Anatolian Journal of Botany
Anatolian Journal of Botany
2(2): 60-64 (2018)
doi:10.30616/ajb.413645
Cell growth inhibitory potential of Craterellus cornucopioides (L.) Pers.
together with antioxidant and antimicrobial properties
Sevim KOL, Aykut BOSTANCI, Aytaç KOCABAŞ, Yasin UZUN, Gökhan SADİ*
Karamanoğlu Mehmetbey University, K.Ö. Science Faculty, Department of Biology, Karaman, Turkey
*
[email protected] Antioksidan ve antimiktobiyal özellikleri ile birlikte Craterellus
Received : 09.04.2018
Accepted : 07.05.2018
cornucopioides (L.) Pers. türünün hücre büyümesi baskılama potansiyeli
Abstract: Craterellus cornucopioides (L.) Pers which is also known as trumpet of death or horn of plenty, is a wild edible
macrofungus. This study was conducted to elucidate the potential health beneficial properties of C. cornucopioides. Bioactive
ingredients (phenolics, flavonoids, β-carotene and lycopene) and DPPH radical scavenging activities were determined.
Additionally, cell growth inhibitory effects on HepG2 cells together with some bacteria were evaluated. Accordingly, water and
methanol extracts contains 37.71±1.42 μg/mg and 13.78±1.60 μg/mg phenolic contents, respectively. Similarly, methanolic
extracts have higher β-caroten and lycopene content as compared to aqueous extracts. In parallel with these antioxidants,
methanolic extracts have also higher DPPH scavenging activity (IC50: 5.26±0.67 mg/ml). Besides, water extracts have higher
flavonoid contents (2.13±0.06 μg/mg) then the methanolic extracts. C. cornucopioides has also an important cell growth
inhibitory effects on HepG2 cell (IC50: 18.41±1.10 mg/ml for aqueous extracts and IC50: 3.14±1.07 mg/ml for methanolic
extracts). Moreover, both extracts were effective on six different bacteria tested. As a result, this study indicates that C.
cornucopioides could reduce the cellular oxidative stress because of its high antioxidant ingredients, inhibit the growth of
pathogen microrganisms and have some degree of cell growth inhibitory potential at least to the HepG2 cells.
Key words: Craterellus cornucopioides, antioxidant, antibacterial, cytotoxicity, HepG2
Özet: Ölüm trompeti veya bolluk boynuzu olarak da bilinen Craterellus cornucopioides (L.) Pers, yenilebilir bir
makrofungustur. Bu çalışma Craterellus cornucopioides (L.) Pers mantarının sağlık açısından yararlı özelliklerini açığa
çıkarmak amacıyla yapılmıştır. Çalışmada ilgili mantarın biyoaktif içerikleri (fenolikler, flavonoidler, β-karoten ve likopen) ve
DPPH radikal süpürücü aktiviteleri belirlenmiştir. Ek olarak, HepG2 hücreleri ve bazı bakteri türleri üzrine hücre büyümesini
baskılayıcı etkileri değerlendirilmiştir. Buna göre, su ve metanol ekstraktları sırasıyla 37.71±1.42 μg/mg ve 13.78±1.60 μg/mg
fenolik içeriğe sahiptir. Benzer şekilde, metanol ekstraktları sulu ekstrelere kıyasla daha yüksek β-karoten ve likopen içeriğine
sahiptir. Bu antioksidanlara paralel olarak, metanol ekstraktları da DPPH süpürme aktivitesine daha fazla sahiptir (ICso:
5.26±0.67 mg/ml). Ayrıca su ekstraktları, metanol ekstraklarına göre daha yüksek flavonoid içeriğine (2.13±0.06 μg/mg)
sahiptir. C. cornucopioides, HepG2 hücresi üzerinde de önemli bir hücre büyümesi engelleyici etkiye sahiptir (IC 50: su
ekstratları için 18.41±1.10 mg/ml ve metanol ektraktları için IC50: 3.14±1.07 mg/ml). Buna ek olarak, her iki ekstrakt da test
edilen altı farklı bakteri türü üzeine etkili olmuştur. Sonuç olarak, bu çalışma C. cornucopioides'in yüksek antioksidan
bileşenleri nedeniyle hücresel oksidatif stresi azaltabildiğini, patojen mikroorganizmalarının büyümesini inhibe edebileceğini ve
en azından HepG2 hücrelerine bir miktar hücre büyümesi inhibitör potansiyeline sahip olduğunu göstermektedir.
