Hindawi Publishing Corporation
The Scientific World Journal
Volume 2013, Article ID 870468, 6 pages
http://dx.doi.org/10.1155/2013/870468
Research Article
Heteropterys cotinifolia: A Neuropharmacological and
Phytochemical Approach with Possible Taxonomic Implications
Maira Huerta-Reyes,1,2 Alejandro Zamilpa,1 Rafael Álvarez-Chimal,3
José Ángel Luna-Manzanares,4 María Esther León-Velasco,5 Arturo Aguilar-Rojas,1,6
Manuel Jiménez-Estrada,3 and María Guadalupe Campos-Lara2
1
Centro de Investigación Biomédica del Sur, Instituto Mexicano del Seguro Social, Argentina No. 1, Col. Centro,
CP 62790 Xochitepec, MOR, Mexico
2
Unidad de Investigación Médica en Farmacologı́a, Hospital de Especialidades, Centro Médico Nacional Siglo XXI,
Instituto Mexicano del Seguro Social, Avenida Cuauhtémoc No. 330, Col. Doctores, Del. Cuauhtémoc, CP 06720, DF, Mexico
3
Instituto de Quı́mica, Universidad Nacional Autónoma de México, Del. Coyoacán 04510, DF, Mexico
4
Universidad Tominaga Nakamoto, Luis Freg No. 6 y 12, Col. Lomas de Sotelo, CP 53390, Naucalpan de Juárez,
Estado de México, Mexico
5
Herbario Nacional de México (MEXU), Instituto de Biologı́a, Universidad Nacional Autónoma de México,
Apartado Postal 70-367, Del. Coyoacán 04510, DF, Mexico
6
Unidad de Investigación Médica en Medicina Reproductiva, UMAE en Ginecologı́a y Obstetricia No. 4,
Instituto Mexicano del Seguro Social, Avenida Rı́o Magdalena No. 289, Col. Tizapán San Ángel, CP 01090,
Delegación Álvaro Obregón, DF, Mexico
Correspondence should be addressed to Maira Huerta-Reyes; chilanguisima@yahoo.com
Received 30 August 2013; Accepted 30 September 2013
Academic Editors: D. Benke, M. Bermejo, and N. Zohreh
Copyright © 2013 Maira Huerta-Reyes et al. This is an open access article distributed under the Creative Commons Attribution
License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly
cited.
Heteropterys cotinifolia (Malpighiaceae) has been used in traditional Mexican medicine mainly for the treatment of nervous
disorders. However, the specific neuropharmacological activities responsible for this use remain to be defined. The present study
evaluates the antidepressant and anxiolytic effects produced by the methanolic extract of Heteropterys cotinifolia and the influence
of such effects on motor activity in ICR mice. Our results show that the methanolic extract of Heteropterys cotinifolia produces a
dose-dependent antidepressant effect in the forced swimming test in mice at doses from 31 to 310 mg/kg, with no reduction of mice
locomotion. However, no anxiolytic properties were observed. Our findings suggest that the main extract compounds identified as
chlorogenic acid and rutin may be involved in the antidepressant effects. To our knowledge, the present study constitutes the first
report of pharmacological and phytochemical data of Heteropterys cotinifolia. The presence of flavonoids in the methanolic extract
of Heteropterys cotinifolia may also provide further data to characterize taxonomically this species in order to be distinguished from
others species closely related and belonging to the same genus.
1. Introduction
Depression and anxiety are the most frequent mental disorders in all communities all over the world. Around 350
million people are estimated to suffer from depression [1],
while anxiety affects one eight of the population worldwide
[2]. The prevalence of comorbidity of depression and anxiety
is high and by far the most frequent mixture of symptoms
among mental disorders [3]. The current pharmacological
treatments for depression and anxiety are effective only in
a certain percentage of the population and, moreover, most
drugs have many adverse side effects including hypotension,
arrhythmias, insomnia and sexual dysfunction in the case
of antidepressant synthetic nitrogen-bearing compounds
[4], and sedation, muscle relaxation, amnesia, and physical
dependence when benzodiazepines are used [5]. Therefore,
2
there is a need for research and development of more effective
pharmacotherapies with little or no side effects.
