Antibacterial, Trichomonacidal, and Cytotoxic Activities of Pleopeltis crassinervata Extracts
Abstract
:1. Introduction
2. Materials and Methods
2.1. Bacterial Strains
2.2. Parasites
2.3. Cell Culture
2.4. Plant Material, Extraction, and Fractionation
2.5. Antibacterial Assay
2.6. Trichomonacidal Assay
2.7. Cytotoxic Assay
2.8. Screening for Synergistic Effects of the Fractions against T. vaginalis
2.9. GC/MS Analysis
2.10. Statistical Analysis
3. Results
3.1. Antibacterial Assay
3.2. Effect of P. crassirnervata in T. vaginalis Trophozoites and Cell Viability
3.3. Synergistic Effect of P. crassinervata Trichomonacidal Subfractions
3.4. GC/MS Analysis of Hsf6
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Atanasov, A.G.; Waltenberger, B.; Pferschy-Wenzig, E.M.; Linder, T.; Wawrosch, C.; Uhrin, P.; Temml, V.; Wang, L.; Schwaiger, S.; Heiss, E.H.; et al. Discovery and resupply of pharmacologically active plant-derived natural products: A review. Biotechnol. Adv. 2015, 33, 1582–1614. [Google Scholar] [CrossRef] [PubMed]
- Rodríguez-Hernández, A.A.; Flores-Soria, F.G.; Patiño-Rodríguez, O.; Escobedo-Moratilla, A. Sanitary Registries and Popular Medicinal Plants Used in Medicines and Herbal Remedies in Mexico (2001–2020): A Review and Potential Perspectives. Horticulturae 2022, 8, 377. [Google Scholar] [CrossRef]
- Maldonado Miranda, J.J. Chapter 7. In Medicinal Plants and Their Traditional Uses in Different Locations, in Phytomedicine; Bhat, R.A., Hakeem, K.R., Dervash, M.A., Eds.; Academic Press: Cambridge, MA, USA, 2021; pp. 207–223. [Google Scholar]
- Hennipman, E.; Veldhoen, P.; Kramer, K.U. Polypodiaceae. In Pteridophytes and Gymnosperms; Springer: Berlin/Heidelberg, Germany, 1990; pp. 203–230. [Google Scholar]
- Cao, H.; Chai, T.T.; Wang, X.; Morais-Braga, M.F.B.; Yang, J.H.; Wong, F.C.; Wang, R.; Yao, H.; Cao, J.; Cornara, L.; et al. Phytochemicals from fern species: Potential for medicine applications. Phytochem. Rev. 2017, 16, 379–440. [Google Scholar] [CrossRef]
- Fernández-Nava, R.; Ramos-Zamora, D.; Carranza-González, E. Notas sobre plantas medicinales del estado de Querétaro. Polibotánica 2001, 12, 1–39. [Google Scholar]
- Newman, D.J.; Cragg, G.M. Natural Products as Sources of New Drugs over the Nearly Four Decades from 01/1981 to 09/2019. J. Nat. Prod. 2020, 83, 770–803. [Google Scholar] [CrossRef]
- Fernández-Villa, D.; Aguilar, M.R.; Rojo, L. Folic Acid Antagonists: Antimicrobial and Immunomodulating Mechanisms and Applications. Int. J. Mol. Sci. 2019, 20, 4996. [Google Scholar] [CrossRef]
- World Health Organization (WHO). Antibiotic Resistance. Available online: https://www.who.int/news-room/fact-sheets/detail/antibiotic-resistance (accessed on 29 February 2024).
