304
Views
1
CrossRef citations to date
0
Altmetric
Research Article

Protective effects of resveratrol against genotoxicity induced by nano and bulk hydroxyapatite in Drosophila melanogaster

ORCID Icon

References

  • Abdalaziz, M. A., B. Annangi, and R. Marcos. 2014. Testing the genotoxic potential of nanomaterials using Drosophila in genotoxicity and DNA repair, 297–304. New York: Springer.
  • Abdel-Daim, M. M., I. A. Eissa, A. Abdeen, H. M. Abdel-Latif, M. Ismail, M. A. Dawood, and A. M. Hassan. 2019. Lycopene and resveratrol ameliorate zinc oxide nanoparticles-induced oxidative stress in Nile tilapia, Oreochromis niloticus. Environ. Toxicol. Pharmacol 69:44–50. doi:10.1016/j.etap.2019.03.016.
  • Abdul Halim, N. A., M. Z. Hussein, and M. K. Kandar. 2021. Nanomaterials-upconverted hydroxyapatite for bone tissue engineering and a platform for drug delivery. Int. J. Nanomed 16:6477–96. doi:10.2147/IJN.S298936.
  • Abolaji, A. O., V. O. Ajala, J. O. Adigun, I. A. Adedara, H. W. Kinyi, and E. O. Farombi. 2019. Protective role of resveratrol, a natural polyphenol, in sodium fluoride-induced toxicity in Drosophila melanogaster. Exp. Biol. Med 244 (18):1688–94. doi:10.1177/1535370219890334.
  • Abraham, S. K., N. Khandelwal, H. Hintzsche, and H. Stopper. 2016. Antigenotoxic effects of resveratrol: Assessment of in vitro and in vivo response. Mutagenesis 31 (1):27–33. doi:10.1093/mutage/gev048.
  • Alaraby, M., A. Hernandez, B. Annangi, E. Demir, J. Bach, L. Rubio, A. Creus, and R. Marcos. 2015a. Antioxidant and antigenotoxic properties of CeO 2 NPs and cerium sulphate: Studies with Drosophila melanogaster as a promising in vivo model. Nanotoxicology 69 (6):749–59. doi:10.3109/17435390.2014.976284.
  • Alaraby, M., E. Demir, A. Hernández, and R. Marcos. 2015b. Assessing potential harmful effects of CdSe quantum dots by using Drosophila melanogaster as in vivo model. Sci. Total Environ 15:66–75. doi:10.1016/j.scitotenv.2015.05.069.
  • Alaraby, M., B. Annangi, R. Marcos, and A. Hernández. 2016. Drosophila melanogaster as a suitable in vivo model to determine potential side effects of nanomaterials: A review. J. Toxicol. Environ. Health B 19 (2):65–104. doi:10.1080/10937404.2016.1166466.
  • Alaraby, M., S. Romero, A. Hernández, and R. Marcos. 2019. Toxic and genotoxic effects of silver nanoparticles in Drosophila. Environ. Mol. Mutagen 60 (3):277–85. doi:10.1002/em.22262.
  • Alaraby, M., E. Demir, J. Domenech, A. Velázquez, A. Hernández, and R. Marcos. 2020. In vivo evaluation of the toxic and genotoxic effects of exposure to cobalt nanoparticles using Drosophila melanogaster. Environ. Sci. Nano 7 (2):610–22. doi:10.1039/C9EN00690G.
  • Almeida, I. M. C., J. C. M. Barreira, M. B. P. P. Oliveira, and I. C. F. R. Ferreira. 2011. Dietary antioxidant supplements: Benefits of their combined use. Food Chem. Toxicol 49 (12):3232–37. doi:10.1016/j.fct.2011.09.012.
  • Arcos, D., and M. Vallet-Regí. 2020. Substituted hydroxyapatite coatings of bone implants. J. Mater. Chem B 8 (9):1781–800. doi:10.1039/C9TB02710F.
  • Bertilli, A. A., L. Giovannini, D. Gianessi, M. Migliori, W. Bernini, M. Fregoni, and A. Bertilli. 1995. Antiplatelet activity of synthetic and natural resveratrol in red wine. Int. J. Tissue. React 17 (1):1–3.
  • Bordea, I. R., S. Candrea, G. T. Alexescu, S. Bran, M. Băciuț, G. Băciuț, O. Lucaciu, C. M. Dinu, and D. A. Todea. 2020. Nano-hydroxyapatite use in dentistry: A systematic review. Drug Metab. Rev 52 (2):319–32. doi:10.1080/03602532.2020.1758713.
