Activation of p38 MAPK in primary afferent neurons by noxious stimulation and its involvement in the development of thermal hyperalgesia

Pain

Volumn 113, Issue 1-2, 2005, Pages 51-60

  Mizushima, Toshiyuki ^a,b   Obata, Koichi ^a   Yamanaka, Hiroki ^a   Dai, Yi ^a   Fukuoka, Tetsuo ^a   Tokunaga, Atsushi ^a   Mashimo, Takashi ^b   Noguchi, Koichi ^a  

^a HYOGO COLLEGE OF MEDICINE   (Japan)

^b OSAKA UNIVERSITY MEDICAL SCHOOL   (Japan)

Author keywords

Capsaicin; Dorsal root ganglion; ERK; p38; Thermal stimuli; TRPV1

Indexed keywords

1 [7 (4 FLUOROPHENYL) 1,2,3,4 TETRAHYDRO 8 (4 PYRIDYL)PYRAZOLO[5,1 C][1,2,4]TRIAZIN 2 YL] 2 PHENYLETHANEDIONE; CAPSAICIN; ION CHANNEL; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; HYPERALGESIA; IMMUNOREACTIVITY; MALE; MUSCLE SPINDLE AFFERENT NERVE; NOCICEPTIVE STIMULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; SPINAL GANGLION; THERMAL STIMULATION;

ANIMALS; CAPSAICIN; CELL COUNT; DOSE-RESPONSE RELATIONSHIP, DRUG; DOSE-RESPONSE RELATIONSHIP, RADIATION; DRUG INTERACTIONS; ENZYME ACTIVATION; GANGLIA, SPINAL; HEAT; HYPERALGESIA; IMMUNOHISTOCHEMISTRY; ION CHANNELS; MALE; MITOGEN-ACTIVATED PROTEIN KINASE 6; NEUROFILAMENT PROTEINS; NEURONS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PAIN MEASUREMENT; PYRAZOLES; PYRIDINES; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS; TRPV CATION CHANNELS;

EID: 11144338758     PISSN: 03043959     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pain.2004.09.038     Document Type: Article

References (71)

