 135, 4757.CrossRefGoogle ScholarPubMed
Revets, H., Dekegel, D., Deleersnijder, W., De Jonckheere, J., Peeters, J., Leysen, E. and Hamers, H. (1989). Identification of virus-like particles in Eimeria stiedae. Molecular and Biochemical Parasitology 36, 209216.CrossRefGoogle ScholarPubMed
Roditi, I., Wyler, T., Smith, N. and Braun, R. (1994). Virus-like particles in Eimeria nieschulzi are associated with multiple RNA segments. Molecular and Biochemical Parasitology 63, 275282.CrossRefGoogle ScholarPubMed
Ruef, B. J., Dowling, S. C., Conley, P. G., Perryman, L. E., Brown, W. C., Jasmer, D. P. and Rice-Ficht, A. C. (2000). A unique Babesia bovis spherical body protein is conserved among geographic isolates and localizes to the infected erythrocyte membrane. Molecular and Biochemical Parasitology 105, 112.CrossRefGoogle Scholar
Saeed, S., Carter, V., Tremp, A. Z. and Dessens, J. T. (2010). Plasmodium berghei crystalloids contain multiple LCCL proteins. Molecular and Biochemical Parasitology 170, 4953.CrossRefGoogle ScholarPubMed
Scholtyseck, E. and Ghaffar, F. A. (1981). Eimeria falciformis – merozoites with refractile bodies. Zeitschrift für Parasitenkunde 65, 117120.CrossRefGoogle ScholarPubMed
Schrével, J. (1971). Observations biologiques et ultrastrcturales sur les Selenidiidae et leurs conséquences sur la systématique des Grégarinomorphes. Journal of Protozoology 18, 448470.CrossRefGoogle Scholar
Schrével, J. and Philippe, M. (1993). The Gregarines. In Parasitic Protozoa vol. 4 (ed. Kreler, J. P.), pp. 133245. Academic Press, Inc., San Diego, CA, USA.Google Scholar
Schuster, F. L. (1969). Intranuclear viruslike bodies in the amoebofiageliate Naegleria gruberi. Journal of Protozoology 16, 724727.CrossRefGoogle ScholarPubMed
Sinden, R. E. and Strong, K. (1978). An ultrastructural study of the sporogonic development of Plasmodium falciparum in Anopheles gambiae. Transactions of the Royal Society of Tropical Medicine and Hygiene 72, 477491.CrossRefGoogle ScholarPubMed
Smallridge, C. and Paperna, I. (2000). Ultrastructure of Hemolivia mariae gamonts in the blood of the lizard Tiliqua rugosa and their development to oocyst stage in the tick Amblyomma limbatum. Parasitology Research 86, 563569.CrossRefGoogle ScholarPubMed
Speer, C. A. and Dubey, J. P. (1989). Ultrastructure of sporozoites and zoites of Hammondia heydorni. Journal of Protozoology 36, 488493.CrossRefGoogle ScholarPubMed
Speer, C. A., Dubey, J. P., McAllister, M. M. and Blixt, J. A. (1999). Comparative ultrastructure of tachyzoites, bradyzoites, and tissue cysts of Neospora caninum and Toxoplasma gondii. International Journal for Parasitology 29, 15091519.CrossRefGoogle ScholarPubMed
Sundermann, C. A. and Lindsay, D. S. (1989). Ultrastructure of in vivo-produced caryocysts containing the coccidian Caryospora bigenetica (Apicomplexa: Eimeriidae). Journal of Protozoology 36, 8186.CrossRefGoogle ScholarPubMed
Tenter, A. M., Barta, J. R., Beveridge, I., Duszynski, D. W., Mehlhorn, H., Morrison, D. A., Thompson, R. C. and Conrad, P. A. (2002). The conceptual basis for a new classification of the coccidia. International Journal for Parasitology 32, 595616.CrossRefGoogle ScholarPubMed
Terkawi, M. A., Seuseu, F. J., Eko-Wibowo, P., Huyen, N. X., Minoda, Y., AbouLaila, M., Kawai, S., Yokoyama, N., Xuan, X. and Igarashi, I. (2011). Secretion of a new spherical body protein of Babesia bovis into the cytoplasm of infected erythrocytes. Molecular and Biochemical Parasitology 178, 4045.CrossRefGoogle ScholarPubMed
Terzakis, J. A., Vanderberg, J. P. and Weiss, M. M. (1976). Viruslike particles in malaria parasites. Journal of Parasitology 62, 366371.CrossRefGoogle ScholarPubMed
Tetley, L., Brown, S. M. A., McDonald, V. and Coombs, G. H. (1998). Ultrastructural analysis of the sporozoite of Cryptosporidium parvum. Microbiology 144, 32493255.CrossRefGoogle ScholarPubMed
Trefiak, W. D. and Desser, S. S. (1973). Crystalloid inclusions in species of Leucoeytozoon, Parahaemoproteus and Plasmodium. Journal of Protozoology 20, 7380.CrossRefGoogle ScholarPubMed
Upton, S. J. and Barnard, S. M. (1988). Development of Caryospora bigenetica (Apicomplexa: Eimeriorina) in experimentally infected mice. International Journal for Parasitology 18, 1520.CrossRefGoogle ScholarPubMed
Uzureau, P., Barale, J. C., Janse, C. J., Waters, A. P. and Breton, C. B. (2004). Gene targeting demonstrates that the Plasmodium berghei subtilisin PbSUB2 is essential for red cell invasion and reveals spontaneous genetic recombination events. Cellular Microbiology 6, 6578.CrossRefGoogle ScholarPubMed
Vermeulen, A. N., Kok, J. J., van den Boogaart, P., Dijkema, R. and Claessens, J. A. (1993). Eimeria refractile body proteins contain two potentially functional characteristics: transhydrogenase and carbohydrate transport. FEMS Microbiology Letters 110, 223229.CrossRefGoogle ScholarPubMed
Vlemmas, I., Kakanoudis, G., Tsangaris, T. H., Theodorides, I. and Kaldrymidou, E. (1989). Ultrastructure of Sarcocystis tenella (Sarcocystis ovicanis). Veterinary Parasitology 33, 207217.CrossRefGoogle ScholarPubMed
Wang, A. L., Wang, C. C. and Alderete, J. F. (1987). Trichomonas vaginalis phenotypic variation occurs only among trichomonad infected with the double-stranded RNA virus. Journal of Experimental Medicine 166, 142150.CrossRefGoogle ScholarPubMed
Wong, T. C. and Desser, S. S. (1976). Fine structure of oocyst transformation and the sporozoites of Leucocytozoon dubreuili. Journal of Protozoology 23, 115126.CrossRefGoogle ScholarPubMed
Yeh, E. and DeRisi, J. L. (2011). Chemical Rescue of Malaria Parasites Lacking an Apicoplast Defines Organelle Function in Blood-Stage Plasmodium falciparum. PLoS Biology 9: e1001138. doi:10.1371/journal.pbio.1001138.CrossRefGoogle ScholarPubMed