Skip to main content
Log in

Biochemical CuSO4 Toxicity in Drosophila melanogaster Depends on Sex and Developmental Stage of Exposure

  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

Copper is a transition metal that exists in different chemical forms (e.g., Cu2+,Cu+, and Cu0) and at high concentrations it is toxic. Here, we investigated the Cu2+-induced toxicity in Drosophila melanogaster, evaluating the survival, locomotion, and the activity of acetylcholinesterase (AChE) and glutathione S-transferase (GST) enzymes. Flies were exposed to Cu2+(0.1–1 mmol CuSO4/kg of diet or approximately 0.1–1 mM Cu2+) and allowed to mate during 24 h. GST and AChE enzymes were evaluated in the larvae and in the head and the body (thorax + abdomen) of the adult male and females flies. The total number of adult females (0.4–1 mM) and males (0.75 and 1 mM) was decreased by CuSO4. The climbing ability was hampered in flies exposed to 1 mM Cu2+. In larvae, Cu2+(0.4–1 mM) increased AChE activity (P < 0.002). In males’ heads, 0.4 mM Cu2+ increased the AChE activity (P < 0.01). In adults’ bodies, Cu2+inhibited the activity in both sexes, but with greater effectiveness in males (0.1 to 1 mM) than in females (1 mM). Regarding GST activity, 0.1 mM Cu2+increased, but 1 mM decrease GST in larvae. In the head of flies, Cu2+decreased the GST activity at intermediate (0.4 mM) and increased GST at the highest concentration (1 mM) in males. In the bodies, the effect of Cu2+was similar. In conclusion, Cu2+exposure in D. melanogaster disrupted locomotion and enzymatic parameters that can be related to changes in AChE and in the detoxifying GST enzyme.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  1. Linder MC, Hazegh-Azam M (1996) Copper biochemistry and molecular biology. Am J Clin Nutr 63:797S–811S

    CAS  PubMed  Google Scholar 

  2. Bahadorani S, Mukai S, Egli D, Hilliker AJ (2010) Overexpression of metal-responsive transcription factor (MTF-1) in Drosophila melanogaster ameliorates life-span reductions associated with oxidative stress and metal toxicity. Neurobiol Aging 31:1215–1226

    Article  CAS  PubMed  Google Scholar 

  3. Mercer SW, Wang J, Burke R (2017) In vivo modeling of the pathogenic effect of copper transporter mutations that cause Menkes and Wilson diseases, motor neuropathy, and susceptibility to Alzheimer’s disease. J Biol Chem 292(10):4113–4122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Schlichting D, Sommerfeld C, Müller-Graf C, Selhorst T, Greiner M, Gerofke A, Ulbig E, Gremse C, Spolders M, Schafft H, Lahrssen-Wiederholt M (2017) Copper and zinc content in wild game shot with lead or non-lead ammunition – implications for consumer health protection. PLoS One 12(9):e0184946

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Alaraby M, Hernández A, Marcos R (2017) Copper oxide nanoparticles and copper sulphate act as antigenotoxic agents in drosophila melanogaster. Environ Mol Mutagen 58(1):46–55

    Article  CAS  PubMed  Google Scholar 

  6. Eskici G, Axelsen PH (2012) Copper and oxidative stress in the pathogenesis of Alzheimer’s disease. Biochemistry 51:6289–6311

    Article  CAS  PubMed  Google Scholar 

  7. Ballinski MA, Woodruff R (2017) Differential sexual survival of Drosophila melanogaster on copper sulfate. Genetica 145:131–137

    Article  CAS  Google Scholar 

  8. Barceloux DG (1999) Copper. J Toxicol. Clin Toxicol 37(2):217–230

    Article  CAS  PubMed  Google Scholar 

  9. Montes S, Rivera-Mancia S, Diaz-ruiz A, Tristan-Lopez L, Rios C (2014) Copper and copper proteins in Parkinson’s disease. Oxidative Med Cell Longev 147251

  10. Osredkar J, Sustar N (2011) Copper and zinc, biological role and significance of copper/zinc imbalance. Journal of Clinical Toxicology S:3

  11. Squitti R, Ventriglia M, Barbati G, Cassetta E, Ferreri F, Dal Forno G, Ramires S, Zappasodi F, Rossini PM (2007) ‘Free’ copper in serum of Alzheimer’s disease patients correlates with markers of liver function. J Neural Transm 114:1589–1594

