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Participation of IL-1β in temporomandibular nociception in rats with CFA-induced inflammation

  • Ju, Jin-Sook (Department of Oral Physiology, School of Dentistry, Kyungpook National University) ;
  • Choi, Seung-Ho (Department of Oral Physiology, School of Dentistry, Kyungpook National University) ;
  • Kim, Hye-Jin (Department of Oral Physiology, School of Dentistry, Kyungpook National University) ;
  • Son, Jo-Young (Department of Oral Physiology, School of Dentistry, Kyungpook National University) ;
  • Ahn, Dong-Kuk (Department of Oral Physiology, School of Dentistry, Kyungpook National University)
  • Received : 2016.07.28
  • Accepted : 2016.08.17
  • Published : 2016.09.30

Abstract

The aim of the present study was to develop an animal model for evaluation of temporomandibular (TMJ) nociception under TMJ inflammation. We also investigated the participation of $IL-1{\beta}$ in inflammation-induced TMJ nociception. Experiments were carried out using male Sprague-Dawley rats. Intra-articular injection of 3% formalin was administered to evaluate hyperalgesia 3 days after CFA injection. Intra-articular injection of 3% formalin did not produce nociceptive behavior in normal rats. Although intra-articular injection of 3 doses of CFA produced TMJ inflammation, only 1:3 diluted CFA produced hyperalgesia when formalin was injected intra-articularly 3 days after CFA injection. Co-administration of IL-1 receptor inhibitor with formalin into the TMJ cavity 3 days after CFA injection was performed. Co-administration of IL-1 receptor inhibitor significantly inhibited formalin-induced hyperalgesia in rats with CFA-induced TMJ inflammation. These results suggested that intra-articular injection of formalin produced hyperalgesia under chronic TMJ inflammation. Moreover, $IL-1{\beta}$ plays an important role in TMJ hyperalgesia under chronic inflammation and blockade of $IL-1{\beta}$ is a potential therapeutic target for inflammatory TMJ pain.

Acknowledgement

Supported by : National Research Foundation of Korea (NRF)

