Ligustilide attenuates inflammatory pain via inhibition of NFκB-mediated chemokines production in spinal astrocytes

European Journal of Neuroscience

Volumn 39, Issue 8, 2014, Pages 1391-1402

  Zhao, Lin Xia ^a   Jiang, Bao Chun ^a   Wu, Xiao Bo ^a   Cao, De Li ^a   Gao, Yong Jing ^a  

^a NANTONG UNIVERSITY   (China)

Author keywords

Astrocyte; Chemokines; Chronic pain; Complete freund's adjuvant; Neuroinflammation

Indexed keywords

3 (4 METHYLPHENYLSULFONYL) 2 PROPENENITRILE; GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; KERATINOCYTE DERIVED CHEMOKINE; LIGUSTILIDE; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; CCL2 PROTEIN, MOUSE; CHEMOKINE; GAMMA BUTYROLACTONE;

ALLODYNIA; ANALGESIC ACTIVITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; ASTROCYTE; CHRONIC INFLAMMATION; CONTROLLED STUDY; DOSE RESPONSE; DRUG DOSE COMPARISON; DRUG MECHANISM; DRUG MEGADOSE; GENE EXPRESSION; HYPERALGESIA; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATORY PAIN; KERATINOCYTE DERIVED CHEMOKINE GENE; LOW DRUG DOSE; MALE; MONOCYTE CHEMOTACTIC PROTEIN 1 GENE; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS INHIBITION; ANALOGS AND DERIVATIVES; ANGELICA SINENSIS; ANIMAL; CELL CULTURE; CHEMISTRY; DRUG EFFECTS; GENETICS; INSTITUTE FOR CANCER RESEARCH MOUSE; METABOLISM; NOCICEPTION; NOCICEPTIVE PAIN; PATHOLOGY; SPINAL CORD;

4-BUTYROLACTONE; ANGELICA SINENSIS; ANIMALS; ASTROCYTES; CELLS, CULTURED; CHEMOKINE CCL2; CHEMOKINES; HYPERALGESIA; MALE; MICE; MICE, INBRED ICR; NF-KAPPA B; NOCICEPTION; NOCICEPTIVE PAIN; RNA, MESSENGER; SPINAL CORD;

EID: 84899094007     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12502     Document Type: Article

References (53)

