Peripheral formalin injury induces 2 stages of microglial activation in the spinal cord

Journal of Pain

Volumn 11, Issue 11, 2010, Pages 1056-1065

  Li, Kai ^a   Lin, Ting ^a   Cao, Ye ^a   Light, Alan R ^b   Fu, Kai Yuan ^a  

^a PEKING UNIVERSITY   (China)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

formalin; Microglia; mitogen activated protein kinases; p38; spinal cord

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; FORMALDEHYDE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CHRONIC PAIN; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; HYPERALGESIA; MALE; MICROGLIA; NOCICEPTION; NONHUMAN; PAIN; PROTEIN EXPRESSION; RAT; SPINAL CORD DORSAL HORN;

ACUTE DISEASE; ANIMALS; CHRONIC DISEASE; DISEASE MODELS, ANIMAL; HYPERALGESIA; MALE; MAP KINASE SIGNALING SYSTEM; MICROGLIA; NOCICEPTORS; PAIN MEASUREMENT; PAIN, INTRACTABLE; POSTERIOR HORN CELLS; PROTEIN KINASE INHIBITORS; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD;

EID: 78149283821     PISSN: 15265900     EISSN: 15288447     Source Type: Journal    
DOI: 10.1016/j.jpain.2010.01.268     Document Type: Article

References (50)

