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

Journal of Neuroscience

Volumn 26, Issue 13, 2006, Pages 3551-3560

  Zhuang, Zhi Ye ^a   Wen, Yeong Ray ^a,b   Zhang, De Ren ^a   Borsello, Tiziana ^c   Bonny, Christophe ^c,d   Strichartz, Gary R ^a   Decosterd, Isabelle ^c,e   Ji, Ru Rong ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b SHIN KONG WU HO SU MEMORIAL HOSPITAL   (Taiwan)

^c UNIVERSITY OF LAUSANNE   (Switzerland)

^d UNIVERSITY OF LAUSANNE   (Switzerland)

^e LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

Dorsal root ganglion; Glia; MAP kinase; Nerve injury; Neuropathy; Spinal cord

Indexed keywords

2 AMINOADIPIC ACID; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; GREEN FLUORESCENT PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; STRESS ACTIVATED PROTEIN KINASE INHIBITOR;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; CONTROLLED STUDY; DRUG POTENCY; ENZYME ACTIVATION; MALE; MICROGLIA; NERVE LIGATION; NEUROPATHIC PAIN; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SENSORY NERVE CELL; SPINAL CORD; SPINAL NERVE;

ANIMALS; ASTROCYTES; ENZYME ACTIVATION; GANGLIA, SPINAL; HYPERALGESIA; MALE; MAP KINASE KINASE 4; NEURALGIA; NEURONS, AFFERENT; PEPTIDES; RATS; RATS, SPRAGUE-DAWLEY; SPINAL NERVES;

EID: 33645460235     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5290-05.2006     Document Type: Article

References (49)

