Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-26T01:17:41.677Z Has data issue: false hasContentIssue false
  • English
  • Français

Life cycle of Cryptosporidium muris in two rodents with different responses to parasitization

Published online by Cambridge University Press:  11 October 2013

JANKA MELICHEROVÁ ,
JANA ILGOVÁ ,
MARTIN KVÁČ ,
BOHUMIL SAK ,
BŘETISLAV KOUDELA  and
ANDREA VALIGUROVÁ
JANKA MELICHEROVÁ
Affiliation:
Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 2, 611 37 Brno, Czech Republic
JANA ILGOVÁ
Affiliation:
Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 2, 611 37 Brno, Czech Republic
MARTIN KVÁČ
Affiliation:
Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, Branišovská 31, 370 05 České Budějovice, Czech Republic
BOHUMIL SAK
Affiliation:
Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, Branišovská 31, 370 05 České Budějovice, Czech Republic
BŘETISLAV KOUDELA
Affiliation:
Department of Pathological Morphology and Parasitology, University of Veterinary and Pharmaceutical Sciences, Palackého 1/3, 612 42 Brno, Czech Republic
ANDREA VALIGUROVÁ*
Affiliation:
Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 2, 611 37 Brno, Czech Republic
*
* Corresponding author: Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 2, 611 37 Brno, Czech Republic. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

This study focuses on mapping the life cycle of Cryptosporidium muris in two laboratory rodents; BALB/c mice and the southern multimammate rat Mastomys coucha, differing in their prepatent and patent periods. Both rodents were simultaneously experimentally inoculated with viable oocysts of C. muris (strain TS03). Animals were dissected and screened for the presence of the parasite using a combined morphological approach and nested PCR (SSU rRNA) at different times after inoculation. The occurrence of first developmental stages of C. muris in stomach was detected at 2·5 days post-infection (dpi). The presence of Type II merogony, appearing 36 h later than Type I merogony, was confirmed in both rodents. Oocysts exhibiting different size and thickness of their wall were observed from 5 dpi onwards in stomachs of both host models. The early phase of parasitization in BALB/c mice progressed rapidly, with a prepatent period of 7·5–10 days; whereas in M. coucha, the developmental stages of C. muris were first observed 12 h later in comparison with BALB/c mice and prepatent period was longer (18–21 days). Similarly, the patent periods of BALB/c mice and M. coucha differed considerably, i.e. 10–15 days vs chronic infection throughout the life of the host, respectively.

Keywords

cryptosporidiadevelopmentgastricoocystpathologyType II merogony
Type
Research Article
Information
Parasitology , Volume 141 , Issue 2 , February 2014 , pp. 287 - 303
Check for updates
Copyright
Copyright © Cambridge University Press 2013 