References

  1. 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. 2001;94:185-191. https://doi.org/10.1016/S0304-3959(01)00357-8
  2. Ahn DK, Chae JM, Choi HS, Kyung HM, Kwon OW, Park HS, Youn DH, Bae YC. Central cyclooxygenase inhibitors reduced IL-1${\beta}$-induced hyperalgesia in temporomandibular joint of freely moving rats. Pain. 2005;117:204-213. doi: 10.1016/j.pain.2005.06.009. https://doi.org/10.1016/j.pain.2005.06.009
  3. Won KA, Kang YM, Lee MK, Park MK, Ju JS, Bae YC, Ahn DK. Participation of microglial p38 MAPK in formalininduced temporomandibular joint nociception in rats. J Orofac Pain. 2012;26:132-141.
  4. 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. 1998;18:8056-8064. https://doi.org/10.1523/JNEUROSCI.18-19-08056.1998
  5. Yu XM, Sessle BJ, Vernon H, Hu JW. Effects of inflammatory irritant application to the rat temporomandibular joint on jaw and neck muscle activity. Pain. 1995;60:143-149. https://doi.org/10.1016/0304-3959(94)00104-M
  6. Ren K. An improved method for assessing mechanical allodynia in the rat. Physiol Behav. 1999;67:711-716. https://doi.org/10.1016/S0031-9384(99)00136-5
  7. Ren K, Dubner R. Inflammatory Models of Pain and Hyperalgesia. ILAR J. 1999;40:111-118. https://doi.org/10.1093/ilar.40.3.111
  8. Miller LC, Lynch EA, Isa S, Logan JW, Dinarello CA, Steere AC. Balance of synovial fluid IL-1 beta and IL-1 receptor antagonist and recovery from Lyme arthritis. Lancet. 1993; 341:146-148. https://doi.org/10.1016/0140-6736(93)90006-3
  9. Dinarello CA. Interleukin-1, interleukin-1 receptors and interleukin-1 receptor antagonist. Int Rev Immunol. 1998;16: 457-499. doi: 10.3109/08830189809043005. https://doi.org/10.3109/08830189809043005
  10. Jouvenne P, Vannier E, Dinarello CA, Miossec P. Elevated levels of soluble interleukin-1 receptor type II and interleukin-1 receptor antagonist in patients with chronic arthritis: correlations with markers of inflammation and joint destruction. Arthritis Rheum. 1998;41:1083-1089. doi: 10.1002/1529-0131(199806)41:6<1083::AID-ART15>3.0.CO;2-9. https://doi.org/10.1002/1529-0131(199806)41:6<1083::AID-ART15>3.0.CO;2-9
  11. Alstergren P, Ernberg M, Kvarnstrim M, Kopp S. Interleukin-1 ${\beta}$ in synovial fluid from the arthritic temporomandibular joint and its relation to pain, mobility, and anterior open bite. J Oral Maxillofac Surg. 1998;56:1059-1065. https://doi.org/10.1016/S0278-2391(98)90256-7
  12. Kubota E, Imamura H, Kubota T, Shibta T, Murakami K. Interleukin 1 beta and stromelysin (MMP3) activity of synovial fluid as possible markers of osteoarthritis in the temporomandibular joint. J Oral Maxillofac Surg. 1997;55:20-27. https://doi.org/10.1016/S0278-2391(97)90438-9
  13. Arend WP, Dayer JM. Cytokines and cytokine inhibitors or antagonists in rheumatoid arthritis. Arthritis Rheum. 1990;33:305-315. https://doi.org/10.1002/art.1780330302
  14. Harada M, Takeuchi M, Fukao T, Katagiri K. A simple method for the quantitative extraction of dye extravasated into the skin. J Pharm Pharmacol. 1971;23:218-219. https://doi.org/10.1111/j.2042-7158.1971.tb08647.x
  15. Haas DA, Nakanishi O, MacMillan RE, Jordan RC, Hu JW. Development of an orofacial model of acute inflammation in the rat. Arch Oral Biol. 1992;37:417-422. https://doi.org/10.1016/0003-9969(92)90026-5
  16. Choi HS, Jung SC, Choi BJ, Ahn DK. Intra-articular injection of IL-1${\beta}$ facilitated formalin-induced temporomandibular joint pain in freely moving rats. Korean J Physiol Pharmacol. 2005;9:23-27. doi: 10.1016/j.pain.2005.06.009. https://doi.org/10.1016/j.pain.2005.06.009
  17. Lee MK, Choi BY, Yang GY, Jeon HJ, Kyung HM, Kwon OW, Park HS, Bae YC, Mokha SS, Ahn DK. Low doses of cannabinoids enhance the antinociceptive effects of intracisternally administered mGluRs groups II and III agonists in formalin-induced TMJ nociception in rats. Pain. 2008;139:367-375. doi: 10.1016/j.pain.2008.05.005. https://doi.org/10.1016/j.pain.2008.05.005
  18. 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. 2003;27:613-618. doi: 10.1016/S0278-5846(03)00049-6. https://doi.org/10.1016/S0278-5846(03)00049-6
  19. Won KA, Lim NH, Lee MK, Park MK, Yang GY, Park YY, Ahn DK, Bae YC. A blockade of central MAPK pathway attenuates referred pain in rats with complete Freund's adjuvant-induced inflammation of the temporomandibular joint. Int J Oral Biol. 2010;35:83-89.
  20. McNeill C. Management of temporomandibular disorders: concepts and controversies. J Prosthet Dent. 1997;77:510-522. https://doi.org/10.1016/S0022-3913(97)70145-8
  21. Yatani H, Studts J, Cordova M, Carlson CR, Okeson JP. Comparison of sleep quality and clinical and psychologic characteristics in patients with temporomandibular disorders. J Orofac Pain. 2002;16:221-228.
