Chemical Composition and In Vitro and In Silico Biological Activities of <i>Myrciaria tenella</i> (DC.) O.Berg (Myrtaceae) Essential Oil from Brazil

Ferreira, Oberdan Oliveira; Costa, Vanessa Guimarães; Cruz, Jorddy Nevez; Kataoka, Maria Sueli da Silva; Pinheiro, João de Jesus Viana; Nascimento, Lidiane Diniz do; Varela, Everton Luiz Pompeu; Cascaes, Márcia Moraes; Percário, Sandro; Mali, Suraj N.; Menezes, Tatiany Oliveira de Alencar; de Oliveira, Mozaniel Santana; Andrade, Eloisa Helena de Aguiar

doi:https://doi.org/10.1155/2024/2848736

Journal of Food Biochemistry

On this page

Abstract Introduction Materials and Methods Results and Discussion Conclusions Data Availability Conflicts of Interest Authors’ Contributions Acknowledgments References Copyright Related Articles

Research Article | Open Access

Volume 2024 | Article ID 2848736 | https://doi.org/10.1155/2024/2848736

Chemical Composition and In Vitro and In Silico Biological Activities of Myrciaria tenella (DC.) O.Berg (Myrtaceae) Essential Oil from Brazil

Oberdan Oliveira Ferreira,¹Vanessa Guimarães Costa,²Jorddy Nevez Cruz,³Maria Sueli da Silva Kataoka,⁴João de Jesus Viana Pinheiro,⁴Lidiane Diniz do Nascimento,⁵Everton Luiz Pompeu Varela,⁶Márcia Moraes Cascaes,⁷Sandro Percário,^1,6Suraj N. Mali,⁸Tatiany Oliveira de Alencar Menezes,²and Mozaniel Santana de Oliveira^5,9 et al.

Academic Editor: Minaxi Sharma

Received29 Jan 2024

Revised11 Apr 2024

Accepted25 Apr 2024

Published08 May 2024

Abstract

Myrciariatenella O.Berg, a native plant species of Brazil, exhibits pharmacological applications, including antitumor activity. In this study, we isolated the essential oil (EO) of M. tenella and identified its phytochemical profile. In addition, we determined the in vitro and in silico cytotoxic activities of EO in nontumor and tumor cell lines (gingival fibroblasts and oral squamous cell carcinoma, respectively) and its free radical scavenging activity (i.e., antioxidant activity) using ABTS and DPPH assays. The EO of M. tenella primarily constitutes hydrocarbons and oxygenated sesquiterpenes, with (E)-caryophyllene (33.95%), δ-cadinene (7.4%), caryophyllene oxide (4.74%), and viridiflorene (4.49%) as its four major components. EO effectively suppressed the cell viability of CAL-27 tumor cells to below 70% at concentrations of 125 and 250 μg/mL and exhibited a free radical inhibition potential of 75.63 ± 0.41% and 28.46 ± 0.36%, respectively, in the DPPH and ABTS assays. This chemical and biological potential may be attributed to the major compounds present in EO, as well as the molecular coupling simulations conducted, which revealed the anticancer mechanism of EO in the sesquiterpenes (E)-caryophyllene, δ-cadinene, caryophyllene oxide, and viridiflorene.

1. Introduction

Aromatic plants have been used in ancient civilizations to treat various diseases [1]. To date, researchers have extracted various pharmacologically active molecules from plant species, which are cost-effective, less toxic, and more accessible compared with synthetic drugs [2, 3]. The volatile compounds present in essential oils (EOs) are biosynthesized as secondary metabolites of aromatic plants. These are complex, lipophilic, and volatile mixtures that can be extracted from buds, fruits, flowers, roots, leaves, and branches. Empirical data on EOs reveal their pharmaceutical potential, emphasizing the need to explore their bioactivities [4].

The genus Myrciaria of the plant family Myrtaceae comprises approximately 30 species that are distributed predominantly among countries on the American continent [5]. Twenty-two species of Myrciaria, including Myrciaria tenella O.Berg, are native to Brazil. The leaves of M. tenella, known as cambuí-açu or jabuticaba-macia, exhibit anti-inflammatory, antibacterial, and astringent properties and are widely used by traditional communities [6, 7]. In vivo and in vitro studies have shown that M. tenella metabolites reduce edema, capture free radicals that trigger oxidative stress, and exhibit antimicrobial activities. M. tenella, originating from the Amazon, exhibits antioxidant potential by suppressing the overproduction of reactive oxygen species, which trigger diseases and degenerative processes [8]. Among these processes, the triggering of cancer, which is associated with the excess of free radicals in the body, is noteworthy [9]. Therefore, it is feasible to explore new alternatives, particularly in natural products, aligning with studies on M. tenella that have reported its antiproliferative activity against cancer cell lines [10–12].

