333
ISSN 1990-7478, Biochemistry (Moscow), Supplement Series A: Membrane and Cell Biology, 2018, Vol. 12, No. 4, pp. 333–343. © Pleiades Publishing, Ltd., 2018.
Original Russian Text © A.A. Martyanov, F.A. Balabin, A.S. Maiorov, E.V. Shamova, M.A. Panteleev, A.N. Sveshnikova, 2018, published in Biologicheskie Membrany, 2018,
Vol. 35, No. 5, pp. 364–375.
Mathematical Model of Platelet Intracellular Signaling After
Activation by Fucoidan
A. A. Martyanov
a, b, c,
*, F. A. Balabin
a
, A. S. Maiorov
a, b, c
, E. V. Shamova
d
,
M. A. Panteleev
a, b, c
, and A. N. Sveshnikova
a, b, c
a
Center for Theoretical Problems of Physicochemical Pharmacology,
Russian Academy of Sciences, Moscow, 119991 Russia
b
Faculty of Physics, Moscow Lomonosov State University, GSP-1, Moscow, 119991 Russia
c
National Scientific and Practical Center of Pediatric Hematology, Oncology
and Immunology named after Dmitry Rogachev, Moscow, 117198 Russia
d
Belarusian State University, Faculty of Physics, Department of Biophysics,
Minsk, 220030 Republic of Belarus
*e-mail: aa.martyanov@physics.msu.ru
Received November 16, 2017; in final form, January 9, 2018
Abstract—Blood platelets are the cells responsible for prevention of the blood loss. Fucoidan is a brown algae
extract that is known to activate platelets via C-type lectin receptor of the second type. On the other hand,
different fucoidans are now considered as perspective immunomodulators. Thus, application of fucoidan as
a medicinal drug seems to be contradictory. In this work we studied activation of platelets by fucoidan in silico
and in vitro. The computational model describes the behavior of the participants of the fucoidan receptor sig-
naling cascade. The model was validated with available experimental data published earlier. In order to con-
firm the model predictions, the fucoidan-induced activation of platelets was assessed in flow cytometry and
aggregometry experiments. The resultant model describes changes in the activity of tyrosine kinases of Syk
and Sarc family and subsequent activation of phospholipase Cγ2. One of the main model prediction is a sig-
nificant increase in the platelet cytosolic calcium level after the activation by fucoidan. This prediction was
confirmed in the experiments. Thus, fucoidan, as a true platelet activator, cannot be applied in therapy.
Keywords: intracellular signaling, computer modeling, flow cytometry
DOI: 10.1134/S1990747818050033
INTRODUCTION
Sulfated, fucose-enriched polysaccharides—
fucoidans—are complex molecules, that consist of
mixtures of structurally related polysaccharides with
variations in structural residues (L-fucopiranose or
non-fucose residues), as well as non-carbohydrate
substitutes (mostly sulfate or acetyl residues) [1].
Obtained from marine organisms, these compounds
are considered as promising biologically active mole-
cules that can act as the basis for new drugs. It has been
demonstrated that these biopolymers have anticoagu-
lant properties and prevent both inflammation develop-
ment and angiogenesis [2]. This class of molecules is of
most interest as a perspective substitute for heparin ther-
apy, which is used in the case of thromboembolism.
Anticoagulant and antithrombotic properties of
sulfated polysaccharides are determined by their capa-
bility to potentiate interaction of thrombin with anti-
thrombin (ATIII) and/or heparin cofactor (HCII).
Main structural feature of fucoidans that should be
taken into account in investigations of their biological
activity include degree and pattern of sulfatation, as
well as molecular weight [2]. Fucoidan from Fucus
vesiculosis has a low sulfatation degree; yet, due to the
fact that availability of this fucoidan is significantly
higher than that of the others, it is considered as a
main therapeutic agent. Fucoidan from Fucus vesicu-
losis will be hereinafter referred to as “fucoidan” [1, 2].
Despite the fact that fucoidan prolongs coagulation
time in APTT and TT tests, it was shown to have pro-
coagulant properties and can activate platelets via
receptor CLEC-2 [3].
Abbreviations: ADP, adenosine diphosphate; AT III, antithrom-
bin III; PTT, partial thromboplastin time; TT, thrombin time;
CLEC-2, C-type lectine-like receptor of type II; DAG, diacyl
glycerol; DUSP-3, dual specificity phosphatase 3; GP-VI, gly-
coprotein VI receptor; HC II, heparin cofactor II; IP
3
, inositol
3,4,5-trisphosphate; ITAM, immune tyrosine activation motif;
LAT, linker for activation of T cells; PGE
1
, prostaglandin E-1;
PH, plextrin homology domain; PI3K, phosphoinositol 3 kinase;
PIP
2(3)
, phosphoinositol 4,5(3)-bisphosphate (trisphosphate);
PLCγ2, phospholipase C γ2; poly-P, polyproline; PRP, platelet-
rich plasma; SFK, Src family kinases; SH-2(3), Src homology
domain 2 (3); SHP-1(2), SH-2 domain phosphotase (2); TxA
2
,
tromboxane A 2.
ARTICLES