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The effects of rises in external K+ on the hyperpolarization-activated cation current I h in rat dorsal root ganglion neurons

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Abstract

The effects of rises in external K+ (Kext) were examined on the hyperpolarization-activated cation current (I h) in rat dorsal root ganglion neurons using the whole-cell patch clamp technique. The results showed that Kext increased I h in a certain concentration and voltage-dependent manner. At the basal Kext level (4 mmol/L), I h had a maximal amplitude of 1085 ± 340 pA which was enhanced by ∼45% and ∼92% at 8 and 16 mmol/L Kext, respectively. The midpoint activation voltage was significantly shifted from −98 mV in the hyperpolarizing direction by 8 and 12 mV at 8 and 16 mmol/L Kext, respectively with alteration of the activation course of I h. The short time constants of activation became longer with the increasing amplitude of the command potential upon rises in Kext. The long time constants became shorter. The reversal potentials were shifted in the positive direction without significant alterations upon rises in Kext. According to the functional role of I h, Kext increased I h, resulting in an enhanced neuronal excitability, which might produce activation potential abnormality and perhaps neuropathic pain involved.

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References

  1. Liu C N, Michaelis M, Amir R, Devor M. Spinal nerve injury enhances sub-threshold membrane potential oscillations in DRG neurons: Relation to neuropathic pain. J Neurophysiol, 2000,84:205–215

    CAS  Google Scholar 

  2. Luo F. Pathology ache and dorsal root ganglion (in Chinese). Shanghai J Acupunct Moxibusti, 2005, 242: 36–36

    Google Scholar 

  3. Banks M Y, Pearce R A, Smith P. Hyperpolarization-activated cation current (I h) in neurons of the medial nucleus of the trapezoid body; voltage-clamp analysis and enhancement by norepinephrine and cAMP suggest a modulatory mechanism in the auditory brain stem. J Neurophysiol, 1993, 70: 1420–1430

    CAS  Google Scholar 

  4. DiFrancesco D. Block and activation of the pace-maker channel in calf purkinje fibres: Effects of potassium, caesium and rubidium. J Physiol, 1982, 329: 485–507

    CAS  Google Scholar 

  5. Wang Z, Van B D, Ypey D L. Hyperpolarization-activated currents in the growth cone and soma of neonatal rat dorsal root ganglion neurons in culture. J Neurophysiol, 1997, 78: 177–186

    CAS  Google Scholar 

  6. McCormick D A, Pape H C. Properties of a hyperpolarization-activated cation current and its role in rhythmic oscillation in thalamic relay neurons. J Physiol, 1990, 431:291–318

    CAS  Google Scholar 

  7. Pape H C. Queer current and pacemaker: The hyperpolarization-activated cation current in neurons. Annu Rev Physiol, 1996, 58: 299–327

    Article  CAS  Google Scholar 

  8. Scroggs R S, Todorovic S M, Andeson E G, Fox A P. Variation in I H, I IR, I LEAK between acutely isolated adualt rat dorsal root ganglion neurons of different size. Neurophysiol, 1994, 1: 71–279

    Google Scholar 

  9. Surges R, Freiman T M, Feuerstein T J. K+-induced changes in the properties of the hyperpolarization-activated cation current I h rat CA1 pyramidal cells. Neurosci Lett, 2002, 332: 136–140

    Article  CAS  Google Scholar 

  10. Deng L B, Cao X J, Yao L, Han J S, Wan Y. Alteration of hyperpolarization-activated current (I h) in dorsal root ganglion neurons in rats with neuropathic pain induced by spinal nerve ligation (in Chinese). J Peking Univ, 2002, 34: 252–255

    CAS  Google Scholar 

  11. Gabriel S, Eilers A, Kivil A, Kovacs R, Schulze K, Lehmann T N, Heinemann U. Effects of barium on stimulus induced changes in extracellular potassium concentration in area CA1 of hippocampal slices from normal and pilocarpine-treated epileptic rats. Neurosci Lett, 1998, 242: 9–12

    Article  CAS  Google Scholar 

  12. Chaplan S R, Guo H Q, Lee D H, Luo L, Liu C, Kuei C, Velumian A A, Butler M P, Brown S M, Dubin A E, Neuronal hyperpolarization-activated pacemaker channels drive neuropathic pain. J Neurosci, 2003,23(4): 1169–1178

    CAS  Google Scholar 

  13. Dalle C, Eisenach J C, Peripheral block of the hyperpolarization-activated cation current (I h) reduces mechanical allodynia in animal models of postoperative and neuropathic pain. Reg Anesth Pain Med, 2005, 30(3): 243–248

