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Articles

Usnic acid attenuates genomic instability in Chinese hamster ovary (CHO) cells as well as chemical-induced preneoplastic lesions in rat colon

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References

  • Acésio, N. O., G. S. Carrijo, T. H. Batista, J. L. Damasceno, M. B. Côrrea, M. G. Tozatti, and D. C. Tavares. 2017. Assessment of the antioxidant, cytotoxic, and genotoxic potential of the Annona muricata leaves and their influence on genomic stability. J. Toxicol. Environ. Health A 80:1290–300. doi:10.1080/15287394.2017.1377653.
  • Benetou, V., A. Lagiou, and P. Lagiou. 2015. Chemoprevention of cancer: Current evidence and future prospects. F1000Research 4:1–10. doi:10.12688/f1000research.5779.5.
  • Bird, R. P. 1987. Observation and quantification of aberrant crypts in the murine colon treated with a colon carcinogen: Preliminary findings. Cancer Lett. 37:147–51.
  • Bolton, J. L., T. L. Dunlap, and B. M. Dietz. 2018. Formation and biological targets of botanical o-quinones. Food Chem. Toxicol. 120:700–07. doi:10.1016/j.fct.2018.07.050.
  • Chang, W. W. 1984. Histogenesis of colon cancer in experimental animals. Scand. J. Gastroenterol. Suppl. 104:27–43.
  • Chen, S., V. N. Dobrovolsky, F. Liu, Y. Wu, Z. Zhang, N. Mei, and L. Guo. 2014. The role of autophagy in usnic acid-induced toxicity in hepatic cells. Toxicol. Sc. 142:33–44. doi:10.1093/toxsci/kfu154.
  • Chen, S., Z. Zhang, T. Qing, Z. Ren, D. Yu, L. Couch, and L. Guo. 2017. Activation of the Nrf2 signaling pathway in usnic acid-induced toxicity in HepG2 cells. Arch. Toxicol. 91:1293–307. doi:10.1007/s00204-016-1775-y.
  • Choudhary, G., and H. Hansen. 1998. Human health perspective of environmental exposure to hydrazines: A review. Chemosphere 37:801–43.
  • Cocchietto, M., N. Skert, P. Nimis, and G. Sava. 2002. A review on usnic acid, an interesting natural compound. Naturwissenschaften 8:137–46. doi:10.1007/s00114-002-0305-3.
  • Dylawerska, A., W. Barczak, A. Wegner, W. Golusinski, and W. M. Suchorska. 2017. Association of DNA repair genes polymorphisms and mutations with increased risk of head and neck cancer: A review. J. Med. Oncol. 34:197–204. doi:10.1007/s12032-017-1057-4.
  • Eastmond, D. A., and J. D. Tucker. 1989. Identification of aneuploidy-inducing agents using cytokinesis-blocked human lymphocytes and an antikinetochore antibody. Environ. Mol. Mutagen. 13:34–43.
  • Erexson, G. L., M. V. Periago, and C. S. Spicer. 2001. Differential sensitivity of Chinese hamster V79 and Chinese hamster ovary (CHO) cells in the in vitro micronucleus screening assay. Mutat. Res. 495:75–80. doi:10.1016/S1383-5718(01)00199-1.
  • Fenech, M. 2000. The in vitro micronucleus technique. Mutat. Res. 455:81–95. doi:10.1016/S0027-5107(00)00065-8.
  • Fernández-Moriano, C., P. K. Divakar, A. Crespo, and M. P. Gómez-Serranillos. 2017. Protective effects of lichen metabolites evernic and usnic acids against redox impairment-mediated cytotoxicity in central nervous system-like cells. Food Chem. Toxicol. 105:262–77. doi:10.1016/j.fct.2017.04.030.
  • Finn, N. A., H. W. Findley, and M. L. Kemp. 2011. A switching mechanism in doxorubicin bioactivation can be exploited to control doxorubicin toxicity. PLoS Comput. Biol. 7:e1002151. doi:10.1371/journal.pcbi.1002244.
  • Forman, H. J., K. J. Davies, and F. Ursini. 2014. How do nutritional antioxidants really work: Nucleophilic tone and para-hormesis versus free radical scavenging in vivo. Free Radic. Biol. Med. 66:24–35. doi:10.1016/j.freeradbiomed.2013.05.045.
