Biotechnology Research and Innovation Journal
http://www.biori.periodikos.com.br/article/doi/10.4322/biori.00102023
Biotechnology Research and Innovation Journal
Research paper

Antiparasitic activity of lipid extracts from the subantarctic macroalgae Iridea cordata against Trichomonas vaginalis

Tallyson Nogueira Barbosa; Mara Thais de Oliveira Silva; Ângela Sena-Lopes; Frederico Schmitt Kremer; Cláudio Martin Pereira de Pereira; Fernanda Severo Sabedra Sousa; Fabiana Kommling Seixas; Tiago Veiras Collares; Sibele Borsuk

Downloads: 1
Views: 159

Abstract

In this study, we demonstrate the promising antiparasitic activity of natural extracts as an alternative treatment for trichomoniasis. We evaluated the in vitro and in silico antiparasitic activity of Iridea cordata extracts, obtained in two distinct development phases: Iridea cordata tetrasporaphyte phase (IFT) and Iridea cordata cystocarp phase (IFC). To determine the minimum inhibitory concentration (MIC) and 50% inhibitory concentration (IC50), we tested five concentrations of the extracts against Trichomonas vaginalis (ATCC 30236). To gain insights into the mechanisms underlying the antiparasitic activity and possible adverse effects, the extracts were subjected to cytotoxicity assays in VERO and human vaginal epithelial (HVMII) cells, gene expression analyses, and their components’ interactions with T. vaginalis proteins were analyzed through molecular docking. In the in vitro biological assay, IFT and IFC exhibited a MIC of 600 μg/mL while showing an IC50 of 150 μg/mL and 300 μg/mL and inhibiting 80% and 97% of T. vaginalis trophozoites, respectively. Importantly, no cytotoxic effects were observed on VERO and HMVII cells for IFC and IFT at 600 μg/mL, indicating their safety. IFC and IFT induced significant differences in gene expression compared to the negative control, DMSO, and metronidazole, suggesting their potential modulation of T. vaginalis genes. Moreover, in silico analysis revealed that constituents of both extracts interacted, with significant free-binding energy, with proteins that are important for T. vaginalis survival. Overall, this study provides evidence of the antiparasitic activity of Iridea cordata extracts against T. vaginalis and supports further evaluation of its extracts as a promising treatment for trichomoniasis.

Keywords

Natural extracts, Anti-protozoan, Trichomonacidal

References

Alkaabi, H. M., & Almayali, H. M. (2018). Effect of bioactive compounds extracted from green algae Spirogyra sp. in reducing the protoscolices viability in vitro compared with albendazole drug. Journal of Pure & Applied Microbiology, 12(3), 1221-1231. http://dx.doi.org/10.22207/JPAM.12.3.23.

Álvarez-Bardón, M., Pérez-Pertejo, Y., Ordóñez, C., Sepúlveda- Crespo, D., Carballeira, N. M., Tekwani, B. L., Murugesan, S., Martinez-Valladares, M., García-Estrada, C., Reguera, R. M., & Balaña-Fouce, R. (2020). Screening marine natural products for new drug leads against trypanosomatids and malaria. Marine Drugs, 18(4), 1-42. http://dx.doi.org/10.3390/md18040187. PMid:32244488.

Alves, M. S. D., das Neves, R. N., Sena-Lopes, Â., Domingues, M., Casaril, A. M., Segatto, N. V., Nogueira, T. C. M., Souza, M. V. N., Savegnago, L., Seixas, F. K., Collares, T., & Borsuk, S. (2020). Antiparasitic activity of furanyl N-acylhydrazone derivatives against Trichomonas vaginalis: In vitro and in silico analyses. Parasites & Vectors, 13(1), 59. http://dx.doi.org/10.1186/ s13071-020-3923-8. PMid:32046788.

Aquino, M. F. K., Hinderfeld, A. S., & Simoes-Barbosa, A. (2020). Trichomonas vaginalis. Trends in Parasitology, 36(7), 646-647. http://dx.doi.org/10.1016/j.pt.2020.01.010. PMid:32526176.

