Anti-Cancer Agents in Medicinal Chemistry
Send Orders for Reprints to reprints@benthamscience.ae
Anti-Cancer Agents in Medicinal Chemistry, 2017, 17, 1777-1785
1777
RESEARCH ARTICLE
Design, Synthesis and Biological Evaluation of Betulinic Acid
Derivatives as New Antitumor Agents for Leukemia
Fernanda Waechter
a
, Gloria N.S. da Silva
a
, Júlia B. Willig
b
, Cristiane B. de Oliveira
a
, Bruna D. Vieira
c
,
Daniela B.B. Trivella
c
, Aline R. Zimmer
a
, Andréia Buffon
b
, Diogo A. Pilger
b
and Simone C.B. Gnoatto
a,*
a
Laboratório de Fitoquímica e Síntese Orgânica, Faculdade de Farmácia, Universidade Federal do Rio Grande do Sul, Avenida
Ipiranga, 2752, Porto Alegre, 90610-000, Brazil.;
b
Laboratório de Análises Bioquímicas e Citológicas, Faculdade de Farmácia,
Universidade Federal do Rio Grande do Sul, Avenida Ipiranga, 2752, Porto Alegre, 90610-000, Brazil;
c
Laboratório Nacional de
Biociências, Centro Nacional de Pesquisa em Energia e Materiais, Rua Giuseppe Maximo Scolfaro, 10000, Campinas, 13083-970,
Brazil
Abstract: Background: Chronic myeloid leukemia (CML) is currently treated with imatinib, a Bcr-Abl
inhibitor. However, resistance to this drug usually develops over time. Triptolide, a diterpenoid triepoxide, has
been shown active against CML cells resistant to imatinib, acting mainly on the level of Bcr-Abl transcription
inhibition.
Objective: Here, we used the triterpene betulinic acid, a known proteasome inhibitor with potential antileukemic
activity, as a scaffold for the generation of analogues with predicted triptolide biological activity.
Method: Betulinic acid derivatives were designed based on the structure-activity relationship of triptolide and
evaluated for their cytotoxic effects in CML cells, lymphocytes and human keratinocytes (HaCaT), as well as
against the proteasome complex. The main modification performed on betulinic acid was fluorination at C-28
and epoxidation, both of which are responsible for enhancing activity of triptolide. A total of 10 compounds
were obtained: 6 previously described and 4 novel compounds. The cytotoxic activity over a CML cell line
(K562) was assessed using flow cytometry and compared to lymphocytes and HaCaT.
Result: The results show that betulinic acid was the most cytotoxic compound against CML cells, showing a
good selectivity index for cancer over normal cells. The most important trend for the activity in betulinic
acid derivatives is the presence of a free hydroxyl group at C-3 and a carboxyl group at C-28. Results also
indicated that the epoxide is important for enhancing the activity, while modification at C-28 worsens the
activity.
Conclusion: Proteasome inhibition assays suggest that proteasome is the main target for betulinic acid and its
derivatives.
Keywords: Betulinic acid, cancer chemotherapy, triptolide, chronic myeloid leukemia, fluorination, epoxidation, proteasome inhibition.
1. INTRODUCTION
Chronic myeloid leukemia (CML) is mainly caused by aberrant
Bcr-Abl kinases, which are responsible for 95% of the uncontrolled
proliferation of myeloid cells in CML. This disease is usually
treated with imatinib (Glivec
®
), a tyrosine kinase inhibitor also
used for the treatment of other types of cancers. However, clinical
resistance is observed in patients treated with imatinib, mainly due
to mutations in the Bcr-Abl imatinib binding site. This situation
leaves the patients with few options and in general, the disease
progresses to blast crisis and death [1, 2].
*Address correspondence to this author at the Laboratório de Fitoquímica e
Síntese Orgânica, Faculdade de Farmácia, Universidade Federal do Rio
Grande do Sul, Avenida Ipiranga, 2752, Porto Alegre, 90610-000, Brazil;
Tel/Fax: +55-51-3308-5451, +55-51-3308-5313;
E-mail: simone.gnoatto@ufrgs.br
Recently, pre-clinical studies were carried out with triptolide
(compound 1, Fig. 1A), a molecule which showed activity in vitro
and in vivo against CML cells resistant to imatinib [3], offering a
potential alternative therapeutic for patients.
Triptolide is a diterpene present in Tripterygium wilfordii [4], a
plant used for centuries in Chinese medicine to treat inflammation
and auto-immune diseases [5]. Triptolide was found to reduce Bcr-
Abl levels, resulting in induced mitochondrial-dependent apoptosis
in either CML and CML cells containing the Bcr-Abl-T315I clini-
cal mutation. It has been shown to work following a mechanism
that is independent of either caspase and proteasome activation [3].
RNA polymerases I and II were identified as the main biological
targets of 1 [6]. The data available for its structure-activity relation-
ship [7-10] reveals that the epoxides present in 1 are important for
its antitumor activity [7], while the hydroxyl group at C-14 leads to
greater activity when in the β position. In addition, when the hy-
droxyl group is replaced by fluorine, the activity further increases
A R T I C L E H I S T O R Y
Received: September 19, 2016
Revised: March 23, 2017
Accepted: March 30, 2017
DOI:
10.2174/1871521409666170412143638
1875-5992/17 $58.00+.00 © 2017 Bentham Science Publishers