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Prolonged high-pressure treatments in mammalian skeletal muscle result in loss of functional sodium channels and altered calcium channel kinetics

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Abstract

Activation and inactivation of ion channels involve volume changes from conformal rearrangements of channel proteins. These volume changes are highly susceptible to changes in ambient pressure. Depending on the pressure level, channel function may be irreversibly altered by pressure. The corresponding structural changes persist through the post-decompression phase. High-pressure applications are a useful tool to evaluate the pressure dependence as well as pressure limits for reversibility of such alterations. Mammalian cells are only able to tolerate much lower pressures than microorganisms. Although some limits for pressure tolerance in mammalian cells have been evaluated, the mechanisms of pressure-induced alteration of membrane physiology, in particular of channel function, are unknown. To address this question, we recorded fast inward sodium (INa) and slowly activating L-type calcium (ICa) currents in single mammalian muscle fibers in the post-decompression phase after a prolonged 3-h, high-pressure treatment of up to 20 MPa. INa and ICa peak amplitudes were markedly reduced after pressure treatment at 20 MPa. This was not from a general breakdown of membrane integrity as judged from in situ high-pressure fluorescence microscopy. Membrane integrity was preserved even for pressures as high as 35 MPa at least for pressure applications of shorter durations. Therefore, the underlying mechanisms for the observed amplitude reductions have to be determined from the activation (time-to-peak [TTP]) and inactivation (τdec) kinetics of INa and ICa. No major changes in INa kinetics, but marked increases, both in TTP and τdec for ICa, were detected after 20 MPa. The apparent molecular volume changes (activation volumes) ΔV ‡ for the pressure-dependent irreversible alteration of channel gating approached zero for Na+ channels. For Ca2+ channels, ΔV‡ was very large, with approx 2.5-fold greater values for channel activation than inactivation (approx 210 Å3). We conclude, that in skeletal muscle, high pressure differentially and irreversibly affects the gating properties and the density of functional Na+ and Ca2+ channels. Based on these results, a model of high pressure-induced alterations to the channel conformation is proposed.

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Authors and Affiliations

  1. Medical Biophysics, Institute of Physiology & Pathophysiology, INF 326, Ruprecht-Karls-University, Heidelberg, Germany

    O. Friedrich, K. R. Kress & R. H. A. Fink

  2. Lehrstuhl für Maschinen-und Apparatekunde, Technische Universität München, Am Forum 2, 85350, Freising, Germany

    M. Hartmann & K. Sommer

  3. Lehrstuhl für Energie- und Umwelttechnik der Lebensmittelindustrie, Technische Universität München, Weihenstephaner Steig 22, 85350, Freising, Germany

    B. Frey

  4. Institute of Pharmacy & Molecular Biotechnology, University of Heidelberg, INF 346, Heidelberg, Germany

    H. Ludwig

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Friedrich, O., Kress, K.R., Hartmann, M. et al. Prolonged high-pressure treatments in mammalian skeletal muscle result in loss of functional sodium channels and altered calcium channel kinetics. Cell Biochem Biophys 45, 71–83 (2006). https://doi.org/10.1385/CBB:45:1:71

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