Evaluation of seeds ethanolic extracts of Triplaris gardneriana Wedd. using in vitro and in vivo toxicological methods

References

• Almeida, T. S., J. J. L. Neto, N. M. de Sousa, I. P. Pessoa, L. R. Vieira, J. L. de Medeiros, A. A. Boligon, A. R. M. Hamers, D. F. Farias, A. Peijnenburg, et al. 2017. Phenolic compounds of Triplaris gardneriana can protect cells against oxidative stress and restore oxidative balance. Biomed. Pharmacother. 93:1261–68. doi:10.1016/j.biopha.2017.07.050.
   PubMed Web of Science ®Google Scholar
• Alminger, M., A.-M. Aura, T. Bohn, C. Dufour, S. N. El, A. Gomes, S. Karakaya, M. C. Martínez-Cuesta, G. J. McDougall, T. Requena, et al. 2014. In vitro models for studying secondary plant metabolite digestion and bioaccessibility. Compr. Rev. Food Sci. Food Saf. 13:413–36. doi:10.1111/1541-4337.12081.
   PubMed Web of Science ®Google Scholar
• Ashrap, P., G. Zheng, Y. Wan, T. Li, W. Hu, W. Li, H. Zhang, Z. Zhang, and J. Hu. 2017. Discovery of a widespread metabolic pathway within and among phenolic xenobiotics. Proc. Natl. Acad. Sci. USA. 114,:6062–67. doi:10.1073/pnas.1700558114.
   PubMed Web of Science ®Google Scholar
• Baumann, E., G. Stoya, A. Völkner, W. Richter, C. Lemke, and W. Linss. 2000. Hemolysis of human erythrocytes with saponin affects the membrane structure. Acta Histochem. 102:21–35. doi:10.1078/0065-1281-00534.
   PubMed Web of Science ®Google Scholar
• Bernheimer, A. W. 1988. Assay of hemolytic toxins. In Methods in enzymology, microbial toxins: Tools in enzymology, 213–17. Academic Press. doi:10.1016/S0076-6879(88)65033-6.
   Google Scholar
• Braga, R. 1976. Plantas do Nordeste, especialmente do Ceará. 3rd ed. Mossoró, Brazil: Escola Superior de Agricultura de Mossoró.
   Google Scholar
• Camones, M. A. I., C. Fuertes Ruiton, B. Jurado Teixeira, I. G. Mondragón Tarrillo, E. D. R. Taype Espinoza, and H. Ostos Flor. 2010. Estudio farmacognóstico, actividad antioxidante y toxicidad a dosis límite de Triplaris americana L. (Tangarana colorada). Revista de la Sociedad Química del Perú 76:34–42.
   Google Scholar
• Cartaxo, S. L., M. M. de Almeida Souza, and U. P. de Albuquerque. 2010. Medicinal plants with bioprospecting potential used in semi-arid northeastern Brazil. J Ethnopharmacol 131:326–42. doi:10.1016/j.jep.2010.07.003.
   PubMed Web of Science ®Google Scholar
• Chen, D.-Q., H. Chen, L. Chen, -D.-D. Tang, H. Miao, and -Y.-Y. Zhao. 2016. Metabolomic application in toxicity evaluation and toxicological biomarker identification of natural product. Chem. Biol. Interact. 252:114–30. doi:10.1016/j.cbi.2016.03.028.
   PubMed Web of Science ®Google Scholar
• Cheok, C. Y., H. A. K. Salman, and R. Sulaiman. 2014. Extraction and quantification of saponins: A review. Food Res. Int. 59:16–40. doi:10.1016/j.foodres.2014.01.057.
   Web of Science ®Google Scholar
• Crozier, A., D. Del Rio, and M. N. Clifford. 2010. Bioavailability of dietary flavonoids and phenolic compounds. Mol. Aspects Med. Phytochem. Cardiovasc. Prot. 31:446–67. doi:10.1016/j.mam.2010.09.007.
   PubMed Web of Science ®Google Scholar
• Da Silva, F. C., J. N. Picada, N. F. Romão, F. O. S. de Sobral, D. Lemos, S. V. de Schons, T. L. de Mello, W. M. Silva, R. S. da Oliveira, C. P. Lucas, et al. 2019. Antigenotoxic and antimutagenic effects of Myrciaria dubia juice in mice submitted to ethanol 28-day treatment. J. Toxicol. Environ. Health A 82:956–68. doi:10.1080/15287394.2019.1671279.
