The mechanism of αIIbβ3 antagonism by savignygrin and its implications for the evolution of anti-hemostatic strategies in soft ticks

Insect Biochemistry and Molecular Biology

Volumn 34, Issue 6, 2004, Pages 573-584

  Mans, Ben J ^a   Neitz, Albert W ^a  

^a UNIVERSITY OF PRETORIA   (South Africa)

Author keywords

IIb 3; Anti hemostatic; Platelet aggregation inhibition; Savignygrin; Tick

Indexed keywords

ACARI; ARGASIDAE; ORNITHODOROS MOUBATA;

ANTITHROMBOCYTIC AGENT; FIBRINOGEN RECEPTOR; HEMOSTATIC AGENT; INSECT PROTEIN; PROTEIN; SAVIGNYGRIN PROTEIN, ORNITHODOROS SAVIGNYI;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; FLOW CYTOMETRY; GENETICS; METABOLISM; METHODOLOGY; MOLECULAR EVOLUTION; MOLECULAR GENETICS; PHYSIOLOGY; PROTEIN BINDING; THROMBOCYTE; THROMBOCYTE AGGREGATION; TICK;

AMINO ACID SEQUENCE; ANIMALS; ARGASIDAE; BLOOD PLATELETS; EVOLUTION, MOLECULAR; FLOW CYTOMETRY; HEMOSTATICS; INSECT PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PLATELET AGGREGATION; PLATELET AGGREGATION INHIBITORS; PLATELET GLYCOPROTEIN GPIIB-IIIA COMPLEX; PROTEIN BINDING; PROTEINS;

EID: 2442539131     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2004.03.005     Document Type: Article

References (50)

