Local inflammation in rat dorsal root ganglion alters excitability and ion currents in small-diameter sensory neurons

Anesthesiology

Volumn 107, Issue 2, 2007, Pages 322-332

  Wang, Jun Gang ^a   Strong, Judith A ^a   Xie, Wenrui ^a   Zhang, Jun Ming ^a,b  

^a Pain Research Center   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TETRODOTOXIN;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ISOLATION; CONTROLLED STUDY; DISEASE MODEL; EXCITABILITY; FEMALE; INFLAMMATION; ION CURRENT; NERVE INJURY; NONHUMAN; PAIN THRESHOLD; PATCH CLAMP; POTASSIUM CURRENT; PRIORITY JOURNAL; RAT; SENSORY NERVE CELL; SODIUM CURRENT; SPINAL GANGLION; WHOLE CELL;

ACTION POTENTIALS; ANESTHETICS, LOCAL; ANIMALS; CELLS, CULTURED; DISEASE MODELS, ANIMAL; ELECTRIC CONDUCTIVITY; ELECTROPHYSIOLOGY; FEMALE; GANGLIA, SPINAL; INFLAMMATION; ION CHANNEL GATING; MEMBRANE POTENTIALS; NEURAL CONDUCTION; NEURONS, AFFERENT; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNELS, VOLTAGE-GATED; RATS; RATS, SPRAGUE-DAWLEY; SODIUM CHANNELS; TETRODOTOXIN;

EID: 34547566548     PISSN: 00033022     EISSN: 15281175     Source Type: Journal    
DOI: 10.1097/01.anes.0000270761.99469.a7     Document Type: Article

References (60)

