Acute p38-mediated modulation of tetrodotoxin-resistant sodium channels in mouse sensory neurons by tumor necrosis factor-α

Journal of Neuroscience

Volumn 26, Issue 1, 2006, Pages 246-255

  Jin, Xiaochun ^a   Gereau IV, Robert W ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

DRG; MAPK; Nav1.8; Nociceptor; Pain; Phosphorylation; Sensitization; TNF

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 HYDROXYPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; CYTOKINE; SODIUM CHANNEL; SYNAPTOPHYSIN; TETRODOTOXIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; BRAIN REGION; CONTROLLED STUDY; HYPERSENSITIVITY; MALE; MECHANOTRANSDUCTION; MOUSE; NEUROPATHIC PAIN; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SENSORY NERVE; SODIUM TRANSPORT; SPINAL GANGLION; WILD TYPE;

ANIMALS; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG RESISTANCE; ENZYME INHIBITORS; GANGLIA, SPINAL; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED ICR; MICE, KNOCKOUT; NEURONS, AFFERENT; P38 MITOGEN-ACTIVATED PROTEIN KINASES; SODIUM CHANNELS; TETRODOTOXIN; TUMOR NECROSIS FACTOR-ALPHA;

EID: 30644463076     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3858-05.2006     Document Type: Article

References (73)

