Propentofylline attenuates allodynia, glial activation and modulates GABAergic tone after spinal cord injury in the rat

Pain

Volumn 138, Issue 2, 2008, Pages 410-422

  Gwak, Young Seob ^a   Crown, Eric D ^a   Unabia, Geda C ^a   Hulsebosch, Claire E ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

Author keywords

Astrocytes; Central neuropathic pain; Glutamic acid decarboxylase; Microglia; Spinal cord injury

Indexed keywords

4 AMINOBUTYRIC ACID; GLUTAMATE DECARBOXYLASE 65; PROPENTOFYLLINE;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; CELL ACTIVATION; CONTROLLED STUDY; DOSE RESPONSE; DRUG MECHANISM; GABAERGIC TRANSMISSION; GLIA CELL; HYPERTROPHY; MALE; MICROGLIA; NERVE EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPINAL CORD DORSAL HORN; SPINAL CORD INJURY;

ANIMALS; GAMMA-AMINOBUTYRIC ACID; MALE; NEUROGLIA; PAIN; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD INJURIES; TIME FACTORS; XANTHINES;

EID: 49049093990     PISSN: 03043959     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pain.2008.01.021     Document Type: Article

References (52)

1. Arriagada O., Constandil L., Hernandez A., Barra R., Soto-Moyano R., and Laurido C. Effects of interleukin-1beta on spinal cord nociceptive transmission in intact and propentofylline-treated rats. Int J Neurosci 117 (2007) 617-625
2. Basso D.M., Beattie M.S., and Bresnahan J.C. A sensitive and reliable locomotor rating scale for open field testing in rats. J Neurotrauma 12 (1995) 1-21
3. Borden L.A. GABA transporter heterogeneity: pharmacology and cellular localization. Neurochem Int 29 (1996) 335-356
4. Broer A., Deitmer J.W., and Broer S. Astroglial glutamine transport by system N is upregulated by glutamate. Glia 48 (2004) 298-310
5. Chaplan S.R., Bach F.W., Pogrel J.W., Chung J.M., and Yaksh T.L. Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 53 (1994) 55-63
6. Chatton J.Y., Pellerin L., and Magistretti P.J. GABA uptake into astrocytes is not associated with significant metabolic cost: implication for brain imaging of inhibitory transmission. PNAS 100 (2003) 12456-12461
7. Choi Y., Yoon Y.W., Na H.S., Kim S.H., and Chung J.M. Behavioral signs of ongoing pain and cold allodynia in a rat model of neuropathic pain. Pain 59 (1994) 369-376
8. Christensen M.D., Everhart A.W., Pickelman J.T., and Hulsebosch C.E. Mechanical and thermal allodynia in chronic central pain following spinal cord injury. Pain 68 (1996) 97-107
9. Christensen M.D., and Hulsebosch C.E. Chronic central pain after spinal cord injury. J Neurotrauma 14 (1997) 517-537
10. Chung J.M., Surmeier D.J., Lee D.J., Sorkin L.S., Honda C.N., Tsong Y., et al. Classification of primate spinothalamic and somatosensory thalamic neurons based on cluster analysis. J Neurophysiol 56 (1986) 308-327
11. Colburn R.W., Rickman A.J., and DeLeo J.A. The effect of site and type nerve injury on spinal glial activation and neuropathic pain behavior. Exp Neurol 157 (1999) 289-304
12. Crown E.D., Ye Z., Johnson K.M., Xu G.Y., McAdoo D.J., and Hulsebosch C.E. 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 199 (2006) 397-407
13. Crown E.D., Ye Z., Johnson K.M., Xu G.Y., McAdoo D.J., Westlund K.N., et al. Upregulation of the phosphorylated form of CREB in spinothalamic tract cells following spinal cord injury: relation to central neuropathic pain. Neurosci Lett 384 (2005) 139-144
14. DeLeo J., Toth L., Schubert P., Rudolphi K., and Kreutzberg G.W. Ischemia-induced neuronal cell death, calcium accumulation, and glial response in the hippocampus of the Mongolian gerbil and protection by propentofylline (HWA 285). J Cereb Blood Flow Metab 7 (1987) 745-751
