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Effect of hydrogen peroxide on electrical coupling between identified Lymnaea neurons

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Invertebrate Neuroscience

Abstract

The pair of giant reciprocally coupled neurons VD1 and RPaD2 within the CNS of the freshwater pond snail Lymnaea stagnalis was used to analyse the effect of hydrogen peroxide on gap-junction connection. Electrical activity of VD1/RPaD2 was recorded with intracellular microelectrodes in order to analyse gap-junction signalling. Hydrogen peroxide application (1 × 10−4 M) results in a rapid, 1.3-fold, increase in VD1/RPaD2 spiking frequency within 30 s after application. This was accompanied by a slight reduction in action potential amplitude. In addition, H2O2 induced a significant reduction in the steady-state bidirectional coupling ratio between the neurons. The maximal reduction in the coupling ratio, 1.8–1.9 fold, was measured 3 min after H2O2 application. However, the network input resistance did not undergo a detectable change. The voltage-gated Ca2+ channel blocker, nifedipine (1 × 10−4 M), abolished the effect of H2O2 on the coupling ratio and firing frequency. All the effects of H2O2 were reversible, that is, washing the preparation with standard physiological saline restored the properties of the neuronal coupling to the pre-treatment value. These data are consistent with a dynamic modulation of the gap-junction properties by H2O2 between these two neurons.

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References

  • Benjamin PR, Ings CT (1972) Golgi–Cox studies on the central nervous system of a gastropod mollusk. Zeitschr Zellforsch 128:564–582

    Article  CAS  Google Scholar 

  • Benjamin PR, Pilkington JB (1986) The electrotonic location of low-resistance intercellular junctions between a pair of giant neurones in the snail Lymnaea. J Physiol 370:111–126

    PubMed  CAS  Google Scholar 

  • Bennet MVL (1997) Gap junctions as electrical synapses. J Neurocytol 26:349–366

    Article  Google Scholar 

  • Bennet MVL, Barrio LC, Bargiello TA, Spray DC, Hertzberg E, Saez JC (1991) Gap junctions: new tools, new answers, new questions. Neuron 6:305–320

    Article  Google Scholar 

  • Camello-Almaraz C, Gomes-Pinilla PG, Pozo MJ, Camello PJ (2006) Mitochondrial reactive oxygen species and Ca2+ signaling. Am J Physiol Cell Physiol 291:C1082–C1088

    Article  PubMed  CAS  Google Scholar 

  • Catterall WA (2011) Voltage-gated calcium channels. Cold Spring Harbor Persp Biol 3:a003947

    Article  Google Scholar 

  • Colton CA, Colton JS, Gilbert DL (1986) Changes in synaptic transmission produced by hydrogen peroxide. Free Radic Biol Med 2:141–148

    CAS  Google Scholar 

  • Egelhaaf V, Benjamin PR (1983) Coupled neuronal oscillators in the snail Lymnaea stagnalis: endogenous cellular properties and network interactions. J Exp Biol 12:93–114

    Google Scholar 

  • Elofsson R, Carlberg M, Moroz L, Nezlin L, Sakharov D (1993) Is nitric oxide (NO) produced by invertebrate neurones? NeuroReport 4:279–282

    Article  PubMed  CAS  Google Scholar 

  • Finkel T (1998) Oxygen radicals and signalling. Curr Opin Cell Biol 10:248–253

    Article  PubMed  CAS  Google Scholar 

  • Getting PA (1989) Emerging principles governing the operation of neural networks. Annu Rev Neurosci 12:185–204

    Article  PubMed  CAS  Google Scholar 

  • Giniatullin AR, Giniatullin RA (2003) Dual action of hydrogen peroxide on synaptic transmission at the frog neuromuscular junction. J Physiol 552:283–293

    Article  PubMed  CAS  Google Scholar 

  • Heitler WJ, Edwards DH (1998) Effect of temperature on a voltage-sensitive electrical synapse in crayfish. J Exp Biol 201:503–513

    PubMed  CAS  Google Scholar 

  • Jefferys JGR (1995) Nonsynaptic modulation of neuronal activity in the brain: electrical currents and extracellular ions. Physiol Rev 75:689–723

    PubMed  CAS  Google Scholar 

  • Johnston MF, Ramón F (1981) Electrotonic coupling in internally perfused crayfish segmented axons. J Physiol 317:509–518

    PubMed  CAS  Google Scholar 

  • Katsuki H, Nakanishi C, Saito H, Matsuki N (1997) Biphasic effect of hydrogen peroxide on field potentials in rat hippocampal slices. Eur J Pharmacol 337:213–218