1. Bethea, J.R., Castro, M., Keane, R.W., Lee, T.T., Dietrich, W.D. & Yezierski, R.P. (1998) Traumatic spinal cord injury induces nuclear factor-kappaB activation. J. Neurosci., 18, 3251-3260.
2. Bhangoo, S., Ren, D., Miller, R.J., Henry, K.J., Lineswala, J., Hamdouchi, C., Li, B., Monahan, P.E., Chan, D.M., Ripsch, M.S. & White, F.A. (2007) Delayed functional expression of neuronal chemokine receptors following focal nerve demyelination in the rat: a mechanism for the development of chronic sensitization of peripheral nociceptors. Mol. Pain, 3, 38.
3. Cao, H. & Zhang, Y.Q. (2008) Spinal glial activation contributes to pathological pain states. Neurosci. Biobehav. R., 32, 972-983.
4. Dixon, W.J. (1980) Efficient analysis of experimental observations. Annu. Rev. Pharmacol., 20, 441-462.
5. Du, J., Yu, Y., Ke, Y., Wang, C., Zhu, L. & Qian, Z.M. (2007) Ligustilide attenuates pain behavior induced by acetic acid or formalin. J. Ethnopharmacol., 112, 211-214.
6. Feng, Z., Lu, Y., Wu, X., Zhao, P., Li, J., Peng, B., Qian, Z. & Zhu, L. (2012) Ligustilide alleviates brain damage and improves cognitive function in rats of chronic cerebral hypoperfusion. J. Ethnopharmacol., 144, 313-321.
7. Gao, Y.J. & Ji, R.R. (2010) Targeting astrocyte signaling for chronic pain. Neurotherapeutics, 7, 482-493.
8. Gao, Y.J., Zhang, L., Samad, O.A., Suter, M.R., Yasuhiko, K., Xu, Z.Z., Park, J.Y., Lind, A.L., Ma, Q. & Ji, R.R. (2009) JNK-induced MCP-1 production in spinal cord astrocytes contributes to central sensitization and neuropathic pain. J. Neurosci., 29, 4096-4108.
9. Gao, Y.J., Xu, Z.Z., Liu, Y.C., Wen, Y.R., Decosterd, I. & Ji, R.R. (2010) 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, 148, 309-319.
10. Gorina, R., Font-Nieves, M., Marquez-Kisinousky, L., Santalucia, T. & Planas, A.M. (2011) Astrocyte TLR4 activation induces a proinflammatory environment through the interplay between MyD88-dependent NFkappaB signaling, MAPK, and Jak1/Stat1 pathways. Glia, 59, 242-255.
11. Gosselin, R.D., Varela, C., Banisadr, G., Mechighel, P., Rostene, W., Kitabgi, P. & Melik-Parsadaniantz, S. (2005) Constitutive expression of CCR2 chemokine receptor and inhibition by MCP-1/CCL2 of GABA-induced currents in spinal cord neurones. J. Neurochem., 95, 1023-1034.
12. Gosselin, R.D., Suter, M.R., Ji, R.R. & Decosterd, I. (2010) Glial cells and chronic pain. Neuroscientist, 16, 519-531.
13. Hui, J., Zhang, Z.J., Zhang, X., Shen, Y. & Gao, Y.J. (2013) Repetitive Hyperbaric Oxygen Treatment Attenuates Complete Freund's Adjuvant-Induced Pain and Reduces Glia-Mediated Neuroinflammation in the Spinal Cord. J. Pain, 14, 747-758.
14. Hylden, J.L. & Wilcox, G.L. (1980) Intrathecal morphine in mice: a new technique. Eur. J. Pharmacol., 67, 313-316.
15. Ji, R.R., Berta, T. & Nedergaard, M. (2013) Glia and pain: Is chronic pain a gliopathy? Pain, 154(Suppl 1), S10-S28.
16. Knerlich-Lukoschus, F., Juraschek, M., Blomer, U., Lucius, R., Mehdorn, H.M. & Held-Feindt, J. (2008) Force-dependent development of neuropathic central pain and time-related CCL2/CCR2 expression after graded spinal cord contusion injuries of the rat. J. Neurotraum., 25, 427-448.
17. Kuang, X., Yao, Y., Du, J.R., Liu, Y.X., Wang, C.Y. & Qian, Z.M. (2006) Neuroprotective role of Z-ligustilide against forebrain ischemic injury in ICR mice. Brain Res., 1102, 145-153.
18. Kuang, X., Du, J.R., Liu, Y.X., Zhang, G.Y. & Peng, H.Y. (2008) Postischemic administration of Z-Ligustilide ameliorates cognitive dysfunction and brain damage induced by permanent forebrain ischemia in rats. Pharmacol. Biochem. Be., 88, 213-221.
