Antisense knock down of TRPA1, but not TRPM8, alleviates cold hyperalgesia after spinal nerve ligation in rats

Experimental Neurology

Volumn 200, Issue 1, 2006, Pages 112-123

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

^a HYOGO COLLEGE OF MEDICINE   (Japan)

Author keywords

Dorsal root ganglion; Neuropathic pain; Spared neurons; TRPA1; TRPM8

Indexed keywords

ANTISENSE OLIGODEOXYNUCLEOTIDE; MESSENGER RNA; PROTEIN TYROSINE KINASE A; RECEPTOR SUBTYPE; TRANSIENT RECEPTOR POTENTIAL CATION CHANNEL M 8; TRANSIENT RECEPTOR POTENTIAL CHANNEL; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL SIZE; COLD HYPERALGESIA; COLD SENSITIVITY; CONTROLLED STUDY; HINDLIMB; HYPERALGESIA; HYPERSENSITIVITY; MALE; MUSCLE SPINDLE AFFERENT NERVE; NERVE INJURY; NEUROPATHIC PAIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RECEPTOR INTRINSIC ACTIVITY; SPECIES COMPARISON; SPINAL CORD HEMISECTION; SPINAL GANGLION; UPREGULATION;

ANIMALS; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS; COLD; GENE TARGETING; HINDLIMB; HYPERALGESIA; LIGATION; MALE; OLIGONUCLEOTIDES, ANTISENSE; PAIN MEASUREMENT; RATS; RATS, SPRAGUE-DAWLEY; SPINAL NERVES; TIME FACTORS; TRPM CATION CHANNELS;

EID: 33746083982     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2006.01.031     Document Type: Article

References (86)

