Advertisement

Journal of Molecular Neuroscience

, Volume 48, Issue 1, pp 86–96 | Cite as

Expression of K2P Channels in Sensory and Motor Neurons of the Autonomic Nervous System

  • Alba Cadaveira-Mosquera
  • Montse Pérez
  • Antonio Reboreda
  • Paula Rivas-Ramírez
  • Diego Fernández-Fernández
  • J. Antonio LamasEmail author
Article

Abstract

Several types of neurons within the central and peripheral somatic nervous system express two-pore-domain potassium (K2P) channels, providing them with resting potassium conductances. We demonstrate that these channels are also expressed in the autonomic nervous system where they might be important modulators of neuronal excitability. We observed strong mRNA expression of members of the TRESK and TREK subfamilies in both the mouse superior cervical ganglion (mSCG) and the mouse nodose ganglion (mNG). Motor mSCG neurons strongly expressed mRNA transcripts for TRESK and TREK-2 subunits, whereas TASK-1 and TASK-2 subunits were only moderately expressed, with only few or very few transcripts for TREK-1 and TRAAK (TRESK ≈ TREK-2 > TASK-2 ≈ TASK-1 > TREK-1 > TRAAK). Similarly, the TRESK and TREK-1 subunits were the most strongly expressed in sensorial mNG neurons, while TASK-1 and TASK-2 mRNAs were moderately expressed, and fewer TREK-2 and TRAAK transcripts were detected (TRESK ≈ TREK-1 > TASK-1 ≈ TASK-2 > TREK-2 > TRAAK). Moreover, cell-attached single-channel recordings showed a major contribution of TRESK and TREK-1 channels in mNG. As the level of TRESK mRNA expression was not statistically different between the ganglia analysed, the distinct expression of TREK-1 and TREK-2 subunits was the main difference observed between these structures. Our results strongly suggest that TRESK and TREK channels are important modulators of the sensorial and motor information flowing through the autonomic nervous system, probably exerting a strong influence on vagal reflexes.

Keywords

K2P channels Superior cervical ganglion Nodose ganglion Mouse Immunocytochemistry qRT-PCR Cell-attached patch Perforated patch 

Notes

Acknowledgments

This work was supported by grants from the Spanish Government (MICINN BFU2008-02952/BFI and CONSOLIDER CSD2008-00005), the Galician Government (INBIOMED 2009/063) and the University of Vigo to JAL. SGIker technical and human support (UPV/EHU) is gratefully acknowledged. We also thank Vanesa Domínguez for her technical assistance.

