Participation of NMDA and non-NMDA glutamate receptors in the formalin-induced inflammatory temporomandibular joint nociception

  • Yang, Gwi-Y. (Department of Oral Physiology, School of Dentistry, Kyungpook National University) ;
  • Lee, Ju-H. (Department of Oral Physiology, School of Dentistry, Kyungpook National University) ;
  • Ahn, Dong-K. (Department of Oral Physiology, School of Dentistry, Kyungpook National University)
  • Published : 2007.06.30

Abstract

It has been well known that excitatory amino acids, primarily glutamate, are involved in the transmission of nociception in pathological and physiological conditions in the spinal and brainstem level. Recently, peripheral glutamate also play a critical role in the peripheral nociceptive transmissions. The present study investigated the role of N-methyl-D-aspartic acid (NMDA) or non-NMDA ionotropic glutamate receptors in formalin-induced TMJ pain. Experiments were carried out on male Sprague-Dawley rats weighing 220-280 g. Intra-articular injection was performed under halothane anesthesia. Under anesthesia, AP-7 (10, $100\;{\mu}M$, $1\;mM/20\;{\mu}L$), a NMDA receptor antagonist, or CNQX disodium salt (0.5, 5, 50, $500\;{\mu}M/20\;{\mu}L$), a non-NMDA receptor antagonist, were administered intra-articularly 10 min prior to the application of 5% formalin. For each animal, the number of behavioral responses, such as rubbing and/or scratching the TMJ region, was recorded for nine successive 5-min intervals. Intra-articular pretreatment with 1 mM of AP-7 or $50\;{\mu}M$ CNQX significantly decreased the formalin-induced scratching behavioral responses during the second phase. Intra-articular pretreatment with $500\;{\mu}M$ of CNQX significantly decreased the formalin-induced scratching behavior during both the first and the second phase. These results indicate that the intra-articular administration of NMDA or non-NMDA receptor antagonists inhibit formalin-induced TMJ nociception, and peripheral ionotropic glutamate receptors may play an important role in the TMJ nociception.

Keywords

References

  1. Ahn, DK., Chae, JM., Choi, HS., Kyung, HM., Kwon, OW., Park, HS., Youn, DH., Bae, YC.: Central cyclooxygenase inhibitors reduced IL-1beta-induced hyperalgesia in temporomandibular joint of freely moving rats. Pain. 117:204-213, 2005 https://doi.org/10.1016/j.pain.2005.06.009
  2. Ahn, DK., Choi, HS., Yeo, SP., Woo, YW., Lee, MK., Yang, GY., Jeon, HJ., Park, JS., Mokha, SS.: Blockade of central cyclooxygenase (COX) pathways enhances the cannabinoid -induced antinociceptive effects on inflammatory temporomandibular joint (TMJ) nociception. Pain. 2007 Epub ahead Feb/22 in press
  3. Ahn, DK., Jung, CY., Lee, HJ., Choi, HS., Ju, JS., Bae, YC.: Peripheral glutamate receptors participate in interleukin- 1beta-induced mechanical allodynia in the orofacial area of rats. Neurosci Lett. 357:203-206, 2004 https://doi.org/10.1016/j.neulet.2003.12.097
  4. Beirith, A., Santos, AR., Calixto, JB.: Mechanisms underlying the nociception and paw oedema caused by injection of glutamate into the mouse paw. Brain Res. 924:219-228, 2002 https://doi.org/10.1016/S0006-8993(01)03240-1
  5. Cairns, BE., Gambarota, G., Svensson, P., Arendt-Nielsen, L., Berde, CB.: Glutamate-induced sensitization of rat masseter muscle fibers. Neuroscience. 109:389-399, 2002a https://doi.org/10.1016/S0306-4522(01)00489-4
  6. Cairns, BE., Sessle, BJ., Hu, JW.: Evidence that excitatory amino acid receptors within the temporomandibular joint region are involved in the reflex activation of the jaw muscles. J Neurosci. 18:8056-8064, 1998 https://doi.org/10.1523/JNEUROSCI.18-19-08056.1998
