Peripheral and central mechanisms of trigeminal neuropathic and inflammatory pain

Journal of Oral Biosciences

Volumn 53, Issue 4, 2011, Pages 318-329

  Takeda, Mamoru ^a   Matsumoto, Shigeji ^a   Sessle, Barry J ^b   Shinoda, Masamichi ^c   Iwata, Koichi ^c  

^a NIPPON DENTAL UNIVERSITY   (Japan)

^b UNIVERSITY OF TORONTO   (Canada)

^c NIHON UNIVERSITY   (Japan)

Author keywords

Astroglia; Pathological pain; Satellite glial cells; Trigeminal ganglion neurons; Trigeminal spinal nucleus caudalis

Indexed keywords

EID: 84255205025     PISSN: 13490079     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1349-0079(11)80025-3     Document Type: Review

References (84)

1. Cao, H. and Zhang, Y. Q. Spinal glial activation contributes to pathological pain states. Neurosci. Biobehav. Rev. 32: 972-983, 2008.
2. Scholz, J. and Woolf, C. J. Can we conquer pain? Nat. Neurosci. 5 Suppl 1062-1067, 2002. (Pubitemid 35247200)
3. Garry, M. G. and Hargreaves, K. M. Enhanced release of immunoreactive CGRP and substance P from spinal dorsal horn slices occurs during carrageenan inflammation. Brain Res. 582: 139-142, 1992.
4. Bereiter, D. A. and Benetti, A. P. Excitatory amino release within spinal trigeminal nucleus after mustard oil injection into the temporomandibular joint region of the rat. Pain 67: 451-459, 1996. (Pubitemid 26376765)
5. Carleson, J., Alstergren, P., Appelgren, A., Appelgren, B., Kopp, S., Theodorsson, E. and Lundeberg, T. A model for experimental induction of acute temporomandibular joint inflammation in rats: effects of substance P (SP) on neuropeptide-like immunoreactivity. Life Sci. 59: 1193-1201, 1996. (Pubitemid 26322916)
6. Dubner, R. and Ruda, M. A. Activity-dependent neuronal plasticity following tissue injury and inflammation. Trends Neurosci. 15: 96-103, 1992.
7. Coderre, T. J., Katz, J., Vaccarino, A. L. and Melzack, R. Contribution of central neuroplasticity to pathological pain: review of clinical and experimental evidence. Pain 52: 259-285, 1993. (Pubitemid 23080546)
8. Zhou, Q., Imbe, H., Dubner, R. and Ren, K. Persistent Fos protein expression after orofacial deep or cutaneous tissue inflammation in rats: implications for persistent orofacial pain. J. Comp. Neurol. 412 276-291, 1999. (Pubitemid 29395365)
9. Millan, M. J. The induction of pain: an integrative review. Prog. Neurobiol. 571-164, 1999.
10. Watkins, L. R., Martin, D., Ulrich, P., Tracey, K. J. and Maier, S. F. Evidence for the involvement of spinal cord glia in subcutaneous formalin induced hyperalgesia in the rat. Pain 71: 225-235, 1997. (Pubitemid 27288136)
11. Watkins, L. R., Milligan, E. D. and Maier, S. F. Glial activation: a driving force for pathological pain. Trends Neurosci. 24: 450-455, 2001. (Pubitemid 32695356)
12. Ren, K. and Dubner, R. Neuron-glia crosstalk gets serious: role in pain hypersensitivity. Curr. Opin. Anaesthesiol. 21: 570-579, 2008.
13. Hanani, M. Satellite glial cells in sensory ganglia from form to function. Brain Res. Rev. 48: 457-476, 2005. (Pubitemid 40725401)
14. Orkand, R. K., Nicholls, J. G. and Kuffler, S. W. Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia. J. Neurophysiol. 29: 788-806, 1966.
15. +siphoning. Science 225: 1174-1175, 1984. (Pubitemid 14029102)
16. Vit, J. P., Ohara, P. T., Bhargava, A., Kelley, K. and Jasmin, L. Silencing the Kir4. 1 potassium channel subunit in satellite glial cells of the rat trigeminal ganglion results in pain-like behavior in the absence of nerve injury. J. Neurosci. 28: 4161-4171, 2008.
17. Takeda, M., Takahashi, M. and Matsumoto, S. Contribution of the activation of satellite glia in sensory ganglia to pathological pain. Neurosci. Biobehav. Rev. 33: 784-792, 2009.