19. Ledeboer, A., Gamanos, M., Lai, W., Martin, D., Maier, S.F., Watkins, L.R. & Quan, N. (2005) Involvement of spinal cord nuclear factor kappaB activation in rat models of proinflammatory cytokine-mediated pain facilitation. Eur. J. Neurosci., 22, 1977-1986.
20. Lee, M.K., Han, S.R., Park, M.K., Kim, M.J., Bae, Y.C., Kim, S.K., Park, J.S. & Ahn, D.K. (2011) Behavioral evidence for the differential regulation of p-p38 MAPK and p-NF-kappaB in rats with trigeminal neuropathic pain. Mol. Pain, 7, 57.
21. Liu, J., Burdette, J.E., Xu, H., Gu, C., van Breemen, R.B., Bhat, K.P., Booth, N., Constantinou, A.I., Pezzuto, J.M., Fong, H.H., Farnsworth, N.R. & Bolton, J.L. (2001) Evaluation of estrogenic activity of plant extracts for the potential treatment of menopausal symptoms. J. Agric. Food Chem., 49, 2472-2479.
22. Lucas, S.M., Rothwell, N.J. & Gibson, R.M. (2006) The role of inflammation in CNS injury and disease. Brit. J. Pharmacol., 147(Suppl 1), S232-S240.
23. Meunier, A., Latremoliere, A., Dominguez, E., Mauborgne, A., Philippe, S., Hamon, M., Mallet, J., Benoliel, J.J. & Pohl, M. (2007) Lentiviral-mediated targeted NF-kappaB blockade in dorsal spinal cord glia attenuates sciatic nerve injury-induced neuropathic pain in the rat. Mol. Ther., 15, 687-697.
24. Mika, J., Zychowska, M., Popiolek-Barczyk, K., Rojewska, E. & Przewlocka, B. (2013) Importance of glial activation in neuropathic pain. Eur. J. Pharmacol., 716, 106-119.
25. Minghetti, L. (2005) Role of inflammation in neurodegenerative diseases. Curr. Opin. Neurol., 18, 315-321.
26. Mirabelli-Badenier, M., Braunersreuther, V., Viviani, G.L., Dallegri, F., Quercioli, A., Veneselli, E., Mach, F. & Montecucco, F. (2011) CC and CXC chemokines are pivotal mediators of cerebral injury in ischaemic stroke. Thromb. Haemostasis, 105, 409-420.
27. Miyoshi, K., Obata, K., Kondo, T., Okamura, H. & Noguchi, K. (2008) Interleukin-18-mediated microglia/astrocyte interaction in the spinal cord enhances neuropathic pain processing after nerve injury. J. Neurosci., 28, 12775-12787.
28. Najjar, S., Pearlman, D.M., Alper, K., Najjar, A. & Devinsky, O. (2013) Neuroinflammation and psychiatric illness. J. Neuroinflamm., 10, 43.
29. Nakagawa, T. & Kaneko, S. (2010) Spinal astrocytes as therapeutic targets for pathological pain. J. Pharmacol. Sci., 114, 347-353.
30. Omari, K.M., John, G., Lango, R. & Raine, C.S. (2006) Role for CXCR2 and CXCL1 on glia in multiple sclerosis. Glia, 53, 24-31.
31. Peng, H.Y., Du, J.R., Zhang, G.Y., Kuang, X., Liu, Y.X., Qian, Z.M. & Wang, C.Y. (2007) Neuroprotective effect of Z-ligustilide against permanent focal ischemic damage in rats. Biol. Pharm. Bull., 30, 309-312.
32. Peng, B., Zhao, P., Lu, Y.P., Chen, M.M., Sun, H., Wu, X.M. & Zhu, L. (2013) Z-ligustilide activates the Nrf2/HO-1 pathway and protects against cerebral ischemia-reperfusion injury in vivo and in vitro. Brain Res., 1520, 168-177.
33. Pineau, I., Sun, L., Bastien, D. & Lacroix, S. (2010) Astrocytes initiate inflammation in the injured mouse spinal cord by promoting the entry of neutrophils and inflammatory monocytes in an IL-1 receptor/MyD88-dependent fashion. Brain Behav. Immun., 24, 540-553.
34. Raghavendra, V., Tanga, F.Y. & Deleo, J.A. (2004) Complete Freunds adjuvant-induced peripheral inflammation evokes glial activation and proinflammatory cytokine expression in the CNS. Eur. J. Neurosci., 20, 467-473.
35. Ren, K. & Dubner, R. (2008) Neuron-glia crosstalk gets serious: role in pain hypersensitivity. Curr. Opin. Anaesthesio., 21, 570-579.
36. Savarin-Vuaillat, C. & Ransohoff, R.M. (2007) Chemokines and chemokine receptors in neurological disease: raise, retain, or reduce? Neurotherapeutics, 4, 590-601.
