Role of mitogen-activated protein kinase activation in injured and intact primary afferent neurons for mechanical and heat hypersensitivity after spinal nerve ligation

Journal of Neuroscience

Volumn 24, Issue 45, 2004, Pages 10211-10222

  Obata, Koichi ^a   Yamanaka, Hiroki ^a   Kobayashi, Kimiko ^a   Dai, Yi ^a   Mizushima, Toshiyuki ^a   Katsura, Hirokazu ^a   Fukuoka, Tetsuo ^a   Tokunaga, Atsushi ^a   Noguchi, Koichi ^a  

^a HYOGO COLLEGE OF MEDICINE   (Japan)

Author keywords

Brain derived neurotrophic factor; C Jun N terminal kinase stress activated protein kinase; Extracellular signal regulated protein kinase; Neuropathic pain; p38 mitogen activated protein kinase; TRPV1

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; NERVE GROWTH FACTOR ANTIBODY; NEUROPEPTIDE Y; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR; VANILLOID RECEPTOR 1;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; HEAT; HYPERALGESIA; HYPERSENSITIVITY; IMMUNOREACTIVITY; LUMBAR SPINE; MECHANICAL STIMULATION; MUSCLE SPINDLE AFFERENT NERVE; NERVE FIBER TRANSECTION; NERVE INJURY; NERVE LIGATION; NEUROPATHIC PAIN; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; RAT; RHIZOTOMY; SPINAL GANGLION; SPINAL NERVE; UPREGULATION;

ANIMALS; ANTHRACENES; BRAIN-DERIVED NEUROTROPHIC FACTOR; BUTADIENES; ENZYME ACTIVATION; GANGLIA, SPINAL; GENE EXPRESSION REGULATION; HEAT; HYPERALGESIA; IMIDAZOLES; ION CHANNELS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LIGATION; LUMBAR VERTEBRAE; MALE; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; NEURONS, AFFERENT; NITRILES; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHYSICAL STIMULATION; PYRAZOLES; PYRIDINES; RATS; RATS, SPRAGUE-DAWLEY; RHIZOTOMY; SPINAL NERVES; STRESS, MECHANICAL; TRPV CATION CHANNELS;

EID: 8544239374     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3388-04.2004     Document Type: Article

References (96)

