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Anti-complement activity in the saliva of phlebotomine sand flies and other haematophagous insects

Published online by Cambridge University Press:  09 October 2003

R. R. CAVALCANTE ,
M. H. PEREIRA  and
N. F. GONTIJO
R. R. CAVALCANTE
Affiliation:
Departamento de Parasitologia e Microbiologia, CCS, Universidade Federal do Piauí, Teresina, PI
M. H. PEREIRA
Affiliation:
Departamento de Parasitologia, ICB, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Cx. Postal 486, CEP 31 270 901, Brazil
N. F. GONTIJO
Affiliation:
Departamento de Parasitologia, ICB, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Cx. Postal 486, CEP 31 270 901, Brazil
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Abstract

The saliva of haematophagous insects has a series of pharmacological activities which may favour blood feeding. In the present study, an inhibitory effect on the complement system was observed in salivary extracts obtained from the phlebotomine sand flies Lutzomyia longipalpis and Lu. migonei. Saliva from Lu. longipalpis was capable of inhibiting both the classical and alternative pathways, while that from Lu. migonei acted only on the former. Other haematophagous insect species were screened for inhibition of the classical pathway. The triatomine bugs Panstrongylus megistus, Triatoma brasiliensis and Rhodnius prolixus were also able to inhibit the classical pathway whereas the mosquito Aedes aegyti and flea Ctenocephalides felis were not. The activity of Lu. longipalpis saliva on the classical pathway was partially characterized. The inhibitor is a protein of Mr 10000–30000 Da, which is very resistant to denaturation by heat. The inhibition of the complement system by phlebotomine sand flies may have a role in the transmission of Leishmania to the vertebrate hosts. The inhibitor molecule is thus a promising component of a vaccine to target salivary immunomodulators.

Keywords

Lutzomyia longipalpishaematophagous insectscomplement inhibitioninsect salivaLeishmania transmissionhaematophagy
Type
Research Article
Information
Parasitology , Volume 127 , Issue 1 , July 2003 , pp. 87 - 93
Copyright
2003 Cambridge University Press