Anahtar Kelimeler: Craterellus cornucopioides, antioksidan, antibakteriyel, sitotoksisite, HepG2
1. Introduction cellular components such as organelles (Yıldız et al.,
2015, Manivannan et al., 2011) and they are quenched by
Fungi are eukaryotic and heterotrofic organisms that are
antioxidant molecules or related antioxidant enzymes.
composed of tubular filamentous cells, free chlorophyll
Mushrooms gain importance according to rich bioactive
and create spores. They could not produce their own foods
compounds such as polyphenols, polysaccharides,
thus which live as saprophyts, mycorrhizal and parasite.
vitamins, carotenoids and minerals (Kozarski et al. 2015,
Edible mushrooms contain macro-molecules, which are
Cheung et al., 2002). Studies have shown that antioxidant
normally 19 to 35% protein, and all protein content almost
rich foods might play an important role in reducing the
comprises essential amino-acids. They also include
risk of disease, such as cardiovascular diseases, stroke and
polyunsaturated fatty acids (72-85%) and carbohydrates
cancer (Gan et al., 2013, Barros et al., 2007; Jagadish et
(51-88%) according to dry or fresh weight (Chang et al.,
al. 2009). Therefore, antioxidants in edible mushrooms
1996). Medicinal mushrooms have important therapeutic
might act against reactive oxygen species and contribute
features and, due to these features, they have been used
to create antioxidant responses. Macrofungi also gain
against many kinds of disease for treatment in traditional
importance in cancer inhibition and treatment with the
medicine. For example, many genre mushroom such as
secondary metabolites found in their structure. Moreover,
Agaricus, Aleurodiscus, Clitocybe, Coprinus, Daedalea,
they also could be used against microbial infections. Some
Ganoderma, Lentinula, Merulius, Pleurotus, Polyporus,
metabolites might prevent the growth of certain bacterial
Poria, Psathyrella and Tricholoma rise in value due to
and fungal pathogens (Alves et al., 2012).
their major properties such as anti-microbial (Chang et al.,
2012), anti-viral (Pan et al. 2013), anti-oxidant (Palacios For example, applanoxidic acid A isolated from
et al., 2011), anti-cancer (Mattila et al., 2000). Ganoderma annulare (Fr.) Gilbn. has been showed to be
effective against Trichophyton mentagrophytes. Moreover,
Free radicals have been generated by many biological
5a-ergosta- 7,22-dien-3b-ol 5,8-epidioxy-5a,8a-ergosta-
pathways or infections in organisms, damaging the
60
Kol et al.- Cell growth …
6,22-dien-3b-ol isolated from Ganoderma applanatum β-carotene content (mg/100 mg) =0.216 A663 - 0.304 A505
(Pers.) Pat., have been shown to affect several gram- + 0.452 A453
positive and gram-negative microorganisms (Smania et
Lycopene content (mg/100 mg) = −0.0458 A663 + 0.372
al., 1999, Smania et al., 2003). In this study, C.
A505 - 0.0806 A453
cornucopioides was investigated for its antimicrobial,
antioxidant, and cytotoxic properties to contribute the 2.5. Identification and Quantification of Main
studies that are done in pharmaceutical area. Phenolic Compounds by HPLC
2. Materials and Method Phenolic substance identification was carried out with
HPLC (Shimadzu LC-20AD system, Japan). Data was
2.1. Preparation of Fungal Extracts
processed using LC Solution software (Shimadzu, Japan).
Craterellus cornucopioides (L.) Pers that was used in this As mobile phase; (A) 0.1% (v/v) formic acid and (B)
study was collected from Trabzon province with a voucher acetonitrile mixtures were used as gradient. Gradient
number of Yuzun 1852. The samples are kept at elution conditions are as follows: Starting 20% B; 0-10
Karamanoglu Mehmetbey University, Kamil Özdağ min 20% -30% B; 10-40 min 30-40% B; 40-60 min 40% -
Science Faculty, Department of Biology. Water and 560% B; 60-80 min 60-80% B; and finally, 90 min from
methanol extracts were prepared to examine cytotoxic, 80% -20% B. The flow rate was set to 1 ml/min, the
antioxidant and antimicrobial effects. Ten grams of entire column temperature was fixed at 30ᵒC. Phenolic
mushrooms were homogenized by using liquid nitrogen, compounds were identified by using standards that were in
mortar and pestle and exposed to extraction in 300 ml known concentration. Gallic acid, catechin, epicatechin,
methanol or distilled water with Soxhlet extraction epigallocatechin gallate, syringic acid, p-coumaric acid,
apparatus. Then, extracts were concentrated in a rotary rosmarinic acid, t-resveratrol and quercetin standard
evaporator, lyophilized and stored at +4 ° C for further curves were constructed and the amount of these phenolics
use. in C. cornucopioides extracts were quantitatively
determined. At least three applications were performed for
2.2. Determination of Total Phenolic Content
each sample (Standard or sample) and sample absorbances
Folin-Ciocalteu method was used for the determination of were monitored at 271 nm, 280 nm and 309 nm.