1. Aley KO, Martin A, McMahon T, Mok J, Levine JD, Messing RO (2001) Nociceptor sensitization by extracellular signal-regulated kinases. J Neurosci 21:6933-6939.
2. Ali Z, Ringkamp M, Hartke TV, Chien HF, Flavahan NA, Campbell JN, Meyer RA (1999) Uninjured C-fiber nociceptors develop spontaneous activity and alpha-adrenergic sensitivity following L6 spinal nerve ligation in monkey. J Neurophysiol 81:455-466.
3. Amaya F, Oh-hashi K, Naruse Y, Iijima N, Ueda M, Shimosato G, Tominaga M, Tanaka Y, Tanaka M (2003) Local inflammation increases vanilloid receptor 1 expression within distinct subgroups of DRG neurons. Brain Res 963:190-196.
4. Apfel SC, Wright DE, Wiideman AM, Dormia C, Snider WD, Kessler JA (1996) Nerve growth factor regulates the expression of brain-derived neurotrophic factor mRNA in the peripheral nervous system. Mol Cell Neurosci 7:134-142.
5. Averill S, Delcroix JD, Michael GJ, Tomlinson DR, Fernyhough P, Priestley JV (2001) Nerve growth factor modulates the activation status and fast axonal transport of erk 1/2 in adult nociceptive neurones. Mol Cell Neurosci 18:183-196.
6. Bennett GJ, Xie YK (1988) A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 33:87-107.
7. Boucher TJ, Okuse K, Bennett DL, Munson JB, Wood JN, McMahon SB (2000) Potent analgesic effects of GDNF in neuropathic pain states. Science 290:124-127.
8. Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, Petersen-Zeitz KR, Koltzenburg M, Basbaum AI, Julius D (2000) Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288:306-313.
9. Ciruela A, Dixon AK, Bramwell S, Gonzalez MI, Pinnock RD, Lee K (2003) Identification of MEK1 as a novel target for the treatment of neuropathic pain. Br J Pharmacol 138:751-756.
10. Colburn RW, Rickman AJ, DeLeo JA (1999) The effect of site and type of nerve injury on spinal glial activation and neuropathic pain behavior. Exp Neurol 157:289-304.
11. Cui JG, Holmin S, Mathiesen T, Meyerson BA, Linderoth B (2000) Possible role of inflammatory mediators in tactile hypersensitivity in rat models of mononeuropathy. Pain 88:239-248.
12. Dai Y, Iwata K, Fukuoka T, Kondo E, Tokunaga A, Yamanaka H, Tachibana T, Liu Y, Noguchi K (2002) Phosphorylation of extracellular signal-regulated kinase in primary afferent neurons by noxious stimuli and its involvement in peripheral sensitization. J Neurosci 22:7737-7745.
13. Davis JB, Gray J, Gunthorpe MJ, Hatcher JP, Davey PT, Overend P, Harries MH, Latcham J, Clapham C, Atkinson K, Hughes SA, Ranee K, Grau E, Harper AJ, Pugh PL, Rogers DC, Bingham S, Randall A, Sheardown SA (2000) Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature 405:183-187.
14. Decosterd I, Woolf CJ (2000) Spared nerve injury: an animal model of persistent peripheral neuropathic pain. Pain 87:149-158.
15. Delcroix JD, Valletta JS, Wu C, Hunt SJ, Kowal AS, Mobley WC (2003) NGF signaling in sensory neurons: evidence that early endosomes carry NGF retrograde signals. Neuron 39:69-84.
16. Devor M (1991) Neuropathic pain and injured nerve: peripheral mechanisms. Br Med Bull 47:619-630.
17. Devor M, Seltzer Z (1999) Pathophysiology of damaged nerves in reaction to chronic pain. In: Textbook of pain (Wall PD, Melzack R, eds), pp 129-164. London: Churchill Livingstone.
18. Dina OA, McCarter GC, de Coupade C, Levine JD (2003) Role of the sensory neuron cytoskeleton in second messenger signaling for inflammatory pain. Neuron 39:613-624.
19. Eschenfelder S, Habler HJ, Janig W (2000) Dorsal root section elicits signs of neuropathic pain rather than reversing them in rats with L5 spinal nerve injury. Pain 87:213-219.
20. Fukuoka T, Noguchi K (2002) Contribution of the spared primary afferent neurons to the pathomechanisms of neuropathic pain. Mol Neurobiol 26:57-67.
21. Fukuoka T, Tokunaga A, Kondo E, Miki K, Tachibana T, Noguchi K (1998) Change in mRNAs for neuropeptides and the GABA(A) receptor in dorsal root ganglion neurons in a rat experimental neuropathic pain model. Pain 78:13-26.
22. FukuokaT, Kondo E, Dai Y, Hashimoto N, Noguchi K (2001) Brain-derived neurotrophic factor increases in the uninjured dorsal root ganglion neurons in selective spinal nerve ligation model. J Neurosci 21:4891-4900.
23. Fukuoka T, Tokunaga A, Tachibana T, Dai Y, Yamanaka H, Noguchi K (2002) VR1, but not P2X(3), increases in the spared L4 DRG in rats with L5 spinal nerve ligation. Pain 99:111-120.
