Chemopreventive effect and induction of DNA repair by oenothein B ellagitannin isolated from leaves of Eugenia uniflora in Swiss Webster treated mice

References

• Aladaileh, S. H., F. K. Al-Swailmi, M. H. Abukhalil, A. F. Ahmeda, and A. M. Mahmoud. 2021. Punicalagin prevents cisplatin-induced nephrotoxicity by attenuating oxidative stress, inflammatory response, and apoptosis in rats. Life Sci. 286:120071. doi:10.1016/j.lfs.2021.120071.
   PubMed Web of Science ®Google Scholar
• Amararathna, M., M. R. Johnston, and H. P. Vasantha Rupasinghe. 2016. Plant polyphenols as chemopreventive agents for lung cancer. Int. J. Mol. Sci. 17 (8):1352. doi:10.3390/ijms17081352.
   PubMed Web of Science ®Google Scholar
• Aoki, K., H. Maruta, F. Uchiumi, T. Hatano, T. Yoshida, and S. I. Tanuma. 1995. A macrocircular ellagitannin, oenothein b, suppresses mouse mammary tumor gene expression via inhibition of poly(ADP-ribose) glycohydrolase. Biochem. Biophys. Res. Commun. 210 (2):329–37. doi:10.1006/bbrc.1995.1665.
   PubMed Web of Science ®Google Scholar
• Aoki, K., K. Nishimura, H. Abe, H. Maruta, H. Sakagami, T. Hatano, T. Okuda, T. Yoshida, Y. Tsai, J. Uchiumi, et al. 1993. Novel inhibitors of poly(ADP-ribose) glycohydrolase. Biochim. Biophys. Acta - Gen. Subj. 1158(3):251–56. doi:10.1016/0304-4165(93)90022-Z.
   Google Scholar
• Asma, S. T., U. Acaroz, K. Imre, A. Morar, S. R. A. Shah, S. Z. Hussain, D. Arslan-Acaroz, H. Demirbas, Z. Hajrulai-Musliu, F. R. Istanbullugil, et al. 2022. Natural products/bioactive compounds as a source of anticancer drugs. Cancers. 14(24):6203. doi:10.3390/cancers14246203.
   PubMed Web of Science ®Google Scholar
• Barreca, D. 2020. Mechanisms of plant antioxidants actions. Plants 10 (1):35. doi:10.3390/plants10010035.
   Google Scholar
• Carabajal, M. P. A., M. I. Isla, and I. C. Zampini. 2017. Evaluation of antioxidant and antimutagenic activity of herbal teas from native plants used in traditional medicine in Argentina. South Afr. J. Bot. 110:258–65. doi:10.1016/j.sajb.2016.10.006.
   Web of Science ®Google Scholar
• Carneiro, C. C., S. da Costa Santos, R. de Souza Lino, M. T. F. Bara, B. A. Chaibub, P. R. de Melo Reis, D. A. Chaves, A. J. R. da Silva, L. S. Silva, D. de Melode Melo e Silva, et al. 2016. Chemopreventive effect and angiogenic activity of punicalagin isolated from leaves of lafoensia pacari A. St.-Hil. Toxicol. App. l Pharmacol. 310:1–8. doi:10.1016/j.taap.2016.08.015.
   PubMed Web of Science ®Google Scholar
• Carneiro, C. C., A. V. M. Filho, A. S. Fernandes, S. da C Santos, and L. Chen-Chen. 2016. Cytotoxic and chemopreventive effects of gemin D against different mutagens using in vitro and in vivo assays. Anti-Cancer Agents Med. Chem. 16:1–7. doi:10.2174/18715206166661609060925.
   Google Scholar
• Chaitanya, G. V., J. S. Alexander, and P. Prakash Babu. 2010. PARP-1 cleavage fragments: Signatures of cell-death proteases in neurodegeneration. Cell Commun. Signal 8 (1):31. doi:10.1186/1478-811X-8-31.
   PubMed Web of Science ®Google Scholar
• Chakraborty, P., S. K. U. Hossain, N. M. Jayanta, K. Das, S. Pal, and S. Bhattacharya. 2009. Modulation of cyclophosphamide-induced cellular toxicity by diphenylmethyl selenocyanate in vivo, an Enzymatic study. J. Cancer Mol. 4:183–89. doi:10.29685/JCM.200902.0004.
