Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-24T08:24:29.222Z Has data issue: false hasContentIssue false
  • English
  • Français

Changes in lipophosphoglycan and gene expression associated with the development of Leishmania major in Phlebotomus papatasi

Published online by Cambridge University Press:  06 April 2009

E. M. B. Saraiva ,
P. F. P. Pimenta ,
T. N. Brodin ,
E. Rowton ,
G. B. Modi  and
D. L. Sacks
E. M. B. Saraiva
Affiliation:
Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892
P. F. P. Pimenta
Affiliation:
Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892
T. N. Brodin
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, DC 20307
G. B. Modi
Affiliation:
Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892
D. L. Sacks
Affiliation:
Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892
Get access Rights & Permissions [Opens in a new window]

Summary

Stage-specific molecular and morphogenic markers were used to follow the kinetics of appearance, number, and position of metacyclic promastigotes developing during the course of L. major infection in a natural vector, Phlebotomus papatasi. Expression of surface lipophosphoglycan (LPG) on transformed promastigotes was delayed until the appearance of nectomonad forms on day 3, and continued to be abundantly expressed by all promastigotes thereafter. An epitope associate with arabinose substitution of LPG side-chain oligosaccharides, identified by its differential expression by metacyclics in vitro, was detected on the surface of a low proportion of midgut promastigotes beginning on day 5, and on up to 60% of promatigotes on days 10 and 15. In contrast 100% of the parasites egested from the mouthparts during forced feeding of 15 day infected flies stained strongly for this epitope. At each time-point, the surface expression of the modified LPG was restricted to morphologically distinguished metacyclic forms. Ultrastructural study of the metacyclic surface revealed an approximate 2-fold increase in the thickness of the surface coat compared to nectomonad forms, suggesting elongation of LPG as occurs during metacyclogenesis in vitro. A metacyclic-associated transcript (MAT-1), another marker identified by its differential expression in vitro, also showed selective expression by promastigotes in the fly, and was used in in situ hybridization studies to demonstrate the positioning of metacyclics in the anterior gut.

Keywords

Leishmaniasand flymetacycliclipophosphoglycan
Type
Research Article
Information
Parasitology , Volume 111 , Issue 3 , September 1995 , pp. 275 - 287
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