1. K.O. Aley, A. Martin, T. McMahon, J. Mok, J.D. Levine, and R.O. Messing Nociceptor sensitization by extracellular signal-regulated kinases J Neurosci 21 2001 6933 6939
2. F. Amaya, I. Decosterd, T.A. Samad, C. Plumpton, S. Tate, R.J. Mannion, M. Costigan, and C.J. Woolf Diversity of expression of the sensory neuron-specific TTX-resistant voltage-gated sodium ion channels SNS and SNS2 Mol Cell Neurosci 15 2000 331 342
3. C.M. Atkins, J.C. Selcher, J.J. Petraitis, J.M. Trzaskos, and J.D. Sweatt The MAPK cascade is required for mammalian associative learning Nat Neurosci 1 1998 602 609
4. S. Averill, J.D. Delcroix, G.J. Michael, D.R. Tomlinson, P. Fernyhough, and J.V. Priestley Nerve growth factor modulates the activation status and fast axonal transport of erk 1/2 in adult nociceptive neurones Mol Cell Neurosci 18 2001 183 196
5. J. Baraban, R.S. Fiore, J.S. Sanghera, H.B. Paddon, and S.L. Pelech Identification of p42 mitogen-activated protein kinase as a tyrosine kinase substrate activated by maximal electroconvulsive shock in hippocampus J Neurochem 60 1993 330 336
6. D.L. Bennett, G.J. Michael, N. Ramachandran, J.B. Munson, S. Averill, Q. Yan, S.B. McMahon, and J.V. Priestley A distinct subgroup of small DRG cells express GDNF receptor components and GDNF is protective for these neurons after nerve injury J Neurosci 18 1998 3059 3072
7. V.Y. Bolshakov, L. Carboni, M.H. Cobb, S.A. Siegelbaum, F. Belardetti, and Dual MAP kinase pathways mediate opposing forms of long-term plasticity at CA3-CA1 synapses Nat Neurosci 3 2000 1107 1112
8. M.J. Caterina, M.A. Schumacher, M. Tominaga, T.A. Rosen, J.D. Levine, and D. Julius The capsaicin receptor: a heat-activated ion channel in the pain pathway Nature 389 1997 816 824
9. M.J. Caterina, A. Leffler, A.B. Malmberg, W.J. Martin, J. Trafton, K.R. Petersen-Zeitz, M. Koltzenburg, A.I. Basbaum, and D. Julius Impaired nociception and pain sensation in mice lacking the capsaicin receptor Science 288 2000 306 313
10. Y. Dai, K. Iwata, T. Fukuoka, E. Kondo, A. Tokunaga, H. Yamanaka, T. Tachibana, Y. Liu, and K. Noguchi Phosphorylation of extracellular signal-regulated kinase in primary afferent neurons by noxious stimuli and its involvement in peripheral sensitization J Neurosci 22 2002 7737 7745
11. Y. Dai, K. Iwata, T. Fukuoka, E. Kondo, A. Tokunaga, H. Yamanaka, T. Tachibana, Y. Liu, and K. Noguchi Contribution of sensitized P2X receptors in inflamed tissue to the mechanical hypersensitivity revealed by phosphorylated ERK in DRG neurons Pain 108 2004 258 266
12. J.B. Davis, J. Gray, M.J. Gunthorpe, J.P. Hatcher, P.T. Davey, P. Overend, M.H. Harries, J. Latcham, C. Clapham, K. Atkinson, S.A. Hughes, K. Rance, E. Grau, A.J. Harper, P.L. Pugh, D.C. Rogers, S. Bingham, A. Randall, and S.A. Sheardown Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia Nature 405 2000 183 187
13. J.D. Delcroix, J.S. Valletta, C. Wu, S.J. Hunt, A.S. Kowal, and W.C. Mobley NGF signaling in sensory neurons: evidence that early endosomes carry NGF retrograde signals Neuron 39 2003 69 84
14. S.M. Durek, and R.D. Fields Mitogen-activated protein kinase/extracellular signal-regulated kinase activation in somatodendritic compartments: roles of action potentials, frequency, and model of calcium entry J Neurosci 21 2001 RC122
15. J.D. English, and J.D. Sweatt Activation of p42 mitogen-activated protein kinase in hippocampal long-term potentiation J Biol Chem 271 1996 24329 24332
16. R.D. Fields Effects of ion channel activity on development of dorsal root ganglion neurons J Neurobiol 37 1998 158 170
17. 2+, cAMP-responsive element binding proteins, and mitogen-activated protein kinase signaling J Neurosci 17 1997 7252 7266