Atolani, O., Areh, E. T., Oguntoye, O. S., Zubair, M. F., Fabiyi, O. A., Oyegoke, R. A., Tarigha, D. E., Adamu, N., Adeyemi, O. S., Kambizi, L., & Olatunji, G. A. (2019). Chemical composition, antioxidant, anti-lipooxygenase, antimicrobial, anti-parasite and cytotoxic activities of P olyalthia longifolia seed oil. Medicinal Chemistry Research, 28(4), 515-527. http://dx.doi.org/10.1007/ s00044-019-02301-z.

Besednova, N. N., Zaporozhets, T. S., Andryukov, B. G., Kryzhanovsky, S. P., Ermakova, S. P., Kuznetsova, T. A., Voronova, A. N., & Shchelkanov, M. Y. (2021). Antiparasitic effects of sulfated polysaccharides from marine hydrobionts. Marine Drugs, 19(11), 1-25. http://dx.doi.org/10.3390/md19110637. PMid:34822508.

Bligh, E. G., & Dyer, W. J. (1959). A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology, 37(8), 911-917. http://dx.doi.org/10.1139/ o59-099. PMid:13671378.

Brum Vieira, P., Giordani, R. B., Macedo, A. J., & Tasca, T. (2015). Natural and synthetic compound anti-Trichomonas vaginalis: an update review. Parasitology Research, 114(4), 1249-1261. http:// dx.doi.org/10.1007/s00436-015-4340-3. PMid:25786392.

Chellan, P., Stringer, T., Shokar, A., Au, A., Tam, C., Cheng, L. W., Smith, G. S., & Land, K. M. (2019). Antiprotozoal activity of palladium(II) salicylaldiminato thiosemicarbazone complexes on metronidazole resistant Trichomonas vaginalis. Inorganic Chemistry Communications, 102, 1-4. http://dx.doi. org/10.1016/j.inoche.2019.01.033.

Cheng, W. H., Huang, K. Y., Huang, P. J., Hsu, J. H., Fang, Y. K., Chiu, C. H., & Tang, P. (2015). Nitric oxide maintains cell survival of Trichomonas vaginalis upon iron depletion. Parasites & Vectors, 8(1), 393. http://dx.doi.org/10.1186/s13071-015- 1000-5. PMid:26205151.

Deng, L. J., Qi, M., Li, N., Lei, Y. H., Zhang, D. M., & Chen, J. X. (2020). Natural products and their derivatives: Promising modulators of tumor immunotherapy. Journal of Leukocyte Biology, 108(2), 493-508. http://dx.doi.org/10.1002/JLB.3MR0320-444R. PMid:32678943.

Diamond, L. S. (1957). The establishment of various trichomonads of animals and man in axenic cultures. The Journal of Parasitology, 43(4), 488-490. http://dx.doi.org/10.2307/3274682. PMid:13463700.

Ghosh, A. P., Aycock, C., & Schwebke, J. R. (2018). In vitro study of the susceptibility of clinical isolates of Trichomonas vaginalis to metronidazole and secnidazole. Antimicrobial Agents and Chemotherapy, 62(4), 10-1128. http://dx.doi.org/10.1128/ AAC.02329-17. PMid:29439963.

Graves, K. J., Ghosh, A. P., Kissinger, P. J., & Muzny, C. A. (2019). Trichomonas vaginalis virus: a review of the literature. International Journal of STD & AIDS, 30(5), 496-504. http:// dx.doi.org/10.1177/0956462418809767. PMid:30626281.

Ho, C. L. (2020). Comparative genomics reveals differences in algal galactan biosynthesis and related pathways in early and late diverging red algae. Genomics, 112(2), 1536-1544. http://dx.doi. org/10.1016/j.ygeno.2019.09.002. PMid:31494197.

Hopper, M., Yun, J. F., Zhou, B., Le, C., Kehoe, K., Le, R., Hill, R., Jongeward, G., Debnath, A., Zhang, L., Miyamoto, Y., Eckmann, L., Land, K. M., & Wrischnik, L. A. (2016). Auranofin inactivates Trichomonas vaginalis thioredoxin reductase and is effective against trichomonads in vitro and in vivo. International Journal of Antimicrobial Agents, 48(6), 690-694. http://dx.doi. org/10.1016/j.ijantimicag.2016.09.020. PMid:27839893.