1. Ali Z., Ringkamp M., Hartke T.V., Chien H.F., Flavahan N.A., Campbell J.N., and Meyer R.A. Uninjured C-fiber nociceptors develop spontaneous activity and alpha-adrenergic sensitivity following L6 spinal nerve ligation in monkey. J. Neurophysiol. 81 (1999) 455-466
2. Andreev N.Yu., Dimitrieva N., Koltzenburg M., and McMahon S.B. Peripheral administration of nerve growth factor in the adult rat produces a thermal hyperalgesia that requires the presence of sympathetic post-ganglionic neurones. Pain 63 (1995) 109-115
3. Apfel S.C., Wright D.E., Wiideman A.M., Dormia C., Snider W.D., and Kessler J.A. Nerve growth factor regulates the expression of brain-derived neurotrophic factor mRNA in the peripheral nervous system. Mol. Cell. Neurosci. 7 (1996) 134-142
4. Bandell M., Story G.M., Hwang S.W., Viswanath V., Eid S.R., Petrus M.J., Earley T.J., and Patapoutian A. Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin. Neuron 41 (2004) 849-857
5. Barclay J., Patel S., Dorn G., Wotherspoon G., Moffatt S., Eunson L., Abdel'al S., Natt F., Hall J., Winter J., Bevan S., Wishart W., Fox A., and Ganju P. Functional downregulation of P2X3 receptor subunit in rat sensory neurons reveals a significant role in chronic neuropathic and inflammatory pain. J. Neurosci. 22 (2002) 8139-8147
6. Bennett G.J., and Xie Y.K. A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 33 (1988) 87-107
7. Bennett G., al-Rashed S., Hoult J.R., and Brain S.D. Nerve growth factor induced hyperalgesia in the rat hind paw is dependent on circulating neutrophils. Pain 77 (1998) 315-322
8. Choi Y., Yoon Y.W., Na HS., Kim S.H., and Chung J.M. Behavioral signs of ongoing pain and cold allodynia in a rat model of neuropathic pain. Pain 59 (1994) 369-376
9. Chung K., Lee B.H., Yoon Y.W., and Chung J.M. Sympathetic sprouting in the dorsal root ganglia of the injured peripheral nerve in a rat neuropathic pain model. J. Comp. Neurol. 376 (1996) 241-252
10. Clapham D.E. TRP channels as cellular sensors. Nature 426 (2003) 517-524
11. Cui J.G., Holmin S., Mathiesen T., Meyerson B.A., and Linderoth B. Possible role of inflammatory mediators in tactile hypersensitivity in rat models of mononeuropathy. Pain 88 (2000) 239-248
12. Devor M. Neuropathic pain and injured nerve: peripheral mechanisms. Br. Med. Bull. 47 (1991) 619-630
13. Devor M., and Seltzer Z. Pathophysiology of damaged nerves in reaction to chronic pain. In: Wall P.D., and Melzack R. (Eds). Textbook of Pain (1999), Churchill Livingstone, London 129-164
14. Djouhri L., Wrigley D., Thut P.D., and Gold M.S. Spinal nerve injury increases the percentage of cold-responsive DRG neurons. NeuroReport 15 (2004) 457-460
15. Donnerer J., Schuligoi R., and Stein C. Increased content and transport of substance P and calcitonin gene-related peptide in sensory nerves innervating inflamed tissue: evidence for a regulatory function of nerve growth factor in vivo. Neuroscience 49 (1992) 693-698
16. Eschenfelder S., Habler H.J., and Janig W. Dorsal root section elicits signs of neuropathic pain rather than reversing them in rats with L5 spinal nerve injury. Pain 87 (2000) 213-219
17. Fukuoka T., and Noguchi K. Contribution of the spared primary afferent neurons to the pathomechanisms of neuropathic pain. Mol. Neurobiol. 26 (2002) 57-67
18. Fukuoka T., Tokunaga A., Kondo E., Miki K., Tachibana T., and Noguchi K. Change in mRNAs for neuropeptides and the GABA(A) receptor in dorsal root ganglion neurons in a rat experimental neuropathic pain model. Pain 78 (1998) 13-26
19. Fukuoka T., Miki K., Tokunaga A., Kondo E., and Noguchi K. Up-regulation of calcitonin gene-related peptide and preproyachykinin mRNA in L4 dorsal root ganglion neurons following L5 spinal nerve ligation; a rat neuropathic pain model. Neurosci. Abstr. 24 (1998) 1392
20. Fukuoka T., Kondo E., Dai Y., Hashimoto N., and Noguchi K. Brain-derived neurotrophic factor increases in the uninjured dorsal root ganglion neurons in selective spinal nerve ligation model. J. Neurosci. 21 (2001) 4891-4900
