Antioxidant and Antiproliferative Activities of Marine Algae, Gracilaria edulis and Enteromorpha lingulata, from Chennai Coast
Two species of marine algae, Gracilaria edulis and Enteromorpha lingulata, from Chennai coast were evaluated for their antioxidant and antiproliferative activities. Both algae were extracted with three solvents: methanol (M), chloroform (C) and ethyl acetate (E). The M, C, E extracts were investigated for 2, 2-diphenyl-1-picrylhydrazyl (DPPH) radical-scavenging, Beta-carotene Bleaching (BCB), total reducing (TRA) and Growth Inhibitory (GI) activities and Total Phenolic Content (TPC). Thin Layer Chromatography (TLC) was used for qualitatively compare DPPH radical-scavenging activity. Except for BCB, E. lingulata extracts showed comparable (TRA) or higher (DPPH radical-scavenging) antioxidant activity, TPC and GI in HCT15 cells than the extracts of G. edulis. E and C extracts of E. lingulata showed greater antioxidant and GI activities in HCT15 cell (no GI in A549) than M extract. Although M extract of G. edulis showed slightly greater DPPH radical-scavenging activity than C and E extracts, M showed lower TRA, TPC, BCB and GI in HCT15 cells than E and C extracts. None of the extracts showed GI in A549 cells but the GI trend in HCT15 cells mirrored the one seen for all extracts of both algae for TPC (E>C>M; E. lingulata>G. edulis). Except for the E extract of G. edulis which showed slight pro-oxidant activity in the BCB assay, its C and M extracts showed greater BCB inhibition than all the E. lingulata extracts. For all extracts of both algae, DPPH radical-scavenging activity in TLC was associated with the more polar compounds in the extracts.
Received: November 17, 2011;
Accepted: January 20, 2012;
Published: February 13, 2012
Marine algae are a group of aquatic autotrophic organisms that are broadly
classified as Chlorophyta (green), Rhodophyta (red seaweeds) or Phaeophyta (brown
seaweeds), based on the presence of photosynthetic pigments. Seaweeds are widely
included in Japanese and Chinese diet and traditional medicine (Fujiwara-Arasaki
et al., 1984; Chengkui et al., 1984)
and have developed biological molecules and approaches which help them survive
in their harsh and extreme environment. Seaweed sulfated polysaccharides like
fucoidan, carrageenan (red seaweed) or algin (brown seaweed) are rich sources
of soluble fibers, which have been reported to perform a varied range of functions
such as antioxidant, antimutagenic, anticoagulant and antitumor (De
Souza et al., 2007; Smit, 2004; Madhusudan
et al., 2011). Caulerpenyne from the Caulerpa spp. (green
algae) (Fischel et al., 1995) and polysaccharides
such as fucoidan and laminarin from brown seaweeds have also been reported to
show antitumor activity (Yamasaki-Miyamoto et al.,
2009). Therefore, the objective of the present study was to explore marine
algae for new compounds possessing antioxidant and antiproliferative activities,
so that these compounds could be used as leads for making more potent, selective
and less toxic drugs with better therapeutic indices. Gracilaria edulis
and Enteromorpha lingulata are edible marine algae. However, in Phillipines,
three fatal poisoning cases have been reported during 2002-2003 due to ingestion
of G. edulis and Acanthophora spicifera (Yotsu-Yamashita
et al., 2004). There are no reports, to date, on the in vitro
antiproliferative activity of G. edulis. To the best of our knowledge,
this is the first report on investigation into antioxidant and antiproliferative
activities of Enteromorpha lingulata and antiproliferative activity of
MATERIALS AND METHODS
Sample collection: Enteromorpha lingulata and Gracilaria edulis were collected from the Chennai coast of Tamil Nadu, India and identified by Dr. Baluswami, Madras Christian College, Chennai.