   Google Scholar
• Chen, C.-Y., C.-L. Kao, and C.-M. Liu. 2018. The cancer prevention, anti-inflammatory and anti-oxidation of bioactive phytochemicals targeting the TLR4 signaling pathway. Int. J. Mol. Sci. 19 (9):2729. doi:10.3390/ijms19092729.
   PubMed Web of Science ®Google Scholar
• Chen, Y., B. Onken, H. Chen, X. Zhang, M. Driscoll, Y. Cao, and Q. Huang. 2020. Healthy lifespan extension mediated by oenothein B isolated from Eucalyptus grandis × Eucalyptus urophylla GL9 in Caenorhabditis elegans. Food Funct. 11 (3):2439–50. doi:10.1039/c9fo02472g.
   PubMed Web of Science ®Google Scholar
• CONCEA. 2016. Normativas do Concea - Lei, Decreto, Portarias, Resoluções Normativas e Orientações Técnicas - 3^a Edição. Brazil. http://www.invitare.com.br/arq/ceua/Arquivo-3-normativas-concea-2016.pdf
   Google Scholar
• Cuce, G., S. Çetinkaya, T. Koc, H. Hasan, C. Limandal, T. Balcı, S. Kalkan, and M. Akoz. 2015. Chemoprotective effect of vitamin E in cyclophosphamide-induced hepatotoxicity in rats. Chem. Biol. Interact. 232:7–11. doi:10.1016/j.cbi.2015.02.016.
   PubMed Web of Science ®Google Scholar
• Da Silva, F. C., J. N. Picada, N. F. Romão, F. O. S. Sobral, D. Lemos, S. V. Schons, T. L. de Mello, W. M. Silva, R. D. S. Oliveira, and C. P. Lucas. 2019. Antigenotoxic and antimutagenic effects of Myrciaria dubia juice in mice submitted to ethanol 28-day treatment. J. Toxicol. Environ. Health A 82 (17):956–68. doi:10.1080/15287394.2019.1671279.
   PubMed Web of Science ®Google Scholar
• Dehelean, C. A., I. Marcovici, C. Soica, M. Mioc, D. Coricovac, S. Iurciuc, O. M. Cretu, and I. Pinzaru. 2021. Plant-derived anticancer compounds as new perspectives in drug discovery and alternative therapy. Molecules 26 (4):1109. doi:10.3390/molecules26041109.
   PubMed Web of Science ®Google Scholar
• Esposito, C., C. Santarcangelo, R. Masselli, G. Buonomo, G. Nicotra, V. Insolia, M. D. Avino, G. Caruso, A. Riccardo, R. Sacchi, et al. 2021. Epilobium angustifolium L. extract with high content in oenothein B on benign prostatic hyperplasia: A monocentric, randomized, double-blind, placebo-controlled clinical trial. Biomed. Pharmacother. 138:111414. doi:10.1016/j.biopha.2021.111414.
   PubMed Web of Science ®Google Scholar
• Fernandes, A. S., J. H. Véras, L. S. Silva, S. C. Puga, E. F. L. C. Bailão, M. G. Oliveira, C. G. Cardoso, C. C. Carneiro, S. C. Santos, and L. Chen-Chen. 2022. Pedunculagin isolated from Plinia cauliflora seeds exhibits genotoxic, antigenotoxic and cytotoxic effects in bacteria and human lymphocytes. J. Toxicol. Environ. Health A 85 (9):353–63. doi:10.1080/15287394.2021.2009947.
   PubMed Web of Science ®Google Scholar
• Ferreira, P. M. P., D. D. R. Arcanjo, and A. P. Peron. 2023. Drug development, Brazilian biodiversity and political choices: Where are we heading? J. Toxicol. Environ. Health B 26 (5):257–74. doi:10.1080/10937404.2023.2193762.
   PubMed Web of Science ®Google Scholar
• Fortes, G. A. C., A. G. Carvalho, R. R. F. Ramalho, A. J. R. da Silva, P. H. Ferri, and S. C. Santos. 2015. Antioxidant activities of hydrolysable tannins and flavonoid glycosides isolated from Eugenia uniflora L. Rec. Nat. Prod. 9:251–56.
