αIIbβ3-mediated outside-in signaling induced by the agonist peptide LSARLAF utilizes ADP and thromboxane A2 receptors to cause α-granule secretion by platelets

Journal of Thrombosis and Haemostasis

Volumn 1, Issue 2, 2003, Pages 363-373

  Cho, M J ^a   Liu, J ^a   Pestina, T I ^b   Steward, S A ^b   Jackson, C W ^b   Gartner, T K ^a  

^a UNIVERSITY OF MEMPHIS   (United States)

^b ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

granule secretion; ADP and TxA2 signaling; Outside in signaling

Indexed keywords

ADENOSINE DIPHOSPHATE; FIBRINOGEN RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; HETEROTRIMERIC GUANINE NUCLEOTIDE BINDING PROTEIN; LEUCYL SERYL ALANYL ARGINYL LEUCYL ALANYL PHENYLALANINE; LEUCYL-SERYL-ALANYL-ARGINYL-LEUCYL-ALANYL-PHENYLALANINE; OLIGOPEPTIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE C; PURINE P2 RECEPTOR; THROMBOXANE RECEPTOR;

ANIMAL; ARTICLE; BLOOD; C57BL MOUSE; DEGRANULATION; DRUG EFFECT; FEMALE; IN VITRO STUDY; MALE; MOUSE; MOUSE MUTANT; PHYSIOLOGY; SIGNAL TRANSDUCTION; THROMBOCYTE; THROMBOCYTE AGGREGATION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ADENOSINE DIPHOSPHATE; ANIMALS; BLOOD PLATELETS; CELL DEGRANULATION; FEMALE; GTP-BINDING PROTEIN ALPHA SUBUNITS, GQ-G11; HETEROTRIMERIC GTP-BINDING PROTEINS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OLIGOPEPTIDES; PLATELET AGGREGATION; PLATELET GLYCOPROTEIN GPIIB-IIIA COMPLEX; PROTEIN KINASE C; RECEPTORS, PURINERGIC P2; RECEPTORS, THROMBOXANE; SIGNAL TRANSDUCTION;

EID: 0141561935     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1046/j.1538-7836.2003.00055.x     Document Type: Article

References (30)

