2
J. U. Song et al. / Bioorg. Med. Chem. Lett. xxx (2015) xxx–xxx
R1
R2
OH
N
OH
N
HO
N
R4
O
N
N
S
N
N
N
S
N
N
O
R3
HO
N
H
N
H
O
O
Allopurinol
Oxypurinol
Febuxostat
Compound 6
Figure 1. Structures of allopurinol, oxypurinol, febuxostat and compound 6 as xanthine oxidase inhibitors.
antimicrobial, anti-inflammatory, analgesic, anticonvulsants, anti-
oxidant and antidiabetic agents,17–19 indicating that indole may
serve as a prospective scaffold in inhibiting xanthine oxidase.
In order to obtain an agent with better pharmacological profile
and in vivo efficacy for the treatment of gout, we incorporated
indole moiety into 6 as an isosteric replacement of phenyl moiety
of febuxostat as shown in Figure 1.
The general synthetic route to 6 is shown in Scheme 1. Amide 2
was synthesized from acid 1 using HBTU [2-(1H-benzotriazole-1-
yl)-1,1,3,3-tetramethyluronium hexafluorophosphate] and ammo-
nium chloride. Amide 2 was converted to thioamides 3 by refluxing
with Lawesson’s agent in THF. Compound 3 and ethyl 2-chloroace-
toacetate were reacted with a catalytic amount of pyridine by
refluxing in ethanol to afford indole-5-thiazole 4 in a reasonable
yield of 70–85%. Compound 4 was reacted with alkyl bromide
and sodium hydride in DMF at room temperature to furnish com-
pound 5, and this type of reaction allowed the modification of R3
group. Ester 5 was hydrolyzed with sodium hydroxide in aqueous
THF and methanol, and the final compound 6 was obtained in a
good yield.
The established synthesis led us to evaluate in vitro xanthine
oxidase inhibition of 6. Assay of in vitro XO inhibition activity
was performed by measuring the inhibitor concentration needed
for 50% inhibition.20 IC50 values of 6e, 6k, 6m and 6n showed the
similar levels to febuxostat. Tables 1–3 represent the inhibitory
activities against XO of the test compound.
The activities of indole 6a–g were initially investigated as
shown in Table 1. Compound 6a (IC50 = 110 nM) with hydrogen
for R1 and isobutyl group for R3 was found as a hit compound.
The previous investigation indicated that an electron-withdrawing
group such as nitro, chloro and cyano groups at 2-position in feb-
uxostat plays an important role on xanthine oxidase inhibition.23
Thus, chloro and nitro groups were introduced at 3-position of
6a. Chloro compounds 6b, 6c and 6d showed remarkably low
IC50 values of 5.7 nM, 7.3 nM and 16.0 nM, respectively. Unfortu-
nately, 6b and 6d were not metabolically stable (Table 1). Although
6c exhibited highly potent inhibitory activity (IC50 = 7.3 nM), it
displayed in vivo uric acid-lowering activity of only 18.9%. Com-
pound 6e with nitro group showed IC50 values of 4.2 nM. However,
6e was less metabolically stable than 6g (Table 1). Compound 6f
exhibited moderate inhibitory activity. Compound 6g with cyano
group showed an IC50 value of 5.5 nM which was ten times more
potent in activity than the original hit compound 6a. Thus, It was
confirmed that substitution with electron-withdrawing group at
3-position of the indole ring increased in vitro XO inhibitory
activity.
In order to examine the effect of the substitution at 3-position
of the thiazole ring, analogs 6h–k were prepared and their XO
inhibitory activities were tested as shown in Table 2. Based on
50% cytotoxic concentration (CC50) using primary rat hepatocytes,
6k (CC50 = 200 lM) was less cytotoxic than 6g (CC50 = 82 lM).
Therefore, isopropyl group was fixed at 1-position for comparison.
Compound 6i with trifluoromethyl group exhibited high IC50 value
of 895.0 nM, and 6j with methoxy group much increased activity
(IC50 = 90.0 nM). Compound 6h (R4 = H) and 6k (R4 = CH3)
displayed better inhibitory activities compared with 6i and 6j. Oral
exposure in rats with 6h and 6k revealed that 6k exhibited high
Cmax and AUC values as shown in Table 2. Therefore, we focused
on the modification of 6k comprising cyano group with various
substituents for R2 and R3.
The substitution effect on XO inhibition is summarized in
Table 3. Most of the compounds in Table 3 showed good XO inhib-
itory activity. Further selection was carried out on the basis of
in vivo uric acid reduction at 10 mg/kg.
In order to check whether the R2 substituent is worthwhile to
be varied, 6l (R2 = CH3) was prepared. It exhibited moderate inhib-
itory activity (IC50 = 10.7 nM) and low in vivo efficacy. Therefore,
our interest was focused on the R3 substituent. Introduction of flu-
oroisopropyl, hydroxyl isopropyl and methoxy isopropyl group
afforded 6m, 6n and 6o, showing potent IC50 values of 4.9 nM,
3.0 nM and 9.0 nM, respectively. Unfortunately, those compounds
displayed weak uric acid lowering activity compared to 6k. Com-
pounds 6p (R3 = methanesulfonylethyl) and 6q (R3 = acetylamino-
ethyl) exhibited moderate inhibitory activities of 9.0 nM and
R1
O
R1
S
R1
O
c
b
a
H2N
H2N
HO
R2
R2
R2
N
H
N
H
N
H
3
2
1
R1
R1
R1
R2
NH
R2
R3
R2
R3
R4
O
d
e
R4
O
N
S
R4
O
N
N
S
N
N
O
HO
S
O
6
4
5
Scheme 1. Reagents and conditions: (a) HBTU, NH4Cl, Et3N, DMF, 74–90%; (b) Lawesson’s agent, THF, reflux, 90–95%; (c) ethyl 2-chloroacetoacetate, pyridine, EtOH, reflux,
70–85%; (d) alkyl bromide, sodium hydride, DMF, 70–80%; (e) THF/MeOH = 1:1, 1 N NaOH, 90%.