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The role of surface glycoconjugates in Leishmania midgut attachment examined by competitive binding assays and experimental development in sand flies

Published online by Cambridge University Press:  23 April 2013

LUCIE JECNA ,
ANNA DOSTALOVA ,
RAY WILSON ,
VERONIKA SEBLOVA ,
KWANG-POO CHANG ,
PAUL A. BATES  and
PETR VOLF
LUCIE JECNA
Affiliation:
Department of Parasitology, Faculty of Science, Charles University, Vinicna 7, 128 44 Prague 2, Czech Republic
ANNA DOSTALOVA
Affiliation:
Department of Parasitology, Faculty of Science, Charles University, Vinicna 7, 128 44 Prague 2, Czech Republic
RAY WILSON
Affiliation:
Centre for Immunity, Infection and Evolution, Institute for Immunology and Infection Research, School of Biological Sciences, University of Edinburgh, Edinburgh, UK
VERONIKA SEBLOVA
Affiliation:
Department of Parasitology, Faculty of Science, Charles University, Vinicna 7, 128 44 Prague 2, Czech Republic
KWANG-POO CHANG
Affiliation:
Department of Microbiology/Immunology, Chicago Medical School/Rosalind Franklin University, North Chicago, Illinois 60064, USA
PAUL A. BATES
Affiliation:
Division of Biomedical and Life Sciences, School of Health and Medicine, Lancaster University, Lancaster LA1 4YQ, UK
PETR VOLF*
Affiliation:
Department of Parasitology, Faculty of Science, Charles University, Vinicna 7, 128 44 Prague 2, Czech Republic
*
*Corresponding author. Department of Parasitology, Charles University, Vinicna 7, 12844 Prague 2, Czech Republic. E-mail: volf@cesnet.cz
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Summary

Binding of promastigotes to the sand fly midgut epithelium is regarded as an essential part of the Leishmania life cycle in the vector. Among Leishmania surface molecules putatively involved in attachment to the sand fly midgut, two GPI-anchored molecules are the most prominent: lipophosphoglycan (LPG) and promastigote surface protease gp63. In this work, we examined midgut attachment of Leishmania lines mutated in GPI-anchored molecules and compared results from 2 different techniques: in vivo development in sand flies and in vitro competitive binding assays using fluorescently labelled parasites. In combination with previous studies, our data provide additional support for (1) an LPG-independent parasite-binding mechanism of Leishmania major within the midgut of the permissive vector Phlebotomus perniciosus, and provide strong support for (2) the crucial role of L. major LPG in specific vector Phlebotomus papatasi, and (3) a role for Leishmania amazonensis gp63 in Lutzomyia longipalpis midgut binding. Moreover, our results suggest a critical role for GPI-anchored proteins and gp63 in Leishmania mexicana attachment to L. longipalpis midguts, as the wild type (WT) line accounted for over 99% of bound parasites.

Keywords

phlebotomine sand fliesLeishmanialipophosphoglycanzinc protease gp63
Type
Research Article
Information
Parasitology , Volume 140 , Issue 8 , July 2013 , pp. 1026 - 1032
Copyright
Copyright © Cambridge University Press 2013 