In vitro tests enable researchers to analyze the cellular behavior of drugs in a controlled environment, which can help minimize their side effects [13]. According to the ISO 10993-5 guidelines published in 2009, in vitro cytotoxicity tests must expose cells directly or indirectly to the desired substance [14, 15]. Such exposure is crucial to evaluate drug biocompatibility and cell viability, including essential cellular functions, such as growth, reproduction, and metabolism [16].

The cytotoxic activity of the EO of M. tenella has not been investigated in cells obtained from the human oral cavity thus far. Therefore, we conducted in vitro studies on the EO of M. tenella to determine its antioxidant activity against ABTS and DPPH free radicals along with cytotoxicity in human gingival fibroblasts (a nontumor cell line) and oral squamous cell carcinoma cells (CAL-27).

2. Materials and Methods

2.1. Collection and Identification of Plants

In October 2018, leaves of M. tenella were gathered in the city of Magalhães Barata, PA, located at a latitude of 00°47′38″ S and a longitude of 47°35′55″ W. The collected sample, identified as MG 237466, was officially registered and is now housed in a collection of aromatic plants within the herbarium of the Museu Paraense Emílio Goeldi in Pará, Brazil.

2.2. Physical and Chemical Characterization of the Sample

The plant material was cold-dried in a temperature-controlled room with air conditioning. The sample was finely ground using a knife mill (Model TE-631/3; Tecnal, Brazil). The moisture content of the plant material was determined using a moisture analyzer (ID50, Marte Científica, Brazil) based on infrared spectroscopy. The extraction yield of EO was calculated according to the procedure described by Santos et al. [17].

2.3. Essential Oil Isolation

To isolate EO from M. tenella leaves, hydrodistillation was carried out using a modified Clevenger-type apparatus, which utilized 151.42 g of the sample. Extraction was performed for 3 h at 100°C. Subsequently, anhydrous Na₂SO₄ was added to the EO and the resulting mixture was centrifuged to eliminate moisture. The purified EO was carefully stored in an amber-type glass ampoule in a refrigerated environment at 5°C to maintain its chemical composition.

2.4. Chemical Evaluation of Essential Oil

To identify the chemical composition, the protocols already described in a previous study were used. The brand and model of the gas chromatograph (CG-MS and GC-FID), chromatographic column, and other procedures are available in the literature [18]. A comparison of the linear retention index and mass spectra of the reference standards was performed, which aligned with the information reported by Adams [19].

2.5. Cell Culture

In this study, CAL-27 strain (derived from human tongue squamous cell carcinoma) and human gingival fibroblasts obtained from the Cell Culture Laboratory at UFPA’s Faculty of Dentistry were used. Thawed cells were cultured in 25 cm² flasks with DMEM-F12 medium supplemented with 10% fetal bovine serum. The cultures were maintained at 37°C in an incubator with 5% CO₂. Daily monitoring and proliferation assessments were performed using an inverted microscope. All the cell manipulations adhered to biosafety standards and were performed in a laminar flow hood. Growth was observed daily, and the culture medium was refreshed every 2–3 days considering cell metabolism. The protocols used in this study were in accordance with those previously reported by Guimarães et al. [20].

2.6. In Vitro Cytotoxicity Assay

For cytotoxicity analysis, gingival fibroblast lines and CAL-27 cells were seeded in 96-well culture plates at a concentration of 1 × 10³ cells/well and incubated at 37°C in a humid environment with 5% CO₂ for 24 and 48 h for adhesion and cell proliferation, respectively. DMSO (LGC Biotechnology, São Paulo, Brazil) was used as a solvent to ensure solubilization of the oily compound in the culture medium. Subsequently, the compound was diluted to 125, 250, 500, and 1000 µg/mL in the culture medium (Sigma, St. Louis, MO, USA). The control group (no treatment) contained only the culture medium, and 0.01% DMSO was used as the solvent control to eliminate the hypothesis that DMSO could interfere with the results. The cells were then exposed to oil for 24 and 48 h [21].

2.7. Cell Viability Analysis

Cell viability was assessed using the MTT assay following a previously reported method [20].

2.8. Antioxidant Assays

2.8.1. DPPH Assay

The scavenging capacity (SC) of the 2,2-diphenyl-1-picrylhydrazyl (DPPH•) radical by M. tenella EO was evaluated using the method outlined by Blois [22]. Trolox served as the positive control, and deionized water was used as the blank control. The samples were assessed in quintuplicate using an ultraviolet-visible (UV-vis) light spectrophotometer (800XI, FEMTO; São Paulo, Brazil). The percentage of inhibition was determined from the observed absorbance and calculated using the formula described in the literature [23].

