TGF-β1 attenuates spinal neuroinflammation and the excitatory amino acid system in rats with neuropathic pain

Journal of Pain

Volumn 14, Issue 12, 2013, Pages 1671-1685

  Chen, Nan Fu ^a,b   Huang, Shi Ying ^a   Chen, Wu Fu ^c   Chen, Chun Hong ^a   Lu, Ching Hsiang ^b   Chen, Chun Lin ^b   Yang, San Nan ^d   Wang, Hui Min ^e   Wen, Zhi Hong ^a  

^a NATIONAL SUN YAT SEN UNIVERSITY   (Taiwan)

^b KAOHSIUNG ARMED FORCES GENERAL HOSPITAL   (Taiwan)

^c CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^d I SHOU UNIVERSITY   (Taiwan)

^e KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

Author keywords

chronic constriction injury; excitatory amino acids; glutamate transporters; Transforming growth factor 1; tumor necrosis factor

Indexed keywords

ASPARTIC ACID; EXCITATORY AMINO ACID TRANSPORTER; EXCITATORY AMINO ACID TRANSPORTER 3; GLUTAMIC ACID; RECOMBINANT TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA; VESICULAR GLUTAMATE TRANSPORTER 1;

ANALGESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINOCICEPTION; ARTICLE; ASTROCYTE; CELL ACTIVATION; CONTROLLED STUDY; DIALYSATE LEVEL; DOWN REGULATION; DRUG EFFECT; GRAY MATTER; HYPERALGESIA; LIGATION; LUMBAR SPINE; MALE; MICROGLIA; MYELITIS; NEUROPATHIC PAIN; NONHUMAN; RAT; SCIATIC NERVE INJURY; SINGLE DRUG DOSE; UPREGULATION;

CHRONIC CONSTRICTION INJURY; EXCITATORY AMINO ACIDS; GLUTAMATE TRANSPORTERS; TRANSFORMING GROWTH FACTOR-Β1; TUMOR NECROSIS FACTOR-Α;

ANIMALS; ASTROCYTES; DOWN-REGULATION; EXCITATORY AMINO ACIDS; INFLAMMATION; INJECTIONS, SPINAL; MALE; MICROGLIA; NEURALGIA; RATS; RATS, WISTAR; SCIATIC NEUROPATHY; SPINAL CORD; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84888621422     PISSN: 15265900     EISSN: 15288447     Source Type: Journal    
DOI: 10.1016/j.jpain.2013.08.010     Document Type: Article

References (116)

