PKCα regulates platelet granule secretion and thrombus formation in mice

Journal of Clinical Investigation

Volumn 119, Issue 2, 2009, Pages 399-407

  Konopatskaya, Olga ^a   Gilio, Karen ^b   Harper, Matthew T ^a   Zhao, Yan ^c   Cosemans, Judith M E M ^b   Karim, Zubair A ^d   Whiteheart, Sidney W ^d   Molkentin, Jeffery D ^e   Verkade, Paul ^a   Watson, Steve P ^c   Heemskerk, Johan W M ^a   Poole, Alastair W ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b MAASTRICHT UNIVERSITY   (Netherlands)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^d UNIVERSITY OF KENTUCKY   (United States)

^e CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; ISOENZYME; PROTEIN KINASE C ALPHA; ADENOSINE DIPHOSPHATE; INTEGRIN; PRKCA PROTEIN, MOUSE; PROTEIN KINASE C; PROTEIN KINASE C BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLEEDING; CELL ACTIVITY; CONTROLLED STUDY; ENZYME REGULATION; GASTROINTESTINAL HEMORRHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TAIL; THROMBOCYTE; THROMBOCYTE ADHESION; THROMBOCYTE AGGREGATION; THROMBOCYTE FUNCTION; THROMBOGENESIS; ANIMAL; CELL GRANULE; DRUG EFFECT; PHYSIOLOGY; SECRETION; SIGNAL TRANSDUCTION; THROMBOSIS; ULTRASTRUCTURE;

ADENOSINE DIPHOSPHATE; ANIMALS; BLOOD PLATELETS; CYTOPLASMIC GRANULES; INTEGRINS; MICE; PLATELET AGGREGATION; PROTEIN KINASE C; PROTEIN KINASE C-ALPHA; SIGNAL TRANSDUCTION; THROMBOSIS;

EID: 61749097572     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI34665     Document Type: Article

References (57)

