Chemopreventive effect of troxerutin against hydrogen peroxide-induced oxidative stress in human leukocytes through modulation of glutathione-dependent enzymes

References

• Akerboom, T. P. M., and H. Sies. 1981. Assay of glutathione, glutathione disulfide, and glutathione mixed disulfides in biological samples. Meth. Enzymol. 77:373–82.
   PubMedGoogle Scholar
• Arroo, R. R. J., M. F. Wang, and A. S. Bhambra. 2020. Chemopreventive potential of flavones, flavonols, and their glycosides. Handb. Dietary Phytochemicals 2013:162750.
   Google Scholar
• Avelar-Freitas, B. A., V. G. Almeida, M. C. X. Pinto, F. A. G. Mourão, A. R. Massensini, O. A. Martins-Filho, E. Rocha-Vieira, and G. E. A. Brito-Melo. 2014. Trypan blue exclusion assay by flow cytometry. Braz. J. Med. Biol. Res. 47:307–15.
   PubMed Web of Science ®Google Scholar
• Baluchnejadmojarad, T., N. Jamali-Raeufy, S. Zabihnejad, N. Rabiee, and M. Roghani. 2017. Troxerutin exerts neuroprotection in 6-hydroxydopamine lesion rat model of Parkinson’s disease: Possible involvement of PI3K/ERΒ signaling. Eur. J. Pharmacol. 801:72–78.
   PubMed Web of Science ®Google Scholar
• Basile, M., S. Gidaro, M. Pacella, P. M. Biffignandi, and G. S. Gidaro. 2001. Parenteral troxerutin and carbazochrome combination in the treatment of post-hemorrhoidectomy status: A randomized, double-blind, placebo-controlled, phase IV study. Curr. Med. Res. Opin. 17:256–61.
   PubMed Web of Science ®Google Scholar
• Bilecová-Rabajdová, M., A. Birková, P. Urban, K. Gregová, E. Ďurovcová, and M. Mareková. 2013. Naturally occurring substances and their role in chemoprotective effects. Cent. Eur. J. Public Health 21:213–19.
   PubMed Web of Science ®Google Scholar
• Cavalcanti, B. C., H. V. N. Júnior, M. H. R. Seleghim, R. G. S. Berlinck, G. M. A. Cunha, M. O. Moraes, and C. Pessoa. 2008. Cytotoxic and genotoxic effects of tambjamine D, an alkaloid isolated from the Nudibranch tambja eliora, on chinese hamster lung fibroblasts. Chem. Biol. Interact. 174:155–62.
   PubMed Web of Science ®Google Scholar
• Cavalcanti, B. C., J. B. de Andrade Neto, A. A. de Sousa Silva, F. S. Barreto, J. R. de Oliveira Ferreira, C. R. da Silva, F. B. S. Aires Do Nascimento, L. G. A. Valente Sá, H. I. F. Magalhães , H. V. Nobre Júnior. 2020b. Evaluation of genotoxicity and mutagenicity of ketamine on human peripheral blood leukocytes and in Salmonella typhimurium. Toxicol. Vitro 62:104718.
   PubMed Web of Science ®Google Scholar
• Cavalcanti, B. C., J. R. O. Ferreira, D. J. Moura, R. M. Rosa, G. V. Furtado, R. R. Burbano, E. R. Silveira, M. A. S. Lima, C. A. G. Camaraf, J. Saffi. 2010. Structure–mutagenicity relationship of kaurenoic acid from Xylopia sericeae (Annonaceae). Mutat. Res. 701:153–63.
   PubMed Web of Science ®Google Scholar
• Cavalcanti, B. C., J. R. O. Ferreira, I. O. Cabral, H. I. F. Magalhães, C. C. de Oliveira, F. A. R. Rodrigues, D. D. Rocha, F. W. A. Barros, C. R. da Silva, H. V.N. Júnior. 2012. Genetic toxicology evaluation of essential oil of Alpinia zerumbet and its chemoprotective effects against H2O2-induced DNA damage in cultured human leukocytes. Food Chem. Toxicol. 50:4051–61.
   PubMed Web of Science ®Google Scholar
• Cavalcanti, B. C., L. G. Do Amaral Valente Sá, J. B. de Andrade Neto, A. A. de Sousa Silva, M. E. F. Rios, F. S. Barreto, J. R. de Oliveira Ferreira, C. R. Silva, F. D. Barroso, H. I. F. Magalhães. 2020a. Etomidate is devoid of genotoxicity and mutagenicity in human lymphocytes and in the Salmonella typhimurium/microsomal activation test. Toxicol. Vitro 68:104946.
