The inhibition of spinal astrocytic JAK2-STAT3 pathway activation correlates with the analgesic effects of triptolide in the rat neuropathic pain model

Evidence-based Complementary and Alternative Medicine

Volumn 2012, Issue , 2012, Pages

  Tang, Jun ^a   Li, Zhi Hong ^a,b   Ge, Shun Nan ^a,b   Wang, Wei ^a   Mei, Xiao Peng ^a   Wang, Wen ^a   Zhang, Ting ^a   Xu, Li Xian ^a   Li, Jin Lian ^a  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 1BETA; INTERLEUKIN 6; JANUS KINASE 2; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; STAT3 PROTEIN; TRIPTOLIDE; TUMOR NECROSIS FACTOR ALPHA;

ANALGESIC ACTIVITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINOCICEPTION; ARTICLE; ASTROCYTE; CONTROLLED STUDY; CORRELATION ANALYSIS; MALE; NERVOUS SYSTEM INFLAMMATION; NEUROPATHIC PAIN; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; UPREGULATION;

EID: 84872794619     PISSN: 1741427X     EISSN: 17414288     Source Type: Journal    
DOI: 10.1155/2012/185167     Document Type: Article

References (54)

1. Costigan M., Scholz J., Woolf C. J., Neuropathic pain: a maladaptive response of the nervous system to damage. Annual Review of Neuroscience 2009 32 1 32 2-s2.0-67651048942 10.1146/annurev.neuro.051508.135531
2. Dworkin R. H., Backonja M., Rowbotham M. C., Allen R. R., Argoff C. R., Bennett G. J., Bushnell M. C., Farrar J. T., Galer B. S., Haythornthwaite J. A., Hewitt D. J., Loeser J. D., Max M. B., Saltarelli M., Schmader K. E., Stein C., Thompson D., Turk D. C., Wallace M. S., Watkins L. R., Weinstein S. M., Advances in neuropathic pain: diagnosis, mechanisms, and treatment recommendations. Archives of Neurology 2003 60 11 1524 1534 2-s2.0-0345445898 10.1001/archneur.60.11.1524 (Pubitemid 37443116)
3. Gao Y. J., Ji R. R., Targeting astrocyte signaling for chronic pain. Neurotherapeutics 2010 7 4 482 493 2-s2.0-77957056575 10.1016/j.nurt.2010.05.016
4. O'Connor A. B., Dworkin R. H., Treatment of neuropathic pain: an overview of recent guidelines. American Journal of Medicine 2009 122 10, supplement S22 S32 2-s2.0-70349481938 10.1016/j.amjmed.2009.04.007
5. Watkins L. R., Martin D., Ulrich P., Tracey K. J., Maier S. F., Evidence for the involvement of spinal cord glia in subcutaneous formalin induced hyperalgesia in the rat. Pain 1997 71 3 225 235 2-s2.0-0030840882 10.1016/S0304-3959(97)03369-1 (Pubitemid 27288136)
6. Milligan E. D., Twining C., Chacur M., Biedenkapp J., O'Connor K., Poole S., Tracey K., Martin D., Maier S. F., Watkins L. R., Spinal glia and proinflammatory cytokines mediate mirror-image neuropathic pain in rats. The Journal of Neuroscience 2003 23 3 1026 1040 2-s2.0-0037320840 (Pubitemid 36206195)
7. Meunier A., Mauborgne A., Masson J., Mallet J., Pohl M., Lentiviral-mediated targeted transgene expression in dorsal spinal cord glia: tool for the study of glial cell implication in mechanisms underlying chronic pain development. The Journal of Neuroscience Methods 2008 167 2 148 159 2-s2.0-36849049311 10.1016/j.jneumeth.2007.07.022 (Pubitemid 350235620)