24. Gold MS (2000) Spinal nerve ligation: what to blame for the pain and why. Pain 84:117-120.
25. Groth R, Aanonsen L (2002) Spinal brain-derived neurotrophic factor (BDNF) produces hyperalgesia in normal mice while antisense directed against either BDNF or trkB, prevent inflammation-induced hyperalgesia. Pain 100:171-181.
26. Ha SO, Kim JK, Hong HS, Kim DS, Cho HJ (2001) Expression of brain-derived neurotrophic factor in rat dorsal root ganglia, spinal cord and gracile nuclei in experimental models of neuropathic pain. Neuroscience 107:301-309.
27. Hashimoto N, Yamanaka H, Fukuoka T, Dai Y, Obata K, Mashimo T, Noguchi K (2001) Expression of HGF and cMet in the peripheral nervous system of adult rats following sciatic nerve injury. NeuroReport 12:1403-1407.
28. Hokfelt T, Zhang X, Wiesenfeld-Hallin Z (1994) Messenger plasticity in primary sensory neurons following axotomy and its functional implications. Trends Neurosci 17:22-30.
29. Hudson LJ, Bevan S, Wotherspoon G, Gentry C, Fox A, Winter J (2001) VR1 protein expression increases in undamaged DRG neurons after partial nerve injury. Eur J Neurosci 13:2105-2114.
30. Ji RR (2004) Mitogen-activated protein kinases as potential targets for pain killers. Curr Opin Investig Drugs 5:71-75.
31. 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.
32. 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.
33. Kafitz KW, Rose CR, Thoenen H, Konnerth A (1999) Neurotrophin-evoked rapid excitation through TrkB receptors. Nature 401:918-921.
34. Kalmar B, Greensmith L, Malcangio M, McMahon SB, Csermely P, Burnstock G (2003) The effect of treatment with BRX-220, a co-inducer of heat shock proteins, on sensory fibers of the rat following peripheral nerve injury. Exp Neurol 184:636-647.
35. Kawashima Y, Takeyoshi I, Otani Y, Koibuchi Y, Yoshinari D, Koyama T, Kobayashi M, Matsumoto K, Morishita Y (2001) FR167653 attenuates ischemia and reperfusion injury of the rat lung with suppressing p38 mitogen-activated protein kinase. J Heart Lung Transplant 20:568-574.
36. Kenney AM, Kocsis JD (1998) Peripheral axotomy induces long-term c-Jun ammo-terminal kinase-1 activation and activator protein-1 binding activity by c-Jun and junD in adult rat dorsal root ganglia in vivo. J Neurosci 18:1318-1328.
37. Kerr BJ, Bradbury EJ, Bennett DL, Trivedi PM, Dassan P, French J, Shelton DB, McMahon SB, Thompson SW (1999) Brain-derived neurotrophic factor modulates nociceptive sensory inputs and NMDA-evoked responses in the rat spinal cord. J Neurosci 19:5138-5148.
38. Kim SH, Chung JM (1992) An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 50:355-363.
39. 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.
40. Koistinaho M, Koistinaho J (2002) Role of p38 and p44/42 mitogen-activated protein kinases in microglia. Glia 40:175-183.
41. Koltzenburg M, Torebjork HE, Wahren LK (1994) Nociceptor modulated central sensitization causes mechanical hyperalgesia in acute chemogenic and chronic neuropathic pain. Brain 117:579-591.
42. Lever I, Cunningham J, Grist J, Yip PK, Malcangio M (2003) Release of BDNF and GABA in the dorsal horn of neuropathic rats. Eur J Neurosci 18:1169-1174.
43. Lewis TS, Shapiro PS, Ahn NG (1998) Signal transduction through MAP kinase cascades. Adv Cancer Res 74:49-139.
44. Li Y, Dorsi MJ, Meyer RA, Belzberg AJ (2000) Mechanical hyperalgesia after an L5 spinal nerve lesion in the rat is not dependent on input from injured nerve fibers. Pain 85:493-502.
45. Liu CN, Wall PD, Ben-Dor E, Michaelis M, Amir R, Devor M (2000) Tactile allodynia in the absence of C-fiber activation: altered firing properties of DRG neurons following spinal nerve injury. Pain 85:503-521.
46. Ma W, Bisby MA (1998a) Increase of calcitonin gene-related peptide immunoreactivity in the axonal fibers of the gracile nuclei of adult and aged rats after complete and partial sciatic nerve injuries. Exp Neurol 152:137-149.
47. Ma W, Bisby MA (1998b) Increase of preprotachykinin mRNA and substance P immunoreactivity in spared dorsal root ganglion neurons following partial sciatic nerve injury. Eur J Neurosci 10:2388-2399.
48. Ma C, Shu Y, Zheng Z, Chen Y, Yao H, Greenquist KW, White FA, LaMotte RH (2003) Similar electrophysiological changes in axotomized and neighboring intact dorsal root ganglion neurons. J Neurophysiol 89:1588-1602.
49. Malcangio M, Lessmann V (2003) A common thread for pain and memory synapses? Brain-derived neurotrophic factor and trkB receptors. Trends Pharmacol Sci 24:116-121.
