Peripheral noxious stimulation reduces withdrawal threshold to mechanical stimuli after spinal cord injury: Role of tumor necrosis factor alpha and apoptosis

Pain

Volumn 155, Issue 11, 2014, Pages 2344-2359

  Garraway, Sandra M ^a   Woller, Sarah A ^a   Huie, J Russell ^b   Hartman, John J ^a   Hook, Michelle A ^a   Miranda, Rajesh C ^c   Huang, Yung Jen ^a   Ferguson, Adam R ^b   Grau, James W ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

Author keywords

Apoptosis; Mechanical allodynia; Nociceptive stimulation; Pain; Spinal cord injury; TNF

Indexed keywords

CASPASE 3; CASPASE 8; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN C JUN; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR 1; TUMOR NECROSIS FACTOR RECEPTOR 2;

ADULT; ALLODYNIA; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BEHAVIOR CHANGE; CELL STRUCTURE; CONTROLLED STUDY; EXPERIMENTAL SPINAL CORD CONTUSION; GENE EXPRESSION; HYPERALGESIA; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; INJURY SEVERITY; MALE; MECHANICAL STIMULATION; MICROGLIA; NERVE CELL; NOCICEPTIVE STIMULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; RAT; SHAM PROCEDURE; SIGNAL TRANSDUCTION; SPINAL CORD INJURY; VON FREY TEST; WITHDRAWAL REFLEX; ANALYSIS OF VARIANCE; ANIMAL; COMPLICATION; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETICS; LOCOMOTION; METABOLISM; PAIN MEASUREMENT; PAIN THRESHOLD; PATHOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT; TIME;

ANALYSIS OF VARIANCE; ANIMALS; APOPTOSIS; CASPASE 3; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; HYPERALGESIA; LOCOMOTION; MALE; MICROGLIA; NEURONS; PAIN MEASUREMENT; PAIN THRESHOLD; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; SPINAL CORD INJURIES; TIME FACTORS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84923530201     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1016/j.pain.2014.08.034     Document Type: Article

References (96)

