Anti-cancer potential of banana flower extract: An in vitro study

Abstract

Banana (Musa paradisiaca) flower is rich in phytochemicals (vitamins, flavornoids, proteins) and has antioxidant properties. The anti-cancer activity of banana flower extract has been evaluated on the cervical cancer cell line HeLa. The antiproliferative effects were evaluated by MTT assay. The extract was further purified by TLC and characterized by LC-MS method. The ethanol extract had significant cytotoxicity to HeLa cells with an IC50 of 20 µg/mL. By thin layer chromatography we could isolate three fractions out of which fraction 2 had exhibited maximum anti-proliferative effects with an IC50 value of <10 µg/mL. By LC-MS analysis, bioactive fraction was found to have an m/ z value of 224.2 indicating it as a novel one.

Full text

Introduction
There is a large amount of experimental evidence which
suggests that consumption of fruits and vegetables
lower the risk of cancer (Chen et al., 2004). Phenolic
compounds are one of the most abundant and ubiqui-
tous group of plant metabolites, and are an integral part
of the human diet. In addition to their primary potent
antioxidant activity, this group of compounds display a
wide variety of biological functions, which are mainly
related to intervention in various stages of cancer
development including initiation, progression, promo-
tion, invasion and metastasis (Kampa et al., 2007;
Ramos, 2008). Musa sp. (Musaceae) also known as
banana is a familiar tropical fruit and important source
of food in the world. From its native South western
Pacific home, the banana plant spread to India by about
600 BC and later on it spread all over the tropical world.
It is possibly the world's oldest cultivated crop (Yusoff,
2008). It possesses efficient medicinal values such as
stem juice is used in nervous affectations like epilepsy,
hysteria and in dysentery and diarrhoea. Several oligo-
saccharides comprising fructose, xylose, galactose, glu-
cose and mannose occur naturally in banana (Debaban-
dya et al., 2010) making it an excellent prebiotic for the
selective growth of beneficial bacteria in the intestine. It
aids in combating diarrhea and dysentery and promo-
tes healing of intestinal lesions in ulcerative colitis.
Roots of Musa paradisiaca are antihelmintic, flowers are
astringent and fruits are mild laxative. It is also useful
in celiac disease, constipation and peptic ulcer (Mallick
et al., 2007). It has been found that bananas have
curative properties both scientifically and traditionally.
The banana flower is rich in phytochemicals like
vitamins, flavonoids and proteins. The flower has been
used to treat bronchitis, constipation and peptic ulcer.
The extract has antioxidant property that prevents free
radicals and control cell and tissue damage. Bhaskar et
al., (2011) reported that glucose uptake in Ehrlich
ascites tumor cells was stimulated by banana (Musa sp.)
flower and pseudostem extracts. China et al., (2011)
reported that, the banana flowers are a potential source
of natural antioxidants.
Based on the main components of banana flower extract
and its antioxidant properties, we hypothesized that the
banana flower extract may have anticancer activities
against cancer cell lines in vitro. However, there are no
such reports.
Materials and Methods
Sample collection, authentication and preparation of extracts:
The flowers of banana were collected from Bangalore,
A Journal of the Bangladesh Pharmacological Society (BDPS); www.bdps.info Bangladesh J Pharmacol 2014; 9: 628-35
Journal homepage: www.banglajol.info
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International Pharmaceutical Abstracts, Open J-gate, Science Citation Index Expanded, SCOPUS and Social Sciences Citation Index
ISSN: 1991-0088; DOI: 10.3329/bjp.v9i4.20610
Abstract
Banana (Musa paradisiaca) flower is rich in phytochemicals (vitamins, flavor-
noids, proteins) and has antioxidant properties. The anti-cancer activity of
banana flower extract has been evaluated on the cervical cancer cell line HeLa.
The antiproliferative effects were evaluated by MTT assay. The extract was
further purified by TLC and characterized by LC-MS method. The ethanol
extract had significant cytotoxicity to HeLa cells with an IC
50
of 20 µg/mL. By
thin layer chromatography we could isolate three fractions out of which
fraction 2 had exhibited maximum anti-proliferative effects with an IC
50
value
of <10 µg/mL. By LC-MS analysis, bioactive fraction was found to have an m/
z value of 224.2 indicating it as a novel one.
Article Info
Received: 7 October 2014
Accepted: 4 November 2014
Available Online: 30 November 2014
Keywords:
Anti-cancer
Banana
Number of Figures: 8
Number of Refs: 22
Correspondence: KN
e-mail:
kn.varalakshmi@jainuniversity.ac.in
This work is licensed under a Creative Commons Attribution 3.0 License. You are free to copy, distribute and perform the work. You must attribute the work in the
manner specified by the author or licensor.
Anti-cancer potential of banana flower extract: An
in vitro
study
Bibechana Timsina and Varalakshmi Kilingar Nadumane
Department of Biotechnology, Centre for Post-Graduate Studies, Jain University, Jayanagar, Bangalore 560 011, India.