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. and Sterling, C. R. (1987). Isolation of Cryptosporidium oocysts and sporozoites using discontinuous sucrose and isopycnic Percoll gradients. Journal of Parasitology 73, 314–319.Google Scholar
Aydin, Y. (1999). The ultrastructure of the parasite and the mucus cell relationship and endogenous stages of Cryptosporidium muris in the stomach of laboratory mice. Turkish Journal of Veterinary and Animal Sciences 23, 117–125.Google Scholar
Aydin, Y. and Ozkul, I. A. (1996). Infectivity of Cryptosporidium muris directly isolated from the murine stomach for various laboratory animals. Veterinary Parasitology 66, 257–262.Google Scholar
Barta, J. R. and Thompson, R. C. (2006). What is Cryptosporidium? Reappraising its biology and phylogenetic affinities. Trends in Parasitology 22, 463–468.Google Scholar
Blackman, M. J. and Bannister, L. H. (2001). Apical organelles of Apicomplexa: biology and isolation by subcellular fractionation. Molecular and Biochemical Parasitology 117, 11–25. doi: 10.1016/S0166-6851(01)00328-0.Google Scholar
Bonnin, A., Gut, J., Dubremetz, J. F., Nelson, R. G. and Camerlynck, P. (1995). Monoclonal antibodies identify a subset of dense granules in Cryptosporidium parvum zoites and gamonts. Journal of Eukaryotic Microbiology 42, 395–401.Google Scholar
Borowski, H., Thompson, R. C., Armstrong, T. and Clode, P. L. (2010). Morphological characterization of Cryptosporidium parvum life-cycle stages in an in vitro model system. Parasitology 137, 13–26. doi: 10.1017/s0031182009990837.Google Scholar
Chappell, C. L., Okhuysen, P. C., Sterling, C. R., Wang, C., Jakubowski, W. and Dupont, H. L. (1999). Infectivity of Cryptosporidium parvum in healthy adults with pre-existing anti-C. parvum serum immunoglobulin G. American Journal of Tropical Medicine and Hygiene 60, 157–164.Google Scholar
Current, W. L. and Bick, P. H. (1989). Immunobiology of Cryptosporidium spp. Pathology and Immunopathology Research 8, 141–160.Google Scholar
Current, W. L. and Reese, N. C. (1986). A comparison of endogenous development of three isolates of Cryptosporidium in suckling mice. Journal of Protozoology 33, 98–108.Google Scholar
Current, W. L., Upton, S. J. and Haynes, T. B. (1986). The life cycle of Cryptosporidium baileyi n. sp. (Apicomplexa, Cryptosporidiidae) infecting chickens. Journal of Protozoology 33, 289–296.Google Scholar
Dubremetz, J. F., Garcia-Reguet, N., Conseil, V. and Fourmaux, M. N. (1998). Apical organelles and host-cell invasion by Apicomplexa. International Journal for Parasitology 28, 1007–1013. doi: 10.1016/s0020-7519(98)00076-9.Google Scholar
Fayer, R. and Santin, M. (2009). Cryptosporidium xiaoi n. sp. (Apicomplexa: Cryptosporidiidae) in sheep (Ovis aries). Veterinary Parasitology 164, 192–200.Google Scholar
Gatei, W., Ashford, R. W., Beeching, N. J., Kamwati, S. K., Greensill, J. and Hart, C. A. (2002). Cryptosporidium muris infection in an HIV-infected adult, Kenya. Emerging Infectious Diseases 8, 204–206.Google Scholar
Ghoshal, N. G. and Bal, H. S. (1989). Comparative morphology of the stomach of some laboratory mammals. Laboratory Animals 23, 21–29.Google Scholar
Guyot, K., Follet-Dumoulin, A., Lelievre, E., Sarfati, C., Rabodonirina, M., Nevez, G., Cailliez, J. C., Camus, D. and Dei-Cas, E. (2001). Molecular characterization of Cryptosporidium isolates obtained from humans in France. Journal of Clinical Microbiology 39, 3472–3480.Google Scholar
Hijjawi, N. S., Meloni, B. P., Morgan, U. M. and Thompson, R. C. (2001). Complete development and long-term maintenance of Cryptosporidium parvum human and cattle genotypes in cell culture. International Journal for Parasitology 31, 1048–1055.Google Scholar
Hijjawi, N., Estcourt, A., Yang, R., Monis, P. and Ryan, U. (2010). Complete development and multiplication of Cryptosporidium hominis in cell-free culture. Veterinary Parasitology 169, 29–36.Google Scholar
Huang, B. Q., Chen, X. M. and LaRusso, N. F. (2004). Cryptosporidium parvum attachment to and internalization by human biliary epithelia in vitro: a morphologic study. Journal of Parasitology 90, 212–221.Google Scholar
Hůrková, L., Hajdúšek, O. and Modrý, D. (2003). Natural infection of Cryptosporidium muris (Apicomplexa: Cryptosporiidae) in Siberian chipmunks. Journal of Wildlife Diseases 39, 441–444.Google Scholar