  • Galanty, A., P. Koczurkiewicz, D. Wnuk, M. Paw, E. Karnas, I. Podolak, and M. Michalik. 2017. Usnic acid and atranorin exert selective cytostatic and anti-invasive effects on human prostate and melanoma cancer cells. Toxicol. In Vitro 40:161–69. doi:10.1016/j.tiv.2017.01.008.
  • Ghadi, F. E., A. Malhotra, A. R. Ghara, and D. K. Dhawan. 2012. Selenium as a modulator of membrane stability parameters and surface changes during the initiation phase of 1,2-dimethylhydrazine induced colorectal carcinogenesis. Mol. Cell. Biochem. 369:119–26. doi:10.1007/s11010-012-1374-z.
  • Gontijo, D. C., M. A. N. Diaz, G. C. Brandão, P. C. Gontijo, A. B. D. Oliveira, L. G. Fietto, and J. P. V. Leite. 2018. Phytochemical characterization and antioxidant, antibacterial and antimutagenic activities of aqueous extract from leaves of Alchornea glandulosa. J. Toxicol. Environ. Health A 81:805–18. doi:10.1080/15287394.2018.1492479.
  • Greenlee, H. 2012. Natural products for cancer prevention. Semin. Oncol. Nurs. 28:29–44. doi:10.1016/j.soncn.2011.11.004.
  • Halici, M., F. Odabasoglu, H. Suleyman, A. Cakir, A. Aslan, and Y. Bayir. 2005. Effects of water extract of Usnea longissima on antioxidant enzyme activity and mucosal damage caused by indomethacin in rats. Phytomedicine 12:656–62. doi:10.1016/j.phymed.2004.06.021.
  • Hasinoff, B. B., J. C. Yalowich, Y. Ling, and J. L. Buss. 1996. The effect of dexrazoxane (ICRF-187) on doxorubicin-and daunorubicin-mediated growth inhibition of Chinese hamster ovary cells. Anticancer Drugs 7:558–67.
  • ICH. 2012. International conference on harmonisation of technical requirements for registration of pharmaceuticals for human use. ICH - S2(R1) Genotoxicity testing and data interpretation for pharmaceuticals intended for human use. https://www.fda.gov/Drugs/GuidanceComplianceRegulatoryInformation/Guidances/default.htm.
  • Ingolfsdottir, K. 2002. Usnic acid. Phytochemistry 61:729–36.
  • Injac, R., and B. Strukelj. 2008. Recent advances in protection against doxorubicin-induced toxicity. Technol. Cancer Res. Treat. 7:497–516. doi:10.1177/153303460800700611.
  • Jacob, D. A., E. G. Gibson, S. L. Mercer, and J. E. Deweese. 2013. Etoposide catechol is an oxidizable topoisomerase II poison. Chem. Res. Toxicol. 26:1156–58. doi:10.1021/tx400205n.
  • Jenkins, G. J. S., S. H. Doak, G. E. Johnson, E. Quick, E. M. Waters, and J. M. Parry. 2005. Do dose response thresholds exist for genotoxic alkylating agents? Mutagenesis 20:389–98. doi:10.1093/mutage/gei054.
  • Knasmüller, S., H. Steinkellner, B. J. Majer, E. C. Nobis, G. Scharf, and F. Kassie. 2002. Search for dietary antimutagens and anticarcinogens: Methodological aspects and extrapolation problems. Food Chem. Toxicol. 40:1051–62.
  • Koparal, A. T. 2015. Anti-angiogenic and antiproliferative properties of the lichen substances (-)-usnic acid and vulpinic acid. Z. Naturforsch. C 70:159–64. doi:10.1515/znc-2014-4178.
  • Korniluk, A., O. Koper, H. Kemona, and V. Dymicka-Piekarska. 2017. From inflammation to cancer. Ir J Med Sci 186:57–62. doi:10.1007/s11845-016-1464-0.
  • Kotecha, R., A. Takami, and J. L. Espinoza. 2016. Dietary phytochemicals and cancer chemoprevention: A review of the clinical evidence. Oncotarget 7:52517–29. doi:10.18632/oncotarget.9593.
  • Langie, S. A., G. Koppen, D. Desaulniers, F. Al-Mulla, R. Al-Temaimi, A. Amedei, and A. K. Charles. 2015. Causes of genome instability: The effect of low dose chemical exposures in modern society. Carcinogenesis 36:61–88. doi:10.1093/carcin/bgv031.