India on July–August 2011. The flower was separated
and cut into small pieces and dried. The dried samples
were ground into a fine powder using a dry grinder,
and then kept in an air-tight container and stored in a
freezer (-20˚C) before extraction. 30 g of dried powder
was used for serial extraction in a soxhlet apparatus
using ethanol. The extracts were filtered and evapora-
ted to dryness in a rotary evaporator. 1 mg/mL of the
extract was prepared by dilution of the stock with
sterile dimethyl sulphoxide (DMSO) (Duraipandiyan et
al., 2006).
Chemicals: DMEM medium, fetal bovine serum (FBS),
penicillin, streptomycin and MTT were procured from
HIMEDIA (India). Caspase Apoptosis Assay Kit was
purchased from G Biosciences (kit 786-205A), USA. All
cell lines were bought from National Center for Cell
Sciences (NCCS), Pune. All other chemicals and sol-
vents used were of the highest purity grade available.
Cell culture plastic ware was from Tarsons (India).
Cell lines and culture: HeLa and CHO cell lines were
procured from National Center for Cell Sciences
(NCCS), Pune. Cells were maintained in DMEM
medium (HIMEDIA, REF – AT065A) supplemented
with 10% fetal bovine serum (HIMEDIA, REF – RM112).
Lymphocyte isolation was carried out from the blood of
few healthy male and female individuals, about 20
years of age, who were free from infection for the past
six months and had not been under any medication.
HiSep medium (HIMEDIA, India) was used for the
isolation. Lymphocytes were used as control cells to
assess the cytotoxicity of the extracts on humans. The
cells were incubated at 37°C with 95% air and 5% CO
2
.
All cells were maintained below passage 20 and used in
experiments during the linear phase of growth.
MTT [3-(4, 5-dimethylthiazol-2yl)-2, 5-diphenyltetrazolium
bromide)] assay: HeLa and CHO cells growing
exponentially were collected after trypsinization and
plated in 96-well microtitre plates in 100 µL of culture
medium and were allowed to adhere for 24 hours
before treatment. Increasing concentrations of ethanol
extract of banana flower dissolved in DMSO were
added to different wells of the micro titer plates. Final
concentration of DMSO in the culture medium was
maintained at 0.4% (v/v) to avoid solvent toxicity. The
cells were incubated for 24, 48 and 72 hours in the
presence and absence of the extracts. Cytotoxicity was
analyzed using MTT assay following the standard
protocol (Mosmann et al., 1983). Cytotoxicity was
expressed as the concentration of the extract inhibiting
cell growth by 50%, relative to cells incubated in the
presence of 0.4% DMSO. The absorbance was read at
540 nm using the ELISA plate reader. Each experiment
was performed in triplicates.
The following formula was used to calculate the
percent of inhibition:
Inhibition (%) = (1-OD
s
/OD) X 100
(Where, OD
s
= Optical density of the sample; OD
= Optical density of the control)
Chromatographic separation of the bioactive compound
(TLC): Thin layer chromatography (TLC) was carried
out using pre-coated TLC plates (Silica gel 60 F 254
Merck) to fractionate the bioactive components from
the crude extracts. The silica gel coated sheet was
activated at 110˚C for 15 min. The extracts dissolved in
ethanol (20 µL) were spotted at the bottom of silica gel
coated sheet. Chromatogram was performed with the
following solvent systems (a) toluene: ethylacetate:
formic acid (2.5:1:1 v/v); (b) chloroform:acetone (6:4
and 8:4 v/v); (c) hexane:acetone (6:4 and 8:2 v/v); (d)
dichloromethane: acetone (6:4 and 8:2 v/v); (e) Toluene.
The chromatograms were detected with the help of a
UV transilluminator (254 and 366 nm) and the Rf value
was calculated for each of the TLC separated fractions.
Detection of the bioactive fraction: For the detection of
active compound separated in TLC, bioactivity guided
fractionation was followed. From the chromatogram
developed as described above, each band was scraped,
mixed with methanol and centrifuged at 3,000 rpm for
15 min. Supernatant was collected in a pre-weighed vial
and kept for evaporation. The partially purified frac-
tions obtained from preparative TLC were tested for
cytotoxicity against the HeLa cells, CHO cells and the
lymphocytes by MTT assay as described earlier.
Fluorescence microscopic analysis by ethidium bromide/
acridine orange (EB/AO) staining: HeLa and CHO cells
growing exponentially were subcultured to 25 cm
2
cul-
ture flasks and were allowed to adhere for 24 hours
before treatment. After this period, the cells were treat-
ed with bioactive fraction 2 from banana flower extract
for 24 hours. After removal of the incubation medium
cells were collected by trypsinization and treated with
EB/AO stain. Stained cells were used to prepare slides
and observed under a fluorescence microscope and
were photographed (Cohen et al., 1993).
Caspase-9 activity assay: Caspase-9 activity was assessed
using the caspase-9 Colorimetric Assay Kit (G Bio-
sciences, kit 786-205A). The assay is based on specto-
photometric detection of the chromophore p-nitro-
aniline (pNA) after cleavage from the labeled substrate
LEHD-pNA. The free pNA can be quantified using a
spectrophotometer or a microtiter plate reader at 405
nm. Comparison of the absorbance of pNA from an
apoptotic sample with an uninduced control allows
determination of the fold increase in caspase-9 activity.
Here, HeLa cells and CHO cells were exposed to the
bioactive fraction 2 (20 μg/mL each) for 24 hours.
Following treatment, the cells were subjected to caspase
-9 activity assay following the manufacturer's instruct-
tions. Percentage increase was calculated using the
Bangladesh J Pharmacol 2014; 9: 628-635 629