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References

REFERENCES

Bates, P. A. and Rogers, M. E. (2004). New insights into the developmental biology and transmission mechanisms of Leishmania. Current Molecular Medicine 4, 601–609.CrossRefGoogle ScholarPubMed
Brittingham, A., Morrison, C. J., McMaster, W. R., McGwire, B. S., Chang, K. P. and Mosser, D. M. (1995). Role of the Leishmania surface protease gp63 in complement fixation, cell adhesion, and resistance to complement-mediated lysis. Journal of Immunology 155, 3102–3111.CrossRefGoogle ScholarPubMed
Brooks, D. R., McCulloch, R., Coombs, G. H. and Mottram, J. C. (2000). Stable transformation of trypanosomatids through targeted chromosomal integration of the selectable marker gene encoding blasticidin S deaminase. FEMS Microbiology Letters 186, 287–291.CrossRefGoogle ScholarPubMed
Cihakova, J. and Volf, P. (1997). Development of different Leishmania major strains in the vector sandflies Phlebotomus papatasi and P. duboscqi. Annals of Tropical Medicine and Parasitology 91, 267–279.CrossRefGoogle ScholarPubMed
Chaudhuri, G., Chaudhuri, M., Pan, A. and Chang, K. P. (1989). Surface acid proteinase (gp63) of Leishmania mexicana. A metalloenzyme capable of protecting liposome-encapsulated proteins from phagolysosomal degradation by macrophages. Journal of Biological Chemistry 264, 7483–7489.CrossRefGoogle ScholarPubMed
Chen, D. Q., Kolli, B. K., Yadava, N., Lu, H. G., Gilman-Sachs, A., Peterson, D. A. and Chang, K. P. (2000). Episomal expression of specific sense and antisense mRNAs in Leishmania amazonensis: modulation of gp63 level in promastigotes and their infection of macrophages in vitro. Infection and Immunity 68, 80–86.CrossRefGoogle ScholarPubMed
Ferguson, M. A. (1994). What can GPI do for you? Parasitology Today 10, 48–52.CrossRefGoogle ScholarPubMed
Hajmova, M., Chang, K. P., Kolli, B. and Volf, P. (2004). Down-regulation of gp63 in Leishmania amazonensis reduces its early development in Lutzomyia longipalpis. Microbes and Infection 6, 646–649.CrossRefGoogle ScholarPubMed
Hilley, J. D., Zawadzki, J. L., McConville, M. J., Coombs, G. H. and Mottram, J. C. (2000). Leishmania mexicana mutants lacking glycosylphosphatidylinositol (GPI):protein transamidase provide insights into the biosynthesis and functions of GPI-anchored proteins. Molecular Biology of the Cell 11, 1183–1195.CrossRefGoogle ScholarPubMed
Ilg, T., Demar, M. and Harbecke, D. (2001). Phosphoglycan repeat-deficient Leishmania mexicana parasites remain infectious to macrophages and mice. Journal of Biological Chemistry 276, 4988–4997.CrossRefGoogle ScholarPubMed
Joshi, P. B., Sacks, D. L., Modi, G. and McMaster, W. R. (1998). Targeted gene deletion of Leishmania major genes encoding developmental stage-specific leishmanolysin (GP63). Molecular Microbiology 27, 519–530.CrossRefGoogle ScholarPubMed
Joshi, P. B., Kelly, B. L., Kamhawi, S., Sacks, D. L. and McMaster, W. R. (2002). Targeted gene deletion in Leishmania major identifies leishmanolysin (GP63) as a virulence factor. Molecular and Biochemical Parasitology 120, 33–40.CrossRefGoogle ScholarPubMed
Kamhawi, S. (2006). Phlebotomine sand flies and Leishmania parasites: friends or foes? Trends in Parasitology 22, 439–445.CrossRefGoogle ScholarPubMed
Kamhawi, S., Modi, G. B., Pimenta, P. F., Rowton, E. and Sacks, D. L. (2000). The vectorial competence of Phlebotomus sergenti is specific for Leishmania tropica and is controlled by species-specific, lipophosphoglycan-mediated midgut attachment. Parasitology 121, 25–33.CrossRefGoogle ScholarPubMed
Kamhawi, S., Ramalho-Ortigao, M., Pham, V. M., Kumar, S., Lawyer, P. G., Turco, S. J., Barillas-Mury, C., Sacks, D. L. and Valenzuela, J. G. (2004). Role for insect galectins in parasite survival. Cell 119, 329–341.CrossRefGoogle ScholarPubMed
Killick-Kendrick, R. (1999). The biology and control of Phlebotomine sand flies. Clinics in Dermatology 17, 279–289.CrossRefGoogle ScholarPubMed
Killick-Kendrick, R., Killick-Kendrick, M. and Tang, Y. (1995). Anthroponotic cutaneous leishmaniasis in Kabul, Afghanistan: the high susceptibility of Phlebotomus sergenti to Leishmania tropica. Transaction of Royal Society of Tropical Medicine and Hygiene 89, 477.CrossRefGoogle ScholarPubMed