  7. Cairns, BE., Sim, Y., Bereiter, DA., Sessle, BJ., Hu, JW.: Influence of sex on reflex jaw muscle activity evoked from the rat temporomandibular joint. Brain Res. 957:338-344, 2002b https://doi.org/10.1016/S0006-8993(02)03671-5
  8. Cairns, BE., Svensson, P., Wang, K., Hupfeld, S., Graven- Nielsen, T., Sessle, BJ., Berde, CB., Arendt-Nielsen, L.: Activation of peripheral NMDA receptors contributes to human pain and rat afferent discharges evoked by injection of glutamate into the masseter muscle. J Neurophysiol. 90:2098-2105, 2003 https://doi.org/10.1152/jn.00353.2003
  9. Carlton, SM., Hargett, GL., Coggeshall, RE.: Localization and activation of glutamate receptors in unmyelinated axons of rat glabrous skin. Neurosci. Lett. 197: 25-28, 1995 https://doi.org/10.1016/0304-3940(95)11889-5
  10. Castillo, PE., Malenka, RC., Nicoll, RA.: Kainate receptors mediate a slow postsynaptic current in hippocampal CA3 neurons. Nature. 388:182-186, 1997 https://doi.org/10.1038/40645
  11. Choi, HS., Jung, SC., Choi, BJ., Ahn, DK.: Intra-articular injection of IL-1a facilitated formalin-induced temporomandibular joint pain in freely moving rats. Korea J Physiol Pharmacol. 9: 23-27, 2005
  12. Choi, HS., Ju, JS., Lee, HJ., Jung, CY., Kim, BC., Park, JS., Ahn, DK.: Effects of TNF-alpha injected intracisternally on the nociceptive jaw-opening reflex and orofacial formalin test in freely moving rats. Prog Neuropsychopharmacol Biol Psychiatry. 27:613-618, 2003a
  13. Choi, HS., Ju, JS., Lee, HJ., Kim, BC., Park, JS., Ahn, DK.: Effects of intracisternal injection of interleukin-6 on nociceptive jaw opening reflex and orofacial formalin test in freely moving rats. Brain Res Bull. 59:365-370, 2003b https://doi.org/10.1016/S0361-9230(02)00931-0
  14. Choi, HS., Lee, HJ., Jung, CY., Ju, JS., Park, JS., Ahn, DK.: Central cyclooxygenase-2 participates in interleukin-1 betainduced hyperalgesia in the orofacial formalin test of freely moving rats. Neurosci Lett. 352:187-190, 2003c https://doi.org/10.1016/j.neulet.2003.08.065
  15. Clavelou, P., Dallel, R., Orliaguet, T., Woda, A., Raboisson, P.: The orofacial formalin test in rats: effects of different formalin concentrations. Pain. 62:295-301, 1995 https://doi.org/10.1016/0304-3959(94)00273-H
  16. Clavelou, , P.: AP., Pajot, J., Dallel, R., Raboissonpplication of the formalin test to the study of orofacial pain in the rat. Neurosci Lett. 103:349-53, 1989 https://doi.org/10.1016/0304-3940(89)90125-0
  17. Clements, JR., Magnusson, KR., Hautman, J., Beitz, AJ.: Rat tooth pulp projections to spinal trigeminal subnucleus caudalis are glutamate-like immunoreactive. J Comp Neurol. 309:281-288, 1991 https://doi.org/10.1002/cne.903090209
  18. Coderre, TJ., Katz, J., Vaccarino, AL., Melzack, R.: Contribution of central neuroplasticity to pathological pain: review of clinical and experimental evidence. Pain. 52:259-285, 1993 https://doi.org/10.1016/0304-3959(93)90161-H
  19. Coderre, TJ., Melzack, R.: The contribution of excitatory amino acids to central sensitization and persistent nociception after formalin-induced tissue injury. J Neurosci. 12:3665- 3670, 1992 https://doi.org/10.1523/JNEUROSCI.12-09-03665.1992
  20. Coggeshall, RE., Carlton, SM.: Ultrastructural analysis of NMDA, AMPA, and kainate receptors on unmyelinated and myelinated axons in the periphery. J. Comp. Neurol. 391:78- 86, 1998 https://doi.org/10.1002/(SICI)1096-9861(19980202)391:1<78::AID-CNE7>3.0.CO;2-O
  21. deGroot, J., Zhou, S., Carlton, SM.: Peripheral glutamate release in the hindpaw following low and high intensity sciatic stimulation. Neuroreport. 11:497-502, 2000 https://doi.org/10.1097/00001756-200002280-00014