References

  1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410PubMedGoogle Scholar
  2. Brown DA, Abogadie FC, Allen TG, Buckley NJ, Caulfield MP, Delmas P, Haley JE, Lamas JA, Selyanko AA (1997) Muscarinic mechanisms in nerve cells. Life Sci 60:1137–1144PubMedCrossRefGoogle Scholar
  3. Brown DA, Constanti A (1980) Intracellular observations on the effects of muscarinic agonists on rat sympathetic neurones. Br J Pharmacol 70:593–608PubMedCrossRefGoogle Scholar
  4. Browning KN, Mendelowitz D (2003) Musings on the wanderer: what's new in our understanding of vago-vagal reflexes?: II. Integration of afferent signaling from the viscera by the nodose ganglia. Am J Physiol Gastrointest Liver Physiol 284:G8–G14PubMedGoogle Scholar
  5. Cadaveira-Mosquera A, Ribeiro SJ, Reboreda A, Pérez M, Lamas JA (2011) Activation of TREK currents by the neuroprotective agent riluzole in mouse sympathetic neurons. J Neurosci 31:1375–1385PubMedCrossRefGoogle Scholar
  6. Czirjak G, Petheo GL, Spat A, Enyedi P (2001) Inhibition of TASK-1 potassium channel by phospholipase C. Am J Physiol Cell Physiol 281:C700–C708PubMedGoogle Scholar
  7. Czirjak G, Toth ZE, Enyedi P (2004) The two-pore domain K+ channel, TRESK, is activated by the cytoplasmic calcium signal through calcineurin. J Biol Chem 279:18550–18558PubMedCrossRefGoogle Scholar
  8. Dobler T, Springauf A, Tovornik S, Weber M, Schmitt A, Sedlmeier R, Wischmeyer E, Doring F (2007) TRESK two-pore-domain K+ channels constitute a significant component of background potassium currents in murine dorsal root ganglion neurones. J Physiol 585:867–879PubMedCrossRefGoogle Scholar
  9. Fink M, Duprat F, Lesage F, Reyes R, Romey G, Heurteaux C, Lazdunski M (1996) Cloning, functional expression and brain localization of a novel unconventional outward rectifier K+ channel. EMBO J 15:6854–6862PubMedGoogle Scholar
  10. Fink M, Lesage F, Duprat F, Heurteaux C, Reyes R, Fosset M, Lazdunski M (1998) A neuronal two P domain K+ channel stimulated by arachidonic acid and polyunsaturated fatty acids. EMBO J 17:3297–3308PubMedCrossRefGoogle Scholar
  11. Han J, Gnatenco C, Sladek CD, Kim D (2003) Background and tandem-pore potassium channels in magnocellular neurosecretory cells of the rat supraoptic nucleus. J Physiol 546:625–639PubMedCrossRefGoogle Scholar
  12. Kang D, Choe C, Kim D (2004a) Functional expression of TREK-2 in insulin-secreting MIN6 cells. Biochem Biophys Res Commun 323:323–331PubMedCrossRefGoogle Scholar
  13. Kang D, Mariash E, Kim D (2004b) Functional expression of TRESK-2, a new member of the tandem-pore K + channel family. J Biol Chem 279:28063–28070PubMedCrossRefGoogle Scholar
  14. Kang D, Han J, Kim D (2006) Mechanism of inhibition of TREK-2 (K2P10.1) by the Gq-coupled M3 muscarinic receptor. Am. J. Physiol. Cell Physiol 291:C649–C656CrossRefGoogle Scholar
  15. Kang D, Kim D (2006) TREK-2 (K2P10.1) and TRESK (K2P18.1) are major background K+ channels in dorsal root ganglion neurons. Am J Physiol Cell Physiol 291:C138–C146PubMedCrossRefGoogle Scholar
  16. Karschin C, Wischmeyer E, Preisig-Muller R, Rajan S, Derst C, Grzeschik KH, Daut J, Karschin A (2001) Expression pattern in brain of TASK-1, TASK-3, and a tandem pore domain K+ channel subunit, TASK-5, associated with the central auditory nervous system. Mol Cell Neurosci 18:632–648PubMedCrossRefGoogle Scholar
  17. Konishi T (1996) Developmental and activity-dependent changes in K+ currents in satellite glial cells in mouse superior cervical ganglion. Brain Res 708:7–15PubMedCrossRefGoogle Scholar
  18. Lamas JA (1999) The role of calcium in M-current inhibition by muscarinic agonists in rat sympathetic neurons. Neuroreport 10:2395–2400PubMedCrossRefGoogle Scholar
  19. Lamas JA, Reboreda A, Codesido V (2002) Ionic basis of the resting membrane potential in cultured rat sympathetic neurons. Neuroreport 13:585–591PubMedCrossRefGoogle Scholar
  20. Lamas JA, Romero M, Reboreda A, Sanchez E, Ribeiro SJ (2009) A riluzole- and valproate-sensitive persistent sodium current contributes to the resting membrane potential and increases the excitability of sympathetic neurones. Pflugers Arch -Eur J Physiol 458:589–599CrossRefGoogle Scholar
  21. Lauritzen I, Blondeau N, Heurteaux C, Widmann C, Romey G, Lazdunski M (2000) Polyunsaturated fatty acids are potent neuroprotectors. EMBO J 19:1784–1793PubMedCrossRefGoogle Scholar
  22. Lembrechts R, Pintelon I, Schnorbusch K, Timmermans JP, Adriaensen D, Brouns I (2011) Expression of mechanogated two-pore domain potassium channels in mouse lungs: special reference to mechanosensory airway receptors. Histochem Cell Biol 136:371–385PubMedCrossRefGoogle Scholar
  23. Lesage F, Guillemare E, Fink M, Duprat F, Lazdunski M, Romey G, Barhanin J (1996) TWIK-1, a ubiquitous human weakly inward rectifying K+ channel with a novel structure. EMBO J 15:1004–1011PubMedGoogle Scholar
