Vol.:(0123456789) 1 3
J Thromb Thrombolysis
DOI 10.1007/s11239-017-1531-z
Involvement of superoxide generated by NADPH oxidase
in the shedding of procoagulant vesicles from human monocytic
cells exposed to bupivacaine
Toshiharu Azma
1,2
· Saori Ogawa
1,3
· Akira Nishioka
2
· Hiroyuki Kinoshita
4
·
Shinji Kawahito
5
· Hiroshi Nagasaka
1
· Nobuyuki Matsumoto
1
© Springer Science+Business Media, LLC 2017
that this simple experimental system is useful to explore the
molecular mechanisms of action of superoxide in the shed-
ding of procoagulant vesicles from human monocytic cells.
Keywords Monocytes · Superoxide · Tissue factor ·
Apoptotic vesicles · Procoagulant vesicles · Bupivacaine
Introduction
Superoxide and its partly reduced oxygen metabolites, hydro-
gen peroxide (H
2
O
2
) or hydroxyl radical yielded by chemical
reactions under some conditions (e.g., Haber–Weiss cycle),
react non-specifcally with a variety of biomolecules (e.g.,
proteins, lipids, or DNA), implicating thus in cell death and
cellular dysfunction in several pathophysiological conditions
[1]. Superoxide dismutase (SOD) is an enzyme that cata-
lyzes the conversion of two superoxide anion molecules to
oxygen and H
2
O
2
[2]. Experimental evidence from animals
that lack the gene expression for certain isoforms of SOD
demonstrated that SOD1 or SOD2, located in cytosol or in
mitochondria, respectively [3], plays pivotal roles in diseases
such as macular degeneration [4], osteoporosis [5], Alzhei-
mer disease [6], and cardiomyopathy [7].
By contrast, SOD3, expressed in the extracellular space,
appeared not to be involved in severe pathophysiological
disorders from animal studies using SOD3 knockout mice
[8]. Several studies including ours using electron spin reso-
nance spectrometry demonstrated that SOD increases the
generation of highly reactive oxygen species hydroxyl radi-
cal even in the presence of transition metals at a trace level
in cell-free superoxide generating conditions [9]. Although
it has been implicated that reactive oxygen species (ROS)
cause apoptotic cell death, a number of studies suggested
the involvement of H
2
O
2
or hydroxyl radical, rather than
Abstract It is known that a variety of sized procoagulant
vesicles that express tissue factor are released from several
types of cells including monocytes by mechanisms related
to the induction of apoptosis, while it has not yet been evalu-
ated whether superoxide is involved in the production of
such vesicles. Here, we report that a local anesthetic bupiv-
acaine induces apoptosis in human monocytic cells THP-1
within a short observation period, where the shedding of
procoagulant vesicles is associated. The property as pro-
coagulant vesicles was evaluated using fow cytometry by
the binding of FITC-conjugated fbrinogen to vesicles in
the presence of fresh frozen plasma and the suppression of
this binding by heparin. Bupivacaine (1 mg/ml) increased
the apoptotic cells and procoagulant vesicles. LY294002
(100 µM), that inhibits the recruiting of intracellular com-
ponent of NADPH oxidase to construct the activated form of
this enzyme complex, or superoxide dismutase (1500 unit/
ml) suppressed bupivacaine-provoked induction of apopto-
sis and the increase of procoagulant vesicles. We suggest
* Toshiharu Azma
azmacci@nifty.com
1
Department of Anesthesiology, Saitama Medical University
Hospital, Moroyama-cho, Iruma-gun, Saitama 350-0495,
Japan
2
Department of Anesthesiology & Pain Medicine, Kohnodai
Hospital, National Center for Global Health and Medicine,
Kohnodai 1-7-1, Ichikawa, Chiba 272-8516, Japan
3
Department of Dental Anesthesiology, Matsumoto
Dental University, Hirooka Goubara 1780, Shiojiri,
Nagano 399-0781, Japan
4
Department of Anesthesiology, Aichi Medical University,
Yazako Karimata 1-1, Nagakute, Aichi 480-1195, Japan
5
Department of Anesthesiology, Tokushima University
Hospital, Kuramoto 3-18-15, Tokushima 770-8503, Japan