18. T. Fukuoka, E. Kondo, Y. Dai, N. Hashimoto, and K. Noguchi Brain-derived neurotrophic factor increases in the uninjured dorsal root ganglion neurons in selective spinal nerve ligation model J Neurosci 21 2001 4891 4900
19. K. Hargreaves, R. Dubner, F. Brown, C. Flores, and J. Joris A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia Pain 32 1988 77 88
20. N. Hashimoto, H. Yamanaka, T. Fukuoka, Y. Dai, K. Obata, T. Mashimo, and K. Noguchi Expression of HGF and cMet in the peripheral nervous system of adult rats following sciatic nerve injury Neuroreport 12 2001 1403 1407
21. B. Hunyady, K. Krempels, G. Harta, and E. Mezey Immunohistochemical signal amplification by catalyzed reporter deposition and its application in double immunostaining J Histochem Cytochem 44 1996 1353 1362
22. R.R. Ji, H. Baba, G.J. Brenner, and C.J. Woolf Nociceptive-specific activation of ERK in spinal neurons contributes to pain hypersensitivity Nat Neurosci 2 1999 1114 1119
23. R.R. Ji, T.A. Samad, S.X. Jin, R. Schmoll, and C.J. Woolf p38 MAPK activation by NGF in primary sensory neurons after inflammation increases TRPV1 levels and maintains heat hyperalgesia Neuron 36 2002 57 68
24. R.R. Ji, T. Kohno, K.A. Moore, and C.J. Woolf Central sensitization and LTP: do pain and memory share similar mechanisms? Trends Neurosci 26 2003 696 705
25. S.X. Jin, Z.Y. Zhuang, C.J. Woolf, and R.R. Ji 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 2003 4017 4022
26. D. Julius, and A.I. Basbaum Molecular mechanisms of nociception Nature 413 2001 203 210
27. F. Karim, C.C. Wang, and R.W. Gereau 4th Metabotropic glutamate receptor subtypes 1 and 5 are activators of extracellular signal-regulated kinase signaling required for inflammatory pain in mice J Neurosci 21 2001 3771 3779
28. Y. Kawashima, I. Takeyoshi, Y. Otani, Y. Koibuchi, D. Yoshinari, T. Koyama, M. Kobayashi, K. Matsumoto, and Y. Morishita FR167653 attenuates ischemia and reperfusion injury of the rat lung with suppressing p38 mitogen-activated protein kinase J Heart Lung Transplant 20 2001 568 574
29. S.Y. Kim, J.C. Bae, J.Y. Kim, H.L. Lee, K.M. Lee, D.S. Kim, and H.J. Cho Activation of p38 MAP kinase in the rat dorsal root ganglia and spinal cord following peripheral inflammation and nerve injury Neuroreport 13 2002 2483 2486
30. M. Koistinaho, and J. Koistinaho Role of p38 and p44/42 mitogen-activated protein kinases in microglia Glia 40 2002 175 183
31. Y. Kominato, T. Tachibana, Y. Dai, H. Tsujino, S. Maruo, and K. Noguchi Changes in phosphorylation of ERK and Fos expression in dorsal horn neurons following noxious stimulation in a rat model of neuritis of the nerve root Brain Res 967 2003 89 97
32. I. Lever, J. Cunningham, J. Grist, P.K. Yip, and M. Malcangio Release of BDNF and GABA in the dorsal horn of neuropathic rats Eur J Neurosci 18 2003 1169 1174
33. T.S. Lewis, P.S. Shapiro, and N.G. Ahn Signal transduction through MAP kinase cascades Adv Cancer Res 74 1998 49 139
34. Y. Liu, K. Obata, H. Yamanaka, Y. Dai, T. Fukuoka, A. Tokunaga, and K. Noguchi Activation of extracellular signal-regulated protein kinase in dorsal horn neurons in the rat neuropathic intermittent claudication model Pain 109 2004 64 72
35. Z. Mao, A. Bonni, F. Xia, M. Nadal-Vicens, and M.E. Greenberg Neuronal activity-dependent cell survival mediated by transcription factor MEF2 Science 286 1999 785 790
36. G.J. Michael, and J.V. Priestley Differential expression of the mRNA for the vanilloid receptor subtype 1 in cells of the adult rat dorsal root and nodose ganglia and its downregulation by axotomy J Neurosci 19 1999 1844 1854