Jalovecká, M., Sak, B., Kváč, M., Květoňová, D., Kučerová, Z. and Salát, J. (2010). Activation of protective cell-mediated immune response in gastric mucosa during Cryptosporidium muris infection and re-infection in immunocompetent mice. Parasitology Research 106, 1159–1166.Google Scholar
Jiang, J., Alderisio, K. A. and Xiao, L. (2005). Distribution of Cryptosporidium genotypes in storm event water samples from three watersheds in New York. Applied and Environmental Microbiology 71, 4446–4454.Google Scholar
Jirků, M., Valigurová, A., Koudela, B., Křížek, J., Modrý, D. and Šlapeta, J. (2008). New species of Cryptosporidium Tyzzer, 1907 (Apicomplexa) from amphibian host: morphology, biology and phylogeny. Folia Parasitologica 55, 81–94.Google Scholar
Katsumata, T., Hosea, D., Ranuh, I. G., Uga, S., Yanagi, T. and Kohno, S. (2000). Short report: possible Cryptosporidium muris infection in humans. American Journal of Tropical Medicine and Hygiene 62, 70–72.Google Scholar
Kilani, R. T. and Sekla, L. (1987). Purification of Cryptosporidium oocysts and sporozoites by cesium chloride and Percoll gradients. American Journal of Tropical Medicine and Hygiene 36, 505–508.Google Scholar
Kodádková, A., Kváč, M., Ditrich, O., Sak, B. and Xiao, L. (2010). Cryptosporidium muris in a reticulated giraffe (Giraffa camelopardalis reticulata). Journal of Parasitology 96, 211–212.Google Scholar
Kváč, M. and Vítovec, J. (2003). Prevalence and pathogenicity of Cryptosporidium andersoni in one herd of beef cattle. Journal of Medicine Series B–Infection Diseases and Veterinary Public Health 50, 451–457.Google Scholar
Kváč, M., Sak, B., Květoňová, D., Ditrich, O., Hofmannová, L., Modrý, D., Vítovec, J. and Xiao, L. (2008). Infectivity, pathogenicity, and genetic characteristics of mammalian gastric Cryptosporidium spp. in domestic ruminants. Veterinary Parasitology 153, 363–367.Google Scholar
Kváč, M., Kodádková, A., Sak, B., Květoňová, D., Jalovecká, M., Rost, M. and Salát, J. (2011). Activated CD8+ T cells contribute to clearance of gastric Cryptosporidium muris infections. Parasite Immunology 33, 210–216.Google Scholar
Lumb, R., Smith, K., O'Donoghue, P. J. and Lanser, J. A. (1988). Ultrastructure of the attachment of Cryptosporidium sporozoites to tissue culture cells. Parasitology Research 74, 531–536.Google Scholar
Lupo, P. J., Langer-Curry, R. C., Robinson, M., Okhuysen, P. C. and Chappell, C. L. (2008). Cryptosporidium muris in a Texas canine population. American Journal of Tropical Medicine and Hygiene 78, 917–921.Google Scholar
Matsubayashi, M., Ando, H., Kimata, I., Nakagawa, H., Furuya, M., Tani, H. and Sasai, K. (2010). Morphological changes and viability of Cryptosporidium parvum sporozoites after excystation in cell-free culture media. Parasitology 137, 1861–1866.Google Scholar
Matsubayashi, M., Ando, H., Kimata, I., Takase, H., Nakagawa, H., Furuya, M., Tani, H. and Sasai, K. (2011). Effect of low pH on the morphology and viability of Cryptosporidium andersoni sporozoites and histopathology in the stomachs of infected mice. International Journal for Parasitology 41, 287–292. doi: 10.1016/j.ijpara.2010.09.009.Google Scholar
McConnell, E. L., Basit, A. W. and Murdan, S. (2008). Measurements of rat and mouse gastrointestinal pH, fluid and lymphoid tissue, and implications for in-vivo experiments. Journal of Pharmacy and Pharmacology 60, 63–70.Google Scholar
McDonald, V., Deer, R., Uni, S., Iseki, M. and Bancroft, G. J. (1992). Immune responses to Cryptosporidium muris and Cryptosporidium parvum in adult immunocompetent or immunocompromised (nude and SCID) mice. Infection and Immunity 60, 3325–3331.Google Scholar
McDonald, V., McCrossan, M. V. and Petry, F. (1995). Localization of parasite antigens in Cryptosporidium parvum-infected epithelial cells using monoclonal antibodies. Parasitology 110, 259–268.Google Scholar
McDonald, V., Robinson, H. A., Kelly, J. P. and Bancroft, G. J. (1996). Immunity to Cryptosporidium muris infection in mice is expressed through gut CD4+ intraepithelial lymphocytes. Infection and Immunity 64, 2556–2562.Google Scholar
McLauchlin, J. and Nichols, G. (2002). Microbiology and the investigation of waterborne outbreaks. In Drinking Water and Infectious Disease (ed. McLauchlin, J. and Nichols, G.), pp. 87–96. CRC Press, Boca Raton, FL, USA.Google Scholar
Miláček, P. and Vítovec, J. (1985). Differential staining of cryptosporidia by aniline-carbol-methyl violet and tartrazine in smears from feces and scrapings of intestinal mucosa. Folia Parasitologica 32, 50.Google Scholar