50. Mamet J, Lazdunski M, Voilley N (2003) How nerve growth factor drives physiological and inflammatory expressions of acid-sensing ion channel 3 in sensory neurons. J Biol Chem 278:48907-48913.
51. Mannion RJ, Costigan M, Decosterd I, Amaya F, Ma QP, Holstege JC, Ji RR, Acheson A, Lindsay RM, Wilkinson GA, Woolf CJ (1999) Neurotrophins: peripherally and centrally acting modulators of tactile stimulus-induced inflammatory pain hypersensitivity. Proc Natl Acad Sci USA 96:9385-9390.
52. Michael GJ, Priestley JV (1999) 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 19:1844-1854.
53. Michael GJ, Averill S, Nitkunan A, Rattray M, Bennett DL, Yan Q, Priestley JV (1997) 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 17:8476-8490.
54. Michaelis M, Liu X, Janig W (2000) Axotomized and intact muscle afferents but no skin afferents develop ongoing discharges of dorsal root ganglion origin after peripheral nerve lesion. J Neurosci 20:2742-2748.
55. Myers RR, Heckman HM, Rodriguez M (1996) Reduced hyperalgesia in nerve-injured WLD mice: relationship to nerve fiber phagocytosis, axonal degeneration, and regeneration in normal mice. Exp Neurol 141:94-101.
56. Nichols ML, Allen BJ, Rogers SD, Ghilardi JR, Honore P, Luger NM, Finke MP, Li J, Lappi DA, Simone DA, Mantyh PW (1999) Transmission of chronic nociception by spinal neurons expressing the substance P receptor. Science 286:1558-1561.
57. Noguchi K, Kawai Y, Fukuoka T, Senba E, Miki K (1995) Substance P induced by peripheral nerve injury in primary afferent sensory neurons and its effect on dorsal column nucleus neurons. J Neurosci 15:7633-7643.
58. Obata K, Noguchi K (2004) MAPK activation in nociceptive neurons and pain hypersensitivity. Life Sci 74:2643-2653.
59. Obata K, Tsujino H, Yamanaka H, Dai Y, Fukuoka T, Hashimoto N, Yonenobu K, Yoshikawa H, Noguchi K (2002) Expression of neurotrophic factors in the dorsal root ganglion in a rat model of lumbar disc herniation. Pain 99:121-132.
60. Obata K, Yamanaka H, Fukuoka T, Dai Y, Tokunaga A, Hashimoto N, Yoshikawa H, Noguchi K (2003a) 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 101:65-77.
61. Obata K, Yamanaka H, Dai Y, Tachibana T, Fukuoka T, Tokunaga A, Yoshikawa H, Noguchi K (2003b) 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 23:4117-4126.
62. Obata K, Yamanaka H, Dai Y, Mizushima T, Fukuoka T, Tokunaga A, Yoshikawa H, Noguchi K (2004) Contribution of degeneration of motor and sensory fibers to pain behavior and the changes in neurotrophic factors in rat dorsal root ganglion. Exp Neurol 188:149-160.
63. Ossipov MH, Bian D, Malan Jr TP, Lai I, Porreca F (1999) Lack of involvement of capsaicin-sensitive primary afferents in nerve-ligation injury induced tactile allodynia in rats. Pain 79:127-133.
64. Ossipov MH, Zhang ET, Carvajal C, Gardell L, Quirion R, Dumont Y, Lai J, Porreca F (2002) Selective mediation of nerve injury-induced tactile hypersensitivity by neuropeptide Y. J Neurosci 22:9858-9867.
65. Pan HL, Khan GM, Alloway KD, Chen SR (2003) Resiniferatoxin induces paradoxical changes in thermal and mechanical sensitivities in rats: mechanism of action. J Neurosci 23:2911-2919.
66. Pezet S, Malcangio M, McMahon SB (2002) BDNF: a neuromodulator in nociceptive pathways? Brain Res Brain Res Rev 40:240-249.
67. 2+ mobilisation and stress kinases in cultured sensory neurones. Neuropharmacology 42:93-106.
68. Porreca F, Lai J, Bian D, Wegert S, Ossipov MH, Eglen RM, Kassotakis L, Novakovic S, Rabert DK, Sangameswaran L, Hunter JC (1999) A comparison of the potential role of the tetrodotoxin-insensitive sodium channels, PN3/SNS and NaN/SNS2, in rat models of chronic pain. Proc Natl Acad Sci USA 96:7640-7644.
69. Prats-Galino A, Puigdellivol-Sanchez A, Ruano-Gil D, Molander C (1999) Representations of hindlimb digits in rat dorsal root ganglia. J Comp Neurol 408:137-145.
70. Ramer MS, French GD, Bisby MA (1997) Wallerian degeneration is required for both neuropathic pain and sympathetic sprouting into the DRG. Pain 72:71-78.
71. Schafers M, Geis C, Svensson CI, Luo ZD, Sommer C (2003a) Selective increase of tumour necrosis factor-alpha in injured and spared myelinated primary afferents after chronic constrictive injury of rat sciatic nerve. Eur J Neurosci 17:791-804.
72. 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.
