Industrial Crops & Products 125 (2018) 5–8

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Industrial Crops & Products

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Chemical composition and biological activities of the essential oils of two T

endemic Nepeta species
⁎
Cengiz Sarikurkcua, Olcay Ceylanb, , Said Targanc, Sanja Ćavar Zeljkovićd,e
a
Department of Analytical Chemistry, Faculty of Pharmacy, Suleyman Demirel University, 32260 Isparta, Turkey
b
Department of Biology, Faculty of Science, Mugla Sitki Kocman University, 48060 Mugla, Turkey
c
Department of Chemistry, Faculty of Science and Literature, Celal Bayar University, 45040 Manisa, Turkey
d
Centre of Region Haná for Biotechnological and Agricultural Research, Central Laboratories and Research Support, Faculty of Science, Palacky University, Šlechtitelů 27,
78371 Olomouc, Czech Republic
e
Centre of the Region Haná for Biotechnological and Agricultural Research, Department of Genetic Resources for Vegetables, Medicinal and Special Plants, Crop Research
Institute, Šlechtitelů 29, 78371 Olomouc, Czech Republic

A R T I C LE I N FO A B S T R A C T

Keywords: The chemical composition, antioxidant activity and several enzyme inhibitions of the essential oils of two en-
Nepeta nuda subsp. glandulifera demic Nepeta species, N. nuda subsp. glandulifera and N. cadmea were investigated for the first time. The major
Nepeta cadmea compounds of N. nuda subsp. glandulifera essential oil were geijerene (61.02%) and neointermedeol (6.07%). On
Essential oil contrary, essential oil of N. cadmea contained 70.94% of 4aβ,7α,7aβ-nepetalactone. The oil of N. nuda subsp.
Antioxidant activity
glandulifera revealed better activity than the oil of N. cadmea against both reducing metal ions and radicals.
Enzyme inhibition activity
Moreover, both oils have relatively weak but still noticeable activity against acetylcholinesterase and butyr-
ylcholinesterase; weak activity against α-glucosidase, but quite high activity against α-amylase. On the other
hand, both essential oils showed significant activity against tyrosinase. Presented results suggest that these two
endemic species have strong potential to be used in food and pharmacological industries, and therefore they
should to be investigated further.

1. Introduction
It is widely known that phytocompounds possess wide range on
pharmacological activities, and therefore, in order to detect and isolate
bioactive components, medicinal plants are in the focus of scientific
communities worldwide. Since artificial antioxidants and preservatives
are found to be toxic (Kahl and Kappus, 1993), in the last few decades,
there is enormous interest in a search for novel natural antioxidants of
plant origin, and in study of their mechanism of action against reactive
oxygen and nitrogen species (Kasote et al., 2015). Those reactive spe-
cies, mainly radicals are responsible for DNA and protein modification
and damage, inactivation of enzymes, as well as lipid peroxidation, and
all those processes lead to several disorders and induce high risk in
human health. Moreover, the most common human disorders of the
modern time are related to the different enzymatic activities. For in-
stance, increased activity of cholinesterase leads to Alzheimer’s disease;
high tyrosinase activity is related to biosynthesis of melanin that is a
key compound in skin pigmentation processes, etc. Similarly, scientists
are searching for natural compounds, with fewer side effects than
artificial ones, to decrease activity of these enzymes. Since plants are
factories of many different compounds that help in health-promotion,
there is considerable interest to search for different enzyme inhibitors
of plant origin (Rauf and Jehan, 2017).
Genus Nepeta (Lamiaceae) consist from more than 250 species na-
tive to Asia, Europe and North Africa (Evans, 1996). The Southwestern
Asia, mainly Turkey and Iran, is the central area for this genus, where
its diversity and richness it the most noticeable. Among 33 species of
Nepeta present in Turkey, 17 of them are being endemic (Davis, 1982).
Number of Nepeta species have different properties such as antitussive,
antiseptic, diaphoretic, sedative, emmenagogue, diuretic etc., and they
are used in folk medicine (Formisano et al., 2011). Several members of
this genus were also investigated for their chemical composition, as
well as biological activities (Alim et al., 2009; Baser et al., 2000;
Formisano et al., 2011). Still, there are many Nepeta species that have
not been studied yet, and among them are endemic N. nuda subsp.
glandulifera and N. cadmea.
In the light of the fact that more phytochemical and biological
studies should be carried out on this genus, this paper presents the

