Cold receptors in the DRG: Basic science and clinical implications

Reviews in Analgesia

Volumn 9, Issue 1, 2006, Pages 31-44

  Obata, Koichi ^a   Kobayashi, Kimiko ^a   Fukuoka, Tetsuo ^a   Noguchi, Koichi ^a  

^a HYOGO COLLEGE OF MEDICINE   (Japan)

Author keywords

Hyperalgesia; NGF; Noxious cold; Primary afferent neurons; TRPA1; TRPM8

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; TRANSIENT RECEPTOR POTENTIAL CATION CHANNEL A1; TRANSIENT RECEPTOR POTENTIAL CHANNEL; TRANSIENT RECEPTOR POTENTIAL CHANNEL M; TRANSIENT RECEPTOR POTENTIAL CHANNEL M8; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1;

CELL SUBPOPULATION; CHRONIC PAIN; COLD SENSITIVITY; ENZYME ACTIVATION; HISTOCHEMISTRY; IN SITU HYBRIDIZATION; INFLAMMATION; KNOCKOUT GENE; MOLECULAR CLONING; NERVE CONDUCTION; NERVE INJURY; NOCICEPTIVE STIMULATION; NONHUMAN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REVIEW; SENSORY NERVE CELL; SPINAL GANGLION;

EID: 33845938447     PISSN: 1542961X     EISSN: 15553876     Source Type: Journal    
DOI: 10.3727/000000006783992871     Document Type: Review

References (96)