1. J.T. Andreasen, A. Bach, M. Gynther, A. Nasser, J. Mogensen, K. Stromgaard, and D.S. Pickering UCCB01-125, a dimeric inhibitor of PSD-95, reduces inflammatory pain without disrupting cognitive or motor performance: Comparison with the NMDA receptor antagonist MK-801 Neuropharmacology 67 2013 193 200
2. A.I. Basbaum, and C.J. Woolf Pain Curr Biol 9 1999 R429 R431
3. G.J. Bennett, and Y.K. Xie A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man Pain 33 1988 87 107
4. E.N. Benveniste, L.P. Tang, and R.M. Law Differential regulation of astrocyte TNF-alpha expression by the cytokines TGF-beta, IL-6 and IL-10 Int J Dev Neurosci 13 1995 341 349
5. U.V. Berger, and M.A. Hediger Distribution of the glutamate transporters GLAST and GLT-1 in rat circumventricular organs, meninges, and dorsal root ganglia J Comp Neurol 421 2000 385 399 (Pubitemid 30253401)
6. B.C. Binns, Y. Huang, V.M. Goettl, K.V. Hackshaw, and R.L. Stephens Jr. Glutamate uptake is attenuated in spinal deep dorsal and ventral horn in the rat spinal nerve ligation model Brain Res 1041 2005 38 47 (Pubitemid 40445387)
7. A. Buss, K. Pech, B.A. Kakulas, D. Martin, J. Schoenen, J. Noth, and G.A. Brook TGF-beta1 and TGF-beta2 expression after traumatic human spinal cord injury Spinal cord 46 2008 364 371 (Pubitemid 351630959)
8. F. Caraci, G. Battaglia, V. Bruno, P. Bosco, V. Carbonaro, M.L. Giuffrida, F. Drago, M.A. Sortino, F. Nicoletti, and A. Copani TGF-beta1 pathway as a new target for neuroprotection in Alzheimer's disease CNS Neurosci Ther 17 2011 237 249
9. A. Chalazonitis, J. Kalberg, D.R. Twardzik, R.S. Morrison, and J.A. Kessler Transforming growth factor beta has neurotrophic actions on sensory neurons in vitro and is synergistic with nerve growth factor Dev Biol 152 1992 121 132
10. W.F. Chen, C.S. Sung, Y.H. Jean, T.M. Su, H.C. Wang, J.T. Ho, S.Y. Huang, C.S. Lin, and Z.H. Wen Suppressive effects of intrathecal granulocyte colony-stimulating factor on excessive release of excitatory amino acids in the spinal cerebrospinal fluid of rats with cord ischemia: Role of glutamate transporters Neuroscience 165 2010 1217 1232
11. D.W. Choi, M. Maulucci-Gedde, and A.R. Kriegstein Glutamate neurotoxicity in cortical cell culture J Neurosci 7 1987 357 368 (Pubitemid 17017465)
12. R.W. Colburn, A.J. Rickman, and J.A. DeLeo The effect of site and type of nerve injury on spinal glial activation and neuropathic pain behavior Exp Neurol 157 1999 289 304 (Pubitemid 29260737)
13. 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 (Pubitemid 28174047)
14. N.C. Danbolt Glutamate uptake Prog Neurobiol 65 2001 1 105 (Pubitemid 32479155)
15. J.A. DeLeo, R.W. Colburn, and A.J. Rickman Cytokine and growth factor immunohistochemical spinal profiles in two animal models of mononeuropathy Brain Res 759 1997 50 57 (Pubitemid 27286343)
16. A. Dobolyi, C. Vincze, G. Pal, and G. Lovas The neuroprotective functions of transforming growth factor Beta proteins Int J Mol Sci 13 2012 8219 8258
17. S. Duan, C.M. Anderson, E.C. Keung, Y. Chen, and R.A. Swanson P2X7 receptor-mediated release of excitatory amino acids from astrocytes J Neurosci 23 2003 1320 1328 (Pubitemid 36258910)
18. N. Dunker, and K. Krieglstein Targeted mutations of transforming growth factor-beta genes reveal important roles in mouse development and adult homeostasis Eur J Biochem 267 2000 6982 6988 (Pubitemid 32009439)
19. S. Echeverry, X.Q. Shi, A. Haw, H. Liu, Z.W. Zhang, and J. Zhang Transforming growth factor-beta1 impairs neuropathic pain through pleiotropic effects Mol Pain 5 2009 16
20. K.C. Flanders, R.F. Ren, and C.F. Lippa Transforming growth factor-betas in neurodegenerative disease Prog Neurobiol 54 1998 71 85 (Pubitemid 28049820)