Chemicals: Ascorbic acid, beta-carotene, BHA (butylated hydroxyanisole), DPPH (2, 2-diphenyl-1-picrylhydrazyl), gallic acid, linoleic acid, DMEM growth medium and resazurin sodium salt were purchased from Sigma-Aldrich, India. Quercetin was purchased from Fluka, India. All other chemicals were purchased from SRL, India. Bromophenol blue, trichloroacetic acid (TCA) and other cell culture materials were purchased from HiMedia, India. TLC plates (TLC Silica gel 60 F254) were purchased from Merck, India. Cell lines were obtained from the National Centre for Cell Sciences in Pune, India.
Algal extract preparation: The samples were washed thoroughly in fresh
water and subsequently shade-dried and powdered (Vinayak et
al., 2011). Five grams of the dry powder was extracted twice for 16
h each time, with 50 mL of each solvent (methanol, chloroform or ethyl acetate
separately) in a rotary shaker at 37°C. The extracts were filtered and the
solvent was removed completely by using a rotary evaporator (Buchi Rotavapor
R215, Switzerland). The crude extract was stored at -20°C and reconstituted
in methanol for assays.
DPPH radical-scavenging activity: The free radical-scavenging potential
of the algal extracts was analyzed according to previously reported methods
(Zubia et al., 2009; Butkhup
and Samappito, 2011; Jain et al., 2011; Amatya
and Tuladhar, 2011; Hanachi et al., 2006).
The concentrations of M (methanol), C (chloroform) and E (ethyl acetate) extracts
taken for the experiment were 10, 50 and 100 μg mL-1. A methanolic
solution of DPPH (200 μL, 20 mg L-1) was added to 22 μL
of each extract in a 96 well plate. Ascorbic acid was used as a positive control
while 200 μL of DPPH solution plus 22 μL methanol without any extract
was used as a control, to calculate the extent of scavenging. The plate was
incubated in the dark for 2 h at room temperature and the absorbance measured
at 492 nm spectrophotometrically (Fluostar Optima BMG Labtech Gmbh).
% DPPH radical scavenging activity was determined by the formula:
||Absorbance with extract
||Absorbance of control (200 μL of DPPH, 22 μL of methanol)
Beta-carotene bleaching assay: The antioxidant potential of marine algae
was measured by modifying the beta-carotene bleaching assay described earlier
(Zubia et al., 2009; Duan
et al., 2006; Amatya and Tuladhar, 2011;
Hanachi et al., 2006). About 210 μL of a
solution of beta-carotene (1 mg mL-1) in chloroform was taken in
a round bottom flask containing 5 μL of linoleic acid and 42 μL of
Tween-20. The chloroform was removed in a rotary evaporator at 40°C and
10 mL of distilled water was added to form an emulsion with continuous shaking.
Approximately 200 μL of the above emulsion was added to 50 μL of extracts
(100 μg mL-1) taken in a 96 well microplate. Emulsion without
beta-carotene was used as a blank, BHA was used as a positive control and wells
containing the beta-carotene emulsion with methanol instead of extract served
to calculate the extent of bleaching. The plate was immediately read at 450
nm (0 h) and after 2 h of incubation at 50°C in the dark. Antioxidant activity
(AA) was measured by using the formula:
|At0 and At2
||Absorbance with extracts measured at 0 and 2 h, respectively
|Ac0 and Ac2
||Absorbance of control (beta-carotene-containing emulsion and methanol
instead of extract) measured at 0 and 2 h, respectively
Total reducing activity: The reducing power of marine algae was determined
by using the assay described earlier (Zubia et al.,
2009; Ashawat et al., 2007). To 200 μL
of the M, C and E extracts, 200 μL of phosphate buffer (200 mM, pH 6.6)
and 200 μL of 1% potassium ferricyanide solution were added. The mixture
was incubated at 50°C for 30 min and 200 μL of 10% TCA solution added
after the mixture had cooled down. After mixing, 125 μL of the above mixture
was transferred to a 96 well plate and 20 μL of 0.1% ferric chloride solution
was added. The formation of a Prussian blue complex indicated the reducing power
of the samples. The absorbance was measured at 620 nm in a plate reader (Fluostar
Optima BMG Labtech GmbH). Ascorbic acid was used as positive control and the
reaction mixture with methanol instead of the extract was used as (negative)
control. The total reducing activity was determined by using the formula:
||Absorbance of control (reaction mixture with methanol instead
||Absorbance with extracts
Total phenolic content: The total phenolic content present in G.
edulis and E. lingulata extracts was determined by using the Folin-Ciocalteu
method described earlier (Masaldan and Iyer, 2011).