Bates, P. A. (1994). Complete development cycle of Leishtnania Mexicana in axenic culture Parasitology 108, 1–9.CrossRefGoogle ScholarPubMed
Brodin, T. N., Heath, S. & Sacks, D. L. (1992). Genes selectively expressed in the infectious (metacyclic) stage of L. major promastigotes encode a potential basic-zipper structural motif. Molecular and Biochemical Parasitology 52, 241–50.Google Scholar
Da Silva, R. P. & Sacks, D. L. (1987). Metacyclogcnesis is a major determinant of Leishmania promastigote virulence and attenuation. Infection and Immunity 55, 2802–7.CrossRefGoogle Scholar
Davies, C. R., Cooper, A. M., Peacock, C., Lane, R. P. & Blackwell, J. M. (1990). Expression of LPG and GP63 by different developmental stages of L. major in the sandfly Phlebotomus papatasi. Parasitology 101, 337–43.CrossRefGoogle ScholarPubMed
De Ibarra, A. A., Howard, J. D. & Snary, D. (1982). Monoclonal antibodies to L. tropica major: specificities and antigen location. Parasitology 85, 523–31.CrossRefGoogle Scholar
Dillon, R. J. & Lane, R. P. (1993). Influence of Leishmania infection on blood-meal digestion in the sandflies Phlebotomus papatasi and P. langeroni. Parasitology Research 79, 492–6.Google Scholar
Howard, M. K., Sayers, G. & Miles, M. A. (1987). L. donovani metacyclic promastigotes: transformation in vitro, lectin agglutination, complement resistance and infectivity. Experimental Parasitology 64, 147–56.CrossRefGoogle Scholar
Jordon, C. A. (1990). In situ hybridization in cells and tissue sections. In In Situ Hybridization Histochemistry, (ed. Chessele, M. F.), pp. 39–70. Boca Raton, FL: CRC Press.Google Scholar
Kelleher, M., Curtis, J. M., Sacks, D. L., Handman, E. & Bacic, A. (1994). Epitope mapping of monoclonal antibodies directed against lipophosphoglycan of Leishmania major promastigotes. Molecular and Biochemical Parasitology 66, 187–200.Google Scholar
Kotler, D. P., Wilson, C. S., Haroutiounian, G. & Fox, c. H. (1989). Detection of human immunodeficiency virus-1 by 35S-RNA by in situ hybridization on solitary esophageal ulcers in two patients with acquired immunodeficiency syndrome. American Journal of Gastroenterology 84, 313–17.Google Scholar
Lang, T., Warburg, A., Sacks, D. L., Croft, S. L., Lane, R. P. & Blackwell, J. M. (1991). Transmission and scanning EM-immunogold labelling 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 L. major in Phlebotomus duboscqui and Sergentomyia schwetzi. American Journal of Tropical Medicine and Hygiene 43, 31–43.CrossRefGoogle Scholar
McConville, M., Turco, S. J., Ferguson, M. A. & Sacks, D. L. (1992). Developmental modification of lipophosphoglycan during the differentiation of L. 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. I, (ed. Peters, W. & Killick-Kendrick, R.), pp. 121–175. London: Academic Press.Google Scholar
Pimenta, P. F. P. & De Souza, W. (1985). Fine structure and cytochemistry of the endoplasmic reticulum and its association with the plasma membrane of L. mexicana amazonensis. Journal of Submicroscopic Cytology 17, 413–19.Google Scholar
Pimenta, P., Da Silva, R., Sacks, D. L. & Da Silva, P. (1989). Cell surface nanonanatomy of Leishmania major as revealed by fracture-flip. A surface meshwork of 44 nm fusiform filaments identifies infective developmental stage promastigotes. European Journal of Cell Biology 48, 180–7.Google ScholarPubMed
Pimenta, P., Turco, S. J., McConville, M. J., Lawyer, P. G., Perkins, P. V. & Sacks, D. L. (1992). Stage-specific adhesion of Leishmania promastigotes to the sandfly midgut. Science 256, 1812–15.Google Scholar
Puentes, S. M., Sacks, D. L., Da Silva, R. P. & Joiner, K. A. (1988). Complement binding by two developmental stages of L. major promastigotes varying in expression of a surface lipophosphoglycan. Journal of Experimental Medicine 167, 887–902.CrossRefGoogle Scholar
Puentes, S. M., Da Silva, R. P., Sacks, D. L., Hammer, C. H. & Joiner, K. A. (1991). Serum resistance of metacyclic stage L. major promastigotes is due to release of C5b–9. Journal of Immunology 145, 4311–16.CrossRefGoogle Scholar
Sacks, D. L. (1992). The structure and function of the surface lipophosphoglycan on different developmental stages of Leishmania promastigotes. Infectious Agents and Disease 1, 200–5.Google Scholar
Sacks, D. L., Brodin, T. N. & Turco, S. J. (1990). Developmental modification of the lipophosphoglycan from L. major promastigotes during metacyclogenesis. Molecular and Biochemical Parasitology 42, 225–32.Google Scholar
Sacks, D. L. & Da Silva, R. p. (1987). The generation of infective stage L. major promastigotes is associated with the cell surface expression and release of a developmcntally regulated glycolipid. Journal of Immunology 139, 3099–106.CrossRefGoogle Scholar
Saraiva, E. M. B., Pimenta, P. F. P., Pereira, M. E. A. & De Souza, W. (1983). Isolation and purification of amastigotes of L. mexicana amazonensis by a gradient of metrizamide. Journal of Parasitology 79, 627–9.Google Scholar
Walters, L. L., Modi, G. B., Chaplin, G. L. & Tesh, R. B. (1989). Ultrastructural development of L. chagasi in its vector, Lutzomyia longipalpis. American Journal of Tropical Medicine and Hygiene 41, 295–317.CrossRefGoogle Scholar
Warburg, A., Hamada, G. S., Schlein, Y. & Shire, D. (1986). Scanning electron microscopy of L. major in P. papatasi. Zeitschrift für Parasitenkunde 72, 423–31.Google Scholar
Warburg, A. & Schlein, Y. (1986). The effect of post-bloodmeal nutrition of Phlebotumus papatasi on the transmission of Leishmania major. American Journal of Tropical Medicine and Hygiene 35, 926–30.CrossRefGoogle Scholar