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Research Article

Preventive activity of Copaifera langsdorffii Desf. leaves extract and its major compounds, afzelin and quercitrin, on DNA damage in in vitro and in vivo models

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References

  • Abrão, F., L. D. De-Araújo-Costa, J. M. Alves, J. M. Senedese, P. T. De-Castro, S. R. Ambrósio, R. C. Veneziani, J. K. Bastos, D. C. Tavares, and C. H. G. Martins. 2015. Copaifera langsdorffii oleoresin and its isolated compounds: Antibacterial effect and antiproliferative activity in cancer cell lines. BMC Complem. Altern. M. 15:1–10. doi:10.1186/s12906-015-0961-4.
  • Agrawal, P. K. 1989. Carbon-13 NMR of Flavonoids. 1st ed. Netherlands: Elsevier.
  • Alves, J. M., C. C. Munari, M. A. B. Monteiro-Neto, R. A. Furtado, J. M. Senedese, J. K. Bastos, and D. C. Tavares. 2013. In vivo protective effect of Copaifera langsdorffii hydroalcoholic extract on micronuclei induction by doxorubicin. J. Appl. Toxicol. 33:854–60. doi:10.1002/jat.2777.
  • Arruda, C., J. A. A. Mejía, V. P. Ribeiro, C. H. G. Borges, C. H. G. Martins, R. C. S. Veneziani, S. R. Ambrósio, and J. K. Bastos. 2019. Occurrence, chemical composition, biological activities and analytical methods on Copaifera genus – A review. Biomed. Pharmacother. 109:1–20. doi:10.1016/j.biopha.2018.10.030.
  • Bernstein, L., J. Kaldor, J. Mccann, and M. C. Pike. 1982. An empirical approach to the statistical analysis of mutagenesis data from the Salmonella test. Mutat. Res. 97:267–81. doi:10.1016/0165-1161(82)90026-7.
  • Brancalion, A. P., R. B. Oliveira, J. P. Sousa, M. Groppo, A. A. Berretta, M. E. Barros, M. A. Boim, and J. K. Bastos. 2012. Effect of hydroalcoholic extract from Copaifera langsdorffii leaves on urolithiasis induced in rats. Urol. Res. 40:475–81. doi:10.1007/s00240-011-0453-z.
  • Burlinson, B., R. R. Tice, G. Speit, E. Agurell, S. Y. Brendler-Schwaab, A. W. Collins, P. Escobar, M. Honma, T. S. Kumaravel, M. Nakajima, et al. 2007. Fourth International Workgroup on Genotoxicity testing: Results of the in vivo Comet assay workgroup. Mutat. Res. 627:31–35. doi:10.1016/j.mrgentox.2006.08.011.
  • Caesar, L. K., and N. B. Cech. 2019. Synergy and antagonism in natural product extracts: When 1 + 1 does not equal 2. Nat. Prod. Rep. 36:869–88. doi:10.1039/c9np00011a.
  • Campbell, J. K., J. L. King, M. Harmston, M. A. Lila, and J. W. Erdman-Jr. 2006. Synergistic effects of flavonoids on cell proliferation in Hepa-1c1c7 and LNCaP cancer cell lines. J. Food Sci. 71:S358–S363. doi:10.1111/j.1750-3841.2006.00013.x.
  • Cao, P., J. Cai, and R. C. Gupta. 2010. Effect of green tea catechins and hydrolyzable tannins on benzo[a]pyrene-induced DNA adducts and structure-activity relationship. Chem. Res. Toxicol. 23:771–77. doi:10.1021/tx900412a.
  • Dabeek, W. M., and M. V. Marra. 2019. Dietary quercetin and kaempferol: Bioavailability and potential cardiovascular-related bioactivity in humans. Nutrients 11:2288. doi:10.3390/nu11102288.
  • Dutra, R. C., M. M. Campos, A. R. S. Santos, and J. B. Calixto. 2016. Medicinal plants in Brazil: Pharmacological studies, drug discovery, challenges and perspectives. Pharmacol. Res. 112:4–29. doi:10.1016/j.phrs.2016.01.021.