   PubMed Web of Science ®Google Scholar
• De Sousa, J. A., L. S. da Prado, B. L. Alderete, F. B. M. Boaretto, M. C. Allgayer, F. M. Miguel, J. T. De Sousa, N. P. Marroni, M. L. B. Lemes, D. S. Corrêa, et al. 2019. Toxicological aspects of Campomanesia xanthocarpa Berg. associated with its phytochemical profile. J. Toxicol. Environ. Health A 82:62–74. doi:10.1080/15287394.2018.1562392.
   PubMed Web of Science ®Google Scholar
• Eisen, M. B., P. T. Spellman, P. O. Brown, and D. Botstein. 1998. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. U.S.A. 95:14863–68. doi:10.1073/pnas.95.25.14863.
   PubMed Web of Science ®Google Scholar
• Farias, D. F., M. P. Viana, G. R. de Oliveira, M. A. Beneventi, B. M. Soares, C. Pessoa, I. P. Pessoa, L. P. Silva, I. M. Vasconcelos, M. F. de Sá Grossi, et al. 2014. Evaluation of cytotoxic and antimicrobial effects of two Bt Cry proteins on a GMO safety perspective. Biomed. Res. Int. 2014:1–14. doi:10.1155/2014/810490.
   Google Scholar
• Farias, D. F., T. M. Souza, M. P. Viana, B. M. Soares, A. P. Cunha, I. M. Vasconcelos, N. M. P. S. Ricardo, P. M. P. Ferreira, V. M. M. Melo, and A. F. U. Carvalho. 2013. Antibacterial, antioxidant, and anticholinesterase activities of plant seed extracts from Brazilian semiarid region. Biomed. Res. Int. doi:10.1155/2013/510736.
   Web of Science ®Google Scholar
• Filipa Brito, A., M. Ribeiro, A. Margarida Abrantes, A. Salome Pires, R. Jorge Teixo, J. Guilherme Tralhao, and M. Filomena Botelho. 2015. Quercetin in cancer treatment, alone or in combination with conventional therapeutics? Accessed November 28, 2019. https://www.ingentaconnect.com/content/ben/cmc/2015/00000022/00000026/art00003.
   Google Scholar
• Franco, E. S., M. E. B. Mélo, G. C. G. Militão, R. E. T. Rocha, L. T. G. A. Silva, B. J. A. Jatobá, P. B. N. Silva, A. L. B. D. Santana, A. A. R. Silva, T. G. Silva, et al. 2015. Evaluation of the acute toxicity, cytotoxicity, and genotoxicity of Chresta martii (Asteraceae). J. Toxicol. Environ. Health A 78:1083–93. doi:10.1080/15287394.2014.1004007.
   PubMed Web of Science ®Google Scholar
• George, P. 2011. Concerns regarding the safety and toxicity of medicinal plants – An overview. J. Appl. Pharm. Sci. 1:40–44.
   Google Scholar
• Gibellini, L., M. Pinti, M. Nasi, J. P. Montagna, S. De Biasi, E. Roat, L. Bertoncelli, E. L. Cooper, and A. Cossarizza. 2011. Quercetin and cancer chemoprevention. Evidence-Based Comp. Altern. Med. 2011:1–15. doi:10.1093/ecam/neq053.
   Web of Science ®Google Scholar
• Guttula, S. V., A. Allam, and R. S. Gumpeny. 2012. Analyzing microarray data of Alzheimer’s using cluster analysis to identify the biomarker genes. Int. J. Alzheimer’s Dis. 2012:1–5. doi:10.1155/2012/649456.
   Google Scholar
• Hamidi, M. R., B. Jovanova, and T. Kadifkova Panovska. 2014. Toxicological evaluation of the plant products using brine shrimp (Artemia salina L.) model Maced. Pharm. Bull. 60:9–18. doi:10.33320/maced.pharm.bull.2014.60.01.002.
   Google Scholar
• Herwig, R., C. Hardt, M. Lienhard, and A. Kamburov. 2016. Analyzing and interpreting genome data at the network level with ConsensusPathDB. Nat Protoc 11:1889–907. doi:10.1038/nprot.2016.117.
   PubMed Web of Science ®Google Scholar
• Hsieh, C. L., C.-H. Lin, K. C. Chen, -C.-C. Peng, and R. Y. Peng. 2015. The teratogenicity and the action mechanism of gallic acid relating with brain and cervical muscles. PLoS ONE 10:e0119516. doi:10.1371/journal.pone.0119516.
