Russian Chemical Bulletin, International Edition, Vol. 69, No. 1, pp. 158—163, January, 2020 158
Published in Russian in Izvestiya Akademii Nauk. Seriya Khimicheskaya, No. 1, pp. 0158—0163, January, 2020.
1066-5285/20/6901-0158 © 2020 Springer Science+Business Media, Inc.
Synthesis of a new betulinic acid glycoconjugate with N-acetyl-D-galactosamine
for the targeted delivery to hepatocellular carcinoma cells*
A. S. Olshanova,
a
E. Yu. Yamansarov,
a
E. I. Seleznev,
a
S. V. Kovalev,
a
A. V. Lopuhov,
a
D. A. Skvortsov,
a
S. A. Evteev,
a
N. L. Klyachko,
a,b
E. K. Beloglazkina,
a
Ya. A. Ivanenkov,
c,d
and A. G. Majouga
a,e,f
a
Department of Chemistry, Lomonosov Moscow State University,
1 Leninskie Gory, 119991 Moscow, Russian Federation.
Fax: +7 (495) 932 8846. E-mail: jamansar@gmail.com
b
Skolkovo Institute of Science and Technology,
100 ul. Novaya,143025 Skolkovo, Russian Federation.
Fax: +7 (495) 280 1481
c
Institute of Biochemistry and Genetics, Ufa Scientific Center of the Russian Academy of Sciences,
71 prosp. Oktyabrya, 450054 Ufa, Russian Federation.
Fax: +7 (347) 235 6088
d
Moscow Institute of Physics and Technology (State University),
9 Institutskii per., 141701 Dolgoprudnyi, Moscow region, Russian Federation.
Fax: +7 (495) 408 4254
e
National University of Science and Technology MISiS,
4 Leninskii prosp., 119049 Moscow, Russian Federation.
Fax: +7 (499) 236 2105
f
Dmitry Mendeleev University of Chemical Technology of Russia,
1 Build., 9 Miusskaya pl., 125047 Moscow, Russian Federation.
Fax: +7 (499) 978 8660
A new promising conjugate of betulinic acid with N-acetyl-D-galactosamine was synthesized
by the simple reaction sequence: esterification and copper-catalyzed azide-alkyne cycloaddition.
The obtained glycoderivative exhibited high activity against hepatocarcinoma cell lines in vitro,
selectivity of cytotoxic action, and excellent binding to the asialoglycoprotein receptor (ASGPR)
of hepatocytes. Its affinity to the ASGPR was established by surface plasmon resonance spectro-
scopy and confirmed by molecular docking in silico. An original approach was proposed to
enhance the cytotoxic properties of C-28 betulinic esters by introducing a hemioxalate fragment
bearing free carboxyl group into the C(3) position of ring A.
Key words: glycoconjugate, betulinic acid, N-acetyl-D-galactosamine, hemiester, targeted
delivery, liver, asialoglycoprotein receptor, hepatocellular carcinoma.
Hepatocellular carcinoma (HCC) ranks third in the
number of fatal outcomes worldwide among human can-
cer diseases.
1
According to the statistics of World Human
Organization (WHO), 782 500 new cases of HCC were
recorded in 2012 and the mortality from HCC was 700 000
fatal cases.
2
The high fatality rate of HCC is first of all due
to a long latency period, difficult early detection, and
multiresistance to chemotherapy.
3
Severe adverse effects
of anti-HCC medicines (systemic toxicity, anemia, muta-
genicity, etc.) considerably restrict the wide applicability
of chemotherapy. In addition, the production of these
medicines includes large-scale organic synthesis, which
inevitably results in a high cost of treatment for population.
For these reasons, there is an obvious need to develop new
anticancer drugs for the therapy of liver cancer with
improved pharmacological profile and decreased cost of
production.
The use of natural compounds and their semisynthetic
derivatives is an important trend in the search of new and
efficient drug substances.
4,5
Betulinic acid, a pentacyclic
lupine-type triterpenoid which is known to exhibit cyto-
toxic activity against a wide range of cancer cells,
6
includ-
ing HCC cells,
7
is of great interest for the design of anti-
HCC drugs. However, drawbacks associated with its
pharmacological profile and bioavailability restrict its ap-
plication in clinical practice as the anticancer drug.
8
To
solve current problems, betulinic acid (1) derivatives
Dedicated to Academician of the Russian Academy of Sciences
V. V. Lunin on the occasion of his 80th birthday.