Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-26T18:23:03.970Z Has data issue: false hasContentIssue false

Structural Analysis of Cryptosporidium parvum

Published online by Cambridge University Press:  01 October 2004

Franz Petry
Affiliation:
Institute of Medical Microbiology and Hygiene, Johannes Gutenberg University, Mainz, Germany
Get access

Abstract

Cryptosporidium parvum (Apicomplexa, formerly Sporozoa) is the causative agent of cryptosporidiosis, an enteric disease of substantial medical and veterinary importance. C. parvum shows a number of unique features that differ from the rest of the class of coccidea in which it is currently grouped taxonomically. Differences occur in the overall structure of the transmission form and the invasive stages of the parasite, its intracellular location, the presence of recently described additional extracellular stages, the host range and target cell tropism, the ability to autoinfection, the nonresponsiveness to anticoccidial drugs, the immune response of the host, and immunochemical and genetic characteristics. These differences have an important impact on the infectivity, the epidemiology, the therapy, and the taxonomy of the parasite. The present article describes the structural analysis of the parasite using light and electron microscopy with an emphasis on structural details unique to C. parvum.

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

Arrowood, M.J., Sterling, C.R., & Healey, M.C. (1991). Immunofluorescent microscopical visualization of trails left by gliding Cryptosporidium parvum sporozoites. J Parasitol 77, 315317.Google Scholar
Bjorneby, J.M., Riggs, M.W., & Perryman, L.E. (1990). Cryptosporidium parvum merozoites share neutralization-sensitive epitopes with sporozoites. J Immunol 145, 298304.Google Scholar
Bonnin, A., Dubremetz, J.F., & Camerlynck, P. (1991). Characterization and immunolocalization of an oocyst wall antigen of Cryptosporidium parvum (Protozoa: Apicomplexa). Parasitology 103, 171177.Google Scholar
Bonnin, A., Dubremetz, J.F., & Camerlynck, P. (1993). A new antigen of Cryptosporidium parvum micronemes possessing epitopes cross-reactive with macrogamete granules. Parasitol Res 79, 814.Google Scholar
Bonnin, A., Ojcius, D.M., Souque, P., Barnes, D.A., Doyle, P.S., Gut, J., Nelson, R.G., Petersen, C., & Dubremetz, J.F. (2001). Characterization of a monoclonal antibody reacting with antigen-4 domain of gp900 in Cryptosporidium parvum invasive stages. Parasitol Res 87, 589592.Google Scholar
Bouchet, F. & Boulard, Y. (1991). Ultrastructural changes following treatment with a microwave pulse in the oocyst of Eimeria magna Perard, 1925. Parasitol Res 77, 585589.Google Scholar
Bull, S., Chalmers, R., Sturdee, A.P., Curry, A., & Kennaugh, J. (1998). Cross-reaction of an anti-Cryptosporidium monoclonal antibody with sporocysts of Monocystis species. Vet Parasitol 77, 195197.Google Scholar
Carreno, R.A., Martin, D.S., & Barta, J.R. (1999). Cryptosporidium is more closely related to the gregarines than to coccidia as shown by phylogenetic analysis of apicomplexan parasites inferred using small-subunit ribosomal RNA gene sequences. Parasitol Res 85, 899904.Google Scholar
Chen, X.M., Gores, G.J., Paya, C.V., & Larusso, N.F. (1999). Cryptosporidium parvum induces apoptosis in biliary epithelia by a Fas/Fas ligand-dependent mechanism. Am J Physiol 277, G599G608.Google Scholar
Chen, X.M., Levine, S.A., Splinter, P.L., Tietz, P.S., Ganong, A.L., Jobin, C., Gores, G.J., Paya, C.V., & Larusso, N.F. (2001). Cryptosporidium parvum activates nuclear factor kappaB in biliary epithelia preventing epithelial cell apoptosis. Gastroenterology 120, 17741783.Google Scholar
Chen, X.M., Levine, S.A., Tietz, P., Krueger, E., McNiven, M.A., Jefferson, D.M., Mahle, M., & Larusso, N.F. (1998). Cryptosporidium parvum is cytopathic for cultured human biliary epithelia via an apoptotic mechanism. Hepatology 28, 906913.Google Scholar