- Tornimbene, B.; Eremin, S.; Escher, M.; Griskeviciene, J.; Manglani, S.; Pessoa-Silva, C.L.B. WHO global antimicrobial resistance surveillance system early implementation 2016–17. Lancet Infect. Dis. 2018, 18, 241–242. [Google Scholar] [CrossRef]
- Mancuso, G.; Midiri, A.; Gerace, E.; Biondo, C. Bacterial Antibiotic Resistance: The Most Critical Pathogens. Pathogens 2021, 10, 1310. [Google Scholar] [CrossRef]
- Jovanovic, O.; Amábile-Cuevas, C.F.; Shang, C.; Wang, C.; Ngai, K.W. What Water Professionals Should Know about Antibiotics and Antibiotic Resistance: An Overview. ACS EST Water 2021, 1, 1334–1351. [Google Scholar] [CrossRef]
- Morehead, M.S.; Scarbrough, C. Emergence of global antibiotic resistance. Prim. Care Clin. Off. Pract. 2018, 45, 467–484. [Google Scholar] [CrossRef] [PubMed]
- Mirzadeh, M.; Olfatifar, M.; Eslahi, A.V.; Abdoli, A.; Houshmand, E.; Majidiani, H.; Johkool, M.G.; Askari, S.; Hashemipour, S.; Badri, M. Global prevalence of Trichomonas vaginalis among female sex workers: A systematic review and meta-analysis. Parasitol. Res. 2021, 120, 2311–2322. [Google Scholar] [CrossRef] [PubMed]
- Rowley, J.; Vander Hoorn, S.; Korenromp, E.; Low, N.; Unemo, M.; Abu-Raddad, L.J.; Chico, R.M.; Smolak, A.; Newman, L.; Gottlieb, S.; et al. Chlamydia, gonorrhoea, trichomoniasis and syphilis: Global prevalence and incidence estimates, 2016. Bull World Health Organ. 2019, 97, 548–562. [Google Scholar] [CrossRef] [PubMed]
- Menezes, C.B.; Frasson, A.P.; Tasca, T. Trichomoniasis—Are we giving the deserved attention to the most common non-viral sexually transmitted disease worldwide? Microb. Cell 2016, 3, 404–419. [Google Scholar] [CrossRef] [PubMed]
- Wiringa, A.E.; Ness, R.B.; Darville, T.; Beigi, R.H.; Haggerty, C.L. Trichomonas vaginalis, endometritis and sequelae among women with clinically suspected pelvic inflammatory disease. Sex Transm. Infect. 2020, 96, 436–438. [Google Scholar] [CrossRef]
- Rein, M.F. Trichomoniasis. In Hunter’s Tropical Medicine and Emerging Infectious Diseases; Elsevier: Amsterdam, The Netherlands, 2020; pp. 731–733. [Google Scholar]
- Anacleto-Santos, J.; López-Camacho, P.; Mondragón-Flores, R.; Vega-Ávila, E.; Basurto-Islas, G.; Mondragón-Castelán, M.; Carrasco-Ramírez, E. Rivera-Fernández, Anti-toxoplasma, antioxidant and cytotoxic activities of Pleopeltis crassinervata (Fée) T. Moore hexane fraction. Saudi J. Biol. Sci. 2020, 27, 812–819. [Google Scholar] [CrossRef]
- Anacleto-Santos, J.; Calzada, F.; López-Camacho, P.Y.; López-Pérez, T.J.; Carrasco-Ramírez, E.; Casarrubias-Tabarez, B.; Fortoul, T.I.; Rojas-Lemus, M.; López-Valdés, N.; Rivera-Fernández, N. Evaluation of the Anti-Toxoplasma gondii Efficacy, Cytotoxicity, and GC/MS Profile of Pleopeltis crassinervata Active Subfractions. Antibiotics 2023, 12, 889. [Google Scholar] [CrossRef]
- Sarker, S.D.; Nahar, L.; Kumarasamy, W. Microtitre plate-based antibacterial assay incorporating resazurin as an indicator of cell growth, and its application in the in vitro antibacterial screening of phytochemicals. Methods 2007, 42, 321–334. [Google Scholar] [CrossRef]
- Vega-Avila, E.; Tapia-Aguilar, R.; Reyes-Chilpa, R.; Guzmán-Gutiérrez, S.L.; Pérez-Flores, J.; Velasco-Lezama, R. Actividad antibacteriana y antifúngica de Justicia spicigera. Rev. Lat. Quím. 2012, 40, 75–82. [Google Scholar]