1. Basso DM, Beattie MS, Bresnahan JC. A sensitive and reliable locomotor rating scale for open field testing in rats. J Neurotrauma 1995;12:1-21.
2. Baumbauer KM, Hoy Jr KC, Huie JR, Hughes AJ, Woller SA, Puga DA, Setlow B, Grau JW. Timing in the absence of supraspinal input I: variable, but not fixed, spaced stimulation of the sciatic nerve undermines spinally-mediated instrumental learning. Neuroscience 2008;155:1030-47.
3. Beattie MS, Ferguson AR, Bresnahan JC. AMPA-receptor trafficking and injuryinduced cell death. Eur J Neurosci 2010;32:290-7.
4. Beattie MS, Hermann GE, Rogers RC, Bresnahan JC. Cell death in models of spinal cord injury. Progr Brain Res 2002;137:37-47.
5. Beg AA, Baltimore D. An essential role for NF-kappaB in preventing TNF-alphainduced cell death. Science 1996;274:782-4.
6. Bethea JR, Castro M, Keane RW, Lee TT, Dietrich WD, Yezierski RP. Traumatic spinal cord injury induces nuclear factor-kappaB activation. J Neurosci 1998;18:3251-60.
7. Botchkina GI, Meistrell III ME, Botchkina IL, Tracey KJ. Expression of TNF and TNF receptors (p55 and p75) in the rat brain after focal cerebral ischemia. Mol Med 1997;3:765-81.
8. Brambilla R, Bracchi-Ricard V, Hu W-H, Frydel B, Bramwell A, Karmally S, Green EJ, Bethea JR. Inhibition of astroglial nuclear factor jB reduces inflammation and improves functional recovery after spinal cord injury. J Exp Med 2005;202:145-56.
9. Carpentier I, Declercq W, Malinin NL, Wallach D, Fiers W, Beyaert R. TRAF2 plays a dual role in NF-kappaB-dependent gene activation by mediating the TNF-induced activation of p38 MAPK and IkappaB kinase pathways. FEBS Lett 1998;425:195-8.
10. Chen G, Goeddel DV. TNF-R1 signaling: A beautiful pathway. Science 2002;296:1634-5.
11. Chen X, Pang RP, Shen KF, Zimmermann M, Xin WJ, Li YY, Liu XG. TNF-alpha enhances the currents of voltage gated sodium channels in uninjured dorsal root ganglion neurons following motor nerve injury. Exp Neurol 2011;227:279-86.
12. Chen YR, Wang X, Templeton D, Davis RJ, Tan TH. The role of c-Jun N-terminal kinase (JNK) in apoptosis induced by ultraviolet C and gamma radiation. Duration of JNK activation may determine cell death and proliferation. J Biol Chem 1996;271:31929-36.
13. Choi JI, Svensson CI, Koehrn FJ, Bhuskute A, Sorkin LS. Peripheral inflammation induces tumor necrosis factor dependent AMPA receptor trafficking and Akt phosphorylation in spinal cord in addition to pain behavior. PAIN- 2010;149:243-53.
14. Christensen MD, Everhart AW, Pickelman JT, Hulsebosch CE. Mechanical and thermal allodynia in chronic central pain following spinal cord injury. PAIN- 1996;68:97-107.
15. Citron BA, Arnold PM, Sebastian C, Qin F, Malladi S, Ameenuddin S, Landis ME, Festoff BW. Rapid upregulation of caspase-3 in rat spinal cord after injury: mRNA, protein, and cellular localization correlates with apoptotic cell death. Exp Neurol 2000;166:213-26.
16. Cleveland JL, Ihle JN. Contenders in FasL/TNF death signaling. Cell 1995;81:479-82.
17. Crowe MJ, Bresnahan JC, Shuman SL, Masters JN, Beattie MS. Apoptosis and delayed degeneration after spinal cord injury in rats and monkeys. Nat Med 1997;3:73-6.
18. Crown ED, Ferguson AR, Joynes RL, Grau JW. Instrumental learning within the spinal cord: IV. Induction and retention of the behavioral deficit observed after noncontingent shock. Behav Neurosci 2002;116:1032-51.
19. Crown ED, Ye Z, Johnson KM, Xu GY, McAdoo DJ, Hulsebosch CE. Increases in the activated forms of ERK 1/2, p38 MAPK, and CREB are correlated with the expression of at-level mechanical allodynia following spinal cord injury. Exp Neurol 2006;199:397-407.
20. De Smaele E, Zazzeroni F, Papa S, Nguyen DU, Jin R, Jones J, Cong R, Franzoso G. Induction of gadd45beta by NF-kappaB downregulates pro-apoptotic JNK signalling. Nature 2001;414:308-13.
21. Deng Y, Ren X, Yang L, Lin Y, Wu X. A JNK-dependent pathway is required for TNFalpha-induced apoptosis. Cell 2003;115:61-70.
