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The role of the lipophosphoglycan of Leishmania in vector competence

Published online by Cambridge University Press:  06 April 2009

D. L. Sacks ,
E. M. Saraiva ,
E. Rowton ,
S. J. Turco  and
P. F. Pimenta
D. L. Sacks
Affiliation:
Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892
E. M. Saraiva
Affiliation:
Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892
E. Rowton
Affiliation:
Department of Entomology, Walter Reed Army Institute of Research, Washington, D.C. 20307
S. J. Turco
Affiliation:
Department of Biochemistry, University of Kentucky Medical Center, Lexington, KY 40536
P. F. Pimenta
Affiliation:
Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892
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Summary

The surface lipophosphoglycans (LPG) of Leishmania promastigotes express stage- and species-specific polymorphisms that are defined by variations in the type and number of phosphorylated oligosaccharide repeats. We have studied how these polymorphic structures control the development of transmissible infections in the sandfly vector as well as the species-specificity of vectorial competence. Procyclic promastigotes displayed an inherent capacity to bind to midgut epithelial cells of a competent vector. This capacity was lost during their transformation to metacyclic promastigotes, permitting the selective release and anterior migration of infective-stage parasites for subsequent transmission by bite. Midgut attachment and release were found to be controlled by developmental modifications in terminally exposed saccharides on LPG, which, depending on the species of Leishmania, involved either substitution or capping of terminal side-chain sugars, loss of terminal side-chain sugars, substitution or loss of neutral capping sugars. The stage-specific terminal sugars involved in midgut adhesion are, in some cases, also species-specific, and the extent to which these differences affect midgut attachment, forcefully predicted vectorial competence.

Keywords

Leishmanialipophosphoglycansandfliesvector competence.
Type
Research Article
Information
Parasitology , Volume 108 , supplement S1: Symposia of the British Society for Parasitology Volume 31:Functional molecules on the surface of protozoan parasites , March 1994 , pp. S55 - S62
Copyright
Copyright © Cambridge University Press 1994

