Black fly salivary gland extract inhibits proliferation and induces apoptosis in murine splenocytes

Parasite Immunology

Volumn 32, Issue 4, 2010, Pages 275-284

  Tsujimoto, H ^a,b   Gray, E W ^a   Champagne, Donald E ^a,b  

^a UNIVERSITY OF GEORGIA   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

Author keywords

Apoptosis; Black fly; Saliva; T lymphocyte

Indexed keywords

CASPASE 3;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; BLACK FLY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DIVISION; CELL PROLIFERATION; CELL STRUCTURE; ENZYME ACTIVATION; EXTRACT; FLY; IMMUNOMODULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SALIVARY GLAND; SALIVARY GLAND EXTRACT; SALIVATION; SPLEEN CELL;

ANIMALS; APOPTOSIS; CASPASE 3; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; FEMALE; LEUKOCYTES, MONONUCLEAR; MICE; MICE, INBRED BALB C; MOLECULAR WEIGHT; OXAZINES; SALIVARY GLANDS; SALIVARY PROTEINS AND PEPTIDES; SIMULIIDAE; STAINING AND LABELING; XANTHENES;

MURINAE; ONCHOCERCA VOLVULUS; SIMULIIDAE; SIMULIUM NIGRICOXUM; VESICULAR STOMATITIS VIRUS;

EID: 77949433752     PISSN: 01419838     EISSN: 13653024     Source Type: Journal    
DOI: 10.1111/j.1365-3024.2009.01186.x     Document Type: Article

References (38)

