The roles of id, ia and ik in the electrophysiological functions of smalldiameter rat trigeminal ganglion neurons

Current Molecular Pharmacology

Volumn 3, Issue 1, 2010, Pages 30-36

  Matsumoto, Shigeji ^a   Yoshida, Shinki ^a   Takahashi, Masayuki ^a   Saiki, Chikako ^a   Takeda, Mamoru ^a  

^a NIPPON DENTAL UNIVERSITY   (Japan)

Author keywords

4 aminoprydine; Action potential; Allodynia; Alpha dendorotoxin; Tetraethylammonium; Trigeminal ganglion

Indexed keywords

4 AMINOPRYDINE; ALPHA DENDROTOXIN; DENDROTOXIN; POTASSIUM CHANNEL BLOCKING AGENT; TETRYLAMMONIUM; UNCLASSIFIED DRUG; VOLTAGE GATED POTASSIUM CHANNEL;

ARTICLE; CONCENTRATION (PARAMETERS); DEPOLARIZATION; DOMINANT SUSTAINED POTASSIUM CURRENT; ELECTROPHYSIOLOGY; FAST INACTIVATING TRANSIENT POTASSIUM CURRENT; HUMAN; INFERIOR ALVEOLAR NERVE; INFRAORBITAL NERVE; INHIBITION KINETICS; MEMBRANE STEADY POTENTIAL; NERVE INJURY; NERVE POTENTIAL; NONHUMAN; POTASSIUM CURRENT; PRIORITY JOURNAL; SLOW INACTIVATING TRANSIENT POTASSIUM CURRENT; TRIGEMINUS GANGLION; ACTION POTENTIAL; ANIMAL; METABOLISM; NERVE CELL; PHYSIOLOGY; RAT; REVIEW; SIGNAL TRANSDUCTION;

ACTION POTENTIALS; ANIMALS; ELECTROPHYSIOLOGICAL PHENOMENA; NEURONS; POTASSIUM CHANNEL BLOCKERS; POTASSIUM CHANNELS, VOLTAGE-GATED; RATS; SIGNAL TRANSDUCTION; TRIGEMINAL GANGLION;

EID: 77953442062     PISSN: 18744672     EISSN: 18744702     Source Type: Journal    
DOI: 10.2174/1874467211003010030     Document Type: Article

References (85)

