Calcium/calmodulin dependent kinase II contributes to persistent central neuropathic pain following spinal cord injury

Pain

Volumn 153, Issue 3, 2012, Pages 710-721

  Crown, Eric D ^a   Gwak, Young S ^a   Ye, Zaiming ^a   Yu Tan, Huai ^a   Johnson, Kathia M ^a   Xu, Guo Ying ^a   McAdoo, David J ^a   Hulsebosch, Claire E ^a  

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

Author keywords

CaMKII; Central neuropathic pain; Electrophysiology; Immunocytochemistry; Mechanical allodynia; Western immunoblot test

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; N [2 [[N [3 (4 CHLOROPHENYL) 2 PROPENYL] N METHYLAMINO]METHYL]PHENYL] N (2 HYDROXYETHYL) 4 METHOXYBENZENESULFONAMIDE;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRUSH BORDER; CELL ACTIVITY; CHRONIC PAIN; CONTROLLED STUDY; CONTUSION; MALE; MICROGLIA; NERVE CELL; NEUROPATHIC PAIN; NONHUMAN; OLIGODENDROGLIA; PRESSURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SHAM PROCEDURE; SPINAL CORD DORSAL HORN; SPINAL CORD INJURY; SPINOTHALAMIC TRACT; UPREGULATION;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; ANTIGENS, CD11B; BENZYLAMINES; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; GENE EXPRESSION REGULATION; GLIAL FIBRILLARY ACIDIC PROTEIN; HYPERALGESIA; MALE; NEURALGIA; PAIN MEASUREMENT; POSTERIOR HORN CELLS; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD; SPINAL CORD INJURIES; STILBAMIDINES; SULFONAMIDES; TIME FACTORS;

EID: 84857357969     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1016/j.pain.2011.12.013     Document Type: Article

References (60)