   Google Scholar
• Gautam, V., A. Sharma, S. Arora, R. Bhardwaj, A. Ahmad, B. Ahamad, and P. Ahmad. 2020. In vitro antioxidant, antimutagenic and cancer cell growth inhibition activities of rhododendron arboreum leaves and flowers. Saudi. J. Biol. Sci. 27 (7):1788–96. doi:10.1016/j.sjbs.2020.01.030.
   PubMed Web of Science ®Google Scholar
• Granica, S., J. P. Piwowarski, and A. K. Kiss. 2015. Ellagitannins modulate the inflammatory response of human neutrophils ex vivo. Phytomedicine 22 (14):1215–22. doi:10.1016/j.phymed.2015.10.004.
   PubMed Web of Science ®Google Scholar
• Hassimotto, N. M., and F. M. Lajolo. 2011. Antioxidant status in rats after long-term intake of anthocyanins and ellagitannins from blackberries. J. Sci. Food Agric. 91 (3):523–31. doi:10.1002/jsfa.4216.
   PubMed Web of Science ®Google Scholar
• Hatano, T., T. Yasuhara, M. Matsuda, K. Yazaki, T. Yoshida, and T. Okuda. 1990. Oenothein B, a dimeric, hydrolysable tannin with macrocyclic structure, and accompanying tannins from Oenothera erythrosepala. J. Chem. Soc. Perking Trans. 1 (10):2735–43. doi:10.1039/p19900002735.
   Google Scholar
• Heddle, J. A. 1973. A rapid in vivo test for chromosomal damage. Mutat. Res. Mol. Mech. Mutagen 18 (2):187–90. doi:10.1016/0027-5107(73)90035-3.
   PubMedGoogle Scholar
• Hevesi Tóth, B., B. Blazics, and Á. Kéry. 2009. Polyphenol composition and antioxidant capacity of Epilobium species. J. Pharm. Biomed. Anal 49 (1):26–31. doi:10.1016/j.jpba.2008.09.047.
   PubMed Web of Science ®Google Scholar
• Kiss, A. K., A. Bazylko, A. Filipek, S. Granica, E. Jaszewska, U. Kiarszys, A. Kośmider, and J. Piwowarski. 2011. Oenothein B’s contribution to the anti-inflammatory and antioxidant activity of Epilobium sp. Phytomedicine 18 (7):557–60. doi:10.1016/j.phymed.2010.10.016.
   PubMed Web of Science ®Google Scholar
• Ko, Y. S., N. Y. Kim, and J. S. Pyo. 2020. Clinicopathological significance and angiogenic role of the constitutive phosphorylation of the FOXO1 transcription factor in colorectal cancer. Pathol. Res. Pract. 216 (11):153150. doi:10.1016/j.prp.2020.153150.
   PubMed Web of Science ®Google Scholar
• Lichota, A., and K. Gwozdzinski. 2018. Anticancer activity of natural compounds from plant and marine environment. Int. J. Mol. Sci. 19:3533. doi:10.3390/ijms19113533.
   PubMed Web of Science ®Google Scholar
• Li, W., Z. Li, M. J. Peng, X. Zhang, Y. Chen, Y. Y. Yang, X. X. Zhai, G. Liu, and Y. Cao. 2020. Oenothein B boosts antioxidant capacity and supports metabolic pathways that regulate antioxidant defense in Caenorhabditis elegans. Food Funct. 11 (10):9157–67. doi:10.1039/d0fo01635g.
   PubMed Web of Science ®Google Scholar
• Liu, Q., and H. G. Wang. 2012. Anti-cancer drug discovery and development bcl-2 family small molecule inhibitors. Commun. Integr. Biol. 5:557–65. doi:10.4161/cib.21554.
   PubMedGoogle Scholar
• Makhafola, T. J., E. E. Elgorashi, L. J. McGaw, L. Verschaeve, and J. N. Eloff. 2016. The correlation between antimutagenic activity and total phenolic content of extracts of 31 plant species with high antioxidant activity. BMC Complement Altern. Med. 16 (1):1–13. doi:10.1186/s12906-016-1437-x.