1. Ali, Z.; Ringkamp, M.; Hartke, T. V.; Chien, H. F.; Flavahan, N. A.; Campbell, J. N.; Meyer, R. A. Uninjured C-fiber nociceptors develop spontaneous activity and alpha-adrenergic sensitivity following L6 spinal nerve ligation in monkey. J. Neurophysiol. 81:455-466; 1999.
2. Askwith, C. C.; Benson, C. J.; Welsh, M. J.; Snyder, P. M. DEG/ENaC ion channels involved in sensory transduction are modulated by cold temperature. Proc. Natl. Acad. Sci. USA 98:6459-6463; 2001.
3. Babes, A.; Zorzon, D.; Reid, G. Two populations of cold-sensitive neurons in rat dorsal root ganglia and their modulation by nerve growth factor. Eur. J. Neurosci. 20:2276-2282; 2004.
4. Bandell, M.; Story, G. M.; Hwang, S. W.; Viswanath, V.; Eid, S. R.; Petrus, M. J.; Earley, T. J.; Patapoutian, A. Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin. Neuron 41:849-857; 2004.
5. Bautista, D. M.; Movahed, P.; Hinman, A.; Axelsson, H. E.; Sterner, O.; Hogestatt, E. D.; Julius, D.; Jordt, S. E.; Zygmunt, P. M. Pungent products from garlic activate the sensory ion channel TRPA1. Proc. Natl. Acad. Sci. USA 102:12248-12252; 2005.
6. Bautista, D. M.; Jordt, S. E.; Nikai, T.; Tsuruda, P. R.; Read, A. J.; Poblete, J.; Yamoah, E. N.; Basbaum, A. I.; Julius, D. TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 124:1269-1282; 2006.
7. Choi, Y.; Yoon, Y. W.; Na, H. S.; Kim, S. H.; Chung, J. M. Behavioral signs of ongoing pain and cold allodynia in a rat model of neuropathic pain. Pain 59:369-376; 1994.
8. Clapham, D. E. TRP channels as cellular sensors. Nature 426:517-524; 2003.
9. Corey, D. P.; Garcia-Anoveros, J.; Holt, J. R.; Kwan, K. Y.; Lin, S. Y.; Vollrath, M. A.; Amalfitano, A.; Cheung, E. L.; Derfler, B. H.; Duggan, A.; Geleoc, G. S.; Gray, P. A.; Hoffman, M. P.; Rehm, H. L.; Tamasauskas, D.; Zhang, D. S. TRPA1 is a candidate for the mechanosensitive transduction channel of vertebrate hair cells. Nature 432:723-730; 2004.
10. Cui, J. G.; Holmin, S.; Mathiesen, T.; Meyerson, B. A.; Linderoth, B. Possible role of inflammatory mediators in tactile hypersensitivity in rat models of mononeuropathy. Pain 88:239-248; 2000.
11. Dai, Y.; Iwata, K.; Fukuoka, T.; Kondo, E.; Tokunaga, A.; Yamanaka, H.; Tachibana, T.; Liu, Y.; Noguchi, K. Phosphorylation of extracellular signal-regulated kinase in primary afferent neurons by noxious stimuli and its involvement in peripheral sensitization. J. Neurosci. 22:7737-7745; 2002.
12. Dai, Y.; Fukuoka, T.; Wang, H.; Yamanaka, H.; Obata, K.; Tokunaga, A.; Noguchi, K. Contribution of sensitized P2X receptors in inflamed tissue to the mechanical hypersensitivity revealed by phosphorylated ERK in DRG neurons. Pain 108:258-266; 2004.
13. Devor, M. Neuropathic pain and injured nerve: Peripheral mechanisms. Br. Med. Bull. 47:619-630; 1991.
14. Devor, M.; Seltzer, Z. Pathophysiology of damaged nerves in reaction to chronic pain. In: Wall, P. D.; Melzack, R., eds. Textbook of pain. London: Churchill Livingstone; 1999:129-164.
15. Djouhri, L.; Wrigley, D.; Thut, P. D.; Gold, M. S. Spinal nerve injury increases the percentage of cold-responsive DRG neurons. Neuroreport 15:457-460; 2004.
16. Eschenfelder, S.; Habler, H. J.; Janig, W. Dorsal root section elicits signs of neuropathic pain rather than reversing them in rats with L5 spinal nerve injury. Pain 87:213-219; 2000.
17. Fukuoka, T.; Tokunaga, A.; Kondo, E.; Miki, K.; Tachibana, T.; 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 78:13-26; 1998.
18. Fukuoka, T.; Kondo, E.; Dai, Y.; Hashimoto, N.; Noguchi, K. Brain-derived neurotrophic factor increases in the uninjured dorsal root ganglion neurons in selective spinal nerve ligation model. J. Neurosci. 21:4891-4900; 2001.
19. Fukuoka, T.; Noguchi, K. Contribution of the spared primary afferent neurons to the pathomechanisms of neuropathic pain. Mol. Neurobiol. 26:57-67; 2002.
20. Gillespie, P. G.; Dumont, R. A.; Kachar, B. Have we found the tip link, transduction channel, and gating spring of the hair cell? Curr. Opin. Neurobiol. 15:389-396; 2005.
21. Gold, M. S. Spinal nerve ligation: What to blame for the pain and why. Pain 84:117-120; 2000.
22. Kama, A. T. Capsaicin-sensitive primary afferents mediate responses to cold in rats with a peripheral mononeuropathy. Neuroreport 13:461-464; 2002.