1. Bhave G, Gereau RW (2004) Posttranslational mechanisms of peripheral sensitization. J Neurobiol 61:88-106.
2. Cardenas CG, Del Mar LP, Scroggs RS (1995) Variation in serotonergic inhibition of calcium channel currents in four types of rat sensory neurons differentiated by membrane properties. J Neurophysiol 74:1870-1879.
3. Cardenas CG, Del Mar LP, Cooper BY, Scroggs R (1997) 5-HT4 receptors couple positively to tetrodotoxin-insensitive sodium channels in a subpopulation of capsaicin-sensitive rat sensory neurons. J Neurosci 17:7181-7189.
4. Cardenas CG, Mar LP, Vysokanov AV, Arnold PB, Cardenas LM, Surmeier DJ, Scroggs RS (1999) Serotonergic modulation of hyperpolarizationactivated current in acutely isolated rat dorsal root ganglion neurons. J Physiol (Lond) 518:507-523.
5. + channels. J Neurophysiol 86:241-248.
6. Cunha FQ, Poole S, Lorenzetti BB, Ferreira SH (1992) The pivotal role of tumour necrosis factor alpha in the development of inflammatory hyperalgesia. Br J Pharmacol 107:660-664.
7. Cunha TM, Verri Jr WA, Silva JS, Poole S, Cunha FQ, Ferreira SH (2005) A cascade of cytokines mediates mechanical inflammatory hypernociception in mice. Proc Natl Acad Sci USA 102:1755-1760.
8. Diem R, Meyer R, Weishaupt JH, Bahr M (2001) Reduction of potassium currents and phosphatidylinositol 3-kinase-dependent AKT phosphorylation by tumor necrosis factor-α rescues axotomized retinal ganglion cells from retrograde cell death in vivo. J Neurosci 21:2058-2066.
9. Erickson SL, de Sauvage FJ, Kikly K, Carver-Moore K, Pitts-Meek S, Gillett N, Sheehan KCF, Schreiber RD, Goeddel DV, Moore MW (1994) Decreased sensitivity to tumour-necrosis factor but normal T-cell development in TNF receptor-2-deficient mice. Nature 372:560-563.
10. Furukawa K, Mattson MP (1998) The transcription factor NF-kappaB mediates increases in calcium currents and decreases in NMDA- and AMPA/ kainate-induced currents induced by tumor necrosis factor-alpha in hippocampal neurons. J Neurochem 70:1876-1886.
11. Goldblatt F, Isenberg DA (2005) New therapies for rheumatoid arthritis. Clin Exp Immunol 140:195-204.
12. Hanauer SB (2004) Efficacy and safety of tumor necrosis factor antagonists in Crohn's disease: overview of randomized clinical studies. Rev Gastroenterol Disord 4 [Suppl 3]:S18-S24.
13. Homma Y, Brull SJ, Zhang JM (2002) A comparison of chronic pain behavior following local application of tumor necrosis factor alpha to the normal and mechanically compressed lumbar ganglia in the rat. Pain 95:239-246.
14. Hu HJ, Bhave G, Gereau RW (2002) Prostaglandin and protein kinase A-dependent modulation of vanilloid receptor function by metabotropic glutamate receptor 5: potential mechanism for thermal hyperalgesia. J Neurosci 22:7444-7452.
15. Inglis JJ, Nissim A, Lees DM, Hunt SP, Chernajovsky Y, Kidd BL (2005) The differential contribution of tumour necrosis factor to thermal and mechanical hyperalgesia during chronic inflammation. Arthritis Res Ther 7:R807-R816.
16. Inoue K, Tsuda M, Koizumi S (2004) Chronic pain and microglia: the role of ATP. Novartis Found Symp 261:55-64; discussion 64-67, 149-154.
17. Ji RR (2004) Mitogen-activated protein kinases as potential targets for pain killers. Curr Opin Investig Drugs 5:71-75.
18. Ji RR, Strichartz G (2004) Cell signaling and the genesis of neuropathic pain. Sci STKE 2004:reE14.
19. Ji RR, Samad TA, Jin SX, Schmoll R, Woolf CJ (2002) p38 MAPK activation by NGF in primary sensory neurons after inflammation increases TRPV1 levels and maintains heat hyperalgesia. Neuron 36:57-68.
20. Jin SX, Zhuang ZY, Woolf CJ, Ji RR (2003) p38 mitogen-activated protein kinase is activated after a spinal nerve ligation in spinal cord microglia and dorsal root ganglion neurons and contributes to the generation of neuropathic pain. J Neurosci 23:4017-4022.
21. Joseph EK, Levine JD (2004) Caspase signalling in neuropathic and inflammatory pain in the rat. Eur J Neurosci 20:2896-2902.
22. Junger H, Sorkin LS (2000) Nociceptive and inflammatory effects of subcutaneous TNFalpha. Pain 85:145-151.
23. Kagan BL, Baldwin RL, Munoz D, Wisnieski BJ (1992) Formation of ion-permeable channels by tumor necrosis factor-alpha. Science 255:1427-1430.
24. Kim SY, Bae JC, Kim JY, Lee HL, Lee KM, Kim DS, Cho HJ (2002) Activation of p38 MAP kinase in the rat dorsal root ganglia and spinal cord following peripheral inflammation and nerve injury. NeuroReport 13:2483-2486.
25. Lee JC, Laydon JT, McDonnell PC, Gallagher TF, Kumar S, Green D, McNulty D, Blumenthal MJ, Keys JR, Landvatter SW, Strickler JE, McLaughlin MM, Siemens IR, Fisher SM, Livi GP, White JR, Adams JL, Young PR (1994) A protein kinase involved in the regulation of inflammatory cytokine biosynthesis. Nature 372:739-746.