21. Y.J. Gao, L. Zhang, and R.R. Ji Spinal injection of TNF-alpha-activated astrocytes produces persistent pain symptom mechanical allodynia by releasing monocyte chemoattractant protein-1 Glia 58 2010 1871 1880
22. C.J. Garrison, P.M. Dougherty, K.C. Kajander, and S.M. Carlton Staining of glial fibrillary acidic protein (GFAP) in lumbar spinal cord increases following a sciatic nerve constriction injury Brain Res 565 1991 1 7
23. C.E. Gross, M.M. Bednar, D.B. Howard, and M.B. Sporn Transforming growth factor-beta 1 reduces infarct size after experimental cerebral ischemia in a rabbit model Stroke 24 1993 558 562 (Pubitemid 23100743)
24. Y.S. Gwak, J. Kang, G.C. Unabia, and C.E. Hulsebosch Spatial and temporal activation of spinal glial cells: Role of gliopathy in central neuropathic pain following spinal cord injury in rats Exp Neurol 234 2012 362 372
25. 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)
26. 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
27. T.W. Ho, L.A. Bristol, C. Coccia, Y. Li, J. Milbrandt, E. Johnson, L. Jin, O. Bar-Peled, J.W. Griffin, and J.D. Rothstein TGFbeta trophic factors differentially modulate motor axon outgrowth and protection from excitotoxicity Exp Neurol 161 2000 664 675 (Pubitemid 30137023)
28. S.Y. Huang, N.F. Chen, W.F. Chen, H.C. Hung, H.P. Lee, Y.Y. Lin, H.M. Wang, P.J. Sung, J.H. Sheu, and Z.H. Wen Sinularin from indigenous soft coral attenuates nociceptive responses and spinal neuroinflammation in carrageenan-induced inflammatory rat model Mar Drugs 10 2012 1899 1919
29. Y.H. Huang, and D.E. Bergles Glutamate transporters bring competition to the synapse Curr Opin Neurobiol 14 2004 346 352 (Pubitemid 38759865)
30. P. Inquimbert, K. Bartels, O.B. Babaniyi, L.B. Barrett, I. Tegeder, and J. Scholz Peripheral nerve injury produces a sustained shift in the balance between glutamate release and uptake in the dorsal horn of the spinal cord Pain 153 2012 2422 2431
31. Y.H. Jean, W.F. Chen, C.Y. Duh, S.Y. Huang, C.H. Hsu, C.S. Lin, C.S. Sung, I.M. Chen, and Z.H. Wen Inducible nitric oxide synthase and cyclooxygenase-2 participate in anti-inflammatory and analgesic effects of the natural marine compound lemnalol from Formosan soft coral Lemnalia cervicorni Eur J Pharmacol 578 2008 323 331
32. Y.H. Jean, W.F. Chen, C.S. Sung, C.Y. Duh, S.Y. Huang, C.S. Lin, M.H. Tai, S.F. Tzeng, and Z.H. Wen Capnellene, a natural marine compound derived from soft coral, attenuates chronic constriction injury-induced neuropathic pain in rats Br J Pharmacol 158 2009 713 725
33. R.R. Ji, Y. Kawasaki, Z.Y. Zhuang, Y.R. Wen, and I. Decosterd Possible role of spinal astrocytes in maintaining chronic pain sensitization: Review of current evidence with focus on bFGF/JNK pathway Neuron Glia Biol 2 2006 259 269 (Pubitemid 47074743)
34. 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 (Pubitemid 36958419)
35. L.L. Jones, G.W. Kreutzberg, and G. Raivich Transforming growth factor beta's 1, 2 and 3 inhibit proliferation of ramified microglia on an astrocyte monolayer Brain Res 795 1998 301 306 (Pubitemid 28337844)
36. 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
37. R. Kiefer, W.J. Streit, K.V. Toyka, G.W. Kreutzberg, and H.P. Hartung Transforming growth factor-beta 1: A lesion-associated cytokine of the nervous system Int J Dev Neurosci 13 1995 331 339
38. D.S. Kim, K.W. Figueroa, K.W. Li, A. Boroujerdi, T. Yolo, and Z.D. Luo Profiling of dynamically changed gene expression in dorsal root ganglia post peripheral nerve injury and a critical role of injury-induced glial fibrillary acidic protein in maintenance of pain behaviors [corrected] Pain 143 2009 114 122