  • Franken, N. A. P., H. M. Rodermond, J. Stap, J. Haveman, and C. Van-Bree. 2006. Clonogenic assay of cells in vitro. Nat. Protoc. 1:2315–19. doi:10.1038/nprot.2006.339.
  • Furtado, R. A., P. F. Oliveira, J. M. Senedese, S. D. Ozelin, L. D. R. Souza, L. F. Leandro, W. L. Oliveira, J. J. M. Silva, L. C. Oliveira, H. Rogez, et al. 2018. Assessment of genotoxic activity of oleoresins and leaves extracts of six Copaifera species for prediction of potential human risks. J. Ethnopharmacol. 221:119–25. doi:10.1016/j.jep.2018.04.002.
  • Guo, X., J. E. Seo, X. Li, and N. Mei. 2020. Genetic toxicity assessment using liver cell models: Past, present, and future. J. Toxicol. Environ. Health B 23:27–50. doi:10.1080/10937404.2019.1692744.
  • Haque, M. E., S. Azam, R. Balakrishnan, M. Akther, and I. S. Kim. 2020. Therapeutic potential of Lindera obtusiloba: Focus on antioxidative and pharmacological properties. Plants 9:1765. doi:10.3390/plants9121765.
  • Hong, C. O., H. A. Lee, C. H. Rhee, S. Y. Choung, and K. W. Lee. 2013. Separation of the antioxidant compound quercitrin from Lindera obtusiloba Blume and its antimelanogenic effect on B16F10 melanoma cells. Biosci. Biotech. Biochem. 77:58–64. doi:10.1271/bbb.120562.
  • ICH S2(R1). 2011. Guidance on Genotoxicity Testing and Data Interpretation for Pharmaceuticals Intended for Human Use. https://www.ich.org/page/safety-guidelines.
  • Imran, M., B. Salehi, J. Sharifi-Rad, T. A. Gondal, F. Saeed, A. Imran, M. Shahbaz, P. V. T. Fokou, M. U. Arshad, H. Khan, et al. 2019. Kaempferol: A key emphasis to its anticancer potential. Molecules 24:2277. doi:10.3390/molecules24122277.
  • Kumar, S., and A. K. Pandey. 2013. Chemistry and biological activities of flavonoids: An overview. Sci. World J. 2013:162750. doi:10.1155/2013/162750.
  • Lamy, E., F. Kassie, R. Gminski, H. H. Schmeiser, and V. Mersch-Sundermann. 2004. 3-Nitrobenzanthrone (3-NBA) induced micronucleus formation and DNA damage in human hepatoma (HepG2) cells. Toxicol. Lett. 146:103–09. doi:10.1016/j.toxlet.2003.07.001.
  • Lemos, M., J. R. Santin, C. S. Mizuno, T. Boeing, J. P. B. Sousa, D. Nanayakkara, J. K. Bastos, and S. F. Andrade. 2015. Copaifera langsdorffii: Evaluation of potential gastroprotective of extract and isolated compounds obtained from leaves. Rev. Bras. Farmacogn. 25:238–45. doi:10.1016/j.bjp.2015.05.005.
  • Loh, D. S. Y., H. M. Er, and Y. S. Chen. 2009. Mutagenic and antimutagenic activities of aqueous and methanol extracts of Euphorbia hirta. J. Ethnopharmacol. 126:406–14. doi:10.1016/j.jep.2009.09.025.
  • MacGregor, J. T., J. A. Heddle, M. Hite, B. H. Margolin, C. Ramel, M. F. Salamone, R. R. Tice, and D. Wild. 1987. Guidelines for the conduct of micronucleus assay in mammalian bone marrow erythrocytes. Mutat. Res. 189:103–12. doi:10.1016/0165-1218(87)90016-4.
  • Maron, D. M., and B. N. Ames. 1983. Revised methods for the Salmonella mutagenicity test. Mutat. Res. 113:173–215. doi:10.1016/0165-1161(83)90010-9.