8. Watkins L. R., Milligan E. D., Maier S. F., Glial activation: a driving force for pathological pain. Trends in Neurosciences 2001 24 8 450 455 2-s2.0-0035426434 10.1016/S0166-2236(00)01854-3 (Pubitemid 32695356)
9. Fields R. D., Stevens-Graham B., Neuroscience: new insights into neuron-glia communication. Science 2002 298 5593 556 562 2-s2.0-0037131025 10.1126/science.298.5593.556 (Pubitemid 35215303)
10. Gao Y. J., Ji R. R., Chemokines, neuronal-glial interactions, and central processing of neuropathic pain. Pharmacology and Therapeutics 2010 126 1 56 68 2-s2.0-77649274037 10.1016/j.pharmthera.2010.01.002
11. Tsuda M., Beggs S., Salter M. W., Inoue K., Micro and intractable chronic pain. Glia 2012 61 1 55 61 10.1002/glia.22379
12. Zhuo M., Wu G., Wu L. J., Neuronal and microglial mechanisms of neuropathic pain. Molecular Brain 2011 4, article 31 2-s2.0-79960883074 10.1186/1756-6606-4-31
13. Mei X. P., Zhang H., Wang W., Wei Y. Y., Zhai M. Z., Wang W., Xu L. X., Li Y. Q., Inhibition of spinal astrocytic c-Jun N-terminal kinase (JNK) activation correlates with the analgesic effects of ketamine in neuropathic pain. Journal of Neuroinflammation 2011 8 1, article 6 2-s2.0-78751648813 10.1186/1742-2094-8-6
14. Mei X. P., Wang W., Zhu C., Wang W., Chen L., Zhang T., Xu L. X., Wu S. X., Li Y. Q., Combining ketamine with astrocytic inhibitor as a potential analgesic strategy for neuropathic pain. Ketamine, astrocytic inhibitor and pain. Molecular Pain 2010 6, article 50 2-s2.0-77956486990 10.1186/1744-8069-6- 50
15. Tsuda M., Kohro Y., Yano T., Tsujikawa T., Kitano J., Tozaki-Saitoh H., Koyanagi S., Ohdo S., Ji R. R., Salter M. W., Inoue K., JAK-STAT3 pathway regulates spinal astrocyte proliferation and neuropathic pain maintenance in rats. Brain 2011 134 4 1127 1139 2-s2.0-79953660904 10.1093/brain/awr025
16. Herrmann J. E., Imura T., Song B., Qi J., Ao Y., Nguyen T. K., Korsak R. A., Takeda K., Akira S., Sofroniew M. V., STAT3 is a critical regulator of astrogliosis and scar formation after spinal cord injury. The Journal of Neuroscience 2008 28 28 7231 7243 2-s2.0-49049091210 10.1523/JNEUROSCI.1709-08. 2008
17. Dominguez E., Mauborgne A., Mallet J., Desclaux M., Pohl M., SOCS3-mediated blockade of JAK/STAT3 signaling pathway reveals its major contribution to spinal cord neuroinflammation and mechanical allodynia after peripheral nerve injury. The Journal of Neuroscience 2010 30 16 5754 5766 2-s2.0-77951533730 10.1523/JNEUROSCI.5007-09.2010
18. Dominguez E., Rivat C., Pommier B., Mauborgne A., Pohl M., JAK/STAT3 pathway is activated in spinal cord microglia after peripheral nerve injury and contributes to neuropathic pain development in rat. Journal of Neurochemistry 2008 107 1 50 60 2-s2.0-51849153310 10.1111/j.1471-4159.2008.05566.x
19. Nicholson S. E., de Souza D., Fabri L. J., Corbin J., Willson T. A., Zhang J. G., Silva A., Asimakis M., Farley A., Nash A. D., Metcalf D., Hilton D. J., Nicola N. A., Baca M., Suppressor of cytokine signaling-3 preferentially binds to the SHP-2-binding site on the shared cytokine receptor subunit gp130. Proceedings of the National Academy of Sciences of the United States of America 2000 97 12 6493 6498 2-s2.0-0034612271 (Pubitemid 30412741)