following formula:
Percentage activity of Caspase = (OD
control/sample
–
OD
blank
)/OD
blank
x 100
All experiments were performed in triplicate and
repeated at least twice.
LDH cytotoxicity assay: LDH Assay is a colorimetric
method of assaying cellular cytotoxicity. The assay
quantitatively measures a stable cytosolic enzyme
lactate dehydrogenase (LDH), which is released upon
cell lysis. Cells treated with fraction 2 of banana flower
for 24 hours were collected by tripsinization, centri-
fuged at 1,000 rpm for 10 min, and 10 µL of lysis buffer
was added and plated in triplicates in a 96 well plate
along with the controls, positive (1% Triton X-100) and
negative (untreated). 50 µL of substrate was added to
the wells and incubated in the dark for 20 min. After
the incubation period, 50µL of stop solution was added
to all the wells to stop the reaction and readings were
noted down at 490 nm. Percentage cytotoxicity was
measured using the following formula:
Percentage cytotoxicity = (OD
treated
– OD
negative control
)/
OD
positive control
x 100
Cell cycle kinetics: Cells grown in 12-well plates (5.0 x
10
5
cells/mL) were treated with bioactive fraction 2 for
24 hours. Briefly, cell pellets were collected by tripsiniza
-tion, washed twice with PBS and fixed overnight with
70% ethanol at 4°C. After incubation, cells were centri-
fuged again at 5,000 rpm for 10 min and washed twice
with PBS. Cells were resuspended in 1 mL of PBS and
in ribonuclease (100 μg/mL). Then cells were resus-
pended in staining solution [50 μg/mL propidium
iodide, 30 units/mL RNase, 4 mM/L sodium citrate,
and Triton X-100 (pH 7.8)] and incubated at 37°C for 15
min. After incubation in the dark, fluorescence-active-
ted cells were sorted in a FACScan flow cytometer
(equipped with a 488-nm argon laser), and the data
were analyzed on a MACS Quant analyser.
Phytochemical screening of the bioactive fraction: Prelimi-
nary qualitative phytochemical analysis of the banana
flower crude extract and the bioactive fraction 2 were
performed for the determination of the biochemical
constituents with the help of standard protocols
(Harborne, 1973). All the analyses were carried out
using 1 mL of extracts. In the case of tests for carbohy-
drates, Fehling’s and Benedict’s tests were carried out.
Tests for alkaloids (Wagner’s and Mayer’s tests), test for
sterols (Salkowsky test), tests for the detection of
phenolic compounds (test with neutral FeCl
3
) and
tannins, tests for proteins (Biuret test ) and also tests for
the detection of flavonoids (Shinoda test) and saponins,
were performed.
HPLC analysis of the bioactive fraction: To further purify
the active fractions, the TLC purified fraction of banana
flowers were subjected to high performance liquid
chromatography. The HPLC separation was performed
using WATERS HPLC system with 2487 dual λ U-V
detector. The sample and mobile phase were filtered
through 0.22 μm PVDF filter before injecting to the
column.
Spectroscopic analysis: The ESI mass spectra were
recorded using a single quadrupole mass spectrometer
(Hewlett Packard HP 1100 MSD series). Spectra were
acquired over the mass range 50-1500 m/z.
Statistical analysis: All experiments were carried out in
triplicates. The results were expressed as mean ± stan-
dard error values. Statistical significance was calculated
using one- way analysis of variance (ANOVA) with the
help of Graph pad prism software. A value of p<0.05
was taken as statistically significant.
Results
When HeLa and CHO cells were treated with the
ethanolic extracts of the banana flower, there was a
dose and time dependent antiproliferative effect obser-
ved in the case of HeLa cells. Percentage viability
decreased as the period of exposure to the extract
increased from 24 hours to 48 hours and 72 hours. At 5
µg/mL concentration of the extract, the percentage
viability of 24 hours treated HeLa cells was 91% and it
decreased to 50.0% by the end of 72 hours. As the
concentration increased from 5 to 20 µg/mL, the per-
centage viability of HeLa cells further decreased to 38%
(Figure 1). When CHO cells were treated with the
ethanol extract of banana flower, we could see a
decrease in percentage viability with an increase in
concentration. At a concentration of 20 µg/mL, after 72
hours of treatment, the percentage viability was 60.0%
as compared to 86% after 24 hours. It is evident that the
effect was more profound on the HeLa cells than the
CHO cells.
Chromatogram was developed with the solvent toluene
for the extract. The chromatograms were detected with
the help of a UV transilluminator (254 and 366 nm).
Three major fractions were separated from the extract.
The Rf values were 0.06, 0.47 and 0.72.
Fractions recovered from TLC were further tested for
cytotoxicity by the MTT assay. The 2
nd
fraction of the
ethanol extract of banana flower exhibited highest
cytotoxic activity than the other fractions. Fraction 2
reduced the percentage viability of CHO cells to 60%
and HeLa cells to 35% at 20 μg/mL concentration, after
72 hours of treatment (Figure 2). IC
50
value was found
to be 10 μg/mL for this bioactive fraction.
When the bioactive fraction 2 from the flower extract
was checked for cytotoxicity on normal human peri-
pheral lymphocytes, there was not much difference in
the percentage viability at all the tested concentrations
630 Bangladesh J Pharmacol 2014; 9: 628-635