  • Leandro, L. F., C. C. Munari, V. L. F. L. Sato, J. M. Alves, P. F. Oliveira, D. F. P. Mastrocola, and W. R. Cunha. 2013. Assessment of the genotoxicity and antigenotoxicity of (+)-usnic acid in V79 cells and Swiss mice by the micronucleus and comet assays. Mutat. Res. 753:101–06. doi:10.1016/j.mrgentox.2013.03.006.
  • Mayer, M., M. A. O‘Neill, K. E. Murray, N. S. Santos-Magalhães, A. M. A. Carneiro-Leão, A. M. Thompson, and V. C. Appleyard. 2005. Usnic acid: A non-genotoxic compound with anti-cancer properties. Anticancer Drugs 16:805–09.
  • Minotti, G., P. Menna, E. Salvatorelli, G. Cairo, and L. Gianni. 2004. Anthracyclines: Molecular advances and pharmacologic developments in antitumor activity and cardiotoxicity. Pharmacol. Rev. 56:185–229. doi:10.1124/pr.56.2.6.
  • National Research Council. 2011. Guide for the care and use of laboratory animals. 8th ed. The National Academies Collection: Reports funded by National Institutes of Health. doi:10.17226/12910.
  • Nguyen, T. T., S. Yoon, Y. Yang, H. B. Lee, S. Oh, M. H. Jeong, and K. Y. Lee. 2014. Lichen secondary metabolites in Flavocetraria cucullata exhibit anti-cancer effects on human cancer cells through the induction of apoptosis and suppression of tumorigenic potentials. PLoS ONE 9:e111575. doi:10.1371/journal.pone.0111575.
  • O‘Donovan, M. R. 1990. 1,8-dinitropyrene: Comparative mutagenicity in Chinese hamster V79 and CHO cells. Mutagenesis 5:275–78.
  • Odabasoglu, F., A. Cakir, H. Suleyman, A. Aslan, Y. Bayir, M. Halici, and C. Kazaz. 2006. Gastroprotective and antioxidant effects of usnic acid on indomethacin-induced gastric ulcer in rats. J. Ethnopharmacol. 103:59–65. doi:10.1016/j.jep.2005.06.043.
  • OECD (2016), Test no. 487: In Vitro mammalian cell micronucleus test, OECD Guidelines for the Testing of Chemicals, Section 4, OECD Publishing, Paris. doi:10.1787/9789264264861-en.
  • Plsíkova, J., J. Stepankova, J. Kasparkova, V. Brabec, M. Backor, and M. Kozurkova. 2014. Lichen secondary metabolites as DNA-interacting agents. Toxicol. In Vitro 28:182–86. doi:10.1016/j.tiv.2013.11.003.
  • Prokopiev, I. A., E. V. Filippov, G. V. Filippova, and N. P. Gladkina. 2017. Genotoxicity of usnic-acid enantiomers in vitro in human peripheral-blood lymphocytes. Cell Tissue Biol 11:141–46. doi:10.1134/S1990519X17020031.
  • Prokopiev, I. A., G. Filippov, E. Filippova, I. Voronov, I. Sleptsov, and A. Zhanataev. 2019. Genotoxicity of (+)- and (-)-usnic acid in mice. Mutat. Res. 839:36–39. doi:10.1016/j.mrgentox.2019.01.010.
  • Quiles, J. L., J. R. Huertas, M. Battino, J. Mataix, and M. C. Ramı́rez-Tortosa. 2002. Antioxidant nutrients and adriamycin toxicity. Toxicology 180:79–95.
  • Rabi, T., and A. Bishayee. 2009. Terpenoids and breast cancer chemoprevention. Breast Cancer Res. Treat. 115:223–39. doi:10.1007/s10549-008-0118-y.
  • Ribeiro-Costa, R. M., A. J. Alves, N. P. Santos, S. C. Nascimento, E. C. Gonçalves, N. H. Silva, and N. S. Santos-Magalhães. 2004. In vitro and in vivo properties of usnic acid encapsulated into PLGA-microspheres. J Microencapsul 21:371–84. doi:10.1080/02652040410001673919.
  • Saha, S. K., S. B. Lee, J. Won, H. Y. Choi, K. Kim, G. M. Yang, and S. G. Cho. 2017. Correlation between oxidative stress, nutrition, and cancer initiation. Int J Mol Sci 18:1544. doi:10.3390/ijms18071544.
  • Senedese, J. M., J. M. Alves, I. M. de Souza Lima, E. A. P. de 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 Complement. Altern. Med. 13:3–11. doi:10.1186/1472-6882-13-3.