1. 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 Eur J Pain 11 2007 223 230
2. 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 J Neuroimmunol 79 1997 163 175
3. D.E. Coyle Partial peripheral nerve injury leads to activation of astroglia and microglia which parallels the development of allodynic behavior Glia 23 1998 75 83
4. X.Y. Cui, Y. Dai, S.L. Wang, H. Yamanaka, K. Kobayashi, K. Obata, J. Chen, and K. Noguchi Differential activation of p38 and extracellular signal-regulated kinase in spinal cord in a model of bee venom-induced inflammation and hyperalgesia Mol Pain 4 2008 17
5. D. Dubuisson, and S.G. Dennis The formalin test: a quantitative study of the analgesic effects of morphine, meperidine, and brain stem stimulation in rats and cats Pain 4 1977 161 174
6. S. Echeverry, X.Q. Shi, and J. Zhang Characterization of cell proliferation in rat spinal cord following peripheral nerve injury and the relationship with neuropathic pain Pain 135 2008 37 47
7. N.P. Eriksson, J.K. Persson, M. Svensson, J. Arvidsson, C. Molander, and H. Aldskogius A quantitative analysis of the microglial cell reaction in central primary sensory projection territories following peripheral nerve injury in the adult rat Exp Brain Res 96 1993 19 27
8. K.Y. Fu, A.R. Light, G.K. Matsushima, and W. Maixner Microglial reactions after subcutaneous formalin injection into the rat hind paw Brain Res 825 1999 59 67
9. K.Y. Fu, A.R. Light, and W. Maixner Long-lasting inflammation and long-term hyperalgesia after subcutaneous formalin injection into the rat hindpaw J Pain 2 2001 2 11
10. K.Y. Fu, Y.H. Tan, B. Sung, and J. Mao Peripheral formalin injection induces unique spinal cord microglial phenotypic changes Neurosci Lett 449 2009 234 239
11. Y.J. Gao, and R.R. Ji Activation of JNK pathway in persistent pain Neurosci Lett 437 2008 180 183
12. 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 Restor Neurol Neurosci 2 1991 181 198
13. M.B. Graeber, W.J. Streit, and G.W. Kreutzberg Axotomy of the rat facial nerve leads to increased CR3 complement receptor expression by activated microglial cells J Neurosci Res 21 1988 18 24
14. 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 (Phila, Pa 1976) 25 2000 1206 1217
15. 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 87 2000 159 169
16. P. Honore, S.D. Rogers, M.J. Schwei, J.L. Salak-Johnson, N.M. Luger, M.C. Sabino, D.R. Clohisy, and P.W. Mantyh Murine models of inflammatory, neuropathic and cancer pain each generates a unique set of neurochemical changes in the spinal cord and sensory neurons Neuroscience 98 2000 585 598
17. 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 Eur J Neurosci 22 2005 2431 2440
18. R.R. Ji, and M.R. Suter p38 MAPK, microglial signaling, and neuropathic pain Mol Pain 3 2007 33
19. 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 J Neurosci 23 2003 4017 4022
20. A. Ledeboer, E.M. Sloane, E.D. Milligan, M.G. Frank, J.H. Mahony, S.F. Maier, and L.R. Watkins Minocycline attenuates mechanical allodynia and proinflammatory cytokine expression in rat models of pain facilitation Pain 115 2005 71 83
21. 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 J Neuroimmunol 192 2007 40 48
22. W. Ma, and R. Quirion The ERK/MAPK pathway, as a target for the treatment of neuropathic pain Expert Opin Ther Targets 9 2005 699 713
23. S.B. McMahon, W.B. Cafferty, and F. Marchand Immune and glial cell factors as pain mediators and modulators Exp Neurol 192 2005 444 462
24. 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 33 1994 1471 1478
25. E.D. Milligan, K.K. Mehmert, J.L. Hinde, L.O. Harvey, D. Martin, K.J. Tracey, S.F. Maier, and L.R. Watkins Thermal hyperalgesia and mechanical allodynia produced by intrathecal administration of the human immunodeficiency virus-1 (HIV-1) envelope glycoprotein, gp120 Brain Res 861 2000 105 116
26. E.D. Milligan, C. Twining, M. Chacur, J. Biedenkapp, K. O'Connor, S. Poole, K. Tracey, D. Martin, S.F. Maier, and L.R. Watkins Spinal glia and proinflammatory cytokines mediate mirror-image neuropathic pain in rats J Neurosci 23 2003 1026 1040
27. 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 Res 747 1997 122 129
28. K. Obata, H. Katsura, T. Mizushima, J. Sakurai, K. Kobayashi, H. Yamanaka, Y. Dai, T. Fukuoka, and K. Noguchi Roles of extracellular signal-regulated protein kinases 5 in spinal microglia and primary sensory neurons for neuropathic pain J Neurochem 102 2007 1569 1584
29. P.G. Popovich, P. Wei, and B.T. Stokes Cellular inflammatory response after spinal cord injury in Sprague-Dawley and Lewis rats J Comp Neurol 377 1997 443 464
30. C.A. Porro, and M. Cavazzuti Spatial and temporal aspects of spinal cord and brainstem activation in the formalin pain model Prog Neurobiol 41 1993 565 607
31. V. Raghavendra, F. Tanga, and J.A. DeLeo Inhibition of microglial activation attenuates the development but not existing hypersensitivity in a rat model of neuropathy J Pharmacol Exp Ther 306 2003 624 630
32. 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 Eur J Neurosci 20 2004 467 473
33. K. Ren An improved method for assessing mechanical allodynia in the rat Physiol Behav 67 1999 711 716
34. L.S. Sorkin, D.L. Boyle, D. Hammaker, D.S. Herman, E. Vail, and G.S. Firestein MKK3, an upstream activator of p38, contributes to formalin phase 2 and late allodynia in mice Neuroscience 162 2009 462 471
35. R.V. Storkson, A. Kjorsvik, A. Tjolsen, and K. Hole Lumbar catheterization of the spinal subarachnoid space in the rat J Neurosci Methods 65 1996 167 172
36. M.R. Suter, Y.R. Wen, I. Decosterd, and R.R. Ji Do glial cells control pain? Neuron Glia Biol 3 2007 255 268
37. C.I. Svensson, M. Marsala, A. Westerlund, N.A. Calcutt, W.M. Campana, J.D. Freshwater, R. Catalano, Y. Feng, A.A. Protter, B. Scott, and T.L. Yaksh Activation of p38 mitogen-activated protein kinase in spinal microglia is a critical link in inflammation-induced spinal pain processing J Neurochem 86 2003 1534 1544
38. S.M. Sweitzer, R.W. Colburn, M. Rutkowski, and J.A. DeLeo Acute peripheral inflammation induces moderate glial activation and spinal IL-1beta expression that correlates with pain behavior in the rat Brain Res 829 1999 209 221
39. S.M. Sweitzer, P. Schubert, and J.A. DeLeo Propentofylline, a glial modulating agent, exhibits antiallodynic properties in a rat model of neuropathic pain J Pharmacol Exp Ther 297 2001 1210 1217
40. Y.X. Tao, and R.A. Johns Activation and up-regulation of spinal cord nitric oxide receptor, soluble guanylate cyclase, after formalin injection into the rat hind paw Neuroscience 112 2002 439 446
41. A. Tjolsen, O.G. Berge, S. Hunskaar, J.H. Rosland, and K. Hole The formalin test: An evaluation of the method Pain 51 1992 5 17
42. M. Tsuda, Y. Shigemoto-Mogami, S. Koizumi, A. Mizokoshi, S. Kohsaka, M.W. Salter, and K. Inoue P2X4 receptors induced in spinal microglia gate tactile allodynia after nerve injury Nature 424 2003 778 783
43. 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 45 2004 89 95
44. C.J. Vierck, R.P. Yezierski, and A.R. Light Long-lasting hyperalgesia and sympathetic dysregulation after formalin injection into the rat hind paw Neuroscience 153 2008 501 506
45. 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 71 1997 225 235
46. L.R. Watkins, E.D. Milligan, and S.F. Maier Glial activation: A driving force for pathological pain Trends Neurosci 24 2001 450 455
47. Y.R. Wen, M.R. Suter, R.R. Ji, G.C. Yeh, Y.S. Wu, K.C. Wang, T. Kohno, W.Z. Sun, and C.C. Wang Activation of p38 mitogen-activated protein kinase in spinal microglia contributes to incision-induced mechanical allodynia Anesthesiology 110 2009 155 165
48. J. Zhang, C. Hoffert, H.K. Vu, T. Groblewski, S. Ahmad, and D. O'Donnell Induction of CB2 receptor expression in the rat spinal cord of neuropathic but not inflammatory chronic pain models Eur J Neurosci 17 2003 2750 2754
49. Z.Y. Zhuang, P. Gerner, C.J. Woolf, and R.R. Ji ERK is sequentially activated in neurons, microglia, and astrocytes by spinal nerve ligation and contributes to mechanical allodynia in this neuropathic pain model Pain 114 2005 149 159
50. Z.Y. Zhuang, Y.R. Wen, D.R. Zhang, T. Borsello, C. Bonny, G.R. Strichartz, I. Decosterd, and R.R. Ji A peptide c-Jun N-terminal kinase (JNK) inhibitor blocks mechanical allodynia after spinal nerve ligation: Respective roles of JNK activation in primary sensory neurons and spinal astrocytes for neuropathic pain development and maintenance J Neurosci 26 2006 3551 3560