  • Boverhof, D. R., C. M. Bramante, J. H. Butala, S. F. Clancy, M. Lafranconi, J. West, and S. C. Gordon. 2015. Comparative assessment of nanomaterial definitions and safety evaluation considerations. Regul. Toxicol. Pharmacol 73 (1):137–50. doi:10.1016/j.yrtph.2015.06.001.
  • Boyce, A., J. Doehmer, and N. J. Gooderham. 2004. Phytoalexin resveratrol attenuates the mutagenicity of the heterocyclic amines 2-amino-1-methyl-6-phenylimidazo[4,5-b] pyridine and 2-amino-3,8-dimethylimidazo[4,5-f] quinoxaline. J. Chromatogr B 802 (1):217–23. doi:10.1016/j.jchromb.2003.10.057.
  • Burkitt, M. J., and J. Duncan. 2000. Effects of transresveratrol on copper-dependent hydroxyl-radical formation and DNA damage: Evidence for hydroxyl radical scavenging and a novel, glutathione-sparing mechanism of action. Arch. Biochem. Biophys 381 (2):253–63. doi:10.1006/abbi.2000.1973.
  • Cadena, G., M. A. Pereira, R. B. Cordeiro, I. M. Cavalcanti, B. Barros Neto, C. Pimentel Mdo, J. L. Lima Filho, V. L. Silva, and N. S. Santos-Magalhaes. 2013. Nanoencapsulation of quercetin and resveratrol into elastic liposomes. Biochim. Biophys. Acta 1828 (2):309–16. doi:10.1016/j.bbamem.2012.10.022.
  • Carrizzo, A., M. Forte, A. Damato, V. Trimarco, F. Salzano, M. Bartolo, A. Maciag, A. A. Puca, and C. Vecchione. 2013. Antioxidant effects of resveratrol in cardiovascular, cerebral and metabolic diseases. Food Chem. Toxicol 61:215–26. doi:10.1016/j.fct.2013.07.021.
  • Chan, C. C., K. C. Lee, Y. H. Huang, C. K. Chou, H. C. Lin, and F. Y. Lee. 2014. Regulation by resveratrol of the cellular factors mediating liver damage and regeneration after acute toxic liver injury. J. Gastroenterol. Hepatol 29 (3):603–13. doi:10.1111/jgh.12366.
  • Climent, M., G. Viggiani, Y. W. Chen, G. Coulis, and A. Castaldi. 2020. MicroRNA and ROS crosstalk in cardiac and pulmonary diseases. Int. J. Mol. Sci 21 (12):4370. doi:10.3390/ijms21124370.
  • Çolak, D. A., and H. Uysal. 2017. Protective effects of coenzyme Q10 and resveratrol on oxidative stress induced by various dioxins on transheterozigot larvae of Drosophila melanogaster. Toxicol. Res 6 (4):521–25. doi:10.1039/C7TX00027H.
  • Crowther, D. C., R. Page, D. Chandraratna, and D. A. Lomas. 2006. A drosophila model of Alzheimer’s disease. Meth. Enzymol 412:234–55.
  • Cullberg, K. B., J. Olholm, S. K. Paulsen, C. B. Foldager, M. Lind, B. Richelsen, and S. B. Pedersen. 2013. Resveratrol has inhibitory effects on the hypoxia-induced inflammation and angiogenesis in human adipose tissue in vitro. Eur J Pharm Sci 49 (2):251–57. doi:10.1016/j.ejps.2013.02.014.
  • Dan, P., V. Sundararajan, H. Ganeshkumar, B. Gnanabarathi, A. K. Subramanian, G. D. Venkatasubu, S. Ichihara, G. Ichihara, and S. S. Mohideen. 2019. Evaluation of hydroxyapatite nanoparticles-induced in vivo toxicity in Drosophila melanogaster. Appl. Surf. Sci 484:568–77. doi:10.1016/j.apsusc.2019.04.120.
  • Danaei, M., M. Dehghankhold, S. Ataei, D. F. Hasanzadeh, R. Javanmard, A. Dokhani, S. Khorasani, and M. R. Mozafari. 2018. Impact of particle size and polydispersity index on the clinical applications of lipidic nanocarrier systems. Pharmaceutics 10:57.
  • Demir, E., G. Vales, B. Kaya, A. Creus, and R. Marcos. 2011. Genotoxic analysis of silver nanoparticles in Drosophila. Nanotoxicology 5 (3):417–24. doi:10.3109/17435390.2010.529176.
