Resident glial cell activation in response to perispinal inflammation leads to acute changes in nociceptive sensitivity: Implications for the generation of neuropathic pain

Pain

Volumn 154, Issue 1, 2013, Pages 71-81

  Tenorio, Gustavo ^a   Kulkarni, Ashwini ^a   Kerr, Bradley J ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

BSCB; Gliosis; Glutamate transporter; Inflammation; Zymosan

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD BRAIN BARRIER; CELL ACTIVATION; CONTROLLED STUDY; FEMALE; GLIA CELL; INFLAMMATION; MICROGLIA; MOUSE; NEUROPATHIC PAIN; NOCICEPTION; NONHUMAN; PERISPINAL INFLAMMATION; PRIORITY JOURNAL;

EID: 84871629593     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1016/j.pain.2012.09.008     Document Type: Article

References (53)

1. S.M. Agrawal, C. Silva, W.W. Tourtellotte, and V.W. Yong EMMPRIN: a novel regulator of leukocyte transmigration into the CNS in multiple sclerosis and experimental autoimmune encephalomyelitis J Neurosci 31 2011 669 677
2. C.J. Archibald, P.J. McGrath, P.G. Ritvo, J.D. Fisk, V. Bhan, C.E. Maxner, and T.J. Murray Pain prevalence, severity and impact in a clinic sample of multiple sclerosis patients PAIN® 58 1994 89 93
3. S. Beggs, X.J. Liu, C. Kwan, and M.W. Salter Peripheral nerve injury and TRPV1-expressing primary afferent C-fibers cause opening of the blood-brain barrier Mol Pain 6 2010 74
4. S. Beggs, and M.W. Salter Stereological and somatotopic analysis of the spinal microglial response to peripheral nerve injury Brain Behav Immun 21 2007 624 633 (Pubitemid 46829774)
5. J. Bennett, J. Basivireddy, A. Kollar, K.E. Biron, P. Reickmann, W.A. Jefferies, and S. McQuaid Blood-brain barrier disruption and enhanced vascular permeability in the multiple sclerosis model EAE J Neuroimmunol 229 2010 180 191
6. C.C. Bowman, A. Rasley, S.L. Tranguch, and I. Marriott Cultured astrocytes express toll-like receptors for bacterial products Glia 43 2003 281 291 (Pubitemid 37047684)
7. T.A. Brooks, B.T. Hawkins, J.D. Huber, R.D. Egleton, and T.P. Davis Chronic inflammatory pain leads to increased blood-brain barrier permeability and tight junction protein alterations Am J Physiol Heart Circ Physiol 289 2005 H738 H743 (Pubitemid 41129391)
8. K.J. Burchiel, and F.P. Hsu Pain and spasticity after spinal cord injury: mechanisms and treatment Spine 26 2001 S146 S160
9. C.R. Campos, S.M. Ocheltree, S. Hom, R.D. Egleton, and T.P. Davis Nociceptive inhibition prevents inflammatory pain induced changes in the blood-brain barrier Brain Res 1221 2008 6 13
10. L. Cao, and J.A. DeLeo CNS-infiltrating CD4+ T lymphocytes contribute to murine spinal nerve transection-induced neuropathic pain Eur J Immunol 38 2008 448 458
11. D.B. Clifford, and J.L. Trotter Pain in multiple sclerosis Arch Neurol 41 1984 1270 1272 (Pubitemid 15222597)
12. M. Costigan, A. Moss, A. Latremoliere, C. Johnston, M. Verma-Gandhu, T.A. Herbert, L. Barrett, G.J. Brenner, D. Vardeh, C.J. Woolf, and M. Fitzgerald T-cell infiltration and signaling in the adult dorsal spinal cord is a major contributor to neuropathic pain-like hypersensitivity J Neurosci 29 2009 14415 14422
13. M. Costigan, J. Scholz, and C.J. Woolf Neuropathic pain: a maladaptive response of the nervous system to damage Annu Rev Neurosci 32 2009 1 32
14. J.A. Coull, S. Beggs, D. Boudreau, D. Boivin, M. Tsuda, K. Inoue, C. Gravel, M.W. Salter, and Y. De Koninck BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain Nature 438 2005 1017 1021 (Pubitemid 43093974)
15. N.C. Danbolt Glutamate uptake Prog Neurobiol 65 2001 1 105 (Pubitemid 32479155)
16. J.A. DeLeo, and R.P. Yezierski The role of neuroinflammation and neuroimmune activation in persistent pain PAIN® 90 2001 1 6 (Pubitemid 32146552)