- Ibañez-Escribano, A.; Meneses-Marcel, A.; Machado-Tugores, Y.; Nogal-Ruiz, J.J.; Arán-Redó, V.J.; Escario García-Trevijano, J.A.; Gómez-Barrio, A. Validation of a modified fluorimetric assay for the screening of trichomonacidal drugs. Mem. Inst. Oswaldo Cruz 2012, 107, 637–643. [Google Scholar] [CrossRef]
- Barbosa, T.N.; Silva, M.T.O.; Sena-Lopes, Â.; Kremer, F.S.; Sousa, F.S.S.; Seixas, F.K.; Collares, T.V.; de Pereira, C.M.P.; Borsuk, S. Bioprospection of the trichomonacidal activity of lipid extracts derived from marine macroalgae Gigartina skottsbergii. PLoS ONE 2023, 18, e0285426. [Google Scholar] [CrossRef]
- Tawfeek, G.M.; Elwakil, H.S.; Sarhan, R.M. Ultrastructure-based Insights on Anti-Effects of Selected Egyptian Red Sea Marine Resources. Parasitol. Open 2019, 7, 26–39. [Google Scholar] [CrossRef]
- Martínez-Díaz, R.A.; Ponce-Gordo, F.; Rodríguez-Arce, I.; del Martínez-Herrero, M.C.; González, F.G.; Molina-López, R.Á.; Gómez-Muñoz, M.T. Trichomonas gypaetinii n. sp., a new trichomonad from the upper gastrointestinal tract of scavenging birds of prey. Parasitol. Res. 2015, 114, 101–112. [Google Scholar] [CrossRef] [PubMed]
- Kokoska, L.; Kloucek, P.; Leuner, O.; Novy, P. Plant-derived products as antibacterial and antifungal agents in human health care. Curr. Med. Chem. 2019, 26, 5501–5541. [Google Scholar] [CrossRef] [PubMed]
- Aminkhani, A.; Sharifi, S.; Hosseinzadeh, P. Chemical Constituent, Antimicrobial Activity, and Synergistic Effect of the Stem, Leaf, and Flower Essential Oil of the Artemisia fragrans Willd. from Khoy. Chem. Biodivers. 2021, 18, e2100241. [Google Scholar] [CrossRef]
- Tripathi, J.; Gupta, S.; Gautam, S. Alpha-cadinol as a potential ACE-inhibitory volatile compound identified from Phaseolus vulgaris L. through in vitro and in silico analysis. J. Biomol. Struct. Dyn. 2023, 41, 3847–3861. [Google Scholar] [CrossRef] [PubMed]
- Whesu, O.A.; Ogunbamowo, P.O.; Bankole, S.O.; Awotedu, O.L.; Oyediran, R.I. Antibacterial activity and chemical profiling of Bombax glabrum (Pasq.) A. Robyns leaves. J. Med. Herbs 2021, 12, 57–65. [Google Scholar]
- de Jesús Dzul-Beh, A.; Uc-Cachón, A.H.; González-Sánchez, A.A.; Dzib-Baak, H.E.; Ortiz-Andrade, R.; Barrios-García, H.B.; Jiménez-Delgadillo, B.; Molina-Salinas, G.M. Antimicrobial potential of the Mayan medicine plant Matayba oppositifolia (A. Rich.) Britton against antibiotic-resistant priority pathogens. J. Ethnopharmacol. 2023, 300, 115738. [Google Scholar] [CrossRef] [PubMed]
- Tadigiri, S.; Das, D.; Allen, R.; Vishnu, V.; Veena, S.; Karthikeyan, S. Isolation and characterization of chemical constituents from B. amyloliquefaciens and their nematicidal activity. Mortality 2020, 8, 2062–2066. [Google Scholar]
- Roy, R.N.; Laskar, S.; Sen, S.K. Dibutyl phthalate, the bioactive compound produced by Streptomyces albidoflavus. Microbiol. Res. 2006, 161, 121–126. [Google Scholar] [CrossRef]
- Lifen, H.; Shanying, Z.; Haichen, Z.; Li, P.; Hongyan, W.; Keren, G. Effect of β-sitosterol acetate ester on the structural stability of lipid membrane. Food Mach. 2019, 35, 20–25. [Google Scholar] [CrossRef]
- Pacho Saavedra, J.A.; Piñol Jiménez, F.N. Lesiones bucales relacionadas con las enfermedades digestivas. Rev. Cuba. Estomatol. 2006, 43, 50–57. [Google Scholar]
- Koptur, S.; Palacios-Rios, M.; Díaz-Castelazo, C.; Mackay, W.P.; Rico-Gray, V. Nectar secretion on fern fronds associated with lower levels of herbivore damage: Field experiments with a widespread epiphyte of Mexican cloud forest remnants. Ann. Bot. 2013, 111, 1277–1283. [Google Scholar] [CrossRef] [PubMed]