  • Demir, E., F. Turna, B. Kaya, A. Creus, and R. Marcos. 2013. Mutagenic/recombinogenic effects of four lipid peroxidation products in Drosophila. Food Chem. Toxicol 53:221–27. doi:10.1016/j.fct.2012.11.053.
  • Demir, E., F. Turna, S. Aksakal, B. Kaya, and R. Marcos. 2014. Genotoxicity of different sweeteners in Drosophila. Fresenius. Environ. Bull 23:3426–32.
  • Demir, E., and R. Marcos. 2018. Antigenotoxic potential of boron nitride nanotubes. Nanotoxicology 12 (8):868–84. doi:10.1080/17435390.2018.1482379.
  • Demir, E. 2020a. An in vivo study of nanorod, nanosphere, and nanowire forms of titanium dioxide using Drosophila melanogaster: Toxicity, cellular uptake, oxidative stress, and DNA damage. J. Toxicol. Environ. Health Part A 83 (11–12):456–69. doi:10.1080/15287394.2020.1777236.
  • Demir, E. 2020b. Drosophila as a model for assessing nanopesticide toxicity. Nanotoxicology 14 (9):1271–79. doi:10.1080/17435390.2020.1815886.
  • Demir, E. 2021. Adverse biological effects of ingested polystyrene microplastics using Drosophila melanogaster as a model in vivo organism. J. Toxicol. Environ. Health A 84 (16):649–60. doi:10.1080/15287394.2021.1913684.
  • Dikilitas, M., and A. Kocyigit. 2012. Assessment of computerized and manual analysis of slides processed in single cell gel electrophoresis assay. Fresenius. Environ. Bull 21:2981–87.
  • Du, J., S. Gan, Q. Bian, F. D, Y. Wei, K. Wang, Q. Lin, W. Chen, and D. Huang. 2018. Preparation and characterization of porous hydroxyapatite/β-cyclodextrin-based polyurethane composite scaffolds for bone tissue engineering. J. Biomater. Appl 33 (3):402–09. doi:10.1177/0885328218797545.
  • EFSA. 2011. Committee, E.S. Guidance on the risk assessment of the application of nanoscience and nanotechnologies in the food and feed chain. EFSA J 9: 2140.
  • Espinoza, J. L., A. Takami, L. Q. Trung, S. Kato, and S. Nakao. 2012. Resveratrol prevents EBV transformation and inhibits the outgrowth of EBV-immortalized human B cells. Plos. One 7:e51306. doi:10.1371/journal.pone.0051306.
  • Frei, H., and F. E. Würgler. 1988. Statistical methods to decide whether mutagenicity test data from drosophila assays indicate a positive, negative, or inconclusive results. Mutat. Res 203 (4):297–308. doi:10.1016/0165-1161(88)90019-2.
  • Frei, H., and F. E. Würgler. 1995. Optimal experimental design and sample size for the statistical evaluation of data from somatic mutation and recombination tests (SMART) in Drosophila. Mutat. Res 334 (2):247–225. doi:10.1016/0165-1161(95)90018-7.
  • Ghani, N. R. N. A., A. N. M. Sazri, C. Y. Yee, N. Luddin, and K. T. Ponnuraj. 2019. Genotoxicity evaluation of locally produced nano-hydroxyapatite-silica: An in vitro study using the bacterial reverse mutation test. J. Int. Dent. Med. Res 7:12.
  • Ghosh, M., J. Manivannan, S. Sinha, A. Chakraborty, S. K. Mallick, M. Bandyopadhyay, and A. Mukherjee. 2012. In vitro and in vivo genotoxicity of silver nanoparticles. Mutat. Res 749 (1–2):60–69. doi:10.1016/j.mrgentox.2012.08.007.
  • Giordo, R., G. K. Nasrallah, O. Al-Jamal, P. Paliogiannis, and G. Pintus. 2020. Resveratrol inhibits oxidative stress and prevents mitochondrial damage induced by zinc oxide nanoparticles in zebrafish (Danio rerio). Int. J. Mol. Sci 21 (11):3838. doi:10.3390/ijms21113838.
  • Glavis-Bloom, J., M. Muhammed, and E. Mylonakis. 2010. Of model hosts and man: Using Caenorhabditis elegans, Drosophila melanogaster and Galleria mellonella as model hosts for infectious disease research. Adv. Exp. Med. Biol 710:11–17.
  • Graf, U., F. E. Würgler, A. J. Katz, H. Frei, H. Juan, C. B. Hall, and P. G. Kale. 1984. Somatic mutation and recombination test inDrosophila melanogaster. Environ. Mutagen 6 (2):153–88. doi:10.1002/em.2860060206.
