Abstract
Using a patch-clamp technique in the whole-cell configuration, we identified the potassium M-type current and estimated its contribution to the integral depolarization-induced potassium current evoked in cultured hippocampal inhibitory interneurons of the rat. With the help of immunocytochemical labeling, we checked the presence of the KCNQ-family channels responsible for generation of M current in these neurons. It was demonstrated that non-inactivated potassium channels and channels with slow kinetics play the main role in the processes of repolarization of the membrane of inhibitory interneurons. In all studied cells, a potassium current non-inactivated with time and possessing kinetic parameters close to those of the M current developed in response to depolarization. In all cells, positive immunocytochemical labeling with respect to KCNQ2 channels was observed; however, its intensity varied significantly from neuron to neuron. The level of suppression of non-inactivated potassium currents by a blocker of KCNQ channels, linopirdine, varied noticeably in different cells; therefore, the level of expression of these channels in the interneurons under study is probably considerably dissimilar. The reason for incomplete suppression of the M current is perhaps the involvement of other potassium channels (e.g., those of Kv1 family) in the formation of this current.
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References
D. A. Brown, “M currents,” Ion Channels, 1, 55–94 (1988).
C. Yue and Y. Yaari, “KCNQ/M channels control spike afterdepolarization and burst generation in hippocampal neurons,” J. Neurosci., 24, No. 19, 4614–4624 (2004).
T. J. Jentsch, “Neuronal KCNQ potassium channels: physiology and role in disease,” Nat. Rev. Neurosci., 1, No. 1, 21–30 (2000).
D. E. Vetter, J. R. Mann, P. Wangemann, et al., “Inner ear defects induced by null mutation of the isk gene,” Neuron, 17, No. 6, 1251–1264 (1996).
J. Barhanin, F. Lesage, E. Guillemare, et al., “K(V)LQT1 and lsK (minK) proteins associate to form the I(Ks) cardiac potassium current,” Nature, 384, No. 6604, 78–80 (1996).
B. C. Schroeder, S. Waldegger, S. Fehr, et al., “A constitutively open potassium channel formed by KCNQ1 and KCNE3,” Nature, 403, No. 6766, 196–199 (2000).
T. Kharkovets, J. P. Hardelin, S. Safieddine, et al., “KCNQ4, a K+ channel mutated in a form of dominant deafness, is expressed in the inner ear and the central auditory pathway,” Proc. Natl. Acad. Sci. USA, 97, No. 8, 4333–4338 (2000).
E. C. Cooper, E. Harrington, Y. N. Jan, et al., “M channel KCNQ2 subunits are localized to key sites for control of neuronal network oscillations and synchronization in mouse brain,” J. Neurosci., 21, No. 24, 9529–9540 (2001).
N. Burgess, E. A. Maguire, and J. O’Keefe, “The human hippocampus and spatial and episodic memory, ” Neuron, 35, No. 4, 625–641 (2002).
T. F. Freund and G. Buzsaki, “Interneurons of the hippocampus,” Hippocampus, 6, No. 4, 347–470 (1996).
M. M. Shah, M. Mistry, S. J. Marsh, et al., “Molecular correlates of the M-current in cultured rat hippocampal neurons,” J. Physiol., 544, No. 1, 29–37 (2002).
S. A. Fedulova, D. V. Vasilyev, E. V. Isaeva, et al., “Possibility of multiquantal transmission at single inhibitory synapse in cultured rat hippocampal neurons,” Neuroscience, 92, No. 4, 1217–1230 (1999).
N. S. Veselovsky, F. Engert, and H. D. Lux, “Fast local superfusion technique,” Pflügers Arch., 432, No. 2, 351–354 (1996).
A. I. Gulyas, K. Toth, C. J. McBain, et al., “Stratum radiatum giant cells: a type of principal cell in the rat hippocampus,” Eur. J. Neurosci., 10, No. 12, 3813–3822 (1998).
N. Savic, P. Pedarzani, and M. Sciancalepore, “Medium afterhyperpolarization and firing pattern modulation in interneurons of stratum radiatum in the CA3 hippocampal region,” J. Neurophysiol., 85, No. 5, 1986–1997 (2001).
D. A. Brown and P. R. Adams, “Muscarinic suppression of a novel voltage-sensitive K+ current in a vertebrate neurone,” Nature, 283, No. 5748, 673–676 (1980).
A. Chikwendu and C. J. McBain, “Two temporally overlapping ‘delayed-rectifiers’ determine the voltage-dependent potassium current phenotype in cultured hippocampal interneurons,” J. Neurophysiol., 76, No. 3, 1477–1490 (1996).
G. M. Passmore, A. A. Selyanko, M. Mistry, et al., “KCNQ/M currents in sensory neurons: significance for pain therapy,” J. Neurosci., 23, No. 18, 7227–7236 (2003).
J. O. Dolly and D. N. Parcej, “Molecular properties of voltage-gated K+ channels,” J. Bioenerg. Biomembr., 28, No. 3, 231–253 (1996).
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Neirofiziologiya/Neurophysiology, Vol. 38, No. 3, pp. 198–204, May–June, 2006.
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Grigorov, A.O., Moskalyuk, A.A., Fedulova, S.A. et al. Differentiation of potassium currents in cultured inhibitory interneurons of the rat hippocampus (identification of the potassium M-type current). Neurophysiology 38, 163–168 (2006). https://doi.org/10.1007/s11062-006-0040-z
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DOI: https://doi.org/10.1007/s11062-006-0040-z