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Electrophysiological and Molecular Analysis of Kv7/KCNQ Potassium Channels in the Inferior Colliculus of Adult Guinea Pig

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Abstract

Neurons located in the inferior colliculus (IC) are on the path which processes acoustic information converging from the peripheral auditory system and to be sent through ascending pathways to superior structures. Previous in vitro recordings from early stage animals suggest that voltage-gated K channels underlie distinct neuronal discharge patterns observed in the IC. In this study, using reverse transcriptase quantitative polymerase chain reaction, we show the presence of a voltage-gated K channel family (Kv7/KCNQ) in the central nucleus of the IC (ICc) of the adult guinea pig. Whole-cell recordings from neurons in the nucleus were also made in slices from mature animals, and the action of specific openers and blockers demonstrated on the firing patterns. Our results indicate that mRNA from all members of the Kv7 family of channels are expressed in the ICc, but at different levels, and provide evidence that these channels can modulate neuronal excitability in this nucleus.

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References

  • Biervert, C., Schroeder, B. C., Kubisch, C., Berkovic, S. F., Propping, P., Jentsch, T. J., et al. (1998). A potassium channel mutation in neonatal human epilepsy. Science, 279, 403–406. doi:10.1126/science.279.5349.403.

    Article  PubMed  CAS  Google Scholar 

  • Caminos, E., Garcia-Pino, E., Martinez-Galan, J. R., & Juiz, J. M. (2007). The potassium channel KCNQ5/Kv7.5 is localized in synaptic endings of auditory brainstem nuclei of the rat. The Journal of Comparative Neurology, 505, 363–378. doi:10.1002/cne.21497.

    Article  PubMed  CAS  Google Scholar 

  • Coucke, P. J., Van, H. P., Kelley, P. M., Kunst, H., Schatteman, I., Van, V. D., et al. (1999). Mutations in the KCNQ4 gene are responsible for autosomal dominant deafness in four DFNA2 families. Human Molecular Genetics, 8, 1321–1328. doi:10.1093/hmg/8.7.1321.

    Article  PubMed  CAS  Google Scholar 

  • Delmas, P., & Brown, D. A. (2005). Pathways modulating neural KCNQ/M (Kv7) potassium channels. Nature Reviews. Neuroscience, 6, 850–862. doi:10.1038/nrn1785.

    Article  PubMed  CAS  Google Scholar 

  • Gu, N., Vervaeke, K., Hu, H., & Storm, J. F. (2005). Kv7/KCNQ/M and HCN/h, but not K(Ca)2/SK channels, contribute to the somatic medium after-hyperpolarization and excitability control in CA1 hippocampal pyramidal cells. The Journal of Physiology, 566, 689–715. doi:10.1113/jphysiol.2005.086835.

    Article  PubMed  CAS  Google Scholar 

  • Gutman, G. A., et al. (2003). International Union of Pharmacology. XLI. Compendium of voltage-gated ion channels: Potassium channels. Pharmacological Reviews, 55, 583–586. doi:10.1124/pr.55.4.9.

    Article  PubMed  CAS  Google Scholar 

  • Housley, G. D., & Ashmore, J. F. (1992). Ionic currents of outer hair cells isolated from the guinea-pig cochlea. The Journal of Physiology, 448, 73–98.

    PubMed  CAS  Google Scholar 

  • Hurley, K. M., Gaboyard, S., Zhong, M., Price, S. D., Wooltorton, J. R., Lysakowski, A., et al. (2006). M-like K+ currents in type I hair cells and calyx afferent endings of the developing rat utricle. The Journal of Neuroscience, 26, 10253–10269. doi:10.1523/JNEUROSCI.2596-06.2006.

    Article  PubMed  CAS  Google Scholar 

  • Jentsch, T. J. (2000). Neuronal KCNQ potassium channels: Physiology and role in disease. Nature Reviews. Neuroscience, 1, 21–30. doi:10.1038/35036198.

    Article  PubMed  CAS  Google Scholar 

  • Kananura, C., Biervert, C., Hechenberger, M., Engels, H., & Steinlein, O. K. (2000). The new voltage gated potassium channel KCNQ5 and neonatal convulsions. Neuroreport, 11, 2063–2067. doi:10.1097/00001756-200006260-00050.