Heteropterys cotinifolia A. Juss is a woody vine belonging
to the Malpighiaceae family and has been used in traditional
Mexican medicine mainly for the treatment of nervous
disorders [6]. Since the taxonomic point of view, Heteropterys
cotinifolia presents considerable variability which probably
explains why it has been described many times [7]. However, recent geographical data seem to contribute in the
definition of Heteropterys cotinifolia as an endemic species
of Mexico [8]. To the best of our knowledge, there is no
information about scientific evidence that shows the possible
biological properties of Heteropterys cotinifolia. Thus, the
present study focuses on the neuropharmacological activities
of Heteropterys cotinifolia to understand its traditional medicinal applications. The study was conducted to evaluate the
antidepressant and anxiolytic effects, as well as the influence
on the motor activity produced by the extract of Heteropterys
cotinifolia in ICR mice using a variety of models, such as
the elevated plus maze, the forced swimming test, and the
open field test. The extract of Heteropterys cotinifolia was also
analyzed by HPLC to quantify its main constituents.
2. Materials and Methods
2.1. Plant Collection and Identification. The aerial parts of
Heteropterys cotinifolia A. Juss. were collected from the state
of Morelos, Mexico, in October 2007. The identification of
the plant was authenticated by an expert in the field of
plant taxonomy, who is also one of the authors (M.E. LeónVelasco). A voucher was deposited as reference at the Mexican
Institute of Social Security Medicinal Herbarium (IMSSM)
with the number 15451.
2.2. Preparation of Extracts. The plant material was dried in
darkness and at room temperature and subsequently powered
(3000 g). After dewaxing with n-hexane, the plant material
was successively extracted (3x) overnight with methanol
(100%). The extraction volume used was 7.5 L of solvent per
each kg of plant material. The liquid extract was dried by
removal of the solvent under vacuum. The methanolic extract
of Heteropterys cotinifolia (HcMeOH) (257.7 g) was then used
in the pharmacological experiments.
2.3. Animals. The animal experiments were performed in
strict adherence to the official requirements of the Mexican
Regulations of Experimental Animal Care (NOM-062-ZOO1999). The experimental protocol was approved by the institutional research and ethics committees (Registry number
2010-1701-60). For each neuropharmacological assay, groups
of ten ICR albino mice weighing 20–30 g each were housed
in community cages and maintained under regular laboratory
conditions (22±1∘ C, 12 h light-dark cycle, free access to water
and standard rodent chow). All animals were acclimatized
over 3 weeks prior to initiation of the test. The experiments
were conducted in a special adjacent noise-free room with
controlled illumination. Each animal was used only once in
the experiment.
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2.4. Neuropharmacological Assays. HcMeOH was administrated p.o. at a dose of 310 mg/kg. In those assays exhibiting
activity at the initial dose of 310 mg/kg, the dose-dependent
effects were determined by using 100 and 31 mg/kg doses.
The control substances were diazepam (DZP), imipramine
hydrochloride (IMI), and saline solution (ss) as vehicle.
HcMeOH and control substances were dissolved in ss.
2.4.1. Forced Swimming Test (FST). Among all animal models, the FST remains one of the most used tools for screening
antidepressants [9, 10]. The apparatus utilized to perform the
FST consisted of a clear glass cylinder (30 cm high × 12 cm
diameter) with water filled to a depth of 15 cm (25 ± 3∘ C).
The mice were treated with HcMeOH (31, 100 and 310 mg/kg,
experimental treatment, 𝑛 = 10) and ss 0.1% (vehicle, p.o.,
control group, 𝑛 = 10) 1 h prior to the test. IMI (15 mg/kg,
i.p., positive control, 𝑛 = 10) was administered 30 min before
the test. During the test session, a trained observer recorded
the immobility time.