20. Lu L., Li F., Wang X., Novel anti-inflammatory and neuroprotective agents for Parkinson's disease. CNS and Neurological Disorders-Drug Targets 2010 9 2 232 240 2-s2.0-77949899785
21. Li F. Q., Lu X. Z., Liang X. B., Zhou H. F., Xue B., Liu X. Y., Niu D. B., Han J. S., Wang X. M., Triptolide, a Chinese herbal extract, protects dopaminergic neurons from inflammation-mediated damage through inhibition of microglial activation. Journal of Neuroimmunology 2004 148 1-2 24 31 2-s2.0-1242272720 10.1016/j.jneuroim.2003.10.054 (Pubitemid 38229555)
22. Han R., Rostami-Yazdi M., Gerdes S., Mrowietz U., Triptolide in the treatment of psoriasis and other immune-mediated inflammatory diseases. British Journal of Clinical Pharmacology 2012 74 3 424 436 10.1111/j.1365-2125.2012. 04221.x
23. Cibere J., Deng Z., Lin Y., Ou R., He Y., Wang Z., Thorne A., Lehman A. J., Tsang I. K., Esdaile J. M., A randomized double blind, placebo controlled trial of topical Tripterygium wilfordii in rheumatoid arthritis: reanalysis using logistic regression analysis. Journal of Rheumatology 2003 30 3 465 467 2-s2.0-0037334146 (Pubitemid 36301935)
24. Gong Y., Xue B., Jiao J., Jing L., Wang X., Triptolide inhibits COX-2 expression and PGE2 release by suppressing the activity of NF- B and JNK in LPS-treated microglia. Journal of Neurochemistry 2008 107 3 779 788 2-s2.0-53749093009 10.1111/j.1471-4159.2008.05653.x
25. Xue B., Jiao J., Zhang L., Li K. R., Gong Y. T., Xie J. X., Wang X. M., Triptolide upregulates NGF synthesis in rat astrocyte cultures. Neurochemical Research 2007 32 7 1113 1119 2-s2.0-34249695397 10.1007/s11064-006-9253-1 (Pubitemid 46823877)
26. Su Z., Yuan Y., Cao L., Zhu Y., Gao L., Qiu Y., He C., Triptolide promotes spinal cord repair by inhibiting astrogliosis and inflammation. Glia 2010 58 8 901 915 2-s2.0-77952576395 10.1002/glia.20972
27. Zimmermann M., Ethical guidelines for investigations of experimental pain in conscious animals. Pain 1983 16 2 109 110 2-s2.0-0020525719 10.1016/0304-3959(83)90201-4 (Pubitemid 13058546)
28. Wang W., Mei X. P., Wei Y. Y., Neuronal NR2B-containing NMDA receptor mediates spinal astrocytic c-Jun N-terminal kinase activation in a rat model of neuropathic pain. Brain, Behavior, and Immunity 2011 25 7 1355 1366 10.1016/j.bbi.2011.04.002
29. Størkson R. V., Kjørsvik A., Tjølsen A., Hole K., Lumbar catheterization of the spinal subarachnoid space in the rat. The Journal of Neuroscience Methods 1996 65 2 167 172 2-s2.0-0029880852 10.1016/0165- 0270(95)00164-6 (Pubitemid 26132817)
30. Liu Q., Chen T., Chen G., Shu X., Sun A., Ma P., Lu L., Cao X., Triptolide impairs dendritic cell migration by inhibiting CCR7 and COX-2 expression through PI3-K/Akt and NF- B pathways. Molecular Immunology 2007 44 10 2686 2696 2-s2.0-33846903837 10.1016/j.molimm.2006.12.003 (Pubitemid 46240316)