- Victoriano-Romero, E.; García-Franco, J.G.; Mehltreter, K.; Valencia-Díaz, S.; Toledo-Hernández, V.H.; Flores-Palacios, A. Epiphyte associations and canopy soil volume: Nutrient capital and factors influencing soil retention in the canopy. Plant Biol. 2020, 22, 541–552. [Google Scholar] [CrossRef] [PubMed]
- Sebesta, N.; Jones, I.M.; Lake, E.C. Shorter Note First Report of Foliar Nectar Production by Lygodium microphyllum (Lygodiaceae), an Invasive Fern in Florida. Am. Fern J. 2018, 108, 180–183. [Google Scholar] [CrossRef]
- López Romero, J.M. Respuesta fisiológica al estrés abiótico de gametofitos de helechos del bosque de niebla del centro de Veracruz. Ph.D. Thesis, Biotecnología y Ecología Aplicada Universidad Veracruzana, Xalapa, México, July 2023. [Google Scholar]
- Nitta, T.; Takashi, A.; Takamatsu, A.; Inatomi, Y.; Murata, H.; Iinuma, M.; Tanaka, T.; Ito, T.; Asai, F.; Ibrahim, I.; et al. Antibacterial Activity of Extracts Prepared from Tropical and Subtropical Plants on Methicillin-Resistant Staphylococcus aureus. J. Health Sci. 2002, 48, 273–276. [Google Scholar] [CrossRef]
- Martelli, G.; Giacomini, D. Antibacterial and antioxidant activities for natural and synthetic dual-active compounds. Eur. J. Med. Chem. 2018, 158, 91–105. [Google Scholar] [CrossRef] [PubMed]
- Ashvi, S.J.; Hriday, M.S.; Shreerang, V.J.; Prashant, S.K. Drugs for giardiasis, trichomoniasis, and leishmaniasis. In Medicinal Chemistry of Chemotherapeutic Agents; Elsevier: Amsterdam, The Netherlands, 2023; pp. 431–460. [Google Scholar]
- Schwebke, J.R.; Barrientes, F.J. Prevalence of Trichomonas vaginalis isolates with resistance to metronidazole and tinidazole. Antimicrob. Agents Chemother. 2006, 50, 4209–4210. [Google Scholar] [CrossRef] [PubMed]
- Sorokina, M.; Steinbeck, C. Review on natural products databases: Where to find data in 2020. J. Cheminform. 2020, 12, 20. [Google Scholar] [CrossRef] [PubMed]
- Ziaei Hezarjaribi, H.; Nadeali, N.; Fakhar, M.; Soosaraei, M. Medicinal Plants with Anti-Trichomonas vaginalis Activity in Iran: A Systematic Review. Iran. J. Parasitol. 2019, 14, 1–9. [Google Scholar] [CrossRef]
- Bala, V.; Chhonker, Y.S. Recent developments in anti-Trichomonas research: An update review. Eur. J. Med. Chem. 2018, 143, 232–243. [Google Scholar] [CrossRef]
- Isah, M.B.; Tajuddeen, N.; Ishaq, M.; Aliyu, Z.; Mohammed, A.; Ibrahim, M. Chapter 7—Terpenoids as Emerging Therapeutic Agents: Cellular Targets and Mechanisms of Action against Protozoan Parasites. In Studies in Natural Products Chemistry; Atta, R., Ed.; Elsevier: Amsterdam, The Netherlands, 2018; pp. 227–250. [Google Scholar]
Organ | Extract | Bacterial Strain | ||||||
---|---|---|---|---|---|---|---|---|
A | B | C | D | E | F | G | ||
MIC (μg/mL) | ||||||||
Frond | Hexane | >1500 | >1500 | >1500 | >1500 | >1500 | >1500 | >1500 |
Methanol | >1500 | 747 | 373 | 1500 | 1500 | >1500 | >1500 | |
Aqueous | >1500 | 1500 | >1500 | >1500 | 1500 | >1500 | >1500 | |
Rizome | Hexane | >1500 | >1500 | >1500 | >1500 | >1500 | >1500 | >1500 |
Methanol | >1500 | 1500 | 377 | >1500 | 1500 | >1500 | >1500 | |
Aqueous | >1500 | 1500 | >1500 | >1500 | 1500 | >1500 | >1500 | |
Root | Hexane | ND | ND | ND | ND | ND | ND | ND |
Metanol | >1500 | 747 | >1500 | 1500 | 1500 | >1500 | >1500 | |
Aqueous | >1500 | 1500 | >1500 | >1500 | 1500 | >1500 | >1500 |
Bacteria | MeOH Extract | Hexanic Fraction | Precipitate | MetOH Fraction |