Chobotar, W. & Scholtyseck, E. (1982). Ultrastructure. In Biology of the Coccidia, Long, P.L. (Ed.), pp. 101165. Baltimore, MD: University Park Press.
Current, W.L. & Garcia, L.S. (1991). Cryptosporidiosis. Clin Microbiol Rev 4, 325358.Google Scholar
Current, W.L. & Reese, N.C. (1986). A comparison of endogenous development of three isolates of Cryptosporidium in suckling mice. J Protozool 33, 98108.Google Scholar
Denton, H., Brown, S.M., Roberts, C.W., Alexander, J., McDonald, V., Thong, K.W., & Coombs, G.H. (1996). Comparison of the phosphofructokinase and pyruvate kinase activities of Cryptosporidium parvum, Eimeria tenella and Toxoplasma gondii. Mol Biochem Parasitol 76, 2329.Google Scholar
Dubremetz, J.F. & Dissous, C. (1980). Characteristic proteins of micronemes and dense granules from Sarcocystis tenella zoites (Protozoa, Coccidia). Mol Biochem Parasitol 1, 279289.Google Scholar
Dubremetz, J.F., Ferreira, E., & Dissous, C. (1989). Isolation and partial characterization of rhoptries and micronemes from Eimeria nieschulzi zoites (Sporozoa, Coccidia). Parasitol Res 75, 449454.Google Scholar
Dubremetz, J.F., Garcia-Reguet, N., Conseil, V., & Fourmaux, M.N. (1998). Apical organelles and host-cell invasion by Apicomplexa. Int J Parasitol 28, 10071013.Google Scholar
Etzion, Z., Murray, M.C., & Perkins, M.E. (1991). Isolation and characterization of rhoptries of Plasmodium falciparum. Mol Biochem Parasitol 47, 5162.Google Scholar
Farthing, M.J.G. (2000). Clinical aspects of human cryptosporidiosis. In Contributions to Microbiology, Vol. 6: Cryptosporidiosis and Microsporidiosis, Petry, F. (Ed.), pp. 5074. Basel: Karger.
Fayer, R., Morgan, U., & Upton, S.J. (2000). Epidemiology of Cryptosporidium: Transmission, detection and identification. Int J Parasitol 30, 13051322.Google Scholar
Fayer, R., Speer, C.A., & Dubey, J.P. (1997). The general biology of Cryptosporidium. In Cryptosporidium and Cryptosporidiosis, Fayer, R. (Ed.), pp. 141. Boca Raton, FL: CRC Press.
Fayer, R., Trout, J.M., & Jenkins, M.C. (1998). Infectivity of Cryptosporidium parvum oocysts stored in water at environmental temperatures. J Parasitol 84, 11651169.Google Scholar
Forney, J.R., Yang, S., & Healey, M.C. (1996). Protease activity associated with excystation of Cryptosporidium parvum oocysts. J Parasitol 82, 889892.Google Scholar
Fujino, T., Matsui, T., Kobayashi, F., Haruki, K., Yoshino, Y., Kajima, J., & Tsuji, M. (2002). The effect of heating against Cryptosporidium oocysts. J Vet Med Sci 64, 199200.Google Scholar
Göbel, E. & Brändler, U. (1982). Ultrastructure of microgametogenesis, microgametes and gametogony of Cryptosporidium sp. in the small intestine of mice. Protistologica 18, 331344.Google Scholar
Griffiths, J.K. (1998). Human cryptosporidiosis: Epidemiology, transmission, clinical disease, treatment, and diagnosis. Adv Parasitol 40, 3785.Google Scholar
Harris, J.R. (1997). Negative Staining and Cryoelectron Microscopy: The Thin Film Techniques. Oxford: BIOS Scientific Publishers Ltd.
Harris, J.R. & Agutter, P.S. (1970). A negative staining study of human erythrocyte ghosts and rat liver nuclear membranes. J Ultrastruct Res 33, 219232.Google Scholar
Harris, J.R. & Petry, F. (1999). Cryptosporidium parvum: Structural components of the oocyst wall. J Parasitol 85, 839849.Google Scholar
Hijjawi, N.S., Meloni, B.P., Ryan, U.M., Olson, M.E., & Thompson, R.C. (2002). Successful in vitro cultivation of Cryptosporidium andersoni: Evidence for the existence of novel extracellular stages in the life cycle and implications for the classification. Int J Parasitol 32, 17191726.Google Scholar
Hill, B.D., Blewett, D.A., Dawson, A.M., & Wright, S. (1991). Cryptosporidium parvum: Investigation of sporozoite excystation in vivo and the association of merozoites with intestinal mucus. Res Vet Sci 51, 264267.Google Scholar