   PubMed Web of Science ®Google Scholar
• Cinthura, C., R. Gayathri, and V. Priya. 2017. Genotoxicity analysis of mace (Myristica Fragrans) on oral cancer cell line by DNA fragmentation. J. Pharm. Sci. Res. 9:205–07.
   Google Scholar
• Diplock, A. T., J. L. Charleux, G. Crozier-Willi, F. J. Kok, C. Rice-Evans, M. Roberfroid, W. Stahl, and J. Viña-Ribes. 1998. Functional food science and defence against reactive oxidative species. Br. J. Nutr. 80:77–112.
   PubMed Web of Science ®Google Scholar
• Duthie, S. J., W. Johnson, and V. L. Dobson. 1997. The effect of dietary flavonoids on DNA damage (strand breaks and oxidised pyrimidines) and growth in human cells. Mutat. Res. 390:141–51.
   PubMed Web of Science ®Google Scholar
• Elangovan, P., A. Mohamed Jalaludeen, R. Ramakrishnan, and L. Pari. 2016. Protective effect of troxerutin on nickel-induced testicular toxicity in Wistar rats. J. Environ. Pathol. Toxicol. Oncol. 35:133–46.
   PubMed Web of Science ®Google Scholar
• Estrella-Parra, E. A., A. M. Espinosa-González, A. M. García-Bores, S. X. Zamora-Salas, J. C. Benítez-Flores, M. R. González-Valle, C. T. Hernández-Delgado, I. Peñalosa-Castro, and J. G. Avila-Acevedo. 2019. Flavonol glycosides in Dyssodia tagetiflora and its temporal variation, chemoprotective and ameliorating activities. Food Chem. Toxicol. 124:411–22.
   PubMed Web of Science ®Google Scholar
• Farajdokht, F., M. Amani, F. M. Bavil, A. Alihemmati, G. Mohaddes, and S. Babri. 2017. Troxerutin protects hippocampal neurons against amyloid beta-induced oxidative stress and apoptosis. Excli J. 16:1081–89.
   PubMed Web of Science ®Google Scholar
• Fenech, M. 2000. The in vitro micronucleus technique. Mutat. Res. 455:81–95.
   PubMed Web of Science ®Google Scholar
• Gandini, S., F. P. Francesco, H. Johanson, B. Bonanni, and A. Testori. 2009. Why vitamin D for cancer patients? Ecancermedicalscience 3:160.
   PubMedGoogle Scholar
• George, V. C., and H. P. Vasantha Rupasinghe. 2017. Apple flavonoids suppress carcinogen-induced DNA damage in normal human bronchial epithelial cells. Oxid Med Cell Longev 2017:1–12.
   Web of Science ®Google Scholar
• Gibson, D. 2002. Drug-DNA interactions and novel drug design. Pharmacogenomics J. 2:275–76.
   PubMedGoogle Scholar
• Glacet-Bernard, A., G. Coscas, A. Chabanel, A. Zourdani, F. Lelong, and M. M. Samama. 1994. A randomized, double-masked study on the treatment of retinal vein occlusion with troxerutin. Am. J. Ophthalmol. 118:421–29.
   PubMed Web of Science ®Google Scholar
• Goldberg, D. M. 1983. Glutathione reductase. In methods in enzymatic analysis, ed. H. U. Bergmeyer, 258–65. 1st ed. New York: Verlag Chemie Weinheim Academic Press.
   Google Scholar
• Gontijo, D. C., M. A. N. Diaz, G. C. Brandao, P. C. Gontijo, A. B. 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.
   PubMed Web of Science ®Google Scholar
• Gontijo, V. S., M. H. Dos Santos, and C. J. Viegas. 2017. Biological and chemical aspects of natural biflavonoids from plants: A brief review. Mini Rev Med Chem 17:834–62.
   PubMed Web of Science ®Google Scholar
• González-Vallinas, M., M. González-Castejón, A. Rodríguez-Casado, and A. Ramírez deMolina. 2013. Dietary phytochemicals in cancer prevention and therapy: A complementary approach with promising perspectives. Nutr. Rev. 71:585–99.
   PubMed Web of Science ®Google Scholar
• Hartmann, A., and G. Speit. 1997. The contribution of cytotoxicity to DNA-effects in the single cell gel test (comet assay). Toxicol. Lett. 90:183–88.
