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Food Science & Technology

Copper content lower than safety factor 100-fold of acceptable daily intake negatively affects Drosophila melanogaster fruit flies’ nervous function

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Article: 2345436 | Received 17 Jun 2023, Accepted 16 Apr 2024, Published online: 25 Apr 2024

References

  • 56FR26548. (1991). 40 CFR Parts 141 and 142, drinking water regulations maximum contaminant level goals and national primary drinking water reguiations for lead and copper. Federal Register. https://archives.federalregister.gov/issue_slice/1991/6/7/26457-26582.pdf#page=92
  • Council Directive 98/83/EC of 3 November 1998 on the quality of water intended for human consumption, 98/83/EC. (1998). The Council of the European Union 1998.
  • Abdullmajed, H., Al-Ahmad, A., & Hussain, K. (2011). The preparation, characterization and the study of the linear optical properties of a new azo compound. Journal of Basrah Researches. (Sciences), 37, 64.
  • Abolaji, A. O., Fasae, K. D., Iwezor, C. E., Aschner, M., & Farombi, E. O. (2020). Curcumin attenuates copper-induced oxidative stress and neurotoxicity in Drosophila melanogaster. Toxicology Reports, 7, 261–268. https://doi.org/10.1016/j.toxrep.2020.01.015
  • Aebi, H. (1984). [13] Catalase in vitro. In Methods enzymol (Vol. 105, pp. 121–126). Academic Press.
  • Anthony, R. W., Gerd, M., Fran, M., Shayne, B., James, C., Hui, Z., Ashley, I. B., Konrad, B., Colin, L. M., & Roberto, C. (1999). The Alzheimer’s disease amyloid precursor protein modulates copper-induced toxicity and oxidative stress in primary neuronal cultures. Journal of Neuroscience. 19(21), 9170–9179. https://doi.org/10.1523/JNEUROSCI.19-21-09170.1999
  • Armstrong, J. S. (2006). The role of the mitochondrial permeability transition in cell death. Mitochondrion, 6(5), 225–234. https://doi.org/10.1016/j.mito.2006.07.006
  • Bag, J., & Mishra, M. (2020). Biochemical assays to detect the antioxidant level in Drosophila melanogaster. In M. Mishra (Ed.), Fundamental approaches to screen abnormalities in Drosophila (pp. 151–168). Springer US.
  • Behzadfar, L., Abdollahi, M., Sabzevari, O., Hosseini, R., Salimi, A., Naserzadeh, P., Sharifzadeh, M., & Pourahmad, J. (2017). Potentiating role of copper on spatial memory deficit induced by beta amyloid and evaluation of mitochondrial function markers in the hippocampus of rats. Metallomics: integrated Biometal Science, 9(7), 969–980. https://doi.org/10.1039/c7mt00075h
  • Ben Younes, S., & Sayadi, S. (2011). Purification and characterization of a novel trimeric and thermotolerant laccase produced from the ascomycete Scytalidium thermophilum strain. Journal of Molecular Catalysis B: Enzymatic. 73(1-4), 35–42. https://doi.org/10.1016/j.molcatb.2011.07.014
  • Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1-2), 248–254. https://doi.org/10.1016/0003-2697(76)90527-3
  • Cristóvão, J. S., Santos, R., & Gomes, C. M. (2016). Metals and neuronal metal binding proteins implicated in Alzheimer’s disease. Oxidative Medicine and Cellular Longevity, 2016, 9812178. https://doi.org/10.1155/2016/9812178
  • Davis, J. A., Gift, J. S., & Zhao, Q. J. (2011). Introduction to benchmark dose methods and U.S. EPA’s benchmark dose software (BMDS) version 2.1.1. Toxicology and Applied Pharmacology, 254(2), 181–191. https://doi.org/10.1016/j.taap.2010.10.016
