Toward an understanding of the molecular mechanism for successful blood feeding by coupling proteomics analysis with pharmacological testing of horsefly salivary glands

Molecular and Cellular Proteomics

Volumn 7, Issue 3, 2008, Pages 582-590

  Xu, Xueqing ^a,b   Yang, Hailong ^a   Ma, Dongying ^a,b   Wu, Jing ^a,b   Wang, Yipeng ^a,b   Song, Yuzhu ^a,b   Wang, Xu ^c   Lu, Yi ^c   Yang, Junxing ^a   Lai, Ren ^a,c  

^a KUNMING INSTITUTE OF ZOOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c NANJING AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; HYALURONIDASE; INSECT PROTEIN; INTERLEUKIN 10; METALLOTHIONEIN; POLYPEPTIDE ANTIBIOTIC AGENT; PROTEINASE; SERINE PROTEINASE INHIBITOR; TRANSCRIPTOME; VASODILATOR AGENT;

ANIMAL TISSUE; ANTICOAGULATION; ARTHROPOD; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DRUG TARGETING; ECTOPARASITE; FIBRINOGENOLYSIS; HEMOSTASIS; HORSEFLY; HOST PARASITE INTERACTION; IMMUNE RESPONSE; IMMUNE SYSTEM; MOLECULAR BIOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; PEPTIDOMICS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEOMICS; SALIVARY GLAND FUNCTION; THROMBOCYTE AGGREGATION INHIBITION;

AMINO ACID SEQUENCE; ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; CHEMICAL FRACTIONATION; CLONING, MOLECULAR; DIPTERA; DNA, COMPLEMENTARY; FEEDING BEHAVIOR; HYALURONOGLUCOSAMINIDASE; IMMUNOSUPPRESSIVE AGENTS; INSECT PROTEINS; LIPOPOLYSACCHARIDES; METALLOTHIONEIN; MICE; MOLECULAR SEQUENCE DATA; PEPTIDES; PLATELET AGGREGATION; PLATELET AGGREGATION INHIBITORS; PROTEOMICS; SALIVARY GLANDS; SERINE PROTEINASE INHIBITORS; SPLEEN; TISSUE EXTRACTS;

ARTHROPODA; DIPTERA; HYBOMITRA BIMACULATA; INVERTEBRATA; TABANIDAE;

EID: 41549145257     PISSN: 15359476     EISSN: None     Source Type: Journal    
DOI: 10.1074/mcp.M700497-MCP200     Document Type: Article

References (47)

