Differential modulation of murine host immune response by salivary gland extracts from the mosquitoes Aedes aegypti and Culex quinquefasciatus

Medical and Veterinary Entomology

Volumn 18, Issue 2, 2004, Pages 191-199

  Wanasen, N ^a   Nussenzveig, R H ^a   Champagne, D E ^c   Soong, L ^a,b   Higgs, S ^a,b  

^a University of Texas Medical Branch School of Medicine   (United States)

^b UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

^c UNIVERSITY OF GEORGIA   (United States)

Author keywords

Aedes aegypti; Culex quinquefasciatus; Cytokines; Immunomodulation; Mosquito saliva; Mouse; Splenocytes; T cell populations; Th cytokines; Vector host pathogen relationships; Vertebrate immune response

Indexed keywords

CYTOKINE; OVALBUMIN; SALIVA PROTEIN; TISSUE EXTRACT;

DISEASE TRANSMISSION; DISEASE VECTOR; HEMOPHAGY; IMMUNE RESPONSE; MOSQUITO;

AEDES; ANIMAL; ARTICLE; B LYMPHOCYTE; C3H MOUSE; CELL DEATH; CELL DIVISION; CHEMISTRY; CULEX; CYTOLOGY; FEMALE; FLOW CYTOMETRY; GERMFREE ANIMAL; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MOUSE; SALIVARY GLAND; SPLEEN; T LYMPHOCYTE;

AEDES; ANIMALS; B-LYMPHOCYTES; CELL DEATH; CELL DIVISION; CULEX; CYTOKINES; FEMALE; FLOW CYTOMETRY; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C3H; OVALBUMIN; SALIVARY GLANDS; SALIVARY PROTEINS; SPECIFIC PATHOGEN-FREE ORGANISMS; SPLEEN; T-LYMPHOCYTES; TISSUE EXTRACTS;

AEDES AEGYPTI; ANIMALIA; CULEX PIPIENS QUINQUEFASCIATUS; CULICIDAE; DIPTERA; MURINAE; VERTEBRATA;

EID: 2942622237     PISSN: 0269283X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2915.2004.00498.x     Document Type: Article

References (39)