1. Puil, E.; Miura, R. M.; Spigelman, I. Consequences of 4-aminopyridine applications to trigeminal root ganglion neurons. J. Neurophysiol. 1989, 62, 810-820.
2. + currents involves activation of both EP2 and EP4 re-ceptors in neonatal rat nodose ganglion neurones. Br. J. Pharma-col. 2005, 145, 503-513.
3. Matsumoto, S.; Yoshida, S.; Ikeda, M.; Tanimoto, T.; Saiki, C.; Takeda, M.; Shima, Y.; Ohta, H. Effect of 8-bromo-cAMP on the tetrodotoxin-resistant sodium (Nav 1.8) current in small-diameter nodose ganglion neurons. Neuropharmacology 2007, 52, 904-924.
4. + (Nav1.8) currents. The Open Pharmacol. J. 2008, 2, 17-19.
5. Strassman, A. M.; Raymond, S. A. Electrophysiological evidence for tetrodotoxin-resistant sodium channels in slowly conducting dural sensory fibers. J. Neurophysiol. 1999, 81, 413-424.
6. 2+ chelator inhibits spike repolarization in hippocampal neurons. Brain Res. 1987, 435, 387-392.
7. Harper, A. A.; Lawson, S. N. Conduction velocity is related to morphological cell type in rat dorsal root ganglion neurones. J. Physiol., 1985, 359, 31-46.
8. Millan, M.J. The induction of pain: an integrative review. Prog. Neurobiol. 1999, 57, 1-164.
9. Lin, Q.; Peng, Y. B.; Willis, W. D. Role of GABA receptor sub-types in inhibition of primate spinothalamic tract neurons: differ-ence between spinal and periaqueductal gray inhibition. J. Neuro-physiol. 1996, 75, 109-123.
10. Peng, Y. B.; Lin, Q.; Willis, W. D. Effects of GABA and glycine receptor antagonists on the activity and PAG-induced inhibition of rat dorsal horn neurons. Brain Res. 1996, 736, 189-201.
11. Fields, H. L.; Anderson, S. D. Evidence that raphe-spinal neurons mediate opiate and midbrain stimulation-produced analgesias. Pain 1978, 5, 333-349.
12. Alheider A. A.; Lei, S. Z.; Wilcox, G. L. Spinal 5-HT3 receptor-mediated antinociception: possible release of GABA. J. Neurosci. 1991, 11, 1881-1888.
13. + channels by GABA. Trends Neurosci. 1992, 15, 46-51.
14. Takemura, M.; Shimada, T.; Shigenaga, Y. GABA B receptor-mediated effects on expression of c-Fos in rat trigeminal nucleus following highand low-intensity afferent stimulation. Neurosci-ence 2001, 103, 1051-1058.
15. Tanimoto, T.; Takeda, M.; Matsumoto, S. Suppressive effect of vagal afferents on cervical dorsal horn neurons responding to tooth pulp electrical stimulation in the rat. Exp. Brain Res. 2002, 145, 468-479.
16. Ocana, M.; Cendan, C. M.; Cobos, E. J.; Entrena, J. M.; Baeyers, J. M. Potassium channels and pain: present realities and future oppor-tunities. Eur. J. Pharmacol. 2004, 500, 203-219.
17. + channels. Ann. N. Y. Acad. Sci. 1999, 868, 233-285.
18. Kirchhoff, C.; Leah, J. D.; Jung, S.; Reeh, P. W. Excitationof cuta-neous sensory nerve ending in the rat by 4-aminoprydine and tetra-ethlammonium. J. Neurophysiol. 1992, 67, 125-131.
19. Bostock, H.; Sears, T. A.; Sherratt, R. M. The effects of 4-amonoprydine and tetraethylammonium ions on normal and de-myelinated mammalian nerve fibers. J. Physiol. 1981, 313, 310-315.
20. Bowe, C. M.; Kocsis, J. D.; Targ, E. F.; Waxman, S. G. Physio-logical effects of 4-aminoprydine on demyelinated mammalian mo-tor and sensory fibers. Annu. Rev. Neurol. 1987, 22, 264-268.
21. Kitagawa, J.; Takeda, M.; Suzuki, I.; Kadoi, J.; Tsuboi, I.; Honda, K.; Matsumoto, S.; Nakagawa, H.; Tanabe, A.; Iwata, K. Mecha-nisms involved in modulation of trigeminal primary afferent activ-ity in rats with peripheral mononeuropathy. Eur. J. Neurosci. 2006, 24, 1976-1986.
22. Kocsis, J. D.; Bowe, C. M.; Waxman, S. G. Different effects of 4-aminoprydine on sensory and motor fibers: pathogenesis and pares-thesias. Neurology 1986, 36, 117-120.
23. Margeta-Mitrovic, M.; Mitrovic, I.; Riley, R. C.; Jan, L. Y.; Bas-baum, A. I. Immunohistochemical localization of GABAB receptors in the rat central nervous system. J. Comp. Neurol. 1999, 405, 299-321.