17. N. Esen, F.Y. Tanga, J.A. DeLeo, and T. Kielian Toll-like receptor 2 (TLR2) mediates astrocyte activation in response to the Gram-positive bacterium Staphylococcus aureus J Neurochem 88 2004 746 758 (Pubitemid 38140218)
18. B.C. Hains, and S.G. Waxman Activated microglia contribute to the maintenance of chronic pain after spinal cord injury J Neurosci 26 2006 4308 4317 (Pubitemid 44315390)
19. K. Hargreaves, R. Dubner, F. Brown, C. Flores, and J. Joris A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia PAIN® 32 1988 77 88
20. O. Haugeto, K. Ullensvang, L.M. Levy, F.A. Chaudhry, T. Honore, M. Nielsen, K.P. Lehre, and N.C. Danbolt Brain glutamate transporter proteins form homomultimers J Biol Chem 271 1996 27715 27722 (Pubitemid 26367342)
21. 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 Behav Immun 21 2007 599 616 (Pubitemid 46830961)
22. S.P. Hunt, A. Pini, and G. Evan Induction of c-fos-like protein in spinal cord neurons following sensory stimulation Nature 328 1987 632 634 (Pubitemid 17103967)
23. Y. Kawasaki, L. Zhang, J.K. Cheng, and R.R. Ji Cytokine mechanisms of central sensitization: distinct and overlapping role of interleukin-1beta, interleukin-6, and tumor necrosis factor-alpha in regulating synaptic and neuronal activity in the superficial spinal cord J Neurosci 28 2008 5189 5194
24. 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
25. G. McCaffrey, M.J. Seelbach, W.D. Staatz, N. Nametz, C. Quigley, C.R. Campos, T.A. Brooks, and T.P. Davis Occludin oligomeric assembly at tight junctions of the blood-brain barrier is disrupted by peripheral inflammatory hyperalgesia J Neurochem 106 2008 2395 2409
26. J. Mika Modulation of microglia can attenuate neuropathic pain symptoms and enhance morphine effectiveness Pharmacol Rep 60 2008 297 307
27. J. Mika, M. Osikowicz, W. Makuch, and B. Przewlocka Minocycline and pentoxifylline attenuate allodynia and hyperalgesia and potentiate the effects of morphine in rat and mouse models of neuropathic pain Eur J Pharmacol 560 2007 142 149 (Pubitemid 46341303)
28. E.D. Milligan, V. Zapata, M. Chacur, D. Schoeniger, J. Biedenkapp, K.A. O'Connor, G.M. Verge, G. Chapman, P. Green, A.C. Foster, G.S. Naeve, S.F. Maier, and L.R. Watkins Evidence that exogenous and endogenous fractalkine can induce spinal nociceptive facilitation in rats Eur J Neurosci 20 2004 2294 2302 (Pubitemid 39472392)
29. D.E. Moulin, K.M. Foley, and G.C. Ebers Pain syndromes in multiple sclerosis Neurology 38 1988 1830 1834 (Pubitemid 19004573)
30. C.J. Olechowski, A. Parmar, B. Miller, J. Stephan, G. Tenorio, K. Tran, J. Leighton, and B.J. Kerr A diminished response to formalin stimulation reveals a role for the glutamate transporters in the altered pain sensitivity of mice with experimental autoimmune encephalomyelitis (EAE) PAIN® 149 2010 565 572
31. C.J. Olechowski, J.J. Truong, and B.J. Kerr Neuropathic pain behaviours in a chronic-relapsing model of experimental autoimmune encephalomyelitis (EAE) PAIN® 141 2009 156 164
32. A. Osterberg, and J. Boivie Central pain in multiple sclerosis-sensory abnormalities Eur J Pain 14 2010 104 110
33. P.G. Popovich, P.J. Horner, B.B. Mullin, and B.T. Stokes A quantitative spatial analysis of the blood-spinal cord barrier. I. Permeability changes after experimental spinal contusion injury Exp Neurol 142 1996 258 275 (Pubitemid 26414059)
34. D.H. Rodrigues, D. Sachs, and A.L. Teixeira Mechanical hypernociception in experimental autoimmune encephalomyelitis Arq Neuropsiquiatr 67 2009 78 81