  • Graf, U., S. K, J. Abraham, and F. E. W. Guzmán-Rincón. 1998. Antigenotoxicity studies in Drosophila melanogaster. Mutat. Res 402 (1–2):203–09. doi:10.1016/S0027-5107(97)00298-4.
  • Huang, L. H., X. Y. Sun, and J. M. Ouyang. 2019. Shape-dependent toxicity and mineralization of hydroxyapatite nanoparticles in A7R5 aortic smooth muscle cells. Sci Rep 9 (1):1–18. doi:10.1038/s41598-019-55428-9.
  • Hung, C. F., Y. K. Lin, Z. R. Huang, and J. Y. Fang. 2008. Delivery of resveratrol, a red wine polyphenol, from solutions and hydrogels via the skin. Biol. Pharm. Bull 31 (5):955–62. doi:10.1248/bpb.31.955.
  • Irving, P., J. M. Ubeda, D. Doucet, L. Troxler, M. Lagueux, D. Zachary, J. A. Hoffmann, C. Hetru, and M. Meister. 2005. New insights into Drosophila larval haemocyte functions through genome-wide analysis. Cell. Microbiol 7 (3):335–50. doi:10.1111/j.1462-5822.2004.00462.x.
  • Johnson, W. D., R. L, A. L. U. Morrissey, I. Kapetanovic, J. A. Crowell, M. Muzzio, and D. L. McCormick. 2011. Subchronic oral toxicity and cardiovascular safety pharmacology studies of resveratrol, a naturally occurring polyphenol with cancer preventive activity. Food Chem. Toxicol 49 (12):3319–27. doi:10.1016/j.fct.2011.08.023.
  • Kalita, S. J., A. Bhardwaj, and H. A. Bhatt. 2007. Nanocrystalline calcium phosphate ceramics in biomedical engineering. Mate.r Sci. Eng. C 27 (3):441–49. doi:10.1016/j.msec.2006.05.018.
  • Kantharia, N., S. Naik, S. Apte, M. Kheur, S. Kheur, and B. Kale. 2014. Nano-hydroxyapatite and its contemporary applications. J. Dent. Res. Sci. Develop 1 (1):15–19. doi:10.4103/2348-3407.126135.
  • Kavasi, R. M., C. C. Coelho, V. Platania, P. A. Quadros, and M. Chatzinikolaidou. 2021. In vitro biocompatibility assessment of nano-hydroxyapatite. Nanomaterials 11 (5):1152. doi:10.3390/nano11051152.
  • Kermanizadeh, A., I. Gosens, L. MacCalman, H. Johnston, P. H. Danielsen, N. R. Jacobsen, A. G. Lenz, T. Fernandes, R. P. Schins, F. R. Cassee, et al. 2016. A multilaboratory toxicological assessment of a panel of 10 engineered nanomaterials to human health—ENPRA project—the highlights, limitations, and current and future challenges. J. Toxicol. Environ. Health B 19 (1):1–28. doi:10.1080/10937404.2015.1126210.
  • Kermanizadeh, A., L. G. Powell, and V. Stone. 2020. A review of hepatic nanotoxicology - summation of recent findings and considerations for the next generation of study designs. J. Toxicol. Environ. Health B 23 (4):137–76. doi:10.1080/10937404.2020.1751756.
  • Khalid, S., N. Afzal, J. A. Khan, Z. Hussain, A. S. Qureshi, H. Anwar, and Y. Jamil. 2018. Antioxidant resveratrol protects against copper oxide nanoparticle toxicity in vivo. Naunyn-Schmiedeb. Arch. Pharmacol 391 (10):1053–62. doi:10.1007/s00210-018-1526-0.
  • Kim, K. B., S. J. Kwack, J. Y. Lee, S. Kacew, and B. M. Lee. 2021. Current opinion on risk assessment of cosmetics. J. Toxicol. Environ. Health B 24 (4):137–61. doi:10.1080/10937404.2021.1907264.
  • Końca, K., A. Lankoff, A. Banasik, H. Lisowska, T. Kuszewski, S. Góźdź, Z. Koza, and A. Wojcik. 2003. A cross-platform public domain PC image-analysis program for the comet assay. Mutat. Res. Genet. Toxicol. Environ. Mutagen 534 (1–2):15–20. doi:10.1016/S1383-5718(02)00251-6.