⁎
Corresponding author.
E-mail address: oceylan@mu.edu.tr (O. Ceylan).

https://doi.org/10.1016/j.indcrop.2018.09.001
Received 11 May 2018; Received in revised form 30 August 2018; Accepted 1 September 2018
0926-6690/ © 2018 Elsevier B.V. All rights reserved.
C. Sarikurkcu et al. Industrial Crops & Products 125 (2018) 5–8

investigation of chemical composition and biological activities, both Table 1

antioxidant and enzymatic inhibition, of essential oils of two endemic Chemical composition of the essential oils from Nepeta species.
Nepeta species, N. nuda subsp. glandulifera and N. cadmea. RRIExpx RRILity Compound A (%)z B (%)z

1128 1132a Sabinene – 0.73

1212 1213a 1,8-Cineole 1.55 1.18
2. Material and methods
1339 1338b Geijerene 61.02 –
1504 1503b Pregeijerene B 0.93 –
2.1. Plant material 1550 1553a Linalool 0.27 5.87
1593 1594b Pregeijerene 0.88 –
Aerial parts of N. nuda subsp. glandulifera and N. cadmea were col- 1603 1600b β-Elemene 0.38 –
1618 1612a β-Caryophyllene 1.94 6.29
lected during flowering stage from the localities given below. Dr. Olcay
1624 1648c Myrtenal 0.32 –
Ceylan authenticated Nepeta species. 1691 1684a α-Humulene 0.42 –
Nepeta cadmea: Isparta-Barla-Senirkent highway, Isparta-Turkey, 1732 1726a Germacrene D 0.82 –
952 m.s.m., 38° 06′ 53.5″N 30° 50′ 17.9″E, 10 July 2014, (Voucher No. 1780 1776a γ-Cadinene – 0.56
1856 1849a cis-Calamenene – 2.11
MUH5200).
1937 1934d Tetradecanal 0.77 –
Nepeta nuda subsp. glandulifera: Kuyucak region, Derebucak town, 1967 2001a Isocaryophyllene oxide 2.06 –
Beysehir-Konya-Turkey, 37° 20′ 36.9″N 31° 32′ 15.7″E, 10 June 2014, 1988 1988d (E)-2-Tridecenal 0.34 –
1800 m.s.m. (Voucher No. MUH5201). 2017 2016c 4aα,7α,7aα-Nepetalactone – 3.51
2018 2008a Caryophyllene oxide 1.91 3.90
2076 2104a Viridiflorol 0.36 –
2085 2088c 4aβ,7α,7aβ-Nepetalactone – 70.94
2.2. Isolation and analysis of the essential oils 2097 2096b Elemol 1.29 –
2100 2100d n-Heneicosane 0.37 –
Aerial parts of the plant samples were air-dried in shade at room 2145 2144a Spathulenol 0.98 –
temperature for several weeks and ground using a laboratory mill be- 2167 2165e Neointermedeol 6.07 –
2213 2212b trans-Isoosmorhizol 1.62 –
fore isolation of essential oils. By using 100 g of sample for each species, 2220 2219f δ-Cadinol 0.49 –
essential oils were obtained with hydro-distillation (British-type 2256 2255f α-Cadinol – 0.20
Clevenger apparatus, Ildam Ltd., Ankara-Turkey) and stored at 4 °C 2300 2300d n-Tricosane 12.64 –
until analysis. Total identified 97.43 95.29
The oils were analyzed by GC-FID and GC–MS methods using the x
RRIExp; Relative retention indices calculated against n-alkanes on HP-in-
analytical conditions reported by Sarikurkcu et al. (2015). Briefly,
nowax column.
GC–MS analysis was carried out by an Agilent 5975 GC-MSD system y
RRILit; Relative retention indices on given in the literature for the com-
coupled to an Agilent 7890A GC (Agilent Technologies Inc., Santa pound in similar columns (HP-innowax) and analysis conditions from the lit-
Clara, CA), using a HP-Innowax FSC column (60 m × 0.25 mm, i.d., erature [aSource: Tabanca et al. (2006); bSource: Noorizadeh et al. (2011);
0.25 μm), and He carrier gas (1.2 mL/min). GC oven temperature was c
Source: Ali et al. (2016); dSource: Polatoğlu et al. (2017); eSource: Ghosh et al.
kept at 60 °C for 10 min and programmed to 220 °C at a rate of 4 °C/ (2014); fSource: Tabanca et al. (2001)].
z
min, and kept constant at 220 °C for 10 min and then programmed to % calculated from FID data (A and B; N. nuda subsp. glandulifera and N.
240 °C at a rate of 1 °C/min. GC-FID analysis was carried out by si- cadmea, respectively).
multaneous autoinjection using Agilent 7693A series auto sampler.
Essential oil constituents were identified by their relative retention 2.4. Statistical evaluation
indices (RRIExp) determined by co-injection of a homologous series of n-
alkanes (C5–C30), as well as by comparison of their mass spectra with The results were analyzed statistically with Student’s t-test
computer spectral databases and their relative retention indices (RRILit) (α = 0.01) by using the SPSS v22.0 software. All the assays were car-
with those reported in the literature for HP-innowax (Ali et al., 2016; ried out in triplicate and the results were presented as mean ±
Ghosh et al., 2014; Noorizadeh et al., 2011; Polatoğlu et al., 2017; standard deviation (SD).
Tabanca et al., 2006, 2001) column.
3. Results and discussion