    Article  CAS  PubMed  Google Scholar 

  12. Kieffer DA, Medici V (2017) Wilson disease: at the crossroads between genetics and epigenetics - a review of the evidence. Metabolic Brain Disease Vol. 20, No. 4

  13. Kitzberger R, Madl C, Ferenci P (2005) Wilson disease metabolic brain disease 20, No 4, 295–302

  14. Southon A, Burke R, Camakaris J (2013) What can flies tell us about copper homeostasis? Metallomics 5:1346–1356

    Article  CAS  PubMed  Google Scholar 

  15. Strausak D, Mercer JFB, Dieter HH, Stremmel W, Multhaup G (2001) Copper in disorders with neurological symptoms: Alzheimer’s, Menkes, and Wilson diseases. Brain Res Bull 55(2):175–185

    Article  CAS  PubMed  Google Scholar 

  16. Bandmann O, Heinz KW, Kaler SG (2015) Wilson’s disease and other neurological copper disorders. Lancet Neurol 14:103–113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. 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 9:969–980

    Article  CAS  PubMed  Google Scholar 

  18. Letelier ME, Lepe AM, Fáundez M, Salazar J, Maríın R, Aracena P, Speisky H (2005) Possible mechanisms underlying copper-induced damage in biological membranes leading to cellular toxicity. Chem Biol Interact 151:71–82

    Article  CAS  PubMed  Google Scholar 

  19. Letelier ME, 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. Chem Biol Interact 188:220–227

    Article  CAS  PubMed  Google Scholar 

  20. Barresi V, Trovato-Salinaro A, Spampinato G, Musso N, Castorina S, Rizzarelli E, Condorelli DF (2016) Transcriptome analysis of copper homeostasis genes reveals coordinated upregulation ofSLC31A1, SCO1, andCOX11in colorectal cancer. FEBS Open Bio. 6(8):794–806

  21. Hatori Y, Lutsenko S (2013) An expanding range of functions for the copper chaperone/antioxidant protein Atox1. 19(9):945–957. Antioxid Redox Signal

  22. Peña MMO, Lee J, Thiele DJ (1999) A delicate balance: homeostatic control of copper uptake and distribution. J Nutr 129:1251–1260

    Article  PubMed  Google Scholar 

  23. Balamamurugan K, Egli D, Hua H, Rajaram R, Seisenbacher G, Georgiev O, Schaffner W (2007) Copper homeostasis in Drosophila by complex interplay of import, storage and behavioral avoidance. EMBO J 21; 26(4):1035–1044

    Article  CAS  Google Scholar 

  24. Markossian KA, Kurganov BI (2003) Copper chaperones, intracellular copper trafficking proteins. Function, structure, and mechanism of action. Biochem Mosc 68(8):827–837

    Article  CAS  Google Scholar 

  25. Hua H, Günter V, Georgiev O (2011) Distorted copper homeostasis with decreased sensitivity to cisplatin upon chaperone Atox1 deletion in Drosophila. Biometals 24:445–453

    Article  CAS  PubMed  Google Scholar 

  26. Gaetke LM, Chow CK (2003) Copper toxicity, oxidative stress, and antioxidant nutrients. Toxicology 189:147–163

    Article  CAS  PubMed  Google Scholar 

  27. Ottesen R, Gorham S, Pettengill J, Rideout S, Evans P, Brown E (2015) The impact of systemic and copper pesticide applications on the phyllosphere microflora of tomatoes Andrea. J Sci Food Agric 95(5):1116–1125

    Article  CAS  PubMed  Google Scholar 

  28. Georgopoulos PG, Roy A, Yonone-Lioy MJ, Opiekun RE, Lioy PJ (2011) Envinronmetal copper: its dynamics and human exposure issues. J Toxicol Environ Health, Part B: Crit Rev 4(4):341–394

    Article  Google Scholar 

  29. Carmona ER, Inostroza-Blancheteau C, Obando V, Rubio L, Marcos R (2015) Genotoxicity of copper oxide nanoparticles in Drosophila melanogaster. Mutat Res 791:1–11

    Article  CAS  Google Scholar 

  30. Hajipour MJ, Fromm KM, Ashkarran AA, de Aberasturi DJ, de Larramendi IR, Rojo T, Serpooshan V, Parak WJ, Mahmoudi M (2012) Antibacterial properties of nanoparticles. Trends Biotechnol 30:499–511,7

