TECNOCIENCIA CHIHUAHUA, Vol. XVI (2) e 903 ( 2022) https://vocero.uach.mx/index.php/tecnociencia

ISSN-e: 2683-3360

Artículo Científico

Capacidad antioxidante y potencial toxicológico de la

planta Ibervillea sonorae

Antioxidant capacity and toxicologic potential of Ibervillea

sonorae plant

*Correspondencia: angelesujed@hotmail.es (María de los Ángeles Sáenz Esqueda)

DOI: https://doi.org/10.54167/tecnociencia.v16i2.903

Recibido: 05 de enero de 2022; Aceptado: 07 de abril de 2022

Publicado por la Universidad Autónoma de Chihuahua, a través de la Dirección de Investigación y Posgrado.

Abstract

The main objective of this study was to evaluate the antioxidant capacity and toxicological potential

of the infusions prepared from Ibervillea sonorae. Thus, infusions were prepared using I. sonorae roots,

either skin or pulp. Total phenolic compounds and antioxidant capacity of the infusions were

evaluated through the Folin-Ciocalteu method and ABTS and DPPH tests, respectively, whereas the

Artemia salina, the MTT using VERO and MCF-7 cell lines, and the Ames assays were used to evaluate

the toxicological effect. The total phenolic compounds as well as antioxidant capacity by DPPH and

ABTS assays of the I. sonorae infusions varied from 15 to 24 meq GA/g, 14 to 16 %, and 1,147 to

1,191 meq Trolox/g, respectively. Further, the results showed that I. sonorae skin extracts were more

lethal (60-80 %) than pulp (<50 %). Interestingly, I. sonorae pulp showed higher toxicity on VERO cell

line (IC50 = 222 µg / mL) than infusions prepared from skin (IC50 = 379 µg/mL). I. sonorae

concentrations higher than 500 g/mL exhibited high potential mutagenic. The intake of infusions

prepared from the I. sonorae plant could promote health injuries.

Marco A. Peña-Chávez1, Jorge Antonio Zacatecas-Ibáñez4, Jorge Sáenz-Mata2, María José

Rivas-Arreola3, Mónica Azucena Ramírez-Cabrera4, Rafael Minjares-Fuentes1 y María de los

Ángeles Sáenz-Esqueda1*

1 Facultad de Ciencias Químicas, Universidad Juárez del Estado de Durango, Av. Artículo 123 S/N, Fracc.

Filadelfia, C.P. 35010, Gómez Palacio, Durango, México

2 Facultad de Ciencias Biológicas, Universidad Juárez del Estado de Durango, Av. Universidad S/N, Fracc.

Filadelfia, C.P. 35010, Gómez Palacio, Durango, México

3 Facultad de Medicina, Instituto Tecnológico de Estudios Superiores de Monterrey, Campus Guadalajara,

Av. General Ramón Corona #2514 Col. Nuevo México. Zapopan, Jalisco, México

4 Laboratorio de Farmacología Molecular y Modelos Biológicos, Facultad de Ciencias Químicas,

Universidad Autónoma de Nuevo León, Av. Universidad s/n Cd. Universitaria, San Nicolas de los Garza,

Nuevo León, México

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TECNOCIENCIA CHIHUAHUA, Vol. XVI (2) e 903 (2022)

Keywords: Ibervillea sonorae, infusions, antioxidant capacity, cytotoxicity, genotoxicity

Resumen

El objetivo de este estudio fue evaluar la capacidad antioxidante y potencial toxicológico de las

infusiones preparadas a partir de Ibervillea sonorae. Para esto, se prepararon infusiones a partir de la

raíz de I. sonorae, usando la cáscara o la pulpa. Los compuestos fenólicos totales y la capacidad

antioxidante fueron determinados mediante el método de Folin-Ciocalteu y las pruebas ABTS y

DPPH, respectivamente, mientras que, los ensayos con Artemia salina, MTT usando células VERO y

MCF-7, y de Ames fueron usados para evaluar el potencial toxicológico. Los compuestos fenólicos

totales y la capacidad antioxidante por DPPH y ABTS de las infusiones de I. sonorae variaron de 15

a 24 meq GA/g, 14 a 16 % y 1147 a 1191 meq Trolox/g, respectivamente. Las infusiones con

cáscara de I. sonorae fueron más letales (60 – 80 %) que con pulpa (<50 %). Por el contrario, las

infusiones con pulpa exhibieron mayor toxicidad sobre células VERO (IC50 = 222 µg/mL) que con

cáscara (IC50 = 379 µg/mL). Concentraciones >500 g/mL de I. sonorae mostraron elevado potencial

mutagénico. La ingesta de infusiones preparadas a partir de la planta de I. sonorae podría ocasionar

graves daños a la salud.

