Role of glycoprotein Ibα mobility in platelet function

Dianne E. van der Wal; Sandra Verhoef; Roger E. G. Schutgens; Marjolein Peters; Yaping Wu; Jan Willem N. Akkerman

doi:10.1160/TH09-11-0751

Thrombosis and Haemostasis, Inhaltsverzeichnis

Thromb Haemost 2010; 103(05): 1033-1043
DOI: 10.1160/TH09-11-0751

Platelets and Blood Cells

Schattauer GmbH

Role of glycoprotein Ibα mobility in platelet function

Dianne E. van der Wal

¹Department of Clinical Chemistry and Haematology, University Medical Centre Utrecht, Utrecht, The Netherlands

,

Sandra Verhoef

¹Department of Clinical Chemistry and Haematology, University Medical Centre Utrecht, Utrecht, The Netherlands

,

Roger E. G. Schutgens

²Department of Haematology, University Medical Centre Utrecht, Utrecht, The Netherlands

,

Marjolein Peters

³Department of Pediatric-Haematology, Emma Childrens Hospital, Academic Medical Center Amsterdam

,

Yaping Wu

¹Department of Clinical Chemistry and Haematology, University Medical Centre Utrecht, Utrecht, The Netherlands

,

Jan Willem N. Akkerman

¹Department of Clinical Chemistry and Haematology, University Medical Centre Utrecht, Utrecht, The Netherlands

› Institutsangaben

Abstract

Summary

Incubation at 0°C is known to expose β-N-acetyl-D-glucosamine residues on glycoprotein (GP) Ibα inducing receptor clustering and α_Mβ₂-mediated platelet destruction by macrophages. Here we show that incubation at 0/37°C (4 hours at 0°C, followed by 1 hour at 37°C to mimic cold-storage and post-transfusion conditions) triggers a conformational change in the N-terminal flank (NTF, amino acids, aa 1–35) but not in aa 36–282 of GPIbα as detected by antibody binding. Addition of the sugar N-acetyl-D-glucosamine (GN) inhibits responses induced by 0/37°C. Incubation at 0°C shifts GPIbα from the membrane skeleton to the cytoskeleton. Different GPIbα conformations have little effect on VWF/ristocetin-induced aggregation, but arrest of NTF change by GN interferes with agglutination and spreading on a VWF-coated surface under flow. Strikingly, incubation at 0/37°C initiates thromboxane A₂ formation through a von Willebrand factor (VWF)-independent and GPIbα-dependent mechanism, as confirmed in VWF- and GPIbαﺹdeficient platelets. We conclude that the NTF change induced by 0/37°C incubation reflects clustering of GPIbα supports VWF/ristocetin-induced agglutination and spreading and is sufficient to initiate platelet activation in the absence of VWF.