Kulkarni, M. M., McMaster, W. R., Kamysz, E., Kamysz, W., Engman, D. M. and McGwire, B. S. (2006). The major surface-metalloprotease of the parasitic protozoan, Leishmania, protects against antimicrobial peptide-induced apoptotic killing. Molecular Microbiology 62, 1484–1497.CrossRefGoogle ScholarPubMed
McConville, M. J. and Ferguson, M. A. (1993). The structure, biosynthesis and function of glycosylated phosphatidylinositols in the parasitic protozoa and higher eukaryotes. Biochemical Journal 294, 305–324.CrossRefGoogle ScholarPubMed
Myskova, J., Svobodova, M., Beverley, S. M. and Volf, P. (2007). A lipophosphoglycan-independent development of Leishmania in permissive sand flies. Microbes and Infection 9, 317–324.CrossRefGoogle ScholarPubMed
Pereira, F. M., Bernardo, P. S., Dias, P. F. Junior, Silva, B. A., Romanos, M. T., d'Avila-Levy, C. M., Branquinha, M. H. and Santos, A. L. (2009). Differential influence of gp63-like molecules in three distinct Leptomonas species on the adhesion to insect cells. Parasitology Research 104, 347–353.CrossRefGoogle ScholarPubMed
Pereira, F. M., Dias, F. A., Elias, C. G., d'Avila-Levy, C. M., Silva, C. S., Santos-Mallet, J. R., Branquinha, M. H. and Santos, A. L. (2010). Leishmanolysin-like molecules in Herpetomonas samuelpessoai mediate hydrolysis of protein substrates and interaction with insect. Protist 161, 589–602.CrossRefGoogle ScholarPubMed
Rogers, M. E., Ilg, T., Nikolaev, A. V., Ferguson, M. A. and Bates, P. A. (2004). Transmission of cutaneous leishmaniasis by sand flies is enhanced by regurgitation of fPPG. Nature 430, 463–467.CrossRefGoogle ScholarPubMed
Sacks, D. L. and Kamhawi, S. (2001). Molecular aspects of parasite-vector and vector-host interactions in leishmaniasis. Annual Review of Microbiology 55, 453–483.CrossRefGoogle ScholarPubMed
Sacks, D. L., Modi, G., Rowton, E., Späth, G., Epstein, L., Turco, S. J. and Beverley, S. M. (2000). The role of phosphoglycans in Leishmania-sand fly interactions. Proceedings of the National Academy of Sciences, USA 97, 406–411.CrossRefGoogle ScholarPubMed
Sadlova, J., and Volf, P. (2009). Peritrophic matrix of Phlebotomus duboscqi and its kinetics during Leishmania major development. Cell and Tissue Research 337, 313–325.CrossRefGoogle ScholarPubMed
Sadlova, J., Volf, P., Victoir, K., Dujardin, J. C. and Votypka, J. (2006). Virulent and attenuated lines of Leishmania major: DNA karyotypes and differences in metalloproteinase GP63. Folia Parasitologica (Praha) 53, 81–90.CrossRefGoogle ScholarPubMed
Secundino, N., Kimblin, N., Peters, N. C., Lawyer, P., Capul, A. A., Beverley, S. M., Turco, S. J. and Sacks, D. (2010). Proteophosphoglycan confers resistance of Leishmania major to midgut digestive enzymes induced by blood feeding in vector sand flies. Cellular Microbiology 12, 906–918.CrossRefGoogle ScholarPubMed
Späth, G. F., Epstein, L., Leader, B., Singer, S. M., Avila, H. A., Turco, S. J. and Beverley, S. M. (2000). Lipophosphoglycan is a virulence factor distinct from related glycoconjugates in the protozoan parasite Leishmania major. Proceedings of the National Academy of Sciences, USA 97, 9258–9263.CrossRefGoogle ScholarPubMed
Svarovska, A., Ant, T. H., Seblova, V., Jecna, L., Beverley, S. M. and Volf, P. (2010). Leishmania major glycosylation mutants require phosphoglycans (lpg2-) but not lipophosphoglycan (lpg1-) for survival in permissive sand fly vectors. PLoS Neglected Tropical Diseases 4, e580.CrossRefGoogle Scholar
Volf, P. and Myskova, J. (2007). Sand flies and Leishmania: specific versus permissive vectors. Trends in Parasitology 23, 91–92.CrossRefGoogle ScholarPubMed
Volf, P. and Volfova, V. (2011). Establishment and maintenance of sand fly colonies. Journal of Vector Ecology 36, Suppl. 1, S1–S9. doi: 10.1111/j.1948-7134.2011.00106.x.CrossRefGoogle ScholarPubMed
Wilson, R., Bates, M. D., Dostalova, A., Jecna, L., Dillon, R. J., Volf, P. and Bates, P. A. (2010). Stage-specific adhesion of Leishmania promastigotes to sand fly midguts assessed using an improved comparative binding assay. PLoS Neglected Tropical Diseases 4, e816.CrossRefGoogle ScholarPubMed
Yao, C., Donelson, J. E. and Wilson, M. E. (2003). The major surface protease (MSP or GP63) of Leishmania sp. Biosynthesis, regulation of expression, and function. Molecular and Biochemical Parasitology 132, 1–16.CrossRefGoogle ScholarPubMed