Palabras clave: Ibervillea sonorae, infusiones, capacidad antioxidant, citotoxicidad, genotoxicidad

1. Introduction

Plants have widely been used in traditional medicine to treat different diseases (Sharif et al., 2017).

In fact, most of the population has used herbal products as a primary source of healthcare (Ekor,

2014). Nevertheless, around 15 % of clinical studies using herbal medicine as an alternative treatment

have reported information about its safety or side effects (Boullata and Nace, 2000). The safety and

efficacy of herbal medicine has become a public health concern, mainly due to the increased use of

herbal medicinal products, either as primary or complementary treatment (Neergheen-Bhujun,

2013).

México, considered as one of the most biodiverse countries in the world, possesses more than 23,400

plants but only a small group of plants considered medicinal have been studied for their

pharmacological, phytochemical and toxicological effects, as well as for their pharmacokinetics (Bye

et al., 1995; Alonso-Castro et al., 2017). In the traditional Mexican medicine, the root of Ibervillea

sonorae (S. Watson) Greene (syn. Maximowiczia sonorae S. Watson.; Cucurbitaceae), commonly known

as “Wereque” (Déciga-Campos et al., 2007), has been widely used as a topical antibiotic, cathartic,

antirheumatic and antidiabetic (Rivera-Ramírez et al., 2011; Sinagawa-García et al., 2015; Torres-

Moreno et al., 2015). In fact, I. sonorae has become one of the most widely used plants in controlling

diabetes mellitus (Estudillo and García, 1988), a metabolic disorder with the highest incidence and

mortality rate in México (Guariguata et al., 2014). Most of the beneficial effects associated to I. sonorae

plant have been attributed of curcumin on the one hand, and phenolic compounds such as gallic acid

on the other (Zapata-Bustos et al., 2014; Torres-Moreno et al., 2015). However, to the best of our

knowledge, the information about the toxicological effects of I. sonorae is very limited. Thus, the main

aim of this study was to offer a first report of the mutagenic and cytotoxic potential of infusions

prepared from I. sonorae.

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2. Materials and methods

2.1. Plant material

Plants of I. sonorae were collected at the communal land Esperanza (Cd. Obregón, Sonora, Mexico)

(27° 36´ 09.35” N latitude, 109° 54´ 10.7” W longitude). The identification of I. sonorae plants was

confirmed by DNA barcoding. A specimen of I. sonorae (Voucher: JAAA-00001) was deposited in the

JAAA Herbarium (Facultad de Ciencias Biologicas, Universidad Juárez del Estado de Durango).

Infusions of I. sonorae were prepared using 10 g of I. sonorae, either pulp (WP) or skin (WS), suspended

in 100 mL of boiling water for 10 min. The supernatant was separated and lyophilized in a laboratory

scale freeze dryer LABCONCO FreeZone Triad Cascade Benchtop (LABCONCO, Kansas City,

Missouri, USA) operated at 0.01 mBar with condenser and shelf temperatures of −80 °C and −20 °C,

respectively. Lyophilized extracts were stored in anhydrous conditions until analysis.

2.2. Phenolic compounds and antioxidant activity of I. sonorae infusions

Total phenolic compounds were determined according to the Folin−Ciocalteu method previously

described by González-Centeno et al. (2014) in a MultiSkan FC spectrophotometer (Thermo Scientific,

Waltham, MA USA). Antioxidant activity was tested by using 2,2-Azino-bis(3-ethylbenzthiazoline-

6-sulfonic acid) (ABTS) and 2,2'-diphenyl-1-picryl-hydrazyl (DPPH) radical scavenging assays

following the methodology proposed by Rosales-Castro et al. (2012) and Medina-Torres et al. (2016),

respectively. All determinations were performed in triplicated.

2.3. Artemia salina lethality test

In order to assess the possible lethal effect of I. sonorae infusions, the Artemia salina assay was

performed according to the method proposed by Déciga-Campos et al. (2007). Briefly, dried brine

shrimp eggs were hatched by incubation in saline medium for 48 h at room temperature.

