Springer Nature is making Coronavirus research free. View research | View latest news | Sign up for updates

Alteration of membrane integrity and respiratory function of brain mitochondria in the rats chronically exposed to a low dose of acetamiprid

Abstract

The pesticides are used in several fields of agriculture and farms to protect crops against harmful insects and herbs. The increased and uncontrolled use of these pollutants is very hazardous for the population health. Consumption of contaminated food matrices with these pesticides could impair the cell integrity and its molecular function. The main aim of this present study was to evaluate the alteration of the integrity of mitochondrial membranes and respiratory chain potential in the brain of rats exposed during 90 days to acetamiprid (AC), organochlorine of the new generation. After oral administration of AC in rats with 3.14 mg/kg of body weight, the results of this current study showed enhance in mitochondrial oxidative stress status by significant decrease of glutathione (GSH) level, glutathione pyroxidase (GPx), and catalase (CAT) activities. On the other hand, there is an increase in the enzymatic activity of the glutathione s-transferase (GST) and superoxide dismutase (SOD); at the same time, the MDA level was also highly increased. Furthermore, evaluation results of brain mitochondrial integrity revealed a significant increase in membrane permeability and mitochondrial swelling in rats exposed chronically to AC. Instead, other results of this present work showed a significant decrease in mitochondrial respiration potent (O2 consumption) in acetamiprid-treated rats. In conclusion, the long duration exposition of the animals to AC has led to respiratory chain dysfunction, disturbance of matrix oxidative status, and a loss of mitochondrial membranes integrity.

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

References

  1. Adams J, Vorhees CV, Middaugh LD (1990) Developmental neurotoxicity of anticonvulsants: human and animal evidence on phenytoin. Neurotoxicol Teratol 12:203–214

  2. Aebi (1984) Catalase in vivo, methods in enzymology, vol 105. Academic Press, Orlando, pp 121–126

  3. Assefa Z, Van Laethem A, Garmyn M, Agostinis P (2005) Ultraviolet radiation induced apoptosis in keratinocytes: on the role of cytosolic factors. Biochim Biophys Acta 1755:90–106

  4. Baldi I, Bouvier G, Cordier S, Coumoul X, Elbaz A, Gamet-Payrastre L, Lebailly P, Multigner L, Rahmani R, Spinosi J, Van Maele-Fabry G (2013) Pesticides. Effets sur la santé. Synthèse et recommandations. Expertise collective. INSERM. Paris, France, p 146

  5. Baltazar MT, Dinis-Oliveira RJ, de Lourdes BM, Tsatsakis AM, Duarte JA, Carvalho F (2014) Pesticides exposure as etiological factors of Parkinson's disease and other neurodegenerative diseases—a mechanistic approach. Toxicol Lett 230:85–103

  6. Banerjee BD, Seth V, Rs A (2001) Pesticide-induced oxidative stress: perspectives and trends. Environ Health 16:1–40

  7. Beauchamp C, Fridovich I (1971) Assay of superoxide dismutase. Anal Biochem 44:276–287

  8. Bourbia S (2013) Évaluation de la toxicité de mixtures de pesticides sur un bio-indicateur de la pollution des sols Helix aspersa, Doctorat Thesis. Univ Annaba pp177

  9. Bradford M (1976) A rapid and sensitive method for the quantities of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

  10. Carole I, Harvé Q (2011) Désordres métaboliques et réanimation: de la physiopathologie au traitement. Berlin Heidelbeng. New York. ISBN-13: 978–2–287-99026-7.522

  11. Çavas TN (2014) Effects of fullerenol nanoparticles on acetamiprid induced cytoxicity and genotoxicity in cultured human lung fibroblasts. Pests Biochem Physiol 114:1–7 7

  12. Chakroun S, Ezzi L, Grissa I, Kerkeni E, Neffati F, Bhouri R, Sallem A, Najjar MF, Hassine M, Mehdi M, Haouas Z, Ben-Cheikh H (2016) Hematological, biochemical, and toxicopathic effects of subchronic acetamiprid toxicity in Wistar rats. Environ Sci Pollut Res. doi:10.1007/s11356-016-7650-9

  13. Chen X, Ahn DU (1998) Antioxidant activities of six natural phenolics against lipid oxidation induced by Fe2+ or ultraviolet light. JAOCS 75(12):1717–1721