1. N. Attal, F. Guirimand, L. Brasseur, V. Gaude, M. Chauvin, and D. Bouhassira Effects of IV morphine in central pain: a randomized placebo-controlled study Neurology 58 2002 554 563 (Pubitemid 34164936)
2. E. Belanger, and A.D. Levi The acute and chronic management of spinal cord injury J Am Coll Surg 190 2000 603 618 (Pubitemid 30230708)
3. R. Bourtchuladze, B. Frenguelli, J. Blendy, D. Cioffi, G. Schutz, and A.J. Silva Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein Cell 79 1994 59 68
4. I.D. Capel, H.M. Dorrell, E.P. Spencer, and M.W. Davis The amelioration of the suffering associated with spinal cord injury with subperception transcranial electrical stimulation Spinal Cord 41 2003 109 117 (Pubitemid 36174219)
5. D.D. Cardenas, C.A. Warms, J.A. Turner, H. Marshall, M.M. Brooke, and J.D. Loeser Efficacy of amitriptyline for relief of pain in spinal cord injury: results of a randomized controlled trial Pain 96 2002 365 373 (Pubitemid 34327885)
6. S.S. Choi, Y.J. Seo, M.S. Kwon, E.J. Shim, J.Y. Lee, Y.O. Ham, H.K. Lee, and H.W. Suh Increase of phosphorylation of calcium/calmodulin-dependent protein kinase-II in several brain regions by substance P administered intrathecally in mice Brain Res Bull 65 2005 375 381
7. M.D. Christensen, and C.E. Hulsebosch Chronic central pain after spinal cord injury J Neurotrauma 14 1997 517 537 (Pubitemid 27377660)
8. J.M. Chung, D.J. Surmeier, D.J. Lee, L.S. Sorkin, C.N. Honda, Y. Tsong, and W.D. Willis Classification of primate spinothalamic and somatosensory thalamic neurons based on cluster analysis J Neurophysiol 56 1986 308 327 (Pubitemid 16012451)
9. R.J. Colbran Targeting of calcium/calmodulin-dependent protein kinase II Biochem J 378 2004 1 16 (Pubitemid 38299538)
10. E.D. Crown, Y.S. Gwak, Z. Ye, K.M. Johnson, and C.E. Hulsebosch Activation of p38 MAP kinase is involved in central neuropathic pain following spinal cord injury Exp Neurol 213 2008 257 267
11. E.D. Crown, Z. Ye, K.M. Johnson, G.Y. Xu, D.J. McAdoo, and C.E. Hulsebosch 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 (Pubitemid 43928968)
12. E.D. Crown, Z. Ye, K.M. Johnson, G.Y. Xu, D.J. McAdoo, K.N. Westlund, and C.E. Hulsebosch 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 (Pubitemid 40826633)
13. 2+/calmodulin-dependent protein kinase II in the spinal cord contributes to neuropathic pain in a rat model of mononeuropathy Eur J Neurosci 21 2005 2467 2474 (Pubitemid 40813928)
14. P.K. Dash, B. Hochner, and E.R. Kandel Injection of the cAMP-responsive element into the nucleus of Aplysia sensory neurons blocks long-term facilitation Nature 345 1990 718 721
15. T.A. Dyson-Hudson, S.C. Shiflett, S.C. Kirshblum, J.E. Bowen, and E.L. Druin Acupuncture and Trager psychophysical integration in the treatment of wheelchair user's shoulder pain in individuals with spinal cord injury Arch Phys Med Rehabil 82 2001 1038 1046 (Pubitemid 32744329)
16. L. Fang, J. Wu, Q. Lin, and W.D. Willis Calcium-calmodulin-dependent protein kinase II contributes to spinal cord central sensitization J Neurosci 22 2002 4196 4204 (Pubitemid 37465726)
17. L. Fang, J. Wu, X. Zhang, Q. Lin, and W.D. Willis Calcium/calmodulin dependent protein kinase II regulates the phosphorylation of cyclic AMP-responsive element-binding protein of spinal cord in rats following noxious stimulation Neurosci Lett 374 2005 1 4 (Pubitemid 41556536)
18. N.B. Finnerup, F. Biering-Sørensen, I.L. Johannesen, A.J. Terkelsen, G.I. Juhl, A.D. Kristensen, S.H. Sindrup, F.W. Bach, and T.S. Jensen Intravenous lidocaine relieves spinal cord injury pain: a randomized controlled trial Anesthesiology 102 2005 1023 1030 (Pubitemid 40586545)
19. N.B. Finnerup, H. Gottrup, and T.S. Jensen Anticonvulsants in central pain Expert Opin Pharmacother 3 2002 1411 1420 (Pubitemid 35174873)
