Role for platelet glycoprotein Ib-IX and effects of its inhibition in endotoxemia-induced thrombosis, thrombocytopenia, and mortality

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 33, Issue 11, 2013, Pages 2529-2537

  Yin, Hong ^a   Stojanovic Terpo, Aleksandra ^a   Xu, Weidong ^a   Corken, Adam ^d   Zakharov, Alexander ^a   Qian, Feng ^a   Pavlovic, Sasha ^c   Krbanjevic, Aleksandar ^a   Lyubimov, Alexander V ^a   Wang, Zaijie J ^b   Ware, Jerry ^d   Du, Xiaoping ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

^b Department of Medicine   (United States)

^c UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^d UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

Author keywords

endotoxemia; GPIb IX; lipopolysaccharide; platelet; platelet inhibitor; thrombocytopenia; thrombosis

Indexed keywords

ANTITHROMBOCYTIC AGENT; EPTIFIBATIDE; GLYCOPROTEIN; GLYCOPROTEIN IB IX; LIPOPOLYSACCHARIDE; MPALPHAC; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERY THROMBOSIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DRUG EFFECT; ENDOTHELIUM CELL; ENDOTOXEMIA; HUMAN; HUMAN CELL; LIGAND BINDING; MICELLE; MORTALITY; MOUSE; MYRISTYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SHEAR STRESS; SURVIVAL RATE; THROMBOCYTE ACTIVATION; THROMBOCYTE ADHESION; THROMBOCYTE AGGREGATION; THROMBOCYTE FUNCTION; THROMBOCYTOPENIA; UMBILICAL VEIN ENDOTHELIAL CELL;

ENDOTOXEMIA; GPIB-IX; LIPOPOLYSACCHARIDE; PLATELET; PLATELET INHIBITOR; THROMBOCYTOPENIA; THROMBOSIS;

ANIMALS; ENDOTHELIUM, VASCULAR; ENDOTOXEMIA; HUMANS; LIPOPOLYSACCHARIDES; MEMBRANE GLYCOPROTEINS; MICE; MICE, TRANSGENIC; PEPTIDES; PLATELET ADHESIVENESS; PLATELET AGGREGATION INHIBITORS; PLATELET GLYCOPROTEIN GPIB-IX COMPLEX; RECOMBINANT FUSION PROTEINS; THROMBOCYTOPENIA; THROMBOSIS; VON WILLEBRAND FACTOR;

EID: 84887091084     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.113.302339     Document Type: Article

References (46)