  • Miura, T., S. Muraoka, and T. Ogiso. 1995. Adriamycin-Fe3+-induced mitochondrial protein damage with lipid peroxidation. Biol. Pharm. Bull. 18:514–17. doi:10.1248/bpb.18.514.
  • Moon, Y. J., X. Wang, and M. E. Morris. 2006. Dietary flavonoids: Effects on xenobiotic and carcinogen metabolism. Toxicol. In Vitro. 20:187–210. doi:10.1016/j.tiv.2005.06.048.
  • Motta, E. V. S., J. C. Costa, and J. K. Bastos. 2017b. A validated HPLC-UV method for the analysis of galloylquinic acid derivatives and flavonoids in Copaifera langsdorffii leaves. J. Chromatog. B. 1061–1062:240–47. doi:10.1016/j.jchromb.2017.07.027.
  • Motta, E. V. S., M. Lemos, J. C. Costa, V. C. Banderó-Filho, A. Sasse, H. Sheridan, and J. K. Bastos. 2017a. Galloylquinic acid derivatives from Copaifera langsdorffii leaves display gastroprotective activity. Chem-Biol. Interact. 261:145–55. doi:10.1016/j.cbi.2016.11.028.
  • Munari, C. C., P. F. Oliveira, I. M. S. Lima, S. P. L. Martins, J. C. Costa, J. K. Bastos, and D. C. Tavares. 2012. Evaluation of cytotoxic, genotoxic and antigenotoxic potential of Solanum lycocarpum fruits glicoalkaloid extract in V79 cells. Food Chem. Toxicol. 50:3696–701. doi:10.1016/j.fct.2012.07.028.
  • Munari, C. C., F. A. Resende, J. M. Alves, J. P. B. Sousa, J. K. Bastos, and D. C. Tavares. 2008. Mutagenicity and antimutagenicity of Baccharis dracunculifolia extract in chromosomal aberration assays in Chinese hamster ovary cells. Planta Med. 74:1363–67. doi:10.1055/s-2008-1081306.
  • Newman, D. J., and G. M. Cragg. 2020. Natural products as sources of new drugs over the nearly four decades from 01/1981 to 09/2019. J. Nat. Prod. 73:770–803. doi:10.1021/acs.jnatprod.9b01285.
  • Nogueira, M. S., R. A. Furtado, and J. K. Bastos. 2015. Flavonoids and methoxy galloylquinic acid derivatives from the leaf extract of Copaifera langsdorffii Desf. J. Agric. Food Chem. 63:6939–45. doi:10.1021/acs.jafc.5b01588.
  • OECD. 2013. Test No. 474: Mammalian Erythrocyte Micronucleus Test, OECD Guidelines for the Testing of Chemicals, Section 4. Paris: OECD Publishing. doi:10.1787/9789264264762-en.
  • OECD. 2016. Test No. 487: In Vitro Mammalian Cell Micronucleus Test, OECD Guidelines for the Testing of Chemicals, Section 4. Paris: OECD Publishing. doi:10.1787/9789264264861-en.
  • Resende, F. A., L. C. Barbosa, D. C. Tavares, M. S. Camargo, K. C. S. Rezende, M. L. A. Silva, and E. A. Varanda. 2012a. Mutagenicity and antimutagenicity of (−)-hinokinin a trypanosomicidal compound measured by Salmonella microsome and comet assays. BMC Complem. Altern. Med. 12:1–10. doi:10.1186/1472-6882-12-203.
  • Resende, F. A., C. C. Munari, M. A. B. Monteiro-Neto, D. C. Tavares, J. K. Bastos, A. A. Silva-Filho, and E. A. Varanda. 2012b. Comparative studies of the (anti) mutagenicity of Baccharis dracunculifolia and artepillin C by the bacterial reverse mutation test. Molecules 17:2335–50. doi:10.3390/molecules17032335.