23. Hao, J. X.; Yu, W.; Xu, X. J.; Wiesenfeld-Hallin, Z. Capsaicin-sensitive afferents mediate chronic cold, but not mechanical, allodynia-like behavior in spinally injured rats. Brain Res. 722:177-180; 1996.
24. Harrison, J. L.; Davis, K. D. Cold-evoked pain varies with skin type and cooling rate: A psychophysical study in humans. Pain 83:123-135; 1999.
25. Jahanshahi, M.; Pitt, P.; Williams, I. Pain avoidance in rheumatoid arthritis. J. Psychosom. Res. 33:579-589; 1989.
26. Jasmin, L.; Kohan, L.; Franssen, M.; Janni, G.; 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 75:367-382; 1998.
27. Ji, R. R.; Samad, T. A.; Jin, S. X.; Schmoll, R.; Woolf, C. J. p38 MAPK activation by NGF in primary sensory neurons after inflammation increases TRPV1 levels and maintains heat hyperalgesia. Neuron 36:57-68; 2002.
28. Ji, R. R. Mitogen-activated protein kinases as potential targets for pain killers. Curr. Opin. Invest. Drugs 5:71-75; 2004.
29. Jordt, S. E.; McKemy, D. D.; Julius, D. Lessons from peppers and peppermint: The molecular logic of thermosensation. Curr. Opin. Neurobiol. 13:487-492; 2003.
30. Jordt, S. E.; Bautista, D. M.; Chuang, H. H.; McKemy, D. D.; Zygmunt, P. M.; Hogestatt, E. D.; Meng, I. D.; Julius, D. Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427:260-265; 2004.
31. Katsura, H.; Obata, K.; Mizushima, T.; Yamanaka, H.; Kobayashi, K.; Dai, Y.; Fukuoka, T.; Tokunaga, A.; Sakagami, M.; Noguchi, K. Antisense knock down of TRPA1, but not TRPM8, alleviates cold hyperalgesia after spinal nerve ligation in rats. Exp. Neurol. 200:112-123; 2006.
32. Kobayashi, K.; Fukuoka, T.; Obata, K.; Yamanaka, H.; Dai, Y.; Tokunaga, A.; 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. 493:596-606; 2005.
33. Koltzenburg, M.; Torebjork, H. E.; Wahren, L. K. Nociceptor modulated central sensitization causes mechanical hyperalgesia in acute chemogenic and chronic neuropathic pain. Brain 117:579-591; 1994.
34. Kress, M.; Koltzenburg, M.; Reeh, P. W.; Handwerker, H. O. Responsiveness and functional attributes of electrically localized terminals of cutaneous C-fibers in vivo and in vitro. J. Neurophysiol. 68:581-595; 1992.
35. Kwan, K. Y.; Allchorne, A. J.; Vollrath, M. A.; Christensen, A. P.; Zhang, D. S.; Woolf, C. J.; Corey, D. P. TRPA1 contributes to cold, mechanical, and chemical nociception but is not essential for hair-cell transduction. Neuron 50:277-289; 2006.
36. LaMotte, R. H.; Thalhammer, J. G. Response properties of high-threshold cutaneous cold receptors in the primate. Brain Res. 244:279-287; 1982.
37. Leem, J. W.; Willis, W. D.; Chung, J. M. Cutaneous sensory receptors in the rat foot. J. Neurophysiol. 69:1684-1699; 1993.
38. Lewin, G. R.; Mendell, L. M. Nerve growth factor and nociception. Trends Neurosci. 16:353-359; 1993.
39. Li, L.; Xian, C. J.; Zhong, J. H.; Zhou, X. F. Lumbar 5 ventral root transection-induced upregulation of nerve growth factor in sensory neurons and their target tissues: A mechanism in neuropathic pain. Mol. Cell. Neurosci. 23:232-250; 2003.
40. Li, Y.; Dorsi, M. J.; Meyer, R. A.; Belzberg, A. J. Mechanical hyperalgesia after an L5 spinal nerve lesion in the rat is not dependent on input from injured nerve fibers. Pain 85:493-502; 2000.
41. Ma, C.; Shu, Y.; Zheng, Z.; Chen, Y.; Yao, H.; Greenquist, K. W.; White, F. A.; LaMotte, R. H. Similar electrophysiological changes in axotomized and neighboring
42. intact dorsal root ganglion neurons. J. Neurophysiol. 89:1588-1602; 2003.
43. Macpherson, L. J.; Geierstanger, B. H.; Viswanath, V.; Bandell, M.; Eid, S. R.; Hwang, S.; Patapoutian, A. The pungency of garlic: Activation of TRPA1 and TRPV1 in response to allicin. Curr. Biol. 15:929-934; 2005.
44. Marchand, F.; Perretti, M.; McMahon, S. B. Role of the immune system in chronic pain. Nat. Rev. Neurosci. 6: 521-532; 2005.
45. McKemy, D. D.; Neuhausser, W. M.; Julius, D. Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416:52-58; 2002.
46. McKemy, D. D. How cold is it? TRPM8 and TRPA1 in the molecular logic of cold sensation. Mol. Pain 1:16; 2005.
