Reactive oxygen species alters the electrophysiological properties and raises [Ca2+](i) in intracardiac ganglion neurons

Jhansi Dyavanapalli, Katrina Rimmer, Alexander A. Harper

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    Abstract

    Dyavanapalli J, Rimmer K, Harper AA. Reactive oxygen species alters the electrophysiological properties and raises [Ca2+](i) in intracardiac ganglion neurons. Am J Physiol Regul Integr Comp Physiol 299: R42-R54, 2010. First published May 5, 2010; doi:10.1152/ajpregu.00053.2010.-We have investigated the effects of the reactive oxygen species (ROS) donors hydrogen peroxide (H2O2) and tert-butyl hydroperoxide (t-BHP) on the intrinsic electrophysiological characteristics: ganglionic transmission and resting [Ca2+](i) in neonate and adult rat intracardiac ganglion (ICG) neurons. Intracellular recordings were made using sharp microelectrodes filled with either 0.5 M KCl or Oregon Green 488 BAPTA-1, allowing recording of electrical properties and measurement of [Ca2+](i). H2O2 and t-BHP both hyperpolarized the resting membrane potential and reduced membrane resistance. In adult ICG neurons, the hyperpolarizing action of H2O2 was reversed fully by Ba2+ and partially by tetraethylammonium, muscarine, and linopirdine. H2O2 and t-BHP reduced the action potential afterhyperpolarization (AHP) amplitude but had no impact on either overshoot or AHP duration. ROS donors evoked an increase in discharge adaptation to long depolarizing current pulses. H2O2 blocked ganglionic transmission in most ICG neurons but did not alter nicotine-evoked depolarizations. By contrast, t-BHP had no significant action on ganglionic transmission. H2O2 and t- BHP increased resting intracellular Ca2+ levels to 1.6 (+/- 0.6, n = 11, P <0.01) and 1.6 (+/- 0.3, n = 8, P < 0.001), respectively, of control value (1.0, similar to 60 nM). The ROS scavenger catalase prevented the actions of H2O2, and this protection extended beyond the period of application. Superoxide dismutase partially shielded against the action of H2O2, but this was limited to the period of application. These data demonstrate that ROS decreases the excitability and ganglionic transmission of ICG neurons, attenuating parasympathetic control of the heart.

    Original languageEnglish
    Pages (from-to)R42-R54
    Number of pages13
    JournalAmerican Journal of Physiology: Regulatory Integrative and Comparative Physiology
    Volume299
    Issue number1
    DOIs
    Publication statusPublished - Jul 2010

    Keywords

    • synaptic transmission
    • reactive oxygen species
    • intracellular calcium
    • intrinsic cardiac neuron
    • hydrogen peroxide
    • INTRINSIC CARDIAC NEURONS
    • SYNAPTIC-TRANSMISSION
    • HYDROGEN-PEROXIDE
    • INTRACELLULAR CALCIUM
    • MYENTERIC NEURONS
    • OXIDATIVE STRESS
    • NERVOUS-SYSTEM
    • FREE-RADICALS
    • IN-VITRO
    • RAT

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