Joachim, A., Eckert, E., Petry, F., Bialek, R., & Daugschies, A. (2003). Comparison of viability assays for Cryptosporidium parvum oocysts after disinfection. Vet Parasitol 111, 4757.Google Scholar
Kawazoe, U., Tomley, F.M., & Frazier, J.A. (1992). Fractionation and antigenic characterization of organelles of Eimeria tenella sporozoites. Parasitology 104, 19.Google Scholar
Leriche, M.A. & Dubremetz, J.F. (1991). Characterization of the protein content of rhoptries and dense granules of Toxoplasma gondii tachyzoites by subcellular fractionation and monoclonal antibodies. Mol Biochem Parasitol 45, 249260.Google Scholar
Levine, N.D. (1984). Taxonomy and review of the coccidian genus Cryptosporidium (protozoa, apicomplexa). J Protozool 31, 9498.Google Scholar
Lumb, R., Smith, K., O'Donoghue, P.J., & Lanser, J.A. (1988). Ultrastructure of the attachment of Cryptosporidium sporozoites to tissue culture cells. Parasitol Res 74, 531536.Google Scholar
Maréchal, E. & Cesbron-Delauw, M.F. (2001). The apicoplast: A new member of the plastid family. Trends Plant Sci 6, 200205.Google Scholar
McCole, D.F., Eckmann, L., Laurent, F., & Kagnoff, M.F. (2000). Intestinal epithelial cell apoptosis following Cryptosporidium parvum infection. Infect Immun 68, 17101713.Google Scholar
McDonald, V., Deer, R.M., Nina, J.M., Wright, S., Chiodini, P.L., & McAdam, K.P. (1991). Characteristics and specificity of hybridoma antibodies against oocyst antigens of Cryptosporidium parvum from man. Parasite Immunol 13, 251259.Google Scholar
McDonald, V., McCrossan, M.V., & Petry, F. (1995). Localization of parasite antigens in Cryptosporidium parvum-infected epithelial cells using monoclonal antibodies. Parasitology 110, 259268.Google Scholar
McDonald, V., Smith, R., Robinson, H., & Bancroft, G. (2000). Host immune responses against Cryptosporidium. In Contributions to Microbiology, Vol. 6: Cryptosporidiosis and Microsporidiosis, Petry, F. (Ed.), pp. 7591. Basel: Karger.
Meloni, B.P. & Thompson, R.C. (1996). Simplified methods for obtaining purified oocysts from mice and for growing Cryptosporidium parvum in vitro. J Parasitol 82, 757762.Google Scholar
Nelson, R.G. & Rosowsky, A. (2001). Dicyclic and tricyclic diaminopyrimidine derivatives as potent inhibitors of Cryptosporidium parvum dihydrofolate reductase: Structure-activity and structure-selectivity correlations. Antimicrob Agents Chemother 45, 32933303.Google Scholar
Ojcius, D.M., Perfettini, J.L., Bonnin, A., & Laurent, F. (1999). Caspase-dependent apoptosis during infection with Cryptosporidium parvum. Microbes Infect 1, 11631168.Google Scholar
Okhuysen, P.C., Chappell, C.L., Kettner, C., & Sterling, C.R. (1996). Cryptosporidium parvum metalloaminopeptidase inhibitors prevent in vitro excystation. Antimicrob Agents Chemother 40, 27812784.Google Scholar
Petry, F. (2000). Laboratory diagnosis of Cryptosporidium parvum infection. In Contributions to Microbiology, Vol. 6: Cryptosporidiosis and Microsporidiosis, Petry, F. (Ed.), pp. 3349. Basel: Karger.
Petry, F. & Harris, J.R. (1999). Ultrastructure, fractionation and biochemical analysis of Cryptosporidium parvum sporozoites. Int J Parasitol 29, 12491260.Google Scholar
Petry, F., Robinson, H.A., & McDonald, V. (1995). Murine infection model for maintenance and amplification of Cryptosporidium parvum oocysts. J Clin Microbiol 33, 19221924.Google Scholar
Pinckney, R.D., Lindsay, D.S., Toivio-Kinnucan, M.A., & Blagburn, B.L. (1993). Ultrastructure of Isospora suis during excystation and attempts to demonstrate extraintestinal stages in mice. Vet Parasitol 47, 225233.Google Scholar
Pokorny, N.J., Weir, S.C., Carreno, R.A., Trevors, J.T., & Lee, H. (2002). Influence of temperature on Cryptosporidium parvum oocyst infectivity in river water samples as detected by tissue culture assay. J Parasitol 88, 641643.Google Scholar
Reduker, D.W., Speer, C.A., & Blixt, J.A. (1985a). Ultrastructural changes in the oocyst wall during excystation of Cryptosporidium parvum (Apicomplexa; Eucoccidiorida). Can J Zool 63, 18921896.Google Scholar