1. Andersen J.F., Francischetti I.M., Valenzuela J.G., Schuck P., Ribeiro J.M.C. Inhibition of hemostasis by a high affinity biogenic amine-binding protein from the saliva of a blood-feeding insect. Journal of Biological Chemistry. 278:2002;4611-4617
2. Balashov Y.S. Interaction between blood-sucking arthropods and their hosts, and its influence on vector potential. Annual Reviews of Entomology. 29:1984;137-156
3. Bidlingmeyer B.A., Steven A.C., Tarvin T.L. Rapid analysis of amino acid using pre-column derivatization. Journal of Chromatography. 336:1984;93-104
4. 3, the fibrinogen receptor. Proceedings of the Society of Experimental Biology and Medicine. 208:1995;346-360
5. Calvete J.J., McLane M.A., Stewart G.J., Niewiarowski S. Characterization of the cross-linking site of disintegrins albolabrin, bitistatin, echistatin and eristostatin on isolated human platelet integrin GPIIb/IIIa. Biochemical and Biophysical Research Communications. 202:1994;135-140
6. Champagne D.E., Nussenzvieg R.H., Ribeiro J.M.C. Purification, partial characterization and cloning of nitric oxide-carrying heme proteins nitrophorins from salivary glands of the blood-sucking insect Rhodnius prolixus. Journal of Biological Chemistry. 270:1995;8691-8695
7. Cierniewski C.S., Byzova T., Papierak M., Haas T.A., Niewiarowska J., Zhang L., Cieslak M., Plow E.F. Peptide ligands can bind to distinct sites in integrin alphaIIbbeta3 and elicit different functional responses. Journal of Biological Chemistry. 274:1999;16923-16932
8. Cuatrecasas P., Hollenberg M.D. Membrane receptors and hormone action. Advances in Protein Chemistry. 30:1976;251-451
9. Doolittle R.F., Feng D.F. Reconstructing the evolution of vertebrate blood coagulation from a consideration of the amino acid sequences of clotting proteins. Cold Spring Harbor Symposium on Quantitative Biology. LII:1987;869-874
10. D'Souza S.E., Ginsberg M.H., Matsueda G.R., Plow E.F. A discrete sequence in a platelet integrin is involved in ligand recognition. Nature. 350:1991;66-68
11. D'Souza S.E., Haas T.A., Piotrowicz R.S., Byers-Ward V., McGrath D.E., Soule H.R., Cierniewski C., Plow E.F., Smith J.W. Ligand and cation binding are dual functions of a discrete segment of the integrin beta3 subunit: cation displacement is involved in ligand binding. Cell. 79:1994;659-667
12. Francischetti I.M.B., Ribeiro J.M.C., Champagne D., Andersen J. Purification, cloning, expression and mechanism of action of a novel platelet aggregation inhibitor from the salivary glands of the blood-sucking bug, Rhodnius prolixus. Journal of Biological Chemistry. 275:2000;12639-12650
13. Fuentes-Prior P., Noeske-Jungblut C., Donner P., Schleuning W., Huber R., Bode W. Structure of the thrombin complex with triabin, a lipocalin-like exosite-binding inhibitor derived from a triatomine bug. Proceedings of the National Academy of Sciences USA. 94:1997;11845-11850
14. Gould R.J., Polokoff M.A., Friedman P.A., Huang T.F., Holt J.C., Cook J.J., Niewiarowski S. Disintegrins: a family of integrin inhibitory proteins from viper venoms. Proceedings of the Society of Experimental Biology and Medicine. 195:1990;168-171
15. Guex N., Peitsch M.C. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis. 18:1997;2714-2723
16. Hantgan R.R., Rocco M., Nagaswami C., Weisel J.W. Binding of a fibrinogen mimetic stabilizes integrin alphaIIbbeta3's open conformation. Protein Science. 10:2001;1614-1626
17. Huang T.F. What have snakes taught us about integrins? Cellular and Molecular Life Sciences. 54:1998;527-540
18. Hughes A.L. The evolution of functionally novel proteins after gene duplication. Proceedings of the Royal Society of London B. 256:1994;119-124
19. Jeanmougin F., Thompson J.D., Gouy M., Higgins D.G., Gibson T.J. Multiple sequence alignment with ClustalX. Trends in Biochemical Sciences. 23:1998;403-405
20. Karczewski J., Connolly T.M. The interaction of disagregin with the platelet fibrinogen receptor, glycoprotein IIb-IIIa. Biochemical and Biophysical Research Communications. 241:1997;744-748
21. Karczewski J., Endris R., Connolly T.M. Disagregin is a fibrinogen receptor antagonist lacking the Arg-Gly-Asp sequence from the tick, Ornithodoros moubata. Journal of Biological Chemistry. 269:1994;6702-6708
22. Krezel A.M., Wagner G., Seymour-Ulmer J., Lazarus R.A. Structure of the RGD protein decorsin: conserved motif and distinct function in leech proteins that affect blood clotting. Science. 264:1994;1944-1947
23. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:1970;680-685
24. Laskowski M. Jr., Kato I. Protein inhibitors of proteinases. Annual Review of Biochemistry. 49:1980;593-626
25. Law J.H., Ribeiro J.M.C., Wells M.A. Biochemical insights derived from insect diversity. Annual Review of Biochemistry. 64:1992;87-111
26. Lazarus R.A., McDowell R.S. Structural and functional aspects of RGD-containing protein antagonists of glycoprotein IIb-IIIa. Current Opinion in Biotechnology. 4:1993;438-445
