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Clinical and Developmental Immunology
Volume 2013 (2013), Article ID 901420, 8 pages
http://dx.doi.org/10.1155/2013/901420
Research Article

Different Peripheral Tissue Injury Induces Differential Phenotypic Changes of Spinal Activated Microglia

1Center for TMD & Orofacial Pain, Peking University School & Hospital of Stomatology, Zhong Guan Cun South Avenue 22, Beijing 100081, China
2Department of General Dentistry II, Peking University School & Hospital of Stomatology, Beijing 100081, China
3Department of Anesthesiology, University of Utah, Salt Lake City, UT 84132-2304, USA

Received 24 February 2013; Revised 4 May 2013; Accepted 16 May 2013

Academic Editor: Anirban Ghosh

Copyright © 2013 Kai Li 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. S. T. Meller, C. Dykstra, D. Grzybycki, S. Murphy, and G. F. Gebhart, “The possible role of glia in nociceptive processing and hyperalgesia in the spinal cord of the rat,” Neuropharmacology, vol. 33, no. 11, pp. 1471–1478, 1994. View at Publisher · View at Google Scholar · View at Scopus
  2. L. R. Watkins, D. Martin, P. Ulrich, K. J. Tracey, and S. F. Maier, “Evidence for the involvement of spinal cord glia in subcutaneous formalin induced hyperalgesia in the rat,” Pain, vol. 71, no. 3, pp. 225–235, 1997. View at Publisher · View at Google Scholar · View at Scopus
  3. L. R. Watkins, E. D. Milligan, and S. F. Maier, “Glial activation: a driving force for pathological pain,” Trends in Neurosciences, vol. 24, no. 8, pp. 450–455, 2001. View at Publisher · View at Google Scholar · View at Scopus
  4. S. X. Jin, Z. Y. Zhuang, C. J. Woolf, and R. R. Ji, “p38 mitogen-activated protein kinase is activated after a spinal nerve ligation in spinal cord microglia and dorsal root ganglion neurons and contributes to the generation of neuropathic pain,” Journal of Neuroscience, vol. 23, no. 10, pp. 4017–4022, 2003. View at Scopus
  5. C. I. Svensson, M. Marsala, A. Westerlund et al., “Activation of p38 mitogen-activated protein kinase in spinal microglia is a critical link in inflammation-induced spinal pain processing,” Journal of Neurochemistry, vol. 86, no. 6, pp. 1534–1544, 2003. View at Publisher · View at Google Scholar · View at Scopus
  6. M. Tsuda, A. Mizokoshi, Y. Shigemoto-Mogami, S. Koizumi, and K. Inoue, “Activation of p38 mitogen-activated protein kinase in spinal hyperactive microglia contributes to pain hypersensitivity following peripheral nerve injury,” Glia, vol. 45, no. 1, pp. 89–95, 2004. View at Publisher · View at Google Scholar · View at Scopus
  7. R. W. Colburn, J. A. Deleo, A. J. Rickman, M. P. Yeager, P. Kwon, and W. F. Hickey, “Dissociation of microglial activation and neuropathic pain behaviors following peripheral nerve injury in the rat,” Journal of Neuroimmunology, vol. 79, no. 2, pp. 163–175, 1997. View at Publisher · View at Google Scholar · View at Scopus
  8. D. E. Coyle, “Partial peripheral nerve injury leads to activation of astroglia and microglia which parallels the development of allodynic behavior,” Glia, vol. 23, no. 1, pp. 75–83, 1998. View at Publisher · View at Google Scholar
  9. K. Fu, A. R. Light, G. K. Matsushima, and W. Maixner, “Microglial reactions after subcutaneous formalin injection into the rat hind paw,” Brain Research, vol. 825, no. 1-2, pp. 59–67, 1999. View at Publisher · View at Google Scholar · View at Scopus
  10. J. Gehrmann, S. Monaco, and G. W. Kreutzberg, “Spinal cord microglial cells and DRG satellite cells rapidly respond to transection of the rat sciatic nerve,” Restorative Neurology and Neuroscience, vol. 2, no. 4, pp. 181–198, 1991. View at Scopus