Gallic acid (1 mg mL-1) in methanol was used as a standard in concentrations
ranging from 2 to 10 μg mL-1. To 10 μL of standard/extracts
(1 mg mL-1) in a 2 mL tube were added 25 μL of the Folin-Ciocalteus
phenol reagent and 50 μL of 25% sodium carbonate solution. The mixture
was vortexed and the volume was made up to 1 mL with distilled water. The tubes
were then incubated in the dark for 1 h at room temperature and the absorbance
was measured at 725 nm in a spectrophotometer (Beckman Coulter Du 730). Quercetin
(1 mg mL-1) in methanol was used as a positive control.
Thin layer chromatography: Thin layer chromatography was used to qualitatively
determine the antioxidant activity of selected marine algae by the method described
earlier (Masaldan and Iyer, 2011; Jain
et al., 2008). Methanolic solutions of M, C and E extracts were spotted
on precoated silica gel aluminium sheets. These extracts were resolved separately
by using the following three solvent systems listed in the order of increasing
polarity: BEA benzene/ethanol/ammonium hydroxide (90:10:1), CEF-chloroform/ethyl
acetate/formic acid (5:4:1) and EMW-ethyl acetate/methanol/water (40:5.4:5).
The chromatograms obtained were further analyzed with iodine vapor and DPPH
solution (0.2% in methanol).
Cell culture: A549 (lung adenocarcinoma) cells were grown in DMEM growth medium and HCT15 (colon adenocarcinoma) cells were grown in RPMI growth medium at 37°C in a 5% CO2 atmosphere. The medium was supplemented with 10% FBS and penicillin (100 U mL-1) and streptomycin (100 μg mL-1). For experiments, A549 (2500) cells and HCT15 (4000) cells in 200 μL media well-1 were seeded in a 96 well plate.
Growth inhibition assay: The antiproliferative potential of the marine
algal extracts was studied in the above cell lines by using a resazurin-based
assay (Masaldan and Iyer, 2011; Anoopkumar-Dukie
et al., 2005). Resazurin is the active component of the blue redox
dye, Alamar Blue® which is converted into pink resorufin by the
oxido-reductases in the cytoplasm, mitochondria and microsomes of viable cells.
Cells were seeded in two 96 well plates-T0 and Ti, with
media blank and untreated control and incubated at 37°C in a 5% CO2
atmosphere. After 24 h, the T0 plate was treated with 10% resazurin
(1 mg mL-1 in 50 mM PBS) for 4 h and the absorbance was measured
at 584 nm and 620 nm. At the same time, the Ti plate was treated
with 100 μg mL-1 of M, C and E extracts (in DMSO) and Doxorubicin
(positive control). Medium blank with and without 0.5% DMSO (vehicle blank)
as well as untreated (negative) control with and without 0.5% DMSO were also
included in the Ti plate. After 48 h, the Ti plate was
treated with resazurin like the T0 plate and the absorbance was measured.
% of growth inhibition (GI) was calculated using the formula:
||OD584-620 of untreated cells after 24 h
||OD584-620 of cells treated with test compound after 48 h and
||OD584-620 of negative control cells after 48 h (blanks subtracted
Statistical analysis: All experiments were performed in triplicate (n
= 3) and expressed as Mean±SEM. Means were compared with SPSS v 16.0
software for Windows (SPSS Inc., Chicago, IL) by using one-way ANOVA followed
by the Tukeys post-hoc test. p<0.05 indicated statistical significance.
Pearson correlation coefficient (r) was calculated (p<0.05) to assess the
strength of the linear relationship between two variables.