1. Shattil SJ, Kashiwagi H, Pampori N. Integrin signaling: the platelet paradigm. Blood 1998; 91: 2645-57.
2. Huang MM, Lipfert L, Cunningham M, Brugge JS, Ginsberg MH, Shattil SJ. Adhesive ligand binding to integrin alpha IIb beta 3 stimulates tyrosine phosphorylation of novel protein substrates before phosphorylation of pp125FAK. J Cell Biol 1993; 122: 473-83.
3. Frelinger AL, Lam SC, Plow EF, Smith MA, Loftus JC, Ginsberg MH. Occupancy of an adhesive glycoprotein receptor modulates expression of an antigenic site involved in cell adhesion. J Biol Chem 1988; 263: 12397-402.
4. Frelinger AL, Xiaoping D, Plow EF, Ginsberg MH. Monoclonal antibodies to ligand-occupied conformers of integrin αIIbβ3 (glycoprotein IIb-IIIa) alter receptor affinity, specificity, and function. J Biol Chem 1991; 266: 17106-11.
5. Derrick JM, Taylor DB, Loudon RG, Gartner TK. The peptide LSARLAF causes platelet secretion and aggregation by directly activating the integrin αIIbβ3. Biochem J 1997; 325: 309-13.
6. Bansani RB, French DL, Vilaire G, Brown D, Fangping C, Coller BS, Derrick JM, Gartner TK, Bennett JS, Poncz M. A naturally occurring mutation near the amino terminus of αIIb defines a new region involved in ligand binding to αIIbβ3. Blood 2000; 95: 180-8.
7. Derrick JM, Shattil SJ, Poncz M, Gruppo RA, Gartner TK. Distinct domains of alpha IIb beta 3 support different aspects of outside-in signal transduction and platelet activation induced by LSARLAF, an alpha IIb beta 3 interacting peptide. Thromb Haemost 2001; 86: 894-901.
8. Jin J, Quinton TM, Zhang J, Rittenhouse SE, Kunapuli SP. Adenosine diphosphate (ADP)-induced thromboxane A2 generation in human platelets requires coordinated signaling through integrin αIIbβ3 and ADP receptors. Blood 2002; 99: 139-8.
9. Kauffenstein G, Bergmeier W, Eckly A, Ohlmann P, Leon C, Cazenave JP, Nieswandt B, Gachet C. The P2Y12 receptor induces platelet aggregation through weak activation of the αIIbβ3 integrin - a phosphoinositide 3-kinase-dependent mechanism. FEBS Letter 2001; 505: 281-90.
10. Cho MJ, Pestina TI, Steward SA, Jackson CW, Gartner TK. The roles of LAT in platelet signaling induced by collagen, TxA2, or ADP. Biochem Biophys Res Comm 2002; 292: 916-21.
11. Cho MJ, Pestina TI, Steward SA, Lowell CA, Jackson CW, Gartner TK. Role of the Src family kinase Lyn in TxA2 production, adenosine diphosphate secretion, Akt phosphorylation, and irreversible aggregation in platelets stimulated with γ-thrombin. Blood 2002; 99: 2442-7.
12. Thomas DW, Mannon RB, Mannon PJ, Latour A, Oliver JA, Hoffman M, Smithies O, Koller BH, Coffman TM. Coagulation defects and altered hemodynamic responses in mice lacking receptors for thromboxane A2. J Clin Invest 1998; 102: 1994-2001.
13. Fabre J-E, Nguyen M, Latour A, Keifer JA, Audoly LP, Coffman TM, Koller BH. Decreased platelet aggregation, increased bleeding time and resistance to thromboembolism in P2Y1-deficient mice. Nature Med 1999; 5: 1199-202.
14. Leon C, Hechler B, Freund M, Eckly A, Vial C, Ohlmann P, Dierich A, LeMeur M, Cazenave J-P, Gachet C. Defective platelet aggregation and increased resistance to thrombosis in purinergic P2Y1 receptor-null mice. J Clin Invest 1999; 104: 1731-7.
15. Foster CJ, Prosser DM, Agans JM, Zhai Y, Smith MD, Lachowicz JE, Zhang FL, Gustafson E, Monsma FJ, Wiekowski MT, Abbondanzo SJ, Cook DN, Bayne ML, Lira SA, Chintala MS. Molecular indentification and characterization of the platelet ADP receptor targeted by thienopyridine antithrombotic drugs. J Clin Invest 2001; 107: 1591-8.
16. Pulcinelli FM, Ashby B, Gazzaniga PP, Daniel JL. Protein kinase C activation is not a key step in ADP-mediated exposure of fibrinogen receptors on human platelets. FEBS Lett 1995; 364: 87-90.
17. Paul BZS, Jin J, Kunapuli SP. Molecular mechanism of thromboxane A2-induced platelet aggregation. J Biol Chem 1999; 274: 29108-14.
18. Banfic H, Tang X, Batty IH, Downes CP, Chen C, Rittenhouse SE. A novel integrin-activated pathway forms PKB/Akt-stimulatory phosphatidylinositol 3,4-bisphosphate via phosphatidylinositol 3-phosphate in platelets. J Biol Chem 1998; 273: 13-6.
19. Zhang J, Banfic H, Straforini F, Tosi L, Volinia S, Rittenhouse SE. A type II phosphoinositide 3-kinase is stimulated via activated integrin in platelets. J Biol Chem 1998; 273: 14081-4.
20. Dangelmaier C, Jin J, Smith JB, Kunapuli SP. Potentiation of thromboxane A2-induced platelet secretion by Gi signaling through the phosphoinositide-3 kinase pathway. Thromb Haemost 2001; 85: 341-8.
21. Trumel C, Payrastre B, Plantavid M, Hechler B, Viala C, Presek P, Martinson EA, Cazenave J-P, Chap H, Gachet C. A key role of adenosine diphosphate in the irreversible platelet aggregation induced by the PAR1-activating peptide through the late activation of phosphoinositide 3-kinase. Blood 1999; 94: 4156-65.
22. Boyer JL, Romero-Avila T, Schachter JB, Harden TK. Identification of competitive antagonists of the P2Y1 receptor. Mol Pharmacol 1996; 50: 1323-9.
23. Ingall AH, Dixon J, Bailey A, Coombs ME, Cox D, McInally JI, Hunt SF, Kindon ND, Teobald BJ, Willis PA, Humphries RG, Leff P, Clegg JA, Smith JA, Tomlinson W. Antagonists of the platelet P2T receptor: a novel approach to antithrombotic therapy. J Med Chem 1999; 42: 213-20.
24. 2+ and protein kinase C is the major factor in determining the level of secretion from human platelets. Biochem J 1993; 289: 277-82.
25. Bennet JS, Shattil SJ, Power JW, Gartner TK. Interaction of fibrinogen with its platelet receptor. J Biol Chem 1988; 263: 12948-53.
26. Offermanns S, Toombs CF, Hu Y-H, Simon MI. Defective platelet activation in Gaq-deficient mice. Nature 1997; 389: 183-6.
27. Kovacsovics TJ, Bachelot C, Toker A, Vlahos CJ, Duckworth B, Cantley LC, Hartwig JH. Phosphoinositide 3-kinase inhibition spares actin assembly in activating platelets but reverses platelet aggregation. J Biol Chem 1995; 270: 11358-66.
28. Li R, Babu CR, Lear JD, Wand J, Bennett JS, DeGrado WF. Oligomerization of the integrin αIIbβ3: Roles of the transmembrane and cytoplasmic domains. Proc Natl Acad Sci U S A 2001; 98: 12462-7.
29. Huntgan RR, Paumi C, Rocco M,Weisel JW. Effects of ligand-mimetic peptides Arg-Gly-Asp-X (X=Phe, Trp, Ser) on αIIbβ3 integrin conformation and oligomerization. Biochemistry 1999; 38: 14461-74.
30. Simon MI, Strathmann MP, Gautam N. Diversity of G proteins in signal transduction. Science 1991; 252: 802-8.