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References

REFERENCES

ADLER, S. & THEODOR, O. (1926). The mouthparts, alimentary tract, and salivary apparatus of the female in Phlebotomus papatasi. Annals of Tropical Medicine and Parasitology 20, 109–140.CrossRefGoogle Scholar
ARLAUD, G. J., VOLANAKIS, J. E., THIELENS, N. M., NARAYANA, S. V., ROSSI, V. & XU, Y. (1998). The atypical serine proteases of the complement system. Advances in Immunology 69, 249–307.CrossRefGoogle Scholar
BELKAID, Y., VALENZUELA, J. G., KAMHAWI, S., ROWTON, E., SACKS, D. L. & RIBEIRO, J. M. C. (2000). Delayed-type hypersensitivity to Phlebotomus papatasi sand fly bite: an adaptative response induced by the fly? Proceedings of the National Academy of Sciences, USA 97, 6704–6709.Google Scholar
BEZERRA, H. S. S. & TEIXEIRA, M. J. (2001). Effect of Lutzomyia whitmani (Diptera: Psychodidae) salivary gland lysates on Leishmania (Viannia) braziliensis infection in BALBl/c mice. Memórias do Instituto Oswaldo Cruz 96, 349–351.CrossRefGoogle Scholar
CAVALCANTE, R. R., PERIERA, M. H. & GONTIJO, N. F. (2002). Inhibitory activity against the complement system in the Lutzomyia longipalpis and Lutzomyia migonei saliva. Entomología y Vectores 9, 87.Google Scholar
CHARLAB, R., VALENZUELA, J. G., ROWTON, E. D. & RIBEIRO, J. M. C. (1999). Toward an understanding of the biochemical and pharmacological complexity of the saliva of a haematophagous sand fly Lutzomyia longipalpis. Proceedings of the National Academy of Sciences, USA 96, 15155–15160.CrossRefGoogle Scholar
EIRAS, A. E. & JEPSON, P. C. (1991). Host location by Aedes aegypti (Diptera; Culicidae): a wind tunnel study of chemical cues. Bulletin of Entomological Research 81, 151–160.CrossRefGoogle Scholar
GILLESPIE, R. D., MBOW, M. L. & TITUS, R. G. (2000). The immunomodulatory factors of bloodfeeding arthropod saliva. Parasite Immunology 7, 319–331.CrossRefGoogle Scholar
HALL, L. R. & TITUS, R. G. (1995). Sand fly vector saliva selectively modulates macrophage functions that inhibit killing of Leishmania major and nitric oxide production. Journal of Immunology 155, 3501–3506.Google Scholar
KAMHAWI, S. (2000). The biological and immunomodulatory properties of sand fly saliva and its role in the establishment of Leishmania infections. Microbes and Infection 2, 1765–1773.CrossRefGoogle Scholar
KAMHAWI, S., BELKAIDE, Y., MODI, G., ROWTON, E. & SACKS, D. (2000). Protection against cutaneous leishmaniasis resulting from bites of uninfected sand flies. Science 290, 1351–1354.CrossRefGoogle Scholar
LAWRIE, C. H., RANDOLPH, S. E. & NUTTALL, P. A. (1999). Ixodes ticks: serum sensitivity of anticomplement activity. Experimental Parasitology 93, 207–214.CrossRefGoogle Scholar
LIMA, H. C. & TITUS, R. G. (1996). Effects of sand fly vector saliva on development of cutaneous lesions and the immune response to Leishmania brasiliensis in BALB/c mice. Infection and Immunology 64, 5442–5445.Google Scholar
MAKRIDES, S. C. (1998). Therapeutic inhibition of the complement system. Pharmacological Reviews 50, 59–87.Google Scholar
MELO, M. N., WILLIAMS, P. & TAFURI, W. L. (2001). Influence of lysates of the salivary glands of Lutzomyia longipalpis on the development of a Leishmania major-like parasite in the skin of golden hamster. Annals of Tropical Medicine and Parasitology 95, 59–68.CrossRefGoogle Scholar
MODI, G. B. & TESH, R. B. (1983). A simple technique for mass rearing Lutzomyia longipalpis and Phlebotomus papatasi (Diptera: Psychodidae) in the laboratory. Journal of Medical Entomology 20, 568–569.CrossRefGoogle Scholar
MORRIS, R. V., SHOEMAKER, C. B., DAVID, J. R., LANZARO, G. C. & TITUS, R. G. (2001). Sandfly maxadilan exacerbates infection with Leishmania major and vaccinating against it protects against L. major infection. Journal of Immunology 167, 5226–5230.CrossRefGoogle Scholar
MOSSER, D. M. & BRITTINGHAM, A. (1997). Leishmania, macrophages and complement: a tale of subversion and exploitation. Parasitology 115 (Suppl.), S9–S23.CrossRefGoogle Scholar
