Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-10T11:39:12.092Z Has data issue: false hasContentIssue false

Differential development and emission of Theileria parva sporozoites from the salivary gland of Rhipicephalus appendiculatus

Published online by Cambridge University Press:  06 April 2009

M. K. Shaw
Affiliation:
International Laboratory for Research on Animal Diseases, P.O. Box 30709, Nairobi, Kenya
A. S. Young
Affiliation:
International Laboratory for Research on Animal Diseases, P.O. Box 30709, Nairobi, Kenya

Summary

The initiation of feeding of infected Rhipicephalus appendiculatus adults induces the rapid development of Theileria parva sporoblasts within the salivary gland acini leading to the production of numerous sporozoites which are inoculated into the mammalian host initiating infection. In this study the pattern of development, host cell specificity and emission of T. parva sporozoites within the salivary glands of heavily infected, 4-day fed adult R. appendiculatus ticks was examined. Infected acini were randomly distributed throughout the salivary gland. Sporozoite development within each gland was not synchronized and wide variation in the rate of parasite development, which correlated with the secretory activity of the individual acinus, was observed in all glands examined. Previous studies had shown that T. parva developed primarily in Type III ‘e’ cells. However, in heavily infected salivary glands sporogony and the emission of mature sporozoites also occurred in ‘c’ cells of Type II acini. Sporozoite emission from infected cells occurred by a process similar to apocrine secretion. The loss of the apical membrane of the infected cell allowed sporozoites free access to the lumen of the acinus and into the collecting ducts of the salivary gland. Sporozoite discharge was gradual since few parasites were found in the acinus valve or in the collecting ducts. Furthermore, the small size of the acinar valve aperature ensures that only small numbers of sporozoites can be released at any one time from an infected acinus.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1995

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

Bell, L. J. (1980). Organ culture of Rhipicephalus appendiculatus with maturation of Theileria parva in the tick salivary glands in vitro. Acta Tropica 37, 319–25.Google ScholarPubMed
Binnington, K. C. & Kemp, D. H. (1980). Role of tick salivary glands in feeding and disease transmission. Advances in Parasitology 18, 315–39.Google Scholar
Binnington, K. C., Young, A. S. & Obenchain, F. D. (1983). Morphology of normal and Theileria parva infected salivary glands of Rhipicephalus appendiculatus. Journal of Parasitology 69, 421–4.Google Scholar
Dobbelaere, D. A. E., Spooner, P. R., Barry, W. C. & Irvin, A. D. (1984). Monoclonal antibody neutralizes the sporozoite stage of different Theileria parva stocks. Parasite Immunology 6, 361–70.Google Scholar
Fawcett, D. W., Buscher, G. & Doxsey, S. (1982 a). Salivary gland of the tick vector of East Coast fever. III. The ultrastructure of the sporogony of Theileria parva. Tissue and Cell 14, 183206.Google Scholar
Fawcett, D. W., Buscher, G. & Doxsey, S. (1982 b). Salivary gland of tick vector of East Coast fever. IV. Cell type selectivity and host cell responses to Theileria parva. Tissue and Cell 14, 397414.CrossRefGoogle ScholarPubMed
Fawcett, D. W., Binnington, K. & V'oigt, W. P. (1986). The cell biology of the ixodid tick salivary gland. In Morphology, Physiology and Behavioral Biology of Ticks (ed. Sauer, J. R. & Hair, J. A.), pp. 2245. Chichester: Ellis Horwood.Google Scholar
Fawcett, D. W., Young, A. S. & Leitch, B. L. (1985). Sporogony in Theileria [Apicomplexa: Piroplasmida]. A comparative ultrastructural study. Journal of Submicroscopic Cytology 17, 299314.Google Scholar
Jarrett, W. F. H., Crighton, G. W. & Crighton, G. W. (1969). Theileria parva: kinetics of replication. Experimental Parasitology 24, 925.CrossRefGoogle ScholarPubMed
Joyner, L. P., Cunningham, M. P., Purnell, R. E. & Brown, C. G. D. (1972). The duration of emission of infective particles of Theileria parva by infected ticks fed artificially. Research in Veterinary Science 13, 402–3.CrossRefGoogle ScholarPubMed
Medley, G. F., Perry, B. D. & Young, A. S. (1993). Preliminary analysis of the transmission dynamics of Theileria parva in eastern Africa. Parasitology 106, 251–64.Google Scholar
Mehlhorn, H. & Schein, E. (1984). The piroplasms: life cycle and sexual stages. Advances in Parasitology 23, 37103.Google Scholar
Musoke, A. J., Morzaria, S. P., Nkonge, C., Jones, E. & Nene, V. (1992). A recombinant sporozoite surface antigen of Theileria parva induces protection in cattle. Proceedings of the National Academy of Sciences, USA 89, 514–18.Google Scholar
Musoke, A. J., Nantulya, V. M., Rurangirwa, F. R. & Buscher, G. (1984). Evidence for a common protective antigenic determinant on sporozoites of several Theileria parva strains. Immunology 52, 231–8.Google Scholar
Musoke, A. J., Nene, V. & Morzaria, S. P. (1993). A sporozoite-based vaccine for Theileria parva. Parasitology Today 9, 385–8.Google Scholar
Purnell, R. E. & Joyner, L. P. (1968). The development of Theileria parva in the salivary glands of the tick, Rhipicephalus appendiculatus. Parasitology 58, 725–32.CrossRefGoogle ScholarPubMed
Radley, D. E., Brown, C. G. D., Burridge, M. J., Cunningham, M. P., Pierce, M. A. & Purnell, R. E. (1974). East Coast fever: quantitative studies of Theileria parva in cattle. Experimental Parasitology 36, 278–87.Google Scholar
Shaw, M. K., Tilney, L. G. & McKeever, D. J. (1993). Tick salivary gland extract and interleukin-2 stimulation enhance susceptibility of lymphocytes to infection by Theileria parva sporozoites. Infection and Immunity 61, 1486–95.Google Scholar
Shaw, M. K. & Young, A. S. (1994). The biology of Theileria species in ixodid ticks in relation to parasite transmission. Advances in Disease Vector Research 10, 2363.Google Scholar
Sonenshine, D. E. (1991). Biology of Ticks, Vol. 1. Oxford and New York: Oxford University Press.Google Scholar
Sonenshine, D. E. (1993). Biology of Ticks, Vol. 2. Oxford and New York: Oxford University Press.Google Scholar
Walker, A. R. (1990). Parasitic adaptations in the transmission of Theileria by ticks, a review. Tropical Animal Health Production 22, 2333.Google Scholar
Walker, A. R. & Fletcher, J. D. (1986). Histological study of the attachment site of adult Rhipicephalus appendiculatus on rabbits and cattle. International Journal for Parasitology 16, 399413.Google Scholar
Young, A. S., Dolan, T. T., Mwakima, F. N., Mwaura, S. N., Njihia, G. M., Muthoni, M. W. & Dolan, R. B. (1995). Estimation of heritability of susceptibility to infection with Theileria parva of the tick Rhipicephalus appendiculatus. Parasitology 111, 000–000.CrossRefGoogle ScholarPubMed
Young, A. S. & Morzaria, S. P. (1986). Biology of Babesia. Parasitology Today 2, 211–19.Google Scholar