Rhinocetin, a venom-derived integrin-specific antagonist inhibits collagen-induced platelet and endothelial cell functions

Journal of Biological Chemistry

Volumn 287, Issue 31, 2012, Pages 26235-26244

  Vaiyapuri, Sakthivel ^a   Hutchinson, E Gail ^a   Ali, Marfoua S ^a   Dannoura, Abeer ^a   Stanley, Ronald G ^a   Harrison, Robert A ^b   Bicknell, Andrew B ^a   Gibbins, Jonathan M ^a,c  

^a UNIVERSITY OF READING   (United Kingdom)

^b LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

^c KING SAUD UNIVERSITY   (Saudi Arabia)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM MOBILIZATION; COIMMUNOPRECIPITATION ANALYSIS; COLLAGEN RECEPTORS; DOSE-DEPENDENT MANNER; HUMAN ENDOTHELIAL CELLS; IMMUNOBLOT ANALYSIS; INHIBITORY EFFECT; INTEGRINS; NON-ENZYMATIC; PATHOPHYSIOLOGICAL; PLATELET ACTIVATION; SMOOTH MUSCLE CELLS; THROMBUS FORMATION;

COLLAGEN; ENDOTHELIAL CELLS; MONOCLONAL ANTIBODIES; PHYSIOLOGY;

PLATELETS;

ADENOSINE DIPHOSPHATE; CALCIUM; CARRIER PROTEINS AND BINDING PROTEINS; COLLAGEN; COLLAGEN RELATED PEPTIDE CROSSS LINKED PROTEIN; FIBRINOGEN; HETERODIMER; INHIBITOR PROTEIN; MONOCLONAL ANTIBODY; RHINOCETIN; THROMBIN; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 2;

ALPHA CHAIN; ANTIGEN BINDING; ARTICLE; BETA CHAIN; CALCIUM MOBILIZATION; CELL FUNCTION; CELL GRANULE; CONTROLLED STUDY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; IN VITRO STUDY; INTRACELLULAR SIGNALING; MOLECULAR WEIGHT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN ISOLATION; PROTEIN PURIFICATION; PROTEIN TARGETING; SEQUENCE ANALYSIS; SNAKE; STRUCTURE ANALYSIS; THROMBOCYTE ACTIVATION; THROMBOCYTE AGGREGATION; THROMBOCYTE FUNCTION; THROMBOGENESIS;

AMINO ACID SEQUENCE; ANIMALS; BLOOD COAGULATION; BLOOD PLATELETS; CALCIUM SIGNALING; CELL ADHESION; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; COLLAGEN; ENDOTHELIAL CELLS; HEMATOLOGIC AGENTS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INTEGRIN ALPHA2BETA1; MOLECULAR SEQUENCE DATA; PLATELET AGGREGATION; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; SECRETORY VESICLES; SEQUENCE ANALYSIS, PROTEIN; SEQUENCE HOMOLOGY, AMINO ACID; VIPER VENOMS; VIPERIDAE;

BITIS GABONICA; RHINOCEROS; VIPERINAE;

EID: 84864386809     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.381483     Document Type: Article

References (53)