  11. H. Hashizume, J. A. DeLeo, R. W. Colburn, and J. N. Weinstein, “Spinal glial activation and cytokine expression after lumbar root injury in the rat,” Spine, vol. 25, no. 10, pp. 1206–1217, 2000. View at Publisher · View at Google Scholar · View at Scopus
  12. P. Honore, S. D. Rogers, M. J. Schwei et al., “Murine models of inflammatory, neuropathic and cancer pain each generates a unique set of neurochemical changes in the spinal cord and sensory neurons,” Neuroscience, vol. 98, no. 3, pp. 585–598, 2000. View at Publisher · View at Google Scholar · View at Scopus
  13. C. Molander, J. Hongpaisan, M. Svensson, and H. Aldskogius, “Glial cell reactions in the spinal cord after sensory nerve stimulation are associated with axonal injury,” Brain Research, vol. 747, no. 1, pp. 122–129, 1997. View at Publisher · View at Google Scholar · View at Scopus
  14. P. G. Popovich, P. Wei, and B. T. Stokes, “Cellular inflammatory response after spinal cord injury in Sprague-Dawley and Lewis rats,” Journal of Comparative Neurology, vol. 377, no. 3, pp. 443–464, 1997. View at Publisher · View at Google Scholar
  15. V. Raghavendra, F. Y. Tanga, and J. A. DeLeo, “Complete Freunds adjuvant-induced peripheral inflammation evokes glial activation and proinflammatory cytokine expression in the CNS,” European Journal of Neuroscience, vol. 20, no. 2, pp. 467–473, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. S. M. Sweitzer, R. W. Colburn, M. Rutkowski, and J. A. DeLeo, “Acute peripheral inflammation induces moderate glial activation and spinal IL-1β expression that correlates with pain behavior in the rat,” Brain Research, vol. 829, no. 1-2, pp. 209–221, 1999. View at Publisher · View at Google Scholar · View at Scopus
  17. J. Scholz and C. J. Woolf, “The neuropathic pain triad: neurons, immune cells and glia,” Nature Neuroscience, vol. 10, no. 11, pp. 1361–1368, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. H. Hashizume, M. D. Rutkowski, J. N. Weinstein, and J. A. Deleo, “Central administration of methotrexate reduces mechanical allodynia in an animal model of radiculopathy/sciatica,” Pain, vol. 87, no. 2, pp. 159–169, 2000. View at Publisher · View at Google Scholar · View at Scopus
  19. J. Scholz, A. Abele, C. Marian et al., “Low-dose methotrexate reduces peripheral nerve injury-evoked spinal microglial activation and neuropathic pain behavior in rats,” Pain, vol. 138, no. 1, pp. 130–142, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. C. A. Colton and D. M. Wilcock, “Assessing activation states in microglia,” CNS and Neurological Disorders—Drug Targets, vol. 9, no. 2, pp. 174–191, 2010. View at Scopus
  21. B. C. Hains and S. G. Waxman, “Activated microglia contribute to the maintenance of chronic pain after spinal cord injury,” Journal of Neuroscience, vol. 26, no. 16, pp. 4308–4317, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. Y. H. Tan, K. Li, X. Y. Chen, Y. Cao, A. R. Light, and K. Y. Fu, “Activation of Src family kinases in spinal microglia contributes to formalin-induced persistent pain state through p38 pathway,” Journal of Pain, vol. 13, no. 10, pp. 1008–1015, 2012. View at Publisher · View at Google Scholar