35. A.E. Schellenberg, R. Buist, V.W. Yong, M.R. Del Bigio, and J. Peeling Magnetic resonance imaging of blood-spinal cord barrier disruption in mice with experimental autoimmune encephalomyelitis Magn Reson Med 58 2007 298 305 (Pubitemid 47267647)
36. J. Scholz, and C.J. Woolf The neuropathic pain triad: neurons, immune cells and glia Nat Neurosci 10 2007 1361 1368 (Pubitemid 350014681)
37. E. Sloane, A. Ledeboer, W. Seibert, B. Coats, M. van Strien, S.F. Maier, K.W. Johnson, R. Chavez, L.R. Watkins, L. Leinwand, E.D. Milligan, and A.M. Van Dam Anti-inflammatory cytokine gene therapy decreases sensory and motor dysfunction in experimental multiple sclerosis: MOG-EAE behavioral and anatomical symptom treatment with cytokine gene therapy Brain Behav Immun 23 2009 92 100
38. B. Sung, G. Lim, and J. Mao Altered expression and uptake activity of spinal glutamate transporters after nerve injury contribute to the pathogenesis of neuropathic pain in rats J Neurosci 23 2003 2899 2910 (Pubitemid 36418626)
39. K.B. Svendsen, T.S. Jensen, H.J. Hansen, and F.W. Bach Sensory function and quality of life in patients with multiple sclerosis and pain PAIN® 114 2005 473 481 (Pubitemid 40385885)
40. K.B. Svendsen, T.S. Jensen, K. Overvad, H.J. Hansen, N. Koch-Henriksen, and F.W. Bach Pain in patients with multiple sclerosis: a population-based study Arch Neurol 60 2003 1089 1094 (Pubitemid 36975796)
41. 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 (Pubitemid 37174270)
42. S.M. Sweitzer, W.F. Hickey, M.D. Rutkowski, J.L. Pahl, and J.A. DeLeo Focal peripheral nerve injury induces leukocyte trafficking into the central nervous system: potential relationship to neuropathic pain PAIN® 100 2002 163 170 (Pubitemid 35305133)
43. Y.X. Tao, J. Gu, and R.L. Stephens Jr. Role of spinal cord glutamate transporter during normal sensory transmission and pathological pain states Mol Pain 1 2005 30
44. K. Thibault, B. Calvino, and S. Pezet Characterisation of sensory abnormalities observed in an animal model of multiple sclerosis: a behavioural and pharmacological study Eur J Pain 15 2011 231.e1 231.e16
45. S. Tilleux, and E. Hermans Neuroinflammation and regulation of glial glutamate uptake in neurological disorders J Neurosci Res 85 2007 2059 2070 (Pubitemid 47172138)
46. 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 (Pubitemid 37021707)
47. G.M. Verge, E.D. Milligan, S.F. Maier, L.R. Watkins, G.S. Naeve, and A.C. Foster Fractalkine (CX3CL1) and fractalkine receptor (CX3CR1) distribution in spinal cord and dorsal root ganglia under basal and neuropathic pain conditions Eur J Neurosci 20 2004 1150 1160 (Pubitemid 39233569)
48. L.R. Watkins, E.D. Milligan, and S.F. Maier Glial activation: a driving force for pathological pain Trends Neurosci 24 2001 450 455 (Pubitemid 32695356)
49. R.P. Yezierski Pain following spinal cord injury: pathophysiology and central mechanisms Prog Brain Res 129 2000 429 449 (Pubitemid 35461213)
50. J. Zhang, and Y. De Koninck Spatial and temporal relationship between monocyte chemoattractant protein-1 expression and spinal glial activation following peripheral nerve injury J Neurochem 97 2006 772 783
51. Z. Zhong, R. Deane, Z. Ali, M. Parisi, Y. Shapovalov, M.K. O'Banion, K. Stojanovic, A. Sagare, S. Boillee, D.W. Cleveland, and B.V. Zlokovic ALS-causing SOD1 mutants generate vascular changes prior to motor neuron degeneration Nat Neurosci 11 2008 420 422 (Pubitemid 351441888)
52. 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
53. X. Zou, Q. Lin, and W.D. Willis Enhanced phosphorylation of NMDA receptor 1 subunits in spinal cord dorsal horn and spinothalamic tract neurons after intradermal injection of capsaicin in rats J Neurosci 20 2000 6989 6997