  24. Lin W, Burks CA, Hansen DR, Kinnamon SC, Gilbertson TA (2004) Taste receptor cells express pH-sensitive leak K+ channels. J Neurophysiol 92:2909–2919PubMedCrossRefGoogle Scholar
  25. Lindner M, Leitner MG, Halaszovich CR, Hammond GR, Oliver D (2011) Probing the regulation of TASK potassium channels by PI(4,5)P2 with switchable phosphoinositide phosphatases. J Physiol 589:3149–3162PubMedCrossRefGoogle Scholar
  26. Liu C, Au JD, Zou HL, Cotten JF, Yost CS (2004) Potent activation of the human tandem pore domain K channel TRESK with clinical concentrations of volatile anesthetics. Anesth Analg 99:1715–1722PubMedCrossRefGoogle Scholar
  27. Lotshaw DP (2007) Biophysical, pharmacological, and functional characteristics of cloned and native mammalian two-pore domain K+ channels. Cell Biochem Biophys 47:209–256PubMedCrossRefGoogle Scholar
  28. Maingret F, Lauritzen I, Patel AJ, Heurteaux C, Reyes R, Lesage F, Lazdunski M, Honore E (2000) TREK-1 is a heat-activated background K+ channel. EMBO J 19:2483–2491PubMedCrossRefGoogle Scholar
  29. Martínez-Pinna J, Lamas JA, Gallego R (2002) Calcium current components in intact and dissociated adult mouse sympathetic neurons. Brain Res 951:227–236PubMedCrossRefGoogle Scholar
  30. Medhurst AD, Rennie G, Chapman CG, Meadows H, Duckworth MD, Kelsell RE, Gloger II, Pangalos MN (2001) Distribution analysis of human two pore domain potassium channels in tissues of the central nervous system and periphery. Brain Res Mol Brain Res 86:101–114PubMedCrossRefGoogle Scholar
  31. Reyes R, Duprat F, Lesage F, Fink M, Salinas M, Farman N, Lazdunski M (1998) Cloning and expression of a novel pH-sensitive two pore domain K+ channel from human kidney. J Biol Chem 273:30863–30869PubMedCrossRefGoogle Scholar
  32. Romero M, Reboreda A, Sánchez E, Lamas JA (2004) Newly developed blockers of the M-current do not reduce spike frequency adaptation in cultured mouse sympathetic neurons. Eur J Neurosci 19:2693–2702PubMedCrossRefGoogle Scholar
  33. Sano Y, Inamura K, Miyake A, Mochizuki S, Kitada C, Yokoi H, Nozawa K, Okada H, Matsushime H, Furuichi K (2003) A novel two-pore domain K+ channel, TRESK, is localized in the spinal cord. J Biol Chem 278:27406–27412PubMedCrossRefGoogle Scholar
  34. Shoji Y, Yamaguchi-Yamada M, Yamamoto Y (2010) Glutamate- and GABA-mediated neuron-satellite cell interaction in nodose ganglia as revealed by intracellular calcium imaging. Histochem Cell Biol 134:13–22PubMedCrossRefGoogle Scholar
  35. Simkin D, Cavanaugh EJ, Kim D (2008) Control of the single channel conductance of K2P10.1 (TREK-2) by the amino-terminus: role of alternative translation initiation. J Physiol 586:5651–63.36PubMedCrossRefGoogle Scholar
  36. Suh BC, Hille B (2002) Recovery from muscarinic modulation of M current channels requires phosphatidylinositol 4,5-bisphosphate synthesis. Neuron 35:507–520PubMedCrossRefGoogle Scholar
  37. Talley EM, Sirois JE, Lei Q, Bayliss DA (2003) Two-pore-domain (KCNK) potassium channels: dynamic roles in neuronal function. Neuroscientist 9:46–56PubMedCrossRefGoogle Scholar
  38. Talley EM, Solorzano G, Lei Q, Kim D, Bayliss DA (2001) CNS distribution of members of the two-pore-domain (KCNK) potassium channel family. J Neurosci 21:7491–7505PubMedGoogle Scholar
  39. Winks JS, Hughes S, Filippov AK, Tatulian L, Abogadie FC, Brown DA, Marsh SJ (2005) Relationship between membrane phosphatidylinositol-4,5-bisphosphate and receptor-mediated inhibition of native neuronal M channels. J Neurosci 25:3400–3413PubMedCrossRefGoogle Scholar
  40. Yamamoto Y, Hatakeyama T, Taniguchi K (2009) Immunohistochemical colocalization of TREK-1, TREK-2 and TRAAK with TRP channels in the trigeminal ganglion cells. Neurosci Lett 454:129–133PubMedCrossRefGoogle Scholar
  41. Yoo S, Liu J, Sabbadini M, Au P, Xie GX, Yost CS (2009) Regional expression of the anesthetic-activated potassium channel TRESK in the rat nervous system. Neurosci Lett 465:79–84PubMedCrossRefGoogle Scholar
  42. Zhang H, Craciun LC, Mirshahi T, Rohacs T, Lopes CM, Jin T, Logothetis DE (2003) PIP(2) activates KCNQ channels, and its hydrolysis underlies receptor-mediated inhibition of M currents. Neuron 37:963–975PubMedCrossRefGoogle Scholar
  43. Zhao H, Sprunger LK, Simasko SM (2010) Expression of transient receptor potential channels and two-pore potassium channels in subtypes of vagal afferent neurons in rat. Am J Physiol Gastrointest Liver Physiol 298:G212–G221PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Alba Cadaveira-Mosquera
    • 1
  • Montse Pérez
    • 1
    • 2
  • Antonio Reboreda
    • 1
  • Paula Rivas-Ramírez
    • 1
  • Diego Fernández-Fernández
    • 1
  • J. Antonio Lamas
    • 1
    Email author
  1. 1.Department of Functional Biology, Faculty of BiologyUniversity of VigoVigoSpain
  2. 2.Centro Oceanográfico de VigoInstituto Español de OceanografíaVigoSpain

Personalised recommendations