2.8.2. ABTS Assay

Chemical interactions between EO and ABTS^•+ radicals were determined according to the procedures outlined in the literature [24, 25]. A UV-vis spectrophotometer (800XI, FEMTO; São Paulo, Brazil) was used at a wavelength of 734 nm. Deionized water served as the blank control, whereas Trolox served as the positive control. The percentage of inhibition was determined using the observed absorbance values, which were calculated using the formula described in the literature [23].

2.9. Molecular Modeling

(E)-Caryophyllene, δ-cadinene, caryophyllene oxide, and viridiflorene were drawn using GaussView 5.5 software and optimized at the B3LYP/6-31G level [26, 27] using Gaussian 09 software [28]. The DNA structure used as the molecular target was retrieved from the Protein Data Bank (ID:1BNA) [29]. DNA-ligand docking studies were performed using AutoDock MGLTools 1.5.7 and AutoDock Vina 1.2.0 programs [30–32]. Docking was performed on the entire DNA structure using a grid box of 25 × 32 × 47 and a spacing of 1 Å. The lowest-energy conformation was considered to be the binding mode.

3. Results and Discussion

3.1. Yield and Chemical Profile of the Essential Oil of Myrciaria tenella

Table 1 shows the yield and main chemical compounds in the EO of M. tenella. The EO yield was 0.74% (w/w), which was lower than that found in two samples of M. tenella (specimen A: 2.1%; specimen B: 1.2%) by da Costa et al. [33]. This difference in yield may be attributed to environmental conditions and the collection period [34].

Fifty-eight chemical constituents, accounting for 99.76% of the volatile compounds, were quantified in the EO of M. tenella. The volatile components were categorized as hydrocarbon (78.49%) and oxygenated (21.27%) sesquiterpenes. The major volatile compounds were (E)-caryophyllene (33.95%), δ-cadinene (7.4%), caryophyllene oxide (4.74%), and viridiflorene (4.49%). Our results differed from those reported by Gonçalves et al. [34], who investigated a specimen of M. tenella collected in Restinga da Marambaia, Rio de Janeiro, Brazil, and reported that the main volatile compounds were β-pinene (21.46%), α-pinene (19.43%), and (E)-caryophyllene (10.89%).

According to a research study by Apel et al. [35], certain EOs derived from Myrciaria species are abundant in terpenoids, as exemplified by the EO of M. plinioides [35]. This particular EO is comprised of significant quantities of nonoxygenated and oxygenated monoterpenes and sesquiterpenes. In a separate study by Andrade et al. [36], the EO of M. tenella from Acará, Pará, Brazil, revealed (E)-caryophyllene (32.0%), δ-cadinene (5.1%), and caryophyllene oxide (5.0%) as the predominant volatile compounds. Another specimen of M. tenella, collected from Mogi Guaçu, São Paulo, Brazil, contained (E)-caryophyllene (25.1%) and spathulenol (9.7%), according to Apel et al. [35]. The EO from M. tenella leaves from Rodeio Bonito, RS, Brazil, contains α-pinene (31.5%), β-pinene (19.2%), and 1,8-cineole (6.6%) as the major constituents [11]. The main compounds identified in the EO of M. tenella in this study exhibited noteworthy bioactivity. For instance, (E)-caryophyllene exhibited antimicrobial properties against both Gram-positive and Gram-negative bacteria [37], suggesting its potential use as a disinfectant and preservative. In addition, δ-cadinene inhibited the growth of Streptococcus pneumoniae, a bacterium responsible for respiratory infections, with an MIC of 31.25 μg/mL [38]. Furthermore, caryophyllene oxide exhibited anti-inflammatory and analgesic activities, as reported by Chavan et al. [39]. These findings highlight the diverse and potentially beneficial properties of the main constituents found in the EO obtained from M. tenella.

3.2. Cell Viability

According to the ISO 10993-5 standard, a compound is considered toxic when cell viability in its presence is less than 70% compared with the control group [40]. At 125 and 250 µg/mL, the EO of M. tenella was not toxic to gingival fibroblasts during a 24-h period, as shown in Figure 1. After 48 h, despite the decrease in the percentage of viable gingival fibroblasts, it remained nontoxic at both concentrations. This compound maintains the viability of this cell group, which is crucial for oral tissue regeneration and repair processes.

Oral cancer, the second most prevalent malignant tumor within the head and neck region, is largely dominated by oral squamous cell carcinoma, accounting for over 90% of all cases, as highlighted by the National Cancer Institute [41]. Notably, EO of M. tenella exhibited pronounced antiproliferative effects on CAL-27 cells. In particular, at 24 h, a concentration of 250 µg/mL reduced cell viability to below 70%, as shown in Figure 2. By the second day, all concentrations demonstrated toxicity, underscoring the potent antiproliferative nature of M. tenella in combating this malignant neoplasm. The cytotoxic attributes can be ascribed to the key compounds present in EO. Oliveira et al. [42] emphasized the cytotoxic potential of (E)-caryophyllene, which is a major component in EO of M. tenella.