1. Abbadie C, Lindia JA, Cumiskey AM, Peterson LB, Mudgett JS, Bayne EK, DeMartino JA, MacIntyre DE, Forrest MJ (2003) Impaired neuropathic pain responses in mice lacking the chemokine receptor CCR2. Proc Natl Acad Sci USA 100:7947-7952.
2. Borsello T, Bonny C (2004) Use of cell-permeable peptides to prevent neuronal degeneration. Trends Mol Med 10:239-244.
3. Borsello T, Clarke PG, Hirt L, Vercelli A, Repici M, Schorderet DF, Bogousslavsky J, Bonny C (2003) A peptide inhibitor of c-Jun N-terminal kinase protects against excitotoxicity and cerebral ischemia. Nat Med 9:1180-1186.
4. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL (1994) Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 53:55-63.
5. Coggeshall RE, Lekan HA (1996) Methods for determining numbers of cells and synapses: a case for more uniform standards of review. J Comp Neurol 364:6-15.
6. Coull JA, Beggs S, Boudreau D, Boivin D, Tsuda M, Inoue K, Gravel C, Salter MW, De Koninck Y (2005) BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain. Nature 438:1017-1021.
7. DeLeo JA, Yezierski RP (2001) The role of neuroinflammation and neuroimmune activation in persistent pain. Pain 90:1-6.
8. DeLeo JA, Tanga FY, Tawfik VL (2004) Neuroimmune activation and neuroinflammation in chronic pain and opioid tolerance/hyperalgesia. The Neuroscientist 10:40-52.
9. Gardell LR, Wang R, Ehrenfels C, Ossipov MH, Rossomando AJ, Miller S, Buckley C, Cai AK, Tse A, Foley SF, Gong B, Walus L, Carmillo P, Worley D, Huang C, Engber T, Pepinsky B, Cate RL, Vanderah TW, Lai J, et al. (2003) Multiple actions of systemic artemin in experimental neuropathy. Nat Med 9:1383-1389.
10. Garrison CJ, Dougherty PM, Carlton SM (1994) GFAP expression in lumbar spinal cord of naive and neuropathic rats treated with MK-801. Exp Neurol 129:237-243.
11. Hofstetter CP, Holmstrom NA, Lilja JA, Schweinhardt P, Hao J, Spenger C, Wiesenfeld-Hallin Z, Kurpad SN, Frisen J, Olson L (2005) Allodynia limits the usefulness of intraspinal neural stem cell grafts; directed differentiation improves outcome. Nat Neurosci 8:346-353.
12. Hokfelt T, Zhang X, Wiesenfeld-Hallin Z (1994) Messenger plasticity in primary sensory neurons following axotomy and its functional implications. Trends Neurosci 17:22-30.
13. Honore P, Rogers SD, Schwei MJ, Salak-Johnson JL, Luger NM, Sabino MC, Clohisy DR, Mantyh PW (2000) Murine models of inflammatory, neuropathic and cancer pain each generates a unique set of neurochemical changes in the spinal cord and sensory neurons. Neuroscience 98:585-598.
14. Huck S, Grass F, Hortnagl H (1984) The glutamate analogue α-aminoadipic acid is taken up by astrocytes before exerting its gliotoxic effect in vitro. J Neurosci 4:2650-2657.
15. Ip YT, Davis RJ (1998) Signal transduction by the c-Jun N-terminal kinase (JNK): from inflammation to development. Curr Opin Cell Biol 10:205-219.
16. Ji RR, Strichartz G (2004) Cell signaling and the genesis of neuropathic pain. Sci STKE 2004:reE14.
17. Ji RR, Woolf CJ (2001) Neuronal plasticity and signal transduction in nociceptive neurons: implications for the initiation and maintenance of pathological pain. Neurobiol Dis 8:1-10.
18. Ji RR, Zhang Q, Law PY, Low HH, Elde R, Hokfelt T (1995) Expression of μ-, δ-, and κ-opioid receptor-like immunoreactivities in rat dorsal root ganglia after carrageenan-induced inflammation. J Neurosci 15:8156-8166.
19. Ji RR, Zhang Q, Pettersson RF, Hokfelt T (1996) aFGF, bFGF and NGF differentially regulate neuropeptide expression in dorsal root ganglia after axotomy and induce autotomy. Regul Pept 66:179-189.
20. Ji RR, Befort K, Brenner GJ, Woolf CJ (2002a) ERK MAP kinase activation in superficial spinal cord neurons induces prodynorphin and NK-1 upregulation and contributes to persistent inflammatory pain hypersensitivity. J Neurosci 22:478-485.
21. Ji RR, Samad TA, Jin SX, Schmoll R, Woolf CJ (2002b) p38 MAPK activation by NGF in primary sensory neurons after inflammation increases TRPV1 levels and maintains heat hyperalgesia. Neuron 36:57-68.
22. Jin SX, Zhuang ZY, Woolf CJ, Ji RR (2003) 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 23:4017-4022.
23. Khurgel M, Koo AC, Ivy GO (1996) Selective ablation of astrocytes by intracerebral injections of alpha-aminoadipate. Glia 16:351-358.
24. Kim SH, Chung JM (1992) An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 50:355-363.
25. Kim SY, Bae JC, Kim JY, Lee HL, Lee KM, Kim DS, Cho HJ (2002) Activation of p38 MAP kinase in the rat dorsal root ganglia and spinal cord following peripheral inflammation and nerve injury. NeuroReport 13:2483-2486.