1. Opal SM, Esmon CT. Bench-to-bedside review: functional relationships between coagulation and the innate immune response and their respective roles in the pathogenesis of sepsis. Crit Care. 2003;7:23-38.
2. Hotchkiss RS, Karl IE. The pathophysiology and treatment of sepsis. N Engl J Med. 2003;348:138-150.
3. Bernard GR, Vincent JL, Laterre PF, LaRosa SP, Dhainaut JF, Lopez-Rodriguez A, Steingrub JS, Garber GE, Helterbrand JD, Ely EW, Fisher CJ Jr; Recombinant human protein C Worldwide Evaluation in Severe Sepsis (PROWESS) study group. Effcacy and safety of recombinant human activated protein C for severe sepsis. N Engl J Med. 2001;344:699-709.
4. Benefeld RJ, Drevets DA, Huycke MM, Gentry CA. A multicenter evaluation of the safety of drotrecogin alfa (activated) in patients with baseline bleeding precautions. Curr Drug Saf. 2012;7:3-7.
5. Zhang G, Han J, Welch EJ, Ye RD, Voyno-Yasenetskaya TA, Malik AB, Du X, Li Z. Lipopolysaccharide stimulates platelet secretion and potentiates platelet aggregation via TLR4/MyD88 and the cGMP-dependent protein kinase pathway. J Immunol. 2009;182:7997-8004.
6. Shibazaki M, Nakamura M, Endo Y. Biphasic, organ-specifc, and strain-specifc accumulation of platelets induced in mice by a lipopolysaccharide from Escherichia coli and its possible involvement in shock. Infect Immun. 1996;64:5290-5294.
7. Shibazaki M, Kawabata Y, Yokochi T, Nishida A, Takada H, Endo Y. Complement-dependent accumulation and degradation of platelets in the lung and liver induced by injection of lipopolysaccharides. Infect Immun. 1999;67:5186-5191.
8. Davis RB, Meeker WR, McQuarrie DG. Immediate effects of intravenous endotoxin on serotonin concentrations and blood platelets. Circ Res. 1960;8:234-239.
9. Davis RB, Palmer MJ. Thrombocytopenia and release of platelet amines induced by thrombin and bacterial lipopolysaccharide. Observations after infusion of low molecular weight dextran. Br J Exp Pathol. 1965;46:554-563.
10. Ruggeri ZM, Mendolicchio GL. Adhesion mechanisms in platelet function. Circ Res. 2007;100:1673-1685.
11. Du X. Signaling and regulation of the platelet glycoprotein Ib-IX-V complex. Curr Opin Hematol. 2007;14:262-269.
12. Li Z, Delaney MK, O'Brien KA, Du X. Signaling during platelet adhesion and activation. Arterioscler Thromb Vasc Biol. 2010;30:2341-2349.
13. Brill A, Fuchs TA, Chauhan AK, Yang JJ, De Meyer SF, Köllnberger M, Wakefeld TW, Lämmle B, Massberg S, Wagner DD. von Willebrand factor-mediated platelet adhesion is critical for deep vein thrombosis in mouse models. Blood. 2011;117:1400-1407.
14. Joglekar MV, Ware J, Xu J, Fitzgerald ME, Gartner TK. Platelets, glyco-protein Ib-IX, and von Willebrand factor are required for FeCl(3)-induced occlusive thrombus formation in the inferior vena cava of mice. Platelets. 2013;24:205-212.
15. Ware J. Molecular analyses of the platelet glycoprotein Ib-IX-V receptor. Thromb Haemost. 1998;79:466-478.
16. Fox JE. Identifcation of actin-binding protein as the protein linking the membrane skeleton to glycoproteins on platelet plasma membranes. J Biol Chem. 1985;260:11970-11977.
17. Andrews RK, Fox JE. Identifcation of a region in the cytoplasmic domain of the platelet membrane glycoprotein Ib-IX complex that binds to puri-fed actin-binding protein. J Biol Chem. 1992;267:18605-18611.
18. Du X, Fox JE, Pei S. Identifcation of a binding sequence for the 14-3-3 protein within the cytoplasmic domain of the adhesion receptor, platelet glycoprotein Ib alpha. J Biol Chem. 1996;271:7362-7367.
19. Andrews RK, Harris SJ, McNally T, Berndt MC. Binding of purifed 14-3-3 zeta signaling protein to discrete amino acid sequences within the cytoplasmic domain of the platelet membrane glycoprotein Ib-IX-V complex. Biochemistry. 1998;37:638-647.
20. Mangin P, David T, Lavaud V, Cranmer SL, Pikovski I, Jackson SP, Berndt MC, Cazenave JP, Gachet C, Lanza F. Identifcation of a novel 14-3-3zeta binding site within the cytoplasmic tail of platelet glycoprotein Ibalpha. Blood. 2004;104:420-427.
21. Bodnar RJ, Gu M, Li Z, Englund GD, Du X. The cytoplasmic domain of the platelet glycoprotein Ibalpha is phosphorylated at serine 609. J Biol Chem. 1999;274:33474-33479.
22. Dai K, Bodnar R, Berndt MC, Du X. A critical role for 14-3-3zeta protein in regulating the VWF binding function of platelet glycoprotein Ib-IX and its therapeutic implications. Blood. 2005;106:1975-1981.
23. Jain S, Zuka M, Liu J, Russell S, Dent J, Guerrero JA, Forsyth J, Maruszak B, Gartner TK, Felding-Habermann B, Ware J. Platelet glycoprotein Ib alpha supports experimental lung metastasis. Proc Natl Acad Sci USA. 2007;104:9024-9028.