ANOVA analysis indicated that the difference between the group means was statistically significant (p<0.05). However, except for a high positive correlation observed between the means for GI values in HCT15 and TPC values, none of the other Pearson correlation coefficients were significant for any of the other group mean pairs (p>0.05). Tukeys HSD post-hoc test showed that the differences between the following group mean pairs were statistically significant (p<0.05): DPPH radical scavenging and BCB assay group means; DPPH radical scavenging and A549 GI group means; A549 GI and TRA group means; A549 GI and BCB group means; A549 GI and HCT15 GI group means; HCT15 GI and BCB group means and BCB and TPC group means.
DPPH radical scavenging activity: The antioxidant potential of marine
algae was measured in terms of their ability to scavenge the stable DPPH radical
(Fig. 1). Enteromorpha lingulata C and E extracts (100
μg mL-1) showed higher activity of 15.85 and 15.61%, respectively.
The M extracts of both E. lingulata and G. edulis (100 μg
mL-1) were almost equal in their DPPH radical-scavenging activity
(13.59 and 14.84%, respectively). Lower activity was observed in G. edulis
with 100 μg mL-1 C and E showing 9.01 and 8.47%, respectively.
Tukeys HSD post-hoc test showed that the differences between the DPPH
radical scavenging and BCB assay group means and between the DPPH radical scavenging
and A549 GI group means were statistically significant (p<0.05).
Thin layer chromatography: The chromatograms showed the presence of
organics and DPPH free radical-scavenging molecules when exposed to iodine vapor
and DPPH solution, respectively (Fig. 2, 3).
All organics appeared as brown spots and the scavenging of the DPPH radical
was seen in the form of disappearance of purple color at some spots.
||DPPH radical scavenging activity of the G. edulis and
E. lingulata extracts; M: Methanolic extract, C: Chloroform extract,
E: Ethyl acetate extract
||TLC analysis of G. edulis: methanol (M), chloroform
(C) and ethyl acetate (E) extracts using different eluent systems; A: BEA,
B: CEF and C: EMW (from left to right) treated with (a) iodine vapor for
all organics and (b) DPPH solution for radical scavenging activity
|| TLC analysis of E. lingulata: methanol (M), chloroform
(C) and ethyl acetate (E) extracts using different eluent systems; A: BEA,
B: CEF and C: EMW (from left to right) treated with (a) iodine vapor for
all organics and (b) DPPH solution for radical scavenging activity
Our results suggest that DPPH radical-scavenging activity was associated with
the more polar components in all extracts because the Rf values of
these components increased with increasing polarity of the resolving system.
For all three extracts of both algae, E. lingulata extracts showed strong
DPPH radical-scavenging activity in TLC and C and E extracts of G. edulis
seemed to have stronger DPPH radical-scavenging activity on the TLC plates than
the M extract.
Beta-carotene bleaching assay: Antioxidant activity was also examined
in terms of inhibition of beta-carotene bleaching by linoleic acid (Fig.
4). The highest inhibitory activity (60%) was found in G. edulis C
extract whereas E extract had negligible activity at 100 μg mL-1.
||Beta-carotene bleaching inhibition by G. edulis and
E. lingulata extracts; M: Methanolic extract, C: Chloroform extract,
E: Ethyl acetate extract
||Total reducing activity of the G. edulis and E.
lingulata extracts; M: Methanolic extract, C: Chloroform extract, E:
Ethyl acetate extract
G. edulis M and E. lingulata M, C and E extracts had almost similar
inhibitory activity of around 40%. Tukeys HSD post-hoc test showed that
the differences between A549 GI and BCB group means; HCT15 GI and BCB group
means and BCB and TPC group means were statistically significant (p<0.05).
Total reducing activity: The total antioxidant potential of marine algae was also determined by their reducing power and the results are shown in Fig. 5. The reducing power of the extracts showed concentration dependence with G. edulis C and E extracts having higher values of 38.16 and 37.54% at 200 μg mL-1, respectively. The C and E extracts of E. lingulata also had similar activity (32.21 and 37.41%, respectively) whereas M extracts of both algae showed lower values: G. edulis M: 17.64%; E. lingulata M: 13.64%. Tukeys HSD post-hoc test showed that the differences between A549 GI and TRA group means were statistically significant (p<0.05).
