Table of Contents Author Guidelines Submit a Manuscript
Table of Contents Alerts

To receive news and publication updates for BioMed Research International, enter your email address in the box below.

Journal of Biomedicine and Biotechnology
Volume 2011, Article ID 707985, 11 pages
http://dx.doi.org/10.1155/2011/707985
Research Article

Experimental Model of Zymosan-Induced Arthritis in the Rat Temporomandibular Joint: Role of Nitric Oxide and Neutrophils

Hellíada Vasconcelos Chaves,1,2 Ronaldo de Albuquerque Ribeiro,3 André Mattos Brito de Souza,3 Antonio Alfredo Rodrigues e Silva,1 Antoniella Souza Gomes,3 Mariana Lima Vale,3 Mirna Marques Bezerra,2 and Gerly Anne de Castro Brito4

1Faculty of Dentistry, Federal University of Ceará, Sobral Campus, Avenida Comandante Maurocélio Rocha Pontes, 100 Derby, 62042-280 Sobral, CE, Brazil
2Faculty of Medicine of Sobral , Federal University of Ceará, Sobral Campus, Avenida Comandante Maurocélio Rocha Pontes, 100 Derby, 62042-280 Sobral, CE, Brazil
3Department of Physiology and Pharmacology, Faculty of Medicine, Federal University of Ceará, Rua Coronel Nunes Valente, 1315 Rodolfo Teófilo, 60430-270 Fortaleza, CE, Brazil
4Department of Morphology, Faculty of Medicine, Federal University of Ceará, Rua Delmiro de Farias, Porangabussu, 60440-261 Fortaleza, CE, Brazil

