Identification of novel downstream targets of platelet glycoprotein VI activation by differential proteome analysis: Implications for thrombus formation

Blood

Volumn 115, Issue 20, 2010, Pages 4102-4110

  Schulz, Christian ^a   Leuschen, Nina V ^a,b   Fröhlich, Thomas ^c   Lorenz, Michael ^a   Pfeiler, Susanne ^c   Gleissner, Christian A ^d,e   Kremmer, Elisabeth ^f   Kessler, Mirjam ^a   Khandoga, Alexander G ^a   Engelmann, Bernd ^c   Ley, Klaus ^d   Massberg, Steffen ^a,g   Arnold, Georg J ^c  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF COLOGNE   (Germany)

^c UNIVERSITY OF MUNICH   (Germany)

^d LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^e UNIVERSITY OF HEIDELBERG   (Germany)

^f INSTITUTE OF EPIDEMIOLOGY   (Germany)

^g HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE REDUCTASE; BETA CENTRACTIN; CHARGED MULTIVESICULAR BODY PROTEIN 3; CORTACTIN; GLYCOPROTEIN VI; PLECKSTRIN; PROTEIN ERP57; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; FIBRINOGEN RECEPTOR; MONOCLONAL ANTIBODY; PLATELET MEMBRANE GLYCOPROTEIN VI; PROTEOME;

ARTERY THROMBOSIS; ARTICLE; BLOOD CLOTTING; BLOOD VESSEL INJURY; CONTROLLED STUDY; ENZYME ACTIVITY; HEMOSTASIS; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; THROMBOCYTE ACTIVATION; THROMBOCYTE ADHESION; THROMBOCYTE AGGREGATION; THROMBOGENESIS; ADULT; FEMALE; FLOW CYTOMETRY; MALE; MASS SPECTROMETRY; METABOLISM; SIGNAL TRANSDUCTION; THROMBOCYTE; THROMBOSIS; TWO DIMENSIONAL GEL ELECTROPHORESIS; WESTERN BLOTTING;

ADULT; ANTIBODIES, MONOCLONAL; BIOLOGICAL MARKERS; BLOOD COAGULATION; BLOOD PLATELETS; BLOTTING, WESTERN; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FEMALE; FLOW CYTOMETRY; HUMANS; MALE; PLATELET ACTIVATION; PLATELET AGGREGATION; PLATELET MEMBRANE GLYCOPROTEINS; PROTEOME; SIGNAL TRANSDUCTION; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; THROMBOSIS; YOUNG ADULT;

EID: 77953242217     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2009-07-230268     Document Type: Article

References (52)