Hübner, D. P. G., de Brum Vieira, P., Frasson, A. P., Menezes, C. B., Senger, F. R., Santos da Silva, G. N., Baggio Gnoatto, S. C., & Tasca, T. (2016). Anti-Trichomonas vaginalis activity of betulinic acid derivatives. Biomedicine and Pharmacotherapy, 84, 476-484. http://dx.doi.org/10.1016/j.biopha.2016.09.064. PMid:27685791.

Jofre, J., Celis-Plá, P. S. M., Figueroa, F. L., & Navarro, N. P. (2020). Seasonal variation of mycosporine-like amino acids in three subantarctic red seaweeds. Marine Drugs, 18(2), 1-17. http:// dx.doi.org/10.3390/md18020075. PMid:31991623.

Leitsch, D. (2021). Recent advances in the molecular biology of the protist parasite Trichomonas vaginalis. Faculty Reviews, 10(26), 26. http://dx.doi.org/10.12703/r/10-26. PMid:33718943.

Li, M. M., Jiang, Z., Song, L. Y., Quan, Z. S., & Yu, H. L. (2017). Antidepressant and anxiolytic-like behavioral effects of erucamide, a bioactive fatty acid amide, involving the hypothalamus–pituitary– adrenal axis in mice. Neuroscience Letters, 640, 6-12. http:// dx.doi.org/10.1016/j.neulet.2016.12.072. PMid:28082151.

Martínez–Hernández, G. B., Castillejo, N., Carrión–Monteagudo, M. del M., Artés, F., & Artés-Hernández, F. (2018). Nutritional and bioactive compounds of commercialized algae powders used as food supplements. Food Science & Technology International, 24(2), 172-182. http://dx.doi.org/10.1177/1082013217740000. PMid:29110539.

Mayer, A. M. S., Guerrero, A. J., Rodríguez, A. D., Taglialatela-scafati, O., Nakamura, F., & Fusetani, N. (2021). Marine pharmacology in 2016–2017: Marine compounds with antibacterial, antidiabetic, antifungal, anti-inflammatory, antiprotozoal, antituberculosis and antiviral activities, affecting the immune and nervous systems, and other miscellaneous mechanisms of action. Marine Drugs, 19(2), 49. http://dx.doi.org/10.3390/md19020049. PMid:33494402.

Mead, J. R., Fernadez, M., Romagnoli, P. A., & Secor, W. E. (2006). Use of Trichomonas vaginalis clinical isolates to evaluate correlation of gene expression and metronidazole resistance. The Journal of Parasitology, 92(1), 196-199. http://dx.doi.org/10.1645/ GE-616R.1. PMid:16629339.

Mekinić, I. G., Skroza, D., Šimat, V., Hamed, I., Čagalj, M., & Perković, Z. P. (2019). Phenolic content of brown algae (Pheophyceae) species: Extraction, identification, and quantification. Biomolecules, 9(6), 244. http://dx.doi.org/10.3390/biom9060244. PMid:31234538.

Mendes, L. B. P., Monteiro, L. P. C., & Pontual, L. V. (2020). Avaliação da degradação fotocatalítica do metronidazol em solução aquosa utilizando espectrofotometria. Brazilian Journal of Development, 6(8), 56821-56834. http://dx.doi.org/10.34117/bjdv6n8-189.

Mercer, F., & Johnson, P. J. (2018). Trichomonas vaginalis: Pathogenesis, symbiont interactions, and host cell immune responses. Trends in Parasitology, 34(8), 683-693. http://dx.doi. org/10.1016/j.pt.2018.05.006. PMid:30056833.

Morris, G. M., Ruth, H., Lindstrom, W., Sanner, M. F., Belew, R. K., Goodsell, D. S., & Olson, A. J. (2009). Software news and updates AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility. Journal of Computational Chemistry, 30(16), 2785-2791. http://dx.doi.org/10.1002/jcc.21256. PMid:19399780.

Moss, C. W., Lambert, M. A., & Merwin, W. H. (1974). Comparison of rapid methods for analysis of bacterial fatty acids. Applied Microbiology, 28(1), 80-85. http://dx.doi.org/10.1128/ am.28.1.80-85.1974. PMid:4844271.