1. Parker, P.J., and Murray-Rust, J. 2004. PKC at a glance. J. Cell. Sci. 117:131-132.
2. Harper, M.T., and Poole, A.W. 2007. Isoform-specific functions of PKC: the platelet paradigm. Biochem. Soc. Trans. 35:1005-1008.
3. 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.
4. Walker, T.R., and Watson, S.P. 1993. Synergy between Ca2+ and protein kinase C is the major factor in determining the level of secretion from human platelets. Biochem. J. 289:277-282.
5. Toullec, D., et al. 1991. The bisindolylmaleimide GF 109203X is a potent and selective inhibitor of protein kinase C. J. Biol. Chem. 266:15771-15781.
6. Shattil, S.J., et al. 1992. Regulation of glycoprotein IIb-IIIa receptor function studied with platelets permeabilized by the pore-forming complement proteins C5b-9. J. Biol. Chem. 267:18424-18431.
7. Strehl, A., et al. 2007. Dual role of platelet protein kinase C in thrombus formation: Stimulation of pro-aggregatory an suppression of procoagulant activity in platelets. J. Biol. Chem. 282:7046-7055.
8. Crosby, D., and Poole, A.W. 2002. Interaction of Bruton's tyrosine kinase and protein kinase Ctheta in platelets. Cross-talk between tyrosine and serine/ threonine kinases. J. Biol. Chem. 277:9958-9965.
9. Murugappan, S., Tuluc, F., Dorsam, R.T., Shankar, H., and Kunapuli, S.P. 2004. Differential role of PKC-delta isoform in agonist-induced dense granule secretion in human platelets. J. Biol. Chem. 279:2360-2367.
10. Grabarek, J., et al. 1992. Identification and functional characterization of protein kinase C isozymes in platelets and HEL cells. J. Biol. Chem. 267:10011-10017.
11. Crabos, M., Imber, R., Woodtli, T., Fabbro, D., and Erne, P. 1991. Different translocation of three distinct PKC isoforms with tumor-promoting phorbol ester in human platelets. Biochem. Biophys. Res. Commun. 178:878-883.
12. Baldassare, J.J., Henderson, P.A., Burns, D., Loomis, C., and Fisher, G.J. 1992. Translocation of protein kinase C isozymes in thrombin-stimulated human platelets. Correlation with 1,2-diacylglycerol levels. J. Biol. Chem. 267:15585-15590.
13. Wang, F., et al. 1993. A new protein kinase C, nPKC eta', and nPKC theta are expressed in human platelets: involvement of nPKC eta' and nPKC theta in signal transduction stimulated by PAF. Biochem. Biophys. Res. Commun. 191:240-246.
14. Khan, W.A., et al. 1993. Selective regulation of protein kinase C isoenzymes by oleic acid in human platelets. J. Biol. Chem. 268:5063-5068.
15. Pula, G., et al. 2006. PKCδ regulates collageninduced platelet aggregation through inhibition of VASP-mediated filopodia formation. Blood. 108:4035-4044.
16. Crosby, D., and Poole, A.W. 2003. Physical and functional interaction between PKCδ and Fyn tyrosine kinase in human platelets. J. Biol. Chem. 278:24533-24541.
17. Yoshioka, A., et al. 2001. Identification of protein kinase Calpha as an essential, but not sufficient, cytosolic factor for Ca2+-induced alpha- and densecore granule secretion in platelets. J. Biol. Chem. 276:39379-39385.
18. Tabuchi, A., et al. 2003. Direct demonstration of involvement of protein kinase Cα in the Ca2+-induced platelet aggregation. J. Biol. Chem. 278:26374-26379.
19. Pula, G., Crosby, D., Baker, J., and Poole, A.W. 2005. Functional interaction of protein kinase Cα with the tyrosine kinases Syk and Src in human platelets. J. Biol. Chem. 280:7194-7205.
20. Dempsey, E.C., et al. 2000. Protein kinase C isozymes and the regulation of diverse cell responses. Am. J. Physiol. Lung Cell Mol. Physiol. 279:L429-L438.
21. Oster, H., and Leitges, M. 2006. Protein kinase Cα but not PKCζ suppresses intestinal tumor formation in ApcMin/+ mice. Cancer Res. 66:6955-6963.
22. Hara, T., et al. 2005. Deficiency of protein kinase calpha in mice results in impairment of epidermal hyperplasia and enhancement of tumor formation in two-stage skin carcinogenesis. Cancer Res. 65:7356-7362.
23. Michie, A.M., and Nakagawa, R. 2005. The link between PKCα regulation and cellular transformation. Immunol. Lett. 96:155-162.
24. Lahn, M., et al. 2004. Protein kinase Cα expression in breast and ovarian cancer. Oncology. 67:1-10.
25. Masur, K., et al. 2001. High PKCα and low E-cadherin expression contribute to high migratory activity of colon carcinoma cells. Mol. Biol. Cell. 12:1973-1982.
26. Morse-Gaudio, M., Connolly, J.M., and Rose, D.P. 1998. Protein kinase C and its isoforms in human breast cancer cells: relationship to the invasive phenotype. Int. J. Oncol. 12:1349-1354.
27. Ways, D.K., et al. 1995. MCF-7 breast cancer cells transfected with protein kinase C-α exhibit altered expression of other protein kinase C isoforms and display a more aggressive neoplastic phenotype. J. Clin. Invest. 95:1906-1915.
28. Sliva, D. 2004. Signaling pathways responsible for cancer cell invasion as targets for cancer therapy. Curr. Cancer Drug Targets. 4:327-336.