  14. Clayton D.A. and J.N. Doda, Isolation of mitochondria from cells and tissues. In: Spector DL, Goldman R, Leinwand L (eds) Cells: A laboratory manual. Sci Press, Beijing, China, pp 356–361

  15. Cory-Slechta D, Thiruchelvam M, Ek R, Bk B, Brooks A (2005) Developmental pesticide exposures and the Parkinson’s disease phenotype. Birth Defects Res A Clin Mol Teratol 73:136–139

  16. Di Monte DA, Lavasani M (2002) Manning-bog ab environmental factors in Parkinson’s disease. Neurotoxicology 23:487–502

  17. Di Monte DA, Chan P, Sandy MS (1992) Glutathione in Parkinson’s disease: a link between oxidative stress and mitochondrial damage? Ann Neurol 32(S1):S111–S115

  18. EFSA (2013) Scientific opinion on the developmental neurotoxicity potential of acetamiprid and imidacloprid. EFSA J 11(12):3471

  19. El Hassani, Dacher M, Gary V, Lambin M, Gauthier M, Armengaud C (2008) Effects of sublethal doses of acetamiprid and thiamethoxam on the behavior of the honeybee. Arch Environ Contam Toxicol 54:653–661. doi:10.1007/s00244-007-9071-8

  20. Esterbauer H, Gebicki J, Puhl H, Jungens G (1992) The role of lipid peroxidation and antioxidants in oxidative modification of LDL. Biol Med 13:341

  21. Farhi S (2015) Neurotoxicity study of cadmium on oxidative stress parameters and the protective effect of selenium on this toxicity in rabbits. University Thesis. Trace Elem Med Biol 29:104–10

  22. Flohe, Gunzler (1984) Analysis of glutathione peroxidase. Methods Enzymol 105:114–121

  23. Franco R, Cidlowski JA (2009) Apoptosis and glutathione: beyond an antioxidant. Cell Death Differ 16:1303–1314

  24. Franco R, Sanchez-Olea R, Reyes-Reyes EM, Panayiotidis MI (2009) Environmental toxicity, oxidative stress and apoptosis: menage a trois. Mutat Res 674:3–22

  25. Gao C, Chen X, Juan LJ, Tang Y, Liu L, Chen S, Yu H, Liu L, Yao P (2014) Myocardial mitochondrial oxidative stress and dysfunction in intense exercise: regulatory effects of quercetin. Eur J Appl Physiol 114:695–705

  26. Gasmi S, Rouabhi R, Kebieche M, Salmi A, Boussekine S, Toualbia N, Taib C, Henine S, Bouteraa Z, Djabri B (2016) Neurotoxicity of acetamiprid in male albino rats and the opposite effect of quercetin. Biotechnol Ind J 12(7):113

  27. Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione s-transferases. The first enzymatic step in mercapturic acid formation. Biol Chem 249:7130–7139

  28. Henin S, Rouabhi R, Gasmi S, Amrouche A, Abide A, Salmi A, Toualbia N, Taib C, Bouteraa Z, Chenikher H, Boussekine S, Kebieche M, Aouimeur M (2016) Oxidative stress status, caspase 3, stromal enzymes and mitochondrial respiration and swelling of Paramecium Caudatum in responding to the toxicity of Fe3O4 nanoparticles. Environ Health Sci 8(2):161–167

  29. Iwasa T, Motoyama N, Ambrose JT, Roe MR (2004) Mechanism for the differential toxicity of neonicotinoid insecticides in the honey bee, Apis mellifera. Crop Prot 23:371–378

  30. Jaswinder SB, Christopher AS (1997) Neurodegenerative disorders in humans: the role of glutathione in oxidative stress-mediated neuronal death. Brain Res Rev 25:335–358

  31. Johnson KJ, Weinberg JM (1993) Postischemic renal injury due to oxygen radicals. Curr Opin Nephrol Hypertens 2(4):625–35

  32. Kebieche M, Lakroun Z, Lahouel M, Bouayed J, Meraihi Z, Souliman R (2009) Evaluation of epirubicin-induced acute oxidative stress toxicity in rat liver cells and mitochondria, and the prevention of toxicity through quercetin administration. Exp Toxicol Pathol 61:161–167