22. Detloff MR, Fisher LC, McGaughy V, Longbrake EE, Popovich PG, Basso DM. Remote activation of microglia and pro-inflammatory cytokines predict the onset and severity of below-level neuropathic pain after spinal cord injury in rats. Exp Neurol 2008;212:337-47.
23. Dragunow M, Young D, Hughes P, MacGibbon G, Lawlor P, Singleton K, Sirimanne E, Beilharz E, Gluckman P. Is c-Jun involved in nerve cell death following status epilepticus and hypoxic-ischaemic brain injury? Brain Res Mol Brain Res 1993;18:347-52.
24. Drew GM, Siddall PJ, Duggan AW. Mechanical allodynia following contusion injury of the rat spinal cord is associated with loss of GABAergic inhibition in the dorsal horn. PAIN- 2004;109:379-88.
25. Dubner R, Ruda MA. Activity-dependent neuronal plasticity following tissue injury and inflammation. Trends Neurosci 1992;15:96-103.
26. Estus S, Zaks WJ, Freeman RS, Gruda M, Bravo R, Johnson Jr EM. Altered gene expression in neurons during programmed cell death: identification of c-jun as necessary for neuronal apoptosis. J Cell Biol 1994;127:1717-27.
27. Fairbanks CA, Schreiber KL, Brewer KL, Yu CG, Stone LS, Kitto KF, Nguyen HO, Grocholski BM, Shoeman DW, Kehl LJ, Regunathan S, Reis DJ, Yezierski RP, Wilcox GL. Agmatine reverses pain induced by inflammation, neuropathy, and spinal cord injury. Proc Natl Acad Sci U S A 2000;97:10584-9.
28. Felix ER, Cruz-Almeida Y, Widerstrom-Noga EG. Chronic pain after spinal cord injury: what characteristics make some pains more disturbing than others? J Rehabil Res Dev 2007;44:703-15.
29. Ferguson AR, Christensen RN, Gensel JC, Miller BA, Sun F, Beattie EC, Bresnahan JC, Beattie MS. Cell death after spinal cord injury is exacerbated by rapid TNF alpha-induced trafficking of GluR2-lacking AMPARs to the plasma membrane. J Neurosci 2008;28:11391-400.
30. Ferguson AR, Crown ED, Grau JW. Nociceptive plasticity inhibits adaptive learning in the spinal cord. Neuroscience 2006;141:421-31.
31. Ferguson AR, Huie JR, Crown ED, Baumbauer KM, Hook MA, Garraway SM, Lee KH, Hoy KC, Grau JW. Maladaptive spinal plasticity opposes spinal learning and recovery in spinal cord injury. Front Physiol 2012;3:399.
32. Fontaine V, Mohand-Said S, Hanoteau N, Fuchs C, Pfizenmaier K, Eisel U. Neurodegenerative and neuroprotective effects of tumor necrosis factor (TNF) in retinal ischemia: opposite roles of TNF receptor 1 and TNF receptor 2. J Neurosci 2002;22:RC216.
33. Gangadharan V, Wang R, Ulzhofer B, Luo C, Bardoni R, Bali KK, Agarwal N, Tegeder I, Hildebrandt U, Nagy GG, Todd AJ, Ghirri A, Haussler A, Sprengel R, Seeburg PH, MacDermott AB, Lewin GR, Kuner R. Peripheral calciumpermeable AMPA receptors regulate chronic inflammatory pain in mice. J Clin Invest 2011;121:1608-23.
34. Gao YJ, Xu ZZ, Liu YC, Wen YR, Decosterd I, Ji RR. The c-Jun N-terminal kinase 1 (JNK1) in spinal astrocytes is required for the maintenance of bilateral mechanical allodynia under a persistent inflammatory pain condition. PAIN- 2010;148:309-19.
35. Garraway SM, Petruska JC, Mendell LM. BDNF sensitizes the response of lamina II neurons to high threshold primary afferent inputs. Eur J Neurosci 2003;18:2467-76.
36. Garraway SM, Turtle JD, Huie JR, Lee KH, Hook MA, Woller SA, Grau JW. Intermittent noxious stimulation following spinal cord contusion injury impairs locomotor recovery and reduces spinal brain-derived neurotrophic factor-tropomyosin-receptor kinase signaling in adult rats. Neuroscience 2011;199:86-102.
37. Garraway SM, Xu Q, Inturrisi CE. SiRNA-mediated knockdown of the NR1 subunit gene of the NMDA receptor attenuates formalin-induced pain behaviors in adult rats. J Pain 2009;10:380-90.
38. Grau JW, Huie JR, Garraway SM, Hook MA, Crown ED, Baumbauer KM, Lee KH, Hoy KC, Ferguson AR. Impact of behavioral control on the processing of nociceptive stimulation. Front Physiol 2012;3:262.