1. Massberg S, Schulz C, Gawaz M. Role of platelets in the pathophysiology of acute coronary syndrome. Semin Vasc Med. 2003;3(2):147-162.
2. Clemetson KJ, Clemetson JM. Platelet collagen receptors. Thromb Haemost. 2001;86(1):189-197.
3. Moroi M, Jung SM, Okuma M, Shinmyozu K. A patient with platelets deficient in glycoprotein VI that lack both collagen-induced aggregation and adhesion. J Clin Invest. 1989;84(5):1440-1445.
4. Jandrot-Perrus M, Busfield S, Lagrue AH, et al. Cloning, characterization, and functional studies of human and mouse glycoprotein VI: a platelet-specific collagen receptor from the immunoglobulin superfamily. Blood. 2000;96(5):1798-1807.
5. Gibbins JM, Okuma M, Farndale R, Barnes M, Watson SP. Glycoprotein VI is the collagen receptor in platelets which underlies tyrosine phosphorylation of the Fc receptor gamma-chain. FEBS Lett. 1997;413(2):255-259.
6. Zheng YM, Liu C, Chen H, Locke D, Ryan JC, Kahn ML. Expression of the platelet receptor GPVI confers signaling via the Fc receptor gamma-chain in response to the snake venom convulxin but not to collagen. J Biol Chem. 2001;276(16):12999-13006.
7. Cabeza N, Li Z, Schulz C, et al. Surface expression of collagen receptor Fc receptor-gamma/glycoprotein VI is enhanced on platelets in type 2 diabetes and mediates release of CD40 ligand and activation of endothelial cells. Diabetes. 2004;53(8):2117-2121.
8. Nieswandt B, Watson SP. Platelet-collagen interaction: is GPVI the central receptor? Blood. 2003;102(2):449-461.
9. Sugiyama T, Okuma M, Ushikubi F, Sensaki S, Kanaji K, Uchino H. A novel platelet aggregating factor found in a patient with defective collagen-induced platelet aggregation and autoimmune thrombocytopenia. Blood. 1987;69(6):1712-1720.
10. Sugiyama T, Ishibashi T, Okuma M. Functional role of the antigen recognized by an antiplatelet antibody specific for a putative collagen receptor in platelet-collagen interaction. Int J Hematol. 1993;58(1-2):99-104.
11. Schulte V, Snell D, Bergmeier W, Zirngibl H, Watson SP, Nieswandt B. Evidence for two distinct epitopes within collagen for activation of murine platelets. J Biol Chem. 2001;276(1):364-368.
12. Massberg S, Gawaz M, Gruner S, et al. A crucial role of glycoprotein VI for platelet recruitment to the injured arterial wall in vivo. J Exp Med. 2003;197(1):41-49.
13. Clemetson KJ, Clemetson JM. Collagen receptors as potential targets for novel anti-platelet agents. Curr Pharm Des. 2007;13(26):2673-2683.
14. Unlü M, Morgan M, Minden J. Difference gel electrophoresis: a single gel method for detecting changes in protein extracts. Electrophoresis. 1997;18(11):2071-2077.
15. Thiele T, Steil L, Gebhard S, et al. Profiling of alterations in platelet proteins during storage of platelet concentrates. Transfusion. 2007;47(7):1221-1233.
16. Massberg S, Konrad I, Bultmann A, et al. Soluble glycoprotein VI dimer inhibits platelet adhesion and aggregation to the injured vessel wall in vivo. FASEB J. 2004;18(2):397-399.
17. Vollmar B, Slotta JE, Nickels RM, Wenzel E, Menger MD. Comparative analysis of platelet isolation techniques for the in vivo study of the microcirculation. Microcirculation. 2003;10(2):143-152.
18. Marouga R, David S, Hawkins E. The development of the DIGE system: 2D fluorescence difference gel analysis technology. Anal Bioanal Chem. 2005;382(3):669-678.
19. Schulz C, Schafer A, Stolla M, et al. Chemokine fractalkine mediates leukocyte recruitment to inflammatory endothelial cells in flowing whole blood: a critical role for P-selectin expressed on activated platelets. Circulation. 2007;116(7):764-773.
20. Shattil SJ, Hoxie JA, Cunningham M, Brass LF. Changes in the platelet membrane glycoprotein IIb.IIIa complex during platelet activation. J Biol Chem. 1985;260(20):11107-11114.
21. Müller I, Besta F, Schulz C, Li Z, Massberg S, Gawaz M. Effects of statins on platelet inhibition by a high loading dose of clopidogrel. Circulation. 2003;108(18):2195-2197.
22. Gleissner CA, Sanders JM, Nadler J, Ley K. Upregulation of aldose reductase during foam cell formation as possible link among diabetes, hyperlipidemia, and atherosclerosis. Arterioscler Thromb Vasc Biol. 2008;28(6):1137-1143.
23. Reinhardt C, von Bruhl ML, Manukyan D, et al. Protein disulfide isomerase acts as an injury response signal that enhances fibrin generation via tissue factor activation. J Clin Invest. 2008;118(3):1110-1122.
24. Müller I, Klocke A, Alex M, et al. Intravascular tissue factor initiates coagulation via circulating microvesicles and platelets. FASEB J. 2003;17(3):476-478.
25. Matrix Science. Mascot Database. http://www.matrixscience.com/search- form-select.html. Accessed March 2007.
26. Lim SS, Shin KH, Jung SH, et al. Inhibitory effect of pyridyloxy- or phenoxylphenoxyalkanate derivatives on rat lens aldose reductase and rat platelet aggregation. J Pharm Pharmacol. 2004;56(7):941-945.