73. 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.
74. Scholz J, Woolf CJ (2002) Can we conquer pain? Nat Neurosci [Suppl] 5:1062-1067.
75. Seltzer Z, Dubner R, Shir Y (1990) A novel behavioral model of neuropathic pain disorders produced in rats by partial sciatic nerve injury. Pain 43:205-218.
76. Shamash S, Reichert F, Rotshenker S (2002) The cytokine network of Wallerian degeneration: tumor necrosis factor-α, interleukin-1α, and interleukin-1β. J Neurosci 22:3052-3060.
77. Sheen K, Chung JM (1993) Signs of neuropathic pain depend on signals from injured nerve fibers in a rat model. Brain Res 610:62-68.
78. Sheth RN, Dorsi MJ, Li Y, Murinson BB, Belzberg AJ, Griffin JW, Meyer RA (2002) Mechanical hyperalgesia after an L5 ventral rhizotomy or an L5 ganglionectomy in the rat. Pain 96:63-72.
79. Sommer C, Schafers M (1998) Painful mononeuropathy in C57BL/Wld mice with delayed wallerian degeneration: differential effects of cytokine production and nerve regeneration on thermal and mechanical hypersensitivity. Brain Res 784:154-162.
80. Sukhotinsky I, Ben-Dor E, Raber P, Devor M (2004) Key role of the dorsal root ganglion in neuropathic tactile hypersensibility. Eur J Pain 8:135-143.
81. Tabo E, Jinks SL, Eisele Jr JH, Carstens E (1999) Behavioral manifestations of neuropathic pain and mechanical allodynia, and changes in spinal dorsal horn neurons, following L4-L6 dorsal root constriction in rats. Pain 80:503-520.
82. Takahashi S, Keto Y, Fujita T, Uchiyama T, Yamamoto A (2001) FR167653, a p38 mitogen-activated protein kinase inhibitor, prevents Helicobacter pylori-induced gastritis in Mongolian gerbils. J Pharmacol Exp Ther 296:48-56.
83. Takahashi Y, Nakajima Y, Sakamoto T (1994) Dermatome mapping in the rat hindlimb by electrical stimulation of the spinal nerves. Neurosci Lett 168:85-88.
84. Thompson SW, Bennett DL, Kerr BJ, Bradbury EJ, McMahon SB (1999) Brain-derived neurotrophic factor is an endogenous modulator of nociceptive responses in the spinal cord. Proc Natl Acad Sci USA 96:7714-7718.
85. Tohda C, Sasaki M, Konemura T, Sasamura T, Itoh M, Kuraishi Y (2001) Axonal transport of VR1 capsaicin receptor mRNA in primary afferents and its participation in inflammation-induced increase in capsaicin sensitivity. J Neurochem 76:1628-1635.
86. Tsujino H, Kondo E, Fukuoka T, Dai Y, Tokunaga A, Miki K, Yonenobu K, Ochi T, Noguchi K (2000) Activating transcription factor 3 (ATF3) induction by axotomy in sensory and motoneurons: a novel neuronal marker of nerve injury. Mol Cell Neurosci 15:170-182.
87. Tsuzuki K, Kondo E, Fukuoka T, Yi D, Tsujino H, Sakagami M, Noguchi K (2001) Differential regulation of P2X(3) mRNA expression by peripheral nerve injury in intact and injured neurons in the rat sensory ganglia. Pain 91:351-360.
88. Wakisaka S, Kajander KC, Bennett GJ (1991) Increased neuropeptide Y (NPY)-like immunoreactivity in rat sensory neurons following peripheral axotomy. Neurosci Lett 124:200-203.
89. Widmann C, Gibson S, Jarpe MB, Johnson GL (1999) Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol Rev 79:143-180.
90. Winston J, Toma H, Shenoy M, Pasricha PJ (2001) Nerve growth factor regulates VR-1 mRNA levels in cultures of adult dorsal root ganglion neurons. Pain 89:181-186.
91. Wu G, Ringkamp M, Hartke TV, Murinson BB, Campbell JN, Griffin JW, Meyer RA (2001) Early onset of spontaneous activity in uninjured C-fiber nociceptors after injury to neighboring nerve fibers. J Neurosci 21:RC140(1-5).
92. Yamamoto N, Sakai F, Yamazaki H, Nakahara K, Okuhara M (1996) Effect of FR167653, a cytokine suppressive agent, on endotoxin-induced disseminated intravascular coagulation. Eur J Pharmacol 314:137-142.
93. Yamamoto N, Sakai F, Yamazaki H, Sato N, Nakahara K, Okuhara M (1997) FR167653, a dual inhibitor of interleukin-1 and tumor necrosis factor-alpha, ameliorates endotoxin-induced shock. Eur J Pharmacol 327:169-174.
94. Yamanaka H, He X, Matsumoto K, Shiosaka S, Yoshida S (1999) Protease M/neurosin mRNA is expressed in mature oligodendrocytes. Brain Res Mol Brain Res 71:217-224.
95. Yoon YW, Na HS, Chung JM (1996) Contributions of injured and intact afferents to neuropathic pain in an experimental rat model. Pain 64:27-36.
96. Yoshinari D, Takeyoshi I, Koibuchi Y, Matsumoto K, Kawashima Y, Koyama T, Ohwada S, Morishita Y (2001) 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 29:628-634.