Total phenolic content: As phenols from natural sources are considered
to be good antioxidants, the antioxidant potential observed in the two marine
algae in this study was postulated to be linked to the phenolic constituents.
|| Total phenolic content
|M: Methanolic extract, C: Chloroform extract, E: Ethyl acetate
extract, Quercetin was used as positive control with GAE 8.25±0.15
at 10 μg mL-1. All values are represented as Mean±SEM
(n = 3)
The phenolic content of the algal extracts was measured in terms of Gallic
Acid Equivalents (GAE) from the regression equation y = 0.1249 x+0.0319 of the
gallic acid standard curve (Fig. 6). The E extract of
E. lingulata had the highest phenolic content of 0.54 μg mL-1
GAE, whereas G. edulis M extract had the least phenolic content of 0.14
μg mL-1 GAE for 1 mg mL-1 of the extracts (Table
1). Tukeys HSD post-hoc test showed that the differences between TPC
and BCB group means were statistically significant (p<0.05). Also, a high
positive correlation (Pearson correlation coefficient) was observed between
the means for GI values in HCT15 and TPC value, at p<0.05, suggesting a link
between the TPC and GI observed in HCT15 cells for all these extracts (in particular,
E of E. lingulata).
Growth inhibition assay: The antiproliferative activity of G. edulis and E. lingulata M, C and E extracts showed different trends in HCT 15 and A549 cell lines (Fig. 7). The E. lingulata E extract showed maximal inhibition in the HCT15 cell line of about 19.37% followed by C extract (15.66%); the M extract showed no growth inhibition. G. edulis (E, C and M) extracts showed low growth inhibition of about 7.12, 4.22 and 0.79%, respectively. Neither alga had any growth inhibitory effects on the A549 cell line (Fig. 7). Tukeys HSD post-hoc test showed that the differences between DPPH radical scavenging and A549 GI group means; A549 GI and TRA group means; A549 GI and BCB group means; A549 GI and HCT15 GI group means and HCT15 GI and BCB group means were statistically significant (p<0.05).
||Growth inhibition by G. edulis and E. lingulata-M,
C, E extracts in HCT15 and A549 cell lines at 100 μg mL-1
Reactive oxygen species (free radicals) are highly reactive chemical molecules
that are formed as by-products of normal metabolism and whose levels increase
dramatically due to various environmental stresses or damage. They finally cause
great damage to the cells by interacting with vital cellular components like
DNA or the cell membrane. Antioxidants play an important role in preventing
cellular damage-a major feature of cancer, ageing and various other diseases-by
neutralizing these free radicals (Chanda et al.,
2011; Lompo et al., 2007). Several molecules
and antioxidants from natural sources, such as mushrooms and higher plants have
been reported and used for therapeutic benefit (Dimitrios,
2006; Samchai et al., 2009; Anokwuru
et al., 2011).
Cancer is the most commonly occurring disease worldwide of which,
lung and colon cancers are widely prevalent (Garcia et
al., 2007). Most of the anticancer drugs in clinical use possess deleterious
side effects. Hence, the discovery of novel anticancer drug leads with better
toxicological and pharmacokinetic profiles is of great importance. Phytochemicals,
such as polyphenols, are considered to be good chemo-preventive agents for colorectal
cancer (Sale et al., 2005). Several anticancer
drugs from plant sources, such as taxol, vinblastine, vincristine and etoposide
phosphate, have been in use for the treatment of cancer (Da
Rocha et al., 2001). Antioxidant and antiproliferative studies have
been performed on various marine algae (seaweeds) all over the world (Vinayak
et al., 2011; Zubia et al., 2009;
Yuan and Walsh, 2006; Ismail and
Hong, 2002). In India too, reports have demonstrated antioxidant activity
of marine algae found along the Indian coastline but only few reports describe
antiproliferative activity (Delma et al., 2008;
Sachindra et al., 2010; Ganesan
et al., 2008). Hence, the current study has been conducted to determine
the antioxidant and antiproliferative activities of M, C and E extracts of two
marine algae from the Chennai coast in Tamil Nadu, India.
