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K+ Channels of Squid Giant Axons Open by an Osmotic Stress in Hypertonic Solutions Containing Nonelectrolytes

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Abstract

In hypertonic solutions made by adding nonelectrolytes, K+ channels of squid giant axons opened at usual asymmetrical K+ concentrations in two different time courses; an initial instantaneous activation (I IN) and a sigmoidal activation typical of a delayed rectifier K+ channel (I D). The current–voltage relation curve for I IN was fitted well with Goldman equation described with a periaxonal K+ concentration at the membrane potential above −10 mV. Using the activation–voltage curve obtained from tail currents, K+ channels for I IN are confirmed to activate at the membrane potential that is lower by 50 mV than those for I D. Both I IN and I D closed similarly at the holding potential below −100 mV. The logarithm of I IN/I D was linearly related with the osmolarity for various nonelectrolytes. Solute inaccessible volumes obtained from the slope increased with the nonelectrolyte size from 15 to 85 water molecules. K+ channels representing I D were blocked by open channel blocker tetra-butyl ammonium (TBA) more efficiently than in the absence of I IN, which was explained by the mechanism that K+ channels for I D were first converted to those for I IN by the osmotic pressure and then blocked. So K+ channels for I IN were suggested to be derived from the delayed rectifier K+ channels. Therefore, the osmotic pressure is suggested to exert delayed-rectifier K+ channels to open in shrinking rather hydrophilic flexible parts outside the pore than the pore itself, which is compatible with the recent structure of open K+ channel pore.

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Acknowledgments

I wish to thank Y. Nitani for collecting squid. I also thank members of the National Institute for Physiological Sciences for supporting this work. This work was supported by a grant from JSPS (12670053).

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Authors and Affiliations

  1. Department of Cell Physiology, National Institute for Physiological Sciences, National Institutes of Natural Sciences, Nishigonaka 38, Myodaiji, Okazaki, 444-8585, Japan

    Fumio Kukita

  2. Ine Marine Laboratory of National Institute for Physiological Sciences, National Institutes of Natural Sciences, Ine, Kyoto, 626-0424, Japan

    Fumio Kukita

  3. Department of Physiological Sciences, School of Life Science, The Graduate University for Advanced Studies, Nishigonaka 38, Myodaiji, Okazaki, 444-8585, Japan

    Fumio Kukita

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Kukita, F. K+ Channels of Squid Giant Axons Open by an Osmotic Stress in Hypertonic Solutions Containing Nonelectrolytes. J Membrane Biol 242, 119–135 (2011). https://doi.org/10.1007/s00232-011-9383-5

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