37. G.J. Michael, S. Averill, A. Nitkunan, M. Rattray, D.L. Bennett, Q. Yan, and J.V. Priestley Nerve growth factor treatment increases brain-derived neurotrophic factor selectively in TrkA-expressing dorsal root ganglion cells and in their central terminations within the spinal cord J Neurosci 17 1997 8476 8490
38. E.D. Milligan, K.A. O'Connor, C.B. Armstrong, M.K. Hansen, D. Martin, K.J. Tracey, S.F. Maier, and L.R. Watkins Systemic administration of CNI-1493, a p38 mitogen-activated protein kinase inhibitor, blocks intrathecal human immunodeficiency virus-1 gp120-induced enhanced pain states in rats J Pain 2 2001 326 333
39. K. Noguchi, Y. Kawai, T. Fukuoka, E. Senba, and K. Miki Substance P induced by peripheral nerve injury in primary afferent sensory neurons and its effect on dorsal column nucleus neurons J Neurosci 15 1995 7633 7643
40. H. Nomura, A. Furuta, S.O. Suzuki, and T. Iwaki Dorsal horn lesion resulting from spinal root avulsion leads to the accumulation of stress-responsive proteins Brain Res 893 2001 84 94
41. K. Obata, and K. Noguchi MAPK activation in nociceptive neurons and pain hypersensitivity Life Sci 74 2004 2643 2653
42. K. Obata, H. Tsujino, H. Yamanaka, Y. Dai, T. Fukuoka, N. Hashimoto, K. Yonenobu, H. Yoshikawa, and K. Noguchi Expression of neurotrophic factors in the dorsal root ganglion in a rat model of lumbar disc herniation Pain 99 2002 121 132
43. K. Obata, H. Yamanaka, T. Fukuoka, Y. Dai, A. Tokunaga, N. Hashimoto, H. Yoshikawa, and K. Noguchi Contribution of injured and uninjured DRG neurons to pain behavior and the changes in gene expression following chronic constriction injury of the sciatic nerve in rats Pain 101 2003 65 77
44. K. Obata, H. Yamanaka, Y. Dai, T. Tachibana, T. Fukuoka, A. Tokunaga, H. Yoshikawa, and K. Noguchi Differential activation of extracellular signal-regulated protein kinase in primary afferent neurons regulates brain-derived neurotrophic factor expression after peripheral inflammation and nerve injury J Neurosci 23 2003 4117 4126
45. K. Obata, H. Yamanaka, Y. Dai, T. Mizushima, T. Fukuoka, A. Tokunaga, H. Yoshikawa, and K. Noguchi Contribution of degeneration of motor and sensory fibers to pain behavior and the changes in neurotrophic factors in rat dorsal root ganglion Exp Neurol 188 2004 149 160
46. K. Obata, H. Yamanaka, Y. Dai, T. Mizushima, T. Fukuoka, A. Tokunaga, and K. Noguchi Activation of extracellular signal-regulated protein kinase in the dorsal root ganglion following inflammation near the nerve cell body Neuroscience 126 2004 1011 1021
47. S. Pezet, J. Cunningham, J. Patel, J. Grist, I. Gavazzi, I.J. Lever, and M. Malcangio BDNF modulates sensory neuron synaptic activity by a facilitation of GABA transmission in the dorsal horn Mol Cell Neurosci 21 2002 51 62
48. S. Pezet, M. Malcangio, I.J. Lever, M.S. Perkinton, S.W. Thompson, R.J. Williams, and S.B. McMahon Noxious stimulation induces Trk receptor and downstream ERK phosphorylation in spinal dorsal horn Mol Cell Neurosci 21 2002 684 695
49. 2+ mobilisation and stress kinases in cultured sensory neurones Neuropharmacology 42 2002 93 106
50. M.H. Rashid, M. Inoue, M. Matsumoto, and H. Ueda Switching of bradykinin-mediated nociception following partial sciatic nerve injury in mice J Pharmacol Exp Ther 308 2004 1158 1164
51. 2+) influx-mediated suppression of vitamin D3 up-regulated protein 1 (VDUP1) mRNA in cerebellar granule neurons undergoing apoptosis J Neurochem 78 2001 1267 1276
52. M. Schafers, C.I. Svensson, C. Sommer, and L.S. Sorkin Tumor necrosis factor-alpha induces mechanical allodynia after spinal nerve ligation by activation of p38 MAPK in primary sensory neurons J Neurosci 23 2003 2517 2521
53. J. Scholz, and C.J. Woolf Can we conquer pain? Nat Neurosci 5 2002 1062 1067
54. R. Seger, and E.G. Krebs The MAPK signaling cascade Fed Am Soc Exp Biol J 9 1995 726 735