  • de Lima, D., Roque, G. M., & de Almeida, E. A. (2013). In vitro and in vivo inhibition of acetylcholinesterase and carboxylesterase by metals in zebrafish (Danio rerio). Marine Environmental Research, 91, 45–51. https://doi.org/10.1016/j.marenvres.2012.11.005
  • Desai, V., & Kaler, S. G. (2008). Role of copper in human neurological disorders. The American Journal of Clinical Nutrition, 88(3), 855S–858S. https://doi.org/10.1093/ajcn/88.3.855S
  • Dounce, A. L. (1983). A proposed mechanism for the catalatic ation of catalase. Journal of Theoretical Biology, 105(4), 553–567. https://doi.org/10.1016/0022-5193(83)90219-9
  • Eskici, G., & Axelsen, P. H. (2012). Copper and oxidative stress in the pathogenesis of Alzheimer’s disease. Biochemistry, 51(32), 6289–6311. https://doi.org/10.1021/bi3006169
  • Frasco, M. F., Fournier, D., Carvalho, F., & Guilhermino, L. (2005). Do metals inhibit acetylcholinesterase (AChE)? Implementation of assay conditions for the use of AChE activity as a biomarker of metal toxicity. Biomarkers: biochemical Indicators of Exposure, Response, and Susceptibility to Chemicals, 10(5), 360–375. https://doi.org/10.1080/13547500500264660
  • Fukui, K., Onodera, K., Shinkai, T., Suzuki, S., & Urano, S. (2001). Impairment of learning and memory in rats caused by oxidative stress and aging, and changes in antioxidative defense systems. Annals of the New York Academy of Sciences, 928(1), 168–175. https://doi.org/10.1111/j.1749-6632.2001.tb05646.x
  • Gemma, C., Vila, J., Bachstetter, A., & Bickford, P. C. (2007). Frontiers in neuroscience oxidative stress and the aging brain: From theory to prevention. In D. R. Riddle (Ed.), Brain aging: Models, methods, and mechanisms. CRC Press/Taylor & Francis.
  • Haddadi, M., Jahromi, S. R., Sagar, B. K. C., Patil, R. K., Shivanandappa, T., & Ramesh, S. R. (2014). Brain aging, memory impairment and oxidative stress: A study in Drosophila melanogaster. Behavioural Brain Research, 259, 60–69. https://doi.org/10.1016/j.bbr.2013.10.036
  • Halmenschelager, P. T., & da Rocha, J. B. T. (2019). Biochemical CuSO(4) toxicity in Drosophila melanogaster depends on sex and developmental stage of exposure. Biological Trace Element Research, 189(2), 574–585. https://doi.org/10.1007/s12011-018-1475-y
  • Haverroth, G. M. B., Welang, C., Mocelin, R. N., Postay, D., Bertoncello, K. T., Franscescon, F., Rosemberg, D. B., Dal Magro, J., & Dalla Corte, C. L. (2015). Copper acutely impairs behavioral function and muscle acetylcholinesterase activity in zebrafish (Danio rerio). Ecotoxicology and Environmental Safety, 122, 440–447. https://doi.org/10.1016/j.ecoenv.2015.09.012
  • Hwang, J. E. C., de Bruyne, M., Warr, C. G., & Burke, R. (2014). Copper overload and deficiency both adversely affect the central nervous system of Drosophila. Metallomics: integrated Biometal Science, 6(12), 2223–2229. https://doi.org/10.1039/C4MT00140K
  • Jordan, K. W., Craver, K. L., Magwire, M. M., Cubilla, C. E., Mackay, T. F. C., & Anholt, R. R. H. (2012). Genome-wide association for sensitivity to chronic oxidative stress in Drosophila melanogaster. PloS One, 7(6), e38722. https://doi.org/10.1371/journal.pone.0038722
  • Klimaczewski, C. V., Ecker, A., Piccoli, B., Aschner, M., Barbosa, N. V., & Rocha, J. B. T. (2018). Peumus boldus attenuates copper-induced toxicity in Drosophila melanogaster. Biomedicine & Pharmacotherapy = Biomedecine & pharmacotherapie, 97, 1–8. https://doi.org/10.1016/j.biopha.2017.09.130
  • Lee, B.-M., Kacew, S., & Kim, H. S. (2017). Lu’s basic toxicology: Fundamentals, target organs, and risk assessment. CRC Press.