39. P. Kugler, and A. Schmitt Glutamate transporter EAAC1 is expressed in neurons and glial cells in the rat nervous system Glia 27 1999 129 142 (Pubitemid 29365749)
40. R. Kuner Central mechanisms of pathological pain Nat Med 16 2010 1258 1266
41. A.P. Kuruvilla, R. Shah, G.M. Hochwald, H.D. Liggitt, M.A. Palladino, and G.J. Thorbecke Protective effect of transforming growth factor beta 1 on experimental autoimmune diseases in mice Proc Natl Acad Sci U S A 88 1991 2918 2921 (Pubitemid 21916531)
42. A. Latremoliere, and C.J. Woolf Central sensitization: A generator of pain hypersensitivity by central neural plasticity J Pain 10 2009 895 926
43. J.J. Letterio, and A.B. Roberts TGF-beta: A critical modulator of immune cell function Clin Immunol Immunopathol 84 1997 244 250 (Pubitemid 27398023)
44. L. Leung, and C.M. Cahill TNF-alpha and neuropathic pain - A review J Neuroinflammation 7 2010 27
45. Y.C. Lin, S.Y. Huang, Y.H. Jean, W.F. Chen, C.S. Sung, E.S. Kao, H.M. Wang, C. Chakraborty, C.Y. Duh, and Z.H. Wen Intrathecal lemnalol, a natural marine compound obtained from Formosan soft coral, attenuates nociceptive responses and the activity of spinal glial cells in neuropathic rats Behav Pharmacol 22 2011 739 750
46. O.H. Lowry, N.J. Rosebrough, A.L. Farr, and R.J. Randall Protein measurement with the Folin phenol reagent J Biol Chem 193 1951 265 275
47. D.R. Lucas, and J.P. Newhouse The toxic effect of sodium l-glutamate on the inner layers of the retina AMA Arch Ophthalmol 58 1957 193 201
48. M. Ma, Y. Ma, X. Yi, R. Guo, W. Zhu, X. Fan, G. Xu, W.H. Frey 2nd, and X. Liu Intranasal delivery of transforming growth factor-beta1 in mice after stroke reduces infarct volume and increases neurogenesis in the subventricular zone BMC Neurosci 9 2008 117
49. H. Machelska Dual peripheral actions of immune cells in neuropathic pain Arch Immunol Ther Exp (Warsz) 59 2011 11 24
50. M. Makwana, L.L. Jones, D. Cuthill, H. Heuer, M. Bohatschek, M. Hristova, S. Friedrichsen, I. Ormsby, D. Bueringer, A. Koppius, K. Bauer, T. Doetschman, and G. Raivich Endogenous transforming growth factor beta 1 suppresses inflammation and promotes survival in adult CNS J Neurosci 27 2007 11201 11213 (Pubitemid 47621324)
51. M. Marsala, A.B. Malmberg, and T.L. Yaksh The spinal loop dialysis catheter: Characterization of use in the unanesthetized rat J Neurosci Methods 62 1995 43 53
52. J.C. Martinou, A. Le Van Thai, A. Valette, and M.J. Weber Transforming growth factor beta 1 is a potent survival factor for rat embryo motoneurons in culture Brain Res Dev Brain Res 52 1990 175 181 (Pubitemid 20081075)
53. M.L. Mayer, and G.L. Westbrook The physiology of excitatory amino acids in the vertebrate central nervous system Prog Neurobiol 28 1987 197 276 (Pubitemid 17023404)
54. S.B. McMahon, and M. Malcangio Current challenges in glia-pain biology Neuron 64 2009 46 54
55. H. McNeill, C. Williams, J. Guan, M. Dragunow, P. Lawlor, E. Sirimanne, K. Nikolics, and P. Gluckman Neuronal rescue with transforming growth factor-beta 1 after hypoxic-ischaemic brain injury Neuroreport 5 1994 901 904 (Pubitemid 24138094)
56. E.D. Milligan, K.A. O'Connor, K.T. Nguyen, C.B. Armstrong, C. Twining, R.P. Gaykema, A. Holguin, D. Martin, S.F. Maier, and L.R. Watkins Intrathecal HIV-1 envelope glycoprotein gp120 induces enhanced pain states mediated by spinal cord proinflammatory cytokines J Neurosci 21 2001 2808 2819 (Pubitemid 32298222)
57. E.D. Milligan, E.M. Sloane, and L.R. Watkins Glia in pathological pain: A role for fractalkine J Neuroimmunol 198 2008 113 120
58. E.D. Milligan, and L.R. Watkins Pathological and protective roles of glia in chronic pain Nat Rev Neurosci 10 2009 23 36