21. Fukuoka T., Tokunaga A., Tachibana T., Dai Y., Yamanaka H., and Noguchi K. VR1, but not P2X(3), increases in the spared L4 DRG in rats with L5 spinal nerve ligation. Pain 99 (2002) 111-120
22. Gold M.S. Spinal nerve ligation: what to blame for the pain and why. Pain 84 (2000) 117-120
23. Gold M.S., Weinreich D., Kim C.S., Wang R., Treanor J., Porreca F., and Lai J. Redistribution of Na(V)1.8 in uninjured axons enables neuropathic pain. J. Neurosci. 23 (2003) 158-166
24. Hama A.T. Capsaicin-sensitive primary afferents mediate responses to cold in rats with a peripheral mononeuropathy. NeuroReport 13 (2002) 461-464
25. Hao J.X., Yu W., Xu X.J., and Wiesenfeld-Hallin Z. Capsaicin-sensitive afferents mediate chronic cold, but not mechanical, allodynia-like behavior in spinally injured rats. Brain Res. 722 (1996) 177-180
26. Harrison J.L., and Davis K.D. Cold-evoked pain varies with skin type and cooling rate: a psychophysical study in humans. Pain 83 (1999) 123-135
27. Hashimoto N., Yamanaka H., Fukuoka T., Dai Y., Obata K., Mashimo T., and Noguchi K. Expression of HGF and cMet in the peripheral nervous system of adult rats following sciatic nerve injury. NeuroReport 12 (2001) 1403-1407
28. Hudson L.J., Bevan S., Wotherspoon G., Gentry C., Fox A., and Winter J. VR1 protein expression increases in undamaged DRG neurons after partial nerve injury. Eur. J. Neurosci. 13 (2001) 2105-2114
29. Jasmin L., Kohan L., Franssen M., Janni G., and Goff J.R. The cold plate as a test of nociceptive behaviors: description and application to the study of chronic neuropathic and inflammatory pain models. Pain 75 (1998) 367-382
30. Ji R.R., Samad T.A., Jin S.X., Schmoll R., and Woolf C.J. p38 MAPK activation by NGF in primary sensory neurons after inflammation increases TRPV1 levels and maintains heat hyperalgesia. Neuron 36 (2002) 57-68
31. Jordt S.E., McKemy D.D., and Julius D. Lessons from peppers and peppermint: the molecular logic of thermosensation. Curr. Opin. Neurobiol. 13 (2003) 487-492
32. Jordt S.E., Bautista D.M., Chuang H.H., McKemy D.D., Zygmunt P.M., Hogestatt E.D., Meng I.D., and Julius D. Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427 (2004) 260-265
33. Kim S.H., and Chung J.M. An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 50 (1992) 355-363
34. Kim K.J., Yoon Y.W., and Chung J.M. Comparison of three rodent neuropathic pain models. Exp. Brain Res. 113 (1997) 200-206
35. Kobayashi K., Fukuoka T., Yamanaka H., Dai Y., Obata K., Tokunaga A., and Noguchi K. Differential expression patterns of mRNAs for P2X receptor subunits in neurochemically characterized dorsal root ganglion neurons in the rat. J. Comp. Neurol. 481 (2005) 377-390
36. Kobayashi K., Fukuoka T., Obata K., Yamanaka H., Dai Y., Tokunaga A., and Noguchi K. Distinct expression of TRPM8, TRPA1 and TRPV1 mRNAs in rat primary afferent neurons with Aδ/C-fibers and colocalization with Trk receptors. J. Comp. Neurol. 493 (2005) 596-606
37. Koltzenburg M., Torebjork H.E., and Wahren L.K. Nociceptor modulated central sensitization causes mechanical hyperalgesia in acute chemogenic and chronic neuropathic pain. Brain 117 (1994) 579-591
38. Kress M., Koltzenburg M., Reeh P.W., and Handwerker H.O. Responsiveness and functional attributes of electrically localized terminals of cutaneous C-fibers in vivo and in vitro. J. Neurophysiol. 68 (1992) 581-595
39. Lai J., Gold M.S., Kim C.S., Bian D., Ossipov M.H., Hunter J.C., and Porreca F. Inhibition of neuropathic pain by decreased expression of the tetrodotoxin-resistant sodium channel, NaV1.8. Pain 95 (2002) 143-152
40. LaMotte R.H., and Thalhammer J.G. Response properties of high-threshold cutaneous cold receptors in the primate. Brain Res. 244 (1982) 279-287
41. Lee B.H., Yoon Y.W., Chung K., and Chung J.M. Comparison of sympathetic sprouting in sensory ganglia in three animal models of neuropathic pain. Exp. Brain Res. 120 (1998) 432-438
42. Lewin G.R., and Mendell L.M. Nerve growth factor and nociception. Trends Neurosci. 16 (1993) 353-359