  33. Kristal BS, Park BK, Yu BP (1996) 4-hydroxynonénal est un puissant inducteur de la transition de perméabilité mitochondriale. Biol Chem 271:6033–6038

  34. Lahouel A, Kebieche M, Lakroun Z, Rouabhi R, Fetoui H, Chtourou Y, Zama D, Soulimani R (2016) Nurobehavioral deficits and brain oxidative stress induced by chronic low dose exposure of persistent organic pollutants mixture in adult female rat. Environ Sci Pollut Res. doi:10.1007/s11356-016-6913-9

  35. Lakroun Z, Kebieche M, Lahouel A, Zama D, Soulimani R (2015) Oxidative stress and brain mitochondria swelling induced by endosulfan and protective role of quercetin in rat. Environ Sci Pollut Res. doi:10.1007/s11356-014-3885-5

  36. Pasteur L (2013) La maladie d'Alzheimer : intérêt des molécules d'origine naturelle. Thèse d'exercice en Pharmacie, bibliothèque de l’UPS, Université Toulouse III - Paul Sabatier.

  37. Lukaszewicz-Hussain A (2008) Subchronic intoxication with chlorfenvinphos, an organophosphate insecticide, affects rat brain antioxidative enzymes and glutathione level. Food Chem Toxicol 46(1):82–86

  38. Mandal PS, Mondal S, Karnam SS, Purohit K (2015) A behavioral study on learning a memory in adult Sprague Dawley rat in induced acetamiprid toxicity. Explor Anim Med Res 5(1):27–32

  39. Morris G, Berk M (2015) The many roads to mitochondria dysfunction in neuroimmune and neuropsychiatric disorders. BMC Med 13:68–75

  40. Nawaza A, Abid N, Muhammad I, Syed S, Hussain S, Muhammad RA, Zahid A (2015) Determination and extraction of acetamiprid residues in fruits and vegetables. IJFAAS 1(2):63–66

  41. Rouabhi R, Gasmi S, Boussekine S, Kebieche M (2015) Hepatic oxidative stress induced by zinc and opposite effect of selenium in Oryctolagus cuniculus. Environ Anal Toxicol 5:289

  42. Sauer E (2014) Liver delta-aminolevulinate deshydratase activity is inhibited by neonicotinoids and restored by antioxidants agents. Environ Res Public Health 11(11):11676–11690

  43. Seaton TP, Mursdenf CD (1996) Mitochondrial respiratory enzyme function and superoxide dismutase activity following brain glutathione depletion in the rat. Biochem Pharmacol 52:1657–1663

  44. Shi H, Hudson LG, Liu KJ (2004) Oxidative stress and apoptosis in metal ion induced carcinogenesis. Free Radic Biol Med 37:582–593

  45. Silva MH, Gammon D (2009) An assessment of the developmental, reproductive, and neurotoxicity of endosulfan. Birth Defects Res Dev Reprod Toxicol 86:1–28

  46. Testud F (2014) Insecticides néonicotinoïdes. EMC-Pathologie professionnelle et de l’environnement. EMC Toxicol Pathol. doi:10.1016/S1877-7856(13)62786-5

  47. Tian YW (2016) A colorimetric detection method of pesticide acetamiprid by fine-tuning aptamer length. Anal Biochem 513:87–92

  48. Uttara B, Sing AV, Zamboni P, Mahajan RT (2009) Oxidative stress and neurodegenerative diseases. PMC 7(1):65–74

  49. Weckbercker G, Cory JG (1988) Ribonucleotide reductase activity and growth of glutathione-depended mouse leukemia L1210 cells in vitro. Cancer Lett 40:257–264

  50. Yousef MI, El-Demerdash F, Ibrahim K, Al-Salhen K (2003) Changes in some hematological and biochemical indices of rabbits induced by isofla vones and cypermethrin. Toxicology 189:223–234

Download references

Author information

Correspondence to Mohammed Kebieche.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Gasmi, S., Kebieche, M., Rouabhi, R. et al. Alteration of membrane integrity and respiratory function of brain mitochondria in the rats chronically exposed to a low dose of acetamiprid. Environ Sci Pollut Res 24, 22258–22264 (2017). https://doi.org/10.1007/s11356-017-9901-9

Download citation

Keywords

  • Acetamiprid
  • Brain mitochondria
  • Mitochondrial swelling
  • Membrane permeability
  • Oxidative stress
  • Rats