  22. Dickenson, AH., Chapman, V., Green, GM.: The pharmacology of excitatory and inhibitory amino acid-mediated events in the transmission and modulation of pain in the spinal cord. Gen Pharmacol. 28:633-638, 1997 https://doi.org/10.1016/S0306-3623(96)00359-X
  23. Dingledine, R., Borges, K., Bowie, D., Traynelis, SF.: The glutamate receptor ion channels. Pharmacol Rev. 51:7-61, 1999
  24. Fisher, K., Lefebvre, C., Coderre, TJ.: Antinociceptive effects following intrathecal pretreatment with selective metabotropic glutamate receptor compounds in a rat model of neuropathic pain. Pharmacol Biochem Behav. 73:411-418, 2002 https://doi.org/10.1016/S0091-3057(02)00832-8
  25. Gerber, G., Cerne, R., Randic, M.: Participation of excitatory amino acid receptors in the slow excitatory synaptic transmission in rat spinal dorsal horn. Brain Res. 561:236-251, 1991 https://doi.org/10.1016/0006-8993(91)91600-6
  26. Haas, DA., Nakanishi, O., MacMillan, RE., Jordan, RC., Hu, JW.: Development of an orofacial model of acute inflammation in the rat. Arch Oral Biol. 37:417-422, 1992 https://doi.org/10.1016/0003-9969(92)90026-5
  27. Harada, M., Takeuchi, M., Fukao, T., Katagiri, K.: A simple method for the quantitative extraction of dye extravasated into the skin. J Pharm Pharmacol. 23:218-219, 1971 https://doi.org/10.1111/j.2042-7158.1971.tb08647.x
  28. Hollmann, M., Heinemann, S.: Cloned glutamate receptors. Annu Rev Neurosci. 17:31-108, 1994 https://doi.org/10.1146/annurev.ne.17.030194.000335
  29. Iwata, K., Tashiro, A., Tsuboi, Y., Imai, T., Sumino, R., Morimoto, T., Dubner, R., Ren, K.: Medullary dorsal horn neuronal activity in rats with persistent temporomaridibular joint and perioral inflammation. J Neurophysiol. 82:1244-1253, 1999 https://doi.org/10.1152/jn.1999.82.3.1244
  30. Jackson, DL., Graff, CB., Richardson, JD., Hargreaves, KM.: Glutamate participates in the peripheral modulation of thermal hyperalgesia in rats. Eur J Pharmacol. 284:321-325, 1995 https://doi.org/10.1016/0014-2999(95)00449-U
  31. Jang, JH., Kim, DW., Sang NAM, T., Se Paik, K., Leem, JW.: Peripheral glutamate receptors contribute to mechanical hyperalgesia in a neuropathic pain model of the rat. Neuroscience. 128:169-176, 2004 https://doi.org/10.1016/j.neuroscience.2004.06.040
  32. Lam, DK., Sessle, BJ., Cairns, BE., Hu, JW.: Peripheral NMDA receptor modulation of jaw muscle electromyographic activity induced by capsaicin injection into the temporomandibular joint of rats. Brain Res. 1046:68-76, 2005 https://doi.org/10.1016/j.brainres.2005.03.040
  33. Lawand, NB., McNearney, T., Westlund, KN.: Amino acid release into the knee joint: key role in nociception and inflammation. Pain. 86:69-74, 2000 https://doi.org/10.1016/S0304-3959(99)00311-5
  34. Lawand, NB., Willis, WD., Westlund, KN.: Excitatory amino acid receptor involvement in peripheral nociceptive transmission in rats. Eur J Pharmacol. 324:169-177, 1997 https://doi.org/10.1016/S0014-2999(97)00072-1
  35. Lerma, J.: Roles and rules of kainate receptors in synaptic transmission. Nat Rev Neurosci. 4:481-495, 2003 https://doi.org/10.1038/nrn1118
  36. Mao, J., Price, DD., Hayes, RL., Lu, J., Mayer, DJ., Frenk, H.: Intrathecal treatment with dextrorphan or ketamine potently reduces pain-related behaviors in a rat model of peripheral mononeuropathy. Brain Res. 605:164-168, 1993 https://doi.org/10.1016/0006-8993(93)91368-3
  37. Monaghan, DT., Bridges, RJ., Cotman, CW.: The excitatory amino acid receptors: their classes, pharmacology, and distinct properties in the function of the central nervous system. Annu Rev Pharmacol Toxicol. 29:365-402, 1989 https://doi.org/10.1146/annurev.pa.29.040189.002053