and at 20 µg/mL, the percentage viability was seen to
be decreased to 92% at 72 hours, indicating that this
fraction would be comparatively safer on humans
(Figure 3).
By phytochemical screening, among the different tests
performed, the samples (crude extract and the bioactive
fraction 2) indicated the presence of phenols (results not
shown). Based on the observation, the functional group
of the active component was tentatively identified as a
phenol.
Staining with EB/AO of the HeLa cells treated with the
bioactive fraction from the banana flower extract,
showed viable cells in the control flasks as green
(Figure 4a) with intact nuclei and the non-viable cells in
the treated flasks were bright orange (Figures 4b and
4c). Apoptosis was visible by the appearance of
breaking up of the nuclei. The effect of the bioactive
fraction 2 from banana flower extract on the activity of
initiator caspase-9 is shown in Figure 5. The fraction
was found to significantly increase the activity of
caspase-9 in HeLa cells treated for 48 hours. There was
a 2-fold increase of caspase activity in the treated HeLa
cells as compared to the control HeLa, confirming the
Figure 1: Effect of banana (Musa paradisiaca) flower ethanol extract on HeLa and CHO Cell Lines.*p<0.05 compared with control.
**p<0.001 as compared to the control
Figure 2: Effect of bioactive fraction 2 of banana flower extract on HeLa and CHO cells for 24, 48 and 72 hours. *p<0.05 compared
with control. **p<0.001 as compared to the control
Bangladesh J Pharmacol 2014; 9: 628-635 631