Approximately 100 µL of saline medium containing 10 larvae were transferred into a 96-well plate

containing 100 L of I. sonorae at different concentration (10, 50, 250, 500 and 1000 µg/mL). Survivors

were counted after 24 h. The toxicological effect was expressed as mortality percentage and

interpreted as follow: 0 – 10 % non-toxic, 11 – 50 % moderately toxic, 51 – 90 % highly toxic and

100 % extremely toxic. The average lethal concentration (LC50) was calculated using PROBIT analysis

and expressed in µg/mL. The LC50 values higher than 1000 µg/mL of extract were classified as no toxic

(Déciga-Campos et al., 2007). K2Cr2O7 was used as a positive control (LC50: 12.5 µg/mL). All

determinations were carried out in triplicate.

2.4. Cytotoxic effect of I. sonorae

2.4.1. Cell culture

Breast cancer (MCF-7) and African green monkey kidney (VERO) cell lines were supplied by

Monterrey Institute Technology of Higher Education (ITESM) and Autonomous University of Nuevo

León (UANL), respectively. MCF-7 and VERO cell lines were cultured in Dulbeco’s Modified Eagle

Medium (DMEM) supplemented with 10 % heat-inactivated fetal bovine serum (FBS), 50 µg/ml

streptomycin and 50 UI/mL penicillin and incubated in a ThermoScientific at 37 °C with 5 % of CO2

and 95 % relative humidity to attain a confluent monolayer. Cells were suspended in 0.05 % trypsin-

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EDTA solution for 5 min and centrifuged at 1000 rpm for 10 min at 25 °C in an Eppendorf 5804R

centrifuge. Finally, the cells were suspended in DMEM and manually counted using the Neubauer’s

method.

2.4.2. MTT assay

Cell viability was tested by 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT)

assay. The MTT assay was conducted using a 96-well flat bottom cell culture plate and a confluent

layer of MCF-7 and VERO cells. The cytotoxic potential of the I. sonorae, either WP or WS, were

performed at different concentration (125, 250, 500 and 1000 µg/mL). Briefly, 250 µL of supplemented

DMEM and 50 µL of I. sonorae infusion were placed in 96-well plate and incubated for 72 h, for

triplicate. After incubation, 10 µL of MTT solution and 90 µL of supplemented DMEM were added

and incubated for 4 h in culture conditions. The media containing MTT was removed and 100 µL

isopropanol was added to remove the color produced due to the reaction. The absorbance was

measured at 550 nm in a microplate reader (Bio-Rad iMark). The results were expressed as IC50 values

which were calculated by regression analysis. The percentage of viability was calculated using the

following equation:

󰇛󰇜

 

2.5. Genotoxic effect of I. sonorae infusions

Genotoxic potential was performed in vitro through one bacteria assay based on the modified

Ames test modified for liquid culture and 96-well plate scale, with and without metabolic activation,

referred as S-9 by using one histidine-dependent auxotrophic mutant of S. typhimurium TA100. The

assay was purchased from EBPI bio-detection products (Mississauga, Ontario) known as Muta-

Chromo Plate. On each Muta-Chromo test plate, infusions of I. sonorae infusions (WP and WS) were

combined with a reaction mixture. The I. sonorae infusions were tested at 500 and 1000 µg/mL due to

being the bioactive concentrations in the brine shrimp lethality test. 2-aminoanthracene (2-AA) and

sodium azide (NaN3) were included as positive control for treatments with and without S-9 mixture,

respectively. Background plates containing sterile water, reaction buffer and S. typhimurium TA100

were used to determine spontaneous mutations occurring during incubation. All plates were

incubated for 5 days at 37 ºC (GI2-2 SheL Lab Digital Incubator). The number of revertant colonies in

the samples was scored and compared to the number of positive wells in background plates. All

results were analyzed using Bio-Informatics Toolkit software provided by EPBI.

2.6. Statistical analysis

The phenolic compounds, antioxidant capacity and cytotoxicity of the Ibervillea sonorae extracts,

either WP or WS, were statistically analyzed using analysis of variance (ANOVA) with a p-value of

0.05. Tukey test was used as post-hoc analysis using a significant value of 0.05. All calculations were

performed using Minitab 18 statistical software.

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3. Results and discussions

3.1. Total phenolic compounds and antioxidant capacity

The total phenolic compounds of the I. sonorae infusions are shown in Table 1. As can be seen, the

total phenolic compounds accounted for about 24 meq GA/g in WS infusions whereas for WP

infusions it was 15 meq GA/g. On the other hand, the antioxidant capacity and percentage inhibition

of I. sonorae infusions were tested by ABTS and DPPH assays, respectively. As can be seen in Table 1,

the antioxidant capacity of both infusions, WP and WS, measured by ABTS assay was 1,146.9 and

1,191.4 meq Trolox/100 g, respectively, whereas the DPPH radical scavenging capacity was 13.79 %

for the WP extract and 16.39 % for the WS extract.

