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Oxidative stress status, caspase-3, stromal enzymes and mitochondrial respiration and swelling of Paramecium caudatum in responding to the toxicity of Fe3O4 nanoparticles

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Abstract

The number of industrial and consumer products which contain engineered nanomaterials (ENMs, materials with at least one dimension 1–100 nm) are increasing exponentially and there is a concern regarding their occupational and environmental safety. Fe3O4 nanoparticles are the most widely used metal oxide nanoparticles especially, in biomedical applications. Although, nanoparticles can enter to the different organs, little is known so far on the toxicity potential and oxidative stress of Fe3O4. Here the understanding of the effect of Fe3O4 nanoparticles on the general Redox state of a unicellular protozoa Paramecium and the effect on mitochondrial swelling and respiration were assessed. Fe3O4 resulted in increase of toxicity markers, lipid peroxidation, protein and ROS formation. Mitochondrial enzymes and swelling were elevated with decreased respiration level. Caspase 3 activity was also increased.

Finally, our study suggested that the mitochondrial disease and dysfunction with elevated oxidative stress in Paramecia treated with 200 and 300 ppm during 15 days is the original of toxicity and maybe the original cause of many environmental pathologies.

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References

  1. Gottschalk, F., Kost, E. & Nowack, B. Engineered nanomaterials in water and soils: a risk quantification based on probabilistic exposure and effect modeling. Environ. Toxicol. Chem. 32, 1278–1287 (2013).

    Article  CAS  PubMed  Google Scholar 

  2. Chen, C. L. et al. A New Nano-sized Iron Oxide Particle with High Sensitivity for Cellular Magnetic Resonance Imaging. Mol. Imag. Biol. 13, 825–839 (2010).

    Article  Google Scholar 

  3. Alexiou, C., Tietze, R., Schreiber, E. & Lyer, S. Nanomedicine: Magnetic nanoparticles for drug delivery and hyperthermia -new chances for cancer therapy. Bundesgesundheitsblatt Gesundheitsforschung. Gesundheitsschutz 53, 839–845 (2005).

    Google Scholar 

  4. McBain, S. C., Yiu, H. H. P. & Dobson, J. Magnetic nanoparticles for gene and drug delivery. Int. J. Nanomedicine. 3, 169–180 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Puppi, J. et al. Use of a Clinically Approved Iron Oxide MRI Contrast Agent to Label Human Hepatocytes. Cel. Transplant. 20, 963–975 (2011).

    Article  Google Scholar 

  6. Rümenapp, C., Gleich, B. & Haase, A. Magnetic Nanoparticles in Magnetic Resonance Imaging and Diagnostics. Pharm. Res. 29, 1165–1179 (2012).

    Article  PubMed  Google Scholar 

  7. Cochran, D. B. et al. Suppressing iron oxide nanoparticle toxicity by vascular targeted antioxidant polymer nanoparticles. Biomaterials 34, 9615–9622 (2013).

    Article  CAS  PubMed  Google Scholar 

  8. Zhu, M. T. et al. Oxidative stress and apoptosis induced by iron oxide nanoparticles in cultured human umbilical endothelial cells. J. Nanosci. Nanotechnol. 10, 8584–8590 (2010).

    Article  CAS  PubMed  Google Scholar 

  9. Wilson, M. R. et al. Interactions between ultrafine particles and transition metals in vivo and in vitro. Toxicol. Appl. Pharmacol. 184, 172–179 (2002).

    Article  CAS  PubMed  Google Scholar 

  10. Zhu, M. T. et al. Endothelial dysfunction and inflammation induced by iron oxide nanoparticle exposure: risk factors for early atherosclerosis. Toxicol. Lett. 203, 162–171 (2011).

    Article  CAS  PubMed  Google Scholar 

  11. Remyaa, A. S. et al. Iron oxide nanoparticles to an Indian major carp, Labeo rohita: Impacts on hematology, iono-regulation and gill Na+/K+ ATPase activity. J. of King Saud University Science. 27, 151–160 (2015).

    Article  Google Scholar 

  12. Gräbsch, C. et al. Cytotoxicity assessment of Gliotoxin and Penicillic acid in Tetrahymena pyriformis. Environ. Toxicol. 21, 111–117 (2006).

    Article  PubMed  Google Scholar 

  13. Van der Oost, R., Beyer, J. & Vermeulen, N. P. E. Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ. Toxicol. Phar. 13, 57149 (2003).

    Google Scholar 

  14. Dive, D. et al. A bioassay using the measurement of the growth inhibition of a ciliate protozoan: Colpidium campylum stokes. Hydrobiologia 188/189, 181–188 (1989b).