1. Ribeiro, J. M. (1995) Blood-feeding arthropods: live syringes or invertebrate Pharmacologists? Infect Agents Dis. 4, 143-152
2. Charlab, R., Valenzuela, J. G., Rowton, E. D., and Ribeiro, J. M. (1999) Toward an understanding of the biochemical and pharmacological complexity of the saliva of a hematophagous sand fly Lutzomyia longipalpis. Proc. Natl. Acad. Sci. U. S. A. 96, 15155-15160
3. Takác, P., Nunn, M. A., Mészáros, J., Pechánová, O., Vrbjar, N., Vlasáková, P., Kozánek, M., Kazimirová, M., Hart G., Nuttall, P. A., and Labuda, M. (2006) Vasotab, a vasoactive peptide from horse fly Hybomitra bimaculata (Diptera, Tabanidae) salivary glands. J. Exp. Biol. 209, 343-352
4. Ribeiro, J. M. C. (1992) Characterization of a vasodilator from the salivary glands of the yellow fever mosquito Aedes aegypti. J. Exp. Biol. 165, 61-71
5. Arcs, B., Lombardo, F., de Lara Capurro, M., della Torre, A., Dimopoulos, G., James, A. A., and Coluzzi, M. (1999) Trapping cDNAs encoding secreted proteins from the salivary glands of the malaria vector Anopheles gambiae. Proc. Natl. Acad. Sci U. S. A. 96, 1516-1521
6. Arocha-Pin̂ango, C. L., Marchi, R., Carvajal, Z., and Guerrero, B (1999) Invertebrate compounds acting on the hemostatic mechanism. Blood Coagul. Fibrinolysis 10, 43-68
7. Markwardt, F. (1994) Coagulation inhibitors from animals feeding on blood. Rev. Iberoam. Thromb. Hemost. 7, 225-231
8. Kazimírová, M., Sulanová, M., Kozánek, M., Takác, P., Labuda, M., and Nuttall, P. A. (2001) Identification of anticoagulant activities in salivary gland extracts of four horsefly species (Diptera, tabanidae). Haemostasis 31, 294-305
9. Wikel, S. K. (ed) (1996) The Immunology of Host-Ectoparesitic Arthropod Relationships, CAB International, Wallingford, UK
10. Ribeiro, J. M. C. (1987) Ixodes dammini: salivary anti-complement activity. Exp. Parasitol. 64, 347-353
11. Ribeiro, J. M. C., and Spielman, A. (1986) Ixodes dammini: salivary anaphylatoxin inactivating activity. Exp. Parasitol. 62, 292-297
12. Ribeiro, J. M. C., Weiss, J. J., and Telford, S. R., III (1990) Saliva of the tick Ixodes dammini inhibits neutrophil function. Exp. Parasitol. 70, 382-388
13. Urioste, S., Hall, L. E., Telford, S. R., III, and Titus, R. (1994) Saliva of the Lyme disease vector, Ixodes dammini, blocks cell activation by a non-prostaglandin E2-dependent mechanism. J. Exp. Med. 180, 1077-1085
14. Kopecky, J., and Kuthejlová, M. (1998) Suppressive effect of Ixodes ricinus salivary gland extract on mechanisms of natural immunity in vitro. Parasite Immunol. (Oxf.) 20, 169-174
15. Ferreira, B. R., and Silva, J. S. (1999) Successive tick infestations selectively promote a T-helper 2 cytokine profile in mice. Immunology 96, 434-439
16. Kopecky, J., Kuthejlová, M., and Pechová, J. (1999) Salivary gland extract from Ixodes ricinus ticks inhibits production of interferon-γ by the up-regulation of interleukin-10. Parasite Immunol. (Oxf.) 21, 351-356
17. Konik, P., Slavíková, V., Salát, J., Reznicková, J., Dvorozniková, E., and Kopecký, J. (2006) Anti-tumour necrosis factor-α activity in Ixodes ricinus saliva. Parasite Immunol. (Oxf.) 28, 649-656
18. Hollander, A. L., and Wright, R. E. (1980) Impact of tabanids on cattle: blood meal size and preferred feeding sites. J. Econ. Entomol. 73, 431-433
19. Zhang, Y., Wisner, A., Xiong, Y., and Bon, C. (1995) A novel plasminogen activator from snake venom. Purification, characterization, and molecular cloning. J. Biol. Chem. 270, 10246-10255
20. Li, J., Xu, X., Xu, C., Zhou, W., Zhang, K., Yu, H., Zhang, Y., Zheng, Y., Rees, H. H., Lai, R., Yang, D., and Wu, J. (2007) Anti-infection peptidomics of amphibian skin. Mol. Cell. Proteomics 6, 882-894
21. Grevelink, S. A., Youssef, D. E., Loscalzo, J., and Lemer, E. A. (1993) Salivary gland extracts from the deerfly contain a potent inhibitor of platelet aggregation. Proc. Natl. Acad. Sci. U. S. A. 90, 9155-9158
22. Wang, X., Coons, L. B., Taylor, D. B., Stevens, S. E., Jr., Gartner, and T. K. Variabilin (1996) A novel RGD-containing antagonist of glycoprotein IIb-IIIa and platelet aggregation inhibitor from the hard tick Dermacentor variabilis. J. Biol. Chem. 271, 17785-17790
23. Seymour, J. L., Henzel, W. J., Nevins, B., Stults, J. T., and Lazarus, R. A. (1990) Decorsin. A potent glycoproteln IIb-IIIa antagonist and platelet aggregation inhibitor from the leech Macrobdella decora. J. Biol. Chem. 265, 10143-10147
24. Mazur, P., Henzel, W. J., Seymour, J. L., and Lazarus, R. A. (1991) Omatins: potent glycoprotein IIb-IIIa antagonists and platelet aggregation inhibitors from the leech Placobdella omata. Eur. J. Biochem. 202, 1073-1082
25. Gould, R. J., Polokoff, M. A., Friedman, P. A., Huang, T. F., Holt, J. C., Cook, J. J., and Niewiarowski, S. (1990) Disintegrins: a family of integrin inhibitory proteins from viper venoms. Proc. Soc. Exp. Biol. Med. 195, 168-171
26. Blobel, C. P., and White, J. M. (1992) Structure, function and evolutionary relationship of proteins containing a disintegrin domain. Curr. Opin. Cell Biol. 4, 760-765