Furthermore, Jun et al. [43] reported the cytotoxicity of caryophyllene oxide, another major compound in the EO of M. tenella. Caryophyllene, a natural sesquiterpene present in plants, exhibits potent anticancer effects and enhances drug efficacy. BCP, a phytocannabinoid, binds strongly to CB2 and lacks CB1 affinity. BCPO, an oxidative derivative, is independent of the endocannabinoid system. BCPO alters cancer-related pathways and selectively activates CB2, making BCP a potential natural analgesic. The correlation between anticancer and antioxidant properties highlights a crucial interplay in disease prevention and treatment. Antioxidants, by neutralizing harmful free radicals and reducing oxidative stress, contribute to lowering the risk of cancer development. Moreover, many natural compounds exhibiting potent antioxidant activity also demonstrate anticancer effects, suggesting a shared mechanism. These dual functionalities underscore the potential of antioxidant-rich diets and therapies in combating cancer and promoting overall health [42, 43]. Its dual anticancer and analgesic roles influence chemotherapy efficacy and are valuable in oncology [44]. Giacomo et al. [45] highlighted the anticarcinogenic activity of both caryophyllene oxide and (E)-caryophyllene against human colorectal adenocarcinoma (Caco-2) and T-cell leukemia (CCRF/CEM), which resulted in a significant reduction in cell viability. These findings collectively underscore the potential therapeutic significance of EO of M. tenella and its major constituents, particularly (E)-caryophyllene and caryophyllene oxide, in combating oral squamous cell carcinoma [46, 47].

3.3. Antioxidant Potential

Figure 3 shows the antioxidant potential of EO of M. tenella against the ABTS^•+ and DPPH^• radicals. The SC of the EO was defined as the decrease in the concentration of radicals. Trolox was used as a positive control. The benefits of EO in the medical and food fields can be attributed to their antioxidant properties [48]. Therefore, the antioxidant activity of EO of M. tenella was assessed via ABTS^•+ and DPPH^• radical scavenging assays [49]. The EO of M. tenella exhibited a strong SC (75%) in the DPPH assay and good antioxidant activity (28%) in the ABTS assay compared with the Trolox standard. Moraes et al. [50] reported that the EO of M. floribunda exhibited excellent scavenging activity for both ABTS^•+ and DPPH^• radicals. This result was attributed to the high levels of oxygenated monoterpene 1,8-cineole in the EO. The EO of M. tenella primarily comprises hydrocarbon sesquiterpenes with 33.95% (E)-caryophyllene content. In addition, the differences in the antioxidant activities of the EO of M. tenella in the DPPH and ABTS assays may correspond to the synergistic interactions between their components. This difference was partially attributed to the reaction medium (ethanol for the DPPH assay and phosphate-buffered saline for the ABTS assay) and reaction time (5 min for the ABTS assay and 30 min for the DPPH assay). All these factors facilitate radical scavenging kinetics [51, 52].

3.4. Molecular Modeling

MD studies have demonstrated that these compounds interact favorably with DNA. (E)-Caryophyllene, δ-cadinene, caryophyllene oxide, and viridiflorene exhibited binding energies of −4.9, −5.1, −4.5, and −4.8 kcal/mol, respectively.

Morávek et al. [53] found that small compounds, such as volatile compounds in EO of M. tenella, exhibited a greater binding affinity for the minor groove of DNA, aligning with our docking study results. This phenomenon could be partially attributed to the molecular size of the ligands, which renders the formation of a stable complex with the major groove of DNA difficult. However, the compounds exhibited only a few chemical interactions with the minor groove of the DNA. In this study, these interactions were sufficient to form a stable and energetically favorable complex, according to the binding affinity energy results reported by Cascaes et al. [54]. The observed chemical interactions were hydrophobic, and electrostatic interactions were not observed because of the absence of polarizable and ionizable groups in the ligands (Figure 4).

The lowest-energy complexes from the docking results were selected as the starting point for the MD simulations, in which the complexes exhibited favorable binding energy values (Table 2). Van der Waals interactions significantly contributed to the formation of these complexes in addition to the favorable contributions of electrostatic and nonpolar interactions.

4. Conclusions

In this study, the essential oil (EO) of M. tenella has revealed significant advancements on various fronts. The identification of the EO’s chemical profile highlighted its main components, especially hydrocarbon and oxygenated sesquiterpenes, such as (E)-caryophyllene, δ-cadinene, caryophyllene oxide, and viridiflorene. Additionally, its antioxidant activity was demonstrated against DPPH and ABTS radicals, indicating its relevance as an antioxidant agent. The evaluation of its cytotoxicity in tumor and nontumor cells revealed a concentration and test period dependency, with promising results in gingival fibroblast cells, suggesting its potential utility in treating oral cavity-related diseases. The in silico analysis underscored the ability of the EOs’ major constituents to interact with molecular targets, corroborating its cytotoxic activity. These findings indicate that the EO of M. tenella holds therapeutic potential, although further investigations are necessary to validate its efficacy and safety in clinical applications. In summary, this research represents a promising step toward the development of economically viable and accessible therapeutic alternatives.