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References

REFERENCES

Adler, S. & Theodor, O. (1927). The transmission of Leishmania tropica from artificially infected sandflies to man. Annals of Tropical Medicine and Parasitology 21, 89–111.CrossRefGoogle Scholar
Adler, S. & Theodor, O. (1930). The exit of Leishmania infantum from the proboscis of Phlebotomus perniciosus. Nature 126, 883.CrossRefGoogle Scholar
Adler, S., Theodor, O. & Wittenberg, G. (1938). Investigations on Mediterranean kala-azar. XI. A study of leishmaniasis on Canea (Crete). Proceedings of the Royal Society, London, B 125, 491–516.Google Scholar
Adler, S. & Ber, M. (1941). The transmission of Leishmania tropica by the bite of Phlebotomus papatasi. Indian Journal of Medical Research 29, 803–9.Google Scholar
Borovsky, D. & Schlein, Y. (1987). Trypsin and chymotrypsin-like enzymes of the sandfly Phlebotomus papatasi infected with Leishmania and their possible role in vector competence. Medical and Veterinary Entomology 1, 235—42.CrossRefGoogle ScholarPubMed
Coelho, M., Falcao, A. R. & Falcao, A. M. (1967). Desenvolvimento de especies do genero Leishmania em especies brasilieiras de Phlebotomos do genero Lutzo myia Franca 1924. Revista do Institute de Medicina Tropical do Sao Paulo 9, 192–6.Google Scholar
da Silva, R. P., Hall, B. F., Joiner, K. A. & Sacks, D. L. (1989). CR1, the C3b receptor, mediates binding of infective Leishmania major metacyclic promastigotes to human macrophages. Journal of Immunology 43, 617–22.CrossRefGoogle Scholar
Davies, C., Cooper, A., Peacock, C., Lane, R. & Blackwell, J. (1990). Expression of LPG and GP63 by different developmental stages of Leishmania major in the sandfly Phlebotomus papatasi. Parasitology 101, 337–43.CrossRefGoogle ScholarPubMed
Grimm, F. & Jenni, L. (1993). Human serum resistant promastigotes of Leishmania infantum in the midgut of Phlebotomus perniciosus. Acta Tropica 52, 267–73.CrossRefGoogle ScholarPubMed
Handman, E. & Coding, J. W. (1985). The Leishmania receptor for macrophages is a lipid containing glycoconjugate. The EMBO Journal 4, 329–36.CrossRefGoogle ScholarPubMed
Heyneman, D. (1963). Leishmaniasis in the Sudan Republic. Comparison of experimental Leishmania donovani infections in Phlebotomus papatasi with natural infections found in man-baited P. orientalis captured in a kala-azar endemic region of the Sudan. Proceedings of the Royal Society, London, B 199, 309–20.Google Scholar
Howard, M. K., Sayers, G. & Miles, M. A. (1987). Leishmania donovani metacyclic promastigotes: transformation in vitro, lectin agglutination, complement resistance and infectivity. Experimental Parasitology 64, 147–56.CrossRefGoogle ScholarPubMed
Ilg, T., Etges, R., Overath, P., McConville, M., Thomas-Oates, J., Thomas, J., Homans, S. W. & Fergusen, M. A. (1992). Structure of Leishmania mexicana lipophosphoglycan. Journal of Biological Chemistry 267, 6834–40.CrossRefGoogle ScholarPubMed
Killick-Kendrick, R. (1979). Biology of Leishmania in phlebotomine sandflies. In Biology of Kinetoplastida, Vol 2 (ed. Lumsden, W. H. R. & Evans, D. A.), pp. 395–460. London: Academic Press.Google Scholar
Killick-Kendrick, R. (1985). Some epidemiological consequences of the evolutionary fit between leishmania and their phlebotomine vectors. Bulletin de la Société de Pathologie Exotique 78, 747–55.Google ScholarPubMed
Lang, T., Warburg, A., Sacks, D. L., Croft, S., Lane, R. P. & Blackwell, J. M. (1991). Transmission and scanning EM-immunogold labeling of Leishmania major lipophosphoglycan in the sandfly Phlebotomus papatasi. European Journal of Cell Biology 55, 362–72.Google ScholarPubMed
Lawyer, P. G., Ngumbi, P. M., Anjili, C. O., Odongo, S. O., Mebrahtu, Y. B., Githure, J. I., Koech, D. K. & Roberts, C. R. (1990). Development of Leishmania major in Phlebotomus duboscqui and Sergentomyia Schwetzi. American Journal of Tropical Medicine and Hygiene 43, 31–43.CrossRefGoogle Scholar
McConville, M. (1991). Glycosylated-phosphatidylinositols of the trypanosomatidae. In Biochemistry of Parasitic Protozoa (ed. Coombs, G.). London: Taylor and Francis Press.Google Scholar
McConville, M., Thomas-Oates, T., Fergusen, M. A. & Homans, S. W. (1990). Structure of the lipophosphoglycan from Leishmania major. Journal of Biological Chemistry 265, 19611–23.CrossRefGoogle ScholarPubMed
McConville, M., Turco, S. J., Ferguson, M. A. & Sacks, D. L. (1992). Developmental modification of lipophosphoglycan during the differentiation of Leishmania major promastigotes to an infectious stage. EMBO Journal 11, 3593–600.CrossRefGoogle Scholar
Molyneux, D. H. & Killick-Kendrick, R. (1987). Morphology, ultrastructure and life cycles. In The Leishmaniases in Biology and Medicine, Vol. 1 (ed. Peters, W. & Killick-Kendrick, R.), pp. 121–75. London: Academic Press.Google Scholar