2.4.2. Elevated Plus Maze (EPM). The EPM test is one of the
most commonly used animal models of anxiety-like behavior
[11]. The maze was constructed of Plexiglas and consisted of a
central platform (5 × 5 cm) with two open (30 × 5 cm) and two
closed arms (30 × 5 cm) and 25 cm high walls. The maze was
elevated 38.5 cm from the floor. The mice were treated 30 min
prior to the test with DZP (1 mg/kg, i.p., positive control,
𝑛 = 10), while ss 0.1% (vehicle, p.o., control group, 𝑛 = 10) and
HcMeOH (310 mg/kg, experimental treatment, 𝑛 = 10) were
administrated 1 h prior to the test. Each animal was placed
at the center of the maze facing one of the open arms. The
number of entries and the time spent in the enclosed and
open arms were recorded during the 5 min test.
2.4.3. Open Field Test (OFT). The open field area was comprised of an opaque-Plexiglas box (60 × 60 × 35 cm) divided
into nine squares of equal size. In this test, the HcMeOH was
administered at doses of 310, 100 and 31 mg/kg (experimental
treatment, 𝑛 = 10), DZP at 1 mg/kg (positive control, 𝑛 =
10) and ss 0.1% (control group, 𝑛 = 10), 60 min before the
beginning of the test [12]. The open field test was used to
evaluate the locomotor activity of mice that had previously
been subjected to the FST and EPM tests.
2.4.4. Statistical Analysis. All data were represented as mean
± standard deviation (S.D.). Data were analyzed by one-way
ANOVA followed by Dunnett’s test for comparisons against
control. Values of 𝑃 ≤ 0.05 (∗) were considered statistically
significant.
2.5. HPLC Analysis. We performed an HPLC analysis of
HcMeOH for detection and quantification of its major
constituents. HPLC analysis was conducted on a Waters
2695 liquid chromatographer equipped with a Waters 2996
photodiode array detector. Separation was carried out by
using a RP C-18 Superspher (Merck) column (240 × 4 mm;
5 𝜇m) with the following solvent ratios for the mobile phase,
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3
150
200
Immobility (s)
150
∗
100
∗
∗
Number of events
∗
100
50
50
0
Veh
0
HcMeOH HcMeOH HcMeOH
(31)
(100)
(310)
Treatment (mg/kg)
Figure 1: Effect of oral administration of Heteropterys cotinifolia
methanolic extract on immobility time of ICR mice exposed to FST.
∗
𝑃 < 0.05 with ANOVA followed by a post hoc Dunnett test (mean
± S.D.). Veh, vehicle; IMI, imipramine hydrochloride; HcMeOH,
methanolic extract of Heteropterys cotinifolia.
where solvent A is 0.1% acetic acid and solvent B is acetonitrile: A : B = 100 : 0 (0–3 min); 90 : 10 (4-5 min); 80 : 20
(6–9 min); 0 : 100 (10–12 min); and 100 : 0 (13–15 min). The
sample injection volume was 10 𝜇L with a 1.0 mL/min flow
rate. The peak analysis and assignment were performed using
commercial standard compounds, which were identified
in accordance with their UV spectra and retention time
(𝑡𝑅 ) in the HPLC chromatogram. The detection wavelength
was scanned at 190–400 nm. Quantification of the main
compounds was achieved by calibrating curves that were
separately constructed with pure standards.
DZP
HcMeOH HcMeOH HcMeOH
(31)
(100)
(310)
Treatment (mg/kg)
Crossings
Rearings
Figure 2: Effect of oral administration of Heteropterys cotinifolia
methanolic extract on the number of total crossings and rearings
of ICR mice exposed to OFT. ∗ 𝑃 < 0.05 with ANOVA followed by
a post hoc Dunnett test (mean ± S.D.). Veh, vehicle; DZP, diazepam;
HcMeOH, methanolic extract of Heteropterys cotinifolia.