1. Kasturiratne, A., Wickremasinghe, A. R., de Silva, N., Gunawardena, N. K., Pathmeswaran, A., Premaratna, R., Savioli, L., Lalloo, D. G., and de Silva, H. J. (2008) The global burden of snakebite: A literature analysis and modeling based on regional estimates of envenoming and deaths. PLoS Med. 5, e218
2. Aird, S. D. (2002) Ophidian envenomation strategies and the role of purines. Toxicon 40, 335-393
3. White, J. (2005) Snake venoms and coagulopathy. Toxicon 45, 951-967
4. Gutiérrez, J. M., Williams, D., Fan, H. W., and Warrell, D. A. (2010) Snake-bite envenoming from a global perspective: Towards an integrated approach. Toxicon 56, 1223-1235
5. Fox, J. W., and Serrano, S. M. (2009) Timeline of key events in snake venom metalloproteinase research. J. Proteomics 72, 200-209
6. Doley, R., and Kini, R. M. (2009) Protein complexes in snake venom. Cell Mol. Life Sci. 66, 2851-2871
7. Kini, R. M. (2005) Serine proteases affecting blood coagulation and fibrinolysis from snake venoms. Pathophysiol. Haemost. Thromb. 34, 200-204
8. Marcinkiewicz, C. (2005) Functional characteristic of snake venom disintegrins: Potential therapeutic implication. Curr. Pharm. Des. 11, 815-827
9. Clemetson, K. J. (2010) Snaclecs (snake C-type lectins) that inhibit or activate platelets by binding to receptors. Toxicon 56, 1236-1246
10. Sajevic, T., Leonardi, A., and Križaj, I. (2011) Haemostatically active proteins in snake venoms. Toxicon 57, 627-645
11. Morita, T. (2005) Structures and functions of snake venom CLPs (C-type lectin-like proteins) with anticoagulant-, procoagulant-, and platelet-modulating activities. Toxicon 45, 1099-1114
12. Zelensky, A. N., and Gready, J. E. (2005) The C-type lectin-like domain superfamily. FEBS J. 272, 6179-6217 (Pubitemid 41815610)
13. Drickamer, K. (1999) C-type lectin-like domains. Curr. Opin. Struct. Biol. 9, 585-590
14. Du, X. Y., Clemetson, J. M., Navdaev, A., Magnenat, E. M., Wells, T. N., and Clemetson, K. J. (2002) Ophioluxin, a convulxin-like C-type lectin from Ophiophagus hannah (king cobra) is a powerful platelet activator via glycoprotein VI. J. Biol. Chem. 277, 35124-35132
15. 4 cyclic tetramer from the venom of Crotalus durissus terrificus. Biochem. Biophys. Res. Commun. 310, 478-482
16. Polgár, J., Clemetson, J. M., Kehrel, B. E., Wiedemann, M., Magnenat, E. M., Wells, T. N., and Clemetson, K. J. (1997) Platelet activation and signal transduction by convulxin, a C-type lectin from Crotalus durissus terrificus (tropical rattlesnake) venom via the p62/GPVI collagen receptor. J. Biol. Chem. 272, 13576-13583 (Pubitemid 27224788)
17. Zhong, S. R., Jin, Y., Wu, J. B., Chen, R. Q., Jia, Y. H., Wang, W. Y., Xiong, Y. L., and Zhang, Y. (2006) Characterization and molecular cloning of dabocetin, a potent antiplatelet C-type lectin-like protein from Daboia russellii siamensis venom. Toxicon 47, 104-112 (Pubitemid 43042401)
18. Peng, M., Lu, W., Beviglia, L., Niewiarowski, S., and Kirby, E. P. (1993) Echicetin: A snake venom protein that inhibits binding of von Willebrand factor and alboaggregins to platelet glycoprotein Ib. Blood 81, 2321-2328 (Pubitemid 23127066)
19. Sarray, S., Srairi, N., Hatmi, M., Luis, J., Louzir, H., Regaya, I., Slema, H., Marvaldi, J., El Ayeb, M., and Marrakchi, N. (2003) Lebecetin, a potent antiplatelet C-type lectin from Macrovipera lebetina venom. Biochim. Biophys. Acta 1651, 30-40 (Pubitemid 38234550)