    Article  PubMed  CAS  Google Scholar 

  • Kharkovets, T., Dedek, K., Maier, H., Schweizer, M., Khimich, D., Nouvian, R., et al. (2006). Mice with altered KCNQ4 K+ channels implicate sensory outer hair cells in human progressive deafness. The EMBO Journal, 25, 642–652. doi:10.1038/sj.emboj.7600951.

    Article  PubMed  CAS  Google Scholar 

  • Kharkovets, T., Hardelin, J. P., Safieddine, S., Schweizer, M., El-Amraoui, A., Petit, C., et al. (2000). KCNQ4, a K+ channel mutated in a form of dominant deafness, is expressed in the inner ear and the central auditory pathway. Proceedings of the National Academy of Sciences of the United States of America, 97, 4333–4338. doi:10.1073/pnas.97.8.4333.

    Article  PubMed  CAS  Google Scholar 

  • Kubisch, C., Schroeder, B. C., Friedrich, T., Lutjohann, B., El-Amraoui, A., Marlin, S., et al. (1999). KCNQ4, a novel potassium channel expressed in sensory outer hair cells, is mutated in dominant deafness. Cell, 96, 437–446. doi:10.1016/S0092-8674(00)80556-5.

    Article  PubMed  CAS  Google Scholar 

  • Liang, G. H., Jin, Z., Ulfendahl, M., & Jarlebark, L. (2006). Molecular analyses of KCNQ1–5 potassium channel mRNAs in rat and guinea pig inner ears: Expression, cloning, and alternative splicing. Acta Oto-Laryngologica, 126, 346–352. doi:10.1080/00016480500416777.

    Article  PubMed  CAS  Google Scholar 

  • Liang, G., Moore, E. J., Ulfendahl, M., Rydqvist, B., & Jarlebark, L. (2005). An M-like potassium current in the guinea pig cochlea. ORL; Journal for Oto-Rhino-Laryngology and Its Related Specialties, 67, 75–82. doi:10.1159/000085439.

    PubMed  CAS  Google Scholar 

  • Marcotti, W., Johnson, S. L., Holley, M. C., & Kros, C. J. (2003). Developmental changes in the expression of potassium currents of embryonic, neonatal and mature mouse inner hair cells. The Journal of Physiology, 548, 383–400. doi:10.1113/jphysiol.2002.034801.

    Article  PubMed  CAS  Google Scholar 

  • Navarro-Lopez, J. D., Alvarado, J. C., Marquez-Ruiz, J., Escudero, M., Delgado-Garcia, J. M., & Yajeya, J. (2004). A cholinergic synaptically triggered event participates in the generation of persistent activity necessary for eye fixation. The Journal of Neuroscience, 24, 5109–5118. doi:10.1523/JNEUROSCI.0235-04.2004.

    Article  CAS  Google Scholar 

  • Neyroud, N., Tesson, F., Denjoy, I., Leibovici, M., Donger, C., Barhanin, J., et al. (1997). A novel mutation in the potassium channel gene KVLQT1 causes the Jervell and Lange–Nielsen cardioauditory syndrome. Nature Genetics, 15, 186–189. doi:10.1038/ng0297-186.

    Article  PubMed  CAS  Google Scholar 

  • Robbins, J. (2001). KCNQ potassium channels: physiology, pathophysiology, and pharmacology. Pharmacology & Therapeutics, 90, 1–19. doi:10.1016/S0163-7258(01)00116-4.

    Article  CAS  Google Scholar 

  • Schenzer, A., Friedrich, T., Pusch, M., Saftig, P., Jentsch, T. J., Grotzinger, J., et al. (2005). Molecular determinants of KCNQ (Kv7) K+ channel sensitivity to the anticonvulsant retigabine. The Journal of Neuroscience, 25, 5051–5060. doi:10.1523/JNEUROSCI.0128-05.2005.