apoptotic induction of cell death in the cervical cancer
cell line HeLa.
The cytotoxicity, as assessed by LDH release by the
HeLa cells treated with 10 µg/mL of fraction 2 for 24
hours, was 32.8% (Figure 6) when compared with that
of the positive control i.e., 1% Triton-X 100, which could
induce all of the HeLa cell death through cytotoxic
effects. This indicates that the bioactive fraction has
released LDH when added to the HeLa cells, and LDH
release assays are an appropriate and possibly prefer-
able means of measuring cellular cytotoxic reactions.
The bioactive fraction 2 of banana flower demonstrated
anticancer activity by inhibiting the growth cycle of an
immortal cancer cell line HeLa. The addition of the
bioactive fraction resulted in decreasing the total
percentage of viable cells to 40.74% with the cell
population in the G
0
/G
1
phase at 27.5% (Figure 7 c and
d), S phase at 3.3% and G
2
/M phase with 5.1% when
assessed after 24 hours of treatment. There were
significantly fewer cells in the S and G2/M phases as
compared to the controls (Figure 7 a and b).
The bioactive fractions separated by TLC and identified
by bio-assay guided fractionation were further charac-
terized by LC-MS analysis. When the bioactive fraction
Figure 3: Effect of the bioactive fraction 2 on Lymphocytes
Figure 4: Fluorescence Microscopic photographs. 4(a) Control HeLa cells 4(b) HeLa treated with 10 µg/mL of bioactive fraction 2.
4(c) HeLa cells treated with 20 µg/mL of bioactive fraction 2. Arrows indicate the breaking up of the nuclei in apoptotic cells. The
treated cells are bright orange in color and fewer in number as compared to the control HeLa cells which are greenish in color and
more in numbers
a b c
Figure 5: Comparision of Caspase level between Control and
samples. *denotes 0.01 level of significance
632 Bangladesh J Pharmacol 2014; 9: 628-635