24. Mathie, A.; Clarke, C. E.; Ranatunga, K. M.; Veale, E. L. What are the roles of many different types of potassium channel expressed in cerebellar granule cells? Cerebellum 2003, 2, 11-25.
25. Mckeown, L.; Swanton, L.; Robinson, P.; Jones, O. T. Surface expression and distribution of voltage gated potassium channels in neurons. Mol. Memb. Biol. 2008, 25, 332-343.
26. Everill, B.; Rizzo, M. A.; Kocsis, J. D. Morphologically identified cutaneous afferent DRG neurons express three different potassium currents in varying proportions. J. Neurophysiol. 1998, 79, 1814-1824.
27. Everill, B.; Kocsis, J. D. Reduction in potassium currents in identi-fied cutaneous afferent dorsal root ganglion neurons after axotomy. J. Neurophysiol. 1999, 82, 700-708.
28. + currents in adult rat sensory neurons. J. Neuro-physiol. 1996, 75, 2629-2646.
29. Ren, K.; Randich, A.; Gebhart, G. F. Vagal afferent modulation of a nociceptive reflex in rats: involvement of spinal opioid and monoamine receptors. Brain Res. 1988, 446, 285-294.
30. + currents and action potentials in tetrodotoxin-resistant adult rat tri-geminal ganglion neurons. J. Pharmacol. Exp. Ther. 2005, 314, 437-445.
31. + currents on the action potentials in tetrodo-toxin-resistant adult rat trigeminal ganglion neurons. Brain Res. 2007, 1152, 64-74.
32. Takeda, M.; Tanimoto, T.; Ikeda, M.; Kadoi, J.; Matsumoto, S. Activaton of GABAB receptor inhibits the excitability of rat small diameter trigeminal root ganglion neurons. Neuroscience 2004, 123, 491-505.
33. Cardenas, C. G.; Del Mar, L. P.; Scroggs, R. S. Variation in sero-tonergic inhibition of calcium channel currents in four types of rat sensory neurons differentiated by membrane properties. J. Neuro-physiol. 1995, 74, 1870-1879.
34. 2+ dependence in rat trigeminal ganglion cells. J. Neurophysiol., 1996, 75, 1503-1514.
35. + channel subtype 1.4-immunoreactivity of trigeminal ganglion neurons in rats. Eur. J. Pain 2008, 12, 189-195.
36. + currents generates dis-tinct firing patterns in different subtypes of adult mouse trigeminal root ganglion neurones. J. Physiol. 2008, 586, 5101-5118.
37. Dray, A. Inflammatory mediators of pain. Br. J. Anaesth. 1995, 75, 125-131.
38. Glazebrook, P. A.; Ramirez, A. N.; Schild, J. H.; Shieh, C. C.; Doan, T.; Wible, B. A.; Kunze, D. L. Potassium channels Kv1.1, Kv1.2 and Kv1.6 influence excitability of rat visceral sensory neu-rons. J. Physiol. 2002, 541, 467-482.
39. Stansfeld, C.; Feltz, A. title typecontributorDendrotoxin-sensitive K channels in dor-sal root ganglion cells. Neurosci. Lett. 1988, 93, 49-55.
40. Wu, R. L.; Barish, M. Eg. Two pharmacologically and kinetically distinct transient potassium currents in cultured embryonic mouse hippocampal neurons. J. Neurosci. 1992, 12, 2235-2246.
41. Yakel, J. L.; Shao, X. M.; Jackson, M. B. The selectivity of the channel coupled to the 5-HT3 receptor. Brain Res. 1990, 533, 46-52.
42. Seifert, G.; Kuprijanova, E.; Zhou, M.; Steinhäuser, C. Develop-mental changes in the expression of Shakerand Shab-related K(+) channels in neurons of the rat trigeminal ganglion. Brain Res. Mol. Brain Res. 1999, 74, 55-68.
43. Mo, Z. L.; Adamson, C. L.; Davis, R. I. Dendrotoxin-sensitive K(+) currents contribute to accommodation in murine spiral gan-glion neurons. J. Physiol. 2002, 542, 763-778.
44. McFarlane, S.; Cooper, E. Kinetics and voltage dependence of A-type currents on neonatal rat sensory neurons. J. Nurophysiol. 1991, 66, 1380-1391.
45. Fedulova, S. A.; Vasilyev, D. V.; Veselovsky, N. S. Voltage-operated potassium currents in the somatic membrane of rat dorsal root ganglion neurons: ontogenetic aspects. Neuroscience 1998, 85, 497-508.
46. + currents influence firing properties of isolectin B4-positive but not isolectin B4-negative primary sensory neurons. J. Neurophysiol. 2005, 93, 3401-3409.