20. Fox, J. W., and Serrano, S. M. (2007) Approaching the golden age of natural product pharmaceuticals from venom libraries: An overview of toxins and toxin derivatives currently involved in therapeutic or diagnostic applications. Curr. Pharm. Des. 13, 2927-2934 (Pubitemid 351545895)
21. Marsh, N., and Williams, V. (2005) Practical applications of snake venom toxins in haemostasis. Toxicon 45, 1171-1181 (Pubitemid 40732589)
22. Read, M. S., Potter, J. Y., and Brinkhous, K. M. (1983) Venom coagglutinin for detection of von Willebrand factor activity in animal plasmas. J. Lab. Clin. Med. 101, 74-82 (Pubitemid 13170297)
23. Vaiyapuri, S., Harrison, R. A., Bicknell, A. B., Gibbins, J. M., and Hutchinson, G. (2010) Purification and functional characterisation of rhinocerase, a novel serine protease from the venom of Bitis gabonica rhinoceros. PLoS One 5, e9687
24. Vaiyapuri, S., Wagstaff, S. C., Harrison, R. A., Gibbins, J. M., and Hutchinson, E. G. (2011) Evolutionary analysis of novel serine proteases in the venom gland transcriptome of Bitis gabonica rhinoceros. PLoS One 6, e21532
25. Vaiyapuri, S., Wagstaff, S. C., Watson, K. A., Harrison, R. A., Gibbins, J. M., and Hutchinson, E. G. (2010) Purification and functional characterization of rhiminopeptidase A, a novel aminopeptidase from the venom of Bitis gabonica rhinoceros. PLoS Negl. Trop. Dis. 4, e796
26. Rice, P., Longden, I., and Bleasby, A. (2000) EMBOSS: The European Molecular Biology Open Software Suite. Trends Genet. 16, 276-277
27. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., and Higgins, D. G. (2007) Clustal W and Clustal X (version 2.0). Bioinformatics 23, 2947-2948
28. Francischetti, I. M., My-Pham, V., Harrison, J., Garfield, M. K., and Ribeiro, J. M. (2004) Bitis gabonica (Gaboon viper) snake venom gland: Toward a catalog for the full-length transcripts (cDNA) and proteins. Gene. 337, 55-69 (Pubitemid 38970105)
29. Kaiser, W. J., Holbrook, L. M., Tucker, K. L., Stanley, R. G., and Gibbins, J. M. (2009) A functional proteomic method for the enrichment of peripheral membrane proteins reveals the collagen binding protein Hsp47 is exposed on the surface of activated human platelets. J. Proteome. Res. 8, 2903-2914
30. Vaiyapuri, S., Jones, C. I., Sasikumar, P., Moraes, L. A., Munger, S. J., Wright, J. R., Ali, M. S., Sage, T., Kaiser, W. J., Tucker, K. L., Stain, C. J., Bye, A. P., Jones, S., Oviedo-Orta, E., Simon, A. M., Mahaut-Smith, M. P., and Gibbins, J. M. (2012) Gap junctions and connexin hemichannels underpin hemostasis and thrombosis. Circulation 125, 2479-2491
31. Spyridon, M., Moraes, L. A., Jones, C. I., Sage, T., Sasikumar, P., Bucci, G., and Gibbins, J. M. (2011) LXR as a novel antithrombotic target. Blood 117, 5751-5761
32. Coller, B. S., Beer, J. H., Scudder, L. E., and Steinberg, M. H. (1989) Collagen- platelet interactions: Evidence for a direct interaction of collagen with platelet GPIa/IIa and an indirect interaction with platelet GPIIb/IIIa mediated by adhesive proteins. Blood 74, 182-192 (Pubitemid 19187427)
33. Harrison, R. A., Oliver, J., Hasson, S. S., Bharati, K., and Theakston, R. D. (2003) Novel sequences encoding venom C-type lectins are conserved in phylogenetically and geographically distinct Echis and Bitis viper species. Gene 315, 95-102 (Pubitemid 37214901)
34. Horii, K., Okuda, D., Morita, T., and Mizuno, H. (2004) Crystal structure of EMS16 in complex with the integrin α2-I domain. J. Mol. Biol. 341, 519-527 (Pubitemid 38992304)
35. 1 integrin-specific antagonist rhodocetin is a cruciform, heterotetrameric molecule. FASEB J. 23, 2917-2927
