Nutrition and Cancer, 60(1), 120–130
Copyright © 2008, Taylor & Francis Group, LLC
ISSN: 0163-5581 print / 1532-7914 online
DOI: 10.1080/01635580701613772
Induction of Apoptosis by Lupeol and Mango Extract
in Mouse Prostate and LNCaP Cells
Sahdeo Prasad, Neetu Kalra, and Yogeshwer Shukla
Proteomics Laboratory, Industrial Toxicology Research Centre, Lucknow, India
Prostate cancer (PCA) is one of the most invasive malignancy
and second leading cause of cancer related deaths in United States
and some other countries. Long latency period makes PCA an
ideal disease for pharmacologic or nutritional chemoprevention.
Lupeol, a triterpene present in mango and other fruits, has shown
to possess anticancer properties in in vivo and in vitro assays.
Here, we recorded the apoptogenic activity in mouse prostate by
lupeol and mango pulp extract (MPE). Testosterone was injected
subcutaneously (5 mg/kg body weight) for 14 consecutive days to
male Swiss albino mice. Lupeol/MPE supplementation resulted in
arrest of prostate enlargement in testosterone-treated animals. In
mouse prostate tissue, lupeol and MPE supplementation resulted in
a significantly high percentage of apoptotic cells in the hypodiploid
region. The induction of apoptosis in mouse prostate cells was pre-
ceded by the loss of mitochondrial transmembrane potential and
DNA laddering. In testosterone-induced mouse prostate, upregula-
tion of antiapoptotic B-cell non-Hodgkin lymphoma-2 and down-
regulation of proapoptotic Bcl-2-associated X protein and caspase-
3 were also recorded. We further observed apoptogenic activities
of lupeol in an in vitro model using human prostate cancer cells
[lymph node carcinoma of the prostate (LNCaP)]. The apopto-
genic response of lupeol-induced changes in LNCaP cells can be
summarized as early increase of reactive oxygen species followed
by induction of mitochondrial pathway leading to cell death. Thus,
the results of this study demonstrate that lupeol/MPE is effective
in combating testosterone–induced changes in mouse prostate as
well as causing apoptosis by modulating cell-growth regulators.
INTRODUCTION
Prostate cancer (PCA) is one of the most invasive malignancy
in males of the United States and many other countries and is the
second leading cause of cancer deaths in American men and the
men of some other countries (1,2). It is estimated that average an-
nual PCA incidence rates in the United States are 110.4 to 180.9,
whereas in India, it ranged from 5.0 to 9.1, per 100,000 (3). Epi-
demiological, experimental, and clinical data point toward an
Submitted 27 January 2007; accepted in final form 19 April 2007.
Address correspondence to Yogeshwer Shukla, Environmental Car-
cinogenesis Division, Industrial Toxicology Research Centre, Mahatma
Gandhi Marg, Lucknow 226001, India. Phone: (+91) 094151-58430.
FAX: (+91) 522-2628227. E-mail: yogeshwer shukla@hotmail.com
and Shukla y@rediffmail.com.
important role of androgens in the development and progres-
sion of this disease (4). An increasing incidence of the disease
and failure of conventional therapy for advanced invasive PCA
leads to the search for new approaches for management of the
disease (5,6). Epidemiological evidences have shown an in-
verse association between consumption of vegetables and risk
of PCA (7,8). Mango (Mangifera indica L.) is a worldwide con-
sumed fruit in the tropical countries around the world. Mango
extract has been shown to be antimutagenic in Salmonella
typhimurium TA1538 (9). Chemical analysis of mango pulp
extract (MPE) has shown that it contains vitamins, organic
acids, carbohydrates, amino acids, polyphenols, and volatile
compounds (10). Lupeol [Lup-20 (29)-en-3-β -ol; Fig. 1]
is a naturally occurring pentacyclic triterpene present predom-
inantly in mango. Lupeol has been shown to exhibit strong
anti-inflammatory, antiarthritic, antimutagenic, and antimalarial
activities (11–13). It has also been shown to possess antitumor-
promoting effects in mouse skin carcinogenesis (14). The oral
administration of lupeol changed the tissue redox system in-
duced by cadmium exposure by scavenging the free radicals
and by improving the antioxidant status of the rat liver (15).
Generally, cancer is a multifactorial disease, which requires
modulation of multiple pathways and targets. These targets in-
clude the activation of apoptosis, suppression of growth factor
expression, or signaling and downregulation of antiapoptotic
proteins (16). Apoptosis is a well organized cell death process
characterized by loss of plasma membrane phospholipid asym-
metry, enzymatic cleavage of the DNA into oligonucleosomal
fragments, and segmentation of the cells into membrane-bound
apoptotic bodies (17). Genetic changes leading to loss of apop-
tosis or derangement of apoptosis-signaling pathways in the
transformed cells are critical for neoplastic changes (18). The
execution process of cells by apoptosis is mediated by caspase-
3, one of a family of cysteine proteases (19,20). Activation of
caspase-3 is tightly regulated by the formation of apoptosome
(21), which is dependent on the cytochrome c release from the
mitochondria into cytosol, which is thought to be regulated by
B-cell non-Hodgkin lymphoma-2 (Bcl-2)-associated X protein
(Bax) and Bcl-2. Proapoptotic Bax forms pores in the outer
mitochondrial membrane, releasing cytochrome c, whereas an-
tiapototic Bcl-2 prevents the opening of mitochondrial transition
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