47. Kashiba, H.; Uchida, Y.; Senba, E. Difference in binding by isolectin B4 to trkA and c-ret mRNA-expressing neurons in rat sen-sory ganglia. Brain Res. Mol. Brain Res. 2001, 95, 18-26.
48. Plenderlieth, M. B.; Snow, P. J. The plant lectin Bandeiraea sim-plicifolia I-B4 identifies a subpopulation of small diameter primary sensory neurones which innervate the skin in the rat. Neurosci. Lett. 1993, 159, 17-20.
49. Rasband, M. N.; Park, E. W.; vanderak, T. W.; Lai, J.; Porreca, F.; Trimmer, J. S. Distinct potassium channels on pain-sensing neu-rons. Proc. Natl. Acad. Sci. USA 2001, 98, 13373-13378.
50. + channels of dorsal root ganglion neurons by the long-duration anesthetic butamben. J. Pharmacol. Exp. Ther. 2005, 314, 1177-1186.
51. Cooper, E. C.; Milroy, A.; Jan, Y. N.; Jan, L.-Y.; Lowenstein, D. H. Presynaptic localization of Kv1.4-containing A-type potassium channels near excitatory synapses in the hippocampus. J. Neurosci. 1998, 18, 965-974.
52. + channel proteins in rat central neurons. Neu-ron 1992, 9, 271-284.
53. Pearce, R. J.; Duchen, M. R. Differential expression of membrane currents in dissociated mouse primary sensory neurons. Neurosci-ence 1994, 63, 1041-1056.
54. Tsutsui, Y.; Ikeda, M.; Takeda, M.; Matsumoto, S. Excitability of small-diameter trigeminal ganglion neurons by 5-HT is mediated by enhancement of the tetrodotoxin-resistant sodium current due to the activation of 5-HT4 receptors and/or by the inhibition of the transient potassium current. Neuroscience 2008, 157, 683-696.
55. Akins, P. T.; McCleskey, E. W. Characterization of potassium currents in adult rat sensory neurons and modulation by opioids and cyclic AMP. Neuroscience 1993, 56, 759-769.
56. Yoshida, S.; Matsuda, Y.; Samejima, A. Tetrodotoxin-resistant sodium and calcium components of action potentials in dorsal root ganglion cells of the adult mouse. J. Neurophysiol. 1978, 41, 1096-1106.
57. Yoshimura, N.; de Groat, W. C. Increasd excitability of afferent neurons innervating rat urinary bladder after chronic bladder in-flammation. J. Neurophysiol. 1999, 19, 4644-4653.
58. Dang, K.; Bielefeldt, K.; Gebhart, G. F. Gastric ulcers reduce A-type potassium currents in rat gastric sensory ganglion neurons. Am. J. Physiol. Gastrointest. Liver. Physiol. 2004, 286, G573-G579.
59. Takeda, M.; Tanimoto, T.; Ikeda, M.; Nasu, M.; Kadoi, J.; Yo-shida, S.; Matsumoto, S. Enhanced excitability of rat trigeminal root ganglion neurons via decrease in A-type potassium currents following temporomandibular joint inflammation. Neuroscience 2006, 138, 621-630.
60. Tanimoto, T.; Takeda, M.; Nasu, M.; Kadoi, J.; Matsumoto, S. Immunohistochemical co-expression of carbonic anhydrase II with Kv1.4 and TRPV1 in rat small-diameter trigeminal ganglion neu-rons. Brain Res. 2005, 1044, 262-265
61. Takeda, M.; Tanimoto, T.; Ito, M.; Nasu, M.; Matsumoto, S. Role of capsaicin-sensitive primary afferent inputs from the masseter muscle in the C1 spinal neurons responding to tooth-pulp stimula-tion in rats. Exp. Brain Res. 2005, 160, 107-117.
62. Takeda, M.; Matsumoto, S. Modulation of Neuronal signal by cross-talk within sensory Ganglia: contribution to pathological pain. Picker, F. L., Ed. Nova Biomedical Books: New York 2008, pp. 115.
63. Laird, J. M.; Bennett, G. J. An electrophysiological study of dorsal horn neurons in the spinal cord of rats with an experimental periph-eral neuropathy. J. Neurophysiol. 1993, 69, 2072-2085.
64. Morales, M.; Wang, S. D. Differential composition of 5-hydroxytryptamine 3 receptors synthesized in the rat CNS and pe-ripheral nervous system. J. Neurosci. 2002, 22, 6732-6741.
65. Derkach, V.; Surprenant, A.; North, R. A. 5-HT3 receptors are membrane ion channels. Nature 1989, 339, 706-709.
66. Hoyer, D.; Matin, G. R. Classification and nomenclature of 5-HT receptors: a comment on current issues. Behav. Brain Res. 1996, 73, 263-268.