   PubMed Web of Science ®Google Scholar
• Huo, D.-S., J.-F. Sun, Z.-P. Cai, X.-S. Yan, H. Wang, J.-X. Jia, and Z.-J. Yang. 2019. The protective mechanisms underlying Ginsenoside Rg1 effects on rat sciatic nerve injury. J. Toxicol. Environ. Health A 82:1027–35. doi:10.1080/15287394.2019.1684028.
   PubMed Web of Science ®Google Scholar
• Kanehisa, M., Y. Sato, M. Furumichi, K. Morishima, and M. Tanabe. 2018. New approach for understanding genome variations in KEGG. Nucleic Acids Res. 47:D590–D595. doi:10.1093/nar/gky962.
   Web of Science ®Google Scholar
• Lamb, J. 2007. the connectivity map: A new tool for biomedical research. Nat. Rev. Cancer 7:54–60. doi:10.1038/nrc2044.
   PubMed Web of Science ®Google Scholar
• Lamb, J., E. D. Crawford, D. Peck, J. W. Modell, I. C. Blat, M. J. Wrobel, J. Lerner, J.-P. Brunet, A. Subramanian, K. N. Ross, et al. 2006. The connectivity map: Using gene-expression signatures to connect small molecules, genes, and disease. Science 313:1929–35. doi:10.1126/science.1132939.
   PubMed Web of Science ®Google Scholar
• Lee, J., J. Lee, S. J. Kim, and J. H. Kim. 2016. Quercetin-3-O-glucoside suppresses pancreatic cancer cell migration induced by tumor-deteriorated growth factors in vitro. Oncol. Rep. 35:2473–79. doi:10.3892/or.2016.4598.
   PubMed Web of Science ®Google Scholar
• Lee, J. H., H.-B. Lee, G. O. Jung, J. T. Oh, D. E. Park, and K. M. Chae. 2013. Effect of quercetin on apoptosis of PANC-1 cells. J Korean Surg Soc 85:249–60. doi:10.4174/jkss.2013.85.6.249.
   PubMedGoogle Scholar
• Lopes Neto, J. J., T. Silva de Almeida, L. C. P. Almeida Filho, T. M. Rocha, P. A. Nogara, K. F. Nogara, J. B. Teixeira da Rocha, L. K. Almeida Moreira Leal, and A. F. Urano Carvalho. 2020. Triplaris gardneriana seeds extract exhibits in vitro anti-inflammatory properties in human neutrophils after oxidative treatment. J Ethnopharmacol 250:112474. doi:10.1016/j.jep.2019.112474.
   PubMed Web of Science ®Google Scholar
• Lopes Neto, J. J., T. S. Almeida, J. L. Medeiros, L. R. Vieira, T. B. Moreira, A. I. V. Maia, P. R. V. Ribeiro, E. S. Brito, D. F. Farias, and A. F. U. Carvalho. 2017. Impact of bioaccessibility and bioavailability of phenolic compounds in biological systems upon the antioxidant activity of the ethanolic extract of Triplaris gardneriana seeds. Biomed. Pharmacother. 88:999–1007. doi:10.1016/j.biopha.2017.01.109.
   PubMed Web of Science ®Google Scholar
• Mandimika, T., H. Baykus, Y. Vissers, P. Jeurink, J. Poortman, C. Garza, H. Kuiper, and A. Peijnenburg. 2007. Differential gene expression in intestinal epithelial cells induced by single and mixtures of potato glycoalkaloids. J. Agric. Food Chem. 55:10055–66. doi:10.1021/jf0724320.
   PubMed Web of Science ®Google Scholar
• Martins, N., L. Barros, and I. C. F. R. Ferreira. 2016. In vivo antioxidant activity of phenolic compounds: Facts and gaps. Trends Food Sci. Technol. 48:1–12. doi:10.1016/j.tifs.2015.11.008.
   Web of Science ®Google Scholar
• Matos, F. J. A. 1988. Introdução à Fitoquímica Experimental. Fortaleza: UFC edições.
   Google Scholar
• Merker, M. P., and L. Levine. 1986. A protein from the marine mollusc Aplysia californica that is hemolytic and stimulates arachidonic acid metabolism in cultured mammalian cells. Toxicon 24:451–65. doi:10.1016/0041-0101(86)90077-2.