    Google Scholar 

  14. Sun Q, Xing G G, Tu H Y, Han J S, Wan Y. Inhibition of hyperpolarization-activated current by ZD7288 suppresses ectopic discharges of injured dorsal root ganglion neurons in a rat model of neuropathic pain. Brain Res, 2005, 1032(1–2): 63–69

    Article  CAS  Google Scholar 

  15. Jauch R, Windmüller O, Lehmann T N, Heinemann U, Gabriel S, Effects of barium, furosemide, ouabaine and 4,4′-diisothiocyanatostilbene-2,2′-disulfonic acid (DIDS) on ionophoretically-induced changes in extracellular potassium concentration in hippocampal slices from rats and from patients with epilepsy. Brain Res, 2002, 925: 18–27

    Article  CAS  Google Scholar 

  16. Wahl-Schott C, Biel M. HCN channels: Structure, cellular regulation and physiological function. Cell Mol Life Sci, 2009, 66(3): 470–494

    Article  CAS  Google Scholar 

  17. Du Z Q, Zhou Y F, Yang P. Sulfur dioxide derivatives increase a hyperpolarization-activated inward current in dorsal root ganglion neurons. Toxicology, 2007, 239: 180–185

    Article  CAS  Google Scholar 

  18. Harris N C, Constanti A. Mechanism of block by ZD7288 of the hyperpolarization-activated inward rectifying current in guinea pig substantia nigra neurons in vitro. J Neurophysiol, 1999, 74: 2366–2378

    Google Scholar 

  19. Satoh T, Yamada M. A bradycardia agent ZD7288 blocks the hyperpolarization-activated current (I h) in retinal rod photoreceptors. Neuropharmacology, 2000,39:1284–1291

    Article  CAS  Google Scholar 

  20. Ingram S L, Wartenson T J. Opioid inhibition of I h via adenylyl cyclase. Neuron, 1994,13:179–186

    Article  CAS  Google Scholar 

  21. Luo L, Chang L, Brown S M, Ao H, Lee D H, Higuera E S, Dubin A E, Chaplan S R. Role of peripheral hyperpolarization-activated cyclic nucleotide-modulated channel pacemaker channels in acute and chronic pain models in the rat. Neuroscience, 2007,144(4):1477–1485

    Article  CAS  Google Scholar 

  22. Marbán E, Cho H C. Biological pacemakers as a therapy for cardiac arrhythmias. Curr Opin Cardiol, 2008, 23(1): 46–54

    Article  Google Scholar 

  23. Lyashchenko A K, Tibbs G R. Ion binding in the open HCN pacemaker channel pore: Fast mechanisms to shape “slow” channels. J Gen Physiol, 2008, 131(3): 227–243

    Article  CAS  Google Scholar 

  24. Kilb W, Dierkes P W, Syková E, Vargová L, Luhmann H J, Hypoosmolar conditions reduce extracellular volume fraction and enhance epileptiform activity in the CA3 region of the immature rat hippocampus. J Neurosci Res, 2006, 84(1): 119–129

    Article  CAS  Google Scholar 

  25. Nie A F, Meng Z Q. Sulfur dioxide derivative modulation of potassium channels in rat ventricular myocytes. Arch Biochem Biophys, 2005, 442:187–195

    Article  CAS  Google Scholar 

  26. Somjen G G. Ion regulation in the brain: Implications for pathophysiology. Neuroscientist, 2002, 8(3): 254–267

    CAS  Google Scholar 

  27. Benninger C, Kadis J, Prince D A, Extracellular calcium and potassium changes in hippocampal slices. Brain Res, 1980, 187: 165–182

    Article  CAS  Google Scholar 

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  1. Department of Environmental Science, Shanxi University of Finance and Economics, Taiyuan, 030006, China

    ZhengQing Du, WenJie Wu & YuFen Zhou

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  1. ZhengQing Du
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  2. WenJie Wu
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  3. YuFen Zhou
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Correspondence to ZhengQing Du.

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Supported by the University of Science and Technology Foundation of Shanxi Province (Grant No. 200713010)

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Du, Z., Wu, W. & Zhou, Y. The effects of rises in external K+ on the hyperpolarization-activated cation current I h in rat dorsal root ganglion neurons. Sci. China Ser. B-Chem. 52, 1258–1263 (2009). https://doi.org/10.1007/s11426-009-0140-x

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  • DOI: https://doi.org/10.1007/s11426-009-0140-x

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