1. Cupp EW Black flies and the agents they transmit. In Beaty BJ & Marquardt WC, (eds): Biology of Disease Vectors, Niwot, CO, University Press of Colorado, 1996; 98-109.
2. Adler PH & McCreadie JW. Black Flies (Simuliidae). In Mullen G & Durden L (eds): Medical and Veterinary Entomology, San Diego, CA, Elsevier Science, 2002: 185-202.
3. Crosskey RW, 1993. Blackflies (Simuliidae). In Lane RP & Crosskey RW, (eds): Medical Insects and Arachnids, New York, NY, Springer, 1993; 241-287.
4. Mead DG, Howerth EW, Murphy MD, Gray EW, Noblet R & Stallknecht DE. Black fly involvement in the epidemic transmission of vesicular stomatitis New Jersey virus (Rhabdoviridae: Vesiculovirus). Vector Borne Zoonotic Dis 2004; 4: 351-359.
5. Mead DG, Ramberg FB, Besselsen DG & Mare CJ. Transmission of vesicular stomatitis virus from infected to noninfected black flies co-feeding on nonviremic deer mice. Science 2000; 287: 485-487.
6. Jacobs JW, Cupp EW, Sardana M & Friedman PA. Isolation and characterization of a coagulation factor Xa inhibitor from black fly salivary glands. Thromb Haemost 1990; 64: 235-238.
7. Cupp MS, Cupp EW & Ramberg FB. Salivary Gland Apyrase in Black Flies (Simulium vittatum). Journal of Insect Physiology 1993; 39: 817-821.
8. Abebe M, Cupp MS, Champagne D & Cupp EW. Simulidin: a black fly (Simulium vittatum) salivary gland protein with antithrombin activity. Journal of Insect Physiology 1995; 41: 1001-1006.
9. Abebe M, Ribeiro JMC, Cupp MS & Cupp EW. Novel anticoagulant from salivary glands of Simulium vittatum (Diptera: Simuliidae) inhibits activity of coagulation factor V. Journal of Medical Entomology 1996; 33: 173-176.
10. Cupp MS, Ribeiro JM & Cupp EW. Vasodilative activity in black fly salivary glands. Am J Trop Med Hyg 1994; 50: 241-246.
11. Cupp MS, Ribeiro JM, Champagne DE & Cupp EW. Analyses of cDNA and recombinant protein for a potent vasoactive protein in saliva of a blood-feeding black fly, Simulium vittatum. J Exp Biol 1998; 201: 1553-1561.
12. Ribeiro JM, Charlab R, Rowton ED & Cupp EW. Simulium vittatum (Diptera: Simuliidae) and Lutzomyia longipalpis (Diptera: Psychodidae) salivary gland hyaluronidase activity. J Med Entomol 2000; 37: 743-747.
13. Volfova V, Hostomska J, Cerny M, Votypka J & Volf P. Hyaluronidase of bloodsucking insects and its enhancing effect on leishmania infection in mice. PLoS Negl Trop Dis 2008; 2: e294.
14. Andersen JF, Pham VM, Meng Z, Champagne DE & Ribeiro JM. Insight into the Sialome of the Black Fly, Simulium vittatum. J Proteome Res. 2009; 8: 1474-1488.
15. Cross ML, Cupp MS, Cupp EW, Galloway AL & Enriquez FJ. Modulation of murine immunological responses by salivary gland extract of Simulium vittatum (Diptera: Simuliidae). J Med Entomol 1993; 30: 928-935.
16. Cross ML, Cupp EW & Enriquez FJ. Modulation of murine cellular immune responses and cytokines by salivary gland extract of the black fly Simulium vittatum. Trop Med Parasitol 1994; 45: 119-124.
17. Wasserman HA, Singh S & Champagne DE. Saliva of the Yellow Fever mosquito, Aedes aegypti, modulates murine lymphocyte function. Parasite Immunol 2004; 26: 295-306.
18. Wanasen N, Nussenzveig RH, Champagne DE, Soong L & Higgs S. Differential modulation of murine host immune response by salivary gland extracts from the mosquitoes Aedes aegypti and Culex quinquefasciatus. Med Vet Entomol 2004; 18: 191-199.
19. Bernardo MJ & Cupp EW. Rearing black flies (Diptera: Simuliidae) in the laboratory: mass-scale in vitro membrane feeding and its application to collection of saliva and to parasitological and repellent studies. J Med Entomol 1986; 23: 666-679.
20. Gray EW & Noblet R. Laboratory Rearing of Black Flies. In Maramorosch K & Mahmood F. (eds): Maintenance of Human, Animal and Plant Pathogen Vectors,, New Delhi and Calcutta, Oxford & IBH Publishing Co. PVT. LTD, 1999: 85-105.
21. Al-Nasiry S, Geusens N, Hanssens M, Luyten C & Pijnenborg R. The use of Alamar Blue assay for quantitative analysis of viability, migration and invasion of choriocarcinoma cells. Hum Reprod 2007; 22: 1304-1309.
22. Kwack K & Lynch RG. A new non-radioactive method for IL-2 bioassay. Mol Cells 2000; 10: 575-578.
23. Larson EM, Doughman DJ, Gregerson DS & Obritsch WF A new, simple, nonradioactive, nontoxic in vitro assay to monitor corneal endothelial cell viability. Invest Ophthalmol Vis Sci 1997; 38: 1929-1933.
24. Beckenbach AT & Borkent A. Molecular analysis of the biting midges (Diptera: Ceratopogonidae), based on mitochondrial cytochrome oxidase subunit 2. Mol Phylogenet Evol 2003; 27: 21-35.
25. Fallon AM & Li L. The C-terminal extension that characterizes mosquito (Diptera: Culicidae) ribosomal protein S6 is widespread among the Culicomorpha. J Med Entomol 2007; 44: 608-616.
26. Miller BR, Crabtree MB & Savage HM. Phylogenetic relationships of the Culicomorpha inferred from 18S and 5.8S ribosomal DNA sequences. (Diptera:Nematocera). Insect Mol Biol 1997; 6: 105-114.
27. Yeates DK & Wiegmann BM. Congruence and controversy: toward a higher-level phylogeny of Diptera. Annu Rev Entomol 1999; 44: 397-428.
28. Grimaldi D & Engel MS. Evolution of the Insects. New York, NY, Cambridge University Press, 2005.
29. Bishop JV, Mejia JS, Perez de Leon AA, Tabachnick WJ & Titus RG. Salivary gland extracts of Culicoides sonorensis inhibit murine lymphocyte proliferation and NO production by macrophages. Am J Trop Med Hyg 2006; 75: 532-536.
30. Kalvachova P, Hribalova V, Kodym P & Volf P. Modulation of murine lymphocyte responsiveness by the saliva of Rhodnius prolixus (Hemiptera: Reduviidae). J Med Entomol 1999; 36: 341-344.
31. Swist SL, Wilkerson MJ, Wyatt CR, Broce AB & Kanost MR. Modulation of bovine lymphocyte response by salivary gland extracts of the stable fly, Stomoxys calcitrans (Diptera: Muscidae). J Med Entomol 2002; 39: 900-907.
32. Boppana VD, Thangamani S, Adler AJ & Wikel SK. SAAG-4 is a novel mosquito salivary protein that programmes host CD4 T cells to express IL-4. Parasite Immunol 2009; 31: 287-295.
33. Golodne DM, Monteiro RQ, Graca-Souza AV, Silva-Neto MA & Atella GC. Lysophosphatidylcholine acts as an anti-hemostatic molecule in the saliva of the blood-sucking bug Rhodnius prolixus. J Biol Chem. 2003; 278: 27766-27771.
34. Garg R, Juncadella IJ, Ramamoorthi N, Ashish Ananthanarayanan SK, Thomas V, Rincon M, Krueger JK, Fikrig E, Yengo CM & Anguita J Cutting edge: CD4 is the receptor for the tick saliva immunosuppressor, Salp15. J Immunol 2006; 177: 6579-6583.
35. Hovius JW, de Jong MA, den Dunnen J, Litjens M, Fikrig E, van der Poll T, Gringhuis SI & Geijtenbeek TB. Salp15 binding to DC-SIGN inhibits cytokine expression by impairing both nucleosome remodeling and mRNA stabilization. PLoS Pathog 2008; 4: e31.
36. Sa-Nunes A, Bafica A, Lucas DA, Conrads TP, Veenstra TD, Andersen JF, Mather TN, Ribeiro JM & Francischetti IM. Prostaglandin E2 is a major inhibitor of dendritic cell maturation and function in Ixodes scapularis saliva. J Immunol 2007; 179: 1497-1505.
37. Tyson K, Elkins C, Patterson H, Fikrig E & de Silva A. Biochemical and functional characterization of Salp20, an Ixodes scapularis tick salivary protein that inhibits the complement pathway. Insect Mol Biol 2007; 16: 469-479.
38. Valenzuela JG, Charlab R, Mather TN & Ribeiro JM. Purification, cloning, and expression of a novel salivary anticomplement protein from the tick, Ixodes scapularis. J Biol Chem 2000; 275: 18717-18723.