   PubMed Web of Science ®Google Scholar
• Kaur, T., R. Gupta, K. Vaiphei, R. Kapoor, N. M. Gupta, and K. L. Khanduja. 2008. Interplay between oncoproteins and antioxidant enzymes in esophageal carcinoma treated without and with chemoradiotherapy: A prospective study. Int. J. Radiat. Oncol. Biol. Phys. 70:563–71.
   PubMed Web of Science ®Google Scholar
• Lemmens, K. J. A., B. van de Wier, N. Vaes, M. Ghosh, M. A. M. J. van Zandvoort, W. J. F. van der Vijgh, A. Bast, and G. R. M. M. Haenen. 2014. The flavonoid 7-mono-o-(β-hydroxyethyl)-rutoside is able to protect endothelial cells by a direct antioxidant effect. Toxicol. Vitro 28:538–43.
   PubMed Web of Science ®Google Scholar
• Lemmens, K. J. A., P. M. Herst, B. A. C. Housmans, M. Moalin, W. J. F. van der Vijgh, A. Bast, and G. R. M. M. Haenen. 2015. The contribution of the major metabolite 4′-o-methylmonoher to the antioxidant activity of the flavonoid monomer. Chem. Biol. Interact. 239:146–52.
   PubMed Web of Science ®Google Scholar
• Liegler, T. J., W. Hyun, T. S. B. Yen, and D. P. Stites. 1995. Detection and quantification of live, apoptotic, and necrotic human peripheral lymphocytes by single-laser flow cytometry. Clin. Diagn. Lab. Immunol. 2:369–76.
   PubMedGoogle Scholar
• Logrado, L. P. L., C. O. Santos, L. A. S. Romeiro, A. M. Costa, J. R. O. Ferreira, B. C. Cavalcanti, O. M. Moraes, L. V. Costa-Lotufo, C. Pessoa, and M. L. Dos Santos. 2010. Synthesis and cytotoxicity screening of substituted isobenzofuranones designed from anacardic acids. Eur J Med Chem 45:3480–89.
   PubMedGoogle Scholar
• Lowry, O. H., N. J. Rosebrough, A. L. Farr, and R. J. Randall. 1951. Protein measurement with the folin phenol reagent. J. Biol. Chem. 193:265–75.
   PubMed Web of Science ®Google Scholar
• Lu, J., D. M. Wu, Z. H. Zheng, Y. L. Zheng, B. Hu, and Z. F. Zhang. 2011. Troxerutin protects against high cholesterol-induced cognitive deficits in mice. Brain 134:783–97.
   PubMed Web of Science ®Google Scholar
• Majolo, F., S. Bitencourt, B. Monteiro, G. Haute, C. Alves, J. Silva, S. Pinteus, R. C. V. Santos, H. F. V. Torquato, E. J. Paredes-Gamero. 2020. Antimicrobial and antileukemic effects: In vitro activity of Calyptranthes grandifolia aqueous leaf extract. J. Toxicol. Environ. Health A 83:1–13.
   PubMed Web of Science ®Google Scholar
• Marnewick, J. L., F. H. van der Westhuizen, E. Joubert, S. Swanevelder, P. Swart, and W. C. A. Gelderblom. 2009. Chemoprotective properties of rooibos (Aspalathus Linearis), honeybush (Cyclopia Intermedia) herbal and green and black (Camellia Sinensis) teas against cancer promotion induced by fumonisin b1 in rat liver. Food Chem. Toxicol. 47:220–29.
   PubMed Web of Science ®Google Scholar
• Marzin, D., H. V. Phi, P. Olivier, and J. Sauzieres. 1987. Study of mutagenic activity of troxerutin, a flavonoid derivative. Toxicol. Lett. 35:297–305.
   PubMed Web of Science ®Google Scholar
• Maurya, D. K., S. Balakrishnan, V. P. Salvi, and C. K. Nair. 2005. Protection of cellular DNA from γ-radiation-induced damages and enhancement in DNA repair by troxerutin. Mol. Cell. Biochem. 280:57–68.
   PubMed Web of Science ®Google Scholar
• Middleton, E., and C. Kandaswami. 1994. The impact of plant flavonoids on 461 mammalian biology: Implications for immunity, inflammation and cancer. In The Flavonoids: Advances in Research Since 1986, ed. J. B. Harborne, 619–52. 1st ed. London: Chapman & Hall.