total phenolic content (Taga et al., 1984). Gallic acid (0.02
2.6. Determination of Reducing Power
to 1.00 mM) was used as standard. Fungal extracts (10
mg/ml) and standards (0.02-1.00 mM) were placed in 20 After the slight modifications that were made to adopt the
μl microplate wells. Afterwards, 20 μl of Folin reagent method to microplate measurement, reducing powers of
(2N) was added and mixed by pipetting. After incubation different extracts were determined according to the
for 3 min in the dark, 20 μl of 35% (w/v) sodium previously prescribed protocol (Sadi et al., 2015). Gallic
carbonate and 140 μl of dH2O were added to the plate and acid (0.010.10 mM) was used as a standard antioxidant.
incubated for 10 min in the dark. The absorbance values Briefly, in a total volume of 200 µl, various concentrations
were recorded against the blank tube at 725 nm and the of 50 µl mushroom extracts (2, 4, 6, 8, 10 mg/ml) were
amount of total phenolic content in one mg extract was mixed with 75 µl phosphate buffer (0.2 M pH: 6.6),75 µl
calculated using a standard calibration curve generated potassium ferricyanide (1% w/v) and incubated at 50°C
with gallic acid. for 20 min. After adding 75 µl trichloroacetic acid (10%
w/v), samples were centrifuged for 10 min at 1000 g and
2.3. Determination of Total Flavonoid Content
supernatants (75 µl) were transferred to another microtiter
Total flavonoids of water and methanol extracts were plate. Then, they were mixed with 75 µl distilled water
determined according to method (Pal et al., 2010) with and 15 µl iron (III) chloride (0.1% w/v).
slight modifications. A volume of 50 µl of extracts (10 Spectrophotometric measurements were employed at 700
mg/ml) were mixed with 215 µl of ethyl alcohol (80% nm and the effective concentrations (EC50) at which the
v/v), 5 µl of aluminum nitrate (10% w/v) and 5 µl absorbance was 0.500 for the reducing power was
potassium acetate (1 M) in microtiter plates and incubated calculated.
for 40 min at room temperature. After reading at 415 nm,
2.7. Determination of DPPH Radical Scavenging
total flavonoid contents were calculated according to
Activity
following equation:
DPPH (2,2-diphenyl-1-picrylhydrazyl) radical scavenging
Total flavonoid contents (µg/mg extract) = (A415 +
activity of C. cornucopioides was measured (Türkoglu et
0.01089)/0.002108
al., 2007) to determine antioxidant power. Accordingly,
2.4. Determination of β‑carotene and Lycopene different concentration C. cornucopioides extracts (0.25 to
Contents 10 mg/ml) and gallic acid (0.005 to 0.2 mM) were
prepared for measuring the elimination activity of DPPH
Different extracts with water and methanol that were radical. From C. cornucopioides extracts and standards, 20
obtained from C. cornucopioides were reextracted with 10 μl was added to each microplate well and 180 μl DPPH
ml of acetone:hexane (4:6) mixture and filtered through (0.06 mM in methanol) was added. After incubation for 60
Whatman No. 4 filter paper to determine β-carotene and min in dark, the reduction of DPPH radical was followed
lycopene contents. After filtration, absorbance of the by the absorbance values that were measured at 517 nm.
filtrates was measured at 453, 505 and 663 nm. β-carotene Free radical capturing activities were calculated according
and lycopene contents were calculated according to to the following formula. The DPPH radical scavenging
following equations. activity (RSA) was calculated as IC50 values for each
sample.
61
Anatolian Journal of Botany
active substances have gained reputation in the
pharmaceutical area.