    Article  Google Scholar 

  15. Nalecz-Jawecki, G., Demkowicz-Dobrzahski, K. & Sawicki, J. Protozoan Spirostomum ambiguum as a highly sensitive bioindicator for rapid and easy determination of water quality. Sci. Total Environ. Suppl. 134, 1227–1234 (1993).

    Article  Google Scholar 

  16. Foissner, W. Soil protozoa as bioindicators: pros and cons, methods, diversity, representative examples. Agr. Ecosyst. Environ. 74, 95–112 (1999).

    Article  Google Scholar 

  17. Rouabhi, R., Djebar, H. & Djebar, M. R. Toxicity evaluation of Flucycloxuron and diflubenzuron on the cellular model. Paramecium sp. Afr. J. Biotechnol. 5, 45–48 (2006a).

    CAS  Google Scholar 

  18. Rouabhi, R., Djebar-Berrebbah, H. & Djebar, M. R. Toxic Effect of a Pesticide. Diflubenzuron on Freshwater Macroinvertebrate (Tetrahymena pyriformis). Chin. J. Appl. Environ. Biol. 12, 514–517 (2006b).

    CAS  Google Scholar 

  19. Mohd, M. H., Nageswara, R. A., Venkata, R. S. & Mohan, B. Low cost micro bioassay test for assessing cytopathological and physiological responses of ciliate model Paramecium caudatum to carbofuran pesticide. Pest. Biochem. Physiol. 90, 66–70 (2008).

    Article  Google Scholar 

  20. Krejc, S. et al. Chronic effects of metals. organophosphates and polycyclic aromatic hydrocarbon (PAH) on Tetrahymena pyriformis. Toxicol. Lett. 172S, S84–S85 (2007).

    Article  Google Scholar 

  21. Kovács, P., Csaba, G., Pallinger, E. & Czaker, R. Effects of taxol treatment on the microtubular system and mitochondria of Tetrahymena. Cell Biol. Int. 31, 724–732 (2007).

    Article  PubMed  Google Scholar 

  22. Guiraud, P. et al. Involvement of Tetrahymena pyriformis and selected fungi in the elimination of anthracene. and toxicity assessment of the biotransformation products. Ecotox. Environ. Safe. 69, 296–305 (2008).

    Article  CAS  Google Scholar 

  23. LeRoith, D. et al. Are messenger moleculs in microbes the ancestors of the vertebrate hormones and tissue factors? Fed. Proc. 42, 2602–2607 (1983).

    CAS  Google Scholar 

  24. Csaba, G. & Kovács, P. Localization of β-endorphin in Tetrahymena by confocal microscopy. Induction of the prolonged production of the hormone by hormonal imprinting. Cell Biol. Int. 23, 695–702 (1999).

    Article  CAS  PubMed  Google Scholar 

  25. Ashley, R. M. et al. Oxidative Stress and Dermal Toxicity of Iron Oxide Nanoparticles in Vitro. Cell Biochem. Biophys. 67, 461–476 (2013).

    Article  Google Scholar 

  26. Rouabhi, R., Gasmi, S., Boussekine, S. & Kebieche, M. Hepatic Oxidative Stress Induced by Zinc and Opposite Effect of Selenium in Oryctolagus cuniculus. J. Environ. Anal. Toxicol. 5, 289 (2015).

    Google Scholar 

  27. García, A. et al. Acute toxicity of cerium oxide. titanium oxide and iron oxide nanoparticles using standardized tests. Desalination 269, 136–141 (2011).

    Article  Google Scholar 

  28. Rouabhi, R., Djebar-Berrebbah, H. & Djebar, M. R. Impact of Flufenoxuron. an IGR pesticide on Gallus domesticus embryonic development in ovo. J. Cell Anim. Biol. 2, 87–91 (2008).

    Google Scholar 

  29. Aruoja, V. et al. Toxicity of 12 metal-based nanoparticles to algae. bacteria and protozoa. Environ. Sci.: Nano. 2, 630–644 (2015).

    CAS  Google Scholar 

  30. Alnemri, E. S. et al. Human ICE/CED-3 protease nomenclature. Cell 87, 171 (1996).

    Article  CAS  PubMed  Google Scholar 

  31. Salvesen, G. S. Caspases: opening the boxes and interpreting the arrows. Cell Deat. Differ. 9, 3–5 (2002).

    Article  Google Scholar 

  32. Ghavami, S. et al. Apoptosis and cancer: mutations within caspase genes. J. Med. Genet. 46, 497–510 (2009).

    Article  CAS  PubMed  Google Scholar 

  33. Boatright, K. M. & Salvesen, G. S. Mechanisms of caspase activation. Curr. Opin. Cel. Biol. 15, 725–731 (2003).

    Article  CAS  Google Scholar 

  34. Zhao, X. et al. TNF-alpha stimulates caspase-3 activation and apoptotic cell death in primary septo-hippocampal cultures. J. Neurosci. Res. 64, 121–131 (2001).