37. Sorge, R.E., LaCroix-Fralish, M.L., Tuttle, A.H., Sotocinal, S.G., Austin, J.S., Ritchie, J., Chanda, M.L., Graham, A.C., Topham, L., Beggs, S., Salter, M.W. & Mogil, J.S. (2011) Spinal cord Toll-like receptor 4 mediates inflammatory and neuropathic hypersensitivity in male but not female mice. J. Neurosci., 31, 15450-15454.
38. Su, Y.W., Chiou, W.F., Chao, S.H., Lee, M.H., Chen, C.C. & Tsai, Y.C. (2011) Ligustilide prevents LPS-induced iNOS expression in RAW 264.7 macrophages by preventing ROS production and down-regulating the MAPK, NF-kappaB and AP-1 signaling pathways. Int. Immunopharmacol., 11, 1166-1172.
39. Suter, M.R., Wen, Y.R., Decosterd, I. & Ji, R.R. (2007) Do glial cells control pain? Neuron Glia Biol., 3, 255-268.
40. Thacker, M.A., Clark, A.K., Bishop, T., Grist, J., Yip, P.K., Moon, L.D., Thompson, S.W., Marchand, F. & Mcmahon, S.B. (2009) CCL2 is a key mediator of microglia activation in neuropathic pain states. Eur. J. Pain, 13, 263-272.
41. Thompson, W.L. & Van Eldik, L.J. (2009) Inflammatory cytokines stimulate the chemokines CCL2/MCP-1 and CCL7/MCP-3 through NFkB and MAPK dependent pathways in rat astrocytes [corrected]. Brain Res., 1287, 47-57.
42. Vallejo, R., Tilley, D.M., Vogel, L. & Benyamin, R. (2010) The role of glia and the immune system in the development and maintenance of neuropathic pain. Pain Pract., 10, 167-184.
43. Van Steenwinckel, J., Reaux-Le Goazigo, A., Pommier, B., Mauborgne, A., Dansereau, M.A., Kitabgi, P., Sarret, P., Pohl, M. & Melik Parsadaniantz, S. (2011) CCL2 released from neuronal synaptic vesicles in the spinal cord is a major mediator of local inflammation and pain after peripheral nerve injury. J. Neurosci., 31, 5865-5875.
44. Wang, J., Du, J.R., Wang, Y., Kuang, X. & Wang, C.Y. (2010) Z-ligustilide attenuates lipopolysaccharide-induced proinflammatory response via inhibiting NF-kappaB pathway in primary rat microglia. Acta Pharmacol. Sin., 31, 791-797.
45. Watkins, L.R., Hutchinson, M.R., Milligan, E.D. & Maier, S.F. (2007) "Listening" and "talking" to neurons: implications of immune activation for pain control and increasing the efficacy of opioids. Brain Res. Rev., 56, 148-169.
46. White, F.A. & Wilson, N.M. (2008) Chemokines as pain mediators and modulators. Curr. Opin. Anaesthesio., 21, 580-585.
47. Wieseler-Frank, J., Maier, S.F. & Watkins, L.R. (2004) Glial activation and pathological pain. Neurochem. Int., 45, 389-395.
48. Wu, X.M., Qian, Z.M., Zhu, L., Du, F., Yung, W.H., Gong, Q. & Ke, Y. (2011) Neuroprotective effect of ligustilide against ischaemia-reperfusion injury via up-regulation of erythropoietin and down-regulation of RTP801. Brit. J. Pharmacol., 164, 332-343.
49. Yim, T.K., Wu, W.K., Pak, W.F., Mak, D.H., Liang, S.M. & Ko, K.M. (2000) Myocardial protection against ischaemia-reperfusion injury by a Polygonum multiflorum extract supplemented 'Dang-Gui decoction for enriching blood', a compound formulation, ex vivo. Phytother. Res., 14, 195-199.
50. Yoon, S.Y., Patel, D. & Dougherty, P.M. (2012) Minocycline blocks lipopolysaccharide induced hyperalgesia by suppression of microglia but not astrocytes. Neuroscience, 221, 214-224.
51. Zang, Y., He, X.H., Xin, W.J., Pang, R.P., Wei, X.H., Zhou, L.J., Li, Y.Y. & Liu, X.G. (2010) Inhibition of NF-kappaB prevents mechanical allodynia induced by spinal ventral root transection and suppresses the re-expression of Nav1.3 in DRG neurons in vivo and in vitro. Brain Res., 1363, 151-158.
52. Zhang, Z.J., Cao, D.L., Zhang, X., Ji, R.R. & Gao, Y.J. (2013) Chemokine contribution to neuropathic pain: respective induction of CXCL1 and CXCR2 in spinal cord astrocytes and neurons. Pain, 154, 2185-2197.
53. Zhuang, Z.Y., Wen, Y.R., Zhang, D.R., Borsello, T., Bonny, C., Strichartz, G.R., Decosterd, I. & Ji, R.R. (2006) 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., 26, 3551-3560.