  38. Omote, K., Kawamata, T., Kawamata, M., Namiki, A.: Formalininduced release of excitatory amino acids in the skin of the rat hindpaw. Brain Res. 787:161-164, 1998 https://doi.org/10.1016/S0006-8993(97)01568-0
  39. Ro, JY.: Contribution of peripheral NMDA receptors in craniofacial muscle nociception and edema formation. Brain Res. 979:78-84, 2003 https://doi.org/10.1016/S0006-8993(03)02873-7
  40. Roveroni, RC., Parada, CA., Cecilia, M., Veiga, FA., Tambeli, CH.: Development of a behavioral model of TMJ pain in rats: the TMJ formalin test. Pain. 94:185-191, 2001 https://doi.org/10.1016/S0304-3959(01)00357-8
  41. Seltzer, Z., Cohn, S., Ginzburg, R., Beilin, B.: Modulation of neuropathic pain behavior in rats by spinal disinhibition and NMDA receptor blockade of injury discharge. Pain. 45:69- 75, 1991 https://doi.org/10.1016/0304-3959(91)90166-U
  42. Shigemoto, R., Ohishi, H., Nakanishi, S., Mizuno, N.: Expression of the mRNA for the rat NMDA receptor (NMDAR1) in the sensory and autonomic ganglion neurons. Neurosci Lett. 144:229-232, 1992 https://doi.org/10.1016/0304-3940(92)90756-W
  43. Song, I., Huganir, RL.: Regulation of AMPA receptors during synaptic plasticity. Trends Neurosci. 25:578-588, 2002 https://doi.org/10.1016/S0166-2236(02)02270-1
  44. Tang, ML., Hass, DA., Hu, JW.: Capsaicin-induced joint inflammation is not blocked by local anesthesia. Anesth Prog. 51:2-9, 2004
  45. Vignes, M., Collingridge, GL.: The synaptic activation of kainate receptors. Nature. 388:179-182, 1997 https://doi.org/10.1038/40639
  46. Wang, C., Wang, Y., Zhao, Z.: Peripheral NMDA and non- NMDA receptors contribute to nociception: an electrophysiological study. Brain Res Bull. 52:31-34, 2000 https://doi.org/10.1016/S0361-9230(99)00277-4
  47. Watkins, JC., Evans, RH.: Excitatory amino acid transmitters. Annu Rev Pharmacol Toxicol. 21:165-204, 1981 https://doi.org/10.1146/annurev.pa.21.040181.001121
  48. Watkins, JC., Krogsgaard-Larsen, P., Honore, T.: Structureactivity relationships in the development of excitatory amino acid receptor agonists and competitive antagonists. Trends Pharmacol Sci. 11:25-33, 1990 https://doi.org/10.1016/0165-6147(90)90038-A
  49. Yoshimura, M., Yonehara, N.: Alteration in sensitivity of ionotropic glutamate receptors and tachykinin receptors in spinal cord contribute to development and maintenance of nerve injury-evoked neuropathic pain. Neurosci Res. 56:21- 28, 2006 https://doi.org/10.1016/j.neures.2006.04.015
  50. Yu, XM., Sessle, BJ., Haas, DA., Izzo, A., Vernon, H., Hu, JW.: Involvement of NMDA receptor mechanisms in jaw electromyographic activity and plasma extravasation induced by inflammatory irritant application to temporomandibular joint region of rats. Pain. 68:169-178, 1996 https://doi.org/10.1016/S0304-3959(96)03181-8
  51. Zhang, GH., Min, SS., Lee, KS., Back, SK., Yoon, SJ., Yoon, YW., Kim, YI., Na, HS., Hong, SK., Han, HC.: Intraarticular pretreatment with ketamine and memantine could prevent arthritic pain: relevance to the decrease of spinal c-fos expression in rats. Anesth Analg. 99:152-158, 2004 https://doi.org/10.1213/01.ANE.0000117141.76392.65
  52. Zhou, S., Bonasera, L., Carlton, SM.: Peripheral administration of NMDA, AMPA or KA results in pain behaviors in rats. Neuroreport. 7:895-900, 1996 https://doi.org/10.1097/00001756-199603220-00012
  53. Zhou, Q., Imbe, H., Dubner, R., 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 https://doi.org/10.1002/(SICI)1096-9861(19990920)412:2<276::AID-CNE7>3.0.CO;2-9