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Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
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Dual Effects of Nitric Oxide on the Large Conductance Calcium-activated Potassium Channels of Rat Brain

  • Lee, Ji-Eun (Department of Physiology and Biophysics, Inha University College of Medicine) ;
  • Kwak, Ji-Yeon (Department of Physiology and Biophysics, Inha University College of Medicine) ;
  • Suh, Chang-Kook (Department of Physiology and Biophysics, Inha University College of Medicine) ;
  • Shin, Jung-Hoon (Department of Physiology and Biophysics, Inha University College of Medicine)
  • Received : 2005.09.13
  • Accepted : 2005.11.25
  • Published : 2006.01.31
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Abstract

Previously, we have shown that nitric oxide (NO) directly activates the Maxi-K channels. In the present study, we have investigated whether NO has prolonged effects on the Maxi-K channels reconstituted in lipid bilayer. Application of S-nitroso-N-acetyl-D, L-penicillamine (SNAP), a NO donor, induced an immediate increase of open probability (Po) of Maxi-K channel in a dose-dependent manner. When SNAP was removed from the cytosolic solution, the Po did not simply returned to, but irreversibly decreased to a level lower than that of the control Po. At 0.2 mM, (Z)-[N-(3-Ammoniopropyl)-N-(n-propyl)amino] diazen-1-ium-1,2-diolate (PAPA-NO), another NO donor, produced a similar increase of Po and decrease of Po upon washout. The increasing effects of SNAP on Po were not blocked by either 50 U/ml superoxide dismutase (SOD) or 2 mM N-ethylmaleimide (NEM) pre-treatments. However, NEM appears to be ineffective when applied after SNAP. These results suggest that NO can modulate Maxi-K channel via direct interaction and chemical modification, such as S-nitrosylation in the brain.