47. Mizushima, T.; Obata, K.; Yamanaka, H.; Dai, Y.; Fukuoka, T.; Tokunaga, A.; Mashimo, T.; Noguchi, K. Activation of p38 MAPK in primary afferent neurons by noxious stimulation and its involvement in the development of thermal hyperalgesia. Pain 113:51-60; 2005.
48. Mizushima, T.; Obata, K.; Katsura, H.; Yamanaka, H.; Kobayashi, K.; Dai, Y.; Fukuoka, T.; Tokunaga, A.; Mashimo, T.; Noguchi, K. Noxious cold stimulation induces MAPK activation in TRPA1-and TRPM8-containing small sensory neurons. Neuroscience 140:1337-1348; 2006.
49. Moran, M. M.; Xu, H.; Clapham, D. E. TRP ion channels in the nervous system. Curr. Opin. Neurobiol. 14:362-369; 2004.
50. Myers, R. R.; Heckman, H. M.; Rodriguez, M. Reduced hyperalgesia in nerve-injured WLD mice: Relationship to nerve fiber phagocytosis, axonal degeneration, and regeneration in normal mice. Exp. Neurol. 141:94-101; 1996.
51. Nagata, K.; Duggan, A.; Kumar, G.; Garcia-Anoveros, J. Nociceptor and hair cell transducer properties of TRPA1, a channel for pain and hearing. J. Neurosci. 25:4052-4061; 2005.
52. Nealen, M. L.; Gold, M. S.; Thut, P. D.; Caterina, M. J. TRPM8 mRNA is expressed in a subset of cold-responsive trigeminal neurons from rat. J. Neurophysiol. 90:515-520; 2003.
53. Obata, K.; Noguchi, K. MAPK activation in nociceptive neurons and pain hypersensitivity. Life Sci. 74:2643-2653; 2004.
54. Obata, K.; Yamanaka, H.; Kobayashi, K.; Dai, Y.; Mizushima, T.; Katsura, H.; Fukuoka, T.; Tokunaga, A.; 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. 24:10211-10222; 2004.
55. Obata, K.; Katsura, H.; Mizushima, T.; Yamanaka, H.; Kobayashi, K.; Dai, Y.; Fukuoka, T.; Tokunaga, A.; Tominaga, M.; Noguchi, K. TRPA1 induced in sensory neurons contributes to cold hyperalgesia after inflammation and nerve injury. J. Clin. Invest. 115:2393-2401; 2005.
56. Obata, K.; Noguchi, K. BDNF in sensory neurons and chronic pain. Neurosci. Res. 55:1-10; 2006.
57. Park, C. K.; Kim, M. S.; Fang, Z.; Li, H. Y.: Jung, S. J.;
58. Choi, S. Y.; Lee, S. J.; Park, K.; Kim, J. S.; Oh, S. B. Functional expression of thermo-transient receptor potential channels in dental primary afferent neurons: Implication for tooth pain. J. Biol. Chem. 281:17304-17311; 2006.
59. Patapoutian, A.; Peier, A. M.; Story, G. M.; Viswanath, V. ThermoTRP channels and beyond: Mechanisms of temperature sensation. Nat. Rev. Neurosci. 4:529-539; 2003.
60. Patapoutian, A. TRP channels and thermosensation. Chem. Senses 30(Suppl. 1):i193-i194; 2005.
61. Peier, A. M.; Moqrich, A.; Hergarden, A. C.; Reeve, A. J.; Andersson, D. A.; Story, G. M.; Barley, T. J.; Dragoni, I.; McIntyre, P.; Bevan, S.; Patapoutian, A. A TRP channel that senses cold stimuli and menthol. Cell 108:705-715; 2002.
62. Perrot, S.; Altal, N.; Ardid, D.; Guilbaud, G. Are mechanical and cold allodynia in mononeuropathic and arthritic rats relieved by systemic treatment with calcitonin or guanethidine? Pain 52:41-47; 1993.
63. Pezet, S.; Malcangio, M.; McMahon, S. B. BDNF: A neuromodulator in nociceptive pathways? Brain Res. Brain Res. Rev. 40:240-249; 2002.
64. Puntambekar, P.; Mukherjea, D.; Jajoo, S.; Ramkumar, V. Essential role of Rac1/NADPH oxidase in nerve growth factor induction of TRPV1 expression. J. Neurochem. 95:1689-1703; 2005.
65. Ramer, M. S.; French, G. D.; Bisby, M. A. Wallerian degeneration is required for both neuropathic pain and sympathetic sprouting into the DRG. Pain 72:71-78; 1997.
66. Rashid, M. H.; Inoue, M.; Matsumoto, M.; Ueda, H. Switching of bradykinin-mediated nociception following partial sciatic nerve injury in mice. J. Pharmacol. Exp. Ther. 308:1158-1164; 2004.
67. Reid, G.; Flonta, M. L. Physiology. Cold current in thermoreceptive neurons. Nature 413:480; 2001.
68. Reid, G.; Flonta, M. L. Cold transduction by inhibition of a background potassium conductance in rat primary sensory neurones. Neurosci. Lett. 297:171-174; 2001.
69. Reid, G.; Babes, A.; Pluteanu, F. A cold- and menthol-activated current in rat dorsal root ganglion neurones: Properties and role in cold transduction. J. Physiol. 545:595-614; 2002.
70. Reid, G. ThermoTRP channels and cold sensing: what are they really up to? Pflugers Arch. 451:250-263; 2005.
71. Ringkamp, M.; Meyer, R. A. Injured versus uninjured afferents: Who is to blame for neuropathic pain? Anesthesiology 103:221-223; 2005.