   Google Scholar
• Milošević-Dordević, O., D. Grujičić, M. Radović, N. Vuković, J. Žižić, and S. Marković. 2015. In vitro chemoprotective and anticancer activities of propolis in human lymphocytes and breast cancer cells. Arch. Biol. Sci. 67:571–81.
   Google Scholar
• Miranda, J. A. L., C. S. da Martins, L. S. de Fideles, M. L. L. Barbosa, J. E. F. Barreto, H. B. Pimenta, F. O. R. Freitas,  P. V. S. Pimentel, C. S. Teixeira, A. G. Scafuri. 2020. Troxerutin prevents 5-fluorouracil induced morphological changes in the intestinal mucosa: Role of cyclooxygenase-2 pathway. Pharmaceuticals 13:10.
   Web of Science ®Google Scholar
• Nafisi, S., M. Adelzadeh, Z. Norouzi, and M. N. Sarbolouki. 2009. Curcumin binding to DNA and RNA. DNA Cell Biol. 28:201–08.
   PubMed Web of Science ®Google Scholar
• Narayanankutty, A., J. T. Job, and V. Narayanankutty. 2019. Glutathione, an antioxidant tripeptide: Dual roles in carcinogenesis and chemoprevention. Curr. Protein Pept. Sci. 20:907–17.
   PubMed Web of Science ®Google Scholar
• Nunes, H. L., K. Tuttis, J. M. Serpeloni, J. R. Nascimento, C. Q. Rocha, V. A. O. Silva, A. H. Lengert, R. M. Reis, and I. M. S. Colus. 2020. Characterization of the in vitro cytotoxic effects of brachtydins isolated from Friderica platyphylla in a prostate cancer cell line. J. Toxicol. Environ. Health A 83:547–58.
   PubMedGoogle Scholar
• Panat, N. A., B. G. Singh, D. K. Maurya, S. K. Sandur, and S. S. Ghaskadbi. 2016. Troxerutin, a natural flavonoid binds to DNA minor groove and enhances cancer cell killing in response to radiation. Chem. Biol. Interact. 251:34–44.
   PubMed Web of Science ®Google Scholar
• Plochmann, K., G. Korte, E. Koutsilieri, E. Richling, P. Riederer, A. Rethwilm, P. Schreier, and C. Scheller. 2007. Structure-activity relationships of flavonoid-induced cytotoxicity on human leukemia cells. Arch. Biochem. Biophys. 460:1–9.
   PubMed Web of Science ®Google Scholar
• Raja, B., and D. P. R. Saranya. 2019. Role of flavonoid troxerutin on blood pressure, oxidative stress and regulation of lipid metabolism. Front. Biosci. 11:121–29.
   Google Scholar
• Rao, M. V., and H. Tiwari. 2006. Amelioration by melatonin of chromosomal anomalies induced by arsenic and/or fluoride in human blood lymphocyte cultures. Fluoride 39:255–60.
   Web of Science ®Google Scholar
• Rauf, S., J. J. Gooding, K. Akhtar, M. A. Ghauri, M. Rahman, M. A. Anwar, and A. M. Khalid. 2005. Electrochemical approach of anticancer drugs-DNA interaction. J. Pharm. Biomed. Anal. 37:205–17.
   PubMed Web of Science ®Google Scholar
• Saks, M., S. Upreti, R. Sv, and R. Dang. 2017. Pharmacy & pharmaceutical science genotoxicity: Mechanisms, testing guidelines and methods. Global J. Pharm. Pharm. Sci. 1:1–6.
   Google Scholar
• Sghaier, B. M., I. Skandrani, N. Nasr, M.-G. D. Franca, L. Chekir-Ghedira, and K. Ghedira. 2011. Flavonoids and sesquiterpenes from Tecurium Ramosissimum promote antiproliferation of human cancer cells and enhance antioxidant activity: A structure-activity relationship study. Environ. Toxicol. Pharmacol. 32:336–48.
   PubMed Web of Science ®Google Scholar
• Shan, Q., J. Zhuang, G. Zheng, Z. Zhang, Y. Zhang, J. Lu, and Y. Zheng. 2017. Troxerutin reduces kidney damage against BDE-47-induced apoptosis via inhibiting NOX2 activity and increasing NRF2 activity. Oxid Med Cell Longev 2017:1–12.
   Web of Science ®Google Scholar
• Sharma, H., R. Kanwal, N. Bhaskaran, and S. Gupta. 2014. Plant flavone apigenin binds to nucleic acid bases and reduces oxidative DNA damage in prostate epithelial cells. PLoS ONE 9:1–9.