Navarrete-Vázquez, G., Chávez-Silva, F., Colín-Lozano, B., Estrada-Soto, S., Hidalgo-Figueroa, S., Guerrero-Álvarez, J., Méndez, S. T., Reyes-Vivas, H., Oria-Hernández, J., Canul- Canché, J., Ortiz-Andrade, R., & Moo-Puc, R. (2015). Synthesis of nitro(benzo)thiazole acetamides and in vitro antiprotozoal effect against amitochondriate parasites Giardia intestinalis and Trichomonas vaginalis. Bioorganic & Medicinal Chemistry, 23(9), 2204-2210. http://dx.doi.org/10.1016/j.bmc.2015.02.059. PMid:25801157.

Nemati, M., Malla, N., Yadav, M., Khorramdelazad, H., & Jafarzadeh, A. (2018). Humoral and T cell–mediated immune response against trichomoniasis. Parasite Immunology, 40(3), 1-11. http://dx.doi. org/10.1111/pim.12510. PMid:29266263.

Neves, R. N., Sena-Lopes, Â., Alves, M. S. D., Rocha Fonseca, B., Silva, C. C., Casaril, A. M., Savegnago, L., Pereira, C. M. P., Ramos, D. F., & Borsuk, S. (2020). Hydroxychalcones as an alternative treatment for trichomoniasis in association with metronidazole. Parasitology Research, 119(2), 725-736. http://dx.doi.org/10.1007/s00436- 019-06568-4. PMid:31853622.

O’Boyle, N. M., Banck, M., James, C. A., Morley, C., Vandermeersch, T., & Hutchison, G. R. (2011). Open Babel: an open chemical toolbo. Journal of Cheminformatics, 3, 33. PMid:21982300. Ozpinar, H., Ozpinar, N., & Eruygur, N. (2019). Effect of Viscum album L. ssp. austriacum (WİESP.) Vollman on metronidazole resistant and sensitive strains of Trichomonas vaginalis. South African Journal of Botany, 125, 81-85. http://dx.doi.org/10.1016/j. sajb.2019.07.008.

Pacheco, B. S., Santos, M. A. Z., Schultze, E., Martins, R. M., Lund, R. G., Seixas, F. K., Colepicolo, P., Collares, T., Paula, F. R., & Pereira, C. M. P. (2018). Cytotoxic activity of fatty acids from Antarctic macroalgae on the growth of human breast cancer cells. Frontiers in Bioengineering and Biotechnology, 6, 185. http://dx.doi.org/10.3389/fbioe.2018.00185. PMid:30560124.

Patel, E. U., Gaydos, C. A., Packman, Z. R., Quinn, T. C., & Tobian, A. A. R. (2018). Prevalence and correlates of Trichomonas vaginalis infection among men and women in the United States. Clinical Infectious Diseases, 67(2), 211-217. http://dx.doi.org/10.1093/ cid/ciy079. PMid:29554238.

Pineda-Alegría, J. A., Sánchez, J. E., González-Cortazar, M., von Son-de Fernex, E., González-Garduño, R., Mendoza-de Gives, P., Zamilpa, A., & Aguilar-Marcelino, L. (2020). In vitro nematocidal activity of commercial fatty acids and β-sitosterol against Haemonchus contortus. Journal of Helminthology, 94, e135. http://dx.doi.org/10.1017/S0022149X20000152. PMid:32127057.

Rada, P., Kellerová, P., Verner, Z., & Tachezy, J. (2019). Investigation of the secretory pathway in trichomonas vaginalis argues against a moonlighting function of hydrogenosomal enzymes. The Journal of Eukaryotic Microbiology, 66(6), 899-910. http://dx.doi. org/10.1111/jeu.12741. PMid:31077495.

Ryan, C. M., Miguel, N. D., & Johnson, P. J. (2011). Trichomonas vaginalis: current understanding of host–parasite interactions. Essays in Biochemistry, 51, 161-175. http://dx.doi.org/10.1042/ bse0510161. PMid:22023448.

Sánchez-Camargo, A. D., Montero, L., Stiger-Pouvreau, V., Tanniou, A., Cifuentes, A., Herrero, M., & Ibáñez, E. (2016). Considerations on the use of enzyme-assisted extraction in combination with pressurized liquids to recover bioactive compounds from algae. Food Chemistry, 192, 67-74. http://dx.doi.org/10.1016/j. foodchem.2015.06.098. PMid:26304321.