    Article  CAS  PubMed  Google Scholar 

  31. Mashock MJ, Zanon T, Kappell AD, Petrella LN, Andersen EC, Hristova KR (2016) Copper oxide nanoparticles impact several toxicological endpoints and cause neurodegeneration in Caenorhabditis elegans. PLoS One 11(12):e0167613

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Baek YW, Na Y (2011) Microbial toxicity of metal oxide nanoparticles (CuO, NiO, ZnO, and Sb2O3) to Escherichia coli, Bacillus subtilis, and Streptococcus aureus. Sci Total Environ 409:1603–1608

    Article  CAS  PubMed  Google Scholar 

  33. Grey B, Steck TR (2001) Concentrations of copper thought to be toxic to Escherichia coli can induce the viable but nonculturable condition. Appl Environ Microbiol 11: 5325–5327

  34. Kasemets K, Suppi S, Kunnis-Beres K, Kahru A (2013) Toxicity of CuO nanoparticles to yeast Saccharomyces cerevisiae BY4741 wild-type and its nine isogenic single-gene deletion mutants. Chem Res Toxicol 26(3):356–367

    Article  CAS  PubMed  Google Scholar 

  35. Greco MA, Hrab DI, Magner W, Daniel JK (1990) Cu, Zn superoxide dismutase and copper deprivation and toxicity in Saccharomyces cerevisiae. J Bacteriol 172:317–325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Boyd WA, Williams PL (2003) Comparison of the sensitivity of three nematode species to copper and their utility in aquatic and soil toxicity tests. Environ Toxicol Chem 11:2768–2774

    Article  Google Scholar 

  37. Yu ZY, Zhang J, Yin DQ (2012) Toxic and recovery effects of copper on Caenorhabditis elegans by various food-borne and water-borne pathways. Chemosphere 11:1361–1367

    Article  CAS  Google Scholar 

  38. Bazar MA, Quinn MJ, Mozzachio K, Bleiler JA, Archer CR, Phillips CT, Johnson MS (2009) Toxicological Responses of Red-Backed Salamanders (Plethodon cinereus) to Soil Exposures of Copper. Arch Environ Arch Environ Contam Toxicol 57:116–122

    Article  CAS  PubMed  Google Scholar 

  39. Semisch A, Ohle J, Witt B, Hartwig A (2014) Cytotoxicity and genotoxicity of nano and microparticulate copper oxide: role of solubility and intracellular bioavailability. Part Fibre Toxicol 11:10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Merker K, Hapke D, Reckzeh K, Schmidt H, Lochs H, Grune T (2005) Copper related toxic effects on cellular protein metabolism in human astrocytes. Biofactors 24(1–4):255–261

    Article  CAS  PubMed  Google Scholar 

  41. Tchounwou PB, Newsome C, Williams J, Glass K (2008) Copper-induced cytotoxicity and transcriptional activation of stress genes in human liver carcinoma (HepG2) cells. Metal Ions Biol Med 10:285–290

    Google Scholar 

  42. Song L, Connolly M, Fernández-Cruz ML, Vijver MG, Fernández M, Conde E, de Snoo GR, Peijnenburg WJ, Navas JM (2014) Species-specific toxicity of copper nanoparticles among mammalian and piscine cell lines. Nanotoxicology 8(4):383–393

    Article  CAS  PubMed  Google Scholar 

  43. Vecchio G (2015) A fruit fly in the nanoworld: once again Drosophila contributes to environment and human health. Nanotoxicology 9:135–137

    Article  CAS  PubMed  Google Scholar 

  44. Demir E, Turna F, Vales G, Kaya B, Creus A, Marcos R (2013) In vivo genotoxicity assessment of titanium, zirconium and aluminium nanoparticles, and their microparticulated forms, in Drosophila. Chemosphere 93:2304–2310

    Article  CAS  PubMed  Google Scholar 

  45. Zhou H, Cadigan KM, Thiele DJ (2003) A copper-regulated transporter required for copper acquisition, pigmentation, and specific stages of development in Drosophila melanogaster. J Biol Chem 278(48):48210–48218

    Article  CAS  PubMed  Google Scholar 

  46. Hwang JEC, De Bruyne M, Warr CG, Burke R (2014) Copper overload and deficiency both adversely affect the central nervous system of Drosophila. Metallomics 6(12):2223–2229