67. Cardenas, L. M.; Cardenas, C. G.; Scroggs, R. S. 5HT increases excitability of nociceptor-like rat dorsal root ganglion neurons via cAMP-coupled TTX-resistant Na(+) channels. J. Neurophysiol. 2001, 86, 241-248.
68. Tsuboi, Y.; Takeda, M.; Tanimoto, T.; Ikeda, M.; Matsumoto, S.; Kitagawa, J.; Teramoto, K.; Shimizu, K.; Yamasaki, Y.; Shima, A.; Ren, K.; Iwata, K. Alteration of the second branch of the trigeminal nerve activity following inferior alveolar nerve transection in rats. Pain 2004, 111, 323-334.
69. Tanimoto, T.; Takeda, M.; Nishikawa, T.; Matsumoto, S. The role of 5-hydroxytryptamine 3 receptors in the vagal afferent activation-induced inhibition of the first cervical dorsal horn spinal neurons projected from tooth pulp in the rat. J. Pharmacol. Exp. Ther. 2004, 311, 803-810.
70. Takeda, M.; Tanimoto, T.; Ikeda, M.; Nsau, M.; Kadoi, J.; Shima, Y.; Ohta, H.; Matsumoto, S. Temporomandibular joint inflamma-tion potentiates the excitability of trigeminal root ganglion neurons innervating the facial skin in rats. J. Neurophysiol. 2005, 93, 2723-2738.
71. Bowery, N. G. GABAB receptor pharmacology. Annu. Rev. Phar-macol. Toxicol. 1993, 33, 109-147.
72. Cutrer, F. M.; Moskowitz, M. A. Wolff Award 1996. The actions of valproate and neurosteroids in a model of trigeminal pain. Headache 36, 579-585.
73. Fromm, G. H. Baclofen as an adjuvant analgesic. J. Pain Symptom Manage. 1994, 9, 500-509.
74. Wilson, P. R.; Yaksh, T. L. Baclofen is antinociceptive in the spi-nal intrathecal space of animals. Eur. J. Pharmacol. 1978, 51, 323-330.
75. Kumamoto, E. The pharmacology of amino-acid responses in sep-tal neurons. Prog. Neurobiol. 1997, 52, 197-259.
76. Jackson, M. B.; Konnerth, A.; Augustine, G. J. Action potential broadening and frequency-dependent facilitation of calcium signals in pituitary nerve terminals. Proc. Natl. Acad. Sci. USA 1991, 88, 380-384.
77. Carlton, S. M.; Dougherty, P. M.; Pover, C. M.; Coggeshall, R. E. Neuroma formation and numbers of axons in a rat model of ex-perimental peripheral neuropathy. Neurosci. Lett. 1991, 131, 88-92.
78. Guilbaud, G.; Benoist, J. M.; Jazat, F.; Gautron, M. Neuronal re-sponsiveness in the ventrobasal thalamic complex of rats with an experimental peripheral mononeuropathy. J. Neurophysiol. 1990, 64, 1537-1554.
79. Woolf, C. J.; Max, M. B. Mechanism-based pain diagnosis: issues for analgesic drug development. Anesthesiology 2001, 95, 241-249.
80. Piaso, L.; Li, H. Y.; Park, C. K.; Cho, I. H.; Pino, Z. G.; Jung, S. J.; Choi, S. Y.; Lee, S. J.; Park, K.; Kim, J. S.; Oh, S. B. Mechanosen-sitivity of voltage-gated K+ cuurents in rat trigeminal ganglion neurons. J. Neurosci. Res. 2006, 83, 1373-1380.
81. Bongenhielm, U.; Robinson, P. P. Spontaneous and mechanically evoked afferent activity originating from myelinated fibres in ferret inferior alveolar nerve neuromas. Pain 1996, 67, 399-406.
82. Chudler, E. H.; Anderson, L. C.; Byers, M. R. Trigeminal ganglion neuronal activity and glial fibrillary acidic protein immunoreactiv-ity after inferior alveolar nerve crush in the adult rat. Pain 1997, 73, 141-149.
83. Golowasch J.; Goldman, M. S.; Abbott, L. F.; Marder, E. Failure of averaging in the construction of a conductance-based neuron model. J. Neurophysiol. 2002, 87, 1129-1131.
84. Schulz, D. J.; Goaillard, J. -M.; Marder, E. Quantitative expression of profiling of identified neurons reveals cell-specific constraints on highly variable levels of gene expression. Proc. Natl. Acad. Sci. USA 2007, 104, 13187-131191.
85. Takeda, M.; Tanimoto, T.; Ikeda, M.; Kadoi, J.; Nasu, M.; Matsu-moto, S. Opioidergic modulation of excitability of rat trigeminal root ganglion neuron projections to the spuperficial layer of cervi-cal dorsal horn. Neuroscience 2004, 125, 995-1008.