---|---|---|---|---|
MIC (µg/mL) | ||||
Escherichia colli | >1500 | >1500 | >1500 | >1500 |
Salmonella typhimurium | 1000 | 1000 | 1000 | 1000 |
Salmonella typhi | 500 | 1000 | 500 | 500 |
Shigella flexneri | 1000 | 1000 | 500 | 500 |
Staphylococcus aureus | 250 | 1000 | 125 | >1500 |
Bacillus subtilis | >1500 | >1500 | >1500 | >1500 |
Proteus mirabilis | >1500 | >1500 | 1000 | >1500 |
Sample | CI50 [µg/mL] |
---|---|
Frond methanolic extract | >200 |
Methanolic fraction | >200 |
Hexane fraction | 82.3 |
Precipitate fraction | >200 |
MTZ | <4 |
Elution Order | Compound | Retention Time (min) | Formula | Area % | Synonyms |
---|---|---|---|---|---|
1 | Hexadecane | 14.821 | C16H34 | 0.813 | n-Cetane |
2 | α-Cadinol | 15.662 | C15H26O | 0.607 | Cadin-4-en-10-ol |
3 | 1-Octadecene | 16.963 | C18H36 | 3.050 | Octadec-1-ene |
4 | Octadacane | 17.028 | C18H38 | 0.668 | n-Octadecane |
5 | 2-Pentadecanone-6,10,14-trimethyl- | 17.541 | C18H36O | 5.170 | Fitone |
6 | (M)Dibutylphthalate | 18.802 | C16H22O4 | 4.046 | dibutyl benzene-1,2-dicarboxylate |
7 | Eicosane | 19.032 | C20H42 | 0.577 | Icosane |
8 | Docosene | 20.819 | C22H44 | 1.370 | docos-1-ene |
9 | Docosane | 20.858 | C22H46 | 0.473 | n-Docosane |
10 | Bis(2-ethylhexil) phthalate | 24.280 | C24H38O4 | 17.975 | Di(2-ethylhexyl)phthalate |
11 | β-Sitosterol acetate | 29.102 | C31H52O2 | 2.761 | Acetyl-beta-sitosterol |
12 | 7-Dehydrodiosgenin | 31.552 | C27H40O3 | 4.422 | Spirosta-5,7-dien-3-ol |
13 | 3-(1,5-Dimethyl-hexyl)-3a,10,10,12b-tetramethyl-1,2,3,3a,4,6,8,9,10,10a,11,12,12a,12b-tetradecahydro-benzo[4,5]cyclohepta[1,2-E]indene | 35.283 | C30H50 | 11.663 | 1(10),9(11)-B-Homolanistadiene |
14 | Stigmasta-3,5-dien-7-one | 36.964 | C29H46O | 1.471 | Tremulone |
15 | Pregn-16-en-20-one, 3-hydroxy-, [3β,5β]- | 42.167 | C21H32O2 | 44.934 | 16-Pregnenolone |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Anacleto-Santos, J.; Vega-Ávila, E.; Pacheco, L.; Lacueva-Arnedo, M.; Gómez-Barrio, A.; Ibáñez-Escribano, A.; López-Pérez, T.d.J.; Casarrubias-Tabarez, B.; Calzada, F.; López-Camacho, P.Y.; et al. Antibacterial, Trichomonacidal, and Cytotoxic Activities of Pleopeltis crassinervata Extracts. Pharmaceutics 2024, 16, 624. https://doi.org/10.3390/pharmaceutics16050624
Anacleto-Santos J, Vega-Ávila E, Pacheco L, Lacueva-Arnedo M, Gómez-Barrio A, Ibáñez-Escribano A, López-Pérez TdJ, Casarrubias-Tabarez B, Calzada F, López-Camacho PY, et al. Antibacterial, Trichomonacidal, and Cytotoxic Activities of Pleopeltis crassinervata Extracts. Pharmaceutics. 2024; 16(5):624. https://doi.org/10.3390/pharmaceutics16050624
Chicago/Turabian StyleAnacleto-Santos, Jhony, Elisa Vega-Ávila, Leticia Pacheco, Manuel Lacueva-Arnedo, Alicia Gómez-Barrio, Alexandra Ibáñez-Escribano, Teresa de Jesús López-Pérez, Brenda Casarrubias-Tabarez, Fernando Calzada, Perla Yolanda López-Camacho, and et al. 2024. "Antibacterial, Trichomonacidal, and Cytotoxic Activities of Pleopeltis crassinervata Extracts" Pharmaceutics 16, no. 5: 624. https://doi.org/10.3390/pharmaceutics16050624
APA StyleAnacleto-Santos, J., Vega-Ávila, E., Pacheco, L., Lacueva-Arnedo, M., Gómez-Barrio, A., Ibáñez-Escribano, A., López-Pérez, T. d. J., Casarrubias-Tabarez, B., Calzada, F., López-Camacho, P. Y., & Rivera-Fernández, N. (2024). Antibacterial, Trichomonacidal, and Cytotoxic Activities of Pleopeltis crassinervata Extracts. Pharmaceutics, 16(5), 624. https://doi.org/10.3390/pharmaceutics16050624