27. Scarborough, R. M., Rose, J. W., Naughton, M. A., Phillips, D. R., Nannizzi, L., Arfsten, A., Campbell, A. M., and Charo, I. F. (1993) Characterization of the integrin specificities of disintegrins isolated from American pit viper venoms. J. Biol. Chem. 268, 1058-1065
28. Tai, H., Wei, Q., Jin, Y., Su, M., Song, J. X., Zhou, X. D., Ouyang, H. M., Wang, W. Y., Xiong, Y. L., and Zhang, Y. (2004) TMVA, a snake C-type lectin-like protein from Trimeresurus mucrosquamatus venom, activates platelet via GPlb. Toxicon 44, 649-656
29. Lu, Q., Navdaev, A., Clemetson, J. M., and Clemetson, K. J. (2004) GPlb is involved in platelet aggregation induced by mucetin, a snake C-type lectin protein from Chinese habu (Trimeresurus mucrosquamatus) venom. Thromb. Haemostasis 91, 1168-1176
30. Lee, W. H., Du, X. Y., Lu, Q. M., Clemetson, K. J., and Zhang Y. (2003) Stejnulxin, a novel snake C-type lectin-like protein from Trimeresurus stejnegeri venom is a potent platelet agonist acting specifically via GPVI. Thromb. Haemostasis 90, 662-671
31. Hannier, S., Liversidge, J., Stemberg, J. M., and Bowman, A. S. (2003) Ixodes ricinus tick salivary gland extract inhibits IL-10 secretion and CD69 expression by mitogen-stimulated murine splenocytes and induces hyporesponsiveness in B lymphocytes. Parasite Immunol. (Oxf.) 25, 27-37
32. Schmidt, T., Stumm-Zollinger, E., Chen, P. S., Böhlen, P., and Stone, S. R. (1989) A male accessory gland peptide with protease inhibitory activity in Drosophila funebris. J. Biol. Chem. 264, 9745-9749
33. Diochot, S., Schweitz, H., Béress, L., and Lazdunski, M. (1998) Sea anemone peptides with a specific blocking activity against the fast inactivating potassium channel Kv3.4. J. Biol. Chem. 273, 6744-6749
34. Krebs, H. C., and Habermehl, G. G. (1987) Isolation and structural determination of a hemolytic active peptide from the sea anemone Metridium senile. Naturwissenschaften 74, 395-396
35. Lai, R., Takeuchi, H., Jonczy, J., Rees, H. H., and Turner, P. C. (2004) A thrombin inhibitor from the ixodid tick, Amblyomma hebraeum. Gene (Amst.) 342, 243-249
36. Delfin, J., Martinez, I., Antuch, W., Morera, V., Gonzalez, Y., Rodriguez, R., Marquez, M., Saroyan, A., Larionova, N., Diaz, J., Padron, G., and Chavez, M. (1996) Purification, characterization and immobilization of protainase inhibitors from Stichodactyla helianthus. Toxicon 34, 1367-1376
37. Tanaka, A. S., Azzolini, S. S., Sasaki, S. D., Campos, I. T. S., Torquato, R. J., and Juliano, M. A. (2005) The role of HM, a serine protease inhibitor from Haematobia Irritans irritans (Diptera: Muscidae) in the control of fly and bacterial proteases. Exp. Parasitol. 111, 30-36
38. Francischetti, I. M., Valenzuela, J. G., Andersen, J. F., Mather, T. N., and Ribelro, J. M. (2002) Ixolaris, a novel recombinant tissue factor pathway inhibitor (TFPI) from the salivary gland of the tick, Ixodes scapularis: identification of factor X and factor Xa as scaffolds for the inhibition of factor Vila/tissue factor complex. Blood 99, 3602-3612
39. Kress, H., Jarrin, A., Thüroff, E., Saunders, R., Weise, C., Schmidt am Busch, M., Knapp, E. W., Wedde, M., and Vilcinskas, A. (2004) A Kunitz type protease inhibitor related protein is synthesized in Drosophila prepupal salivary glands and released into the moulting fluid during pupation. Insect Biochem. Mol. Biol. 34, 855-869
40. Markwardt, F., and Schulz, E. (1960) On the mechanism of the inhibitory effect of tabanine on blood coagulation. Naunyn-Schmiedeberg's Arch. Exp. Pathol. Pharmakol. 238, 320-328
41. Cemá, P., Mikes, L., and Volf, P. (2002) Salivary gland hyaluronidase in various species of phlebotomine sand flies (Diptera: Psychodidae). Insect Biochem. Mol. Biol. 32, 1691-1697
42. Kreil, G. (1995) Hyaluronidases - a group of neglected enzymes. Protein Sci. 4, 1666-1669
43. Neitz, A. W., Howel, C. J., Potgieter, D. J., and Bezuidenhout, J. D. (1978) Proteins and free amino acids in the salivary secretion and haemolymph of the tick Amblyomma hebraeum. Onderstepoort J. Vat. Res. 45, 235-240
44. Ribeiro, J. M. C., Charlab, R., Rowton, E. D., and Cupp, E. W. (2000) Simulium vittatum (Diptera: Simuliidae) and Lutzomyia longipalpis (Diptera: Psychodidae) salivary gland hyaluronidase activity. J. Med. Entomol. 37, 743-747
45. Pinto, A. F., Dobrovolski, R., Veiga, A. B., and Guirnarães, J. A. (2004) Lonofibrase, a novel α-filbrinogenase from Lonomia obliqua caterpillars. Thromb. Res. 113, 147-154
46. Francischetti, I. M., Mather, T. N., and Ribeiro, J. M.(2003) Cloning of a salivary gland metalloprotease and characterization of gelatinase and fibrin(ogen)lytic activities in the saliva of the Lyme disease tick vector ixodes scapularis. Biochem. Biophys. Res. Commun. 305, 869-875
47. Irie, Y., Mori, F., Keung, W. M., Mizushima, Y., and Wakabayashi, K. (2004) Expression of neuronal growth inhibitory factor (metallothionein-III) in the salivary gland. Physiol. Res. 53, 719-723