26. Kuan CY, Whitmarsh AJ, Yang DD, Liao G, Schloemer AJ, Dong C, Bao J, Banasiak KJ, Haddad GG, Flavell RA, Davis RJ, Rakic P (2003) A critical role of neural-specific JNK3 for ischemic apoptosis. Proc Natl Acad Sci USA 100:15184-15189.
27. Ma W, Quirion R (2002) Partial sciatic nerve ligation induces increase in the phosphorylation of extracellular signal-regulated kinase (ERK) and c-Jun N-terminal kinase (JNK) in astrocytes in the lumbar spinal dorsal horn and the gracile nucleus. Pain 99:175-184.
28. Mantyh PW, Clohisy DR, Koltzenburg M, Hunt SP (2002) Molecular mechanisms of cancer pain. Nat Rev Cancer 2:201-209.
29. Migheli A, Piva R, Atzori C, Troost D, Schiffer D (1997) c-Jun, JNK/SAPK kinases and transcription factor NF-kappa B are selectively activated in astrocytes, but not motor neurons, in amyotrophic lateral sclerosis. J Neuropathol Exp Neurol 56:1314-1322.
30. Molander C, Xu Q, Grant G (1984) The cytoarchitectonic organization of the spinal cord in the rat. I. The lower thoracic and lumbosacral cord. J Comp Neurol 230:133-141.
31. Obata K, Noguchi K (2004) MAPK activation in nociceptive neurons and pain hypersensitivity. Life Sci 74:2643-2653.
32. Obata K, Yamanaka H, Dai Y, Tachibana T, Fukuoka T, Tokunaga A, Yoshikawa H, Noguchi K (2003) Differential activation of extracellular signal-regulated protein kinase in primary afferent neurons regulates brain-derived neurotrophic factor expression after peripheral inflammation and nerve injury. J Neurosci 23:4117-4126.
33. Obata K, Yamanaka H, Kobayashi K, Dai Y, Mizushima T, Katsura H, Fukuoka T, Tokunaga A, Noguchi K (2004a) 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 24:10211-10222.
34. Obata K, Yamanaka H, Dai Y, Mizushima T, Fukuoka T, Tokunaga A, Noguchi K (2004b) Differential activation of MAPK in injured and uninjured DRG neurons following chronic constriction injury of the sciatic nerve in rats. Eur J Neurosci 20:2881-2895.
35. Raghavendra V, Tanga F, DeLeo JA (2003) Inhibition of microglial activation attenuates the development but not existing hypersensitivity in a rat model of neuropathy. J Pharmacol Exp Ther 306:624-630.
36. Rodriguez MJ, Martinez-Sanchez M, Bernal F, Mahy N (2004) Heterogeneity between hippocampal and septal astroglia as a contributing factor to differential in vivo AMPA excitotoxicity. J Neurosci Res 77:344-353.
37. Samad TA, Moore KA, Sapirstein A, Billet S, Allchorne A, Poole S, Bonventre JV, Woolf CJ (2001) Interleukin-1beta-mediated induction of Cox-2 in the CNS contributes to inflammatory pain hypersensitivity. Nature 410:471-475.
38. Schafers M, Svensson CI, Sommer C, Sorkin LS (2003) Tumor necrosis factor-α induces mechanical allodynia after spinal nerve ligation by activation of p38 MAPK in primary sensory neurons. J Neurosci 23:2517-2521.
39. Tanga FY, Nutile-McMenemy N, DeLeo JA (2005) The CNS role of Toll-like receptor 4 in innate neuroimmunity and painful neuropathy. Proc Natl Acad Sci USA 102:5856-5861.
40. Tezel G, Yang X, Yang J, Wax MB (2004) Role of tumor necrosis factor receptor-1 in the death of retinal ganglion cells following optic nerve crush injury in mice. Brain Res 996:202-212.
41. Tsuda M, Shigemoto-Mogami Y, Koizumi S, Mizokoshi A, Kohsaka S, Salter MW, Inoue K (2003) P2X4 receptors induced in spinal microglia gate tactile allodynia after nerve injury. Nature 424:778-783.
42. Tsuda M, Mizokoshi A, Shigemoto-Mogami Y, Koizumi S, Inoue K (2004) Activation of p38 mitogen-activated protein kinase in spinal hyperactive microglia contributes to pain hypersensitivity following peripheral nerve injury. Glia 45:89-95.
43. Tsuda M, Inoue K, Salter MW (2005) Neuropathic pain and spinal microglia: a big problem from molecules in "small" glia. Trends Neurosci 28:101-107.
44. Wang J, Van De Water TR, Bonny C, de Ribaupierre F, Puel JL, Zine A (2003) A peptide inhibitor of c-Jun N-terminal kinase protects against both aminoglycoside and acoustic trauma-induced auditory hair cell death and hearing loss. J Neurosci 23:8596-8607.
45. Watkins LR, Maier SF (2003) Glia: a novel drug discovery target for clinical pain. Nat Rev Drug Discov 2:973-985.
46. Watkins LR, Milligan ED, Maier SF (2001) Glial activation: a driving force for pathological pain. Trends Neurosci 24:450-455.
47. Woolf CJ, Mannion RJ (1999) Neuropathic pain: aetiology, symptoms, mechanisms, and management. Lancet 353:1959-1964.
48. Xia Z, Dickens M, Raingeaud J, Davis RJ, Greenberg ME (1995) Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270:1326-1331.
49. Zhuang ZY, Gerner P, Woolf CJ, Ji RR (2005) ERK is sequentially activated in neurons, microglia, and astrocytes by spinal nerve ligation and contributes to mechanical allodynia in this neuropathic pain model. Pain 114:149-159.