   PubMed Web of Science ®Google Scholar
• Meyer, B. N., N. R. Ferrigni, J. E. Putnam, L. B. Jacobsen, D. E. Nichols, and J. L. McLaughlin. 1982. Brine shrimp: A convenient general bioassay for active plant constituents. Planta Medicina 45:31–34. doi:10.1055/s-2007-971236.
   PubMed Web of Science ®Google Scholar
• OECD 423. 2001. Guideline for testing of chemicals: Acute oral toxicity–acute toxic class method. Guideline. Organization for Economic Cooperation and Development.
   Google Scholar
• Olaru, O. T., L. Venables, M. van de Venter, G. M. Nitulescu, D. Margina, D. A. Spandidos, and A. M. Tsatsakis. 2015. Anticancer potential of selected Fallopia adans species. Oncol Lett 10:1323–32. doi:10.3892/ol.2015.3453.
   PubMed Web of Science ®Google Scholar
• Parshina, E. Y. U., L. Y. A. Gendel, and A. B. Rubin. 2009. Hemolytic activity of hybrid antioxidants Ichphans. Biophysics 54:706–08. doi:10.1134/S0006350909060098.
   Google Scholar
• Peteros, N. P., and M. M. Uy. 2010. Antioxidant and cytotoxic activities and phytochemical screening of four Philippine medicinal plants.Journal of Medicinal Plants Research, 4(5), 407–414.
   Google Scholar
• Robinson, M. D., D. J. McCarthy, and G. K. Smyth. 2010. edgeR: A Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–40. doi:10.1093/bioinformatics/btp616.
   PubMed Web of Science ®Google Scholar
• Rocha, T. A., D. F. de Moura, M. M. da Silva, T. G. Dos Santos Souza, M. A. D. C. de Lira, D. M. de Barros, A. G. da Silva, R. M. Ximenes, E. P. S. da Falcão, C. A. Chagas, et al. 2019. Evaluation of cytotoxic potential, oral toxicity, genotoxicity, and mutagenicity of organic extracts of Pityrocarpa moniliformis. J. Toxicol. Environ. Health A 82:216–31. doi:10.1080/15287394.2019.1576563.
   PubMed Web of Science ®Google Scholar
• Rodríguez, M. I., A. Peralta-Leal, F. O’Valle, J. M. Rodriguez-Vargas, A. Gonzalez-Flores, J. Majuelos-Melguizo, L. López, S. Serrano, A. G. Herreros, J. C. De, Rodríguez-manzaneque, et al. 2013. PARP-1 regulates metastatic melanoma through modulation of vimentin-induced malignant transformation. PLoS Genet. 9:e1003531. doi:10.1371/journal.pgen.1003531.
   PubMed Web of Science ®Google Scholar
• Sahreen, S., M. R. Khan, R. A. Khan, and T. B. Hadda. 2015. Evaluation of phytochemical content, antimicrobial, cytotoxic and antitumor activities of extract from Rumex hastatus D. Don roots. BMC Complement Altern Med 15:211. doi:10.1186/s12906-015-0736-y.
   PubMed Web of Science ®Google Scholar
• Saikia, P., V. Fensterl, and G. C. Sen. 2010. The inhibitory action of P56 on select functions of E1 mediates interferon’s effect on human papillomavirus DNA replication. J. Virol. 84:13036–39. doi:10.1128/JVI.01194-10.
   PubMed Web of Science ®Google Scholar
• Scapagnini, G., D. A. Butterfield, C. Colombrita, R. Sultana, A. Pascale, and V. Calabrese. 2004. Ethyl ferulate, a lipophilic polyphenol, induces HO-1 and protects rat neurons against oxidative stress. Antioxidants and Redox Signaling 6:811–18. doi:10.1089/ars.2004.6.811.
   PubMed Web of Science ®Google Scholar
• Schmeits, P. C. J., M. R. Katika, A. A. C. M. Peijnenburg, H. van Loveren, and P. J. M. Hendriksen. 2014. DON shares a similar mode of action as the ribotoxic stress inducer anisomycin while TBTO shares ER stress patterns with the ER stress inducer thapsigargin based on comparative gene expression profiling in Jurkat T cells. Toxicol. Lett. 224:395–406. doi:10.1016/j.toxlet.2013.11.005.