Data Availability

The data used to support the findings of this study are available from the corresponding author upon request.

Conflicts of Interest

The authors declare they have no conflicts of interest.

Authors’ Contributions

Oberdan Oliveira Ferreira, Vanessa Guimarães Costa, and Jorddy Nevez Cruz conceptualized the study and performed investigation. Maria Sueli da Silva Kataoka, João de Jesus Viana Pinheiro, Lidiane Diniz do Nascimento, Everton Luiz Pompeu Varela, Márcia Moraes Cascaes, Sandro Percário, Suraj N. Mali, and Oberdan Oliveira Ferreira proposed the methodology. Tatiany Oliveira de Alencar Menezes, Mozaniel Santana de Oliveira, and Eloisa Helena de Aguiar Andrade validated the data, visualized the data, and performed formal analysis. Lidiane Diniz do Nascimento, Everton Luiz Pompeu Varela, Márcia Moraes Cascaes, Sandro Percário, and Suraj N. Mali provided resources. Oberdan Oliveira Ferreira curated the data. Eloisa Helena de Aguiar Andrade supervised the data and administered the project. All authors participated in result discussions and approved the final manuscript.

Acknowledgments

The authors extend their thanks to the “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) from Brazil” for their support, acknowledged under funding process number 001. Mozaniel Santana de Oliveira extends appreciation to PDPG-POSDOC-Programa de Desenvolvimento da Pós-Graduação (PDPG) Pós-Doutorado Estratégico and CAPES for the scholarship (process number: 88887.852405/2023-00). The authors also acknowledge Edital 02/2023—PAPQ/PROPESP-Universidade Federal do Para for their support.