1. Amino, R., Martins, R.M., Procopio, J., Hirata, I.Y., Juliano, M.A. & Schenkman, S. (2002) Trialysin, a novel pore-forming protein from saliva of hematophagous insects activated by limited proteolysis. Journal of Biological Chemistry, 277, 6207-6213.
2. Bissonnette, E.Y., Rossignol, P.A. & Befus, A.D. (1993) Extracts of mosquito salivary gland inhibit tumour necrosis factor alpha release from mast cells. Parasite Immunology, 15, 27-33.
3. Bogh, C., Pedersen, E.M., Kukoko, D.A. & Ouma, J.H. (1998) Permethrin-impregnated bednet effects on resting and feeding behaviour of lymphatic filariasis vector mosquitoes in Kenya. Medical and Veterinary Entomology, 12, 52-59.
4. CDC (2003) Fact Sheet: Arboviral Encephalitis. Division of Vector-Borne Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, GA, U.S.A. http://www.cdc.gov/ncidod/ dvbid/arbor/arbofact.htm (accessed 11 October 2003).
5. Champagne, D. & Ribeiro, J.M. (1994) Sialokinin I and II: Two salivary tachykinins from the Yellow Fever mosquito, Aedes aegypti. Proceedings of the National Academy of Science USA, 91, 138-142.
6. Champagne, D. & Valenzuela, J.G. (1996) Pharmacology of haematophagous arthropod saliva. The Immunology of Host-Ectoparasitic Arthropod Relationships (ed. by S. K. Wikel), pp. 85-106. CAB International, Wallingford, Oxon, U.K.
7. Chevillon, C., Pasteur, N., Marquine, M., Heyse, D. & Raymond, M. (1995) Population structure and dynamics of selected genes in the mosquito Culex pipiens. Evolution, 49, 997-1007.
8. Christophers, S.R. (1960) Aedes aegypti (L.) The Yellow Fever Mosquito. Its Life History, Bionomics and Structure. Cambridge University Press.
9. Cross, M.L., Cupp, M.S., Cupp, E.W., Galloway, A.L. & Enriquez, F.J. (1993) Modulation of murine immunological responses by salivary gland extract of Simulium vittatum (Diptera: Simuliidae). Journal of Medical Entomology, 30, 928-935.
10. Cross, M.L., Cupp, E.W. & Enriquez, F.J. (1994) Differential modulation of murine cellular immune responses by salivary gland extract of Aedes aegypti. American Journal of Tropical Medicine and Hygiene, 51, 690-696.
11. Edwards, J.F., Higgs, S. & Beaty, B.J. (1998) Mosquito feeding-induced enhancement of Cache Valley Virus (Bunyaviridae) infection in mice. Journal of Medical Entomology, 35, 261-265.
12. Ferreira, B.R. & Silva, J.S. (1998) Saliva of Rhipicephalus sanguineus tick impairs T cell proliferation and IFN-gamma-induced macrophage microbicidal activity. Veterinary Immunology, 64, 279-293.
13. Gaunt, M.W., Sall, A.A., Lamballerie, X., Falconar, A.K., Dzhivanian, T.I. & Gould, E.A. (2001) Phylogenetic relationships of flaviviruses correlate with their epidemiology, disease association and biogeography. Journal of General Virology, 82, 1867-1876.
14. Gillespie, R.D., Mbow, M.L. & Titus, R.G. (2000) The immunomodulatory factors of blood feeding arthropod saliva. Parasite Immunology, 22, 319-331.
15. Gillespie, R.D., Dolan, M.C., Piesman, J. & Titus, R.G. (2001) Identification of an IL-2 binding protein in the saliva of the Lyme disease vector tick, Ixodes scapularis. Journal of Immunology, 166, 4319-4327.
16. Gratz, N.G. (1999) Emerging and resurging vector-borne diseases. Annual Review of Entomology, 44, 51-75.
17. Hall, L.R. & Titus, R.G. (1995) Sandfly vector saliva selectively modulates macrophage functions that inhibit killing of Leishmania major and nitric oxide production. Journal of Immunology, 155, 3501-3506.
18. Higgs, S. & Beaty, B. (1996) Rearing and containment of mosquito vectors. The Biology of Disease Vectors (ed. by B. Beaty & W. C. Marquardt), pp. 595-605. University Press of Colorado, Niwot, CO.
19. Kopecky, J. & Kuthejlova, M. (1998) Suppressive effect of Ixodes ricinus salivary gland extract on mechanisms of natural immunity in vitro. Parasite Immunology. 20, 169-174.
20. Kovar, L., Kopecky, J. & Rihova, B. (2001) Salivary gland extract from Ixodes ricinus tick polarizes the cytokine profile toward Th2 and suppresses proliferation of T lymphocytes in human PBMC culture. Journal of Parasitology, 87, 1342-1348.
21. Kovar, L., Kopecky, J. & Rihova, B. (2002) Salivary gland extract from Ixodes ricinus tick modulates the host immune response towards the Th2 cytokine profile. Parasitology Research, 88, 1066-72.
22. Kubes, M., Fuchsberger, N., Labuda, M., Zuffova, E. & Nuttall, P.A. (1994) Salivary gland extracts of partially fed Dermacentor reticulatus ticks decrease natural killer cell activity in vitro. Immunology, 82, 113-116.
23. Mattingly, P. (1962) Some considerations relating to the role of Culex pipiens fatigans Widemann in the transmission of filariasis. Bulletin of the World Health Organization, 27, 569-578.
24. Mbow, M.L., Bleyenberg, J.A., Hall, L.R. & Titus, R.G. (1998) Phlebotomus papatasi sandfly salivary gland lysate down-regulates a Th1, but up-regulates a Th2, response in mice infected with Leishmania major. Journal of Immunology, 161, 5571-5577.
25. Miller, B.R. & Mitchell, C.J. (1991) Genetic selection of a flavivirus-refractory strain of the yellow fever mosquito Aedes aegypti. American Journal of Tropical Medicine and Hygiene, 45, 399-407.
26. Osorio, J.E., Godsey, M.S., Defoliart, G.R. & Yuill, T.M. (1996) La Crosse viremias in white-tailed deer and chipmunks exposed by injection or mosquito bite. American Journal of Tropical Medicine and Hygiene, 54, 338-342.
27. Qureshi, A.A., Asahina, A., Ohnuma, M., Tajima, M., Granstein, R.D. & Lerner, E.A. (1996) Immunomodulatory properties of maxadilan, the vasodilator peptide from sandfly salivary gland extracts. American Journal of Tropical Medicine and Hygiene, 54, 665-671.
28. Ribeiro, J.M. (1987) Ixodes dammini: salivary anti-complement activity. Experimental Parasitology, 64, 347-353.
29. Ribeiro, J.M. (2000) Blood-feeding in mosquitoes: probing time and salivary gland anti-haemostatic activities in representatives of three genera (Aedes, Anopheles, Culex). Medical and Veterinary Entomology, 14, 142-148.
30. Ribeiro, J.M. & Francischetti, I.M. (2001) Platelet-activating- factor-hydrolyzing phospholipase C in the salivary glands and saliva of the mosquito Culex quinquefasciatus. Journal of Experimental Biology, 204, 3887-3894.
31. Ribeiro, J.M., Makoul, G.T., Levine, J., Robinson, D.R. & Spielman, A. (1985) Antihemostatic, antiinflammatory, and immunosuppressive properties of the saliva of a tick, Ixodes dammini. Journal of Experimental Medicine, 161, 332-344.
32. Schoeler, G.B. & Wikel, S.K. (2001) Modulation of host immunity by haematophagous arthropods. Annals of Tropical Medicine and Parasitology, 95, 755-771.
33. Service, M. (1968) The taxonomy and biology of two sympatric sibling species of Culex, C. pipiens and C. torrentium (Diptera, Culicidae). Journal of Zoology (London), 156, 313-323.
34. Smartt, C.T., Kim, A.P., Grossman, G.L. & James, A.A. (1995) The apyrase gene of the vector mosquito, Aedes aegypti, is expressed specifically in the adult female salivary glands. Experimental Parasitology, 81, 239-248.
35. Titus, R.G. & Ribeiro, J.M. (1988) Salivary gland lysates from the sandfly Lutzomyia longipalpis enhance Leishmania infectivity. Science, 239, 1306-1308.
36. 2-dependent mechanism. Journal of Experimental Medicine, 180, 1077-1085.
37. Waitumbi, J. & Warburg, A. (1998) Phlebotomus papatasi saliva inhibits protein phosphatase activity and nitric oxide production by murine macrophages. Infection and Immunology, 66, 1534-1537.
38. Wikel, S.K. (1996) The Immunology of Host Ectoparasitic Arthropod Relationships. CAB International, Wallingford, Oxon. U.K.
39. Zeidner, N.S., Higgs, S., Happ, C.M., Beaty, B.J. & Miller, B.R. (1999) Mosquito feeding modulates Th1 and Th2 cytokines in flavivirus susceptible mice: an effect mimicked by injection of sialokinins, but not demonstrated in flavivirus resistant mice. Parasite Immunology, 21, 35-44.