Santos, O., Vargas Rigo, G., Frasson, A. P., Macedo, A. J., & Tasca, T. (2015). Optimal reference genes for gene expression normalization in Trichomonas vaginalis. PLoS One, 10(9), e0138331. http:// dx.doi.org/10.1371/journal.pone.0138331. PMid:26393928.

Sena-Lopes, Â., das Neves, R. N., Bezerra, F. S. B., de Oliveira Silva, M. T., Nobre, P. C., Perin, G., Alves, D., Savegnago, L., Begnini, K. R., Seixas, F. K., Collares, T., & Borsuk, S. (2017). Antiparasitic activity of 1,3-dioxolanes containing tellurium in Trichomonas vaginalis. Biomedicine and Pharmacotherapy, 89, 284-287. http://dx.doi.org/10.1016/j.biopha.2017.01.173. PMid:28236702.

Setzer, M. S., Byler, K. G., Ogungbe, I. V., & Setzer, W. N. (2017). Natural products as new treatment options for trichomoniasis: A molecular docking investigation. Scientia Pharmaceutica, 85(1), 5. http://dx.doi.org/10.3390/scipharm85010005. PMid:28134827.

Singh, G., Satija, P., Singh, A., Sanchita, Aulakh, D., Wriedt, M., Ruiz, C. E., Esteban, M. A., Sinha, S., & Sehgal, R. (2019). Synthesis and characterization of microwave-assisted biologically active triazole silanes. Applied Organometallic Chemistry, 33(5), 1-15. http://dx.doi.org/10.1002/aoc.4695.

Trein, M. R., Rodrigues, E., Oliveira, L., Rigo, G. V., Garcia, M. A. R., Petro-Silveira, B., da Silva Trentin, D., Macedo, A. J., Regasini, L. O., & Tasca, T. (2019). Anti-Trichomonas vaginalis activity of chalcone and amino-analogues. Parasitology Research, 118(2), 607-615. http://dx.doi.org/10.1007/s00436-018-6164-4. PMid:30535524.

Trott, O., & Olson, A. J. (2010). AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. Journal of Computational Chemistry, 31(2), 455-461. http://dx.doi.org/10.1002/jcc.21334. PMid:19499576.

Yang, J., Roy, A., & Zhang, Y. (2013). Protein-ligand binding site recognition using complementary binding-specific substructure comparison and sequence profile alignment. Bioinformatics (Oxford, England), 29(20), 2588-2595. http://dx.doi.org/10.1093/ bioinformatics/btt447. PMid:23975762.

Yang, Y., He, P. Y., Zhang, Y., & Li, N. (2020). Natural products targeting the mitochondria in cancers. Molecules (Basel, Switzerland), 26(1), 92. http://dx.doi.org/10.3390/molecules26010092. PMid:33379233.

Zhang, H., Wang, Z., & Liu, O. (2015). Development and validation of a GC-FID method for quantitative analysis of oleic acid and related fatty acids. Journal of Pharmaceutical Analysis, 5(4), 223-230. http://dx.doi.org/10.1016/j.jpha.2015.01.005. PMid:29403935.

Zhao, M., Xu, W. F., Shen, H. Y., Shen, P. Q., Zhang, J., Wang, D. D., Xu, H., Wang, H., Yan, T. T., Wang, L., Hao, H. P., Wang, G. J., & Cao, L. J. (2017). Comparison of bioactive components and pharmacological activities of ophiopogon japonicas extracts from different geographical origins. Journal of Pharmaceutical and Biomedical Analysis, 138, 134-141. http://dx.doi.org/10.1016/j. jpba.2017.02.013. PMid:28196345.

Ziaei Hezarjaribi, H., Nadeali, N., Fakhar, M., & Soosaraei, M. (2019). Medicinal plants with anti-Trichomonas vaginalis activity in Iran: a systematic review. Iranian Journal of Parasitology, 14(1), 1-9.


Submitted date:
04/12/2023

Accepted date:
06/26/2023

65303c1aa9539514997c6572 biori Articles
Links & Downloads

BIORI

Share this page
Page Sections