15. DeLeo J.A., and Yezierski R.P. The role of neuroinflammation and neuroimmune activation in persistent pain. Pain 90 (2001) 1-6
16. Dixon W.J. Efficient analysis of experimental observations. Ann Rev Pharmacol Toxicol 20 (1980) 441-462
17. Drew G.M., Siddall P.J., and Duggan A.W. Mechanical allodynia following contusion injury of the rat spinal cord is associated with loss of GABAergic inhibition in the dorsal horn. Pain 109 (2004) 379-388
18. Erlander M.G., Tillakaratne N.J., Feldblum S., Patel N., and Tobin A.J. Two genes encode distinct glutamate decarboxylases. Neuron 7 (1991) 91-100
19. Garry E.M., Delaney A., Blackburn-Munro G., Dickinson T., Moss A., Nakalembe I., et al. Activation of p38 and p42/44 MAP kinase in neuropathic pain: involvement of VPAC2 and NK2 receptors and mediation by spinal glia. Mol Cell Neurosci 30 (2005) 523-537
20. Grossman S.D., Rosenberg L.J., and Wrathall J.R. Relationship of altered glutamate receptor subunit mRNA expression to acute cell loss after spinal cord contusion. Exp Neurol 168 (2001) 283-289
21. Gwak Y.S., Nam T.S., Paik K.S., Hulsebosch C.E., and Leem J.W. Attenuation of mechanical hyperalgesia following spinal cord injury by administration of antibodies to nerve growth factor in the rat. Neurosci Lett 336 (2003) 117-120
22. Gwak Y.S., and Hulsebosch C.E. Inhibition of astrocytic activation prevents induction and maintenance of central neuropathic pain following spinal cord injury in rat. J Neurotrauma 21 (2004) 1283
23. Gwak Y.S., and Hulsebosch C.E. Upregulation of group I metabotropic glutamate receptors in neurons and astrocytes in the dorsal horn following spinal cord injury. Exp Neurol 195 (2005) 236-243
24. Gwak Y.S., Tan H.Y., Nam T.S., Paik K.S., Hulsebosch C.E., and Leem J.W. Activation of spinal GABA receptors attenuates chronic central neuropathic pain after spinal cord injury. J Neurotrauma 23 (2006) 1111-1124
25. Gwak Y., Unabia G., and Hulsebosch C. Activation of neuronal, not glial, p-38 MAPK maintains hyperexcitability of dorsal horn neurons at caudal region following spinal cord injury in rat. Soc Neurosci Abstr (2007) 286.9/KK13
26. Hains B.C., Everhart A.W., Fullwood S.D., and Hulsebosch C.E. Changes in serotonin, serotonin transporter expression and serotonin denervation supersensitivity: involvement in chronic central pain after spinal hemisection in the rat. Exp Neurol 175 (2002) 347-362
27. Hains B.C., and Waxman S.G. Activated microglia contribute to the maintenance of chronic pain after spinal cord injury. J Neurosci 26 (2006) 4308-4317
28. Hulsebosch C.E. Recent advances in pathophysiology and treatment of spinal cord injury. Adv Physiol Educ 26 (2002) 238-255
29. Hulsebosch C.E. From discovery to clinical trials: treatment strategies for central neuropathic pain after spinal cord injury. Curr Pharm Des 11 (2005) 1411-1420
30. Hwang J.H., and Yaksh T.L. The effect of spinal GABA receptor agonist on tactile allodynia in a surgically-induced neuropathic pain model in the rat. Pain 70 (1997) 15-22
31. Koriyama Y., Chiba K., and Mohri T. Propentofylline protects (β-amyloid protein-induced apoptosis in cultured rat hippocampal neurons. Eur J Pharm 458 (2003) 235-241
32. Liu J., Wolfe D., Hao S., Huang S., Glorioso J.C., Mata M., et al. Peripherally delivered glutamic acid decarboxylase gene therapy for spinal cord injury pain. Mol Ther 10 (2004) 57-66