  • Resende, F. A., I. M. Tomazella, L. C. Barbosa, M. Ponce, R. A. Furtado, A. C. Pereira, J. K. Bastos, M. L. A. Silva, and D. C. Tavares. 2010. Effect of the dibenzylbutyrolactone lignan (-)-hinokinin on doxorubicin and methyl methanesulfonate clastogenicity in V79 Chinese hamster lung fibroblasts. Mutation Res. 700:62–66. doi:10.1016/j.mrgentox.2010.04.023.
  • Santos, F. V., I. M. S. Colus, M. A. Silva, W. Vilegas, and E. A. Varanda. 2006. Assessment of DNA damage induced by extracts and fractions of Strychnos pseudoquina, a Brazilian medicinal plant with antiulcerogenic activity. Food Chem. Toxicol. 44:1585–89. doi:10.1016/j.fct.2006.03.012.
  • Sasaki, Y. F., S. Tsuda, F. Izumiyama, and E. Nishidate. 1997. Detection of chemically induced DNA lesions in multiple mouse organs (liver, lung, spleen, kidney, and bone marrow) using the alkaline single-cell gel electrophoresis (comet) assay. Mutat. Res. 388:33–44. doi:10.1016/s1383-5718(96)00133-7.
  • Senedese, J. M., J. M. Alves, I. M. S. Lima, E. A. P. Andrade, R. A. Furtado, J. K. Bastos, and D. C. Tavares. 2013. Chemopreventive effect of Copaifera langsdorffii leaves hydroalcoholic extract on 1,2-dimethylhydrazine-induced DNA damage and preneoplastic lesions in rat colon. BMC Complem. Altern. Med. 13:2–8. doi:10.1186/1472-6882-13-3.
  • Silva, J. N., N. B. N. Moncao, R. R. S. Farias, A. M. G. L. Cito, M. H. Chaves, M. R. S. Araujo, D. J. B. Lima, C. Pessoa, A. Lima, E. C. C. Araujo, et al. 2020. Toxicological, chemopreventive and cytotoxic potentialities of rare vegetal species and supporting findings for the Brazilian Unified Health System (SUS). J. Toxicol. Environ. Health A. 83:525–45. doi:10.1080/15287394.2020.1780658.
  • Singh, N. P., M. T. Mccoy, R. R. Tice, and E. L. Schneider. 1988. A simple technique for quantification of low levels of DNA damage in individual cells. Exp. Cell Res. 175:184–91. doi:10.1016/0014-4827(88)90265-0.
  • Sousa, J. P. B., A. P. S. Brancalion, M. G. Junior, and J. K. Bastos. 2012. A validated chromatographic method for the determination of flavonoids in Copaifera langsdorffii by HPLC. Nat. Prod. Commun. 7:25–28. doi:10.1177/1934578x1200700110.
  • Tsuboy, M. S., J. P. F. Angeli, M. S. Mantovani, S. Knasmüller, G. A. Umbuzeiro, and L. R. Ribeiro. 2007. Genotoxic, mutagenic and cytotoxic effects of the commercial dye CI disperse blue 291 in the human hepatic cell line HepG2. Toxicol. In Vitro. 21:1650–55. doi:10.1016/j.tiv.2007.06.020.
  • Venancio, V. P., M. C. Marques, M. R. Almeida, L. R. B. Mariutti, V. C. O. Souza, F. Barbosa-Jr, M. L. P. Bianchi, C. M. Marzocchi-Machado, A. Z. Mercadante, and L. M. G. Antunes. 2016. Chrysobalanus icaco L. fruits inhibit NADPH oxidase complex and protect DNA against doxorubicin-induced damage in Wistar male rats. J. Toxicol. Environ. Health A 79:885–93. doi:10.1080/15287394.2016.1193454.
  • Zanotto-Filho, A., V. P. Masamsetti, E. Loranc, S. S. Tonapi, A. Gorthi, X. Bernard, R. M. Gonçalves, J. C. F. Moreira, Y. Chen, and A. J. R. Bishop. 2016. Alkylating agent-induced NRF2 blocks endoplasmic reticulum stress–mediated apoptosis via control of glutathione pools and protein thiol homeostasis. Mol. Cancer Ther. 15:3000–14. doi:10.1158/1535-7163.mct-16-0271.

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