26. Li Y, Ji A, Weihe E, Schafer MK (2004) Cell-specific expression and lipopolysaccharide-induced regulation of tumor necrosis factor α (TNFα) and TNF receptors in rat dorsal root ganglion. J Neurosci 24:9623-9631.
27. Lindenlaub T, Teuteberg P, Hartung T, Sommer C (2000) Effects of neutralizing antibodies to TNF-alpha on pain-related behavior and nerve regeneration in mice with chronic constriction injury. Brain Res 866:15-22.
28. Liu B, Li H, Brull SJ, Zhang JM (2002) Increased sensitivity of sensory neurons to tumor necrosis factor alpha in rats with chronic compression of the lumbar ganglia. J Neurophysiol 88:1393-1399.
29. Milligan ED, Twining C, Chacur M, Biedenkapp J, O'Connor K, Poole S, Tracey K, Martin D, Maier SF, Watkins LR (2003) Spinal glia and proinflammatory cytokines mediate mirror-image neuropathic pain in rats. J Neurosci 23:1026-1040.
30. Mizushima T, Obata K, Yamanaka H, Dai Y, Fukuoka T, Tokunaga A, Mashimo T, Noguchi K (2005) Activation of p38 MAPK in primary afferent neurons by noxious stimulation and its involvement in the development of thermal hyperalgesia. Pain 113:51-60.
31. Nicol GD, Lopshire JC, Pafford CM (1997) Tumor necrosis factor enhances the capsaicin sensitivity of rat sensory neurons. J Neurosci 17:975-982.
32. Obata K, Yamanaka H, Dai Y, Mizushima T, Fukuoka T, Tokunaga A, Noguchi K (2004a) Differential activation of MAPK in injured and uninjured DRG neurons following chronic constriction injury of the sciatic nerve in rats. Eur J Neurosci 20:2881-2895.
33. Obata K, Yamanaka H, Kobayashi K, Dai Y, Mizushima T, Katsura H, Fukuoka T, Tokunaga A, Noguchi K (2004b) Role of mitogen-activated protein kinase activation in injured and intact primary afferent neurons for mechanical and heat hypersensitivity after spinal nerve ligation. J Neurosci 24:10211-10222.
34. Opree A, Kress M (2000) Involvement of the proinflammatory cytokines tumor necrosis factor-α, IL-1β, and IL-6 but not IL-8 in the development of heat hyperalgesia: effects on heat-evoked calcitonin gene-related peptide release from rat skin. J Neurosci 20:6289-6293.
35. Parada CA, Yeh JJ, Joseph EK, Levine JD (2003) Tumor necrosis factor receptor type-1 in sensory neurons contributes to induction of chronic enhancement of inflammatory hyperalgesia in rat. Eur J Neurosci 17:1847-1852.
36. Perkins MN, Kelly D (1994) Interleukin-1 beta induced-desArg9bradykinin- mediated thermal hyperalgesia in the rat. Neuropharmacology 33:657-660.
37. Pfeffer K, Matsuyama T, Kundig TM, Wakeham A, Kishihara K, Shahinian A, Wiegmann K, Ohashi PS, Kronke M, Mak TW (1993) Mice deficient for the 55 kd tumor necrosis factor receptor are resistant to endotoxic shock, yet succumb to L. monocytogenes infection. Cell 73:457-467.
38. 2+ mobilisation and stress kinases in cultured sensory neurones. Neuropharmacology 42:93-106.
39. Ribeiro RA, Vale ML, Thomazzi SM, Paschoalato ABP, Poole S, Ferreira SH, Cunha FQ (2000) Involvement of resident macrophages and mast cells in the writhing nociceptive response induced by zymosan and acetic acid in mice. Eur J Pharmacol 387:111-118.
40. Schafers M, Geis C, Brors D, Yaksh TL, Sommer C (2002) Anterograde transport of tumor necrosis factor-alpha in the intact and injured rat sciatic nerve. J Neurosci 22:536-545.
41. Schafers M, Sorkin LS, Geis C, Shubayev VI (2003a) Spinal nerve ligation induces transient upregulation of tumor necrosis factor receptors 1 and 2 in injured and adjacent uninjured dorsal root ganglia in the rat. Neurosci Lett 347:179-182.
42. Schafers M, Svensson CI, Sommer C, Sorkin LS (2003b) Tumor necrosis factor-α induces mechanical allodynia after spinal nerve ligation by activation of p38 MAPK in primary sensory neurons. J Neurosci 23:2517-2521.
43. Schafers M, Lee DH, Brors D, Yaksh TL, Sorkin LS (2003c) Increased sensitivity of injured and adjacent uninjured rat primary sensory neurons to exogenous tumor necrosis factor-α after spinal nerve ligation. J Neurosci 23:3028-3038.
44. Sharrocks AD, Yang SH, Galanis A (2000) Docking domains and substrate-specificity determination for MAP kinases. Trends Biochem Sci 25:448-453.
45. Shubayev VI, Myers RR (2001) Axonal transport of TNF-alpha in painful neuropathy: distribution of ligand tracer and TNF receptors. J Neuroimmunol 114:48-56.
46. 2+ currents in cultured sympathetic neurons. J Neurosci 12:2665-2671.
47. Sommer C, Kress M (2004) Recent findings on how proinflammatory cytokines cause pain: peripheral mechanisms in inflammatory and neuropathic hyperalgesia. Neurosci Lett 361:184-187.
48. Sommer C, Schmidt C, George A (1998) Hyperalgesia in experimental neuropathy is dependent on the TNF receptor 1. Exp Neurol 151:138-142.