33. Mackie M., Hughes D.I., Maxwell D.J., Tillakaratne N.J., and Todd A.J. Distribution and colocalisation of glutamate decarboxylase isoforms in the rat spinal cord. Neuroscience 119 (2003) 461-472
34. Milligan E.D., Twining C., Chacur M., Biedenkapp J., O'Conner K., Poole S., et al. Spinal glia and proinflammatory cytokines mediate mirror-image neuropathic pain in rats. J Neurosci 23 (2003) 1026-1040
35. Mills C.D., and Hulsebosch C.E. Increased expression of metabotropic glutamate receptor subtype 1 on spinothalamic tract neurons following spinal cord injury in the rat. Neurosci Lett 319 (2002) 59-62
36. Moore K.A., Kohno T., Karchewski L.A., Scholz J., Baba H., and Woolf C.J. Partial peripheral nerve injury promotes a selective loss of GABAergic inhibition in the superficial dorsal horn of the spinal cord. J Neurosci 22 (2002) 6724-6731
37. Nesic O., Lee J., Johnson K.M., Ye Z., Xu G.Y., Unabia G.C., et al. Transcriptional profiling of spinal cord injury-induced central neuropathic pain. J Neurochem 95 (2005) 998-1014
38. Peng X.M., Zhou Z.G., Glorioso J.C., Fink D.J., and Mata M. Tumor necrosis factor-alpha contributes to below-level neuropathic pain after spinal cord injury. Ann Neurol 59 (2006) 843-851
39. Raghavendra V., Tanga F., and DeLeo J.A. 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
40. Scholz J., Broom D.C., Youn D.H., Mills C.D., Kohno T., Suter M.R., et al. 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 25 (2005) 7317-7323
41. Schousboe W., Sarup A., Larsson O.M., and White H.S. GABA transporters as drug targets for modulation of GABAergic activity. Biochem Pharmacol 68 (2004) 1557-1563
42. Schousboe A., Westergaard N., Sonnewald U., Petersen S.B., Huang R., Peng L., et al. Glutamate and glutamine metabolism and compartmentation in astrocytes. Dev Neurosci 15 (1993) 359-366
43. Struzynska L., and Sulkowski G. Relationships between glutamine, glutamate, and GABA in nerve endings under Pb-toxicity conditions. J Inorg Biochem 98 (2004) 951-958
44. Sweitzer S.M., Schubert P., and Deleo J.A. Propentophylline, a glial modulating agent, exhibits antiallodynic properties in a rat model of neuropathic pain. J Pharmacol Exp Ther 297 (2001) 1210-1217
45. Tawfik V.L., Nutile-McMenemy N., LaCroix-Fralish M.L., and DeLeo J.A. Efficacy of propentofylline, a glial modulating agent, on existing mechanical allodynia following peripheral nerve injury. Brain Behav Immun 21 (2007) 238-246
46. Vera-Portocarrero L.P., Mills C.D., Ye Z., Fullwood S.D., McAdoo D.J., and Hulsebosch C.E. Rapid changes in expression of glutamate transporters after spinal cord injury. Brain Res 927 (2002) 104-110
47. Vincler M., Maixner W., Vierck Jr. C.J., and Light A.R. Effects of systemic morphine on escape latency and a hindlimb reflex response in the rat. J Pain 2 (2001) 83-90
48. Watkins L.R., Milligan E.D., and Maier S.F. Spinal cord glia: new players in pain. Pain 93 (2001) 201-205
49. Woolf C.J. Long term alterations in the excitability of the flexion reflex produced by peripheral tissue injury in the chronic decerebrate rat. Pain 18 (1984) 325-343
50. Zhang A.L., Hao J.X., Seiger A., Xu X.J., Wiesenfeld-Hallin Z., Grant G., et al. Decreased GABA immunoreactivity in spinal cord dorsal horn neurons after transient spinal cord ischemic in the rat. Brain Res 656 (1994) 187-190
51. 2 contributes to pain after spinal cord injury. J Neurosci 27 (2007) 2357-2368
52. Zhuang Z.Y., Gerner P., Woolf C.J., and Ji R.R. 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