39. Grau JW, Washburn SN, Hook MA, Ferguson AR, Crown ED, Garcia G, Bolding KA, Miranda RC. Uncontrollable stimulation undermines recovery after spinal cord injury. J Neurotrauma 2004;21:1795-817.
40. Grell M, Douni E, Wajant H, Lohden M, Clauss M, Maxeiner B, Georgopoulos S, Lesslauer W, Kollias G, Pfizenmaier K, Scheurich P. The transmembrane form of tumor necrosis factor is the prime activating ligand of the 80 kDa tumor necrosis factor receptor. Cell 1995;83:793-802.
41. Gruner JA. A monitored contusion model of spinal cord injury in the rat. J Neurotrauma 1992;9:123-6.
42. Hains BC, Waxman SG. Activated microglia contribute to the maintenance of chronic pain after spinal cord injury. J Neurosci 2006;26:4308-17.
43. Hains BC, Yucra JA, Hulsebosch CE. Reduction of pathological and behavioral deficits following spinal cord contusion injury with the selective cyclooxygenase-2 inhibitor NS-398. J Neurotrauma 2001;18:409-23.
44. Herrero JF, Laird JM, Lopez-Garcia JA. Wind-up of spinal cord neurones and pain sensation: much ado about something? Prog Neurobiol 2000;61:169-203.
45. Hook MA, Huie JR, Grau JW. Peripheral inflammation undermines the plasticity of the isolated spinal cord. Behav Neurosci 2008;122:233-49.
46. Hsu H, Shu HB, Pan MG, Goeddel DV. TRADD-TRAF2 and TRADD-FADD interactions define two distinct TNF receptor 1 signal transduction pathways. Cell 1996;84:299-308.
47. Huie JR, Baumbauer KM, Lee KH, Bresnahan JC, Beattie MS, Ferguson AR, Grau JW. Glial tumor necrosis factor alpha (TNFalpha) generates metaplastic inhibition of spinal learning. PLoS One 2012;7:e39751.
48. Huie JR, Garraway SM, Baumbauer KM, Hoy Jr KC, Beas BS, Montgomery KS, Bizon JL, Grau JW. Brain-derived neurotrophic factor promotes adaptive plasticity within the spinal cord and mediates the beneficial effects of controllable stimulation. Neuroscience 2012;200:74-90.
49. Hummon AB, Lim SR, Difilippantonio MJ, Ried T. Isolation and solubilization of proteins after TRIzol extraction of RNA and DNA from patient material following prolonged storage. Biotechniques 2007;42:472.
50. Jenkins R, Hunt SP. Long-term increase in the levels of c-jun mRNA and jun protein-like immunoreactivity in motor and sensory neurons following axon damage. Neurosci Lett 1991;129:107-10.
51. Jenkins R, McMahon SB, Bond AB, Hunt SP. Expression of c-Jun as a response to dorsal root and peripheral nerve section in damaged and adjacent intact primary sensory neurons in the rat. Eur J Neurosci 1993;5:751-9.
52. Jones TL, Sorkin LS. Calcium-permeable alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid/kainate receptors mediate development, but not maintenance, of secondary allodynia evoked by first-degree burn in the rat. J Pharmacol Exp Ther 2004;310:223-9.
53. Joseph EK, Levine JD. Caspase signalling in neuropathic and inflammatory pain in the rat. Eur J Neurosci 2004;20:2896-902.
54. Kim GW, Copin JC, Kawase M, Chen SF, Sato S, Gobbel GT, Chan PH. Excitotoxicity is required for induction of oxidative stress and apoptosis in mouse striatum by the mitochondrial toxin, 3-nitropropionic acid. J Cereb Blood Flow Metab 2000;20:119-29.
55. Knoblach SM, Huang X, VanGelderen J, Calva-Cerqueira D, Faden AI. Selective caspase activation may contribute to neurological dysfunction after experimental spinal cord trauma. J Neurosci Res 2005;80:369-80.
56. Ledeboer A, Gamanos M, Lai W, Martin D, Maier SF, Watkins LR, Quan N. Involvement of spinal cord nuclear factor kappaB activation in rat models of proinflammatory cytokine-mediated pain facilitation. Eur J Neurosci 2005;22:1977-86.
57. Lee YB, Yune TY, Baik SY, Shin YH, Du S, Rhim H, Lee EB, Kim YC, Shin ML, Markelonis GJ, Oh TH. Role of tumor necrosis factor-alpha in neuronal and glial apoptosis after spinal cord injury. Exp Neurol 2000;166:190-5.
58. Lindsey AE, LoVerso RL, Tovar CA, Hill CE, Beattie MS, Bresnahan JC. An analysis of changes in sensory thresholds to mild tactile and cold stimuli after experimental spinal cord injury in the rat. Neurorehab Neural Repair 2000;14:287-300.