NORONHA, F. S. M., NUNES, A. C., SOUZA, K. T., MELO, M. N. & RAMALHO-PINTO, F. J. (1998). Differential sensitivity of New World Leishmania spp. promastigotes to complement-mediated lysis: correlation with the expression of three parasite polypeptides. Acta Tropica 69, 17–29.Google Scholar
NUNES, A. C. & RAMALHO-PINTO, F. J. (1996). Complement resistance of Leishmania amazonensis promastigotes is independent of parasite proteases and lysis of sensitive forms is not due to natural antibodies in normal human serum. Brazilian Journal of Medical and Biological Research 29, 1633–1640.Google Scholar
PAPATEODOROU, V. & BROSSARD, M. (1987). C3 levels in the area of rabbits infested and reinfested with Ixodes ricinus L. and in midguts of fed ticks. Experimental and Applied Acarology 3, 53–59.CrossRefGoogle Scholar
RIBEIRO, J. M., ROSSIGNOL, P. A. & SPIELMAN, A. (1986). Blood-finding strategy of a capillary-feeding sandfly, Lutzomyia longipalpis. Comparative Biochemistry and Physiology A83, 683–686.CrossRefGoogle Scholar
RIBEIRO, J. M. (1987 a). Role of saliva in blood-feeding by arthropods. Annual Review of Entomology 32, 463–478.Google Scholar
RIBEIRO, J. M. (1987 b). Ixodes dammini: salivary anti-complement activity. Experimental Parasitology 64, 347–353.Google Scholar
RIBEIRO, J. M., VACHEREAU, A., MODI, G. B. & TESH, R. B. (1989). A novel vasodilatory peptide from the salivary glands of the sand fly Lutzomyia longipalpis. Science 243, 212–214.CrossRefGoogle Scholar
RIBEIRO, J. M. C. (1995). Blood-feeding Arthropods: live syringes or invertebrate pharmacologists? Infectious Agents and Disease 4, 143–152.Google Scholar
RIBEIRO, J. M. C., SCHNEIDER, M., ISAIAS, T., JURBERG, J. C., GALVÃO, C. & GUIMARÃES, J. A. (1998). Role of salivary antihemostatic components in blood feeding by triatomine bugs (Heteroptera). Journal of Medical Entomology 35, 599–610.CrossRefGoogle Scholar
TITUS, R. G. & RIBEIRO, J. M. C. (1988). Salivary gland lysates from the sand fly Lutzomyia longipalpis enhance Leishmania infectivity. Science 239, 1307–1308.CrossRefGoogle Scholar
TITUS, R. G. & RIBEIRO, J. M. C. (1990). The role of vector saliva in transmission of arthropod borne disease. Parasitology 6, 157–160.CrossRefGoogle Scholar
THEODOS, C. M., RIBEIRO, J. M. C. & TITUS, R. G. (1991). Analyses of the enhancing effect of the sand fly saliva on Leishmania infection in mice. Infection and Immunity 59, 1592–1598.Google Scholar
THEODOS, C. M. & TITUS, R. G. (1993). Salivary gland material from the sand fly Lutzomyia longipalpis has an inhibitory effect on macrophage function in vitro. Parasite Immunology 15, 481–487.CrossRefGoogle Scholar
VALENZUELA, J. G., CHARLAB, R., MATHER, T. N. & RIBEIRO, J. M. (2000). Purification, cloning, and expression of a novel salivary anticomplement protein from the tick, Ixodes scapularis. Journal of Biological Chemistry 25, 18717–18723.CrossRefGoogle Scholar
VALENZUELA, J. G., BELKAIDE, Y., GARFIELD, M. K., MENDEZ, S., KAMHAWI, S., ROWTON, E. D., SACKS, D. L. & RIBEIRO, J. M. C. (2001). Toward a defined anti-Leishmania vaccine targeting vector antigens: characterization of a protective salivary protein. Journal of Experimental Medicine 194, 331–342.CrossRefGoogle Scholar
WARBURG, A., SARAIVA, E., LANZARO, G. C., TITUS, R. G. & NEVA, F. (1994). Saliva of Lutzomyia longipalpis sibling species differs in its composition and capacity to enhance leishmaniasis. Philosophical Transactions of the Royal Society of London, B 345, 223–230.CrossRefGoogle Scholar
WHALEY, K. & NORTH, J. (1997). Haemolytic assays for whole complement activity and individual components. In Complement: a Practical Approach (ed. Dodds, A. W. & Sim, R. B., I.P.), pp. 19–47. Oxford University Press, Oxford.
WIKEL, S. K. & ALLEN, J. R. (1977). Acquired resistance to ticks. III. Cobra venom factor and the resistance response. Immunology 32, 457–465.Google Scholar
ZER, R., YAROSLAVISKI, I., ROSEN, L. & WARBURG, A. (2001). Effect of sand fly saliva on Leishmania uptake by murine macrophages. International Journal for Parasitology 31, 810–814.CrossRefGoogle Scholar