  • Krajnak, K. 2020. Frequency-dependent changes in mitochondrial number and generation of reactive oxygen species in a rat model of vibration-induced injury. J. Toxicol. Environ. Health. Part A 83 (1):20–35. doi:10.1080/15287394.2020.1718043.
  • Kumar, S., C. Gautam, V. K. Mishra, B. S. Chauhan, S. Srikrishna, R. S. Yadav, R. Trivedi, and S. B. Rai. 2019. Fabrication of graphene nanoplatelet-incorporated porous hydroxyapatite composites: Improved mechanical and in vivo imaging performances for emerging biomedical applications. ACS. Omega 4 (4):7448–58. doi:10.1021/acsomega.8b03473.
  • Levinson, S., and R. L. Cagan. 2016. Drosophila cancer models identify functional differences between ret fusions. Cell Rep 16 (11):3052–61. doi:10.1016/j.celrep.2016.08.019.
  • Li, X., W. Liu, L. Sun, K. E. Aifantis, B. Yu, Y. Fan, Q. Feng, F. Cui, and F. Watari. 2015. Effects of physicochemical properties of nanomaterials on their toxicity. J. Biomed. Mater. Res. Part A 103 (7):2499–507. doi:10.1002/jbm.a.35384.
  • Lindsley, D. L., and G. G. Zimm. 1992. The genome of Drosophila melanogaster. San Diego, CA: Academic Press.
  • Liu, Y., Y. L. Wang, S. W. He, M. H. Chen, Z. Zhang, X. P. Fu, B. B. Fu, B. Q. Liao, Y. H. Lin, Z. Q. Qi, et al. 2017. Protective effects of resveratrol against mancozeb induced apoptosis damage in mouse oocytes. Oncotarget 8 (4):6233–45. doi:10.18632/oncotarget.14056.
  • Liu, Y., P. Bhattarai, Z. Dai, and X. Chen. 2019. Photothermal therapy and photoacoustic imaging via nanotheranostics in fighting cancer. Chem Soc Rev 48 (7):2053–108. doi:10.1039/c8cs00618k.
  • Macedo, G. E., P. D. B. Vieira, N. R. Rodrigues, K. K. Gomes, J. F. Rodrigues, J. L. Franco, and T. Posser. 2022. Effect of fungal indoor air pollutant 1-octen-3-ol on levels of reactive oxygen species and nitric oxide as well as dehydrogenases activities in Drosophila melanogaster males. J. Toxicol. Environ. Health. Part A 85 (14):573–85. doi:10.1080/15287394.2022.2054887.
  • Meng, C. Y., Y. F. Han, Y. L. Liu, H. X. Gao, Y. Y. Ren, Q. Z. Qian, Q. Wang, and Q. Z. Li. 2019. Resveratrol alleviate the injury of mice liver induced by cadmium sulfide nanoparticles. Kaohsiung J. Med. Sci 35 (5):297–302. doi:10.1002/kjm2.12056.
  • Mosa, I. F., H. H. Abd, A. Abuzreda, N. Assaf, and A. B. Yousif. 2020. Bio-evaluation of the role of chitosan and curcumin nanoparticles in ameliorating genotoxicity and inflammatory responses in rats’ gastric tissue followed hydroxyapatite nanoparticles’ oral uptake. Toxicol. Res 9 (4):493–508. doi:10.1093/toxres/tfaa054.
  • Mukhopadhyay, I., D. K, M. B. Chowdhuri, and A. Dhawan. 2004. Evaluation of in vivo genotoxicity of cypermethrin in Drosophila melanogaster using the alkaline comet assay. Mutagenesis 19 (2):85–90. doi:10.1093/mutage/geh007.
  • Munir, M. U., S. Salman, I. Javed, S. N. A. Bukhari, N. Ahmad, N. A. Shad, and F. Aziz. 2021. Nano-hydroxyapatite as a delivery system: Overview and advancements. Artif. Cells. Nanomed. Biotechnol 49 (1):717–27. doi:10.1080/21691401.2021.2016785.
  • Pandey, U. B., and C. D. Nichols. 2011. Human disease models in Drosophila melanogaster and the role of the fly in therapeutic drug discovery. Pharmacol. Rev 63:411–36. doi:10.1124/pr.110.003293.
  • Pandey, A., S. Chandra, L. K. S, G. Chauhan, and D. K. C. Narayan. 2013. Cellular internalization and stress response of ingested amorphous silica nanoparticles in the midgut of Drosophila melanogaster. Biochim. Biophys. Acta. Gen. Subj 1830 (1):2256–66. doi:10.1016/j.bbagen.2012.10.001.