1. Scholz J, Woolf CJ: Can we conquer pain? Nat Neurosci 2002; 5 (suppl): 1062-7
2. Abdulla FA, Smith PA: Axotomy- and autotomy-induced changes in Ca2+ and K+ channel currents of rat dorsal root ganglion neurons. J Neurophysiol 2001; 85:644-58
3. Kim YI, Na HS, Kim SH, Han HC, Yoon YW, Sung B, Nam HJ, Shin SL, Hong SK: Cell type-specific changes of the membrane properties of peripherallyaxotomized dorsal root ganglion neurons in a rat model of neuropathic pain. Neuroscience 1998; 86:301-9
4. Moore BA, Stewart TM, Hill C, Vanner SJ: TNBS ileitis evokes hyperexcitability and changes in ionic membrane properties of nociceptive DRG neurons. Am J Physiol Gastrointest Liver Physiol 2002; 282:G1045-51
5. Song XJ, Zhang J-M, Hu SJ, LaMotte RH: Somata of nerve-injured sensory neurons exhibit enhanced responses to inflammatory mediators. Pain 2003; 104:701-9
6. Zhang J-M, Song XJ, LaMotte RH: Enhanced excitability of sensory neurons in rats with cutaneous hyperalgesia produced by chronic compression of the dorsal root ganglion. J Neurophysiol 1999; 82:3359-66
7. Millan MJ: The induction of pain: An integrative review. Prog Neurobiol 1999; 57:1-164
8. Waxman SG, Cummins TR, Dib-Hajj S, Fjell J, Black JA: Sodium channels, excitability of primary sensory neurons, and the molecular basis of pain. Muscle Nerve 1999; 22:1177-87
9. Takeda M, Tanimoto T, Ikeda M, Nasu M, Kadoi J, Yoshida S, Matsumoto S: Enhanced excitability of rat trigeminal root ganglion neurons via decrease in A-type potassium currents following temporomandibular joint inflammation. Neuroscience 2006; 138:621-30
10. Dang K, Bielefeldt K, Gebhart GF: Gastric ulcers reduce A-type potassium currents in rat gastric sensory ganglion neurons. Am J Physiol Gastrointest Liver Physiol 2004; 286:G573-9
11. Yoshimura N, de Groat WC: Increased excitability of afferent neurons innervating rat urinary bladder after chronic bladder inflammation. J Neurosci 1999; 19:4644-53
12. Yang EK, Takimoto K, Hayashi Y, de Groat WC, Yoshimura N: Altered expression of potassium channel subunit mRNA and alpha-dendrotoxin sensitivity of potassium currents in rat dorsal root ganglion neurons after axotomy. Neuroscience 2004; 123:867-74
13. Harriott AM, Dessem D, Gold MS: Inflammation increases the excitability of masseter muscle afferents. Neuroscience 2006; 141:433-42
14. Xu GY, Winston JH, Shenoy M, Yin H, Pasricha PJ: Enhanced excitability and suppression of A-type K+ current of pancreas-specific afferent neurons in a rat model of chronic pancreatitis. Am J Physiol Gastrointest Liver Physiol 2006; 291:G424-31
15. Stewart T, Beyak MJ, Vanner S: Ileitis modulates potassium and sodium currents in guinea pig dorsal root ganglia sensory neurons. J Physiol 2003; 552:797-807
16. Taskinen HS, Roytta M: Increased expression of chemokines (MCP-1, MIP-1alpha, RANTES) after peripheral nerve transection. J Peripher Nerv Syst 2000; 5:75-81
17. Tanaka T, Minami M, Nakagawa T, Satoh M: Enhanced production of monocyte chemoattractant protein-1 in the dorsal root ganglia in a rat model of neuropathic pain: Possible involvement in the development of neuropathic pain. Neurosci Res 2004; 48:463-9
18. Kleinschnitz C, Brinkhoff J, Zelenka M, Sommer C, Stoll G: The extent of cytokine induction in peripheral nerve lesions depends on the mode of injury and NMDA receptor signaling. J Neuroimmunol 2004; 149:77-83
19. Ji RR, Strichartz G: Cell signaling and the genesis of neuropathic pain. Sci STKE 2004; (252):reE14
20. Marchand F, Perretti M, McMahon SB: Role of the immune system in chronic pain. Nat Rev Neurosci 2005; 6:521-32
21. Moalem G, Tracey DJ: Immune and inflammatory mechanisms in neuropathic pain. Brain Res Brain Res Rev 2006; 51:240-64
22. Xie WR, Deng H, Li H, Bowen TL, Strong JA, Zhang J-M: Robust increase of cutaneous sensitivity, cytokine production and sympathetic sprouting in rats with localized inflammatory irritation of the spinal ganglia. Neuroscience 2006; 142:809-22
23. Kawaguchi S, Yamashita T, Yokogushi K, Murakami T, Ohwada O, Sato N: Immunophenotypic analysis of the inflammatory infiltrates in herniated intervertebral discs. Spine 2001; 26:1209-14
24. Satoh K, Konno S, Nishiyama K, Olmarker K, Kikuchi S: Presence and distribution of antigen-antibody complexes in the herniated nucleus pulposus. Spine 1999; 24:1980-4
25. Zhang J-M, Homma Y, Ackerman WE, Brull SJ: Topical application of acidic bupivacaine to the lumbar ganglion induces mechanical hyperalgesia in the rat. Anesth Analg 2001; 93:466-471
26. Anderson P, Storm J, Wheal HV: Thresholds of action potentials evoked by synapses on the dendrites of pyramidal cells in the rat hippocampus in vitro. J Physiol (Lond) 1987; 383:509-26
27. Yu K, Kocsis JD: Schwann cell engraftment into injured peripheral nerve prevents changes in action potential properties. J Neurophysiol 2005; 94:1519-27
28. Zhang J-M, Donnelly DF, Song XJ, Lamotte RH: Axotomy increases the excitability of dorsal root ganglion cells with unmyelinated axons. J Neurophysiol 1997; 78:2790-4
29. Tan ZY, Donnelly DF, LaMotte RH: Effects of a chronic compression of the dorsal root ganglion on voltage-gated Na+ and K+ currents in cutaneous afferent neurons. J Neurophysiol 2006; 95:1115-23
30. Fjell J, Cummins TR, Dib-Hajj SD, Fried K, Black JA, Waxman SG: Differential role of GDNF and NGF in the maintenance of two TTX-resistant sodium channels in adult DRG neurons. Brain Res Mol Brain Res 1999; 67:267-82