References

A. M. Barata, F. Rocha, V. Lopes, and A. M. Carvalho, “Conservation and sustainable uses of medicinal and aromatic plants genetic resources on the worldwide for human welfare,” Industrial Crops & Products, vol. 88, pp. 8–11, 2016.
View at: Google Scholar
R. Badraoui, A. J. Siddiqui, F. Bardakci, and H. Ben-Nasr, “Ethnopharmacology and ethnopharmacognosy: current perspectives and future prospects,” Ethnobotany and Ethnopharmacology of Medicinal and Aromatic Plants, pp. 115–128, 2023.
View at: Google Scholar
R. d. S. Pedroso, G. Andrade, and R. H. Pires, “Plantas medicinais: uma abordagem sobre o uso seguro e racional,” Physis: Revista de Saúde Coletiva, vol. 31, no. 2, 2021.
View at: Publisher Site | Google Scholar
J. A. M. de Castro, O. S. Monteiro, D. F. Coutinho, A. A. C. Rodrigues, J. K. R. da Silva, and J. G. S. Maia, “Seasonal and circadian study of a thymol/γ-terpinene/p-cymene type oil of ocimum gratissimum L. And its antioxidant and antifungal effects,” Journal of the Brazilian Chemical Society, vol. 30, no. 5, pp. 930–938, 2018.
View at: Publisher Site | Google Scholar
L. L. Borges, E. C. Conceição, and D. Silveira, “Active compounds and medicinal properties of Myrciaria genus,” Food Chemistry, vol. 153, pp. 224–233, 2014.
View at: Publisher Site | Google Scholar
M. M. Monteiro, A. Giaretta, O. J. Pereira, and L. F. T. d. Menezes, “Composição e estrutura de uma restinga arbustiva aberta no norte do Espírito Santo e relações florísticas com formações similares no Sudeste do Brasil,” Rodriguesia, vol. 65, no. 1, pp. 61–72, 2014.
View at: Publisher Site | Google Scholar
A. C. P. d. Menezes Filho, “Myrciaria glazioviana, Myrciaria strigipes e Myrciaria trunciflora: análise sistemática, reprodução, fitoquímica e farmacologia,” Scientific Electronic Archives, vol. 14, no. 8, 2021.
View at: Publisher Site | Google Scholar
C. S. M. d. Silva and R. H. V. Mourão, “Atividade antioxidante de extratos de Myrciaria dubia (camu-camu) Myrtaceae,” Research, Society and Development, vol. 11, no. 2, p. e5811225130, 2022.
View at: Publisher Site | Google Scholar
C. Yang, H. Chen, H. Chen, B. Zhong, X. Luo, and J. Chun, “Antioxidant and anticancer activities of essential oil from gannan navel orange peel,” Molecules, vol. 22, no. 8, pp. 1391–1410, 2017.
View at: Publisher Site | Google Scholar
A. R. Ribeiro, M. L. Cordeiro, L. M. Silva et al., “Myrciaria tenella (DC.) O. Berg (Myrtaceae) leaves as a source of antioxidant compounds,” Antioxidants, vol. 8, no. 8, p. 310, 2019.
View at: Publisher Site | Google Scholar
N. F. Z. Schneider, N. F. Moura, T. Colpo, K. Marins, C. Marangoni, and A. Flach, “Estudo dos compostos voláteis e atividade antimicrobiana da Myrciaria tenella (cambuí),” Revista Brasileira Farmacognosia, vol. 89, no. 2, pp. 131–133, 2008.
View at: Google Scholar
V. de Carvalho Martins, L. P. França, Y. da Silva Ferreira et al., “Determination of the phytochemical composition and antioxidant potential of eugenia copacabanensis and Myrciaria tenella leaves (Myrtaceae) using a Saccharomyces cerevisiae model,” Chemistry and Biodiversity, vol. 18, no. 6, p. e2100054, 2021.
View at: Publisher Site | Google Scholar
C.-P. Segeritz and L. Vallier, “Cell culture: growing cells as model systems in vitro,” in Basic Science Methods for Clinical Researchers, pp. 151–172, Elsevier, Amsterdam, Netherlands, 2017.
View at: Google Scholar
I. Bédoui, H. B. Nasr, K. Ksouda et al., “Phytochemical composition, bioavailability and pharmacokinetics of scorzonera undulata methanolic extracts: antioxidant, anticancer, and apoptotic effects on MCF7 cells,” Pharmacognosy Magazine, vol. 20, no. 1, pp. 218–229, 2023.
View at: Publisher Site | Google Scholar
F. Rahmouni, L. Hamdaoui, M. Saoudi, R. Badraoui, and T. Rebai, “Antioxidant and antiproliferative effects of Teucrium polium extract: computational and in vivo study in rats,” Toxicology Mechanisms and Methods, pp. 1–12, 2024.
View at: Publisher Site | Google Scholar
F. L. Heggendorn, L. Gonçalves, E. Cardoso, M. Lutterbach, and V. Lione, “Biocompatibility tests: cultivation of animal cells and their applications in toxicity studies,” Conexão Ciência (Online), vol. 15, no. 1, pp. 67–77, 2020.
View at: Publisher Site | Google Scholar
A. S. Santos, S. de M. Alves, F. J. C. Figueiredo, and O. G. Da Rocha Neto, Descrição de sistema e de métodos de extração de óleos essenciais e determinação de umidade de biomassa em laboratório, Embrapa Amaz. Orient, Belém, Brazil, 2004.
O. O. Ferreira, S. H. M. da Silva, M. S. de Oliveira, and E. H. d. A. Andrade, “Chemical composition and antifungal activity of myrcia multiflora and eugenia Florida essential oils,” Molecules, vol. 26, no. 23, p. 7259, 2021.