Keywords

Glycoprotein Ibα - cold-storage - cytoskeleton - platelet - thromboxane A₂

Volltext

Referenzen

References
1 Clemetson KJ, Clemetson JM. Platelet GPIb complex as a target for anti-thrombotic drug development. Thromb Haemost 2008; 99: 473-479.
2 Pennings MT, Derksen RH, van Lummel M. et al. Platelet adhesion to dimeric beta-glycoprotein I under conditions of flow is mediated by at least two receptors: glycoprotein Ibalpha and apolipoprotein E receptor 2‘. J Thromb Haemost 2007; 05: 369-377.
3 Shen Y, Cranmer SL, Aprico A. et al. Leucine-rich repeats 2–4 (Leu60-Glu128) of platelet glycoprotein Ibalpha regulate shear-dependent cell adhesion to von Willebrand factor. J Biol Chem 2006; 281: 26419-26423.
4 Hartwig JH, DeSisto M. The cytoskeleton of the resting human blood platelet: structure of the membrane skeleton and its attachment to actin filaments. J Cell Biol 1991; 112: 407-425.
5 Englund GD, Bodnar RJ, Li Z. et al. Regulation of von Willebrand factor binding to the platelet glycoprotein Ib-IX by a membrane skeleton-dependent inside-out signal. J Biol Chem 2001; 276: 16952-16959.
6 Calverley DC, Kavanagh TJ, Roth GJ. Human signaling protein 14–3–3zeta interacts with platelet glycoprotein Ib subunits Ibalpha and Ibbeta. Blood 1998; 91: 1295-1303.
7 Du X. Signaling and regulation of the platelet glycoprotein Ib-IX-V complex. Curr Opin Hematol 2007; 14: 262-269.
8 Munday AD, Berndt MC, Mitchell CA. Phosphoinositide 3-kinase forms a complex with platelet membrane glycoprotein Ib-IX-V complex and 14–3–3zeta. Blood 2000; 96: 577-584.
9 Hoffmeister KM, Felbinger TW, Falet H. et al. The clearance mechanism of chilled blood platelets. Cell 2003; 112: 87-97.
10 Hoffmeister KM, Josefsson EC, Isaac NA. et al. Glycosylation restores survival of chilled blood platelets. Science 2003; 301: 1531-1534.
11 Badlou BA, Wu YP, Smid WM. et al. Platelet binding and phagocytosis by macrophages. Transfusion 2006; 46: 1432-1443.
12 Nichols WL, Hultin MB, James AH. et al. von Willebrand disease (VWD): evidence-based diagnosis and management guidelines, the National Heart, Lung, and Blood Institute (NHLBI) Expert Panel report (USA). Haemophilia 2008; 14: 171-232.
13 Huizinga EG, Tsuji S, Romijn RA. et al. Structures of glycoprotein Ibalpha and its complex with von Willebrand factor A1 domain. Science 2002; 297: 1176-1179.
14 Hulstein JJ, de Groot PG, Silence K, Veyradier A, Fijnheer R, Lenting PJ. A novel nanobody that detects the gain-of-function phenotype of von Willebrand factor in ADAMTS13 deficiency and von Willebrand disease type 2B. Blood 2005; 106: 3035-3042.
15 Weeterings C, Adelmeijer J, Myles T. et al. Glycoprotein Ibalpha-mediated platelet adhesion and aggregation to immobilized thrombin under conditions of flow. Arterioscler Thromb Vasc Biol 2006; 26: 670-675.
16 Shen Y, Romo GM, Dong JF. et al. Requirement of leucine-rich repeats of glyco-protein (GP) Ibalpha for shear-dependent and static binding of von Willebrand factor to the platelet membrane GP Ib-IX-V complex. Blood 2000; 95: 903-910.
17 Badlou BA, Spierenburg G, Ulrichts H. et al. Role of glycoprotein Ibalpha in phagocytosis of platelets by macrophages. Transfusion 2006; 46: 2090-2099.
18 Fox JE. Linkage of a membrane skeleton to integral membrane glycoproteins in human platelets. Identification of one of the glycoproteins as glycoprotein Ib. J Clin Invest 1985; 76: 1673-1683.
19 Remijn JA, Wu YP, IJsseldijk MJ. et al. Absence of fibrinogen in afibrinogenemia results in large but loosely packed thrombi under flow conditions. Thromb Haemost 2001; 85: 736-742.
20 Litjens PE, Kroner CI, Akkerman JW. et al. Cytoplasmic regions of the beta3 subunit of integrin alphaIIbbeta3 involved in platelet adhesion on fibrinogen under flow conditions. J Thromb Haemost 2003; 01: 2014-2021.
21 Bergmeier W, Bouvard D, Eble JA. et al. Rhodocytin (aggretin) activates platelets lacking alpha(2)beta(1) integrin, glycoprotein VI, and the ligand-binding domain of glycoprotein Ibalpha. J Biol Chem 2001; 276: 25121-25126.
22 Fijnheer R, Modderman PW, Veldman H. et al. Detection of platelet activation with monoclonal antibodies and flow cytometry. Changes during platelet storage. Transfusion 1990; 30: 20-25.
23 Christodoulides N, Feng S, Resendiz JC. et al. Glycoprotein Ib/IX/V binding to the membrane skeleton maintains shear-induced platelet aggregation. Thromb Res 2001; 102: 133-142.
24 Wu Y, Asazuma N, Satoh K. et al. Interaction between von Willebrand factor and glycoprotein Ib activates Src kinase in human platelets: role of phosphoinositide 3-kinase. Blood 2003; 01 (101) 3469-3476.
25 Garcia A, Quinton TM, Dorsam RT. et al. Src family kinase-mediated and Erk-mediated thromboxane A2 generation are essential for VWF/GPIb-induced fibrinogen receptor activation in human platelets. Blood 2005; 106: 3410-3414.
26 Liu J, Pestina TI, Berndt MC. et al. Botrocetin/VWF-induced signaling through GPIb-IX-V produces TxA2 in an alphaIIbbeta3– and aggregation-independent manner. Blood 2005; 106: 2750-2756.
27 Wencel-Drake JD, Painter RG, Zimmerman TS. et al. Ultrastructural localization of human platelet thrombospondin, fibrinogen, fibronectin, and von Willebrand factor in frozen thin section. Blood 1985; 65: 929-938.
28 Uff S, Clemetson JM, Harrison T, Clemetson KJ, Emsley J. Crystal structure of the platelet glycoprotein Ib(alpha) N-terminal domain reveals an unmasking mechanism for receptor activation. J Biol Chem 2002; 277: 35657-35663.
29 Kasirer-Friede A, Ware J, Leng L. et al. Lateral clustering of platelet GP Ib-IX complexes leads to up-regulation of the adhesive function of integrin alpha IIbbeta 3. J Biol Chem 2002; 277: 11949-11956.
30 Mistry N, Cranmer SL, Yuan Y. et al. Cytoskeletal regulation of the platelet glyco-protein Ib/V/IX-von willebrand factor interaction. Blood 2000; 96: 3480-3489.
31 Lu Q, Clemetson JM, Clemetson KJ. Translocation of GPIb and Fc receptor gamma-chain to cytoskeleton in mucetin-activated platelets. J Thromb Haemost 2005; 03: 2065-2076.
32 Navdaev A, Clemetson KJ. Glycoprotein Ib cross-linking/ligation on echicetin-coated surfaces or echicetin-IgMkappa in stirred suspension activates platelets by cytoskeleton modulated calcium release. J Biol Chem 2002; 277: 45928-45934.
33 Shrivastava M. The platelet storage lesion. Transfus Apher Sci 2009; 41: 105-113.
34 Cauwenberghs N, Vanhoorelbeke K, Vauterin S. et al. Epitope mapping of inhibitory antibodies against platelet glycoprotein Ibalpha reveals interaction between the leucine-rich repeat N-terminal and C-terminal flanking domains of glycoprotein Ibalpha. Blood 2001; 98: 652-660.