18. Cheng, J. K. and Ji, R. R. Intracellular signaling in primary sensory neurons and persistent pain. Neurochem. Res. 33: 1970-1978, 2008.
19. Gold, M. S. and Gebhart, G. F. Nociceptor sensitization in pain pathogenesis. Nat. Med. 16: 1248-1257, 2010.
20. Catterall, W. A., Perez-Reyes, E., Snutch, T. P. and Striessnig, J. International Union of Pharmacology. XLVIII. Nomenclature and structure-function relationships of voltage-gated calcium channels. Pharmacol. Rev. 57: 411-425, 2005. (Pubitemid 43036432)
21. Jevtovic-Todorovic, V. and Todorovic, S. M. The role of peripheral T-type calcium channels in pain transmission. Cell Calcium. 40: 197-203, 2006. (Pubitemid 43942301)
22. Hucho, T. and Levine, J. D. Signaling pathways in sensitization : toward a nociceptor cell biology. Neuron 55: 365-376, 2007. (Pubitemid 47126268)
23. Petho, G., Derow, A. and Reeh, P. W. Bradykinininduced nociceptor sensitization to heat is mediated by cyclooxygenase products in isolated rat skin. Eur. J. Neurosci. 14: 210-218, 2001. (Pubitemid 32777629)
24. +currents involves activation of both EP2 and EP4 receptors in neonatal rat nodose ganglion neurones. Br. J. Pharmacol. 145: 503-513, 2005. (Pubitemid 40966280)
25. Kadoi, J., Takeda, M. and Matsumoto, S. Prostaglandin E2 potentiates the excitability of small diameter trigeminal root ganglion neurons projecting onto the superficial layer of the cervical dorsal horn in rats. Exp. Brain Res. 176: 227-236, 2007. (Pubitemid 44837098)
26. Tsutsui, Y., Ikeda, M., Takeda, M. and Matsumoto, S. Excitability of small-diameter trigeminal ganglion neurons by 5-HT is mediated by enhancement of the tetrodotoxin-resistant sodium current due to the activation of 5-HT4 receptors and/or by the inhibition of the transient potassium current. Neuroscience 157: 683-696, 2008.
27. Yoshimura, N. and de Groat, W. C. Increased excitability of afferent neurons innervating rat urinary bladder after chronic bladder inflammation. J. Neurosci. 19: 4644-4653, 1999. (Pubitemid 29241112)
28. Moore, B. A., Stewart, T. M., Hill, C. and Vanner, S. J. TNBS ileitis evokes hyperexcitability and changes in ionic membrane properties of nociceptive DRG neurons. Am. J. Physiol. Gastrointest. Liver Physiol. 282: G1045-1051, 2002. (Pubitemid 34651611)
29. Stewart, T., Beyak, M. J. and Vanner, S. Ileitis modulates potassium and sodium currents in guinea pig dorsal root ganglia sensory neurons. J. Physiol. 552 797-807, 2003. (Pubitemid 37428421)
30. Dang, K., Bielefeldt, K. and Gebhart, G. F. Gastric ulcers reduce A-type potassium currents in rat gastric sensory ganglion neurons. Am. J. Physiol. Gastrointest. Liver Physiol. 286: G573-579, 2004. (Pubitemid 38374976)
31. Beyak, M. J. and Vanner, S. Inflammation-induced hyperexcitability of nociceptive gastrointestinal DRG neuronesthe role of voltage-gated ion channels. Neurogastroenterol. Motil. 17: 175-186, 2005. (Pubitemid 40476677)
32. Morgan, J. R. and Gebhart, G. F. Characterization of a model of chronic orofacial hyperalgesia in the rat contribution of NA V 1. 8. J. Pain. 9: 522-531, 2008.
33. Flake, N. M. and Gold, M. S. Inflammation alters sodium currents and excitability of temporomandibular joint afferents. Neurosci. Lett. 384: 294-299, 2005. (Pubitemid 40836017)
34. Takeda, M., Tanimoto, T., Ikeda, M., Nasu, M., Kadoi, J., Yoshida, S. and Matsumoto, S. Enhanced excitability of rat trigeminal root ganglion neurons via decrease in A-type potassium currents following temporomandibular joint inflammation. Neuroscience 138: 621-630, 2006. (Pubitemid 43255570)