20. A. Galan, J.M. Laird, and F. Cervero In vivo recruitment by painful stimuli of AMPA receptor subunits to the plasma membrane of spinal cord neurons Pain 112 2004 315 323 (Pubitemid 39550732)
21. Y.S. Gwak, E.D. Crown, G.C. Unabia, and C.E. Hulsebosch Profentofylline attenuates allodynia, glial activation and modulates GABAergic tone after spinal cord injury in the rat Pain 138 2008 410 422
22. Gwak YS, Hassler SN, Hulsebosch CE. Reactive oxygen species modulate central neuropathic pain following spinal cord injury [abstract 80.9/TT15]. Presented at 40th annual meeting for society for neuorscience, November 13-17, San Diego, CA, USA; 2010.
23. 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)
24. B.C. Hains, W.D. Willis, and C.E. Hulsebosch Serotonin receptors 5-HT1A and 5-HT3 reduce hyperexcitability of dorsal horn neurons after chronic spinal cord hemisection injury in rat Exp Brain Res 149 2003 174 186 (Pubitemid 36315367)
25. A.L. Hicks, K.A. Martin, D.S. Ditor, A.E. Latimer, C. Craven, J. Bugaresti, and N. McCartney Long-term exercise training in persons with spinal cord injury: effects on strength, arm ergometry performance and psychological well-being Spinal Cord 41 2003 34 43 (Pubitemid 36132541)
26. C.E. Hulsebosch, B.C. Hains, E.D. Crown, and S.M. Carlton Mechanisms of chronic central neuropathic pain after spinal cord injury Brain Res Rev 60 2009 202 213
27. C.E. Hulsebosch From discovery to clinical trials: treatment strategies for central neuropathic pain after spinal cord injury Curr Pharm Des 11 2005 1411 1420 (Pubitemid 40590189)
28. R.R. Ji, T. Kohno, K.A. Moore, and C.J. Woolf Central sensitization and LTP: do pain and memory share similar mechanisms? Trends Neurosci 26 2003 696 705 (Pubitemid 37415022)
29. R.R. Ji, and F. Rupp Phosphorylation of transcription factor CREB in rat spinal cord after formalin-induced hyperalgesia: relationship to c-fos induction J Neurosci 17 1997 1776 1785 (Pubitemid 27089822)
30. K. Kitamura, M. Kanasashi, C. Suga, S. Saito, S. Yoshida, and Z. Ikezawa Cutaneous reactions induced by calcium channel blocker: high frequency of psoriasiform eruptions J Dermatol 20 1993 279 286 (Pubitemid 23205539)
31. 2+/calmodulin-dependent protein kinase II at spinal nociceptive synapses after acute noxious stimulation J Neurosci 26 2006 4198 4205 (Pubitemid 44315379)
32. R. Levi, C. Hultling, and A. Seiger The Stockholm Spinal Cord Injury Study: 2. Associations between clinical patient characteristics and post-acute medical problems Paraplegia 33 1995 585 594
33. D. Liu, W. Thangnipon, and D.J. McAdoo Excitatory amino acids rise to toxic levels upon impact injury to the rat spinal cord Brain Res 547 1991 344 348
34. W. Ma, and R. Quirion Increased phosphorylation of cyclic AMP response element-binding protein (CREB) in the superficial dorsal horn neurons following partial sciatic nerve ligation Pain 93 2001 295 301 (Pubitemid 32763186)
35. R.C. Malenka, and R.A. Nicoll Long-term potentiation - a decade of progress? Science 285 1999 1870 1874
36. D.J. Messersmith, D.J. Kim, and M.J. Iadarola Transcription factor regulation of prodynorphin gene expression following rat hindpaw inflammation Brain Res Mol Brain Res 53 1998 260 269
37. G. Miletic, M.T. Pankratz, and V. Miletic Increases in the phosphorylation of cyclic AMP response element binding protein (CREB) and decreases in the content of calcineurin accompany thermal hyperalgesia following chronic constriction injury in rats Pain 99 2002 493 500 (Pubitemid 35284281)
38. C.D. Mills, and C.E. Hulsebosch 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 (Pubitemid 34127931)
39. C.D. Mills, K.M. Johnson, and C.E. Hulsebosch Group I metabotropic glutamate receptors in spinal cord injury: roles in neuroprotection and the development of chronic central pain J Neurotrauma 19 2002 23 42 (Pubitemid 34117094)
