Binding of plasma factor XIII to thrombin-receptor activated
human platelets
Béla Nagy Jr
1
; Zsuzsa Simon
1
; Zsuzsa Bagoly
2
; László Muszbek
2
; János Kappelmayer
1
1
Department of Clinical Biochemistry and Molecular Pathology, Medical and Health Science Center, University of Debrecen, Debrecen,
Hungary;
2
Clinical Research Center and Thrombosis, Haemostasis and Vascular Biology Research Group, Hungarian Academy of Sciences,
Medical and Health Science Center, University of Debrecen, Debrecen, Hungary
Summary
Platelet-bound coagulation factor XIII (FXIII) is targeted and
concentrated at the site where platelet-rich thrombi are form-
ed. Previous studies were in disagreement about the nature of
FXIII binding to platelets. In this study, thrombin-receptor acti-
vating peptide (TRAP)-stimulated human whole blood and
washed platelets were analysed by flow cytometry for the bind-
ing of FXIII using a monoclonal antibody against the A subunit of
FXIII (FXIII-A). Here, we demonstrate that FXIII-A positivity sig-
nificantly increased on activated platelets in whole blood com-
pared to unstimulated sample, but not in washed platelets.
GPIIb/IIIa receptor plays an essential role in FXIII binding, as fi-
brinogen receptor antagonist eptifibatide and fibrinogen binding
inhibitor RGDS tetrapeptide significantly prevented the binding
Keywords
Factor XIII, platelet activation, TRAP, fibrinogen
of FXIII. Furthermore, stimulated platelets from a patient with
severe type I Glanzmann thrombasthenia showed insignificant
FXIII-A positivity versus healthy controls. In addition, basal neg-
ligible amount of FXIII on washed platelets was only slightly in-
creased when highly purified plasma FXIII (FXIII-A
2
B
2
) was
added upon platelet activation by TRAP. Similarly, no remarkable
FXIII-A positivity was observed when we used FXIII-A
2
B
2
with
γA/γA fibrinogen. However, γA/γ' fibrinogen significantly aug-
mented FXIII binding on TRAP-stimulated platelets in the pres-
ence of non-activated FXIII-A
2
B
2
. We conclude that FXIII-A
2
B
2
of plasma origin binds to thrombin-receptor activated platelets
via GPIIb/IIIa receptor-bound fibrinogen with γ'-chain and is not
capable of direct platelet binding.
Thromb Haemost 2009; 101: 83–89
Platelets and Blood Cells
Correspondence to:
János Kappelmayer, MD, PhD, Dsc
Department of Clinical Biochemistry and Molecular Pathology
Medical and Health Science Center, University of Debrecen
Nagyerdei krt. 98. H-4032, Debrecen, Hungary
Tel.: +36 52 340 006, Fax: +36 52 417 631
E-mail: kappelmayer@med.unideb.hu
Received: January 22, 2009
Accepted after minor revision: March 14, 2009
Prepublished online: May 11, 2009
doi:10.1160/TH09-01-0054
© 2009 Schattauer GmbH, Stuttgart
83
Introduction
Blood coagulation factor XIII (FXIII) is a protransglutaminase
that is essential for maintaining haemostasis as a key regulator of
fibrinolysis (1). Plasma FXIII is a heterotetrameric zymogen
(FXIII-A
2
B
2
) that consists of two potentially active A subunits
(FXIII-A) and two carrier/inhibitory B subunits (FXIII-B) (2).
The cellular form of FXIII (FXIII-A
2
) that is a dimer of two A
subunits, is present in monocytes, macrophages and the platelet
cytosol (reviewed in [2, 3]).
FXIII is targeted and concentrated at the site where platelet
clots are formed (2). FXIII increases the fibrinolytic resistance
of platelet-rich thrombi through the cross-linking of α
2
-antiplas-
min to fibrin (4, 5) and the presence of platelets accelerates the
cross-linking process (5). The interaction between activated
FXIII (FXIIIa) and platelets has been investigated in a few for-
mer studies (6–8), and a saturable and specific binding of FXIIIa
to thrombin-stimulated, but not to resting platelets was demon-
strated (6–8). However, data on the binding site of FXIIIa were
contradictory. In the first study, GPIIb/IIIa receptor and platelet-
bound fibrin(ogen) were excluded as binding site for FXIIIa;
RGD peptide did not influence the interaction between FXIIIa
and platelets, and FXIIIa binding to platelets from two patients
with severe Glanzmann thrombasthenia (GT) was normal (6).
The binding of FXIIIa to thrombin-activated platelets was in-
hibited by plasmin (7). In a later study, however, the GPIIb/IIIa
receptor was shown to mediate the binding of FXIIIa to throm-
bin-stimulated platelets, and indirect binding of FXIIIa through
fibrinogen associated with its receptor was also demonstrated
(8).
In contrast to previous studies, here we investigated the bind-
ing of intact non-activated plasma factor XIII to human platelets
stimulated with thrombin-receptor activating peptide (TRAP).
Our working hypothesis was that FXIII can bind to platelets in
non-activated form, then on the surface of activated platelets it
becomes easily activated by locally formed thrombin and exerts
its cross-linking action. We confirmed that intracellular platelet
FXIII-A
2
is not exposed on the cell surface during platelet acti-
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