59. K. Miyoshi, K. Obata, T. Kondo, H. Okamura, and K. Noguchi Interleukin-18-mediated microglia/astrocyte interaction in the spinal cord enhances neuropathic pain processing after nerve injury J Neurosci 28 2008 12775 12787
60. G. Moalem, and D.J. Tracey Immune and inflammatory mechanisms in neuropathic pain Brain Res Rev 51 2006 240 264 (Pubitemid 43902971)
61. Y. Murata, A. Onda, B. Rydevik, I. Takahashi, K. Takahashi, and K. Olmarker Changes in pain behavior and histologic changes caused by application of tumor necrosis factor-alpha to the dorsal root ganglion in rats Spine 31 2006 530 535
62. R.R. Myers, and V.I. Shubayev The ology of neuropathy: An integrative review of the role of neuroinflammation and TNF-alpha axonal transport in neuropathic pain J Peripher Nerv Syst 16 2011 277 286
63. I.A. Napier, S.A. Mohammadi, and M.J. Christie Glutamate transporter dysfunction associated with nerve injury-induced pain in mice J Neurophysiol 107 2012 649 657
64. H. Nie, and H.R. Weng Impaired glial glutamate uptake induces extrasynaptic glutamate spillover in the spinal sensory synapses of neuropathic rats J Neurophysiol 103 2010 2570 2580
65. O'Brien MF, Lenke LG, Lou J, Bridwell KH, Joyce ME: Astrocyte response and transforming growth factor-beta localization in acute spinal cord injury. Spine 19:2321-2329; discussion 2330, 1994.
66. S. Ohtori, K. Takahashi, H. Moriya, and R.R. Myers TNF-alpha and TNF-alpha receptor type 1 upregulation in glia and neurons after peripheral nerve injury: Studies in murine DRG and spinal cord Spine 29 2004 1082 1088 (Pubitemid 38649821)
67. S.M. Park, J.S. Jung, M.S. Jang, K.S. Kang, and S.K. Kang Transforming growth factor-beta1 regulates the fate of cultured spinal cord-derived neural progenitor cells Cell Prolif 41 2008 248 264 (Pubitemid 351367491)
68. J.H. Prehn, C. Backhauss, and J. Krieglstein Transforming growth factor-beta 1 prevents glutamate neurotoxicity in rat neocortical cultures and protects mouse neocortex from ischemic injury in vivo J Cereb Blood Flow Metab 13 1993 521 525 (Pubitemid 23129406)
69. J.H. Prehn, and J. Krieglstein Opposing effects of transforming growth factor-beta 1 on glutamate neurotoxicity Neuroscience 60 1994 7 10 (Pubitemid 24147602)
70. G.J. Prud'homme, and C.A. Piccirillo The inhibitory effects of transforming growth factor-beta-1 (TGF-beta1) in autoimmune diseases J Autoimmun 14 2000 23 42 (Pubitemid 30080536)
71. M.K. Racke, S. Dhib-Jalbut, B. Cannella, P.S. Albert, C.S. Raine, and D.E. McFarlin Prevention and treatment of chronic relapsing experimental allergic encephalomyelitis by transforming growth factor-beta 1 J Immunol 146 1991 3012 3017
72. M.K. Racke, B. Cannella, P. Albert, M. Sporn, C.S. Raine, and D.E. McFarlin Evidence of endogenous regulatory function of transforming growth factor-beta 1 in experimental allergic encephalomyelitis Int Immunol 4 1992 615 620
73. 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 (Pubitemid 36886161)
74. K. Ren, and R. Dubner Neuron-glia crosstalk gets serious: Role in pain hypersensitivity Curr Opin Anaesthesiol 21 2008 570 579
75. J.D. Rothstein, L. Martin, A.I. Levey, M. Dykes-Hoberg, L. Jin, D. Wu, N. Nash, and R.W. Kuncl Localization of neuronal and glial glutamate transporters Neuron 13 1994 713 725 (Pubitemid 24300175)
76. J.D. Rothstein, M. Dykes-Hoberg, C.A. Pardo, L.A. Bristol, L. Jin, R.W. Kuncl, Y. Kanai, M.A. Hediger, Y. Wang, J.P. Schielke, and D.F. Welty Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate Neuron 16 1996 675 686 (Pubitemid 26103145)
77. M. Rowland, and T.N. Tozer Assessment of AUC D. Balado, Clinical Pharmacokinetics: Concepts and Applications 3rd ed. 1995 Lippincott Williams and Wilkins Philadelphia 469 470