  • Paolillo, R., R. C. Carratelli, and A. Rizzo. 2011. Effects of resveratrol and quercetin in experimental infection by Salmonella enteric serovartyphimurium. Int. Immunopharmacol 11 (2):149–56. doi:10.1016/j.intimp.2010.10.019.
  • Pappus, S. A., B. Ekka, S. Sahu, D. Sabat, P. Dash, and M. Mishra. 2017. A toxicity assessment of hydroxyapatite nanoparticles on development and behaviour of Drosophila melanogaster. J. Nanopart. Res 19 (4):136. doi:10.1007/s11051-017-3824-8.
  • Peritore, C. S., A. Ho, S. E. Schaus, and S. E. Schaus. 2012. Resveratrol attenuates L-DOPA-induced hydrogen peroxide toxicity in neuronal cells. Neuroreport 23 (17):989–94. doi:10.1097/WNR.0b013e32835a4ea4.
  • Qian, C. P., J. H. Ma, P. H. Zhang, A. T. Luo, C. Wang, Z. Q. Ren, L. H. Kong, S. Zhang, X. J. Wang, and Y. Wu. 2012. Resveratrol attenuates the Na+ dependent intracellular Ca2+ overload by inhibiting H2O2-induced increase in late sodium current in ventricular myocytes. Plos. One 7 (12):12. doi:10.1371/journal.pone.0051358.
  • Rauf, A., M. Imran, M. S. Butt, M. Nadeem, D. G. Peters, and M. S. Mubarak. 2018. Resveratrol as an anti-cancer agent: A review. Crit Rev Food Sci Nutr 58 (9):1428–47. doi:10.1080/10408398.2016.1263597.
  • Reddy, L. H., J. L. Arias, J. Nicolas, and P. Couvreur. 2012. Magnetic nanoparticles: Design and characterization, toxicity and biocompatibility, pharmaceutical and biomedical applications. Chem. Rev 112 (11):5818–78. doi:10.1021/cr300068p.
  • Remya, N. S., S. Syama, V. Gayathri, H. K. Varma, and P. V. Mohanan. 2011. An in vitro study on the interaction of hydroxyapatite nanoparticles and bone marrow mesenchymal stem cells for assessing the toxicological behavior. Colloids. Surf. B 117:389–97. doi:10.1016/j.colsurfb.2014.02.004.
  • Remya, N. S., S. Syama, A. Sabareeswaran, and P. V. Mohanan. 2017. Investigation of chronic toxicity of hydroxyapatite nanoparticles administered orally for one year in Wistar rats. Mate.r Sci. Eng. C 76:518–27. doi:10.1016/j.msec.2017.03.076.
  • San Miguel, S. M., L. A. Opperman, E. P. Allen, J. Zielinski, and K. K. H. Svoboda. 2012. Bioactive polyphenol antioxidants protect oral fibroblasts from ROS-inducing agents. Arch. Oral Biol 57 (12):1657–67. doi:10.1016/j.archoralbio.2012.04.021.
  • Sebastià, N., M. Almonacid, J. I. Villaescusa, J. Cervera, E. Such, M. A. Silla, J. M. Soriano, and A. Montoro. 2013. Radioprotective activity and cytogenetic effect of resveratrol in human lymphocytes: An in vitro evaluation. Food Chem. Toxicol 51:391–95. doi:10.1016/j.fct.2012.10.013.
  • Severino, P., J. F. Fangueiro, M. V. Chaud, J. Cordeiro, A. M. Silva, and E. B. Souto. 2016. Advances in nanobiomaterials for topical administrations: New galenic and cosmetic formulations. In Nanobiomaterials in galenic formulations and cosmetics, ed. A. Grumezescu, 1–23. Amsterdam, The Netherlands: Elsevier.
  • Sgambato, A., R. Ardito, B. Faraglia, A. Boninsegna, F. I. Wolf, and A. Cittadini. 2001. Resveratrol, a natural phenolic compound, inhibits cell proliferation and prevents oxidative DNA damage. Mutat. Res 469 (1–2):171–80. doi:10.1016/S1383-5718(01)00232-7.
  • Shi, G., L. Rao, H. Yu, H. Xiang, H. Yang, and R. Ji. 2008. Stabilization and encapsulation of photosensitive resveratrol within yeast cell. Int J Pharm 349 (1–2):83–93. doi:10.1016/j.ijpharm.2007.07.044.
  • Shi, Z., X. Huang, Y. Cai, R. Tang, and D. Yang. 2009. Size effect of hydroxyapatite nanoparticles on proliferation and apoptosis of osteoblast-like cells. Acta. Biomater 5 (1):338–45. doi:10.1016/j.actbio.2008.07.023.