   PubMedGoogle Scholar
• Maron, D. M., and B. N. Ames. 1983. Revised methods for the Salmonella mutagenicity test. Mutat. Res. Mutagen. Relat. Subj. 113 (3–4):173–215. doi:10.1016/0165-1161(83)90010-9.
   PubMed Web of Science ®Google Scholar
• Matsuno, T., Y. Atsumi, M. Alauddin, M. M. Rana, H. Fujimori, M. Hyodo, A. Shimizo, T. Ikuta, H. Tani, H. Torigoe, et al. 2020. Resveratrol and its related polyphenols contribute to the maintenance of genome stability. Sci. Rep. 10(1):5388. doi:10.1038/s41598-020-62292-5.
   PubMed Web of Science ®Google Scholar
• Miyamoto, K., M. Nomura, T. Murayama, T. Furukawa, T. Hatano, T. Yoshida, R. Koshiura, and T. Okuda. 1993. Antitumor activities of ellagitannins against sarcoma-180 in mice. Biol. Pharm. Bull. 16 (4):379–87. doi:10.1248/bpb.16.379.
   PubMed Web of Science ®Google Scholar
• Miyamoto, K., M. Nomura, M. Sasakura, E. Matsui, R. Koshiura, T. Murayama, T. Furukawa, T. Hatano, T. Yoshida, and T. Okuda. 1993. Antitumor activity of oenothein B, a unique macrocyclic ellagitannin. Japanese J. Cancer Res. 84: 99–103. 10.1111/j.1349-7006.1993.tb02790.x
   PubMedGoogle Scholar
• Mortelmans, K., and E. Zeiger. 2000. The Ames Salmonella/microsome mutagenicity assay. Mutat. Res. Mol. Mech. Mutagen 455 (1–2):29–60. doi:10.1016/S0027-5107(00)00064-6.
   PubMed Web of Science ®Google Scholar
• OECD. 2016. Test No. 489: In Vivo Mammalian Alkaline Comet Assay, OECD Guidelines for the Testing of Chemicals, Section 4, OECD. Paris. doi:10.1787/9789264264885-en.
   Google Scholar
• Okuda, T., T. Yoshida, and T. Hatano. 1993. Classification of oligomeric hydrolysable tannins and specificity of their occurrence in plants. Phytochemistry 32 (3):507–21. doi:10.1016/S0031-9422(00)95129-X.
   Web of Science ®Google Scholar
• Pascal, J. M. 2018. The comings and goings of PARP-1 in response to DNA damage. DNA Rep. 71:177–82. doi:10.1016/j.dnarep.2018.08.022.
   PubMed Web of Science ®Google Scholar
• Pei, X., J. Xiao, G. Wei, Y. Zhang, F. Lin, Z. Xiong, L. Lu, X. Wang, G. Pang, Y. Jiang, et al. 2019. Oenothein B inhibits human non-small cell lung cancer A549 cell proliferation by ROS-mediated PI3K/Akt/NF-κB signaling pathway. Chem. Biol. Interact. 298:112–20. doi:10.1016/j.cbi.2018.09.021.
   PubMed Web of Science ®Google Scholar
• Ramstead, A. G., I. A. Schepetkin, M. T. Quinn, M. A. Jutila, and R. Jacobs. 2012. Oenothein B, a cyclic dimeric ellagitannin isolated from Epilobium angustifolium, enhances IFNγ production by lymphocytes. PLoS One 7 (11):e50546. doi:10.1371/journal.pone.0050546.
   PubMed Web of Science ®Google Scholar
• Ramstead, A. G., I. A. Schepetkin, K. Todd, J. Loeffelholz, J. G. Berardinelli, M. T. Quinn, and M. A. Jutila. 2015. Aging influences the response of T cells to stimulation by the ellagitannin, oenothein B. Int. Immunopharmacol. 26 (2):367–77. doi:10.1016/j.intimp.2015.04.008.
   PubMed Web of Science ®Google Scholar
• Ranjan, A., S. Ramachandram, N. Gupta, I. Kaushik, S. Wright, S. Srivastava, H. Das, S. Srivastava, S. Prasad, and S. K. Srivastava. 2019. Role of phytochemicals in cancer prevention. Int. J. Mol. Sci. 20 (20):4981. doi:10.3390/ijms20204981.