49. Sommer C, Lindenlaub T, Teuteberg P, Schafers M, Hartung T, Toyka KV (2001) Anti-TNF-neutralizing antibodies reduce pain-related behavior in two different mouse models of painful mononeuropathy. Brain Res 913:86-89.
50. Sorkin LS, Doom CM (2000) Epineurial application of TNF elicits an acute mechanical hyperalgesia in the awake rat. J Peripher Nerv Syst 5:96-100.
51. Sorkin LS, Xiao WH, Wagner R, Myers RR (1997) Tumour necrosis factor-alpha induces ectopic activity in nociceptive primary afferent fibres. Neuroscience 81:255-262.
52. Souslova VA, Fox M, Wood JN, Akopian AN (1997) Cloning and characterization of a mouse sensory neuron tetrodotoxin-resistant voltage-gated sodium channel gene, Scn10a. Genomics 41:201-209.
53. Svensson CI, Hua XY, Protter AA, Powell HC, Yaksh TL (2003a) Spinal p38 MAP kinase is necessary for NMDA-induced spinal PGE(2) release and thermal hyperalgesia. NeuroReport 14:1153-1157.
54. Svensson CI, Marsala M, Westerlund A, Calcutt NA, Campana WM, Freshwater JD, Catalano R, Feng Y, Protter AA, Scott B, Yaksh TL (2003b) Activation of p38 mitogen-activated protein kinase in spinal microglia is a critical link in inflammation-induced spinal pain processing. J Neurochem 86:1534-1544.
55. Svensson CI, Schafers M, Jones TL, Powell H, Sorkin LS (2005a) Spinal blockade of TNF blocks spinal nerve ligation-induced increases in spinal P-p38. Neurosci Lett 379:209-213.
56. Svensson CI, Fitzsimmons B, Azizi S, Powell HC, Hua XY, Yaksh TL (2005b) Spinal p38beta isoform mediates tissue injury-induced hyperalgesia and spinal sensitization. J Neurochem 92:1508-1520.
57. Sweitzer S, Martin D, DeLeo JA (2001) Intrathecal interleukin-1 receptor antagonist in combination with soluble tumor necrosis factor receptor exhibits an anti-allodynic action in a rat model of neuropathic pain. Neuroscience 103:529-539.
58. Sweitzer SM, Medicherla S, Almirez R, Dugar S, Chakravarty S, Shumilla JA, Yeomans DC, Protter AA (2004a) Antinociceptive action of a p38alpha MAPK inhibitor, SD-282, in a diabetic neuropathy model. Pain 109:409-419.
59. Sweitzer SM, Peters MC, Ma JY, Kerr I, Mangadu R, Chakravarty S, Dugar S, Medicherla S, Protter AA, Yeomans DC (2004b) Peripheral and central p38 MAPK mediates capsaicin-induced hyperalgesia. Pain 111:278-285.
60. Tchelingerian JL, Quinonero J, Booss J, Jacque C (1993) Localization of TNF alpha and IL-1 alpha immunoreactivities in striatal neurons after surgical injury to the hippocampus. Neuron 10:213-224.
61. Toussirot E, Wendling D (2004) The use of TNF-alpha blocking agents in rheumatoid arthritis: an overview. Expert Opin Pharmacother 5:581-594.
62. Tsuda M, Inoue K, Salter MW (2005) Neuropathic pain and spinal microglia: a big problem from molecules in "small" glia. Trends Neurosci 28:101-107.
63. Wacnik PW, Eikmeier LJ, Simone DA, Wilcox GL, Beitz AJ (2005) Nociceptive characteristics of tumor necrosis factor-alpha in naive and tumor-bearing mice. Neuroscience 132:479-491.
64. Wagner R, Myers RR (1996) Endoneurial injection of TNF-alpha produces neuropathic pain behaviors. NeuroReport 7:2897-2901.
65. Wagner R, Janjigian M, Myers RR (1998) Anti-inflammatory interleukin-10 therapy in CCI neuropathy decreases thermal hyperalgesia, macrophage recruitment, and endoneurial TNF-alpha expression. Pain 74:35-42.
66. Wendling D, Toussirot E (2004) Anti-TNF-alpha therapy in ankylosing spondylitis. Expert Opin Pharmacother 5:1497-1507.
67. Wittmack EK, Rush AM, Hudmon A, Waxman SG, Dib-Hajj SD (2005) Voltage-gated sodium channel Nav1.6 is modulated by p38 mitogen-activated protein kinase. J Neurosci 25:6621-6630.
68. Wood JN, Boorman JP, Okuse K, Baker MD (2004a) Voltage-gated sodium channels and pain pathways. J Neurobiol 61:55-71.
69. Wood JN, Abrahamsen B, Baker MD, Boorman JD, Donier E, Drew LJ, Nassar MA, Okuse K, Seereeram A, Stirling CL, Zhao J (2004b) Ion channel activities implicated in pathological pain. Novartis Found Symp 261:32-40, discussion 40-54.
70. Woolf CJ, Allchorne A, Safieh-Garabedian B, Poole S (1997) Cytokines, nerve growth factor and inflammatory hyperalgesia: the contribution of tumour necrosis factor alpha. Br J Pharmacol 121:417-424.
71. Wu H (2004) Assembly of post-receptor signaling complexes for the tumor necrosis factor receptor superfamily. Adv Protein Chem 68:225-279.
72. Yang D, Gereau RW (2004) Group II metabotropic glutamate receptors inhibit cAMP-dependent protein kinase-mediated enhancement of tetrodotoxin-resistant sodium currents in mouse dorsal root ganglion neurons. Neurosci Lett 357:159-162.
73. Zhang JM, Li H, Liu B, Brull SJ (2002) Acute topical application of tumor necrosis factor alpha evokes protein kinase A-dependent responses in rat sensory neurons. J Neurophysiol 88:1387-1392.