    Article  CAS  PubMed  Google Scholar 

  35. Utaisincharoen, P. et al. TNF-alpha induces caspase 3 (CPP 32) dependent apoptosis in human cholangiocarcinoma cell line. Southeast Asian J. Trop. Med. Publi. Health. 31, 167–170 (2000).

    Google Scholar 

  36. Zou, X.-Y., Xu, B., Yu, C.-P. & Zhang, H.-W. Combined toxicity of ferroferric oxide nanoparticles and arsenic to the ciliated protozoa Tetrahymena pyriformis. Aquat. Toxicol. 134-135, 66–73 (2013).

    Article  CAS  PubMed  Google Scholar 

  37. Yang, S., Thor, A. D., Edgerton, S. & Yang, X. Caspase3 mediated feedback activation of apical caspases in doxorubicin and TNF-alpha induced apoptosis. Apoptosis 11, 1987–1997 (2006).

    Article  CAS  PubMed  Google Scholar 

  38. Zhang, G. et al. Hydroxycamptothecin-Loaded Fe3O4 Nanoparticles Induce Human Lung Cancer Cell Apoptosis through Caspase-8 Pathway Activation and Disrupt Tight Junctions. Cance. Sci. 102, 1216–1222 (2011).

    Article  CAS  Google Scholar 

  39. Baratli, Y. et al. Age Modulates Fe3O4 Nanoparticles Liver Toxicity: Dose-Dependent Decrease in Mitochondrial Respiratory Chain Complexes Activities and Coupling in Middle-Aged as Compared to Young Rats. BioMed Res. Int. (2014). DOI:10.1155/2014/474081.

    Google Scholar 

  40. Kakkar, P., Das, B. & Viswanathan, P. A modified spectrophotometric assay of superoxide dismutase. Indian J. Biochem. Biophys. 21, 130–132 (1984).

    CAS  PubMed  Google Scholar 

  41. Flohe, L. & Gunzler, W. A. Assays of glutathione peroxidase. Method. Enzymol. 105, 114–121 (1984).

    Article  CAS  Google Scholar 

  42. Cakmak, I. & Horst, W. J. Effect of aluminum on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max). Physiol. Plantarum. 83, 463–468 (1991).

    Article  CAS  Google Scholar 

  43. Habig, H., Pabst, M. J. & Jokoby, W. B. GlutathioneS-transferase: the first enzymatic step in mercapturic acid formation. J. Biol. Chem. 249, 7130–7139 (1974).

    CAS  PubMed  Google Scholar 

  44. Weckbker, G. & Cory, J. G. Ribonucleotide reductase activity and growth of Glutathoine-depleted mouse leukemia L1210 cells in vitro. Cance. Lett. 40, 257–264 (1988).

    Article  Google Scholar 

  45. Esterbaer, H., Gebicki, J., Puhl, H. & Jungens, G. The role of lipid peroxidation and antioxidants in oxidative modification of LDL. Free Radic. Biol. Med. 13, 341 (1992).

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  47. Kristal, B. S., Park, B. K. & Yu, B. P. 4-hydroxynonénal est un puissant inducteur de la transition de perméabilité mitochondriale. J. Biol. Chem. 271, 6033–6038 (1996).

    Article  CAS  PubMed  Google Scholar 

  48. Rouabhi, R., Djebar, H. & Djebar, M. R. Toxic Effects of Combined Molecule from Novaluron and Diflubenzuron on Paramecium caudatum. Am-Euras. J. Toxicol. Sci. 1, 74–80 (2009).

    Google Scholar 

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Authors and Affiliations

  1. Applied Biology department, Tebessa University, 12000, Tebessa, Algeria

    Henine Sara, Rouabhi Rachid, Gasmi Salim, Amrouche Aml, Abide Amna, Salmi Aya, Toualbia Nadjiba, Taib Chahinez, Bouteraa Zina, Chenikher Hajer, Boussekine Samira & Djabri Belgacem

  2. Laboratory of pharmacology and phyotochemestry, University of Jijel, Jijel, Algeria

    Kebieche Mohamed

  3. Molecular and cellular biology department, Eloued University, Eloued, 39000, Algeria

    Aouimeur Mariem

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  1. Henine Sara
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Correspondence to Rouabhi Rachid.

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Sara, H., Rachid, R., Salim, G. et al. Oxidative stress status, caspase-3, stromal enzymes and mitochondrial respiration and swelling of Paramecium caudatum in responding to the toxicity of Fe3O4 nanoparticles. Toxicol. Environ. Health Sci. 8, 161–167 (2016). https://doi.org/10.1007/s13530-016-0273-1

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  • DOI: https://doi.org/10.1007/s13530-016-0273-1

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