2.3. Biological activity 3.1. Composition of essential oil

The essential oils from two endemic Nepeta species were dissolved
in ethanol. For antioxidant activities, the essential oils were in-
vestigated by using assays that are based on chelating of metal ion,
reduction of cations (phosphomolybdenum method, CUPRAC, and
FRAP tests), and assays based on reduction of free radicals (DPPH and
ABTS). The assays were performed by using previously reported ex-
perimental conditions (Zengin et al., 2015).
For enzyme inhibitory activities, the essential oils were analyzed
toward acetylcholinesterase (AChE), butyrylcholinesterase (BChE), α-
amylase, α-glucosidase, and tyrosinase by using previously reported
experimental conditions (Sarikurkcu et al., 2015).
Results of both type biological activities were presented as IC50
values, which correspond to the concentration of the oil (mg/mL) re-
quired to inhibit 50% of the initial concentration of oxidant/enzyme.
Trolox and EDTA were used as positive controls for antioxidant assays,
and galanthamine, kojic acid, and acarbose were used for enzymatic
assays.
Essential oils yielded 0.56% (v/w) and 0.99% (v/w) for Nepeta nuda
subsp. glandulifera and N. cadmea, respectively. The chemical compo-
sition of isolated oils from these two Nepeta species was summarized in
Table 1. Twenty-eight compounds were identified in the both oils,
comprising 97.43% and 95.29% for N. nuda subsp. glandulifera and N.
cadmea, respectively.
In general, these two Nepeta oils significantly differ in their chemical
composition, but, the major constituents of the both oils are in very
high concentrations, and they both can be classified as quite homo-
genous, especially the oil of N. cadmea. The major compounds of N.
nuda subsp. glandulifera essential oil were terpenoids geijerene
(61.02%) and neointermedeol (6.07%), following with quite high
amount of long-chain alkane tricosane (12.64%). On contrary, essential
oil of N. cadmea consisted from 70.94% of irridoid monoterpene
4aβ,7α,7aβ-nepetalactone. Other abundant compounds were β-car-
yophyllene (6.29%) and linalool (5.87%).
Literature survey showed just few papers on essential oil