59. Liu XZ, Xu XM, Hu R, Du C, Zhang SX, McDonald JW, Dong HX, Wu YJ, Fan GS, Jacquin MF, Hsu CY, Choi DW. Neuronal and glial apoptosis after traumatic spinal cord injury. J Neurosci 1997;17:5395-406.
60. Liu ZG, Hsu H, Goeddel DV, Karin M. Dissection of TNF receptor 1 effector functions: JNK activation is not linked to apoptosis while NF-kappaB activation prevents cell death. Cell 1996;87:565-76.
61. Maione S, Siniscalco D, Galderisi U, de Novellis V, Uliano R, Di Bernardo G, Berrino L, Cascino A, Rossi F. Apoptotic genes expression in the lumbar dorsal horn in a model neuropathic pain in rat. Neuroreport 2002;13:101-6.
62. Marchetti L, Klein M, Schlett K, Pfizenmaier K, Eisel UL. Tumor necrosis factor (TNF)-mediated neuroprotection against glutamate-induced excitotoxicity is enhanced by N-methyl-D-aspartate receptor activation. Essential role of a TNF receptor 2-mediated phosphatidylinositol 3-kinase-dependent NF-kappa B pathway. J Biol Chem 2004;279:32869-81.
63. Martin LJ, Al-Abdulla NA, Brambrink AM, Kirsch JR, Sieber FE, Portera-Cailliau C. Neurodegeneration in excitotoxicity, global cerebral ischemia, and target deprivation: A perspective on the contributions of apoptosis and necrosis. Brain Res Bull 1998;46:281-309.
64. McAlpine FE, Lee JK, Harms AS, Ruhn KA, Blurton-Jones M, Hong J, Das P, Golde TE, LaFerla FM, Oddo S, Blesch A, Tansey MG. Inhibition of soluble TNF signaling in a mouse model of Alzheimer's disease prevents pre-plaque amyloid-associated neuropathology. Neurobiol Dis 2009;34: 163-77.
65. McCoy MK, Martinez TN, Ruhn KA, Szymkowski DE, Smith CG, Botterman BR, Tansey KE, Tansey MG. Blocking soluble tumor necrosis factor signaling with dominant-negative tumor necrosis factor inhibitor attenuates loss of dopaminergic neurons in models of Parkinson's disease. J Neurosci 2006;26:9365-75.
66. McCoy MK, Tansey MG. TNF signaling inhibition in the CNS: implications for normal brain function and neurodegenerative disease. JNeuroinflamm2008;5:45.
67. Mendell LM. Physiological properties of unmyelinated fiber projection to the spinal cord. Exp Neurol 1966;16:316-32.
68. Mendell LM, Wall PD. Responses of single dorsal cord cells to peripheral cutaneous unmyelinated fibres. Nature 1965;206:97-9.
69. Moore KA, Kohno T, Karchewski LA, Scholz J, Baba H, Woolf CJ. Partial peripheral nerve injury promotes a selective loss of GABAergic inhibition in the superficial dorsal horn of the spinal cord. J Neurosci 2002;22:6724-31.
70. Nesic O, Lee J, Johnson KM, Ye Z, Xu GY, Unabia GC, Wood TG, McAdoo DJ, Westlund KN, Hulsebosch CE, Regino Perez-Polo J. Transcriptional profiling of spinal cord injury-induced central neuropathic pain. J Neurochem 2005;95:998-1014.
71. Rossignol S, Schwab M, Schwartz M, Fehlings MG. Spinal cord injury: time to move? J Neurosci 2007;27:11782-92.
72. Sang CN, Gracely RH, Max MB, Bennett GJ. Capsaicin-evoked mechanical allodynia and hyperalgesia cross nerve territories. Evidence for a central mechanism. Anesthesiology 1996;85:491-6.
73. Schafers M, Sorkin LS, Geis C, Shubayev VI. Spinal nerve ligation induces transient upregulation of tumor necrosis factor receptors 1 and 2 in injured and adjacent uninjured dorsal root ganglia in the rat. Neurosci Lett 2003;347:179-82.
74. Schafers M, Svensson CI, Sommer C, Sorkin LS. Tumor necrosis factor-alpha induces mechanical allodynia after spinal nerve ligation by activation of p38 MAPK in primary sensory neurons. J Neurosci 2003;23:2517-21.
75. Scholz J, Broom DC, Youn DH, Mills CD, Kohno T, Suter MR, Moore KA, Decosterd I, Coggeshall RE, Woolf CJ. Blocking caspase activity prevents transsynaptic neuronal apoptosis and the loss of inhibition in lamina II of the dorsal horn after peripheral nerve injury. J Neurosci 2005;25:7317-23.
76. Sekiguchi M, Sekiguchi Y, Konno S, Kobayashi H, Homma Y, Kikuchi S. Comparison of neuropathic pain and neuronal apoptosis following nerve root or spinal nerve compression. Eur Spine J 2009;18:1978-85.