36. Gibbins, J. M. (2004) Platelet adhesion signaling and the regulation of thrombus formation. J. Cell Sci. 117, 3415-3425
37. Coughlin, S. R. (2005) Protease-activated receptors in hemostasis, thrombosis, and vascular biology. J. Thromb. Haemost. 3, 1800-1814
38. Calderwood, D. A. (2004) Integrin activation. J. Cell Sci. 117, 657-666
39. Hathaway, D. R., and Adelstein, R. S. (1979) Human platelet myosin light chain kinase requires the calcium-binding protein calmodulin for activity. Proc. Natl. Acad. Sci. U.S.A. 76, 1653-1657 (Pubitemid 9175375)
40. Shattil, S. J., and Brass, L. F. (1987) Induction of the fibrinogen receptor on human platelets by intracellular mediators. J. Biol. Chem. 262, 992-1000 (Pubitemid 17028403)
41. Berridge, M. J., Bootman, M. D., and Roderick, H. L. (2003) Calcium signaling: Dynamics, homeostasis, and remodeling. Nat. Rev. Mol. Cell Biol. 4, 517-529 (Pubitemid 36773404)
42. Smith, R. A., Mosesson, M. W., Rooney, M. M., Lord, S. T., Daniels, A. U., and Gartner, T. K. (1997) The role of putative fibrinogen Aα-, Bβ-, and γA-chain integrin binding sites in endothelial cell-mediated clot retraction. J. Biol. Chem. 272, 22080-22085 (Pubitemid 27382834)
43. Marcinkiewicz, C., Lobb, R. R., Marcinkiewicz, M. M., Daniel, J. L., Smith, J. B., Dangelmaier, C., Weinreb, P. H., Beacham, D. A., and Niewiarowski, S. (2000) Isolation and characterization of EMS16, a C-lectin type protein from Echis multisquamatus venom, a potent and selective inhibitor of the α2β1 integrin. Biochemistry 39, 9859-9867 (Pubitemid 30626834)
44. Wang, R., Kini, R. M., and Chung, M. C. (1999) Rhodocetin, a novel platelet aggregation inhibitor from the venom of Calloselasma rhodostoma (Malayan pit viper): synergistic and noncovalent interaction between its subunits. Biochemistry 38, 7584-7593
45. Staniszewska, I., Walsh, E. M., Rothman, V. L., Gaathon, A., Tuszynski, G. P., Calvete, J. J., Lazarovici, P., and Marcinkiewicz, C. (2009) Effect of VP12 and viperistatin on inhibition of collagen receptor-dependent melanoma metastasis. Cancer Biol. Ther. 8, 1507-1516
46. Calvete, J. J., Marcinkiewicz, C., Monleón, D., Esteve, V., Celda, B., Juárez, P., and Sanz, L. (2005) Snake venom disintegrins: Evolution of structure and function. Toxicon 45, 1063-1074 (Pubitemid 40732581)
47. Tuckwell, D., Calderwood, D. A., Green, L. J., and Humphries, M. J. (1995) Integrin α2 I-domain is a binding site for collagens. J. Cell Sci. 108, 1629-1637
48. Marsh, N. A., and Whaler, B. C. (1974) Separation and partial characterization of a coagulant enzyme from Bitis gabonica venom. Br J. Haematol 26, 295-306
49. Clemetson, K. J., and Clemetson, J. M. (2002) Platelet receptors in Platelets (Michelson, A. D., ed.) 2nd Ed., pp. 117-143, Elsevier, Burlington, MA
50. 1 integrin is expressed during neointima formation in rat arteries and mediates collagen matrix reorganization. J. Clin. Invest. 97, 2469-2477
51. Topol, E. J., Byzova, T. V., and Plow, E. F. (1999) Platelet GPIIb-IIIa blockers. Lancet 353, 227-231 (Pubitemid 29088046)
52. Latallo, Z. S., and Teisseyre, E. (1971) Evaluation of Reptilase R and thrombin clotting time in the presence of fibrinogen degradation products and heparin. Scand. J. Haematol. Suppl. 13, 261-266
53. Tokunaga, F., Nagasawa, K., Tamura, S., Miyata, T., Iwanaga, S., and Kisiel, W. (1988) The factor V-activating enzyme (RVV-V) from Russell's viper venom. Identification of isoproteins RVV-Vα, -Vβ, and -Vγ and their complete amino acid sequences. J. Biol. Chem. 263, 17471-17481 (Pubitemid 19029331)