35. Everill, B. and Kocsis, J. D. Reduction in potassium currents in identified cutaneous afferent dorsal root ganglion neurons after axotomy. J. Neurophysiol. 82 700-708, 1999. (Pubitemid 29387844)
36. Takeda, M., Tsuboi, Y., Kitagawa, J., Nakagawa, K., Iwata, K. and Matsumoto, S. Potassium channels as a potential therapeutic target for trigeminal neuropathic and inflammatory pain. Mol. Pain. 75, 2011.
37. Chaplan, S. R., Guo, H. Q., Lee, D. H., Luo, L., Liu, C., Kuei, C., Velumian, A. A., Butler, M. P., Brown, S. M. and Dubin, A. E. Neuronal hyperpolarization-activated pacemaker channels drive neuropathic pain. J. Neurosci. 23: 1169-1178, 2003. (Pubitemid 36258896)
38. Yao, H., Donnelly, D. F., Ma, C. and LaMotte, R. H. Upregulation of the hyperpolarization-activated cation current after chronic compression of the dorsal root ganglion. J. Neurosci. 23: 2069-2074, 2003. (Pubitemid 36368894)
39. Tsuboi, Y., Takeda, M., Tanimoto, T., Ikeda, M., Matsumoto, S., Kitagawa, J., Teramoto, K., Simizu, K., Yamazaki, Y., Shima, A., Ren, K. and Iwata, K. Alteration of the second branch of the trigeminal nerve activity following inferior alveolar nerve transection in rats. Pain 111: 323-334, 2004. (Pubitemid 39201154)
40. Kitagawa, J., Takeda, M., Suzuki, I., Kadoi, J., Tsuboi, Y., Honda, K., Matsumoto, S., Nakagawa, H., Tanabe, A. and Iwata, K. Mechanisms involved in modulation of trigeminal primary afferent activity in rats with peripheral mononeuropathy. Eur. J. Neurosci. 24:1976-1986, 2006. (Pubitemid 44583481)
41. Cho, H. J., Staikopoulos, V., Furness, J. B. and Jennings, E. A. Inflammation-induced increase in hyperpolarization-activated, cyclic nucleotide-gated channel protein in trigeminal ganglion neurons and the effect of buprenorphine. Neuroscience 162: 453-461, 2009.
42. Lee, D. H., Chang, L., Sorkin, L. S. and Chaplan, S. R. Hyperpolarization-activated, cation-nonselective, cyclic nucleotide-modulated channel blockade alleviates mechanical allodynia and suppresses ectopic discharge in spinal nerve ligated rats. J. Pain. 6: 417-424, 2005. (Pubitemid 40922692)
43. 2+ channels in trigeminal ganglion neurons from neonatal rats. Life Sci. 73: 1175-1187, 2003. (Pubitemid 36724918)
44. Borgland, S. L., Connor, M., Ryan, R. M., Ball, H. J. and Christie, M. J. Prostaglandin E2 inhibits calcium current in two sub-populations of acutely isolated mouse trigeminal sensory neurons. J. Physiol. 539: 433-444, 2002. (Pubitemid 35175399)
45. Hingtgen, C. M. and Vasko, M. R. Prostacyclin enhances the evoked-release of substance P and calcitonin gene-related peptide from rat sensory neurons. Brain Res. 655: 51-60, 1994. (Pubitemid 24262991)
46. Hingtgen, C. M., Waite, K. J. and Vasko, M. R. Prostaglandins facilitate peptide release from rat sensory neurons by activating the adenosine 3, 5-cyclic monophosphate transduction cascade. J. Neurosci. 15: 5411-5419, 1995.
47. Woolf, C. J. and Ma, Q. Nociceptors: noxious stimulus detectors. Neuron 55353-364, 2007.
48. Takeda, M., Tanimoto, T., Ikeda, M., Kadoi, J. and Matsumoto, S. Activaton of GABAB receptor inhibits the excitability of rat small diameter trigeminal root ganglion neurons. Neuroscience 123: 491-505, 2004. (Pubitemid 38032925)
49. Takeda, M., Kadoi, J., Takahashi, M., Nasu, M. and Matsumoto, S. Somatostatin inhibits the excitability of rat small-diameter trigeminal ganglion neurons that innervate nasal mucosa and project to the upper cervical dorsal horn via activation of somatostatin 2a receptor. Neuroscience 148: 744-756, 2007. (Pubitemid 47418376)
50. Takeda, M., Tanimoto, T., Ikeda, M., Kadoi, J., Nasu, M. and Matsumoto, S. Opioidergic modulation of excitability of rat trigeminal root ganglion neuron projections to the superficial layer of cervical dorsal horn. Neuroscience 125: 995-1008, 2004. (Pubitemid 38553906)