    Article  PubMed  Google Scholar 

  47. Pérez-Rafael S, Kurz A, Guirola M, Capdevila M, Palaciosa O, Atrian S Is MtnE, the fifth Drosophila metallothionein, functionally distinct from the other members of this polymorphic protein family. Metallomics 4:342–349

  48. Abolaji AO, Kamdem JP, Lugokenski TH, Nascimento TK, Waczuk EP, Farombi EO, Loreto ÉL, Rocha JB (2014) Involvement of oxidative stress in 4-vinylcyclohexene-induced toxicity in Drosophila melanogaster. Free Radic Biol Med 82:204–205

    Article  CAS  Google Scholar 

  49. Abolaji AO, Babalola OV, Adegoke AK, Farombi EO (2017) Hesperidin, a citrus bioflavonoid, alleviates trichloroethylene-induced oxidative stress in Drosophila melanogaster. Environ Toxicol Pharmacol 55:202–207

    Article  CAS  PubMed  Google Scholar 

  50. Calap-Quintana P, González-Fernández J, Sebastiá-Ortega N, Lorens JV, Moltó, M. D (2017) Drosophila melanogaster models of metal-related human diseases and metal toxicity Int J Mol Sci, 18 (7), art. no. 1456

  51. Massadeh A, Al-Momani F, Elbetieha A (2008) Assessment of heavy metals concentrations in soil samples from the vicinity of busy roads: influence on Drosophila melanogaster life cycle. Biol Trace Elem Res 122:292–299

    Article  CAS  PubMed  Google Scholar 

  52. Egli D, Yepiskoposyan H, Selvaraj A, Balamurugan K, Rajaram R, Simons A, Multhaup G, Mettler S, Vardanyan A, Georgiev O, Schaffner W (2006) A family knockout of all four Drosophila metallothioneins reveals a central role in copper homeostasis and detoxification. Mol Cell Biol 26(6):2286–2296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Han X, Geller B, Moniz K, Das P, Chippindale AK, Walker VK (2014) Monitoring the developmental impact of copper and silver nanoparticle exposure in Drosophila and their microbiomes. Sci Total Environ 487:822–829

    Article  CAS  PubMed  Google Scholar 

  54. Christie NT, David G, Gosslee DG, Bate LC, Jacobson KB (1983) Quantitative aspect of metal ion content and toxicity in Drosophila. Toxicology 26:295–312

    Article  CAS  PubMed  Google Scholar 

  55. Lenaerts C, Cools D, Verdonck R, Verbakel L, Broeck JV, Marchal E (2017) The ecdysis triggering hormone system is essential for successful moulting of a major hemimetabolous pest insect, Schistocerca gregária. Sci Rep 7:46502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Ding L, Wang Y (2006) Effect of copper on the development, protein and esterase isozymes of Drosophila melanogaster. Integrative Zool 2:73–77

    Article  CAS  Google Scholar 

  57. Adedara IA, Klimaczewski CV, Barbosa NBV, Farombi EO, Souza DO, Rocha JBT (2015) Influence of diphenyl diselenide on chlorpyrifos-induced toxicity in Drosophila melanogaster. J Trace Elem Med Biol 32:52–59

    Article  CAS  PubMed  Google Scholar 

  58. Klimaczewski CV, Ecker A, Piccoli B, Aschner M, Barbosa NV, Rocha JBT (2018) Peumus boldus attenuates copper-induced toxicity in Drosophila melanogaster. Biomed Pharmacother 97:1–8

    Article  CAS  PubMed  Google Scholar 

  59. Rand MD, Montgomery SL, Prince L, Vorojeikina D (2014) Developmental toxicity assays using the Drosophila mode. Curr Protoc Toxicol 1.12:1-1.12.20

    Google Scholar 

  60. Ali YO, Escala W, Ruan K R. Zhai RG (2011) Assaying locomotor, learning, and memory deficits in Drosophila models of neurodegeneration. Journal of Visualized Experiments (Jove) 49

  61. Lowry OH, Rosebrough NJ, Farr AL, Randall RL (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193(1):265–275

    CAS  PubMed  Google Scholar 

  62. Bailey SA, Zidell RH, Perry RW (2004) Relationships between organ weight and body/brain weight in the rat: what is the best analytical endpoint? Toxicol Pathol 32:448–466

    Article  PubMed  Google Scholar 

  63. Chernoff N, Hill DJ, Chorus I, Diggs DL, Huang H., King D., Lang J. R, Le T.-T., Schmid J. E, Travlos GS, Whitley EM, Wilson RE Wood CR (2018) Cylindrospermopsin toxicity in mice following a 90- d oral exposure. J Toxicol Environ Health, Part A, 1528–7394 (Print) 1087–2620 (Online)