40. T. Miyabe, and V. Miletic Multiple kinase pathways mediate the early sciatic ligation-associated activation of CREB in the rat spinal dorsal horn Neurosci Lett 381 2005 80 85 (Pubitemid 40693146)
41. K. Obata, H. Yamanaka, K. Kobayashi, Y. Dai, T. Mizushima, H. Katsura, T. Fukuoka, A. Tokunaga, and K. Noguchi Role of mitogen-activated protein kinase activation in injured and intact primary afferent neurons for mechanical and heat hypersensitivity after spinal nerve ligation J Neurosci 24 2004 10211 10212
42. G. Paxinos, and G. Watson The rat brain in stereotaxic coordinates 3rd ed 1997 Academic Press New York
43. J. Sandkuhler Learning and memory in pain pathways Pain 88 2000 113 118
44. P.J. Siddall, M. Gray, S. Rutkowski, and M.J. Cousins Intrathecal morphine and clonidine in the management of spinal cord injury pain: a case report Pain 59 1994 147 148 (Pubitemid 24311181)
45. P. Siddall, R. Yezierski, and J. Loeser Pain following spinal cord injury: clinical features, prevalence, and taxonomy IASP Newsl 3 2000 3 7
46. P.J. Siddall, and J.D. Loeser Pain following spinal cord injury Spinal Cord 39 2001 63 73 (Pubitemid 32229131)
47. T.R. Soderling, and V.A. Derkach Postsynaptic protein phosphorylation and LTP Trends Neurosci 23 2000 75 80 (Pubitemid 30084764)
48. D.P. Stirling, K. Khodarahmi, J. Liu, L.T. McPhail, C.B. McBride, J.D. Steeves, M.S. Ramer, and W. Tetzlaff Minocycline treatment reduces delayed oligodendrocyte death, attenuates axonal dieback, and improves functional outcome after spinal cord injury J Neurosci 24 2004 2182 2190 (Pubitemid 38314550)
49. Y.G. Suh, and U. Oh Activation and activators of TRPV1 and their pharmaceutical implication Curr Pharm Des 11 2005 2687 2698 (Pubitemid 41051878)
50. Tan H, Johnson KM, Hulsebosch CE. Role of ionotropic glutamate receptors in a rodent model of central neuropathic pain [abstract 34]. Presented at 34th annual meeting for society for neuroscience, October 23-27, San Diego, CA, USA; 2004.
51. M. Vincler, W. Maixner, C.J. Vierck Jr, and A.R. Light Effects of systemic morphine on escape latency and a hindlimb reflex response in the rat J Pain 2 2001 83 90 (Pubitemid 32295072)
52. D.T. Wade, P. Robson, H. House, P. Makela, and J. Aram A preliminary controlled study to determine whether whole-plant cannabis extracts can improve intractable neurogenic symptoms Clin Rehabil 17 2003 21 29 (Pubitemid 36230977)
53. J.E. Wells, T.K. Rice, R.K. Nuttall, D.R. Edwards, H. Zekki, S. Rivest, and V.W. Yong An adverse role for matrix metalloproteinase 12 after spinal cord injury in mice J Neurosci 23 2003 10107 10115 (Pubitemid 37392558)
54. E.G. Widerstrom-Noga, R. Duncan, E. Felipe-Cuervo, and C. Turk Assessment of the impact of pain and impairments associated with spinal cord injuries Arch Phys Med Rehabil 83 2002 395 404 (Pubitemid 34204823)
55. W.D. Willis Jr Long term potentiation in spinothalamic neurons Brain Res Brain Res Rev 40 2002 202 214
56. W.D. Willis Jr, and R.E. Coggeshall Sensory mechanisms of the spinal cord 3rd ed 2004 Plenum New York
57. C.J. Woolf 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 (Pubitemid 14129546)
58. J. Wu, L. Fang, Q. Lin, and W.D. Willis Jr The role of nitric oxide in the phosphorylation of cyclic adenosine monophosphate-responsive element-binding protein in the spinal cord after intradermal injection of capsaicin J Pain 3 2002 190 198 (Pubitemid 34663607)
59. C.G. Yu, and R.P. Yezierski Activation of the ERK1/2 signaling cascade by excitotoxic spinal cord injury Brain Res Mol Brain Res 138 2005 244 255 (Pubitemid 41138044)
60. K.P. Zeitz, K.P. Giese, A.J. Silva, and A.I. Basbaum The contribution of autophosphorylated alpha-calcium-calmodulin kinase II to injury-induced persistent pain Neuroscience 128 2004 889 898 (Pubitemid 39302631)