   PubMed Web of Science ®Google Scholar
• Sahin, T. K., B. Bilir, and O. Kucuk. 2023. Modulation of inflammation by phytochemicals to enhance efficacy and reduce toxicity of cancer chemotherapy. Crit. Ver. Food Sci. Nutr 63 (15):2494–508. doi:10.1080/10408398.2021.1976721.
   PubMed Web of Science ®Google Scholar
• Santos, S. C., A. G. Carvalho, G. A. C. Fortes, P. H. Ferri, and A. E. De Oliveira. 2014. Variable-temperature NMR and conformational analysis of oenothein B. J. Braz. Chem. Soc. 25:282–89. doi:10.5935/0103-5053.20130295.
   Web of Science ®Google Scholar
• Santos, S. C., G. A. C. Fortes, L. T. F. M. Camargo, A. J. Camargo, and P. H. Ferri. 2021. Antioxidant effects of polyphenolic compounds and structure-activity relationship predicted by multivariate regression tree. LWT- Food Sci. Technol 137:110366. doi:10.1016/j.lwt.2020.110366.
   Web of Science ®Google Scholar
• Sarac, N. 2015. Antioxidant, mutagenic, and antimutagenic activities of tragopogon longirostis var. longirostis, an edible wild plant in Turkey. Indian J. Pharmacol. 47:414–18. doi:10.4103/0253-7613.161267.
   PubMed Web of Science ®Google Scholar
• Sbardelotto, A. B., F. W. A. Barros-Nepomuceno, B. M. Soares, B. C. Cavalcanti, R. W. R. Souza, M. P. Costa, O. D. L. Pessoa, C. Pessoa, and P. M. P. Ferreira. 2021. Cellular and biochemical antileukemic mechanisms of the meroterpenoid oncocalyxone a. J. Toxicol. Environ. Health A 84 (3):95–111. doi:10.1080/15287394.2020.1835763.
   PubMed Web of Science ®Google Scholar
• Sghaier, M. B., W. Bhouri, I. Bouhlel, I. Skandrani, J. Boubaker, L. Chekir-Ghedira, and K. Ghedira. 2011. Inhibitory effect of Teucrium ramosissimum extracts on aflatoxin B1, benzo[a]pyrene, 4-nitro-o-phenylenediamine and sodium azide induced mutagenicity: Correlation with antioxidant activity. South Afr. J. Bot. 77 (3):730–40. doi:10.1016/j.sajb.2011.03.014.
   Web of Science ®Google Scholar
• Silva, R. M., L. D. Pereira, J. H. Veras, C. R. Do Vale, L. Chen-Chen, and S. da C Santos. 2016. Protective effect and induction of DNA repair by myrciaria cauliflora seed extract and pedunculagin on cyclophosphamide-induced genotoxicity. Mutat. Res. Genet. Toxicol. Environ. Mutagen 810:40–47. doi:10.1016/j.mrgentox.2016.10.001.
   PubMed Web of Science ®Google Scholar
• Silva, C. A., C. R. Silva, J. H. Véras, L. Chen-Chen, P. H. Ferri, and S. da C Santos. 2014. Genotoxicity and cytotoxicity evaluation of oenothein B and its protective effect against mitomycin C-induced mutagenic action. Mutat. Res. Genet. Toxicol. Environ. Mutagen 767:8–12. doi:10.1016/j.mrgentox.2014.04.003.
   PubMed Web of Science ®Google Scholar
• Singh, V. K., D. Arora, M. I. Ansari, and P. K. Sharma. 2019. Phytochemicals based chemopreventive and chemotherapeutic strategies and modern technologies to overcome limitations for better clinical applications. Phytother. Res. 33 (12):3064–89. doi:10.1002/ptr.6508.
   PubMed Web of Science ®Google Scholar
• Singh, N. P., M. T. McCoy, R. R. Tice, and E. L. Schneider. 1988. A simple technique for quantitation of low levels of DNA damage in individual cells. Exp. Cell Res. 175:184–91. doi:10.1016/0014-4827(88)90265-0.