  • Letelier, M. E., Sánchez-Jofré, S., Peredo-Silva, L., Cortés-Troncoso, J., & Aracena-Parks, P. (2010). Mechanisms underlying iron and copper ions toxicity in biological systems: Pro-oxidant activity and protein-binding effects. Chemico-Biological Interactions, 188(1), 220–227. https://doi.org/10.1016/j.cbi.2010.06.013
  • Lu, Q., Zhang, Y., Zhao, C., Zhang, H., Pu, Y., & Yin, L. (2022). Copper induces oxidative stress and apoptosis of hippocampal neuron via pCREB/BDNF/and Nrf2/HO-1/NQO1 pathway. Journal of Applied Toxicology: JAT, 42(4), 694–705. https://doi.org/10.1002/jat.4252
  • Mirzoyan, Z., Sollazzo, M., Allocca, M., Valenza, A. M., Grifoni, D., & Bellosta, P. (2019). Drosophila melanogaster: A model organism to study cancer. Frontiers in Genetics, 10, 51. https://doi.org/10.3389/fgene.2019.00051
  • Mukherjee, S., & Mishra, M. (2020). Biochemical estimation to detect the metabolic pathways of Drosophila. In M. Mishra (Ed.), Fundamental approaches to screen abnormalities in Drosophila (pp. 135–149). Springer US.
  • Najimi, S., Bouhaimi, A., Daubèze, M., Zekhnini, A., Pellerin, J., Narbonne, J. F., & Moukrim, A. (1997). Use of acetylcholinesterase in Perna perna and Mytilus galloprovincialis as a biomarker of pollution in Agadir Marine Bay (South of Morocco). Bulletin of Environmental Contamination and Toxicology, 58(6), 901–908. https://doi.org/10.1007/s001289900419
  • Nunes, B. (2011). The use of cholinesterases in ecotoxicology. In D. M. Whitacre (Ed.), Reviews of environmental contamination and toxicology (Vol. 12, pp. 29–59). Springer New York.
  • Oliveira, C. S., Nogara, P. A., Lima, L. S., Galiciolli, M. E. A., Souza, J. V., Aschner, M., & Rocha, J. B. T. (2022). Toxic metals that interact with thiol groups and alteration in insect behavior. Current Opinion in Insect Science, 52, 100923. https://doi.org/10.1016/j.cois.2022.100923
  • Pandey, U. B., & Nichols, C. D. (2011). Human disease models in Drosophila melanogaster and the role of the fly in therapeutic drug discovery. Pharmacological Reviews, 63(2), 411–436. https://doi.org/10.1124/pr.110.003293
  • Pepeu, G., & Giovannini, M. G. (2004). Changes in acetylcholine extracellular levels during cognitive processes. Learning & Memory (Cold Spring Harbor, N.Y.), 11(1), 21–27. https://doi.org/10.1101/lm.68104
  • Pilehvar, A., Town, R. M., & Blust, R. (2020). The effect of copper on behaviour, memory, and associative learning ability of zebrafish (Danio rerio). Ecotoxicology and Environmental Safety, 188, 109900. https://doi.org/10.1016/j.ecoenv.2019.109900
  • Pyle, G. G., & Mirza, R. S. (2007). Copper-impaired chemosensory function and behavior in aquatic animals. Human & Ecological Risk Assessment. 13(3), 492–505. https://doi.org/10.1080/10807030701340995
  • QCVN. (2009). National technical regulation on drinking water quality (Vol. QCVN 01:2009/BYT). Ministry of Health of Viet Nam.