    Article  PubMed  CAS  Google Scholar 

  • Kim JH, Choi SH, Kim J, Lee BK, Lee KW, Lee HJ (2009) Differential regulation of the hydrogen-peroxide-induced inhibition of gap-junction intercellular communication by resveratrol and butylated hydroxyanisole. Mutat Res 671:40–44

    Article  PubMed  CAS  Google Scholar 

  • Lin D, Takemoto DJ (2005) Oxidative activation of protein kinase Cgamma through the C1 domain. Effects on gap junction. J Biol Chem 280:13682–13693

    Article  PubMed  CAS  Google Scholar 

  • Lin X, Veenstra RD (2004) Action potential modulation of connexin40 gap junction conductance. Am J Physiol Heart Circ Physiol 286:H1726–H1735

    Article  PubMed  CAS  Google Scholar 

  • Loewenstein WR (1981) Junctional intercellular communication: the cell-to-cell membrane channel. Physiol Rev 61:829–913

    PubMed  CAS  Google Scholar 

  • McMahon DG, Knapp AG, Dowling JE (1989) Horizontal cell gap junctions: single-channel conductance and modulation by dopamine. Proc Natl Acad Sci USA 86:7639–7643

    Article  PubMed  CAS  Google Scholar 

  • Murrant CL, Reid M (2001) Detection of reactive oxygen and reactive nitrogen species in skeletal muscle. Microsc Res Tech 55:236–248

    Article  PubMed  CAS  Google Scholar 

  • Pellmar TC (1995) Use of brain slices in the study of free-radical actions. J Neurosci Methods 59:93–98

    Article  PubMed  CAS  Google Scholar 

  • Ramachandran S, Xie LH, John SA, Subramaniam S, Lal R (2007) A novel role for connexin hemichannel in oxidative stress and smoking-induced cell injury. PLoS One 2:e712

    Article  PubMed  Google Scholar 

  • Rose B, Loewenstein WR (1976) Permeability of a cell junction and the local cytoplasmic free ionized calcium concentration: a study with aequorin. J Membr Biol 28:87–119

    Article  PubMed  CAS  Google Scholar 

  • Rouach N, Calvo CF, Duquennoy H, Glowinski J, Giaume C (2004) Hydrogen peroxide increases gap junctional communication and induce astrocyte toxicity: regulation by brain macrophages. Glia 45:28–38

    Article  PubMed  Google Scholar 

  • Sáez JC, Berthoud VM, Brañes MC, Martínez AD, Beyer EC (2003) Plasma membrane channels formed by connexins: their regulation and functions. Physiol Rev 83:1359–1400

    PubMed  Google Scholar 

  • Sidorov AV, Kazakevich VB, Moroz LL (1999) Nitric oxide selectively enhances cAMP levels and electrical coupling between identified RPaD2/VD1 neurons in the CNS of Lymnaea stagnalis (L.). Acta Biol Hung 50:229–233

    PubMed  CAS  Google Scholar 

  • Spray DC, Harris AL, Bennett MVL (1981) Gap junctional conductance is a simple and sensitive function of intracellular pH. Science 211:712–715

    Article  PubMed  CAS  Google Scholar 

  • Trexler EB, Bennet MVL, Bargiello TA, Verselis VK (1996) Voltage gating and permeation in a gap junction hemichannel. Proc Natl Acad Sci USA 93:5836–5841

    Article  PubMed  CAS  Google Scholar 

  • Turrens JF (2003) Mitochondrial formation of reactive oxygen species. J Physiol 552:335–344

    Article  PubMed  CAS  Google Scholar 

  • Weiss JS (1986) Oxygen, ischemia and inflammation. Acta Physiol Scand 548:9–37

    CAS  Google Scholar 

  • Wildering WC, van der Roest M, de Vlieger TA, Janse C (1991) Age-related changes in junctional and non-junctional conductances in two electrically coupled peptidergic neurons of the mollusk Lymnaea stagnalis. Brain Res 547:89–98

    Article  PubMed  CAS  Google Scholar 

  • Winlow W, Benjamin PR (1976) Neuronal mapping of the brain of the pond snail, Lymnaea stagnalis (L.). In: Salanki J (ed) Neurobiology of invertebrates. Gastropoda Brain. Academiai Kiado, Budapest, pp 41–59

    Google Scholar 

Download references

Acknowledgments

This work was supported by BRFFR (Grant B08R-075) and State Program for Scientific Research “Convergence” (task 3.3.03.4).

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Correspondence to Alexander V. Sidorov.

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Sidorov, A.V. Effect of hydrogen peroxide on electrical coupling between identified Lymnaea neurons. Invert Neurosci 12, 63–68 (2012). https://doi.org/10.1007/s10158-012-0128-7

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  • DOI: https://doi.org/10.1007/s10158-012-0128-7

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