   Web of Science ®Google Scholar
• Silva, J. N., N. B. N. Moncao, R. R. S. deFarias, A. M. G. L. Cito, H. M. Chaves, M. R. S. de 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 supported findings for the Brazilian Unified Health System (SUS). J. Toxicol. Environ. Health A 83:525–45.
   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.
   PubMed Web of Science ®Google Scholar
• Squadrito, F., D. Altavilla, and S. Oliaro Bosso. 2000. Double-blind, randomized clinical trial of troxerutin-carbazochrome in patients with hemorrhoids. Eur Rev Med Pharmacol Sci 4:21–24.
   PubMedGoogle Scholar
• Subastri, A., C. H. Ramamurthy, A. Suyavaran, R. Mareeswaran, P. Lokeswara Rao, M. Harikrishna, M. Suresh Kumar, V. Sujatha, and C. Thirunavukkarasu. 2015. Spectroscopic and molecular docking studies on the interaction of troxerutin with DNA. Int. J. Biol. Macromol. 78:122–29.
   PubMed Web of Science ®Google Scholar
• Tai, W. M., and H. C. Toh. 2013. Statins: Emerging role in chemoprevention for hepatocellular carcinoma? Hepatobiliary Surg Nutr 2:117–20.
   PubMedGoogle Scholar
• Thomas, N. S., K. George, and A. A. A. Selvam. 2019. Anticancer mechanism of troxerutin via targeting Nrf2 and NF-ΚB signalling pathways in hepatocarcinoma cell line. Toxicol. Vitro 54:317–29.
   PubMed Web of Science ®Google Scholar
• Tice, R. R., E. Agurell, D. Anderson, B. Burlinson, A. Hartmann, H. Kobayashi, Y. Miyamae, E. Rojas, J. C. Ryu, and Y. F. Sasaki. 2000. Single cell gel/comet assay: Guidelines for in vitro and in vivo genetic toxicology testing. Environ. Mol. Mutagen. 35:206–21.
   PubMed Web of Science ®Google Scholar
• Tuttis, K., D. Costa, H. Nunes, A. Specian, J. Serpeloni, L. Santos, E. Varanda, W. Vilegas, W. Martínez-López, and I. M. Colus. 2018. Pouteria ramiflora (Mart.) Radlk. extract: Flavonoids quantification and chemopreventive effect on HEPG2 cells. J. Toxicol. Environ. Health Part A 81:1–13.
   PubMed Web of Science ®Google Scholar
• Vinothkumar, R., R. Vinoth Kumar, M. Sudha, P. Viswanathan, T. Balasubramanian, and N. Nalini. 2014b. Modulatory effect of troxerutin on biotransforming enzymes and preneoplasic lesions induced by 1,2-dimethylhydrazine in rat colon carcinogenesis. Exp. Mol. Pathol. 96:15–26.
   PubMed Web of Science ®Google Scholar
• Vinothkumar, R., R. Vinoth Kumar, V. Karthikkumar, P. Viswanathan, J. Kabalimoorthy, and N. Nalini. 2014a. Oral supplementation with troxerutin (trihydroxyethylrutin), modulates lipid peroxidation and antioxidant status in 1,2-dimethylhydrazine-induced rat colon carcinogenesis. Environ. Toxicol. Pharmacol. 37:174–84.
   PubMed Web of Science ®Google Scholar
• Wang, Y., S. Wei, L. Chen, J. Pei, H. Wu, Y. Pei, Y. Chen, and D. Wang. 2017. Transcriptomic analysis of gene expression in mice treated with troxerutin. PLoS ONE 12:1–21.
   Web of Science ®Google Scholar
• Zhang, S., X. Sun, R. Kong, and M. Xu. 2015b. Studies on the interaction of apigenin with calf thymus DNA by spectroscopic methods. Spectrochim. Acta 136:1666–70.
   PubMed Web of Science ®Google Scholar
• Zhang, Z. F., Y. Q. Zhang, S. H. Fan, J. Zhuang, Y. L. Zheng, J. Lu, D. M. Wu, Q. Shan, and B. Hu. 2015a. Troxerutin protects against 2,2ʹ,4,4ʹ-tetrabromodiphenyl ether (BDE-47)-induced liver inflammation by attenuating oxidative stress-mediated NAD+-depletion. J. Hazard. Mater. 283:98–109.
   PubMed Web of Science ®Google Scholar