  • Riaz, B., Zahoor, M. K., Zahoor, M. A., Majeed, H. N., Javed, I., Ahmad, A., Jabeen, F., Zulhussnain, M., & Sultana, K. (2018). Toxicity, phytochemical composition, and enzyme inhibitory activities of some Indigenous weed plant extracts in fruit fly, Drosophila melanogaster. Evidence-Based Complementary and Alternative Medicine: eCAM, 2018, 2325659–2325611. https://doi.org/10.1155/2018/2325659
  • Siddique, Y. H., Haidari, M., Khan, W., Fatima, A., Jyoti, S., Khanam, S., Naz, F., Rahul, Ali, F., Singh, B. R., Beg, T., Mohibullah, & Naqvi, A. H. 2015. Toxic potential of copper-doped ZnO nanoparticles in Drosophila melanogaster (Oregon R). Toxicology Mechanisms and Methods, 25(6), 425–432. https://doi.org/10.3109/15376516.2015.1045653
  • Sparks, D. L., & Schreurs, B. G. (2003). Trace amounts of copper in water induce β-amyloid plaques and learning deficits in a rabbit model of Alzheimer’s disease. Proceedings of the National Academy of Sciences of the United States of America, 100(19), 11065–11069. https://doi.org/10.1073/pnas.1832769100
  • Squitti, R., Lupoi, D., Pasqualetti, P., Forno, G. D., Vernieri, F., Chiovenda, P., Rossi, L., Cortesi, M., Cassetta, E., & Rossini, P. M. (2002). Elevation of serum copper levels in Alzheimer’s disease. Neurology, 59(8), 1153–1161. https://doi.org/10.1212/wnl.59.8.1153
  • Strausak, D., Mercer, J. F. B., Dieter, H. H., Stremmel, W., & Multhaup, G. (2001). Copper in disorders with neurological symptoms: Alzheimer’s, Menkes, and Wilson diseases. Brain Research Bulletin, 55(2), 175–185. https://doi.org/10.1016/S0361-9230(01)00454-3
  • Sun, Q., Ying, M., Ma, Q., Huang, Z., Zou, L., Liu, J., Zhuang, Z., & Yang, X. (2016). Proteomic analysis of hippocampus in mice following long-term exposure to low levels of copper. Toxicology Research, 5(4), 1130–1139. https://doi.org/10.1039/c5tx00456j
  • Tanaka, D., Nakada, K., Takao, K., Ogasawara, E., Kasahara, A., Sato, A., Yonekawa, H., Miyakawa, T., & Hayashi, J.-I. (2008). Normal mitochondrial respiratory function is essential for spatial remote memory in mice. Molecular Brain, 1(1), 21. https://doi.org/10.1186/1756-6606-1-21
  • Taylor, P. (2017). Anticholinesterase agents. In L. L. Brunton, R. Hilal-Dandan, & B. C. Knollmann (Eds.), Goodman & Gilman’s: The pharmacological basis of therapeutics (13rd ed.). McGraw-Hill Education.
  • Tilton, F., Tilton, S. C., Bammler, T. K., Beyer, R., Farin, F., Stapleton, P. L., & Gallagher, E. P. (2008). Transcriptional biomarkers and mechanisms of copper-induced olfactory injury in zebrafish. Environmental Science & Technology, 42(24), 9404–9411. https://doi.org/10.1021/es801636v
  • Waggoner, D. J., Bartnikas, T. B., & Gitlin, J. D. (1999). The role of copper in neurodegenerative disease. Neurobiology of Disease, 6(4), 221–230. https://doi.org/10.1006/nbdi.1999.0250
  • Wong, R., Piper, M. D. W., Wertheim, B., & Partridge, L. (2009). Quantification of food intake in Drosophila. PloS One, 4(6), e6063. https://doi.org/10.1371/journal.pone.0006063
  • World Health Organization (WHO). (2004). Copper in drinking-water, background document for development of who guidelines for drinking-water quality (Vol. WHO/SDE/WSH/03.04/88). World Health Organization.
  • Yamaguchi, M., & Yoshida, H. (2018). Drosophila as a model organism. In Drosophila models for human diseases (pp. 1–10). Elsevier.
  • Yordanova, E. (2017). “In vitro” and “in vivo” inhibitory effect of copper sulphate upon the activity of blood catalase. Scripta Scientifica Medica, 11, 97–103. doi:https://doi.org/10.14748/ssm.v11i0.3553
  • Zamberlan, D. C., Halmenschelager, P. T., Silva, L. F. O., & da Rocha, J. B. T. (2020). Copper decreases associative learning and memory in Drosophila melanogaster. The Science of the Total Environment, 710, 135306. https://doi.org/10.1016/j.scitotenv.2019.135306
  • Zhang, T., Xu, L., Wu, J.-J., Wang, W.-M., Mei, J., Ma, X.-F., & Liu, J.-X. (2015). Transcriptional responses and mechanisms of copper-induced dysfunctional locomotor behavior in zebrafish embryos. Toxicological Sciences: An Official Journal of the Society of Toxicology, 148(1), 299–310. https://doi.org/10.1093/toxsci/kfv184