Miller, T. A. and Schaefer, F. W. III (2007). Characterization of a Cryptosporidium muris infection and reinfection in CF-1 mice. Veterinary Parasitology 144, 208–221.Google Scholar
O'Hara, S. P., Yu, J. R. and Lin, J. J. (2004). A novel Cryptosporidium parvum antigen, CP2, preferentially associates with membranous structures. Parasitology Research 92, 317–327.Google Scholar
O'Hara, S. P., Huang, B. Q., Chen, X. M., Nelson, J. and LaRusso, N. F. (2005). Distribution of Cryptosporidium parvum sporozoite apical organelles during attachment to and internalization by cultured biliary epithelial cells. Journal of Parasitology 91, 995–999.Google Scholar
Ozkul, I. A. and Aydin, Y. (1994). Natural Cryptosporidium muris infection of the stomach in laboratory mice. Veterinary Parasitology 55, 129–132.Google Scholar
Palmer, C. J., Xiao, L., Terashima, A., Guerra, H., Gotuzzo, E., Saldias, G., Bonilla, J. A., Zhou, L., Lindquist, A. and Upton, S. J. (2003). Cryptosporidium muris, a rodent pathogen, recovered from a human in Peru. Emerging Infectious Diseases 9, 1174–1176.Google Scholar
Pavlásek, I. and Ryan, U. (2007). The first finding of a natural infection of Cryptosporidium muris in a cat. Veterinary Parasitology 144, 349–352.Google Scholar
Petry, F. (2004). Structural analysis of Cryptosporidium parvum . Microscopy and Microanalysis 10, 586–601.Google Scholar
Petry, F. and Harris, J. R. (1999). Ultrastructure, fractionation and biochemical analysis of Cryptosporidium parvum sporozoites. International Journal for Parasitology 29, 1249–1260.Google Scholar
Robert, B., Antoine, H., Dreze, F., Coppe, P. and 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. Veterinary Research 25, 384–398.Google Scholar
Sauch, J. F., Flanigan, D., Galvin, M. L., Berman, D. and Jakubowski, W. (1991). Propidium iodide as an indicator of Giardia cyst viability. Applied and Environmental Microbiology 57, 3243–3247.Google Scholar
Tarazona, R., Blewett, D. A. and Carmona, M. D. (1998). Cryptosporidium parvum infection in experimentally infected mice: infection dynamics and effect of immunosuppression. Folia Parasitologica 45, 101–107.Google Scholar
Taylor, M. A., Marshall, R. N., Green, J. A. and Catchpole, J. (1999). The pathogenesis of experimental infections of Cryptosporidium muris (strain RN 66) in outbred nude mice. Veterinary Parasitology 86, 41–48.Google Scholar
Tetley, L., Brown, S. M., McDonald, V. and Coombs, G. H. (1998). Ultrastructural analysis of the sporozoite of Cryptosporidium parvum . Microbiology 144, 3249–3255.Google Scholar
Tiangtip, R. and Jongwutiwes, S. (2002). Molecular analysis of Cryptosporidium species isolated from HIV-infected patients in Thailand. Tropical Medicine & International Health 7, 357–364.Google Scholar
Tyzzer, E. E. (1907). A sporozoan found in the peptic glands of the common mouse. Proceedings of the Society for Experimental Biology and Medicine 5, 12–13. doi: 10.3181/00379727-5-5 Google Scholar
Tyzzer, E. E. (1910). An extracellular Coccidium, Cryptosporidium muris (Gen. Et Sp. Nov.), of the gastric glands of the common mouse. Journal of Medical Research 23, 487–510.Google Scholar
Uni, S., Iseki, M., Maekawa, T., Moriya, K. and Takada, S. (1987). Ultrastructure of Cryptosporidium muris (strain RN 66) parasitizing the murine stomach. Parasitology Research 74, 123–132.Google Scholar
Valigurová, A., Hofmannová, L., Koudela, B. and Vávra, J. (2007). An ultrastructural comparison of the attachment sites between Gregarina steini and Cryptosporidium muris . Journal of Eukaryotic Microbiology 54, 495–510. doi: 10.1111/j.1550-7408.2007.00291.x.Google Scholar
Valigurová, A., Jirků, M., Koudela, B., Gelnar, M., Modrý, D. and Šlapeta, J. (2008). Cryptosporidia: epicellular parasites embraced by the host cell membrane. International Journal for Parasitology 38, 913–922. doi: 10.1016/j.ijpara.2007.11.003.Google Scholar
Vetterling, J. M., Takeuchi, A. and Madden, P. A. (1971). Ultrastructure of Cryptosporidium wrairi from the guinea pig. Journal of Protozoology 18, 248–260.Google Scholar
Ward, F. W. and Coates, M. E. (1987). Gastrointestinal pH measurement in rats: influence of the microbial flora, diet and fasting. Laboratory Animals 21, 216–222.Google Scholar
Xiao, L., Escalante, L., Yang, C., Sulaiman, I., Escalante, A. A., Montali, R. J., Fayer, R. and Lal, A. A. (1999). Phylogenetic analysis of Cryptosporidium parasites based on the small-subunit rRNA gene locus. Applied and Environmental Microbiology 65, 1578–1583.Google Scholar