© Schattauer 2013 Thrombosis and Haemostasis 110.4/2013
751
Red cell-derived microparticles (RMP) as haemostatic agent
Wenche Jy; Max E. Johansen; Carlos Bidot Jr.; Lawrence L. Horstman; Yeon S. Ahn
The Wallace H Coulter Platelet Laboratory, Division of Hematology/Oncology, Department of Medicine, University of Miami Miller School of Medicine, Miami, Florida, USA
Summary
Among circulating cell-derived microparticles, those derived from red
cells (RMP) have been least well investigated. To exploit potential hae-
mostatic benefit of RMP, we developed a method of producing them in
quantity, and here report on their haemostatic properties. High-press-
ure extrusion of washed RBC was employed to generate RMP. RMP
were identified and enumerated by flow cytometry. Their size distribu-
tion was assessed by Doppler electrophoretic light scattering analysis
(DELSA). Interaction with platelets was studied by platelet aggrego-
metry, and shear-dependent adhesion by Diamed IMPACT-R. Thrombin
generation and tissue factor (TF) expression was also measured. The
effect of RMP on blood samples of patients with bleeding disorders
was investigated ex vivo by thromboelastography (TEG). Haemostatic
efficacy in vivo was assessed by measuring reduction of blood loss
and bleeding time in rats and rabbits. RMP have mean diameter of
0.45 μm and 50% of them exhibit annexin V binding, a proxy for pro-
coagulant phospholipids (PL). No TF could be detected by flow cyto-
metry. At saturating concentrations of MPs, RMP generated thrombin
robustly but after longer delay compared to PMP and EMP. RMP en-
hanced platelet adhesion and aggregation induced by low-dose ADP
or AA. In TEG study, RMP corrected or improved haemostatic defects
in blood of patients with platelet and coagulation disorders. RMP re-
duced bleeding time and blood loss in thrombocytopenic rabbits (bu-
sulfan-treated) and in Plavix-treated rats. In conclusion, RMP has
broad haemostatic activity, enhancing both primary (platelet) and sec-
ondary (coagulation) haemostasis, suggesting potential use as hae-
mostatic agent for treatment of bleeding.
Keywords
Animal bleeding models, haemostatic agent, RMP–platelet interac-
tion, red cell microparticles (RMP), thromboelastography
Correspondence to:
Wenche Jy, PhD
University of Miami Miller School of Medicine
1600 NW 10th Ave., RMSB 7109, R36-A
Miami, FL 33136, USA
Tel.: +1 305 243 6617, Fax: +1 305 243 5957
E-mail: wjy@med.miami.edu
Financial support:
The research is supported and funded by the Wallace H Coulter Foundation and a
grant from NIH NHLBI (1R01HL098031).
Received: March 2, 2013
Accepted after major revision: July 3, 2013
Prepublished online: September 12, 2013
doi:10.1160/TH12-12-0941
Thromb Haemost 2013; 110: 751–760
Blood Coagulation, Fibrinolysis and Cellular Haemostasis
Introduction
Cell-derived microparticles (C-MP) are membranous vesicles re-
leased during cell activation and apoptosis (1). Release of C-MP is
associated with reversal of membrane asymmetry, exposing proco-
agulant phospholipids such as phosphatidyl serine (PS) to the ex-
ternal medium. This provides negatively charged phospholipid
membrane surface for the binding of clotting factors and assembly
of tenase and prothrombinase, thereby accelerating thrombin gen-
eration and blood clotting (2). They are found in normal circu-
lation at low levels and at higher levels in thrombotic, inflamma-
tory, and cardiovascular disorders (3).
The role of C-MP in haemostasis and thrombosis has been re-
ceiving increased attention in recent years (3-5). Among the many
species of circulating C-MP, those from red cells (RMP) have been
investigated least in regard to their role in haemostasis and throm-
bosis. RBCs have traditionally been viewed as comparatively inert
in haemostasis and thrombosis (6). However, a number of clinical
and laboratory observations suggest a significant role in coagu-
lation and inflammation (7, 8).
Platelet-derived MP (PMP) has been proposed as an infusible
haemostatic agent for treatment of bleeding disorders (9-11) but
development was apparently halted. Our studies in vitro, together
with in vivo animal studies (12-15), suggested that RMP would
have broad haemostatic activity and appear well suited for use as
haemostatic agent.
In this paper, we report on indicators of haemostatic activity of
RMP by in vitro and ex vivo methods, and also document in vivo
efficacy in rats and rabbits.
Materials and methods
Preparation of RMP
Packed red blood cells (40 ml) were diluted 2.5-fold with isotonic
saline, centrifuged at 650 x g for 10 minutes (min) and supernatant
discarded. The RBCs were re-suspended in 40 ml saline and sub-
jected to high-pressure extrusion via the TS2 Bench-top Cell Dis-
ruptor (Constant Systems, Kennesaw, GA, USA). The output was
centrifuged at 250 x g for 10 min to remove large debris; the pellets
and bottom 1 ml of each tube was discarded. The remaining super-
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