43. Li Y., Dorsi M.J., Meyer R.A., and Belzberg A.J. Mechanical hyperalgesia after an L5 spinal nerve lesion in the rat is not dependent on input from injured nerve fibers. Pain 85 (2000) 493-502
44. Ma W., and Bisby M.A. 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 (1998) 137-149
45. Ma W., and Bisby M.A. Increase of preprotachykinin mRNA and substance P immunoreactivity in spared dorsal root ganglion neurons following partial sciatic nerve injury. Eur. J. Neurosci. 10 (1998) 2388-2399
46. Ma C., Shu Y., Zheng Z., Chen Y., Yao H., Greenquist K.W., White F.A., and LaMotte R.H. Similar electrophysiological changes in axotomized and neighboring intact dorsal root ganglion neurons. J. Neurophysiol. 89 (2003) 1588-1602
47. Macpherson L.J., Geierstanger B.H., Viswanath V., Bandell M., Eid S.R., Hwang S., and Patapoutian A. The pungency of garlic: activation of TRPA1 and TRPV1 in response to allicin. Curr. Biol. 15 (2005) 929-934
48. McKemy D.D. How cold is it? TRPM8 and TRPA1 in the molecular logic of cold sensation. Mol. Pain 1 (2005) 16
49. McKemy D.D., Neuhausser W.M., and Julius D. Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416 (2002) 52-58
50. Michael G.J., and Priestley J.V. 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
51. Michaelis M., Liu X., and Janig W. Axotomized and intact muscle afferents but no skin afferents develop ongoing discharges of dorsal root ganglion origin after peripheral nerve lesion. J. Neurosci. 20 (2000) 2742-2748
52. Moran M.M., Xu H., and Clapham D.E. TRP ion channels in the nervous system. Curr. Opin. Neurobiol. 14 (2004) 362-369
53. Myers R.R., Heckman H.M., and Rodriguez M. Reduced hyperalgesia in nerve-injured WLD mice: relationship to nerve fiber phagocytosis, axonal degeneration, and regeneration in normal mice. Exp. Neurol. 141 (1996) 94-101
54. Nagata K., Duggan A., Kumar G., and Garcia-Anoveros J. Nociceptor and hair cell transducer properties of TRPA1, a channel for pain and hearing. J. Neurosci. 25 (2005) 4052-4061
55. Namer B., Seifert F., Handwerker H.O., and Maihofner C. TRPA1 and TRPM8 activation in humans: effects of cinnamaldehyde and menthol. NeuroReport 16 (2005) 955-959
56. Nealen M.L., Gold M.S., Thut P.D., and Caterina M.J. TRPM8 mRNA is expressed in a subset of cold-responsive trigeminal neurons from rat. J. Neurophysiol. 90 (2003) 515-520
57. Noguchi K., Kawai Y., Fukuoka T., Senba E., and Miki K. 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
58. Obata K., Yamanaka H., Fukuoka T., Dai Y., Tokunaga A., Hashimoto N., Yoshikawa H., and Noguchi K. 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
59. Obata K., Yamanaka H., Dai Y., Tachibana T., Fukuoka T., Tokunaga A., Yoshikawa H., and Noguchi K. 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
60. Obata K., Yamanaka H., Dai Y., Mizushima T., Fukuoka T., Tokunaga A., Yoshikawa H., and Noguchi K. 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
61. Obata K., Yamanaka H., Kobayashi K., Dai Y., Mizushima T., Katsura H., Fukuoka T., Tokunaga A., and Noguchi K. Role of the MAPK activation in injured and intact primary afferent neurons for mechanical and heat hypersensitivity after spinal nerve ligation. J. Neurosci. 24 (2004) 10211-10222
62. Obata K., Yamanaka H., Dai Y., Mizushima T., Fukuoka T., Tokunaga A., and Noguchi K. Differential activation of MAPK in injured and uninjured DRG neurons following chronic constriction injury of the sciatic nerve in rats. Eur. J. Neurosci. 20 (2004) 2881-2895
63. Obata K., Katsura H., Mizushima T., Yamanaka H., Kobayashi K., Dai Y., Fukuoka T., Tokunaga A., Tominaga M., and Noguchi K. TRPA1 induced in sensory neurons contributes to cold hyperalgesia after inflammation and nerve injury. J. Clin. Invest. 115 (2005) 2393-2401
64. Obata K., Yamanaka H., Kobayashi K., Dai Y., Mizushima T., Katsura H., Fukuoka T., Tokunaga A., and Noguchi K. The effect of site and type of nerve injury on the expression of brain-derived neurotrophic factor in the dorsal root ganglion and on neuropathic pain behavior. Neuroscience 137 (2006) 961-970