2 was subjected to HPLC, there were 3 peaks, one at RT
4.9, second larger peak at RT 6.9 and third at RT 10.1.
The larger peak has shown a mass to charge ratio of
224.20 by ESI-MS analysis (Figure 8). This m/z value
does not corresponding to that of any of the earlier
reported anticancer bioactive compounds identified
when checked in the anticancer database and hence
appears to be a novel one.
Discussion
In this study we evaluated the anticancer potential of
banana flower ethanol extract on the cervical cancer cell
line HeLa. As it has exhibited very good cytotoxic and
antiproliferative effects, we further purified it by TLC.
Three fractions were separated and all were tested for
antiproliferative properties on HeLa, CHO cells and
Figure 6: Cytotoxic effects of fraction 2 of banana flower extract determined by LDH leakage experiment using the cytotoxicity
detection kit
0
20
40
60
80
100
120
Positive control
Negative control
10 µg
Cytotoxicity (% of positive control)
Samples
7a 7b
7c 7d
Figure 7: Cell cycle analysis of the HeLa cells. 7a&b: control HeLa cells. 7c&d: HeLa treated with bioactive fraction 2
Bangladesh J Pharmacol 2014; 9: 628-635 633

normal human lymphocytes. Fraction 2 was showing
best results with an IC
50
of <10 µg/mL concentration.
This fraction was found to be a phenol by
phytochemical screening. This bioactive fraction could
induce apoptosis in the treated HeLa cells as evidenced
by the two-fold increase in caspase 9 activity assay as
compared to the control Hela cells. The apoptosis
induction ability was more profound on HeLa rather
than CHO cells. When the bioactive fraction 2 was
subjected to HPLC, there were 3 peaks, one at RT 4.9,
second larger peak at RT 6.9 and a third one at RT 10.1.
The larger peak has shown a mass to charge ratio of
224.2. This molecular weight is not corresponding to
that of any other earlier reported bioactive compounds,
so it could be a novel one with higher anticancer and
anti-proliferative effects. Furthermore, this fraction was
least toxic to human lymphocytes indicating that this
can serve as a better and safer source for identifying a
lead molecule in anticancer drug development.
However, further characterization and animal studies
are required to prove this. Till now there are several
reports on the pharmacological properties of banana
which include compounds that have anti-diabietic,
antioxidant (dopamine) antimicrobial, and antiulcer
(leucocyanidin) activities (Kanazawa and Sakakibara,
2000). Antifungal and antibiotic principles are found in
the peel and pulp of fully ripe bananas. The antibiotic
acts against Mycobacteria. A fungicide in the peel and
pulp of green fruits is active against a fungus disease of
tomato plants. Along with other fruits and vegetables,
consumption of bananas is associated with a reduced
risk of colorectal cancer (Deneo-Pellegrini et al., 1996),
renal cell carcinoma (Rashidkhani et al., 2005) and
breast cancer in women (Zhang et al., 2009). Banana
stem extract from the Musaceae family had been
suggested to be a useful agent in the treatment of
patients with hyperoxaluric urolithiasis (Poonguzhali
and Chegu, 1994), kidney stones and high blood
pressure. Oral administration of chloroform extract of
the M. sapientum flowers had been found to cause a
significant reduction in blood glucose and glycosylated
hemoglobin, increase in total hemoglobin and prevents
Figure 8: LC-MS analysis of TLC purified fraction 2 of banana flower extract
Upper panel: HPLC chromatogram of fraction 2 showing 3 peaks. Second peak was largest at RT 6.88 min.; Lower panel: LC-MS
spectra of the second fraction, m/z 224.20
634 Bangladesh J Pharmacol 2014; 9: 628-635

decrease in body weight (Pari and Uma-Maheswari,
1999). Though there are some studies on the bioactivity
of different parts of Musa species, the anticancer
potential of banana flower extract has not been
investigated so far.
This study shows that banana flower can serve as a
very good natural source for the development of an
anticancer lead molecule with least side effects.
Acknowledgement
The financial support by way of the grant provided by
Department of Science and Technology (No. SR/SO/HS-
0072/2012) is greatly acknowledged by the authors. The
authors are grateful to the management of Jain Group of
Institutions for the Junior Research Fellowship and
infrastructural facilities provided to carry out the work
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