   PubMed Web of Science ®Google Scholar
• Stankevicins, L., C. Aiub, L. C. de Santa Maria, G. Lobo-Hajdu, and I. Felzenszwalb. 2008. Genotoxic and antigenotoxic evaluation of extracts from Arenosclera brasiliensis, a Brazilian marine sponge. Toxicol. Vitro 22 (8):1869–77. doi:10.1016/j.tiv.2008.09.003.
   PubMed Web of Science ®Google Scholar
• Sung, H., J. Ferlay, R. L. Siegel, M. Laversanne, I. Soerjomataram, A. Jemal, and F. Bray. 2021. Global cancer statistics 2020: Globocan estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 71:209–49. doi:10.3322/caac.21660.
   PubMed Web of Science ®Google Scholar
• Torre, L. A., F. Bray, R. L. Siegel, J. Ferlay, J. Loutet-Tieulent, and A. Jemal. 2015. Global cancer statistics 2012. CA Cancer J. Clin. 65 (2):87–108. doi:10.3322/caac.21262.
   PubMed Web of Science ®Google Scholar
• Turrini, E., C. Calcabrini, M. Tacchini, T. Efferth, G. Sacchetti, A. Guerrini, G. Paganetto, E. Catanzaro, G. Greco, and C. Fimognare. 2018. In vitro study of the cytotoxic, cytostatic, and antigenotoxic profile of hemidesmus indicus. Toxins 10 (2):70. doi:10.3390/toxins10020070.
   PubMed Web of Science ®Google Scholar
• Vodicka, P., S. Vodenkova, A. Oppatova, and L. Vodickova. 2019. DNA damage and repair measured by comet assay in cancer patients. Mutat. Res. Genet. Toxicol. Environ 843:95–110. doi:10.1016/j.mrgentox.2019.05.009.
   PubMed Web of Science ®Google Scholar
• Von Ledebur, M., and W. Schmid. 1973. The micronucleus test methodological aspects. Mutat. Res. Fundam. Mol. Mech. Mutagen 19 (1):109–17. doi:10.1016/0027-5107(73)90118-8.
   PubMedGoogle Scholar
• Wang, C. C., L. G. Chen, and L. L. Yang. 1999. Antitumor activity of four macrocyclic ellagitannins from Cuphea hyssopifolia. Cancer Lett. 140:195–200. doi:10.1016/S0304-3835(99)00071-3.
   PubMed Web of Science ®Google Scholar
• Xu, L., W. Li, S. Y. Chen, X. W. Deng, W. F. Deng, G. Liu, Y. J. Chen, and Y. Cao. 2022. Oenothein B ameliorates hepatic injury in alcoholic liver disease mice by improving oxidative stress and inflammation and modulating the gut microbiota. Front. Nutr. 9:1–17. doi:10.3389/fnut.2022.1053718.
   Web of Science ®Google Scholar
• Yoshida, T., Y. Amakura, and M. Yoshimura. 2010. Structural features and biological properties of ellagitannins in some plant families of the order myrtales. Int. J. Mol. Sci. 11:79–106. doi:10.3390/ijms11010079.
   PubMed Web of Science ®Google Scholar
• Yoshida, T., M. Yoshimura, and Y. Amakura. 2018. Chemical and biological significance of oenothein B and related ellagitannin oligomers with macrocyclic structure. Molecules 23 (3):552. doi:10.3390/molecules23030552.
   PubMed Web of Science ®Google Scholar
• Zeiger, E. 2000. Death and antimutagenicity. Mutat. Res. - Genet. Toxicol. Environ. Mutagen 466:125–27. doi:10.1016/S1383-5718(00)00008-5.
   Web of Science ®Google Scholar
• Zeiger, E. 2019. The test that changed the world: The Ames test and the regulation of chemicals. Mutat. Res. Genet. Toxicol. Environ. Mutagen 841:43–48. doi:10.1016/j.mrgentox.2019.05.007.
   PubMed Web of Science ®Google Scholar
• Zhu, Y., Q. Yang, H. Liu, Z. Song, and W. Chen. 2020. Phytochemical compounds targeting on Nrf2 for chemoprevention in colorectal cancer. Eur. J. Pharmacol. 887:173588. doi:10.1016/j.ejphar.2020.173588.
   PubMed Web of Science ®Google Scholar