31. Rush AM, Craner MJ, Kageyama T, Dib-Hajj SD, Waxman SG, Ranscht B: Contactin regulates the current density and axonal expression of tetrodotoxin-resistant but not tetrodotoxin-sensitive sodium channels in DRG neurons. Eur J Neurosci 2005; 22:39-49
32. Wu ZZ, Pan HL: Tetrodotoxin-sensitive and -resistant Na+ channel currents in subsets of small sensory neurons of rats. Brain Res 2004; 1029:251-8
33. Ogata N, Ohishi Y: Molecular diversity of structure and function of the voltage-gated Na+ channels. Jpn J Pharmacol 2002; 88:365-77
34. Amaya F, Decosterd I, Samad TA, Plumpton C, Tate S, Mannion RJ, Costigan M, Woolf CJ: Diversity of expression of the sensory neuron-specific TTX-resistant voltage-gated sodium ion channels SNS and SNS2. Mol Cell Neurosci 2000; 15:331-42
35. Devor M: Response of nerves to injury in relation to neuropathic pain, Textbook of Pain, 5th edition. Edited by McMahon SB, Koltzenburg M. Philadelphia, Churchill Livingstone, Elsevier, 2006, pp 905-27
36. Schild JH, Kunze DL: Experimental and modeling study of Na+ current heterogeneity in rat nodose neurons and its impact on neuronal discharge. J Neurophysiol 1997; 78:3198-209
37. Krause JE, Chenard BL, Cortright DN: Transient receptor potential ion channels as targets for the discovery of pain therapeutics. Curr Opin Investig Drugs 2005; 6:48-57
38. Chaplan SR, Guo HQ, Lee DH, Luo L, Liu C, Kuei C, Velumian AA, Butler MP, Brown SM, Dubin AE: Neuronal hyperpolarization-activated pacemaker channels drive neuropathic pain. J Neurosci 2003; 23:1169-78
39. Cao YQ: Voltage-gated calcium channels and pain. Pain 2006; 126:5-9
40. Cummins TR, Waxman SG: Downregulation of tetrodotoxin-resistant sodium currents and upregulation of a rapidly repriming tetrodotoxin-sensitive sodium current in small spinal sensory neurons after nerve injury. J Neurosci 1997; 17:3503-14
41. Roy ML, Narahashi T: Differential properties of tetrodotoxin-sensitive and tetrodotoxin-resistant sodium channels in rat dorsal root ganglion neurons. J Neurosci 1992; 12:2104-11
42. Caffrey JM, Eng DL, Black JA, Waxman SG, Kocsis JD: Three types of sodium channels in adult rat dorsal root ganglion neurons. Brain Res 1992; 592:283-97
43. Elliott AA, Elliott JR: Characterization of TTX-sensitive and TTX-resistant sodium currents in small cells from adult rat dorsal root ganglia. J Physiol (Lond) 1993; 463:39-56
44. Cummins TR, Dib-Hajj SD, Black JA, Akopian AN, Wood JN, Waxman SG: A novel persistent tetrodotoxin-resistant sodium current in SNS-null and wild-type small primary sensory neurons. J Neurosci 1999; 19:RC43 (41-6)
45. Coste B, Osorio N, Padilla F, Crest M, Delmas P: Gating and modulation of presumptive NaV1.9 channels in enteric and spinal sensory neurons. Mol Cell Neurosci 2004; 26:123-34
46. Maruyama H, Yamamoto M, Matsutomi T, Zheng T, Nakata Y, Wood JN, Ogata N: Electrophysiological characterization of the tetrodotoxin-resistant Na+ channel, Na (v) 1.9, in mouse dorsal root ganglion neurons. Pflugers Arch 2004; 449:76-87
47. Rogers M, Tang L, Madge DJ, Stevens EB: The role of sodium channels in neuropathic pain. Semin Cell Dev Biol 2006; 17:571-81
48. Tanaka M, Cummins TR, Ishikawa K, Dib-Hajj SD, Black JA, Waxman SG: SNS Na+ channel expression increases in dorsal root ganglion neurons in the carrageenan inflammatory pain model. Neuroreport 1998; 9:967-72
49. Black JA, Liu S, Tanaka M, Cummins TR, Waxman SG: Changes in the expression of tetrodotoxin-sensitive sodium channels within dorsal root ganglia neurons in inflammatory pain. Pain 2004; 108:237-47
50. Beyak MJ, Ramji N, Krol KM, Kawaja MD, Vanner SJ: Two TTX-resistant Na+ currents in mouse colonic dorsal root ganglia neurons and their role in colitis-induced hyperexcitability. Am J Physiol Gastrointest Liver Physiol 2004; 287:G845-55
51. Bielefeldt K, Ozaki N, Gebhart GF: Mild gastritis alters voltage-sensitive sodium currents in gastric sensory neurons in rats. Gastroenterology 2002; 122:752-61
52. Molliver DC, Snider WD: Nerve growth factor receptor TrkA is down-regulated during postnatal development by a subset of dorsal root ganglion neurons. J Comp Neurol 1997; 381:428-38
53. Everill B, Rizzo MA, Kocsis JD: Morphologically identified cutaneous afferent DRG neurons express three different potassium currents in varying proportions. J Neurophysiol 1998; 79:1814-24
54. Akins PT, McCleskey EW: Characterization of potassium currents in adult rat sensory neurons and modulation by opioids and cyclic AMP. Neuroscience 1993; 56:759-69
55. Takeda M, Tanimoto T, Ikeda M, Kadoi J, Matsumoto S: Activation of GABAB receptor inhibits the excitability of rat small diameter trigeminal root ganglion neurons. Neuroscience 2004; 123:491-505
56. Yoshida S, Matsumoto S: Effects of alpha-dendrotoxin on K+ currents and action potentials in tetrodotoxin-resistant adult rat trigeminal ganglion neurons. J Pharmacol Exp Ther 2005; 314:437-45
57. Gold MS, Shuster MJ, Levine JD: Characterization of six voltage-gated K+ currents in adult rat sensory neurons. J Neurophysiol 1996; 75:2629-46
58. Mongan LC, Hill MJ, Chen MX, Tate SN, Collins SD, Buckby L, Grubb BD: The distribution of small and intermediate conductance calcium-activated potassium channels in the rat sensory nervous system. Neuroscience 2005; 131:161-75
59. Marder E, Prinz AA: Modeling stability in neuron and network function: The role of activity in homeostasis. Bioessays 2002; 24:1145-54
60. Liu L, Yang TM, Liedtke W, Simon SA: Chronic IL-1beta signaling potentiates voltage-dependent sodium currents in trigeminal nociceptive neurons. J Neurophysiol 2006; 95:1478-90