Keywords

References

  1. Atkinson, N. S., Robertson, G. A. and Ganetzky, B. (1991) A component of calcium-activated potassium channels encoded by the Drosophila slo locus. Science 253, 551-555. https://doi.org/10.1126/science.253.5015.91
  2. Bolotina, V. M., Najibi, S., Palacino, J. J., Pagano, P. J. and Cohen, R. A. (1994) Nitric oxide directly activates calciumdependent potassium channels in vascular smooth muscle. Nature 368, 850-853. https://doi.org/10.1038/368850a0
  3. Bon C. L. and Garthwaite J. (2001) Nitric oxide-induced potentiation of CA1 hippocampal synaptic transmission during baseline stimulation is strictly frequency-dependent. Neuropharmacology 40, 501-507. https://doi.org/10.1016/S0028-3908(00)00193-3
  4. Bon C. L. and Garthwaite J. (2003) On the role of nitric oxide in hippocampal long-term potentiation. J. Neurosci. 23, 1941-1948. https://doi.org/10.1523/JNEUROSCI.23-05-01941.2003
  5. Butler, A., Tsunoda, S., McCobb, D. P., Wei, A. and Salkoff, L. (1993) mSlo, a complex mouse gene encoding 'maxi' calciumactivated potassium channels. Science 261, 221-224. https://doi.org/10.1126/science.7687074
  6. Dawson, T. M. and Snyder, S. H. (1994) Gases as biological messengers: nitric oxide and carbon monoxide in the brain. J. Neurosci. 14, 5147-5159. https://doi.org/10.1523/JNEUROSCI.14-09-05147.1994
  7. Dawson, T. M., Dawson, V. L. and Snyder, S. H. (1994) Molecular mechanisms of nitric oxide actions in the brain. Ann. N. Y. Acad. Sci.738, 76-85.
  8. Fagni, L. and Bockaert, J. (1996) Effects of nitric oxide on glutamate-gated channels and other ionic channels. J. Chem. Neuroanat. 10, 231-240. https://doi.org/10.1016/0891-0618(95)00140-9
  9. Gally, J. A., Montague, P. R., Reeke, G. N. and Edelman, G. M. (1990) The NO hypothesis: possible effects of a short-lived, rapidly diffusible signal in the development and function of the nervous system. Proc. Natl. Acad. Sci. USA 87, 3547-3551. https://doi.org/10.1073/pnas.87.9.3547
  10. Ha, T. S., Jeong, S. Y., Cho, S. W., Jeon H. K., Roh, G. S., Choi, W. S. and Park, C. S. (2000) Functional characteristics of two BKCa channel variants differentially expressed in rat brain tissues. Eur. J. Biochem. 267, 910-918. https://doi.org/10.1046/j.1432-1327.2000.01076.x
  11. Hawkins R. D., Son H. and Arancio O. (1998) Nitric oxide as a retrograde messenger during long-term potentiation in hippocampus. Prog. Brain Res. 118, 155-172. https://doi.org/10.1016/S0079-6123(08)63206-9
  12. Jeong, S. Y., Ha, T. S., Park, C. -S., Uhm, D. Y. and Chung, S. (2001) Nitric Oxide Directly Activates Large Conductance $Ca^{2+}$ -activated $K^{+}$ Channels (rSlo). Mol. Cell 12, 97-102.
  13. Knaus, H. G., Schwarzer, C., Koch, R. O., Eberhart, A., Kaczorowski, G. J., Glossmann, H., Wunder, F., Pongs, O., Garcia, M. L. and Sperk, G. (1996) Distribution of highconductance Ca(2+)-activated $K^{+}$ channels in rat brain: targeting to axons and nerve terminals. J. Neurosci. 16, 955-963. https://doi.org/10.1523/JNEUROSCI.16-03-00955.1996
  14. Lancaster, B., Nicoll, R. A. and Perkel, D. J. (1991) Calcium activates two types of potassium channels in rat hippocampal neurons in culture. J. Neurosci. 11, 23-30. https://doi.org/10.1523/JNEUROSCI.11-01-00023.1991
  15. Lei, S. Z., Pan, Z. H., Aggarwal, S. K., Chen, H. S., Hartman, J., Sucher, N. J. and Lipton, S.A. (1992) Effect of nitric oxide production on the redox modulatory site of the NMDA receptor-channel complex. Neuron 8, 1087-1099. https://doi.org/10.1016/0896-6273(92)90130-6
  16. Malen, P. L. and Chapman, P. F. (1997) Nitric oxide facilitates long-term potentiation, but not long-term depression. J. Neurosci. 17, 2645-2651. https://doi.org/10.1523/JNEUROSCI.17-07-02645.1997
  17. Nelson, M. T., Cheng, H., Rubart, M., Santana, L. F., Bonev, A. D., Knot, H. J. and Lederer, W. J. (1995) Relaxation of arterial smooth muscle by calcium sparks. Science 270, 633-637. https://doi.org/10.1126/science.270.5236.633
  18. Pineda, J., Kogan, J. H. and Aghajanian, G. K. (1996) Nitric oxide and carbon monoxide activate locus coeruleus neurons through a cGMP-dependent protein kinase: involvement of a nonselective cationic channel. J. Neurosci. 16, 1389-1399. https://doi.org/10.1523/JNEUROSCI.16-04-01389.1996
  19. Reinhart, P. H., Chung, S. and Levitan, I. B. (1989) A family of calcium-dependent potassium channels from rat brain. Neuron 2, 1031-1041. https://doi.org/10.1016/0896-6273(89)90227-4
  20. Shin, J. H., Chung, S., Park, E. J., Uhm, D. Y. and Suh, C. K. (1997) Nitric oxide directly activates calcium-activated potassium channels from rat brain reconstituted into planar lipid bilayer. FEBS Lett. 415, 299-302. https://doi.org/10.1016/S0014-5793(97)01144-7
  21. Tseng-Crank, J., Foster, C. D., Krause, J. D., Mertz, R., Godinot, N., DiChiara, T. J. and Reinhart, P. H. (1994) Cloning, expression, and distribution of functionally distinct Ca(2+)- activated $K^+$ channel isoforms from human brain. Neuron 13, 1315-1330. https://doi.org/10.1016/0896-6273(94)90418-9
  22. Wang, Z. W., Nara, M., Wang, Y. X. and Kotlikoff, M. I. (1997) Redox regulation of large conductance Ca(2+)-activated $K^+$ channels in smooth muscle cells. J. Gen. Physiol. 110, 35-44. https://doi.org/10.1085/jgp.110.1.35

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