  22. Oral K, Bal Kucuk B, Ebeoglu B, Dincer S. Etiology of temporomandibular disorder pain. Agri. 2009;21:89-94.
  23. Harper RP, Kerins CA, McIntosh JE, Spears R, Bellinger LL. Modulation of the inflammatory response in the rat TMJ with increasing doses of complete Freund's adjuvant. Osteoarthritis Cartilage. 2001;9:619-624. doi: 10.1053/joca.2001.0461. https://doi.org/10.1053/joca.2001.0461
  24. 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 temporomandibular joint and perioral inflammation. J Neurophysiol. 1999;82:1244-1253. https://doi.org/10.1152/jn.1999.82.3.1244
  25. 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. 1999;412:276-291. https://doi.org/10.1002/(SICI)1096-9861(19990920)412:2<276::AID-CNE7>3.0.CO;2-9
  26. 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. 2002;957:338-344. https://doi.org/10.1016/S0006-8993(02)03671-5
  27. Nordahl S, Alstergren P, Appelgren A, Appelgren B, Eliasson S, Kopp S. Pain, tenderness, mandibular mobility, and anterior open bite in relation to radiographic erosions in temporomandibular joint disease. Acta Odontol Scand. 1997;55:18-22. https://doi.org/10.3109/00016359709091935
  28. Dreier R, Grӓssel S, Fuchs S, Schaumburger J, Bruckner P. Pro-MMP-9 is a specific macrophage product and is activated by osteoarthritic chondrocytes via MMP-3 or a MT1-MMP/MMP-13 cascade. Exp Cell Res. 2004;297:303-312. doi: 10.1016/j.yexcr.2004.02.027. https://doi.org/10.1016/j.yexcr.2004.02.027
  29. Borsiczky B, Szabo Z, Jaberansari MT, Mack PP, Roth E. Activated PMNs lead to oxidative stress on chondrocytes. A study of swine knees. Acta Orthop Scand. 2003;74:190-195. doi: 10.1080/00016470310013941. https://doi.org/10.1080/00016470310013941
  30. Chin JE, Winterrowd GE, Krzesicki RF, Sanders ME. Role of cytokines in inflammatory synovitis. The coordinate regulation of intercellular adhesion molecule 1 and HLA class I and class II antigens in rheumatoid synovial fibroblasts. Arthritis Rheum. 1990;33:1776-1786. https://doi.org/10.1002/art.1780331204
  31. Steiner G, Tohidast-Akrad M, Witzmann G, Vesely M, Studnicka-Benke A, Gal A, Kunaver M, Zenz P, Smolen JS. Cytokine production by synovial T cells in rheumatoid arthritis. Rheumatology. 1999;38:202-213. https://doi.org/10.1093/rheumatology/38.3.202
  32. Tominaga K, Alstergren P, Kurita H, Matsukawa A, Fukuda J, Kopp S. Interleukin-1${\beta}$ in antigen-induced arthritis of the rabbit temporomandibular joint. Arch Oral Biol. 2001;46:539-544. https://doi.org/10.1016/S0003-9969(01)00009-7
  33. Harper RP, Kerins CA, McIntosh JE, Spears R, Bellinger LL. Modulation of the inflammatory response in the rat TMJ with increasing doses of complete Freund's adjuvant. Osteoarthritis Cartilage. 2001;9:619-624. doi: 10.1053/joca.2001.0461. https://doi.org/10.1053/joca.2001.0461
  34. Spears R, Dees LA, Sapozhnikov M, Bellinger LL, Hutchins B. Temporal changes in inflammatory mediator concentrations in an adjuvant model of temporomandibular joint inflammation. J Orofac Pain. 2005;19:34-40.
  35. Nordahl S, Alstergren P, Eliasson S, Kopp S. Interleukin-1${\beta}$ in plasma and synovial fluid in relation to radiographic changes in arthritic temporomandibular joints. Eur J Oral Sci. 1998;106:559-563. https://doi.org/10.1046/j.0909-8836.1998.eos106104.x
  36. Takahashi T, Kondoh T, Fukuda M, Yamazaki Y, Toyosaki T, Suzuki R. Proinflammatory cytokines detectable in synovial fluids from patients with temporomandibular disorders. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 1998;85:135-141. https://doi.org/10.1016/S1079-2104(98)90415-2
  37. Ferreira SH, Lorenzetti BB, Bristow AF, Poole S. Interleukin-1 ${\beta}$ as a potent hyperalgesic agent antagonized by a tripeptide analogue. Nature. 1988;334:698-700. doi: 10.1038/334698a0. https://doi.org/10.1038/334698a0
  38. Maier SF, Wiertelak EP, Martin D, Watkins LR. Interleukin-1 mediates the behavioral hyperalgesia produced by lithium chloride and endotoxin. Brain Res. 1993;623:321-324. https://doi.org/10.1016/0006-8993(93)91446-Y
  39. Watkins LR, Wiertelak EP, Goehler LE, Smith KP, Martin D, Maier SF. Characterization of cytokine-induced hyperalgesia. Brain Res. 1994;654:15-26. https://doi.org/10.1016/0006-8993(94)91566-0
  40. Safieh-Garabedian B, Poole S, Allchorne A, Winter J, Woolf CJ. Contribution of interleukin-1${\beta}$ to the inflammationinduced increase in nerve growth factor levels and inflammatory hyperalgesia. Br J Pharmacol. 1995;115: 1265-1275. https://doi.org/10.1111/j.1476-5381.1995.tb15035.x
  41. Ahn DK, Jung CY, Lee HJ, Choi HS, Ju JS, Bae YC. Peripheral glutamate receptors participate in interleukin-1${\beta}$-induced mechanical allodynia in the orofacial area of rats. Neurosci Lett. 2004;357:203-206. doi: 10.1016/j.neulet.2003.12.097. https://doi.org/10.1016/j.neulet.2003.12.097