    Article  PubMed  CAS  Google Scholar 

  • Schroeder, B. C., Hechenberger, M., Weinreich, F., Kubisch, C., & Jentsch, T. J. (2000). KCNQ5, a novel potassium channel broadly expressed in brain, mediates M-type currents. The Journal of Biological Chemistry, 275, 24089–24095. doi:10.1074/jbc.M003245200.

    Article  PubMed  CAS  Google Scholar 

  • Schroeder, B. C., Kubisch, C., Stein, V., & Jentsch, T. J. (1998). Moderate loss of function of cyclic-AMP-modulated KCNQ2/KCNQ3 K+ channels causes epilepsy. Nature, 396, 687–690. doi:10.1038/25367.

    Article  PubMed  CAS  Google Scholar 

  • Sivaramakrishnan, S., & Oliver, D. L. (2001). Distinct K currents result in physiologically distinct cell types in the inferior colliculus of the rat. The Journal of Neuroscience, 21, 2861–2877.

    PubMed  CAS  Google Scholar 

  • Tatulian, L., Delmas, P., Abogadie, F. C., & Brown, D. A. (2001). Activation of expressed KCNQ potassium currents and native neuronal M-type potassium currents by the anti-convulsant drug retigabine. The Journal of Neuroscience, 21, 5535–5545.

    PubMed  CAS  Google Scholar 

  • van Rijn, C. M., & Willems-van, B. E. (2003). Synergy between retigabine and GABA in modulating the convulsant site of the GABAA receptor complex. European Journal of Pharmacology, 464, 95–100. doi:10.1016/S0014-2999(03)01426-2.

    Article  PubMed  Google Scholar 

  • Wang, H. S., Pan, Z., Shi, W., Brown, B. S., Wymore, R. S., Cohen, I. S., et al. (1998). KCNQ2 and KCNQ3 potassium channel subunits: Molecular correlates of the M-channel. Science, 282, 1890–1893. doi:10.1126/science.282.5395.1890.

    Article  PubMed  CAS  Google Scholar 

  • Wu, S. H. (2005). Biophysical properties of Inferior colliculus neurons. In J. A. Winer & C. E. Schreiner (Eds.), The inferior colliculus (pp. 282–311). New York: Springer.

    Chapter  Google Scholar 

  • Yeung, S. Y., Pucovsky, V., Moffatt, J. D., Saldanha, L., Schwake, M., Ohya, S., et al. (2007). Molecular expression and pharmacological identification of a role for K(v)7 channels in murine vascular reactivity. British Journal of Pharmacology, 151, 758–770. doi:10.1038/sj.bjp.0707284.

    Article  PubMed  CAS  Google Scholar 

  • Yue, C., & Yaari, Y. (2006). Axo-somatic and apical dendritic Kv7/M channels differentially regulate the intrinsic excitability of adult rat CA1 pyramidal cells. Journal of Neurophysiology, 95, 3480–3495. doi:10.1152/jn.01333.2005.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by the Wellcome Trust, Fundación Martin Escudero, Spanish Government fellows (JCI-2005-1775-25 and CD06/175) and the EU Marie Curie scheme. We would like to thank Dr. Vega-Avelaira for his advice on molecular experiments and Dr. Yajeya and Dr. de la Fuente for helpful comments.

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Authors and Affiliations

  1. Department of Physiology and UCL EAR Institute, University College London, Gower Street, London, WC1E 6BT, UK

    Juan Navarro-López & Jonathan F. Ashmore

  2. Department of Anatomy and Developmental Biology, UCL, Gower Street, London, WC1E 6BT, UK

    Lydia Jiménez-Díaz & Sandrine M. Géranton

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  1. Juan Navarro-López
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  2. Lydia Jiménez-Díaz
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  3. Sandrine M. Géranton
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  4. Jonathan F. Ashmore
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Correspondence to Juan Navarro-López.

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Navarro-López, J., Jiménez-Díaz, L., Géranton, S.M. et al. Electrophysiological and Molecular Analysis of Kv7/KCNQ Potassium Channels in the Inferior Colliculus of Adult Guinea Pig. J Mol Neurosci 37, 263–268 (2009). https://doi.org/10.1007/s12031-008-9130-2

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  • DOI: https://doi.org/10.1007/s12031-008-9130-2

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