Received 15 September 2010; Revised 2 December 2010; Accepted 9 December 2010

Academic Editor: Oreste Gualillo

Copyright © 2011 Hellíada Vasconcelos Chaves et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. B. E. Cairns, “Pathophysiology of TMD pain—basic mechanisms and their implications for pharmacotherapy,” Journal of Oral Rehabilitation, vol. 37, no. 6, pp. 391–410, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  2. J. G. Broton and B. J. Sessle, “Reflex excitation of masticatory muscles induced by algesic chemicals applied to the temporomandibular joint of the cat,” Archives of Oral Biology, vol. 33, no. 10, pp. 741–747, 1988. View at Google Scholar · View at Scopus
  3. D. A. Haas, O. Nakanishi, R. E. MacMillan, R. C. Jordan, and J. W. Hu, “Development of an orofacial model of acute inflammation in the rat,” Archives of Oral Biology, vol. 37, no. 5, pp. 417–422, 1992. View at Publisher · View at Google Scholar · View at Scopus
  4. X. M. Yu, B. J. Sessle, H. Vernon, and J. W. Hu, “Effects of inflammatory irritant application to the rat temporomandibular joint on jaw and neck muscle activity,” Pain, vol. 60, no. 2, pp. 143–149, 1995. View at Publisher · View at Google Scholar · View at Scopus
  5. J. Carleson, P. Alstergren, A. Appelgren, B. Appelgren, S. Kopp, E. Theodorsson, and T. Lundeberg, “A model for experimental induction of acute temporomandibular joint inflammation in rats: effects of substance P(SP) on neuropeptide-like immunoreactivity,” Life Sciences, vol. 59, no. 15, pp. 1193–1201, 1996. View at Publisher · View at Google Scholar · View at Scopus
  6. J. Carleson, P. Alstergren, and P. Alstergren, “Effects of adjuvant on neuropeptide-like immunoreactivity in experimentally induced temporomandibular arthritis in rats,” Archives of Oral Biology, vol. 41, no. 7, pp. 705–712, 1996. View at Publisher · View at Google Scholar · View at Scopus
  7. J. Carleson, P. Alstergren, A. Appelgren, B. Appelgren, S. Kopp, E. Theodorsson, and T. Lundeberg, “A model for the study of experimentally induced temporomandibular arthritis in rats: the effect of human recombinant interleukin-1α on neuropeptide-like immunoreactivity,” Journal of Orofacial Pain, vol. 10, no. 1, pp. 9–14, 1996. View at Google Scholar · View at Scopus
  8. Y. Kowai, E. Kubota, and E. Okabe, “Reactive oxygen species participation in experimentally induced arthritis of the temporomandibular joint in rats,” Journal of Dental Research, vol. 79, no. 7, pp. 1489–1495, 2000. View at Google Scholar · View at Scopus
  9. P. M. Fiorentino, B. E. Cairns, and J. W. Hu, “Development of inflammation after application of mustard oil or glutamate to the rat temporomandibular joint,” Archives of Oral Biology, vol. 44, no. 1, pp. 27–32, 1999. View at Publisher · View at Google Scholar · View at Scopus
  10. K. Tominaga, P. Alstergren, H. Kurita, and S. Kopp, “Clinical course of an antigen-induced arthritis model in the rabbit temporomandibular joint,” Journal of Oral Pathology and Medicine, vol. 28, no. 6, pp. 268–273, 1999. View at Google Scholar · View at Scopus
  11. K. Ren, “An improved method for assessing mechanical allodynia in the rat,” Physiology and Behavior, vol. 67, no. 5, pp. 711–716, 1999. View at Publisher · View at Google Scholar · View at Scopus
  12. R. P. Harper, C. A. Kerins, and C. A. Kerins, “Meal pattern analysis in response to temporomandibular joint inflammation in the rat,” Journal of Dental Research, vol. 79, no. 9, pp. 1704–1711, 2000. View at Google Scholar · View at Scopus
  13. R. C. Roveroni, C. A. Parada, M. Cecília, F. A. Veiga, and C. H. Tambeli, “Development of a behavioral model of TMJ pain in rats: the TMJ formalin test,” Pain, vol. 94, no. 2, pp. 185–191, 2001. View at Publisher · View at Google Scholar · View at Scopus
  14. M. L. Tang, D. A. Haas, and J. W. Hu, “Capsaicin-induced joint inflammation is not blocked by local anesthesia,” Anesthesia Progress, vol. 51, no. 1, pp. 2–9, 2004. View at Google Scholar · View at Scopus
  15. T. Lundeberg, P. Alstergren, A. Appelgren, B. Appelgren, J. Carleson, S. Kopp, and E. Theodorsson, “A model for experimentally induced temperomandibular joint arthritis in rats: effects of carrageenan on neuropeptide-like immunoreactivity,” Neuropeptides, vol. 30, no. 1, pp. 37–41, 1996. View at Publisher · View at Google Scholar · View at Scopus
