Display options
Share it on

Biol Open. 2016 Apr 15;5(4):381-8. doi: 10.1242/bio.014936.

The neurotoxic effects of hydrogen peroxide and copper in Retzius nerve cells of the leech Haemopis sanguisuga.

Biology open

Zorica D Jovanovic, Marija B Stanojevic, Vladimir B Nedeljkov

Affiliations

  1. Department of Pathological Physiology, Faculty of Medical Sciences, University of Kragujevac, 34000 Kragujevac, Serbia [email protected].
  2. Institute for Pathological Physiology, School of Medicine, University of Belgrade, 11000 Belgrade, Serbia.

PMID: 26935393 PMCID: PMC4890660 DOI: 10.1242/bio.014936

Abstract

Oxidative stress and the generation of reactive oxygen species (ROS) play an important role in cellular damage. Electrophysiological analyses have shown that membrane transport proteins are susceptible to ROS. In the present study, oxidative stress was induced in Retzius nerve cells of the leechHaemopis sanguisugaby bath application of 1 mM of hydrogen peroxide (H2O2) and 0.02 mM of copper (Cu) for 20 min. The H2O2/Cu(II) produced considerable changes in the electrical properties of the Retzius nerve cells. Intracellular recording of the resting membrane potential revealed that the neuronal membrane was depolarized in the presence of H2O2/Cu(II). We found that the amplitude of action potentials decreased, while the duration augmented in a progressive way along the drug exposure time. The combined application of H2O2and Cu(II) caused an initial excitation followed by depression of the spontaneous electrical activity. Voltage-clamp recordings revealed a second effect of the oxidant, a powerful inhibition of the outward potassium channels responsible for the repolarization of action potentials. The neurotoxic effect of H2O2/Cu(II) on the spontaneous spike electrogenesis and outward K(+)current of Retzius nerve cells was reduced in the presence of hydroxyl radical scavengers, dimethylthiourea and dimethyl sulfoxide, but not mannitol. This study provides evidence for the oxidative modification of outward potassium channels in Retzius nerve cells. The oxidative mechanism of the H2O2/Cu(II) system action on the electrical properties of Retzius neurons proposed in this study might have a wider significance, referring not only to leeches but also to mammalian neurons.

© 2016. Published by The Company of Biologists Ltd.

Keywords: Antioxidants; Copper; Hydrogen peroxide; Leech; Potassium current

References

  1. Circ Res. 2012 Feb 3;110(3):471-80 - PubMed
  2. Cell Physiol Biochem. 2008;22(1-4):119-26 - PubMed
  3. Free Radic Biol Med. 1993 Oct;15(4):435-45 - PubMed
  4. J Neurosci Res. 2001 Jan 15;63(2):176-84 - PubMed
  5. Neuroscience. 2015 Mar 19;289:85-98 - PubMed
  6. J Pharmacol Exp Ther. 2006 Jul;318(1):214-22 - PubMed
  7. Auton Neurosci. 2009 Jan 28;145(1-2):44-9 - PubMed
  8. Neuropharmacology. 2005 Oct;49(5):669-86 - PubMed
  9. J Pept Sci. 2009 Feb;15(2):95-106 - PubMed
  10. Cell Signal. 2012 May;24(5):981-90 - PubMed
  11. J Mol Cell Cardiol. 1992 May;24(5):523-34 - PubMed
  12. Clin Exp Pharmacol Physiol. 2006 Jan-Feb;33(1-2):146-51 - PubMed
  13. Brain Res. 1995 Jun 19;683(2):275-8 - PubMed
  14. Nat Neurosci. 2009 May;12(5):611-7 - PubMed
  15. Arch Biochem Biophys. 1995 Jan 10;316(1):515-22 - PubMed
  16. J Exp Biol. 1989 Jan;141:1-20 - PubMed
  17. Oxid Med Cell Longev. 2014;2014:360438 - PubMed
  18. J Neurobiol. 1995 Jul;27(3):434-45 - PubMed
  19. Sheng Li Xue Bao. 2009 Jun 25;61(3):285-91 - PubMed
  20. Circ Res. 2013 Jan 18;112(2):382-92 - PubMed
  21. Auton Neurosci. 2009 Oct 5;150(1-2):45-52 - PubMed
  22. Ann Ist Super Sanita. 2005;41(2):143-64 - PubMed
  23. Pflugers Arch. 2001 May;442(2):263-72 - PubMed
  24. J Biol Chem. 2013 Feb 8;288(6):4128-34 - PubMed
  25. Eur J Neurosci. 2006 May;23(9):2375-84 - PubMed
  26. J Neurosci Res. 2005 Jan 1-15;79(1-2):157-65 - PubMed
  27. Exp Anim. 2013;62(1):9-17 - PubMed
  28. J Physiol. 2000 Jan 1;522 Pt 1:19-31 - PubMed
  29. Brain Res. 2013 Jul 3;1520:61-9 - PubMed
  30. J Neurosci. 2012 Mar 21;32(12 ):4133-44 - PubMed
  31. FEBS Lett. 2000 Dec 1;486(1):10-3 - PubMed
  32. Free Radic Biol Med. 2002 May 1;32(9):822-32 - PubMed
  33. Proc Natl Acad Sci U S A. 1995 Dec 5;92(25):11796-800 - PubMed
  34. Prog Neurobiol. 1977;8(2):81-117 - PubMed
  35. Circulation. 1999 Apr 6;99(13):1719-25 - PubMed
  36. Life Sci. 2012 Mar 10;90(11-12):424-31 - PubMed
  37. Eur J Pharmacol. 2009 Aug 1;615(1-3):40-9 - PubMed
  38. Redox Biol. 2014 Feb 23;2:535-62 - PubMed
  39. Physiol Rev. 1999 Jul;79(3):917-1017 - PubMed
  40. Microsc Res Tech. 2001 Nov 15;55(4):236-48 - PubMed
  41. J Comp Physiol A. 1999 Jan;184(1):49-61 - PubMed
  42. Biomaterials. 2005 Sep;26(26):5321-9 - PubMed
  43. J Neurochem. 2006 Jun;97(6):1634-58 - PubMed
  44. J Neurosci. 1997 Jul 1;17(13):4942-55 - PubMed
  45. J Mol Histol. 2012 Aug;43(4):383-99 - PubMed
  46. Ann N Y Acad Sci. 1994 Nov 17;738:8-14 - PubMed
  47. PLoS One. 2012;7(9):e46392 - PubMed
  48. Am J Physiol Cell Physiol. 2004 Oct;287(4):C963-70 - PubMed
  49. Biochem Biophys Res Commun. 2006 Apr 21;342(4):1389-95 - PubMed
  50. Neuroscience. 2014 Mar 14;262:53-69 - PubMed
  51. Front Plant Sci. 2013 Nov 25;4:479 - PubMed
  52. Curr Opin Neurobiol. 2001 Dec;11(6):757-64 - PubMed
  53. J Pharmacol Toxicol Methods. 2011 Mar-Apr;63(2):209-15 - PubMed
  54. J Neurophysiol. 2011 Dec;106(6):3045-55 - PubMed
  55. Am J Physiol Cell Physiol. 2002 Mar;282(3):C461-71 - PubMed

Publication Types