Gracilaria edulis and Enteromorpha lingulata are edible marine
algae. There are no reports, to date, on the in vitro antiproliferative
activity of G. edulis although three fatal poisoning cases have been
reported during 2002-2003 in Phillipines, due to ingestion of G. edulis
and Acanthophora spicifera (Yotsu-Yamashita et
al., 2004). Our TLC results suggest that the relatively polar compounds
that have been extracted by all three solvents (methanol, chloroform, ethyl
acetate) from both algae are likely to be strong contributors to the observed
DPPH radical scavenging activity. While it is difficult to correlate the qualitative
results of TLC with the quantitative ones of the DPPH radical-scavenging assay,
E. lingulata extracts showed strong DPPH radical-scavenging activity
in both TLC and the assay. M extract of G. edulis showed greater DPPH
radical-scavenging activity at all concentrations in the assay in contrast to
the results of TLC analysis. In contrast, Devi et al.
(2008) had reported a value of 25% for the DPPH radical-scavenging activity
of the methanolic extract of G. edulis at 100 μg mL-1.
However, they used different concentrations of DPPH and a different incubation
period in their assay. No reports were found on the antioxidant activity of
In contrast to the higher activity seen for E. lingulata in other assays, the BCB assay showed that G. edulis C extract had the highest inhibitory activity of about 60% at 100 μg mL-1, with the others being almost comparable to the positive control, BHA (100 μg mL-1, 39%), except for E extract of G. edulis which showed slight pro-oxidant activity.
Total reducing activity of the E extract of E. lingulata was the highest of all, followed by C and E extracts of G. edulis and the C extract of E. lingulata, with the M extracts of both algae showing the least total reducing activity. Total phenolic content was higher for E. lingulata (E>C>M for both algae).
Reports suggest that the widely prevalent cancer of the colon can metastasize
into other organs, such as the lungs and vice versa (Dishop
and Kuruvilla, 2008). Hence, the antiproliferative effects of the algae
were tested on HCT15 (colon carcinoma) and A549 (lung adenocarcinoma) cells.
The results show no growth inhibitory effects of any of the extracts on A549
cells; in fact, the E. lingulata extracts (M>C>E) showed varying
growth-promoting effects. However, the C and E extracts (E>C) of E. lingulata
showed very modest growth inhibition (15.7 and 19.4%) in HCT15 cells. The M,
C, E extracts of G. edulis and the M extract of E. lingulata showed
very negligible or no inhibitory effects on the growth of HCT15 cells. A higher
Pearson correlation coefficient (>0.8) between TPC and HCT15 GI means suggests
a role for phenolic compounds in the antiproliferative activity of the E extract
of E. lingulata.
In summary, the above results suggest that the compounds extracted by methanol, chloroform and ethyl acetate into M, C and E extracts of both algae show different levels of antioxidant activities. Regardless of the differences observed for the various assays, it appears that the relatively more polar components extracted from Enteromorpha lingulata by ethyl acetate and chloroform showed higher antioxidant (DPPH radical-scavenging, TRA) activities than the others. In contrast, the methanolic (M) extracts of both algae, especially of G. edulis, showed the lowest antioxidant activities (DPPH, TRA). The similar trend of total phenolic content (E, C>M and E. lingulata>G. edulis) warrants further investigation into the nature of the compounds in the E and C extracts of E. lingulata that have shown the observed antioxidant and antiproliferative activities (in HCT15 cells).
The authors would like to thank the Department of Science and Technology (DST), India, for financial support. We are also grateful to Dr. Baluswami, Madras Christian College, Chennai, for his valuable help in identifying the algae and to Ms. S. Sowmya, VIT University, Vellore, for her valuable inputs into the statistical analysis.
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