Reduker, D.W., Speer, C.A., & Blixt, J.A. (1985b). Ultrastructure of Cryptosporidium parvum oocysts and excysting sporozoites as revealed by high resolution scanning electron microscopy. J Protozool 32, 708711.Google Scholar
Regan, S., Cama, V., & Sterling, C.R. (1991). Cryptosporidium merozoite isolation and purification using differential centrifugation techniques. J Protozool 38, 202S204S.Google Scholar
Riggs, M.W., McNeil, M.R., Perryman, L.E., Stone, A.L., Scherman, M.S., & O'Connor, R.M. (1999). Cryptosporidium parvum sporozoite pellicle antigen recognized by a neutralizing monoclonal antibody is a beta-mannosylated glycolipid. Infect Immun 67, 13171322.Google Scholar
Riggs, M.W., Stone, A.L., Yount, P.A., Langer, R.C., Arrowood, M.J., & Bentley, D.L. (1997). Protective monoclonal antibody defines a circumsporozoite-like glycoprotein exoantigen of Cryptosporidium parvum sporozoites and merozoites. J Immunol 158, 17871795.Google Scholar
Robert, B., Antoine, H., Dreze, F., Coppe, P., & Collard, A. (1994). Characterization of a high molecular weight antigen of Cryptosporidium parvum micronemes possessing epitopes that are cross-reactive with all parasitic life cycle stages. Vet Res 25, 384398.Google Scholar
Spano, F., Puri, C., Ranucci, L., Putignani, L., & Crisanti, A. (1997). Cloning of the entire COWP gene of Cryptosporidium parvum and ultrastructural localization of the protein during sexual parasite development. Parasitology 114, 427437.Google Scholar
Strong, W.B., Gut, J., & Nelson, R.G. (2000). Cloning and sequence analysis of a highly polymorphic Cryptosporidium parvum gene encoding a 60-kilodalton glycoprotein and characterization of its 15- and 45-kilodalton zoite surface antigen products. Infect Immun 68, 41174134.Google Scholar
Tetley, L., Brown, S.M.A., McDonald, V., & Coombs, G.H. (1998). Ultrastructural analysis of the sporozoite of Cryptosporidium parvum. Microbiology 144, 32493255.Google Scholar
Tilley, M., Eggleston, M.T., & Upton, S.J. (1993). Multiple oral inoculations with Cryptosporidium parvum as a means of immunization for production of monoclonal antibodies. FEMS Microbiol Lett 113, 235240.Google Scholar
Tilley, M. & Upton, S.J. (1991). Sporozoites and merozoites of Cryptosporidium parvum share a common epitope recognized by a monoclonal antibody and two-dimensional electrophoresis. J Protozool 38, 48S49S.Google Scholar
Tilley, M. & Upton, S.J. (1994). Both CP15 and CP25 are left as trails behind gliding sporozoites of Cryptosporidium parvum (Apicomplexa). FEMS Microbiol Lett 120, 275278.Google Scholar
Tyzzer, E.E. (1912). Cryptosporidium parvum (sp. nov.), a coccidium found in the small intestine of the common mouse. Arch Protistenkd 26, 394412.Google Scholar
Tzipori, S. & Griffiths, J.K. (1998). Natural history and biology of Cryptosporidium parvum. Adv Parasitol 40, 636.Google Scholar
Uni, S., Iseki, M., Maekawa, T., Moriya, K., & Takada, S. (1987). Ultrastructure of Cryptosporidium muris (strain RN 66) parasitizing the murine stomach. Parasitol Res 74, 123132.Google Scholar
Upton, S.J. (1997). In vitro cultivation. In Cryptosporidium and cryptosporidiosis, Fayer, R. (Ed.), pp. 181207. Boca Raton, FL: CRC Press.
Upton, S.J., Tilley, M., & Brillhart, D.B. (1995). Effects of select medium supplements on in vitro development of Cryptosporidium parvum in HCT-8 cells. J Clin Microbiol 33, 371375.Google Scholar
Widmer, G., Corey, E.A., Stein, B., Griffiths, J.K., & Tzipor, I.S. (2000). Host cell apoptosis impairs Cryptosporidium parvum development in vitro. J Parasitol 86, 922928.Google Scholar
Wolinsky, E. (1990). Mycobacteria. In Microbiology, Davis, B.D., Dulbecco, R. Eisen, H.N. & Ginsberg, H.S. (Eds.), pp. 647664. Philadelphia: J.B. Lippincott.
Woods, K.M., Nesterenko, M.V., & Upton, S.J. (1996). Efficacy of 101 antimicrobials and other agents on the development of Cryptosporidium parvum in vitro. Ann Trop Med Parasitol 90, 603615.Google Scholar