27. Enomoto S, Okada Y, Guvenc A, Erdurak CS, Coskun M, Okuyama T. Inhibitory effect of traditional Turkish folk medicines on aldose reductase (AR) and hematological activity, and on AR inhibitory activity of quercetin-3-O-methyl ether isolated from Cistus laurifolius L. Biol Pharm Bull. 2004;27(7):1140-1143.
28. Ellgaard L, Ruddock LW. The human protein disulphide isomerase family: substrate interactions and functional properties. EMBO Rep. 2005;6(1):28-32.
29. García A, Prabhakar S, Hughan S, et al. Differential proteome analysis of TRAP-activated platelets: involvement of DOK-2 and phosphorylation of RGS proteins. Blood. 2004;103(6):2088-2095.
30. García A, Senis YA, Antrobus R, et al. A global proteomics approach identifies novel phosphorylated signaling proteins in GPVI-activated platelets: involvement of G6f, a novel platelet Grb2-binding membrane adapter. Proteomics. 2006;6(19):5332-5343.
31. Minden J. Comparative proteomics and difference gel electrophoresis. Biotechniques. 2007;43(6):739-745.
32. Kador PF, Robison WG Jr, Kinoshita JH. The pharmacology of aldose reductase inhibitors. Annu Rev Pharmacol Toxicol. 1985;25:691-714.
33. Judzewitsch RG, Jaspan JB, Polonsky KS, et al. Aldose reductase inhibition improves nerve conduction velocity in diabetic patients. N Engl J Med. 1983;308(3):119-125.
34. Tomlinson MG, Calaminus SD, Berlanga O, et al. Collagen promotes sustained glycoprotein VI signaling in platelets and cell lines. J Thromb Haemost. 2007;5(11):2274-2283.
35. Ohmura C, Watada H, Azuma K, et al. Aldose reductase inhibitor, epalrestat, reduces lipid hydroperoxides in type 2 diabetes. Endocr J. 2009;56(1):149-156.
36. Matsumoto T, Ono Y, Kuromiya A, Toyosawa K, Ueda Y, Bril V. Long-term treatment with ranirestat (AS-3201), a potent aldose reductase inhibitor, suppresses diabetic neuropathy and cataract formation in rats. J Pharmacol Sci. 2008;107(3):340-348.
37. Carr ME. Diabetes mellitus: a hypercoagulable state. J Diabetes Complications. 2001;15(1):44-54.
38. Colwell JA. Antiplatelet agents for the prevention of cardiovascular disease in diabetes mellitus. Am J Cardiovasc Drugs. 2004;4(2):87-106.
39. Colwell JA, Nesto RW. The platelet in diabetes: focus on prevention of ischemic events. Diabetes Care. 2003;26(7):2181-2188.
40. Yamashiro K, Tsujikawa A, Ishida S, et al. Platelets accumulate in the diabetic retinal vasculature following endothelial death and suppress bloodretinal barrier breakdown. Am J Pathol. 2003;163(1):253-259.
41. Hatahet F, Ruddock LW. Protein disulfide isomerase: a critical evaluation of its function in disulfide bond formation. Antioxid Redox Signal. 2009;11(11):2807-2850.
42. Corbett EF, Oikawa K, Francois P, et al. Ca2+ regulation of interactions between endoplasmic reticulum chaperones. J Biol Chem. 1999;274(10):6203-6211.
43. Maattanen P, Kozlov G, Gehring K, Thomas DY. ERp57 and PDI: multifunctional protein disulfide isomerases with similar domain architectures but differing substrate-partner associations. Biochem Cell Biol. 2006;84(6):881-889.
44. Manickam N, Sun X, Li M, Gazitt Y, Essex DW. Protein disulphide isomerase in platelet function. Br J Haematol. 2008;140(2):223-229.
45. Holbrook LM, Watkins NA, Simmonds AD, Jones CI, Ouwehand WH, Gibbins JM. Platelets release novel thiol isomerase enzymes which are recruited to the cell surface following activation. Br J Haematol. Prepublished on December 8, 2009, as DOI 10.1111/j.1365-2141.2009.07994.x.
46. Toker A, Cantley LC. Signalling through the lipid products of phosphoinositide-3-OH kinase. Nature. 1997;387(6634):673-676.
47. Schafer DA, Gill SR, Cooper JA, Heuser JE, Schroer TA. Ultrastructural analysis of the dynactin complex: an actin-related protein is a component of a filament that resembles F-actin. J Cell Biol. 1994;126(2):403-412.
48. Lees-Miller JP, Helfman DM, Schroer TA. A vertebrate actin-related protein is a component of a multisubunit complex involved in microtubulebased vesicle motility. Nature. 1992;359(6392):244-246.
49. Clark SW, Staub O, Clark IB, et al. Beta-centractin: characterization and distribution of a new member of the centractin family of actin-related proteins. Mol Biol Cell. 1994;5(12):1301-1310.
50. Clark IB, Meyer DI. Overexpression of normal and mutant Arp1alpha (centractin) differentially affects microtubule organization during mitosis and interphase. J Cell Sci. 1999;112(pt 20):3507-3518.
51. Tehrani S, Tomasevic N, Weed S, Sakowicz R, Cooper JA. Src phosphorylation of cortactin enhances actin assembly. Proc Natl Acad Sci U S A. 2007;104(29):11933-11938.
52. Dukes JD, Richardson JD, Simmons R, Whitley P. A dominant-negative ESCRT-III protein perturbs cytokinesis and trafficking to lysosomes. Biochem J. 2008;411(2):233-239.