29. Pfeifhofer, C., et al. 2006. Defective IgG2a/2b class switching in PKC?-/- mice. J. Immunol. 176:6004-6011.
30. von Essen, M., et al. 2006. Protein Kinase C (PKC)α and PKCθ are the major PKC isotypes involved in TCR down-regulation. J. Immunol. 176:7502-7510.
31. Leitges, M., et al. 2002. Knockout of PKCα enhances insulin signaling through PI3K. Mol. Endocrinol. 16:847-858.
32. Braz, J.C., et al. 2004. PKC-α regulates cardiac contractility and propensity toward heart failure. Nat. Med. 10:248-254.
33. Han, J., et al. 2006. Reconstructing and deconstructing agonist-induced activation of integrin αIIbβ3. Curr. Biol. 16:1796-1806.
34. Samani, N.J., et al. 2007. Genomewide association analysis of coronary artery disease. N. Engl. J. Med. 357:443-453.
35. The Wellcome Trust Case Control Consortium. 2007. Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature. 447:661-678.
36. Shattil, S.J., and Newman, P.J. 2004. Integrins: dynamic scaffolds for adhesion and signaling in platelets. Blood. 104:1606-1615.
37. Soriani, A., et al. 2006. A role for PKCθ in outsidein αIIbβ3 signaling. J. Thromb. Haemost. 4:648-655.
38. Buensuceso, C.S., et al. 2005. Regulation of outside-in signaling in platelets by integrin-associated protein kinase Cβ. J. Biol. Chem. 280:644-653.
39. Polgar, J., Lane, W.S., Chung, S.-H., Houng, A.K., and Reed, G.L. 2003. Phosphorylation of SNAP-23 in activated human platelets. J. Biol. Chem. 278:44369-44376.
40. Hepp, R., et al. 2005. Phosphorylation of SNAP-23 regulates exocytosis from mast cells. J. Biol. Chem. 280:6610-6620.
41. Quinton, T.M., et al. 2002. Protein kinase C- and calcium-regulated pathways independently synergize with Gi pathways in agonist-induced fibrinogen receptor activation. Biochem. J. 368:535-543.
42. Auger, J.M., Kuijpers, M.J.E., Senis, Y.A., Watson, S.P., and Heemskerk, J.W.M. 2005. Adhesion of human and mouse platelets to collagen under shear: a unifying model. FASEB J. 19:825-827.
43. Falati, S., Gross, P., Merrill-Skoloff, G., Furie, B.C., and Furie, B. 2002. Real-time in vivo imaging of platelets, tissue factor and fibrin during arterial thrombus formation in the mouse. Nat. Med. 8:1175-1181.
44. Kalia, N., Auger, J.M., Atkinson, B., and Watson, S.P. 2008. Critical role of FcR γ-chain, LAT, PLCγ2 and thrombin in arteriolar thrombus formation upon mild, laser-induced endothelial injury in vivo. Microcirculation. 15:325-335.
45. Meadows, T.A., and Bhatt, D.L. 2007. Clinical aspects of platelet inhibitors and thrombus formation. Circ. Res. 100:1261-1275.
46. Crittenden, J.R., et al. 2004. CalDAG-GEFI integrates signaling for platelet aggregation and thrombus formation. Nat. Med. 10:982-986.
47. Scarborough, R.M., Kleiman, N.S., and Phillips, D.R. 1999. Platelet glycoprotein IIb/IIIa antagonists: what are the relevant issues concerning their pharmacology and clinical use? Circulation. 100:437-444.
48. Cosemans, J.M.E.M., et al. 2006. Continuous signaling via PI3K isoforms beta and gamma is required for platelet ADP receptor function in dynamic thrombus stabilization. Blood. 108:3045-3052.
49. Remijn, J.A., et al. 2002. Role of ADP Receptor P2Y12 in platelet adhesion and thrombus formation in flowing blood. Arterioscler. Thromb. Vasc. Biol. 22:686-691.
50. Morgan, A., et al. 2005. Regulation of exocytosis by protein kinase C. Biochem. Soc. Trans. 33:1341-1344.
51. Fitzgerald, M.L., and Reed, G.L. 1999. Rab6 is phosphorylated in thrombin-activated platelets by a protein kinase C-dependent mechanism: effects on GTP/GDP binding and cellular distribution. Biochem. J. 342:353-360.
52. Reed, G.L., Houng, A.K., and Fitzgerald, M.L. 1999. Human platelets contain SNARE proteins and a Sec1p homologue that interacts with syntaxin 4 and is phosphorylated after thrombin activation: implications for platelet secretion. Blood. 93:2617-2626.
53. Hall, K.J., et al. 2008. Genetic analysis of the role of protein kinase Cθ in platelet function and thrombus formation. PLoS ONE. 3:e3277.
54. Hanauske, A.R., Sundell, K., and Lahn, M. 2004. The role of protein kinase C-α (PKC-α) in cancer and its modulation by the novel PKC-α-specific inhibitor aprinocarsen. Curr. Pharm. Des. 10:1923-1936.
55. Lahn, M., Sundell, K., and Kohler, G. 2006. The role of protein kinase C-α in hematologic malignancies. Acta Haematol. 115:1-8.
56. Kuijpers, M.J.E., et al. 2003. Complementary roles of platelet glycoprotein VI and integrin α2β1 in collagen-induced thrombus formation in flowing whole blood ex vivo. FASEB J. 17:685-687.
57. Munnix, I.C.A., et al. 2007. Segregation of platelet aggregatory and procoagulant microdomains in thrombus formation: regulation by transient integrin activation. Arterioscler. Thromb. Vasc. Biol. 27:2484-2490.