  64. Ellman GL (1959) Tissue sulphydril groups. Arch Biochem Biophys 82(1):70–77

    Article  CAS  PubMed  Google Scholar 

  65. Habig WH, Jakoby WB (1981) Assays for differentiation of glutathione S-transferases. Methods Enzymol 77:398–405

    Article  CAS  PubMed  Google Scholar 

  66. Navarro JA, Schneuwly S (2017) Copper and zinc homeostasis: lessons from Drosophila melanogaster. Front Genet 8:223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Balamurugan K, Schaffner W (2006) Copper hoeostasis in eukaryotes: teetering on a tightrope. Biochim Biophys Acta 1763:737–746

    Article  CAS  PubMed  Google Scholar 

  68. Momani FA, Massadeh AM (2005) Effect of different heavy-metal concentrations on Drosophila melanogaster larval growth and development biological trace element research 108 (1–3)-0271

  69. Garlapow ME, Huang W, Yarboro MT, Peterson KR, Mackay TFC (2015) Quantitative genetics of food intake in Drosophila melanogaster. PLoS One 10(9):0138129

    Article  CAS  Google Scholar 

  70. Ferri A, Duffard R, Stürtz N, Duffard AME (2003) Iron, zinc and copper levels in brain, serum and liver of neonates exposed to 2,4-dichlorophenoxyacetic acid. Neurotoxicol Teratol 25:607–613

    Article  CAS  PubMed  Google Scholar 

  71. Siddique YH, Haidari M, Khan W, Fatima A, Jyoti S, Khanam S, Naz F, Rahul, Ali F, Singh BR, Beg T, Mohibullah, Naqvi AH (2015) Toxic potential of copper-doped ZnO nanoparticles in Drosophila melanogaster (Oregon R). Toxicol Mech Methods 25(6):425–432

    Article  CAS  PubMed  Google Scholar 

  72. Zhang T, Xu L, Wu J, Wang W, Mei J, Ma X, Liu J (2015) Transcriptional responses and mechanisms of copper-induced dysfunctional locomotor behavior in zebrafish embryos. Toxicol Sci 148(1):299310

    Article  CAS  Google Scholar 

  73. Abbaoui A, Hiba OE, Gamrani H (2016) Copper poisoning induces neurobehavioral features of Parkinson’s disease in rat: alters dopaminergic system and locomotor performance. Abstracts/Parkinsonism and related disorders 22 e149ee192

  74. Nichols CD, Becnel J, Pandey UB (2012) Methods to assay Drosophila behavior. J Vis Exp 61:3795

    Google Scholar 

  75. Madabattula ST, Strautman JC, Bysice AM, O’Sullivan JA, Androschuk A, Rosenfelt C, Doucet K, Rouleau G, Bolduc F (2015) Quantitative analysis of climbing defects in a Drosophila model of neurodegenerative disorders. J Vis Exp 100:52741

    Google Scholar 

  76. 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. Toxicol Res 5:1130–1139

    Article  CAS  Google Scholar 

  77. Cristóvão JS, Santos R, Gomes CM (2016) Metals and neuronal metal binding proteins implicated in Alzheimer’s disease Oxidative Medicine and Cellular Longevity 9812178

  78. Sun Y, Zhang G, He Z, Wang Y, Cui J, Li Y (2016) Effects of copper oxide nanoparticles on developing zebrafish embryos and larvae. Int J Nanomedicine 11:905–918

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Pauls D, Essen AV, Lyutova R, Giesen LV, Rosner R, Wegener C, Sprecher SG (2015) Potency of transgenic effectors for neurogenetic manipulation in Drosophila larvae. Genetics 199(1):25–37

    Article  CAS  PubMed  Google Scholar 

  80. Bonilla-Ramirez L, Jimenez-Del-Rio M, Velez-Pardo C (2011) Acute and chronic metal exposure impairs locomotion activity in Drosophila melanogaster: a model to study Parkinsonism. Biometals 24:1045–1057

    Article  CAS  PubMed  Google Scholar 

  81. Pomatto LCD, Wong S, Tower J, Davies KJA (2018) Sex-specific adaptive homeostasis in D. melanogaster depends on increased proteolysis by the 20S proteasome: data-in-brief. Data Brief 17:653–661