2.8. Determination of cell growth inhibitory potential In studies of antioxidant, antimicrobial and cytotoxic
activities of macrofungi and other medical effects,
2.8.1. Antimicrobial properties important data have been obtained. In this study,
Six test bacteria; Bacillus subtilis, Enterococcus faecalis, antioxidant, antimicrobial and cytotoxic activities of
Bacillus licheniformis, Staphylococcus aureus (ATCC Craterellus cornucopioides (L.) Pers. is researched.
2921) as Gram Positive; Agrobacterium tumefaciens and Amount of bioactive compounds present in aqueous and
Escherichia coli (0157: H7 ATCC 43895) as Gram methanolic extracts of C. cornucopioides are summarized
negative were grown in liquid Mueller Hinton Broth in Table 1. Results demonstrated that water extracts of C.
overnight in a shaker incubator. The concentrations of the cornucopioides has very high amount of total phenolics
microorganisms were adjusted to be equal to 0.5 (37.71±1.42 µg/mg) which is also in parallel with the
McFarland standard (1.5x10+8 CFU/ml). The empty discs main phenolics; gallic acid and p-coumaric acid
were loaded with 20 μl of stock 200 mg/ml C. determined with HPLC analysis. Similarly, total flavonoid
cornucopioides extracts and placed on petri plates for disk contents (2.13±0.06 µg/mg) were also higher as compared
diffusion method. Gentamicin was used as the standard with methanolic extracts (1.83±0.02 µg/mg). On the
antibiotic. Then A. tumefaciens (28°C) and other other hand, methanolic extracts have higher content of the
microorganisms (35°C) were incubated overnight to β-carotene and lycopene. Additionally, the phenolic
examine the antimicrobial activity in the petri dishes. At compounds such as gallic acid, catechin, epicatechin,
the end of this period, the zones of inhibition around the epigallocatechin gallate, syringic acid, p-coumaric acid,
discs were measured by means of a digital ruler. rosmarinic acid, t-resveratrol and quercetin in C.
2.8.2. Cytotoxic effects on HepG2 cells cornucopioides extracts were quantitatively determined by
HPLC but, the amount of other phenolic compounds,
HepG2 (human hepatocellular cancer) cells were used to except p-coumaric acid and gallic acid was either under
investigate of cytotoxic effect of aqueous and methanol HPLC limit or had no in C. cornucopioides extracts.
extracts of C. cornucopioides. Growth medium (RPMI
with L-glutamine) was heated to 37°C and cells were Table 1: Antioxidant activity, reducing power and bioactive
ingredients of C. cornucopioides extracts.
added. Then, they were grown in a 5% CO2 incubator
(Sanyo, USA) at 37 °C with 95% humidity. One day after, Bioactive C. cornucopioides
the cells were washed with PBS and detached by Content
Ingredients extract
trypsinization when 80-90% saturation was reached.
DPPH scavenging Water 12.01±1.72
Passaged cells were grown again at 37 °C in 5% CO 2
(IC50 : mg/ml) MeOH 5.26±0.67
(Sanyo MCO 17AIC, USA) until confluency of 90%. The
cytotoxic effects of C. cornucopioides extracts were Reducing power Water 4.54±0.61
determined in accordance with the manufacturer's protocol (EC50: mg/ml) MeOH 6.52±1.53
with the XTT cell proliferation assay kit (Biological
Water 37.71±1.42
Industries, Israel). For this, 50 μl of activated XTT (Cell Phenolics
Proliferation Assay Kit) was added to the cells which were (µg//mg) MeOH 13.78±1.59
preincubated with different concentration of C. Water 3.89±0.06
ß-carotene
cornucopioides extracts for 48 hours at 37 ° C, 5% CO 2. (µg/mg) MeOH 6.34±0.08
At the end of the 5 h XTT incubation, absorbance values
at 450 nm was measured with a microplate reader Lycopene Water 2.49±0.01
(MultiskanTM GO, Thermo Scientific, USA) and IC50 (µg/mg) MeOH 5.55±0.08
values were calculated. Water 2.13± 0.06
Flavonoid
2.9. Statistical Analyses (µg/mg) MeOH 1.83±0.02
All the assays were carried out at least in triplicate Gallic Acid Water 0.55 ± 0.02
measurements. The results are expressed as mean values (µg/mg) MeOH 0.29 ± 0.02
and standard error of mean (SEM). Antioxidant,
p-coumaric acid Water 3.73 ± 0.01
antibacterial and cytotoxicity activities were analyzed
(µg/mg) MeOH 1.76 ± 0.01
using Student t-test and values with P < 0.05 were
considered as statistically significant. IC 50 and EC50 values
DPPH radical scavenging activities were measured with
were calculated with non-lineer regression analysis. For
different concentrations of C. cornucopioides up to 10
all statistical calculations Statistical Package for Social
mg/ml of extracts and scavenging activities enhanced with
Sciences (SPSS®, version 21.0) were utilized.