51. Takeda, M., Tanimoto, T., Ikeda, M., Nasu, M., Kadoi, J., Shima, Y., Ohta, H. and Matsumoto, S. Temporomandibular joint inflammation potentiates the excitability of trigeminal root ganglion neurons innervating the facial skin in rats. J. Neurophysiol. 93: 2723-2738, 2005. (Pubitemid 40570852)
52. Safieh-Garabedian, B., Poole, S., Allchorne, A., Winter, J. and Woolf, C. J. Contribution of interleukin-1 beta to the inflammation-induced increase in nerve growth factor levels and inflammatory hyperalgesia. Br. J. Pharmacol. 115: 1265-1275, 1995.
53. Stephenson, J. L. and Byers, M. R. GFAP immunoreactivity in trigeminal ganglion satellite cells after tooth injury in rats. Exp. Neurol. 131: 11-22, 1995.
54. Cherkas, P. S., Huang, T. Y., Pannicke, T., Tal, M., Reichenbach, A. and Hanani, M. The effects of axotomy on neurons and satellite glial cells in mouse trigeminal ganglion. Pain 110: 290-298, 2004. (Pubitemid 38953294)
55. Dray, A. Inflammatory mediators of pain. Br. J. Anaesth. 75: 125-131, 1995.
56. Bianchi, M., Dib, B. and Panerai, A. E. Interleukin-1 and nociception in the rat. J. Neurosci. Res. 53 645-650, 1998. (Pubitemid 28423872)
57. Wolf, G., Yirmiya, R., Goshen, I., Iverfeldt, K., Holmlund, L., Takeda, K. and Shavit, Y. Impairment of interleukin-1IL-1 signaling reduces basal pain sensitivity in micegenetic, pharmacological and developmental aspects. Pain 104: 471-480, 2003. (Pubitemid 37289046)
58. Hashizume, H., DeLeo, J. A., Colburn, R. W. and Weinstein, J. N. Spinal glial activation and cytokine expression after lumbar root injury in the rat. Spine Phila Pa 1976. 25: 1206-1217, 2000.
59. Shi, L., Smolders, I., Umbrain, V., Lauwers, M. H., Sarre, S., Michotte, Y., Zizi, M. and Camu, F. Peripheral inflammation modifies the effect of intrathecal IL-1beta on spinal PGE2 production mainly through cyclooxygenase-2 activity. A spinal microdialysis study in freely moving rats. Pain 120: 307-314, 2006. (Pubitemid 43172865)
60. Marriott, I. The role of tachykinins in central nervous system inflammatory responses. Front Biosci. 9: 2153-2165, 2004.
61. Martin, F. C., Charles, A. C., Sanderson, M. J. and Merrill, J. E. Substance P stimulates IL-1 production by astrocytes via intracellular calcium. Brain Res. 599: 13-18, 1992. (Pubitemid 23024911)
62. Martin, F. C., Anton, P. A., Gornbein, J. A., Shanahan, F. and Merrill, J. E. Production of interleukin-1 by microglia in response to substance Prole for a nonclassical NK-1 receptor. J. Neuroimmunol. 42: 53-60, 1993. (Pubitemid 23025192)
63. Wienrich, M. and Kettenmann, H. Activation of substance P receptors leads to membrane potential responses in cultured astrocytes. Glia 2: 155-160, 1989.
64. Takeda, M., Tanimoto, T., Kadoi, J., Nasu, M., Takahashi, M., Kitagawa, J. and Matsumoto, S. Enhanced excitability of nociceptive trigeminal ganglion neurons by satellite glial cytokine following peripheral inflammation. Pain 129: 155-166, 2007. (Pubitemid 46551374)
65. Takeda, M., Kitagawa, J., Takahashi, M. and Matsumoto, S. Activation of interleukin-1beta receptor suppresses the voltage-gated potassium currents in the small-diameter trigeminal ganglion neurons following peripheral inflammation. Pain 139: 594-602, 2008.
66. Takeda, M., Tanimoto, T., Nasu, M., Ikeda, M., Kadoi, J. and Matsumoto, S. Activation of NK1 receptor of trigeminal root ganglion via substance P paracrine mechanism contributes to the mechanical allodynia in the temporomandibular joint inflammation in rats. Pain 116: 375-385, 2005. (Pubitemid 40957142)