    Article  PubMed  PubMed Central  Google Scholar 

  82. Pomatto LCD, Wong S, Tower J, Davies KJA (2017) Sexual dimorphism in oxidant-induced adaptive homeostasis in multiple wild-type D. melanogaster strains. Arch Biochem Biophys 636:57–70

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Signor SA, Abbasi M, Marjora P, Nuzhdin SV (2017) Conservation of social effects (Ψ) between two species of Drosophila despite reversal of sexual dimorphism. Ecol Evol 7(23):10031–10041

    Article  PubMed  PubMed Central  Google Scholar 

  84. Chandegra B, Tang JLY, Chi H, Alic N (2017) Sexually dimorphic effects of dietary sugar on lifespan, feeding and starvation resistance in Drosophila. Aging 9(12):2521–2528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. De Nobrega AK, Lyons LC (2016) Circadian modulation of alcohol-induced sedation and recovery in male and female Drosophila. J Biol Rhythm 31(2):142–160

    Article  CAS  Google Scholar 

  86. Gruntenko NE, Karpova EK, Burdina EV, Adonyeva NV, Andreenkova OV, Alekseev AA, Rauschenbach IY (2016) Probable mechanism of sexual dimorphism in insulin control of Drosophila heat stress resistance. Physiol Entomol 41(1):59–66

    Article  CAS  Google Scholar 

  87. Neckameyer WS, Nieto-Romero AR (2015) Response to stress in Drosophila is mediated by gender, age and stress paradigm. Stress 18(2):254–266

    Article  PubMed  PubMed Central  Google Scholar 

  88. Smith LA, Habib I, Shirkey S, Talon B, Milne A, Nadolski J (2011) Sexual dimorphism in the effect of a taurine supplemented diet on life span in adult Drosophila melanogaster. Int J Zool Res 7(1):34–48

    Article  CAS  Google Scholar 

  89. Cachero S, Ostrovsky AD, Yu JY, Dickson BJ, Jefferis GSXE (2010) Sexual dimorphism in the fly brain. Curr Biol 20(18):1589–1601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Frasco MF, Fournier D, Carvalho F, Guilhermino L (2004) Do metals inhibit acetylcholinesterase (AChE)? Implementation of assay conditions for the use of AChE activity as a biomarker of metal toxicity. Biomarkers 1; 10(5):360–375

    Article  CAS  Google Scholar 

  91. Lima D, Roque GM, Almeida EA (2013) In vitro and in vivo inhibition of acetylcholinesterase and carboxylesterase by metals in zebrafish (Danio rerio). Mar Environ Res 91:45–51

    Article  CAS  PubMed  Google Scholar 

  92. Roling JA, Baldwin WS (2006) Alterations in hepatic gene expression by trivalent chromium in Fundulus heteroclitus. Mar Environ Res 62:122–127

    Article  CAS  Google Scholar 

  93. Gupta YR, Sellegounder D, Kannan M, Deepa S, Senthilkumaran B, Basavaraju Y (2016) Effect of copper nanoparticles exposure in the physiology of the common carp (Cyprinus carpio): biochemical, histological and proteomic approaches. Aquac Fish 1:15–23

    Article  Google Scholar 

  94. Carvalho CS, Bernusso VA, Araújo HSS, Espíndola ELG, Fernandes MN (2012) Biomarker responses as indication of contaminant effects in Oreochromis niloticus. Chemosphere 89:60–69

    Article  CAS  Google Scholar 

  95. Mercer SW, Burke R (2016) Evidence for a role for the putative Drosophila hGRX1 orthologue in copper homeostasis. Biometals 29:705–713

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This study received financial support from the Institutional Scholarship Program (PIBIC), Brazilian National Council for Scientific and Technological Development (CNPq), Coordination of Improvement of Higher Level Personnel (CAPES), Financier of Studies and Projects (FINEP), and Foundation of Support to the State of Rio Grande do Sul research (FAPERGS).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to João Batista Teixeira da Rocha.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethical Approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Electronic supplementary material

ESM 1

(DOCX 16 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Halmenschelager, P.T., da Rocha, J.B.T. Biochemical CuSO4 Toxicity in Drosophila melanogaster Depends on Sex and Developmental Stage of Exposure. Biol Trace Elem Res 189, 574–585 (2019). https://doi.org/10.1007/s12011-018-1475-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-018-1475-y

Keywords

Navigation