31. Hamm R. J., Pike B. R., O'Dell D. M., Lyeth B. G., Jenkins L. W., The rotarod test: an evaluation of its effectiveness in assessing motor deficits following traumatic brain injury. Journal of Neurotrauma 1994 11 2 187 196 2-s2.0-0028229190 (Pubitemid 24174507)
32. Chaplan S. R., Bach F. W., Pogrel J. W., Chung J. M., Yaksh T. L., Quantitative assessment of tactile allodynia in the rat paw. The Journal of Neuroscience Methods 1994 53 1 55 63 2-s2.0-0027933374 10.1016/0165-0270(94) 90144-9 (Pubitemid 24238751)
33. Svensson C. I., Brodin E., Spinal astrocytes in pain processing: non-neuronal cells as therapeutic targets. Molecular Interventions 2010 10 1 25 38 2-s2.0-76349102800 10.1124/mi.10.1.6
34. Parpura V., Basarsky T. A., Liu F., Jeftinija K., Jeftinija S., Haydon P. G., Glutamate-mediated astrocyte-neuron signalling. Nature 1994 369 6483 744 747 2-s2.0-0028225677 10.1038/369744a0 (Pubitemid 24225363)
35. Perea G., Araque A., Astrocytes potentiate transmitter release at single hippocampal synapses. Science 2007 317 5841 1083 1086 2-s2.0-34548203204 10.1126/science.1144640 (Pubitemid 47330192)
36. Vallejo R., Tilley D. M., Vogel L., Benyamin R., The role of glia and the immune system in the development and maintenance of neuropathic pain. Pain Practice 2010 10 3 167 184 2-s2.0-77954877647 10.1111/j.1533-2500.2010.00367.x
37. Pan X. D., Chen X. C., Zhu Y. G., Chen L. M., Zhang J., Huang T. W., Ye Q. Y., Huang H. P., Tripchlorolide protects neuronal cells from microglia-mediated β -amyloid neurotoxicity through inhibiting NF- B and JNK signaling. Glia 2009 57 11 1227 1238 2-s2.0-69749088327 10.1002/glia.20844
38. Zhou H. F., Liu X. Y., Niu D. B., Li F. Q., He Q. H., Wang X. M., Triptolide protects dopaminergic neurons from inflammation-mediated damage induced by lipopolysaccharide intranigral injection. Neurobiology of Disease 2005 18 3 441 449 2-s2.0-14744284455 10.1016/j.nbd.2004.12.005 (Pubitemid 40332703)
39. Jiao J., Xue B., Zhang L., Gong Y., Li K., Wang H., Jing L., Xie J., Wang X., Triptolide inhibits amyloid- β 1-42-induced TNF- α and IL-1 β production in cultured rat microglia. Journal of Neuroimmunology 2008 205 1-2 32 36 2-s2.0-56649095794 10.1016/j.jneuroim.2008.08.006
40. He F., Ge W., Martinowich K., Becker-Catania S., Coskun V., Zhu W., Wu H., Castro D., Guillemot F., Fan G., de Vellis J., Sun Y. E., A positive autoregulatory loop of Jak-STAT signaling controls the onset of astrogliogenesis. Nature Neuroscience 2005 8 5 616 625 2-s2.0-20944442861 10.1038/nn1440 (Pubitemid 40594203)
41. Damiani C. L., O'Callaghan J. P., Recapitulation of cell signaling events associated with astrogliosis using the brain slice preparation. Journal of Neurochemistry 2007 100 3 720 726 2-s2.0-33846261492 10.1111/j.1471-4159.2006. 04321.x (Pubitemid 46095621)
42. Yamauchi K., Osuka K., Takayasu M., Usuda N., Nakazawa A., Nakahara N., Yoshida M., Aoshima C., Hara M., Yoshida J., Activation of JAK/STAT signalling in neurons following spinal cord injury in mice. Journal of Neurochemistry 2006 96 4 1060 1070 2-s2.0-33645105944 10.1111/j.1471-4159.2005.03559.x