Table 1. Total phenol content (TPC) and antioxidant activity measured by the DPPH and ABTS assays of

I. sonorae.

Tabla 1. Contenido de compuestos fenólicos totales y capacidad antioxidante evaluada por los métodos

DPPH y ABTS de I. sonorae

Sample

TPC

DPPH

ABTS

(meq GA/g)

(% inhibition)

(meq Trolox/100 g)

24.14

0.50

16.39

1.36

1,191.40

46.8

15.24

0.05

13.79

1.87

1,146.90

89.1

The results obtained in the present study, either WS or WP, showed moderately low and low TPC,

respectively, according to the categories proposed by Chew et al. (2011). Interestingly, similar TPC

results have been reported by Zapata-Bustos et al. (2014) and Núñez-Gastélum et al. (2018) for extracts

of I. sonorae. In particular, Zapata-Bustos et al. (2014) reported that I. sonorae extracts contained about

1.4 g GAE/kg of phenolic compounds, while Núñez-Gastélum et al. (2018) found about 10 mg GAE/g.

Interestingly, gallic acid has been identified as the most abundant phenolic compound in I. sonorae

extracts which has also been considered as the main responsible for the anti-diabetic properties of I.

sonorae (Zapata-Bustos et al., 2014).

Although the information about the antioxidant capacity of I. sonorae extracts is scarce, several

authors have observed that I. sonorae extracts exhibit a poor antioxidant capacity, in particular free

radical scavenging capacity, which has been related to the low content of phenolic compounds

(Ramírez-Ortíz et al., 2017; Núñez-Gastélum et al., 2018).

3.2. Artemia salina lethality test

A wide variety of biologically active chemical compounds are toxic to brine shrimp, the death of

this organism when exposed to varying concentrations of these compounds is the basis for this

toxicity test. The results of the lethality test are shown in Figure 1. As can be seen, the lethality of I.

sonorae infusions increased as the concentration increased. Interestingly, the WS extract showed

higher lethality (80 %) than WP extract (47 %) at the maximum concentration (1000 µg/mL).

According to the percentage lethality, those infusions prepared from I. sonorae skin are considered as

highly toxic, while infusions from I. sonorae pulp are moderately toxic.

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Figure 1. Results of the lethality test of I. sonorae infusions on Artemia salina.

Figura 1. Resultados del ensayo de letalidad de las infusiones de I. sonorae sobre Artemia salina

The A. salina lethality test is often used as a first toxicological indicator for plant extracts. Also, the

toxicity to A. salina has been correlated with possible antitumor activity (Naidu et al., 2014; Leite et

al., 2015). Those extracts with LC50 values below 1000 μg/mL have been considered as a harmful and

noxious to the organism (Meyer et al., 1982; Déciga-Campos et al., 2007). Based on this premise, WP

infusions could be considered as safe, since LC50 was higher than 1000 µg/mL whereas infusions of I.

sonorae skin could not (LC50 of 359 µg/mL). According to Meyer et al. (1982) only those extracts

obtained from WP could be safely used for human consumption. The results obtained in this study

were similar to those reported by Aarland et al. (2015) who reported a LC50 >1000 µg/mL for the

hexane extract I. sonorae. To the best of our knowledge, this is the first report using in A. salina larvae

model to evaluate the toxicology of aqueous extracts prepared from I. sonorae.

3.3. Cytotoxicity of I. sonorae infusions by MTT assay

The results of the cytotoxicity of I. sonorae infusions using MCF-7 and VERO cell lines are shown

in Figure 2 and Table 2. As can be seen, I. sonorae infusions, either WP or WS, promoted a significant

decrease in the viability of MCF-7 as well as VERO cells (p<0.05). The viability of MCF-7 was reduced

from ~91 % up to ~46 % when the WP concentration increased from 125 to 1000 g/mL whereas a

90 % to 61 % decrease was estimated for WS infusion. Interestingly, no significant differences in MCF-

7 viability were observed when WP and WS extracts were tested at concentrations of 125 and 250

µg/mL (Figure 2a).

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Figure 2. Cell viability of (a) MCF-7 and (b) VERO lines in the presence of I. sonorae infusions.

Figura 2. Viabilidad celular de las líneas (a) MCF-7 y (b) VERO in presencia de las infusiones de I. sonorae.

Figure 2a

Figure 2b

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Table 2. Cytotoxic activity of I. sonorae infusions on VERO and MCF-7 cell lines.

Table 2. Actividad citotóxica de las infusiones de I. sonorae sobre las líneas celulares

VERO y MCF-7.