78. J.M. Rubio-Perez, and J.M. Morillas-Ruiz A review: Inflammatory process in Alzheimer's disease, role of cytokines Scientific World Journal 2012 2012 756357
79. A. Ruocco, O. Nicole, F. Docagne, C. Ali, L. Chazalviel, S. Komesli, F. Yablonsky, S. Roussel, E.T. MacKenzie, D. Vivien, and A. Buisson A transforming growth factor-beta antagonist unmasks the neuroprotective role of this endogenous cytokine in excitotoxic and ischemic brain injury J Cereb Blood Flow Metab 19 1999 1345 1353 (Pubitemid 30013626)
80. C.Y. Saab, S.G. Waxman, and B.C. Hains Alarm or curse? The pain of neuroinflammation Brain Res Rev 58 2008 226 235
81. J. Sandkuhler Models and mechanisms of hyperalgesia and allodynia Physiol Rev 89 2009 707 758
82. A. Schober, R. Hertel, U. Arumae, L. Farkas, J. Jaszai, K. Krieglstein, M. Saarma, and K. Unsicker Glial cell line-derived neurotrophic factor rescues target-deprived sympathetic spinal cord neurons but requires transforming growth factor-beta as cofactor in vivo J Neurosci 19 1999 2008 2015 (Pubitemid 29133379)
83. J. Scholz, and C.J. Woolf The neuropathic pain triad: Neurons, immune cells and glia Nat Neurosci 10 2007 1361 1368 (Pubitemid 350014681)
84. C. Sommer, C. Schmidt, and A. George Hyperalgesia in experimental neuropathy is dependent on the TNF receptor 1 Exp Neurol 151 1998 138 142 (Pubitemid 28223862)
85. C. Sommer, T. Lindenlaub, P. Teuteberg, M. Schafers, T. Hartung, and K.V. Toyka Anti-TNF-neutralizing antibodies reduce pain-related behavior in two different mouse models of painful mononeuropathy Brain Res 913 2001 86 89 (Pubitemid 32786935)
86. L.S. Sorkin, and C.M. Doom Epineurial application of TNF elicits an acute mechanical hyperalgesia in the awake rat J Peripher Nerv Syst 5 2000 96 100 (Pubitemid 30451711)
87. S.L. Stuesse, W.L. Cruce, J.A. Lovell, D.L. McBurney, and T. Crisp Microglial proliferation in the spinal cord of aged rats with a sciatic nerve injury Neurosci Lett 287 2000 121 124 (Pubitemid 30353062)
88. S.L. Stuesse, T. Crisp, D.L. McBurney, J.B. Schechter, J.A. Lovell, and W.L. Cruce Neuropathic pain in aged rats: Behavioral responses and astrocytic activation Exp Brain Res 137 2001 219 227 (Pubitemid 32250034)
89. 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)
90. R. Suzuki, E.A. Matthews, and A.H. Dickenson Comparison of the effects of MK-801, ketamine and memantine on responses of spinal dorsal horn neurones in a rat model of mononeuropathy Pain 91 2001 101 109 (Pubitemid 32274179)
91. 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 (Pubitemid 32472523)
92. K. Tanaka, K. Watase, T. Manabe, K. Yamada, M. Watanabe, K. Takahashi, H. Iwama, T. Nishikawa, N. Ichihara, T. Kikuchi, S. Okuyama, N. Kawashima, S. Hori, M. Takimoto, and K. Wada Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1 Science 276 1997 1699 1702 (Pubitemid 27421977)
93. F. Tao, W.J. Liaw, B. Zhang, M. Yaster, J.D. Rothstein, R.A. Johns, and Y.X. Tao Evidence of neuronal excitatory amino acid carrier 1 expression in rat dorsal root ganglion neurons and their central terminals Neuroscience 123 2004 1045 1051 (Pubitemid 38130112)
94. 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
95. V.L. Tawfik, M.L. Lacroix-Fralish, K.K. Bercury, N. Nutile-McMenemy, B.T. Harris, and J.A. Deleo Induction of astrocyte differentiation by propentofylline increases glutamate transporter expression in vitro: Heterogeneity of the quiescent phenotype Glia 54 2006 193 203 (Pubitemid 44230856)
96. S. Tilleux, and E. Hermans Neuroinflammation and regulation of glial glutamate uptake in neurological disorders J Neurosci Res 85 2007 2059 2070 (Pubitemid 47172138)
97. R. Vallejo, D.M. Tilley, L. Vogel, and R. Benyamin The role of glia and the immune system in the development and maintenance of neuropathic pain Pain Pract 10 2010 167 184