  16. Y. Takeuchi, J. L. Zeredo, R. Fujiyama, T. Amagasa, and K. Toda, “Effects of experimentally induced inflammation on temporomandibular joint nociceptors in rats,” Neuroscience Letters, vol. 354, no. 2, pp. 172–174, 2004. View at Publisher · View at Google Scholar · View at Scopus
  17. A. Denadai-Souza, L. D. L. Camargo, M. T. C. P. Ribela, J. E. Keeble, S. K. P. Costa, and M. N. Muscará, “Participation of peripheral tachykinin NK receptors in the carrageenan-induced inflammation of the rat temporomandibular joint,” European Journal of Pain, vol. 13, no. 8, pp. 812–819, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  18. E. C. Keystone, H. U. Schorlemmer, C. Pope, and A. C. Allison, “Zymosan-induced arthritis: a model of chronic proliferative arthritis following activation of the alternative pathway of complement,” Arthritis and Rheumatism, vol. 20, no. 7, pp. 1396–1401, 1977. View at Google Scholar · View at Scopus
  19. P. Gegout, P. Gillet, D. Chevrier, C. Guingamp, B. Terlain, and P. Netter, “Charactertzation of zymosan-induced arthritis in the rat: effects on joint inflammation and cartilage metabolism,” Life Sciences, vol. 55, no. 17, pp. 321–326, 1994. View at Publisher · View at Google Scholar
  20. F. A. C. Rocha, A. G. M. Aragao Jr., R. C. Oliveira, M. M. L. Pompeu, M. R. Vale, and R. A. Ribeiro, “Periarthritis promotes gait disturbance in zymosan-induced arthritis in rats,” Inflammation Research, vol. 48, no. 9, pp. 485–490, 1999. View at Publisher · View at Google Scholar · View at Scopus
  21. S. Moncada, R. M. J. Palmer, and E. A. Higgs, “Nitric oxide: physiology, pathophysiology, and pharmacology,” Pharmacological Reviews, vol. 43, no. 2, pp. 109–142, 1991. View at Google Scholar · View at Scopus
  22. H. Homma, T. Takahashi, H. Seki, M. Ohtani, T. Kondoh, and M. Fukuda, “Immunohistochemical localization of inducible nitric oxide synthase in synovial tissue of human temporomandibular joints with internal derangement,” Archives of Oral Biology, vol. 46, no. 1, pp. 93–97, 2001. View at Publisher · View at Google Scholar · View at Scopus
  23. S. A. Tesser-Viscaíno, A. Denadai-Souza, and A. Denadai-Souza, “Putative antinociceptive action of nitric oxide in the caudal part of the spinal trigeminal nucleus during chronic carrageenan-induced arthritis in the rat temporomandibular joint,” Brain Research, vol. 1302, pp. 85–96, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  24. M. M. Bezerra, S. D. Brain, S. Greenacre, S. M. Bezerra Jerônimo, L. B. De Melo, J. Keeble, and F. A. Castro Da Rocha, “Reactive nitrogen species scavenging, rather than nitric oxide inhibition, protects from articular cartilage damage in rat zymosan-induced arthritis,” British Journal of Pharmacology, vol. 141, no. 1, pp. 172–182, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  25. S. M. Wahl, N. McCartney-Francis, J. Chan, R. Dionne, L. Ta, and J. M. Orenstein, “Nitric oxide in experimental joint inflammation: benefit or detriment?” Cells Tissues Organs, vol. 174, no. 1-2, pp. 26–33, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  26. C. L. Kwan, J. W. Hu, and B. J. Sessle, “Neuroplastic effects of neonatal capsaicin on neurons in adult rat trigeminal nucleus principalis and subnucleus oralis,” Journal of Neurophysiology, vol. 75, no. 1, pp. 298–310, 1996. View at Google Scholar · View at Scopus
  27. P. P. Bradley, R. D. Christensen, and G. Rothstein, “Cellular and extracellular myeloperoxidase in pyogenic inflammation,” Blood, vol. 60, no. 3, pp. 618–622, 1982. View at Google Scholar · View at Scopus
  28. G. Vaudo, S. Marchesi, and S. Marchesi, “Endothelial dysfunction in young patients with rheumatoid arthritis and low disease activity,” Annals of the Rheumatic Diseases, vol. 63, no. 1, pp. 31–35, 2004. View at Publisher · View at Google Scholar · View at Scopus
  29. D. M. Yaillen, P. A. Shapiro, E. S. Luschei, and G. R. Feldman, “Temporomandibular joint meniscectomy: effects of joint structure and masticatory function in Macaca fascicularis,” Journal of Maxillofacial Surgery, vol. 7, no. 4, pp. 255–264, 1979. View at Google Scholar · View at Scopus