Sample

IC50 (µg/mL)

VERO

MCF-7

222

902.8

51.97

379

ND*

*ND: not determined

Regarding to VERO cell line, an initial viability of 50 % was observed which decreased to 30 % and

to 20 % using WS and WP, respectively (p<0.05) (see Figure 2b). Interestingly, VERO cells (IC50 <400

µg/mL) were more sensitive than MCF-7 cells (IC50 <1000 µg/mL) to the I. sonorae infusions, either WP

or WS. It is important to note that the MCF-7 and VERO viability exhibited a concentration-

dependent behavior since the viability decreased as the concentration increased.

Cytotoxicity is defined as an alteration of basic cellular functions that can result in cell damage

(Arencibia et al., 2019). The MTT assay is a colorimetric methodology considered as a useful tool for

the determination of the cytotoxic potential of various chemicals, drugs, environmental pollutants

and plant extracts (Sharif et al., 2017). The antiproliferative activity of I. sonorae has been shown in

several studies (Vega-Avila et al., 2009; Torres-Moreno et al., 2015; Quintanilla-Licea et al., 2016).

Interestingly, cucurbitacin, the main compound present in the Cucurbitaceae family, has been

considered as the main responsible, not only of the bitterness and toxicity, but also, for the

antiproliferative effect associated with these plants (Achenbach et al., 1993; Tannin-Spitz et al., 2007;

Patel and Krishnamurthy, 2013). In the last decade, I. sonorae has gained great interest in the cancer

treatment due to the presence of cucurbitacin which has demonstrated biological activity against

glioblastoma (Yuan et al., 2014), human multiple myeloma (Yang et al., 2017) and human breast cancer

(Duangmano et al., 2012).

3.4. Genotoxicity of I. sonorae infusions by Ames test

The genotoxic effect of the I. sonorae, either WP or WS, was assessed by the modified Ames method

using a 96-wells microplate. The results of the modified Ames method are shown in Figures 3a and

3b. As can be seen, WP and WS extracts, at concentrations of 500 and 1000 µg/mL, with the S-9

mixture showed a lower number of positive wells compared to the background and 2-AA in the first

three days of incubation. After this time, the number of positive wells increased as incubation time

increased regardless of the extract (Figure 3a).

On the contrary, the number of positive wells (CFU hys+) observed using WP and WS extracts

was higher than that of the background when these were tested without S-9 mixture. It is important

to note that the number of positive wells of the WP and WS extracts did not exceed the positive wells

of the positive control (NaN3) during the incubation time (see Figure 3b).

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Figure 3. Genotoxic effect induced by infusion of I. sonorae on S. thyphimurium TA100 (a) with and (b) without S-

9 mixture

Figura 3. Efecto genotóxico inducido por la infusión de I. sonorae sobre S. thyphimurium TA100 (a) con y (b) sin

mezcla S-9.

Figure 3a

Figure 3b

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On the other hand, it was observed that both extracts WP and WS, promoted genotoxic effects in the

S. thyphimurium TA100 (His-) strain, without S-9 mixture. The mutation rate was evaluated by

comparison with “Background” which shows the level of spontaneous mutation of S. thyphimurium.

Interestingly, the presence of the S-9 mixture promoted a lower number of positive wells compared

with the background and 2-AA at the first three days of incubation. The S-9 mixture is commonly

used to simulate the metabolic activity of liver, which is the main organ involved in the metabolism

of xenobiotics [30]. It is important to highlight that the genotoxic effect of aqueous extracts of I. sonorae

has not been reported previously. The present in vitro study showed that the aqueous extract of I.

sonorae could cause gene mutations by substituting base pairs. In theory, a single hit on DNA may be

sufficient to start genomic stability (Zhou et al., 2013).

4. Conclusions

The toxicological potential of I. sonorae, a plant used in traditional medicine in the north of Mexico,

was studied. Thus, those infusions prepared from the pulp (WP) of I. sonorae might be considered as

non-lethal whereas the intake of infusions prepared from skin (WS) could promote health damages.

Interestingly, extracts from both plant tissues demonstrated to reduce not only the cancer cells, such

as MCF-7, but also healthy cells, such as VERO. This could be related to the genotoxic effect observed

by the Ames test. Interestingly, I. sonorae showed to be a plant with a moderate content of phenolic

compounds that possess low radical scavenging capacity. Thus, the intake of infusions prepared

from the I. sonorae plant could promote health injuries. Further studies are required to understand

the different biological mechanisms involved in the toxicological effects observed in the present

study.

Conflict of interest

The authors declare that there is no conflict of interest of any kind in the preparation and

publication of this article.

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