elevated concentrations (Fig. 1). The best radical
3. Results scavenging was obtained with the methanolic extracts of
C. cornucopioides in 10 mg/ml concentration, as over than
Health and nutrition problems are getting increase due to
75% DPPH reduction takes place. Aqueous extracts of the
world population which is irregularly growing. Nowadays,
same mushrooms also possessed 40% inhibition at highest
unconscious consumption of natural resources and
concentration tested. According to IC50 values, methanolic
economic difficulties obligates the use of natural resources
extracts of C. cornucopioides (IC50: 5.26±0.67 mg/ml) are
and this increases the importance of macrofungi in diet. In
more efficient than its aqueous extracts (IC50: 12.01±1.72
addition to the nutritional properties, their biologically
mg/ml).
62
Kol et al.- Cell growth …
Figure 3: Cytotoxicity of aqueous and methanolic extracts from
Figure 1: DPPH radical scavenging activities of aqueous and C. cornucopioides over HepG2 cells after 48 hours exposure
methanolic extracts of C. cornucopioides. time.
Reducing power of a pharmaceutical generally strongly In antibacterial studies, it was revealed that extracts of C.
correlates well with the antioxidant capacity. Therefore, cornucopioides have high antimicrobial potential. As it
EC50 values were determined to describe the extract can be seen clearly in Table 2, C. cornucopioides exerted
concentration yielding an absorbance value of 0.500. antibacterial activity on all tested microorganisms; B.
According to the results, aqueous extracts showed higher subtilis, E. faecalis, B. licheniformis, A tumefaciens, E.
reducing activity than methanolic extracts in general view coli and S. aureus. With its both water and methanolic
(Fig. 2). Aqueous extract of C. cornucopioides had the extracts, C. cornucopioides inhibited microbial growth
highest reducing activity with the lowest EC50 value with inhibitory zone (IZ) values ranging 6-8 mm length.
(4.54±0.61 mg/ml).
Table 2: Antibacterial effects of C. cornucopioides on six
different tested microorganisms.
Tested C. cornucopioides Gentamicin
Extract
Bacteria IZ: mm IZ: cm
Water 6
E. coli 2.3
MeOH 7
Water 6
S. aureus 2.4
MeOH 6
Water 6
B. subtilis 2.5
MeOH 8
Water 6
B. licheniformis 2.4
MeOH 7
Water 6
A. tumefaciens 2.7
MeOH 7
Water 6
E. faecalis 2.5
MeOH 7
Figure 2: Reducing powers of aqueous and methanolic extracts
from C. cornucopioides. In conclusion, in the near feature mashrooms having
nutritional and economical values will be more used in
Cell growth inhibitory potentials of C. cornucopioides medicine, pharmacy and industrial area due to their high
extracts on HepG2 cells were also inspected in this study, antioxidant, antimicrobial, and cytotoxic features. C.
which was not reported previously. Results indicated that cornucopioides shows noticeable activities with its
extracts have some degree of cytotoxicity over HepG2 antioxidant, antibacterial and cell growth inhibitory
cells and cytotoxic effects of the extracts increased with potential together with high gallic acid and p-coumaric
elevated concentrations (Fig. 3). Methanolic extracts of C. acid content. It might be utilized as a promising source of
cornucopioides had the lowest IC50 values (3.14±1.07 therapeutics since it might provide an appropriate source
mg/ml). Considering the water extracts, IC50 values of of antioxidant, antibacterial and cytotoxic natural
18.41±1.10 mg/ml were obtained showing that methanolic compounds and also could be searched as potent
extracts has higher cell growth inhibitory potential. As a antibacterial drugs against infectious diseases.
result, C. cornucopioides might play a role in cancer and
related researches in cytotoxic effect studies. Acknowledgments
This research was supported by Karamanoğlu Mehmetbey
University (10-YL-15).
63
Anatolian Journal of Botany
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Cite this article: Kol S, Bostancı A, Kocabaş A, Uzun Y, Sadi G (2018). Cell growth inhibitory potential of Craterellus
cornucopioides (L.) Pers. together with antioxidant and antimicrobial properties. Anatolian Journal of
Botany 2(2): 60-64.
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