View at: Publisher Site | Google Scholar
R. P. Adams and R. P. Adams, “Identification of Essential Oil Components by Gas Chromatography/Mass Spectrometry,” Allured Publishing Corporation-CAROL STREAM, vol. 8, no. 6, 2007.
View at: Google Scholar
L. H. d. S. Guimarães, G. P. Chemelo, A. C. B. A. Alves et al., “Chemical composition and cytotoxicity evaluation of lippia origanoides kunth (verbenaceae) leaves essential oil on human gingival fibroblasts,” Journal of Essential Oil Bearing Plants, vol. 24, no. 4, pp. 704–713, 2021.
View at: Publisher Site | Google Scholar
R. Beltrami, M. Colombo, K. Rizzo, A. Di Cristofaro, C. Poggio, and G. Pietrocola, “Cytotoxicity of different composite resins on human gingival fibroblast cell lines,” Biomimetics, vol. 6, no. 2, p. 26, 2021.
View at: Publisher Site | Google Scholar
M. S. Blois, “Antioxidant determinations by the use of a stable free radical,” Nature, vol. 181, no. 4617, pp. 1199-1200, 1958.
View at: Publisher Site | Google Scholar
T. Zhang, Z. Zhang, and X. Wang, “Composition and antioxidant ability of extract from different flaxseed cakes and its application in flaxseed oil,” Journal of Oleo Science, vol. 72, no. 1, pp. 59–67, 2023.
View at: Publisher Site | Google Scholar
N. J. Miller, C. Rice-Evans, M. J. Davies, V. Gopinathan, and A. Milner, “A novel method for measuring antioxidant capacity and its application to monitoring the antioxidant status in premature neonates,” Clinical Science, vol. 84, no. 4, pp. 407–412, 1993.
View at: Publisher Site | Google Scholar
R. Re, N. Pellegrini, A. Proteggente, A. Pannala, M. Yang, and C. Rice-Evans, “Antioxidant activity applying an improved ABTS radical cation decolorization assay,” Free Radical Biology and Medicine, vol. 26, no. 9–10, pp. 1231–1237, 1999.
View at: Publisher Site | Google Scholar
A. D. Becke, “Density‐functional thermochemistry. III. The role of exact exchange,” The Journal of Chemical Physics, vol. 98, no. 7, pp. 5648–5652, 1993.
View at: Publisher Site | Google Scholar
C. Lee, W. Yang, and R. G. Parr, “Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density,” Physical Review B: Condensed Matter, vol. 37, no. 2, pp. 785–789, 1988.
View at: Publisher Site | Google Scholar
M. J. Frisch, G. W. Trucks, H. B. Schlegel et al., “Gaussian 09,” pp. 2-3, 2009, https://gaussian.com/glossary/g09/.
View at: Google Scholar
H. R. Drew, R. M. Wing, T. Takano et al., “Structure of a B-DNA dodecamer: conformation and dynamics,” Proceedings of the National Academy of Sciences of the United States of America, vol. 78, no. 4, pp. 2179–2183, 1981.
View at: Publisher Site | Google Scholar
J. Eberhardt, D. Santos-Martins, A. F. Tillack, and S. Forli, “AutoDock Vina 1.2.0: new docking methods, expanded force field, and Python bindings,” Journal of Chemical Information and Modeling, vol. 61, no. 8, pp. 3891–3898, 2021.
View at: Publisher Site | Google Scholar
G. M. Morris, R. Huey, W. Lindstrom et al., “AutoDock4 and AutoDockTools4: automated docking with selective receptor flexibility,” Journal of Computational Chemistry, vol. 30, no. 16, pp. 2785–2791, 2009.
View at: Publisher Site | Google Scholar
V. M. Almeida, Ê. R. Dias, B. C. Souza et al., “Methoxylated flavonols from Vellozia dasypus Seub ethyl acetate active myeloperoxidase extract: in vitro and in silico assays,” Journal of Biomolecular Structure and Dynamics, vol. 40, no. 16, pp. 7574–7583, 2022.
View at: Publisher Site | Google Scholar
J. S. da Costa, W. M. S. Andrade, R. O. de Figueiredo et al., “Chemical composition and variability of the volatile components of Myrciaria species growing in the Amazon region,” Molecules, vol. 27, no. 7, p. 2234, 2022.
View at: Publisher Site | Google Scholar
G. M. Gonçalves, V. d. C. Martins, A. R. H. da Costa et al., “Essential oil of Myrciaria tenella (DC.) O. Berg: effects of distillation time on its chemical composition and evaluation of its anti-inflammatory and antinociceptive effects,” Journal of Essential Oil Research, vol. 33, no. 4, pp. 394–409, 2021.
View at: Publisher Site | Google Scholar
M. A. Apel, M. E. L. Lima, M. Sobral et al., “Anti-inflammatory activity of essential oil from leaves of Myrciaria tenella and Calycorectes sellowianus,” Pharmaceutical Biology, vol. 48, no. 4, pp. 433–438, 2010.
View at: Publisher Site | Google Scholar
E. H. A. Andrade, M. d. G. B. Zoghbi, A. C. M. Silva, A. C. M. Silva, and O. Berg, “Constituents of the essential oil ofMyrciaria tenella(DC.) O. Berg,” Journal of Essential Oil Research, vol. 18, no. 1, pp. 93-94, 2006.
View at: Publisher Site | Google Scholar
R. M. Montanari, L. C. A. Barbosa, A. J. Demuner, C. J. Silva, L. S. Carvalho, and N. J. Andrade, “Chemical composition and antibacterial activity of essential oils from verbenaceae species: alternative sources of (E)-caryophyllene and germacrene-D,” Quimica Nova, vol. 34, no. 9, pp. 1550–1555, 2011.