27. Liu C.Z., Wang Y.W., Shen M.C., Huang T.F. Analysis of human platelet glycoprotein IIb-IIIa by fluorescein isothiocyanate-conjugated disintegrins with flow cytometry. Thrombosis and Haemostasis. 72:1994;919-925
28. Luo B.H., Springer T.A., Takagi J. High affinity ligand binding by integrins does not involve head separation. Journal of Biological Chemistry. 278:2003;17185-17189
29. Mans B.J., Neitz A.W.H. Adaptation of ticks to a blood-feeding environment: evolution from a functional perspective. Insect Biochemistry and Molecular Biology. 34:2004;1-17
30. Mans B.J., Louw A.I., Gaspar A.R.M.D., Neitz A.W.H. Apyrase activity and platelet aggregation inhibitors in the tick Ornithodoros savignyi. Experimental and Applied Acarology. 22:1998;353-366
31. Mans B.J., Venter J.D., Vrey P.J., Louw A.I., Neitz A.W.H. Identification of putative proteins involved in granule biogenesis of tick salivary glands. Electrophoresis. 22:2001;1739-1746
32. Mans B.J., Louw A.I., Neitz A.W.H. Savignygrin, a platelet aggregation inhibitor from the soft tick, Ornithodoros savignyi, presents the RGD integrin recognition motif on the Kunitz-BPTI fold. Journal of Biological Chemistry. 277:2002a;21371-21378
33. Mans B.J., Louw A.I., Neitz A.W.H. Evolution of hematophagy in ticks: common origins for blood coagulation and platelet aggregation inhibitors from soft ticks of the genus Ornithodoros. Molecular Biology and Evolution. 19:2002b;1695-1705
34. Mans B.J., Louw A.I., Neitz A.W.H. Disaggregation of aggregated platelets by savignygrin, a alphaIIb beta3 antagonist from Ornithodoros savignyi. Experimental and Applied Acarology. 27:2002c;231-239
35. Noeske-Jungblut C., Haendler B., Donner P., Alagon A., Possani L., Schleuning W.D. Triabin, a highly potent exosite inhibitor of thrombin. Journal of Biological Chemistry. 270:1995;28629-28634
36. Nuttall P.A., Paesen G.C., Lawrie C.H., Wang H. Vector-host interactions in disease transmission. Journal of Molecular Microbiology and Biotechnology. 2:2000;381-386
37. Reddy V.B., Kounga K., Mariano F., Lerner E.A. Chrysoptin is a potent glycoprotein IIb/IIIa fibrinogen receptor antagonist present in salivary gland extracts of the deerfly. Journal of Biological Chemistry. 275:2000;15861-15867
38. Ribeiro J.M. Blood-feeding arthropods: live syringes or invertebrate pharmacologists? Infectious Agents and Disease. 4:1995;143-152
39. Ribeiro J.M., Francischetti I.M. Role of arthropod saliva in blood feeding: sialome and post-sialome perspectives. Annual Reviews of Entomology. 48:2003;73-88
40. Ribeiro J.M., Schneider M., Guimaraes J.A. Purification and characterization of prolixin S nitrophorin 2, the salivary anticoagulant of the blood-sucking bug Rhodnius prolixus. Biochemical Journal. 308:1995;243-249
41. Ribeiro J.M.C., Andersen J., Silva-Neto M.A.C., Pham V.M., Garfield M.K., Valenzuela J.G. Exploring the sialome of the blood-sucking bug Rhodnius prolixus. Insect Biochemistry and Molecular Biology. 34:2003;61-79
42. Sali A., Potterton L., Yuan F., van Vlijmen H., Karplus M. Evaluation of comparative protein modeling by MODELLER. Proteins. 23:1995;318-326
43. Scarborough R.M., Rose J.W., Hsu M.A., Phillips D.R., Fried V.A., Campbell A.M., Nannizzi L., Charo I.F. Barbourin. A GPIIb-IIIa-specific integrin antagonist from the venom of Sistrurus m. barbouri. Journal of Biological Chemistry. 266:1991;9359-9362
44. Thibault G. Sodium dodecyl sulfate-stable complexes of echistatin and RGD-dependent integrins: a novel approach to study integrins. Molecular Pharmacology. 58:2000;1137-1145
45. Tozer E.C., Liddington R.C., Sutcliffe M.J., Smeeton A.H., Loftus J.C. Ligand binding to integrin alphaIIbbeta3 is dependent on a MIDAS-like domain in the beta3 subunit. Journal of Biological Chemistry. 271:1996;21978-21984
46. Van de Locht A., Stubbs M.T., Bode W., Friedrich T., Bollschweiler C., Hoffken W., Huber R. The ornithodorin-thrombin crystal structure, a key to the TAP enigma? EMBO Journal. 15:1996;6011-6017
47. Wang X., Coons L.B., Taylor D.B., Stevens S.E., Gartner T.K. Variabilin, a novel RGD-containing antagonist of glycoprotein IIb-IIIa and platelet aggregation inhibitor from the hard tick Dermacentor variabilis. Journal of Biological Chemistry. 271:1996;17785-17790
48. Wei A., Alexander R.S., Duke J., Ross H., Rosenfeld S.A., Chang C.H. Unexpected binding mode of tick anticoagulant peptide complexed to bovine factor Xa. Journal of Molecular Biology. 283:1998;147-154
49. Xiong J.P., Stehle T., Zhang R., Joachimiak A., Frech M., Goodman S.L., Arnaout M.A. Crystal structure of the extracellular segment of integrin alphaVbeta3 in complex with an Arg-Gly-Asp ligand. Science. 296:2002;151-155
50. Zolotarjova N.I., Hollis G.F., Wynn R. Unusually stable and long-lived ligand-induced conformations of integrins. Journal of Biological Chemistry. 276:2001;17063-17068