6
C. Sarikurkcu et al.
composition of these two endemic Nepeta species. Generally, this genus
shows chemical polymorphism, and the composition of the oil depends
on variety, growing site, climatic conditions, etc. (Formisano et al.,
2011).
Baser et al. (2000, 1998) analyzed the oil from N. cadmea collected
at several different locations and their results also show that the
4aβ,7α,7aβ-nepetalactone was the major compound, but with sig-
nificant differences in the content of this oxygenated sesquiterpene.
Moreover, Celik et al. (2008) reported more than 80% of this irridoid in
the oil of N. cadmea collected at Honaz Mt. According to the previously
published results and these presented here, it might be concluded that
the essential oil of N. cadmea shows no significant changes in its com-
position under different environmental conditions. On contrary, N.
nuda subsp. glandulifera seems to be more sensitive to the environment.
Baser et al. (2000) also analysed this species collected at two different
localities, and caryophyllene oxide (24.0–30.7%) was found to be the
major compound in both of oils.
Furthermore, the compositions of the essential oils isolated from
different N. nuda subspecies were also reported. Generally, the oils of
this species are classified as 1,8-cineole/linalool chemotype, germa-
crene D chemotype, and 4aβ,7α,7aβ-nepetalactone (Formisano et al.,
2011). The most abundant constituents of oil of Nepeta nuda from
eastern part of Erzurum city of Turkey were 4aα,7β,7aα-nepetalactone
(18.10%), germacrene (15.68%) and elemol (14.38%) (Bozari et al.,
2013). For instance, the oils of N. nuda subsp. albiflora from Turkey
were rich in β-caryophyllene (23.97%), isopulegone (10.11%) (Alim
et al., 2009), and in 4aβ,7α,7aβ-nepetalactone (74.27%) (Bozok et al.,
2017), while the major compounds of the oil of same species from Le-
banon were β-bisabolene (7.8–11.8%) and pulegone (7.2–10.8%)
(Mancini et al., 2009).
3.2. Antioxidant activity
As it was already described in Experimental section, the antioxidant
activity of essential oils of two endemic Nepeta species was tested using
several different assays, based on different reaction mechanisms, i.e.
metal chelating, reduction of ions, and reduction of stable radicals. The
results of these assays are summarized in Table 2. Although these assays
are based on different reaction mechanisms, they can be compared
because results are presented IC50 values, i.e. the concentration of the
oil required to reduce 50% of the initial concentration of oxidant.
Radical scavenging activity was assayed employing two radical
species, stable 2,2-diphenyl-1-picrylhydrazyl radical (DPPH) and 2,2′-
azino-bis(3-ethylbenzothiazoline-6-sulphonic acid) radical cation
(ABTS). Both assays are based on spectrophotometric measurement of
reduction of radicals in certain time, i.e. 7 min for ABTS and 30 min for
DPPH. In general, IC50 values for DPPH assay are higher than for ABTS
assay, but obtained results from both assays strongly correlate (Floegel
et al., 2011). Steric factors have more influence in reduction of DPPH
radical than ABTS radical cation (Cavar et al., 2009). Many large an-
tioxidant compounds that react quickly with radicals may react slowly
or may even be inert in this assay. This might be a reason why the used
concentrations of the oil of N. cadmea were not able to reduce DPPH
radical, i.e. 3D geometry of the major compound of the N. cadmea oil
Table 2
Antioxidant activities (IC50; mg/mL) of the essential oils from Nepeta species by different assays.x
Assays N. cadmea
DPPH radical scavenging na
ABTS radical cation scavenging 23.10 ± 0.03a
Phosphomolybdenum 0.73 ± 0.01a
FRAP reducing 2.65 ± 0.02a
CUPRAC reducing 5.53 ± 0.06a
Ferrous ion chelating 2.93 ± 0.01a
x
Different superscripts in the same row indicate significant differences (p < 0.01). EDTA, ethylenediaminetetraacetic acid (disodium salt). na, not active.
Industrial Crops & Products 125 (2018) 5–8
doesn’t fit to the steric requirements for reduction of DPPH radical.
Adiguzel et al. (2009) also reported inactivity of the oil of N. cataria
against DPPH radical. This oil also contained very similar concentration
of 4aα,7α,7aß-nepetalactone (75.7%). On contrary, the oil of N. nuda
ssp. nuda, with high concentration of this nepetalactone, showed rela-
tively potent activity against DPPH radical (Gkinis et al., 2010). This
discrepancy could be explained by the relatively high presence of 1,8-
cineole in this oil. This oxygenated monoterpene is declared as appro-
priate scavenger of DPPH radical (Moghadam, 2015). The oil of N. nuda
subsp. gladulifera showed weak activity against this radical, about 500-
fold weaker than Trolox. However, both oils were successful to reduce
ABTS radical cation, with IC50 values approximately ten-fold higher for
N. nuda subsp. gladndulifera, and 100-fold higher for N. cadmea, than
Trolox that was used as positive control.
Interestingly, both examined oils revealed much better activity in
reducing metal cations, molybdenum, iron, and coper. These spectro-
photometric assays are based on reduction of Mo(VII) to Mo (V), Fe(III)
to Fe (II), and Cu (II) to Cu (I), by a potent natural reducing agent(s).
Obtained IC50 values in mg/mL were in the range with those for Trolox,
which was used as positive control (Table 2). Again, the oil of N. nuda
subsp. glandulifera revealed better activity than the oil of N. cadmea
against both reducing cations and radicals. On contrary, the oil of N.
nuda failed in ferrous chelating activity. Nepeta cadmea revealed che-
lating ability, but still week in comparison with EDTA, which might be
explained by the high presence of 4aβ,7α,7aβ-nepetalactone which
conjugated lactone moiety has potential to chelate transition metals
(Semić and Ćavar Zeljković, 2015).
To the best of our knowledge, there are only few published papers
that deal with antioxidant activity of the essential oil of N. nuda (Alim
et al., 2009; Gkinis et al., 2010; Kaska et al., 2018). The oil of N. nuda
subsp. albiflora was not able to scavenge stable DPPH radical (Alim
et al., 2009). The oil of this species consisted mainly from non-oxyge-
nated terpenoids which are known to be weak antioxidants. On con-
trary, the oil of N. nuda subsp. nuda rich in 4aβ,7α,7aβ-nepetalactone
and 1,8-cineole showed activity against DPPH radical, comparable with
tert-butylated hydroytoluene (Gkinis et al., 2010). Kaska et al. (2018)
tested antioxidant activity of polar extracts of N. cadmea, and their
results refer much better ability of their extracts to reduce stable cations
and radicals then the essential oil of this species. This fact is supported
by relatively high presence of phenolic compounds found in tested
extracts, which is not the case with the oil of N. cadmea.
3.3. Enzyme inhibitory activity
The essential oils from N. cadmea and N. nuda subsp. glandulifera
were also tested on inhibitory activity on several enzymes that are
known to cause different remedies in humans, i.e. cholinesterase in
connected to Alzehaimer’s disease, tyrosinase to different dermatolo-
gical disorders, and α-amylase and α-glucosidase with Diabetes mellitus.
Results are summarized in Table 3. Both tested oils showed quite si-
milar activities against all five enzymes, with the IC50 values in mg/mL
with same order of magnitude.
According to the presented results, it might be concluded that the
essential oils of these endemic Nepeta species have relatively weak but
N. nuda subsp. glandulifera Trolox EDTA
153.24 ± 1.84a 0.31 ± 0.01b –
2.72 ± 0.01b 0.18 ± 0.01c –
0.18 ± 0.01c 0.59 ± 0.01b –
2.04 ± 0.01b 0.11 ± 0.01c –
2.86 ± 0.01b 0.04 ± 0.001c –
na – 0.04 ± 0.001b
7
C. Sarikurkcu et al. Industrial Crops & Products 125 (2018) 5–8