  • Silva, C. R., K. S. N. Marinho, T. D. S. Silva, D. K. S. Ferreira, G. M. Aguiar, M. C. B. Martins, and N. H. Silva. 2017. Teratogenic effect of usnic acid from Cladonia substellata Vainio during organogenesis. Biomed. Res. Int. 2017:1–7.
  • Smith, N. A., J. A. W. Byl, S. L. Mercer, J. E. Deweese, and N. Osheroff. 2014. Etoposide quinone is a covalent poison of human topoisomerase IIβ. Biochemistry 53:3229–36. doi:10.1021/bi500421q.
  • Sosa, V., T. Moliné, R. Somoza, R. Paciucci, H. Kondoh, and M. E. LLeonart. 2013. Oxidative stress and cancer: An overview. Ageing Res. Rev. 12:376–90. doi:10.1016/j.arr.2012.10.004.
  • Su, Z. Q., Y. H. Liu, H. Z. Guo, C. Y. Sun, J. H. Xie, Y. C. Li, and H. M. Chen. 2017. Effect-enhancing and toxicity-reducing activity of usnic acid in ascitic tumor-bearing mice treated with bleomycin. Int. Immunopharmacol. 46:146–55. doi:10.1016/j.intimp.2017.03.004.
  • Su, Z. Q., Z. Z. Mo, J. B. Liao, X. X. Feng, Y. Z. Liang, X. Zhang, and X. P. Lai. 2014. Usnic acid protects LPS-induced acute lung injury in mice through attenuating inflammatory responses and oxidative stress. Int. Immunopharmacol. 22:371–78. doi:10.1016/j.intimp.2014.06.043.
  • Suwalsky, M., M. Jemiola-Rzeminska, C. Astudillo, M. J. Gallardo, J. P. Staforelli, F. Villena, and K. Strzalka. 2015. An in vitro study on the antioxidant capacity of usnic acid on human erythrocytes and molecular models of its membrane. Biochim. Biophys. Acta 1848:2829–38. doi:10.1016/j.bbamem.2015.08.017.
  • Swenberg, J. A., H. K. Cooper, J. Bücheler, and P. Kleihues. 1979. 1,2-dimethylhydrazine-induced methylation of DNA bases in various rat organs and the effect of pretreatment with disulfiram. Cancer Res. 39:465–67.
  • Thadhani, V. M., and V. Karunaratne. 2017. Potential of lichen compounds as antidiabetic agents with antioxidative properties: A review. Oxid. Med. Cell Longev. 2017:1–10. Article ID 2079697. doi:10.1155/2017/2079697.
  • Tuttis, K., D. L. M. G. Da Costa, H. L. Nunes, A. F. L. Specian, J. M. Serpeloni, L. C. D. Santos, and I. M. S. Cólus. 2018. Pouteria ramiflora (Mart.) Radlk. extract: Flavonoids quantification and chemopreventive effect on HepG2 cells. J. Toxicol. Environ. Health A 81:792–804. doi:10.1080/15287394.2018.1491911.
  • van de Water, B., J. P. Zoeteweij, and J. F. Nagelkerke. 1996. Alkylation-induced oxidative cell injury of renal proximal tubular cells: Involvement of glutathione redox-cycle inhibition. Arch. Biochem. Biophys. 327:71–80. doi:10.1006/abbi.1996.0094.
  • Venkatesh, P., B. Shantala, G. C. Jagetia, K. K. Rao, and M. S. Baliga. 2007. Modulation of doxorubicin-induced genotoxicity by Aegle marmelos in mouse bone marrow: A micronucleus study. Integr. Cancer Ther. 6:42–53. doi:10.1177/1534735406298302.
  • Yu, X., Q. Guo, G. Su, A. Yang, Z. Hu, C. Qu, and X. Chai. 2016. Usnic acid derivatives with cytotoxic and antifungal activities from the lichen Usnea longissima. J. Nat. Prod. 79:1373–80. doi:10.1021/acs.jnatprod.6b00109.
  • Živković, L., S. Borozan, A. Čabarkapa, D. Topalović, U. Ciptasari, V. Bajić, and B. Spremo-Potparević. 2017. Antigenotoxic properties of Agaricus blazei against hydrogen peroxide in human peripheral blood cells. Oxid. Med. Cell Longev. 2017:1–9. Article ID 8759764. doi:10.1155/2017/8759764.

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