(AU)
IMI
3
2.5
2
1.5
1
0.5
0
3
12
0
1
2
3
4
5
6
7 8
(min)
45
6
9 10 11 12 13 14 15
(a) HcMeOH
(AU)
Veh
2
0
3. Results and Discussion
1
2
3
4
5
6
7 8
(min)
9 10 11 12 13 14 15
(b) Chlorogenic acid
3
(AU)
The present study investigated for the first time the CNS
effects of the methanolic extract of the aerial parts of
Heteropterys cotinifolia (HcMeOH) in mice. The FST is the
most widely used and recognized pharmacological model,
for assessing antidepressant activities. The development of
immobility when mice were placed inside an inescapable
cylinder filled with water reflects the cessation of persistent
escape-directed behavior [9, 13]. Our results showed that
HcMeOH induced a significant antidepressant effect in a
dose-dependent manner in the FST since it significantly
diminished the immobility time compared with the control
group (Veh) (𝑃 < 0.05) at doses from 31 to 310 mg/kg
(Figure 1). It is noteworthy that in the FST test, false positive
results can be obtained for agents that stimulate locomotor
activity [14]. Therefore, the observation that HcMeOH did
not increase the number of crossings and rearings in the OFT
(Figure 2) confirms the assumption that the antidepressant
effect of the extract in the FST is specific [15].
The HPCL analysis showed two main compounds in
the active extract HcMeOH (Figure 3(a)). The first (peak 3)
was identified and quantified as chlorogenic acid (36.4 mg/g)
(Figure 3(b)) while the second main compound (peak 6) was
recognized as the flavonoid rutin (17.9 mg/g) (Figure 3(c)),
0
2
1
0
0
1
2
3
4
5
6
7 8
(min)
9 10 11 12 13 14 15
(c) Rutin
Figure 3: HPLC chromatogram comparison between HcMeOH and
commercial standards. (a) Crude extract of HcMeOH; (b) chlorogenic acid commercial standard; (c) rutin commercial standard.
since the UV spectra and 𝑡𝑅 values were in agreement with the
commercial pure standards. Quantification was established
with calibration curves (linear regression where 𝑟2 > 0.9932).
The identity of the rest of the compounds (peaks 1, 2, 4,
and 5) present in HcMeOH (Figure 3(a)) remains unknown
as its 𝑡𝑅 and UV absorption values did not match with
any of the commercial standards used additionally. Likewise,
the scarce amounts observed, particularly for peaks 1 and
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Time/entries into open arms (%)
4
∗
100
Table 1: Retention times and absorbance values of peaks detected in
HcMeOH.
∗
80
Peak
60
40
20
0
Veh
DZP
HcMeOH (310)
Treatment (mg/kg)
EOA
TOA
Figure 4: Effect of oral administration of Heteropterys cotinifolia
methanolic extraction the percentage of time spent in open arms
(TOA) and entries into open arms (EOA) by mice exposed to EPM.
∗
𝑃 < 0.05 in ANOVA followed by a post hoc Dunnett test (mean ±
S.D.). Veh, vehicle; DZP, diazepam; HcMeOH, methanolic extract of
Heteropterys cotinifolia.
2, made difficult the identification (Table 1). Although we
cannot rule out the participation of other components in
the antidepressant effect of HcMeOH, our results suggest
a significant role for chlorogenic acid and rutin in the
antidepressant properties of HcMeOH due to its presence as
major constituents. Rutin has been shown to play an essential
role in the antidepressant activity of plant extracts widely
recognized as antidepressants, such as Hypericum perforatum, participating in the enhancement of the bioavailability
of other compounds present in the extract to confer the entire
biological activity in the FST [16]. The involvement of the
serotonergic, noradrenergic, and/or dopaminergic systems
in the synaptic cleft has been reported as the mechanism
responsible of the antidepressant actions of rutin [17]. Similarly, the potent antidepressant effect of chlorogenic acid,
the other major compound detected in HcMeOH, has been
exhibited in FST when orally administered [18]. Therefore, it
can be suggested that the antidepressant effect observed in
the present work may largely be due to the chlorogenic acid
and/or rutin content detected in HcMeOH. Our findings are
in accordance with reports on chlorogenic acid and rutin as
the main components of extracts widely recognized as antidepressants such as Hypericum extracts [19–21]. Moreover, in
the case of Hypericum origanifolium, these two components
are also the main compounds found in the crude extract, even
over hypericin and hyperforin, the compounds described by
far as the responsible for the antidepressant properties of
Hypericum perforatum (St. John’s wort) [22].