65. Peier A.M., Moqrich A., Hergarden A.C., Reeve A.J., Andersson D.A., Story G.M., Earley T.J., Dragoni I., McIntyre P., Bevan S., and Patapoutian A. A TRP channel that senses cold stimuli and menthol. Cell 108 (2002) 705-715
66. Ramer M.S., French G.D., and Bisby M.A. Wallerian degeneration is required for both neuropathic pain and sympathetic sprouting into the DRG. Pain 72 (1997) 71-78
67. Reid G. ThermoTRP channels and cold sensing: what are they really up to?. Pflugers Arch. 451 (2005) 250-263
68. Saumet J.L., Chery-Croze S., and Duclaux R. Response of cat skin mechanothermal nociceptors to cold stimulation. Brain Res. Bull. 15 (1985) 529-532
69. Schafers M., Lee D.H., Brors D., Yaksh T.L., and Sorkin L.S. Increased sensitivity of injured and adjacent uninjured rat primary sensory neurons to exogenous tumor necrosis factor-alpha after spinal nerve ligation. J. Neurosci. 23 (2003) 3028-3038
70. Scholz J., and Woolf CJ. Can we conquer pain?. Nat. Neurosci. 5 (2002) 1062-1067
71. Seltzer Z., Dubner R., and Shir Y. A novel behavioral model of neuropathic pain disorders produced in rats by partial sciatic nerve injury. Pain 43 (1990) 205-218
72. Shamash S., Reichert F., and Rotshenker S. The cytokine network of Wallerian degeneration: tumor necrosis factor-alpha, interleukin-1alpha, and interleukin-1beta. J. Neurosci. 22 (2002) 3052-3060
73. Sommer C., and Schafers M. 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 (1998) 154-162
74. Story G.M., Peier A.M., Reeve A.J., Eid S.R., Mosbacher J., Hricik T.R., Earley T.J., Hergarden A.C., Andersson D.A., Hwang S.W., McIntyre P., Jegla T., Bevan S., and Patapoutian A. ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112 (2003) 819-829
75. Tamura S., Morikawa Y., and Senba E. TRPV2, a capsaicin receptor homologue, is expressed predominantly in the neurotrophin-3-dependent subpopulation of primary sensory neurons. Neuroscience 130 (2005) 223-228
76. Thut P.D., Wrigley D., and Gold M.S. Cold transduction in rat trigeminal ganglia neurons in vitro. Neuroscience 119 (2003) 1071-1083
77. Tillman D.B., Treede R.D., Meyer R.A., and Campbell J.N. Response of C fibre nociceptors in the anaesthetized monkey to heat stimuli: correlation with pain threshold in humans. J. Physiol. 485 (1995) 767-774
78. Tohda C., Sasaki M., Konemura T., Sasamura T., Itoh M., and Kuraishi Y. Axonal transport of VR1 capsaicin receptor mRNA in primary afferents and its participation in inflammation-induced increase in capsaicin sensitivity. J. Neurochem. 76 (2001) 1628-1635
79. Tominaga M., and Caterina M.J. Thermosensation and pain. J. Neurobiol. 61 (2004) 3-12
80. Tsuzuki K., Kondo E., Fukuoka T., Yi D., Tsujino H., Sakagami M., and Noguchi K. Differential regulation of P2X(3) mRNA expression by peripheral nerve injury in intact and injured neurons in the rat sensory ganglia. Pain 91 (2001) 351-360
81. Wahren L.K., Torebjork E., and Jorum E. Central suppression of cold-induced C fibre pain by myelinated fibre input. Pain 38 (1989) 313-319
82. Watkins L.R., and Maier S.F. Glia: a novel drug discovery target for clinical pain. Nat. Rev., Drug Discov. 2 (2003) 973-985
83. Winston J., Toma H., Shenoy M., and Pasricha P.J. Nerve growth factor regulates VR-1 mRNA levels in cultures of adult dorsal root ganglion neurons. Pain 89 (2001) 181-186
84. Woolf C.J., Ma Q.P., Allchorne A., and Poole S. Peripheral cell types contributing to the hyperalgesic action of nerve growth factor in inflammation. J. Neurosci. 16 (1996) 2716-2723
85. Wu G., Ringkamp M., Hartke T.V., Murinson B.B., Campbell J.N., Griffin J.W., and Meyer R.A. Early onset of spontaneous activity in uninjured C-fiber nociceptors after injury to neighboring nerve fibers. J. Neurosci. 21 (2001) RC140
86. Yamanaka H., He X., Matsumoto K., Shiosaka S., and Yoshida S. Protease M/neurosin mRNA is expressed in mature oligodendrocytes. Brain Res. Mol. Brain Res. 71 (1999) 217-224