Molyneux, D. H., Killick-Kendrick, R. & Ashford, R. W. (1975). Leishmania in phlebotomid sandflies: III. The ultrastructure of Leishmania mexicana amazonensis in the midgut and pharynx of Lutzomyia longipalpis. Proceedings of the Royal Society, London, B 190, 341–57.Google ScholarPubMed
Mosser, D. M. & Edelson, P. J. (1987). The third component of complement (C3) is responsible for the intracellular survival of Leishmania major. Nature 327, 329–31.CrossRefGoogle ScholarPubMed
Parrot, L. & Donatien, A. (1927). Le parasite du bouton d' Orient chez le phlebotomine. Infection naturelle et infection experimentale de Phlebotomus papatasi. Archives de l' Institut Pasteur d' Algérie 5, 9–21.Google Scholar
Pimenta, P. F. P., Saraiva, E. M. B. & Sacks, D. L. (1991).The comparative fine structure and surface glycoconjugate expression of three life stages of Leishmania major. Experimental Parasitology 72, 191–7.CrossRefGoogle ScholarPubMed
Pimenta, P., Turco, S., McConville, M., Lawyer, P.,Perkins, P. & Sacks, D. (1992). Stage-specific adhesion of Leishmania promastigotes to the sand fly midgut. Science 256, 1812–15.CrossRefGoogle Scholar
Puentes, S. M., Sacks, D. L., da Silva, R. P. & Joiner, K. A. (1988). Complement binding by two developmental stages of Leishmania major promastigotes varying in expression of a surface lipophosphoglycan. Journal of Experimental Medicine 167, 887–902.CrossRefGoogle ScholarPubMed
Puentes, S. M., da Silva, R. P., Sacks, D. L., Hammer, C. H. & Joiner, K. A. (1991). Serum resistance of metacyclic stage Leishmania major promastigotes is due to release of C5b–9. Journal of Immunology 145, 4311–16.CrossRefGoogle Scholar
Sacks, D. L. & Perkins, P. V. (1984). Identification of an infective stage of Leishmania promastigotes. Science 223, 1417.CrossRefGoogle ScholarPubMed
Sacks, D. L., Hieny, S. & Sher, A. (1984). Identification of cell surface carbohydrate and antigenic changes between noninfective and infective developmental stages of Leishmania major promastigotes. Journal of Immunology 135, 564—70.CrossRefGoogle Scholar
Sacks, D. L., da Silva, R. (1987). The generation of infective stage Leishmania major promastigotes is associated with the cell-surface expression and release of a developmentally regulated glycolipid. Journal of Immunology 139, 3099–106.CrossRefGoogle ScholarPubMed
Sacks, D. L. (1989). Metacyclogenesis in Leishmania promastigotes. Experimental Parasitology 69, 10–12.CrossRefGoogle ScholarPubMed
Sacks, D. L., Brodin, T. N. & Turco, S. J. (1990). Developmental modification of the lipophosphoglycan from Leishmania major promastigotes during metacyclogenesis. Molecular and Biochemical Parasitology 42, 225–32.CrossRefGoogle ScholarPubMed
Schlein, Y. & Romano, H. (1986). Leishmania major and Leishmania donovani: effects of proteolytic enzymes of Phlebotomus papatasi. Experimental Parasitology 62, 376–80.CrossRefGoogle ScholarPubMed
Schlein, Y., Schnur, L. F. & Jacobson, R. L. (1990). Release conjugate of indigenous Leishmania major enhances survival of a foreign L. major in Phlebotomus papatasi. Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 353–5.CrossRefGoogle Scholar
Schnur, L. F., Greenblatt, C. L. & Zuckerman, A. (1972). Leishmanial serotypes as distinguished by the gel diffusion of factors excreted in vitro and in vivo. Israel Journal of Medical Sciences 8, 932–47.Google ScholarPubMed
Shortt, H. E., Smith, R. O. A., Swaminath, C. S. & Krishnan, K. V. (1931). Transmission of Indian Kalaazar by the bite of Phlebotomus argetipes. Indian Journal of Medical Research 18, 1373–5.Google Scholar
Thomas, J. R.McConville, M., Thomas-Oates, J. E., Homans, S. W., Ferguson, M. A. J., Gorin, P. A. J., Greis, K. D. & Turco, S. J. (1992). Refined structure of the lipophosphoglycan of Leishmania donovani. Journal of Biological Chemistry 267, 6829–33.CrossRefGoogle ScholarPubMed
Turco, S. J. (1988). The lipophosphoglycan of Leishmania. Parasitology Today 4, 255–7.CrossRefGoogle ScholarPubMed
Wallbanks, K. R., Ingram, G. A., Molyneux, D. H. (1986). The agglutination of erythrocytes and Leishmania parasites by sandfly gut extracts: evidence for lectin activity. Tropical Medicine and Parasitology 37, 409–13.Google ScholarPubMed
Walters, L. L., Modi, G. B., Chaplin, G. L. & Tesh, R. B. (1989). Ultrastructural development of Leishmania chagasi in its vector, Lutzomiya longipalpis. American Journal of Tropical Medicine and Hygiene 41, 295–317.CrossRefGoogle Scholar
Warburg, A. & Schlein, Y. (1986). The effect of post- bloodmeal nutrition of Phlebotomus papatasi on the transmission of Leishmania major. American Journal of Tropical Medicine and Hygiene 35, 926–30.CrossRefGoogle ScholarPubMed