  • Shin, S. W., I. H. Song, and S. H. Um. 2015. Role of physicochemical properties in nanoparticle toxicity. Nanomaterials 5 (3):1351–65. doi:10.3390/nano5031351.
  • Shin, J. W., H. S. Lee, J. I. Na, C. H. Huh, K. C. Park, and H. R. Choi. 2020. Resveratrol inhibits particulate matter-induced inflammatory responses in human keratinocytes. Int. J. Mol. Sci 21 (10):3446. doi:10.3390/ijms21103446.
  • Siddique, H. R., D. K. Chowdhuri, D. K. Saxena, and A. Dhawan. 2005. Validation of Drosophila melanogaster as an in vivo model for genotoxicity assessment using modified alkaline comet assay. Mutagenesis 20 (4):285–90.
  • Siddique, Y. H., W. Khan, S. Khanam, S. Jyoti, F. Naz Rahul, B. R. Singh, A. H. Nagvi, and A. H. Naqvi. 2014. Toxic potential of synthesized graphene zinc oxide nanocomposite in the third instar larvae of transgenic Drosophila melanogaster (hsp70-lacZ)Bg9. Biomed. Res. Int 2014:382124. doi:10.1155/2014/382124.
  • 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 (1):184–91. doi:10.1016/0014-4827(88)90265-0.
  • Singh, A., R. Kukreti, L. Saso, and S. Kukreti. 2019. Oxidative stress: A key modulator in neurodegenerative diseases. Molecules 24 (8):1583. doi:10.3390/molecules24081583.
  • Sonmez, E., I. Cacciatore, F. Bakan, H. Turkez, Y. I. Mohtar, B. Togar, and A. D. Stefano. 2016. Toxicity assessment of hydroxyapatite nanoparticles in rat liver cell model in vitro. Human. Exp. Toxicol 35 (10):1073–83. doi:10.1177/0960327115619770.
  • Sreedhar, A., L. Aguilera-Aguirre, and K. K. Singh. 2020. Mitochondria in skin health, aging, and disease. Cell. Death. Dis 11 (6):1–14. doi:10.1038/s41419-020-2649-z.
  • Tao, Z. S., W. S. Zhou, M. Yang, and H. Xu. 2020. Resveratrol reverses the negative effect of alcohol on hydroxyapatite-coated implant osseointegration in senile female rats. Z. Gerontol. Geriatr 53 (6):538–45. doi:10.1007/s00391-019-01595-3.
  • Teixeira, S., M. A. Rodriguez, P. Pena, A. H. De Aza, S. De Aza, M. P. Ferraz, and F. J. Monteiro. 2009. Physical characterization of hydroxyapatite porous scaffolds for tissue engineering. Mate.r Sci. Eng. C 29 (5):1510–14. doi:10.1016/j.msec.2008.09.052.
  • Tice, R. R., P. W. Andrews, and N. P. Singh. 1990. The single cell gel assay. A sensitive technique for evaluating intercellular differences in DNA damage and repair B.M. In DNA damage and repair in human tissues, ed. A. D. W. Sutherland, 291–302. New York, NY: Plenum.
  • Turna, F., S. Aksakal, E. Demir, and B. Kaya. 2014. Antigenotoxic effects of resveratrol in somatic cells of Drosophila melanogaster. Fresenius. Environ. Bull 23:2116–25.
  • Turna Demir, F., and M. Yavuz. 2020. Heavy metal accumulation and genotoxic effects in levant vole (Microtus guentheri) collected from contaminated areas due to mining activities. Environ. Pollut 256:113378. doi:10.1016/j.envpol.2019.113378.
  • Turna Demir, F. 2022. In vivo effects of 1,4-dioxane on genotoxic parameters and behavioral alterations in Drosophila melanogaster. J. Toxicol. Environ. Health A 85 (10):414–30. doi:10.1080/15287394.2022.2027832.
  • Vales, G., E. Demir, B. Kaya, A. Creus, and R. Marcos. 2013. In vivo effects of 1,4-dioxane on genotoxic parameters and behavioral alterations in Drosophila melanogaster. Nanotoxicology 7 (4):462–68. doi:10.3109/17435390.2012.689882.
  • Vervandier-Fasseur, D., and N. Latruffe. 2019. The potential use of resveratrol for cancer prevention. Molecules 24 (24):4506. doi:10.3390/molecules24244506.