67. Liu, L., Yang, T. M., Liedtke, W. and Simon, S. A. Chronic IL-1beta signaling potentiates voltagedependent sodium currents in trigeminal nociceptive neurons. J. Neurophysiol. 95: 1478-1490, 2006.
68. Takeda, M., Takahashi, M. and Matsumoto, S. Contribution of activated interleukin receptors in trigeminal ganglion neurons to hyperalgesia via satellite glial interleukin-1beta paracrine mechanism. Brain. Behav. Immun. 22: 1016-1023, 2008.
69. Sessle, B. J. Peripheral and central mechanisms of orofacial pain and their clinical correlates. Minerva Anestesiol. 71: 117-136, 2005. (Pubitemid 43932943)
70. Gobel, S. Golgi studies of the neurons in layer II of the dorsal horn of the medulla (trigeminal nucleus caudalis). J. Comp. Neurol. 180: 395-413, 1978. (Pubitemid 8345063)
71. Iwata, K., Fukuoka, T., Kondo, E., Tsuboi, Y., Tashiro, A., Noguchi, K., Masuda, Y., Morimoto, T. and Kanda, K. Plastic changes in nociceptive transmission of the rat spinal cord with advancing age. J. Neurophysiol. 87: 1086-1093, 2002. (Pubitemid 34670870)
72. Watkins, L. R. and Maier, S. F. Gliaa novel drug discovery target for clinical pain. Nat. Rev. Drug. Discov. 2: 973-985, 2003. (Pubitemid 37540579)
73. Ji, R. R. and Strichartz, G. Cell signaling and the genesis of neuropathic pain. Sci. STKE. 2004 reE14, 2004.
74. Ji, R. R. Mitogen-activated protein kinases as potential targets for pain killers. Curr. Opin. Invest. Drugs. 5: 71-75, 2004.
75. Tsuda, M., Inoue, K. and Salter, M. W. Neuropathic pain and spinal microgliaa big problem from molecules in "small" glia. Trends Neurosci. 28: 101-107, 2005. (Pubitemid 40178927)
76. Piao, Z. G., Cho, I. H., Park, C. K., Hong, J. P., Choi, S. Y., Lee, S. J., Lee, S., Park, K., Kim, J. S. and Oh, S. B. Activation of glia and microglial p38 MAPK in medullary dorsal horn contributes to tactile hypersensitivity following trigeminal sensory nerve injury. Pain 121: 219-231, 2006.
77. Chiang, C. Y., Wang, J., Xie, Y. F., Zhang, S., Hu, J. W., Dostrovsky, J. O. and Sessle, B. J. Astroglial glutamate- glutamine shuttle is involved in central sensitization of nociceptive neurons in rat medullary dorsal horn. J. Neurosci. 27: 9068-9076, 2007. (Pubitemid 47312060)
78. Chiang, C. Y., Li, Z., Dostrovsky, J. O., Hu, J. W. and Sessle, B. J. Glutamine uptake contributes to central sensitization in the medullary dorsal horn. Neuroreport 19: 1151-1154, 2008.
79. Xie, Y. F., Zhang, S., Chiang, C. Y., Hu, J. W., Dostrovsky, J. O. and Sessle, B. J. Involvement of glia in central sensitization in trigeminal subnucleus caudalis medullary dorsal horn . Brain Behav. Immun. 21: 634-641, 2007. (Pubitemid 46829766)
80. Wei, F., Guo, W., Zou, S., Ren, K. and Dubner, R. Supraspinal glial-neuronal interactions contribute to descending pain facilitation. J. Neurosci. 28: 10482-10495, 2008.
81. Okada-Ogawa, A., Suzuki, I., Sessle, B. J., Chiang, C. Y., Salter, M. W., Dostrovsky, J. O., Tsuboi, Y., Kondo, M., Kitagawa, J., Kobayashi, A., Noma, N., Imamura, Y. and Iwata, K. Astroglia in medullary dorsal horn trigeminal spinal subnucleus caudalis are involved in trigeminal neuropathic pain mechanisms. J. Neurosci. 29: 11161-11171, 2009.
82. Iwata, K., Imai, T., Tsuboi, Y., Tashiro, A., Ogawa, A., Morimoto, T., Masuda, Y., Tachibana, Y. and Hu, J. Alteration of medullary dorsal horn neuronal activity following inferior alveolar nerve transection in rats. J. Neurophysiol. 86: 2868-2877, 2001. (Pubitemid 33139054)
83. Ren, K. Emerging role of astroglia in pain hypersensitivity. Jpn. Dent. Sci. Rev. 4686, 2009.
84. Svensson, CI. and Broden, E. Spinal astrocytes in Pain processing: Non-neuronal cells as therapeutic targets. Mol. Interv. 10: 25-38, 2010.