77. Shu HB, Takeuchi M, Goeddel DV. The tumor necrosis factor receptor 2 signal transducers TRAF2 and c-IAP1 are components of the tumor necrosis factor receptor 1 signaling complex. Proc Natl Acad Sci U S A 1996;93:13973-8.
78. Siddall PJ, Loeser JD. Pain following spinal cord injury. Spinal cord 2001;39:63-73.
79. Simoes AE, Pereira DM, Amaral JD, Nunes AF, Gomes SE, Rodrigues PM, Lo AC, D'Hooge R, Steer CJ, Thibodeau SN, Borralho PM, Rodrigues CM. Efficient recovery of proteins from multiple source samples after TRIzol((R)) or TRIzol((R))LS RNA extraction and long-term storage. BMC Genomics 2013;14:181.
80. Song HY, Regnier CH, Kirschning CJ, Goeddel DV, Rothe M. Tumor necrosis factor (TNF)-mediated kinase cascades: bifurcation of nuclear factor-kappaB and c-jun N-terminal kinase (JNK/SAPK) pathways at TNF receptor-associated factor 2. Proc Natl Acad Sci U S A 1997;94:9792-6.
81. Springer JE, Azbill RD, Knapp PE. Activation of the caspase-3 apoptotic cascade in traumatic spinal cord injury. Nat Med 1999;5:943-6.
82. Stellwagen D, Malenka RC. Synaptic scaling mediated by glial TNF-alpha. Nature 2006;440:1054-9.
83. Sun T, Song WG, Fu ZJ, Liu ZH, Liu YM, Yao SL. Alleviation of neuropathic pain by intrathecal injection of antisense oligonucleotides to p65 subunit of NFkappaB. Br J Anaesth 2006;97:553-8.
84. Tang G, Minemoto Y, Dibling B, Purcell NH, Li Z, Karin M, Lin A. Inhibition of JNK activation through NF-kappaB target genes. Nature 2001;414:313-7.
85. Tweedie D, Ferguson RA, Fishman K, Frankola KA, Van Praag H, Holloway HW, Luo W, Li Y, Caracciolo L, Russo I, Barlati S, Ray B, Lahiri DK, Bosetti F, Greig NH, Rosi S. Tumor necrosis factor-alpha synthesis inhibitor 3,60-dithiothalidomide attenuates markers of inflammation, Alzheimer pathology and behavioral deficits in animal models of neuroinflammation and Alzheimer's disease. J Neuroinflamm 2012;9:106.
86. Van Antwerp DJ, Martin SJ, Kafri T, Green DR, Verma IM. Suppression of TNFalpha-induced apoptosis by NF-kappaB. Science 1996;274:787-9.
87. Wang CY, Mayo MW, Korneluk RG, Goeddel DV, Baldwin AS. NF-kappa B antiapoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation. Science 1998;281:1680-3.
88. West MJ, Slomianka L, Gundersen HJ. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 1991;231:482-97.
89. Willis WD. Long-term potentiation in spinothalamic neurons. Brain Res Rev 2002;40:202-14.
90. Xu J, Fan G, Chen S, Wu Y, Xu XM, Hsu CY. Methylprednisolone inhibition of TNF-a expression and NF-jB activation after spinal cord injury in rats. Mol Brain Res 1998;59:135-42.
91. Xu QH, Garraway SM, Weyerbacher AR, Shin SJ, Inturrisi CE. Activation of the neuronal extracellular signal-regulated kinase 2 in the spinal cord dorsal horn is required for complete Freund's adjuvant-induced pain hypersensitivity. J Neurosci 2008;28:14087-96.
92. Yin HZ, Hsu CI, Yu S, Rao SD, Sorkin LS, Weiss JH. TNF-a triggers rapid membrane insertion of Ca(2+) permeable AMPA receptors into adult motor neurons and enhances their susceptibility to slow excitotoxic injury. Exp Neurol 2012;238:93-102.
93. Zhang AL, Hao JX, Seiger A, Xu XJ, Wiesenfeldhallin Z, Grant G, Aldskogius H. Decreased gaba immunoreactivity in spinal-cord dorsal horn neurons after transient spinal-cord ischemia in the rat. Brain Res 1994;656:187-90.
94. Zhang L, Berta T, Xu ZZ, Liu T, Park JY, Ji RR. TNF-alpha contributes to spinal cord synaptic plasticity and inflammatory pain: distinct role of TNF receptor subtypes 1 and 2. PAIN- 2011;152:419-27.
95. Zhuang ZY, Gerner P, Woolf CJ, Ji RR. ERK is sequentially activated in neurons, microglia, and astrocytes by spinal nerve ligation and contributes to mechanical allodynia in this neuropathic pain model. PAIN- 2005;114:149-59.
96. Zhuang ZY, Wen YR, Zhang DR, Borsello T, Bonny C, Strichartz GR, Decosterd I, Ji RR. 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 2006;26:3551-60.