On the other hand, the findings of the present study
contribute to place the species belonging to the Heteropterys
genus as a potential source of extracts able to relieve
the affections of CNS. For example, the Brazilian species,
Heteropterys aphrodisiaca O. Mach. improved learning and
memory deficits in aged rats [23], and has also showed
a strong reduction in the oxidative stress in young and
1
2
3
4
5
6
Chlorogenic acid
(commercial pure standard)
Rutin
(commercial pure standard)
∗
Retention time
(min)∗
𝜆 (nm)
7.29
7.65
7.96
8.65
9.03
9.41
(213, 220, 273)
(218, 240, 325)
(218, 242, 325)
(218, 242, 325)
(220, 243, 329)
(210, 255, 355)
7.88
(218, 242, 325)
9.14
(210, 255, 355)
Retention time window <5% was employed to identify each compound.
old rat brains [24], whereas the species Heteropterys glabra
Hook & Arn. induced a reduction in motor activity and
alterations in EEG parameters [25]. Recently, our work group
described the antidepressant, anxiolytic, and anticonvulsant
activities in mice without toxicity effects of the methanolic
extract of Heteropterys brachiata (L.) DC. [26]. However,
the hydroalcoholic extracts of roots, branches, and leaves
of Heteropterys tomentosa A. Juss showed no effects when
evaluated in animal models of stress and learning/memory
[27], and no influence on the apoptosis of the hippocampal
cells of aged rats [28]. Interestingly, even when Heteropterys
species could be considered relevant from the neuropharmacological perspective, the studies about the chemical
composition of the active CNS extracts are scarce. Partial
phytochemical screenings for detecting chemical groups such
as glycosides, polyphenols, tannins and alkaloids saponins,
and anthracene derivatives in Heteropterys aphrodisiaca have
been reported [23]. The hydroxycinnamic acids, chlorogenic
acid, and chlorogenic acid methyl ester as responsible for the
neuropharmacological properties in Heteropterys brachiata
have been described [26]. However, although chlorogenic
acid is the major compound identified in HcMeOH in the
present work, it is likely that the differences observed in
neuroactivity compared with those elicited by the methanolic
extract of Heteropterys brachiata may be due to the presence
of flavonoids that appear to be the second main compound
group in HcMeOH; that is, the synergistic effects are crucial
for the observation of neuropharmacological activity as has
been reported widely elsewhere [16].
Regarding the third test, our results show that HcMeOH
does not elicit anxiolytic effects at the dose tested in EPM
since no changes were detected in the percentage of Time
that mice spent in Open Arms (TOA) and the percentage of
Entries into the Open Arms (EOA) with respect to the control
group (Veh) (𝑃 > 0.05) (Figure 4).
In addition to the neuropharmacological relevance of
the Heteropterys extracts, the chemical profiles have been
useful in the definition of the species belonging to this
genus from the taxonomic point of view [29]. Thus, the
chemical composition consisting of chlorogenic acid and
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rutin as main compounds of HcMeOH may provide additional data to characterize the species to be distinguished
from the closely related Heteropterys brachiata in which,
in contrast, flavonoids were not detected in the methanolic
extract. Consequently, our results may also contribute to
provide elements for a quick and simple identification of
Heteropterys cotinifolia species even in the field collecting
zone, where pink flowers and fruits, frequently cause confusion with Heteropterys brachiata. Then, at collecting time
and in combination with the morphological characters, a
positive detection of flavonoids by simple TLC could be
useful to distinguish Heteropterys cotinifolia from other close
species. This discernment technique by TLC has been used
successfully in other plant species with relevant biological
properties [30].
4. Conclusions
The methanolic extract of Heteropterys cotinifolia possesses
antidepressant properties in which chlorogenic acid and rutin
could be involved. To the best of our knowledge, this is
the first report of the biological activities and chemical data
of this species. Our findings support the pharmacological
justification for the traditional use of Heteropterys cotinifolia
in the treatment of nervous disorders and encourage further
studies for the development of this extract as a therapeutic
agent.
Conflict of Interests
The authors declare that there is no conflict of interests
regarding the publication of this paper.
Acknowledgment
This work was supported by Grant FIS/IMSS/PROT/G10/877
from the FIS, Instituto Mexicano del Seguro Social, Mexico
(to Maira Huerta-Reyes).
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