98. M. Vergeli, B. mazzanti, C. Ballerini, B. Gran, L. Amaducci, and L. Massacesi Transforming growth factor-beta 1 inhibits the proliferation of rat astrocytes induced by serum and growth factors J Neurosci Res 40 1995 127 133
99. D. Vivien, M. Bernaudin, A. Buisson, D. Divoux, E.T. MacKenzie, and A. Nouvelot Evidence of type I and type II transforming growth factor-beta receptors in central nervous tissues: Changes induced by focal cerebral ischemia J Neurochem 70 1998 2296 2304 (Pubitemid 28252355)
100. C.K. Vorwerk, R. Naskar, F. Schuettauf, K. Quinto, D. Zurakowski, G. Gochenauer, M.B. Robinson, S.A. Mackler, and E.B. Dreyer Depression of retinal glutamate transporter function leads to elevated intravitreal glutamate levels and ganglion cell death Invest Ophthalmol Vis Sci 41 2000 3615 3621
101. R. Wagner, and R.R. Myers Endoneurial injection of TNF-alpha produces neuropathic pain behaviors Neuroreport 7 1996 2897 2901 (Pubitemid 26426355)
102. S.M. Wahl Transforming growth factor beta (TGF-beta) in inflammation: A cause and a cure J Clin Immunol 12 1992 61 74
103. S. Wang, G. Lim, L. Yang, B. Sung, and J. Mao Downregulation of spinal glutamate transporter EAAC1 following nerve injury is regulated by central glucocorticoid receptors in rats Pain 120 2006 78 85 (Pubitemid 43078589)
104. X. Wang, W. Chen, W. Liu, J. Wu, Y. Shao, and X. Zhang The role of thrombospondin-1 and transforming growth factor-beta after spinal cord injury in the rat J Clin Neurosci 16 2009 818 821
105. L.R. Watkins, and S.F. Maier Glia: A novel drug discovery target for clinical pain Nat Rev Drug Discov 2 2003 973 985 (Pubitemid 37540579)
106. Z.H. Wen, C.H. Chao, M.H. Wu, and J.H. Sheu A neuroprotective sulfone of marine origin and the in vivo anti-inflammatory activity of an analogue Eur J Med Chem 45 2010 5998 6004
107. H.R. Weng, N. Aravindan, J.P. Cata, J.H. Chen, A.D. Shaw, and P.M. Dougherty Spinal glial glutamate transporters downregulate in rats with taxol-induced hyperalgesia Neurosci Lett 386 2005 18 22 (Pubitemid 41019636)
108. W.D. Willis Role of neurotransmitters in sensitization of pain responses Ann N Y Acad Sci 933 2001 142 156
109. W.J. Xin, H.R. Weng, and P.M. Dougherty Plasticity in expression of the glutamate transporters GLT-1 and GLAST in spinal dorsal horn glial cells following partial sciatic nerve ligation Mol Pain 5 2009 15
110. J.T. Xu, W.J. Xin, Y. Zang, C.Y. Wu, and X.G. Liu The role of tumor necrosis factor-alpha in the neuropathic pain induced by Lumbar 5 ventral root transection in rat Pain 123 2006 306 321
111. Xu L, Huang Y, Yu X, Yue J, Yang N, Zuo P: The influence of p38 mitogen-activated protein kinase inhibitor on synthesis of inflammatory cytokine tumor necrosis factor alpha in spinal cord of rats with chronic constriction injury. Anesth Analg 105:1838-1844, table of contents, 2007 (Pubitemid 350190586)
112. T.L. Yaksh, and T.A. Rudy Chronic catheterization of the spinal subarachnoid space Physiol Behav 17 1976 1031 1036 (Pubitemid 8063691)
113. J.M. Zanella, E.N. Burright, K. Hildebrand, C. Hobot, M. Cox, L. Christoferson, and W.F. McKay Effect of etanercept, a tumor necrosis factor-alpha inhibitor, on neuropathic pain in the rat chronic constriction injury model Spine 33 2008 227 234 (Pubitemid 351322926)
114. Y. Zhu, G.Y. Yang, B. Ahlemeyer, L. Pang, X.M. Che, C. Culmsee, S. Klumpp, and J. Krieglstein Transforming growth factor-beta 1 increases bad phosphorylation and protects neurons against damage J Neurosci 22 2002 3898 3909 (Pubitemid 37465698)
115. 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 (Pubitemid 40279096)
116. 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