72. Ro, L. S.; Chen, S. T.; Tang, L. M.; Jacobs, J. M. Effect of NGF and anti-NGF on neuropathic pain in rats following chronic constriction injury of the sciatic nerve. Pain 79:265-274; 1999.
73. Sah, D. W.; Ossipov, M. H.; Porreca, F. Neurotrophic factors as novel therapeutics for neuropathic pain. Nat. Rev. Drug Discov. 2:460-472; 2003.
74. Saumet, J. L.; Chery-Croze, S.; Duclaux, R. Response of cat skin mechanothermal nociceptors to cold stimulation. Brain Res. Bull. 15:529-532; 1985.
75. Schafers, M.; Lee, D. H.; Brors, D.; Yaksh, T. L.; Sorkin,
76. S. Increased sensitivity of injured and adjacent uninjured rat primary sensory neurons to exogenous tumor necrosis factor-alpha after spinal nerve ligation. J. Neurosci. 23:3028-3038; 2003.
77. Scholz, J.; Woolf, C. J. Can we conquer pain? Nat. Neurosci. 5(Suppl.):1062-1067; 2002.
78. Seino, D.; Tokunaga, A.; Tachibana, T.; Yoshiya, S.; Dai, Y.; Obata, K.; Yamanaka, H.; Kobayashi, K.; Noguchi, K. The role of ERK signaling and the P2X receptor on mechanical pain evoked by movement of inflamed knee joint. Pain 123:193-203; 2006.
79. Shamash, S.; Reichert, F.; Rotshenker, S. The cytokine network of Wallerian degeneration: Tumor necrosis factor-alpha, interleukin-1alpha, and interleukin-1beta. J. Neurosci. 22:3052-3060; 2002.
80. Sommer, C.; 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. 784:154-162; 1998.
81. Story, G. M.; Peier, A. M.; Reeve, A. J.; Eid, S. R.; Mosbacher, J.; Hricik, T. R.; Barley, T. J.; Hergarden, A. C.; Andersson, D. A.; Hwang, S. W.; McIntyre, P.; Jegla, T.; Sevan, S.; Patapoutian, A. ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112:819-829; 2003.
82. Suto, K.; Gotoh, H. Calcium signaling in cold cells studied in cultured dorsal root ganglion neurons. Neuroscience 92:1131-1135; 1999.
83. Tanga, F. Y.; Nutile-McMenemy, N.; DeLeo, J. A. The CNS role of Toll-like receptor 4 in innate neuroimmunity and painful neuropathy. Proc. Natl. Acad. Sci. USA 102:5856-5861; 2005.
84. Tillman, D. B.; Treede, R. D.; Meyer, R. A.; Campbell, J. N. Response of C fibre nociceptors in the anaesthetized monkey to heat stimuli: Correlation with pain threshold in humans. J. Physiol. 485:767-774; 1995.
85. Tohda, C.; Sasaki, M.; Konemura, T.; Sasamura, T.; Itoh, M.; Kuraishi, Y. Axonal transport of VR1 capsaicin receptor mRNA in primary afferents and its participation in inflammation-induced increase in capsaicin sensitivity. J. Neurochem. 76:1628-1635; 2001.
86. Tominaga, M.; Caterina, M. J. Thermosensation and pain. J. Neurobiol. 61:3-12; 2004.
87. Tsuda, M.; Shigemoto-Mogami, Y.; Koizumi, S.; Mizokoshi, A.; Kohsaka, S.; Salter, M. W.; Inoue, K. P2X4 receptors induced in spinal microglia gate tactile allodynia after nerve injury. Nature 424:778-783; 2003.
88. Tsuda, M.; Inoue, K.; Salter, M. W. Neuropathic pain and spinal microglia: A big problem from molecules in "small" glia. Trends Neurosci. 28:101-107; 2005.
89. Viana, F.; de la Pena, E.; Belmonte, C. Specificity of cold thermotransduction is determined by differential ionic channel expression. Nat. Neurosci. 5:254-260; 2002.
90. Wahren, L. K.; Torebjork, E.; Jorum, E. Central suppression of cold-induced C fibre pain by myelinated fibre input. Pain 38:313-319; 1989.
91. Wang, H.; Woolf, C. J. Pain TRPs. Neuron 46:9-12; 2005.
92. Watkins, L. R.; Maier, S. F. Glia: A novel drug discovery target for clinical pain. Nat. Rev. Drug Discov. 2:973-985; 2003.
93. Woolf, C. J.; Ma, Q. P.; Allchorne, A.; Poole, S. Peripheral cell types contributing to the hyperalgesic action of nerve growth factor in inflammation. J. Neurosci. 16:2716-2723; 1996.
94. Woolf, C. J.; Salter, M. W. Neuronal plasticity: Increasing the gain in pain. Science 288:1765-1769; 2000.
95. Wu, G.; Ringkamp, M.; Hartke, T. V.; Murinson, B. B.; Campbell, J. N.; Griffin, J. W.; Meyer, R. A. Early onset of spontaneous activity in uninjured C-fiber nociceptors after injury to neighboring nerve fibers. J. Neurosci. 21:RC140; 2001.
96. Xu, H.; Delling, M.; Jun, J. C.; Clapham, D. E. Oregano, thyme and clove-derived flavors and skin sensitizers activate specific TRP channels. Nat. Neurosci. 9:628-635; 2006.