View at: Publisher Site | Google Scholar
A. Pérez-López, A. T. Cirio, V. M. Rivas-Galindo, R. S. Aranda, and N. W. De Torres, “Activity against streptococcus pneumoniae of the essential oil and δ-cadinene isolated from schinus molle fruit,” Journal of Essential Oil Research, vol. 23, no. 5, pp. 25–28, 2011.
View at: Publisher Site | Google Scholar
M. J. Chavan, P. S. Wakte, and D. B. Shinde, “Analgesic and anti-inflammatory activity of Caryophyllene oxide from Annona squamosa L. bark,” Phytomedicine, vol. 17, no. 2, pp. 149–151, 2010.
View at: Publisher Site | Google Scholar
I. Standard, Biological evaluation of medical devices—Part 5: tests for in vitro cytotoxicity, Int. Organ. Stand, Geneva, Switzerland, 2009.
J. E. Klaunig and Z. Wang, “Oxidative stress in carcinogenesis,” Current Opinion in Toxicology, vol. 7, pp. 116–121, 2018.
View at: Publisher Site | Google Scholar
P. F. d. Oliveira, J. M. Alves, J. L. Damasceno et al., “Cytotoxicity screening of essential oils in cancer cell lines,” Revista Brasileira de Farmacognosia, vol. 25, no. 2, pp. 183–188, 2015.
View at: Publisher Site | Google Scholar
N. J. Jun, A. Mosaddik, J. Y. Moon et al., “Cytotoxic activity of β-caryophyllene oxide isolated from Jeju Guava (Psidium cattleianum Sabine) leaf,” Records of Natural Products, vol. 5, no. 3, pp. 242–246, 2011.
View at: Google Scholar
K. Fidyt, A. Fiedorowicz, L. Strządała, and A. Szumny, “β-caryophyllene and β-caryophyllene oxide-natural compounds of anticancer and analgesic properties,” Cancer Medicine, vol. 5, no. 10, pp. 3007–3017, 2016.
View at: Publisher Site | Google Scholar
S. Di Giacomo, A. Di Sotto, G. Mazzanti, and M. Wink, “Chemosensitizing properties of β-caryophyllene and β-caryophyllene oxide in combination with doxorubicin in human cancer cells,” Anticancer Research, vol. 37, no. 3, pp. 1191–1196, 2017.
View at: Google Scholar
D. Ramachandhiran, C. Sankaranarayanan, R. Murali, S. Babukumar, and V. Vinothkumar, “β-Caryophyllene promotes oxidative stress and apoptosis in KB cells through activation of mitochondrial-mediated pathway – an in-vitro and in-silico study,” Archives of Physiology and Biochemistry, vol. 128, no. 1, pp. 148–162, 2022.
View at: Publisher Site | Google Scholar
A. Di Sotto, R. Mancinelli, M. Gullì et al., “Chemopreventive potential of caryophyllane sesquiterpenes: an overview of preliminary evidence,” Cancers, vol. 12, no. 10, p. 3034, 2020.
View at: Publisher Site | Google Scholar
M. Valdivieso-Ugarte, C. Gomez-Llorente, J. Plaza-Díaz, and Á. Gil, “Antimicrobial, antioxidant, and immunomodulatory properties of essential oils: a systematic review,” Nutrients, vol. 11, no. 11, p. 2786, 2019.
View at: Publisher Site | Google Scholar
R. Wołosiak, B. Drużyńska, D. Derewiaka et al., “Verification of the conditions for determination of antioxidant activity by ABTS and DPPH assays—a practical approach,” Molecules, vol. 27, no. 1, p. 50, 2021.
View at: Publisher Site | Google Scholar
Â. A. B. de Moraes, O. O. Ferreira, L. S. da Costa et al., “Phytochemical profile, preliminary toxicity, and antioxidant capacity of the essential oils of Myrciaria floribunda (H. West ex willd.) O. Berg. And myrcia sylvatica (G. Mey) DC. (Myrtaceae),” Antioxidants, vol. 11, no. 10, p. 2076, 2022.
View at: Publisher Site | Google Scholar
K. Mishra, H. Ojha, and N. K. Chaudhury, “Estimation of antiradical properties of antioxidants using DPPH assay: a critical review and results,” Food Chemistry, vol. 130, no. 4, pp. 1036–1043, 2012.
View at: Publisher Site | Google Scholar
M. Huang, A. M. Sanchez‐Moreiras, C. Abel et al., “The major volatile organic compound emitted from Arabidopsis thaliana flowers, the sesquiterpene (E)‐β‐caryophyllene, is a defense against a bacterial pathogen,” New Phytologist, vol. 193, no. 4, pp. 997–1008, 2012.
View at: Publisher Site | Google Scholar
Z. Morávek, S. Neidle, and B. Schneider, “Protein and drug interactions in the minor groove of DNA,” Nucleic Acids Research, vol. 30, no. 5, pp. 1182–1191, 2002.
View at: Publisher Site | Google Scholar
M. M. Cascaes, O. d. S. Carneiro, L. D. d. Nascimento et al., “Essential oils from annonaceae species from Brazil: a systematic review of their phytochemistry, and biological activities,” International Journal of Molecular Sciences, vol. 22, no. 22, p. 12140, 2021.
View at: Publisher Site | Google Scholar

Copyright

Copyright © 2024 Oberdan Oliveira Ferreira 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.

PDF Download Citation

Download other formats

Order printed copies

Views

78

Downloads

40

Citations