  23. E. D. Ponomarev, L. P. Shriver, K. Maresz, and B. N. Dittel, “Microglial cell activation and proliferation precedes the onset of CNS autoimmunity,” Journal of Neuroscience Research, vol. 81, no. 3, pp. 374–389, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. S. Walter, M. Letiembre, Y. Liu et al., “Role of the toll-like receptor 4 in neuroinflammation in Alzheimer's disease,” Cellular Physiology and Biochemistry, vol. 20, no. 6, pp. 947–956, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. E. Ulvestad, K. Williams, C. Vedeler et al., “Reactive microglia in multiple sclerosis lesions have an increased expression of receptors for the Fc part of IgG,” Journal of the Neurological Sciences, vol. 121, no. 2, pp. 125–131, 1994. View at Publisher · View at Google Scholar · View at Scopus
  26. I. M. Dijkstra, A. H. de Haas, N. Brouwer, H. W. G. M. Boddeke, and K. Biber, “Challenge with innate and protein antigens induces CCR7 expression by microglia in vitro and in vivo,” Glia, vol. 54, no. 8, pp. 861–872, 2006. View at Publisher · View at Google Scholar · View at Scopus
  27. U. Hanisch, “Microglia as a source and target of cytokines,” Glia, vol. 40, no. 2, pp. 140–155, 2002. View at Publisher · View at Google Scholar · View at Scopus
  28. K. Fu, Y. Tan, B. Sung, and J. Mao, “Peripheral formalin injection induces unique spinal cord microglial phenotypic changes,” Neuroscience Letters, vol. 449, no. 3, pp. 234–239, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. P. Hu, A. L. Bembrick, K. A. Keay, and E. M. McLachlan, “Immune cell involvement in dorsal root ganglia and spinal cord after chronic constriction or transection of the rat sciatic nerve,” Brain, Behavior, and Immunity, vol. 21, no. 5, pp. 599–616, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. W. J. Streit, M. B. Graeber, and G. W. Kreutzberg, “Peripheral nerve lesion produces increased levels of major histocompatibility complex antigens in the central nervous system,” Journal of Neuroimmunology, vol. 21, no. 2-3, pp. 117–123, 1989. View at Scopus
  31. T. Lin, K. Li, F. Y. Zhang, Z. K. Zhang, A. R. Light, and K. Y. Fu, “Dissociation of spinal microglia morphological activation and peripheral inflammation in inflammatory pain models,” Journal of Neuroimmunology, vol. 192, no. 1-2, pp. 40–48, 2007. View at Publisher · View at Google Scholar · View at Scopus
  32. G. J. Bennett and Y. K. Xie, “A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man,” Pain, vol. 33, no. 1, pp. 87–107, 1988. View at Scopus
  33. M. B. Graeber, W. Tetzlaff, W. J. Streit, and G. W. Kreutzberg, “Microglial cells but not astrocytes undergo mitosis following rat facial nerve axotomy,” Neuroscience Letters, vol. 85, no. 3, pp. 317–321, 1988. View at Scopus
  34. A. K. Clark, C. Gentry, E. J. Bradbury, S. B. McMahon, and M. Malcangio, “Role of spinal microglia in rat models of peripheral nerve injury and inflammation,” European Journal of Pain, vol. 11, no. 2, pp. 223–230, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. A. Ledeboer, J. H. Mahoney, E. D. Milligan, D. Martin, S. F. Maier, and L. R. Watkins, “Spinal cord glia and interleukin-1 do not appear to mediate persistent allodynia induced by intramuscular acidic saline in rats,” Journal of Pain, vol. 7, no. 10, pp. 757–767, 2006. View at Publisher · View at Google Scholar · View at Scopus
  36. X. Y. Hua, C. I. Svensson, T. Matsui, B. Fitzsimmons, T. L. Yaksh, and M. Webb, “Intrathecal minocycline attenuates peripheral inflammation-induced hyperalgesia by inhibiting p38 MAPK in spinal microglia,” European Journal of Neuroscience, vol. 22, no. 10, pp. 2431–2440, 2005. View at Publisher · View at Google Scholar · View at Scopus
  37. F. Y. Zhang, Y. Wan, Z. K. Zhang, A. R. Light, and K. Y. Fu, “Peripheral formalin injection induces long-lasting increases in cyclooxygenase 1 expression by microglia in the spinal cord,” Journal of Pain, vol. 8, no. 2, pp. 110–117, 2007. View at Publisher · View at Google Scholar · View at Scopus