55. Y. Shi, and M. Gaestel In the cellular garden of forking paths: how p38 MAPKs signal for downstream assistance Biol Chem 383 2002 1519 1536
56. K.S. Shindler, and K.A. Roth Double immunofluorescent staining using two unconjugated primary antisera raised in the same species J Histochem Cytochem 44 1996 1331 1335
57. A.K. Stringaris, J. Geisenhainer, F. Bergmann, C. Balshusemann, U. Lee, G. Zysk, T.J. Mitchell, B.U. Keller, U. Kuhnt, J. Gerber, A. Spreer, M. Bahr, U. Michel, and R. Nau Neurotoxicity of pneumolysin, a major pneumococcal virulence factor, involves calcium influx and depends on activation of p38 mitogen-activated protein kinase Neurobiol Dis 11 2002 355 368
58. C.I. Svensson, X.Y. Hua, A.A. Protter, H.C. Powell, and T.L. Yaksh Spinal p38 MAP kinase is necessary for NMDA-induced spinal PGE(2) release and thermal hyperalgesia Neuroreport 14 2003 1153 1157
59. C.I. Svensson, M. Marsala, A. Westerlund, N.A. Calcutt, W.M. Campana, J.D. Freshwater, R. Catalano, Y. Feng, A.A. Protter, B. Scott, and T.L. Yaksh Activation of p38 mitogen-activated protein kinase in spinal microglia is a critical link in inflammation-induced spinal pain processing J Neurochem 86 2003 1534 1544
60. S. Takahashi, Y. Keto, T. Fujita, T. Uchiyama, and A. Yamamoto FR167653, a p38 mitogen-activated protein kinase inhibitor, prevents Helicobacter pylori-induced gastritis in Mongolian gerbils J Pharmacol Exp Ther 296 2001 48 56
61. M. Tominaga, M.J. Caterina, A.B. Malmberg, T.A. Rosen, H. Gilbert, K. Skinner, B.E. Raumann, A.I. Basbaum, and D. Julius The cloned capsaicin receptor integrates multiple pain-producing stimuli Neuron 21 1998 531 543
62. B. Torocsik, and J. Szeberenyi Anisomycin uses multiple mechanisms to stimulate mitogen-activated protein kinases and gene expression and to inhibit neuronal differentiation in PC12 phaeochromocytoma cells Eur J Neurosci 12 2000 527 532
63. M. Tsuda, A. Mizokoshi, Y. Shigemoto-Mogami, S. Koizumi, and K. Inoue Activation of p38 mitogen-activated protein kinase in spinal hyperactive microglia contributes to pain hypersensitivity following peripheral nerve injury Glia 45 2004 89 95
64. H. Wang, Y. Dai, T. Fukuoka, H. Yamanaka, K. Obata, A. Tokunaga, and K. Noguchi Enhancement of stimulation-induced ERK activation in the spinal dorsal horn and gracile neurons in rats with peripheral nerve injury Eur J Neurosci 19 2004 884 890
65. L.R. Watkins, D. Martin, P. Ulrich, K.J. Tracey, and S.F. Maier Evidence for the involvement of spinal cord glia in subcutaneous formalin induced hyperalgesia in the rat Pain 71 1997 225 235
66. L.R. Watkins, E.D. Milligan, and S.F. Maier Glial activation: a driving force for pathological pain Trends Neurosci 24 2001 450 455
67. L.R. Watkins, E.D. Milligan, and S.F. Maier Spinal cord glia: new players in pain Pain 93 2001 201 205
68. C. Widmann, S. Gibson, M.B. Jarpe, and G.L. Johnson Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human Physiol Rev 79 1999 143 180
69. N. Yamamoto, F. Sakai, H. Yamazaki, K. Nakahara, and M. Okuhara Effect of FR167653, a cytokine suppressive agent, on endotoxin-induced disseminated intravascular coagulation Eur J Pharmacol 314 1996 137 142
70. N. Yamamoto, F. Sakai, H. Yamazaki, N. Sato, K. Nakahara, and M. Okuhara FR167653, a dual inhibitor of interleukin-1 and tumor necrosis factor-alpha, ameliorates endotoxin-induced shock Eur J Pharmacol 327 1997 169 174
71. D. Yoshinari, I. Takeyoshi, Y. Koibuchi, K. Matsumoto, Y. Kawashima, T. Koyama, S. Ohwada, and Y. Morishita Effects of a dual inhibitor of tumor necrosis factor-alpha and interleukin-1 on lipopolysaccharide-induced lung injury in rats: involvement of the p38 mitogen-activated protein kinase pathway Crit Care Med 29 2001 628 634