  • Virk, P., N. A. R. Al-Mukhaizeem, S. H. B. Morebah, D. Fouad, and M. Elobeid. 2020. Protective effect of resveratrol against toxicity induced by the mycotoxin, zearalenone in a rat model. Food Chem. Toxicol 146:111840. doi:10.1016/j.fct.2020.111840.
  • Volobaev, V., S. Bach, E. Shchetnikova, E. Vdovina, A. Rosinskiy, and A. Larionov. 2021. Short/long-term cryopreservation prior to comet assay of whole-blood leukocytes and in vitro -cultured lung fibroblasts. Toxicol. Mech. Meth 31 (7):531–37. doi:10.1080/15376516.2021.1933286.
  • Wu, T., Q. Zhan, T. Zhang, S. Ang, J. Ying, K. He, S. Zhang, Y. Xue, and M. Tang. 2017. The protective effects of resveratrol, H2S and thermotherapy on the cell apoptosis induced by CdTe quantum dots. Toxicol. In Vitro 41:106–13. doi:10.1016/j.tiv.2017.02.013.
  • Wu, V. M., and V. Uskoković. 2017. Population effects of calcium phosphate nanoparticles in Drosophila melanogaster: The effects of phase composition, crystallinity, and the pathway of formation. ACS. Biomater. Sci. Eng 3 (10):2348–57. doi:10.1021/acsbiomaterials.7b00540.
  • Wu, G., X. Chen, X. Ma, and L. Liu. 2019. Toxicity evaluation of CdSe nanorods on macrophages and the protective effect of resveratrol. J. Nanopart. Res 21 (2):1–10. doi:10.1007/s11051-019-4473-x.
  • Xiao, X., W. Wang, D. Liu, H. Zhang, P. Gao, L. Geng, Z. Wang, J. Lu, and Z. Wang. 2015. The promotion of angiogenesis induced by three-dimensional porous beta-tricalcium phosphate scaffold with different interconnection sizes via activation of PI3K/ Akt pathways. Sci Rep 5 (1):9409. doi:10.1038/srep09409.
  • Xing, F., Z. Chi, R. Yang, D. Xu, J. Cui, Y. Huang, C. Zhou, and C. Liu. 2021. Chitin-hydroxyapatite-collagen composite scaffolds for bone regeneration. Int. J. Biol. Macromol 184:170–80. doi:10.1016/j.ijbiomac.2021.05.019.
  • Yan, Y., J. Yang, G. Chen, Y. Mou, Y. Zhao, L. Pan, C. Ma, X. Liu, and C. Wu. 2011. Protection of resveratrol and its analogues against ethanol-induced oxidative DNA damage in human peripheral lymphocytes. Mutat. Res 721 (2):171–77. doi:10.1016/j.mrgentox.2011.01.012.
  • Yan, J., C. Wang, X. Jiang, Y. Wei, Q. Wang, K. Cui, X. Xu, F. Wang, and L. Zhang. 2021. Application of phototherapeutic-based nanoparticles in colorectal cancer. Int. J. Biol. Sci 17 (5):1361–81. doi:10.7150/ijbs.58773.
  • Yousef, M. I., H. H. Abd, Y. M. Helmy, and M. A. Kamel. 2021. Synergistic effect of curcumin and chitosan nanoparticles on nano-hydroxyapatite-induced reproductive toxicity in rats. Environ. Sci. Pollut. Res. Int 28 (8):9362–76. doi:10.1007/s11356-020-11395-7.
  • Zaffaroni, N., and G. L. Beretta. 2021. Resveratrol and prostate cancer: The power of phytochemicals. Curr. Med. Chem 28 (24):4845–62. doi:10.2174/0929867328666201228124038.
  • Zhang, W., J. Xue, M. Ge, M. Yu, L. Liu, and Z. Zhang. 2013. Resveratrol attenuates hepatotoxicity of rats exposed to arsenic trioxide. Food. ChemToxicol 51:87–92. doi:10.1016/j.fct.2012.09.023.
  • Zhao, J., and V. Castranova. 2011. Toxicology of nanomaterials used in nanomedicine. Journal of Toxicology and Environmental Health, Part B 14 (8):593–632. doi:10.1080/10937404.2011.615113.
  • Zhao, X., K. J. Ong, J. D. Ede, J. L. Stafford, K. W. Ng, G. G. Goss, and S. C. J. Loo. 2013. Evaluating the toxicity of hydroxyapatite nanoparticles in catfish cells and zebrafish embryos. Small 9 (9–10):1734–41. doi:10.1002/smll.201200639.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.