Table 3
Enzyme inhibitory activities (IC50; mg/mL) of the essential oils from Nepeta species.x
Assays N. cadmea N. nuda subsp. glandulifera Galanthaminey Kojic acid Acarbose

Acetylcholinesterase 1.05 ± 0.01b

1.18 ± 0.01a
1.51 ± 0.01 c
– –
Butyrylcholinesterase 1.02 ± 0.01b 1.35 ± 0.03a 1.77 ± 0.02c – –
Tyrosinase 2.83 ± 0.06a 2.51 ± 0.02b – 0.14 ± 0.01c –
α-Glucosidase 5.93 ± 0.18a 2.43 ± 0.04b – – 0.99 ± 0.01c
α-Amylase 1.35 ± 0.02a 1.15 ± 0.05a – – 1.33 ± 0.01a

x
Different superscripts in the same row indicate significant differences (p < 0.01).
y
As μg/mL.

still noticeable activity against both acetylcholinesterase and butyr-
ylcholinesterase, a thousand-fold weaker than galanthamine which was
used as positive control. Also, antityrosinase activity of the both oils
was noticeable, and approximately 20-fold weaker than kojic acid
(Table 3). On the other hand, both Nepeta essential oils showed sig-
nificant activity against both α-amylase and α-glucosidase, with IC50
values very similar to acarbose.
Although Nepeta species were already tested on wide variety of
biological activities, to the best of our knowledge, this is a very first
report on enzyme inhibitory activity of the oil of any of the member of
Nepeta genus.
4. Conclusions
In conclusion, the essential oils from two endemic Nepeta species
successfully scavenged and neutralized few different reactive oxidant
species, and inhibited various enzymes that are connected with human
diseases of modern times. Presented results suggest that these two en-
demic species have strong potential to be used in food and pharmaco-
logical industries, and therefore they need to be furtherly investigated.
Conflict of interest
The authors have no conflicts of interest.
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