  30. E. Helmy, R. Bays, and M. Sharawy, “Osteoarthrosis of the temporomandibular joint following experimental disc perforation in Macaca fascicularis,” Journal of Oral and Maxillofacial Surgery, vol. 46, no. 11, pp. 979–990, 1988. View at Google Scholar · View at Scopus
  31. J. I. Ishimaru and A. N. Goss, “A model for osteoarthritis of the temporomandibular joint,” Journal of Oral and Maxillofacial Surgery, vol. 50, no. 11, pp. 1191–1195, 1992. View at Google Scholar · View at Scopus
  32. C. Lekkas, “Experimental degenerative temporomandibular joint disease,” International Journal of Oral and Maxillofacial Surgery, vol. 23, no. 6, pp. 423–424, 1994. View at Google Scholar · View at Scopus
  33. H. Imai, I. Sakamoto, T. Yoda, and Y. Yamashita, “A model for internal derangement and osteoarthritis of the temporomandibular joint with experimental traction of the mandibular ramus in rabbit,” Oral Diseases, vol. 7, no. 3, pp. 185–191, 2001. View at Publisher · View at Google Scholar · View at Scopus
  34. A. F. Al-Mobireek, A. M. G. Darwazeh, and M. B. Hassanin, “Experimental induction of rheumatoid arthritis in temporomandibular joint of the guinea pig: a clinical and radiographic study,” Dentomaxillofacial Radiology, vol. 29, no. 5, pp. 286–290, 2000. View at Google Scholar · View at Scopus
  35. T. Zamma, “Adjuvant-induced arthritis in the temporomandibular joint of rats,” Infection and Immunity, vol. 39, no. 3, pp. 1291–1299, 1983. View at Google Scholar · View at Scopus
  36. K. Gado and G. Gigler, “Zymosan inflammation: a new method suitable for evaluating new antiinflammatory drugs,” Agents and Actions, vol. 32, no. 1-2, pp. 119–121, 1991. View at Google Scholar · View at Scopus
  37. M. M. Bezerra, S. D. Brain, V. C. C. Girão, S. Greenacre, J. Keeble, and F. A. C. Rocha, “Neutrophils-derived peroxynitrite contributes to acute hyperalgesia and cell influx in zymosan arthritis,” Naunyn-Schmiedeberg's Archives of Pharmacology, vol. 374, no. 4, pp. 265–273, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  38. L. S. Gazda, E. D. Milligan, and E. D. Milligan, “Sciatic inflammatory neuritis (SIN): behavioral allodynia is paralleled by peri-sciatic proinflammatory cytokine and superoxide production,” Journal of the Peripheral Nervous System, vol. 6, no. 3, pp. 111–129, 2001. View at Publisher · View at Google Scholar · View at Scopus
  39. A. C. Goulart, F. A. Correia, S. C. Sousa, and J. G. Luz, “Study of the inflammatory process induced by injection of carrageenan or formalin in the rat temporomandibular joint,” Pesquisa Odontológica Brasileira, vol. 19, no. 2, pp. 99–105, 2005. View at Google Scholar · View at Scopus
  40. S. Fujita and K. Hoshino, “Histochemical and immunohistochemical studies on the articular disk of the temporomandibular joint in rats,” Acta Anatomica, vol. 134, no. 1, pp. 26–30, 1989. View at Google Scholar · View at Scopus
  41. S. H. Ferreira, I. D. G. Duarte, and B. B. Lorenzetti, “The molecular mechanism of action of peripheral morphine analgesia: stimulation of the cGMP system via nitric oxide release,” European Journal of Pharmacology, vol. 201, no. 1, pp. 121–122, 1991. View at Google Scholar · View at Scopus
  42. H. Holthusen and J. O. Arndt, “Nitric oxide evokes pain in humans on intracutaneous injection,” Neuroscience Letters, vol. 165, no. 1-2, pp. 71–74, 1994. View at Publisher · View at Google Scholar · View at Scopus
  43. A. M. Sousa and W. A. Prado, “The dual effect of a nitric oxide donor in nociception,” Brain Research, vol. 897, no. 1-2, pp. 9–19, 2001. View at Publisher · View at Google Scholar · View at Scopus
  44. J. C. D. S. Rocha, M. E. B. Peixoto, S. Jancar, F. D. Q. Cunha, R. D. A. Ribeiro, and F. A. C. Da Rocha, “Dual effect of nitric oxide in articular inflammatory pain in zymosan-induced arthritis in rats,” British Journal of Pharmacology, vol. 136, no. 4, pp. 588–596, 2002. View at Google Scholar · View at Scopus
  45. K. F. Masuda, T. Yamaza, and T. Yamaza, “Distribution of inducible nitric oxide synthase, interleukin-1β, and interleukin-1 receptor in the temporomandibular joint of normal rats,” Acta Histochemica et Cytochemica, vol. 35, no. 1, pp. 11–21, 2002. View at Publisher · View at Google Scholar