43. Kacimi R., Giffard R. G., Yenari M. A., Endotoxin-activated microglia injure brain derived endothelial cells via NF- B, JAK-STAT and JNK stress kinase pathways. Journal of Inflammation 2011 8, article 7 2-s2.0-79952318766 10.1186/1476-9255-8-7
44. Suzuki S., Tanaka K., Nogawa S., Dembo T., Kosakai A., Fukuuchi Y., Phosphorylation of signal transducer and activator of transcription-3 (Stat3) after focal cerebral ischemia in rats. Experimental Neurology 2001 170 1 63 71 2-s2.0-0034958433 10.1006/exnr.2001.7701 (Pubitemid 32641774)
45. Lee H. L., Lee K. M., Son S. J., Hwang S. H., Cho H. J., Temporal expression of cytokines and their receptors mRNAs in a neuropathic pain model. NeuroReport 2004 15 18 2807 2811 2-s2.0-11244254104
46. Moalem G., Tracey D. J., Immune and inflammatory mechanisms in neuropathic pain. Brain Research Reviews 2006 51 2 240 264 2-s2.0-33745153343 10.1016/j.brainresrev.2005.11.004 (Pubitemid 43902971)
47. Oprée A., Kress M., Involvement of the proinflammatory cytokines tumor necrosis factor- α IL-1 β and IL-6 but not IL-8 in the development of heat hyperalgesia: effects on heat-evoked calcitonin gene-related peptide release from rat skin. The Journal of Neuroscience 2000 20 16 6289 6293 2-s2.0-0034663315 (Pubitemid 30658424)
48. Liou J. T., Liu F. C., Mao C. C., Lai Y. S., Day Y. J., Inflammation confers dual effects on nociceptive processing in chronic neuropathic pain model. Anesthesiology 2011 114 3 660 672 2-s2.0-79952043400 10.1097/ALN. 0b013e31820b8b1e
49. Cha M. H., Nam T. S., Kwak Y., Lee H., Lee B. H., Changes in cytokine expression after electroacupuncture in neuropathic rats. Evidence-Based Complementary and Alternative Medicine 2012 2012 6 792765 10.1155/2012/792765
50. DeLeo J. A., Colburn R. W., Nichols M., Malhotra A., Interleukin-6- mediated hyperalgesia/allodynia and increased spinal IL-6 expression in a rat mononeuropathy model. Journal of Interferon and Cytokine Research 1996 16 9 695 700 2-s2.0-0029783630 (Pubitemid 26330415)
51. Dubový P., Klusákov I., Svíženská I., Brázda V., Satellite glial cells express IL-6 and corresponding signal-transducing receptors in the dorsal root ganglia of rat neuropathic pain model. Neuron Glia Biology 2010 6 1 73 83 2-s2.0-77957332761 10.1017/S1740925X10000074
52. Geng S. J., Liao F. F., Dang W. H., Ding X., Liu X. D., Cai J., Han J. S., Wan Y., Xing G. G., Contribution of the spinal cord BDNF to the development of neuropathic pain by activation of the NR2B-containing NMDA receptors in rats with spinal nerve ligation. Experimental Neurology 2010 222 2 256 266 2-s2.0-77549084615 10.1016/j.expneurol.2010.01.003
53. Svensson C. I., Hua X. Y., Powell H. C., Lai J., Porreca F., Yaksh T. L., Prostaglandin E2 release evoked by intrathecal dynorphin is dependent on spinal p38 mitogen activated protein kinase. Neuropeptides 2005 39 5 485 494 2-s2.0-26644469059 10.1016/j.npep.2005.08.002 (Pubitemid 41443525)
54. Wang W., Wang W., Mei X., Huang J., Wei Y., Wang Y., Wu S., Li Y., Crosstalk between spinal astrocytes and nuerons in nerve injury-injuced neuropathic pain. PLoS ONE 2009 4 9 2-s2.0-70349171800 10.1371/journal.pone. 0006973 e6973