24. Krishnadas A, Rubinstein I, Onyüksel H. Sterically stabilized phospho-lipid mixed micelles: in vitro evaluation as a novel carrier for water-insoluble drugs. Pharm Res. 2003;20:297-302.
25. Kanaji T, Russell S, Ware J. Amelioration of the macrothrombocyto-penia associated with the murine Bernard-Soulier syndrome. Blood. 2002;100:2102-2107.
26. Yin H, Stojanovic A, Hay N, Du X. The role of Akt in the signaling pathway of the glycoprotein Ib-IX induced platelet activation. Blood. 2008;111:658-665.
27. Yin H, Liu J, Li Z, Berndt MC, Lowell CA, Du X. Src family tyrosine kinase Lyn mediates VWF/GPIb-IX-induced platelet activation via the cGMP signaling pathway. Blood. 2008;112:1139-1146.
28. Ware J, Russell S, Ruggeri ZM. Generation and rescue of a murine model of platelet dysfunction: the Bernard-Soulier syndrome. Proc Natl Acad Sci USA. 2000;97:2803-2808.
29. Bergmeier W, Piffath CL, Goerge T, Cifuni SM, Ruggeri ZM, Ware J, Wagner DD. The role of platelet adhesion receptor GPIbalpha far exceeds that of its main ligand, von Willebrand factor, in arterial thrombosis. Proc Natl Acad Sci USA. 2006;103:16900-16905.
30. Stark RJ, Aghakasiri N, Rumbaut RE. Platelet-derived Toll-like receptor 4 (Tlr-4) is suffcient to promote microvascular thrombosis in endotoxemia. PLoS One. 2012;7:e41254.
31. Seok J, Warren HS, Cuenca AG, et al.; Infammation and Host Response to Injury, Large Scale Collaborative Research Program. Genomic responses in mouse models poorly mimic human infammatory diseases. Proc Natl Acad Sci USA. 2013;110:3507-3512.
32. Zheng XL, Sadler JE. Pathogenesis of thrombotic microangiopathies. Annu Rev Pathol. 2008;3:249-277.
33. André P, Denis CV, Ware J, Saffaripour S, Hynes RO, Ruggeri ZM, Wagner DD. Platelets adhere to and translocate on von Willebrand factor presented by endothelium in stimulated veins. Blood. 2000;96:3322-3328.
34. Padilla A, Moake JL, Bernardo A, Ball C, Wang Y, Arya M, Nolasco L, Turner N, Berndt MC, Anvari B, López JA, Dong JF. P-selectin anchors newly released ultralarge von Willebrand factor multimers to the endothe-lial cell surface. Blood. 2004;103:2150-2156.
35. Nguyen TC, Liu A, Liu L, Ball C, Choi H, May WS, Aboulfatova K, Bergeron AL, Dong JF. Acquired ADAMTS-13 defciency in pediatric patients with severe sepsis. Haematologica. 2007;92:121-124.
36. Bockmeyer CL, Claus RA, Budde U, Kentouche K, Schneppenheim R, Lösche W, Reinhart K, Brunkhorst FM. Infammation-associated ADAMTS13 defciency promotes formation of ultra-large von Willebrand factor. Haematologica. 2008;93:137-140.
37. Lerolle N, Dunois-Lardé C, Badirou I, Motto DG, Hill G, Bruneval P, Diehl JL, Denis CV, Baruch D. von Willebrand factor is a major determinant of ADAMTS-13 decrease during mouse sepsis induced by cecum ligation and puncture. J Thromb Haemost. 2009;7:843-850.
38. Chauhan AK, Walsh MT, Zhu G, Ginsburg D, Wagner DD, Motto DG. The combined roles of ADAMTS13 and VWF in murine models of TTP, endotoxemia, and thrombosis. Blood. 2008;111:3452-3457.
39. Romo GM, Dong JF, Schade AJ, Gardiner EE, Kansas GS, Li CQ, McIntire LV, Berndt MC, López JA. The glycoprotein Ib-IX-V complex is a platelet counterreceptor for P-selectin. J Exp Med. 1999;190:803-814.
40. Weeterings C, de Groot PG, Adelmeijer J, Lisman T. The glycoprotein Ib-IX-V complex contributes to tissue factor-independent thrombin generation by recombinant factor VIIa on the activated platelet surface. Blood. 2008;112:3227-3233.
41. Simon DI, Chen Z, Xu H, Li CQ, Dong Jf, McIntire LV, Ballantyne CM, Zhang L, Furman MI, Berndt MC, López JA. Platelet glycoprotein ibalpha is a counterreceptor for the leukocyte integrin Mac-1 (CD11b/CD18). J Exp Med. 2000;192:193-204.
42. Wang Y, Sakuma M, Chen Z, Ustinov V, Shi C, Croce K, Zago AC, Lopez J, Andre P, Plow E, Simon DI. Leukocyte engagement of platelet glycoprotein Ibalpha via the integrin Mac-1 is critical for the biological response to vascular injury. Circulation. 2005;112:2993-3000.
43. Chauhan AK, Goerge T, Schneider SW, Wagner DD. Formation of platelet strings and microthrombi in the presence of ADAMTS-13 inhibitor does not require P-selectin or beta3 integrin. J Thromb Haemost. 2007;5:583-589.
44. Grewal PK, Uchiyama S, Ditto D, Varki N, Le DT, Nizet V, Marth JD. The Ashwell receptor mitigates the lethal coagulopathy of sepsis. Nat Med. 2008;14:648-655.
45. Hoffmeister KM, Felbinger TW, Falet H, Denis CV, Bergmeier W, Mayadas TN, von Andrian UH, Wagner DD, Stossel TP, Hartwig JH. The clearance mechanism of chilled blood platelets. Cell. 2003;112:87-97.
46. Rumjantseva V, Grewal PK, Wandall HH, Josefsson EC, Sørensen AL, Larson G, Marth JD, Hartwig JH, Hoffmeister KM. Dual roles for hepatic lectin receptors in the clearance of chilled platelets. Nat Med. 2009;15:1273-1280.