   PubMed Web of Science ®Google Scholar
• Seo, H.-S., J. M. Ku, H.-S. Choi, Y. K. Choi, J.-K. Woo, M. Kim, I. Kim, C. H. Na, H. Hur, B.-H. Jang, et al. 2016. Quercetin induces caspase-dependent extrinsic apoptosis through inhibition of signal transducer and activator of transcription 3 signaling in HER2-overexpressing BT-474 breast cancer cells. Oncol. Rep. 36:31–42. doi:10.3892/or.2016.4786.
   PubMed Web of Science ®Google Scholar
• Shao, J., L. F. Berger, P. J. M. Hendriksen, A. A. C. M. Peijnenburg, H. van Loveren, and O. L. Volger. 2014. Transcriptome-based functional classifiers for direct immunotoxicity. Arch. Toxicol. 88:673–89. doi:10.1007/s00204-013-1179-1.
   PubMed Web of Science ®Google Scholar
• Sharma, P., and J. D. Sharma. 2001. In vitro hemolysis of human erythrocytes — By plant extracts with antiplasmodial activity. J. Ethnopharmacol. 74:239–43. doi:10.1016/S0378-8741(00)00370-6.
   PubMed Web of Science ®Google Scholar
• Shintyapina, A. B., V. A. Vavilin, O. G. Safronova, and V. V. Lyakhovich. 2017. The gene expression profile of a drug metabolism system and signal transduction pathways in the liver of mice treated with tert-butylhydroquinone or 3-(3ʹ-tert-butyl-4ʹ-hydroxyphenyl)propylthiosulfonate of sodium. PLoS ONE 12:e0176939. doi:10.1371/journal.pone.0176939.
   PubMed Web of Science ®Google Scholar
• Souza, M. S. K., A. T. Dos Santos, F. C. A. Alves, O. A. Paula, A. V. H. Almeida, A. J. R. G. da Silva, S. N. D. Santos, and N. X. Pereira. 2015. Identification of flavonol glycosides and in vitro photoprotective and antioxidant activities of Triplaris gardneriana Wedd. JMPR 9:207–15. doi:10.5897/JMPR2014.5555.
   Google Scholar
• Suwalsky, M., J. Colina, M. J. Gallardo, M. Jemiola-Rzeminska, K. Strzalka, M. Manrique-Moreno, and B. Sepúlveda. 2016. Antioxidant capacity of gallic acid in vitro assayed on human erythrocytes. J. Membr. Biol. 249:769–79. doi:10.1007/s00232-016-9924-z.
   PubMed Web of Science ®Google Scholar
• Tong, W., H. Fang, and D. Mendrick. 2009. Toxicogenomics and cell-based assays for toxicology. Interdiscip. Biol. Cent. 1:10.1–10.5. doi:10.4051/ibc.2009.3.0010.
   Google Scholar
• Waidyanatha, S., E. Mutlu, S. Gibbs, B. Stiffler, J. Andre, B. Burback, and C. V. Rider. 2019. Systemic exposure to Ginkgo biloba extract in male F344/NCrl rats: Relevance to humans. Food Chem. Toxicol. 131:110586. doi:10.1016/j.fct.2019.110586.
   PubMed Web of Science ®Google Scholar
• Wheeler, D. L., T. Barrett, D. A. Benson, S. H. Bryant, K. Canese, V. Chetvernin, D. M. Church, M. DiCuccio, R. Edgar, S. Federhen, et al. 2007. Database resources of the national center for biotechnology information. Nucleic Acids Res. 35:D5–D12. doi:10.1093/nar/gkl1031.
   PubMed Web of Science ®Google Scholar
• Wilson, V. S., N. Keshava, S. Hester, D. Segal, W. Chiu, C. M. Thompson, and S. Y. Euling. 2013. Utilizing toxicogenomic data to understand chemical mechanism of action in risk assessment. Toxicol. Appl. Pharmacol. 271:299–308. doi:10.1016/j.taap.2011.01.017.
   PubMed Web of Science ®Google Scholar
• Xu, C., C. Y.-T. Li, and A.-N. T. Kong. 2005. Induction of phase I, II and III drug metabolism/transport by xenobiotics. Arch. Pharm. Res. 28:249. doi:10.1007/BF02977789.
   PubMed Web of Science ®Google Scholar
• Zhou, X.-L., D. Zeng, Y.-H. Ye, S.-M. Sun, X.-F. Lu, W.-Q. Liang, C.-F. Chen, and H.-Y. Lin. 2018. Prognostic values of the inhibitor of DNA binding family members in breast cancer. Oncol. Rep. 40:1897–906. doi:10.3892/or.2018.6589.
   PubMed Web of Science ®Google Scholar