I. Islam et al. / Bioorg. Med. Chem. Lett. 17 (2007) 1349–1354
1353
Table 2. Efficacy of (rac)2a in rabbit jugular vein thrombolysis model
0.4
0.35
0.3
Dosea
(mg/kg + mg/kg h)
Thrombus
weight (mg)
SEMb
% reduction
in thrombus wt
-thrombomodulin
+thrombomodulin
2 uM rac-2a
PBS
tPA
141
145
82
15
19
21
11
—
0.5 uM rac-2a
—
0.125 uM rac-2a
0.0625 uM rac-2a
tPA + CPI
tPA + (rac)2a
42c
31c
97
a Dose: tPA = 0.01 mg/kg + 0.07 mg/kg h; CPI = 0.5 mg/kg + 0.3 mg/
kg h; (rac)2a = 15 mg/kg + 15 mg/kg h; n = 8–9/group.
b Standard error of the mean.
0.25
0.2
c p < 0.05 Fisher’s PLSD compared to vehicle and tPA.
When either CPI or (rac)2a was given together with the
inefficacious sub-threshold dose of tPA, the effect of tPA
was enhanced with a significant reduction in thrombus
weights being observed when compared to the vehicle
or tPA treated group (Table 2). The assessment of bleed-
ing risk was evaluated by measuring the weight of blood
loss from toe nail clips performed prior to thrombolytic
treatment, and at the end of the study. No significant
differences in bleeding were observed in any of the treat-
ment groups. Thus, TAFIa inhibition with (rac)2a in
combination with tPA enhances fibrinolysis in vivo.
0.15
0.1
0
10
20
30
40
50
60
70
Time (min)
Figure 3. Clot lysis time exhibits dose dependent acceleration by
(rac)2a.
peptidase D (CPD) bound with the related arginine
mimic GEMSA.10 CPD has 50% sequence homology
with CPN and the homology is >87% in the active site.
GEMSA binds Asp192 in CPD via terminal (Ng) guani-
dine nitrogen atoms. SQ-24,798, (ꢀ)2a, and 2d bind
Asp255 in CPB via internal (Ne)and terminal (Ng) gua-
nidine nitrogen atoms. Since replacement of the alkyl
chain with an aromatic ring eliminates the possibility
of a terminal guanidine nitrogen binding conformation,
the selectivity of our inhibitors may stem from the
hydrogen bonds formed by the guanidine moiety.9
In conclusion, the data shown describe the discovery of
a series of cyclic, constrained arginine and lysine mimet-
ics as potent and selective TAFIa inhibitors. Several
inhibitors show significant selectivity against CPN and
CPB. (rac)2a dose dependently accelerates clot lysis in
human plasma in vitro and is efficacious in an in vivo
thrombolysis model as an iv adjunct to tPA. These data
provide further support for TAFIa inhibitors as a treat-
ment for managing thrombosis in the clinic.
References and notes
TAFIa inhibition by aryl guanidine (rac)2a was tested in
an in vitro human plasma clot lysis assay to show that
the inhibition of activated TAFI observed in the enzyme
inhibition assay translated to an effect in human plas-
ma.3b Addition of thrombin, thrombomodulin, and cal-
cium to human plasma leads to activation of TAFI and
subsequent prolongation of clot lysis time. Clot lysis was
monitored by measuring turbidity at 405 nm. Lysis time
is accelerated by (rac)2a in a dose dependent manner
(Fig. 3).
1. For recent reviews, see: (a) Marx, P. F. Curr. Med. Chem.
2004, 11, 2335; (b) Bouma, B. N.; Meijers, J. C. M.
J. Thromb. Haemost. 2003, 1, 1566; (c) Hendriks, D. F. In
Handbook of Proteolytic Enzymes; Barrett, A. J., Raw-
lings, N. D., Woessner, J. F., Eds., 2nd ed.; Elsevier:
London, UK, 2004; pp 825–828; (d) Leurs, J.; Hendriks,
D. I. J. Thromb. Haemost. 2005, 94, 471.
2. (a) Nesheim, M.; Walker, J.; Wang, W.; Boffa, M.;
Horrevoets, A.; Bajzar, L. A. N. Y. Acad. Sci. 2001, 936,
247; (b) Bouma, B. N.; Marx, P. F.; Mosnier, L. O.;
Meijers, J. C. Thromb. Res. 2001, 101, 329; (c) Schatt-
eman, K.; Goossens, F.; Leurs, J.; Verkerk, R.; Scharpe,
S.; Michiels, J. J.; Hendriks, D. Clin. Appl. Thromb.
Hemost. 2001, 7, 93.
3. (a) Klement, P.; Liao, P.; Bajzar, L. Blood 1999, 94, 2735;
(b) Nagashima, M.; Werner, M.; Wang, M.; Zhao, L.;
Light, D. R.; Pagila, R.; Morser, J.; Verhallen, P. Thromb.
Res. 2000, 98, 333; (c) Refino, C. J.; DeGuzman, L.;
Schmitt, D.; Smyth, R.; Jeet, S.; Lipari, M. T.; Eaton, D.;
Bunting, S. Fibrinolysis Proteolysis 2000, 14, 305; (d)
Suzuki, K.; Muto, Y.; Fushihara, K.; Kanemoto, K.; Iida,
H.; Sato, E.; Kikuchi, C.; Matsushima, T.; Kato, E.;
Nomoto, M.; Yoshioka, S.; Ishii, H. J. Pharmacol. Exp.
Ther. 2004, 309, 607; (e) Bjoerkman, J.-A. E.; Abrahams-
son, T. I.; Nerme, V. K.; Mattsson, C. J. Thromb. Res.
2005, 116, 519.
An in vivo rabbit jugular vein thrombolysis model was
used to test the hypothesis that TAFIa inhibition with
(rac)2a in combination with tPA would enhance fibrino-
lysis.3b A segment of the jugular vein was isolated with
ligatures and injected with a mixture of autologous
citrated blood and thromboplastin to induce thrombus
formation. Doses of tPA, CPI, (rac)2a or phosphate-
buffered saline (PBS) vehicle were administered as iv
bolus injections, followed by a constant infusion for
90 min via the right marginal ear vein. Fibrinolysis
was assessed by measuring clot weight at the end of
the study. An inefficacious sub-threshold dose of tPA
was combined with either the TAFIa inhibitor (rac)2a
or the peptidic TAFIa inhibitor CPI. CPI was used as
a positive control to confirm the effect of TAFIa inhibi-
tion in this model.
4. (a) Nagashima, M.; Yin, Z.-F.; Zhao, L.; White, K.; Zhu,
Y.; Lasky, N.; Halks-Miller, M.; Broze, G. J.; Fay, W. P.;