Intrathecal lemnalol, a natural marine compound obtained from Formosan soft coral, attenuates nociceptive responses and the activity of spinal glial cells in neuropathic rats

Behavioural Pharmacology

Volumn 22, Issue 8, 2011, Pages 739-750

  Lin, Ying Chao ^a   Huang, Shi Ying ^b   Jean, Yen Hsuan ^e   Chen, Wu Fu ^c   Sung, Chun Sung ^f   Kao, Erl Shyh ^g   Wang, Hui Min ^d   Chakraborty, Chiranjib ^b   Duh, Chang Yih ^b   Wen, Zhi Hong ^b  

^a BUDDHIST TZU CHI GENERAL HOSPITAL   (Taiwan)

^b NATIONAL SUN YAT SEN UNIVERSITY   (Taiwan)

^c CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^d KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^e PINGTUNG CHRISTIAN HOSPITAL   (Taiwan)

^f NATIONAL YANG MING UNIVERSITY   (Taiwan)

^g CHIENKUO TECHNOLOGY UNIVERSITY   (Taiwan)

Author keywords

astrocytes; marine organisms; microglia; neuropathy; rat; tumor necrosis factor a

Indexed keywords

ANTIINFLAMMATORY AGENT; ANTINOCICEPTIVE AGENT; LEMNALOL; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; ASTROCYTE; CHRONIC CONSTRICTION INJURY; CONTROLLED STUDY; CORAL; DRUG DOSE COMPARISON; GLIA CELL; HYPERALGESIA; IMMUNOHISTOCHEMISTRY; INJURY; LUMBAR SPINAL CORD; MALE; MECHANICAL ALLODYNIA; MICROGLIA; NEUROPATHIC PAIN; NOCICEPTION; NONHUMAN; RAT; THERMAL HYPERALGESIA; TREATMENT RESPONSE; UPREGULATION;

ANIMALS; BEHAVIOR, ANIMAL; HYPERALGESIA; INJECTIONS, SPINAL; MALE; NEURALGIA; NEUROGLIA; NOCICEPTION; PAIN MEASUREMENT; RATS; RATS, WISTAR; SESQUITERPENES; SPINAL CORD;

EID: 80855144783     PISSN: 09558810     EISSN: 14735849     Source Type: Journal    
DOI: 10.1097/FBP.0b013e32834d0ecb     Document Type: Article

References (72)

1. Abad MJ, Bedoya LM, Bermejo P (2008). Natural marine anti-inflammatory products. Mini-Rev Med Chem 8:740-754.
2. Basso DM, Beattie MS, Bresnahan JC (1995). A sensitive and reliable locomotor rating scale for open field testing in rats. J Neurotrauma 12:1-21.
3. Bennett GJ, Xie YK (1988). A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 33:87-107.
4. Bridges D, Thompson SW, Rice AS (2001). Mechanisms of neuropathic pain. Br J Anaesth 87:12-26. (Pubitemid 32631672)
5. Carson MJ, Thrash JC, Walter B (2006). The cellular response in neuroinflamma-tion: the role of leukocytes, microglia and astrocytes in neuronal death and survival. Clin Neurosci Res 6:237-245. (Pubitemid 44849175)
6. Ceccarelli I, Fiorenzani P, Della Seta D, Massafra C, Cinci G, Bocci A, et al. (2009). Perinatal exposure to xenoestrogens affects pain in adult female rats. Neurotoxicol Teratol 31:203-209.
7. 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. (Pubitemid 24238751)
8. Chavarria A, Alcocer-Varela J (2004). Is damage in central nervous system due to inflammation? Autoimmun Rev 3:251-260. (Pubitemid 38887620)
9. Chen WF, Jean YH, Sung CS, Wu GJ, Huang SY, Ho JT, et al. (2008). Intrathecally injected granulocyte colony-stimulating factor produced neuro-protective effects in spinal cord ischemia via the mitogen-activated protein kinase and Akt pathways. Neuroscience 153:31-43.
10. Colburn RW, DeLeo JA, Rickman AJ, Yeager MP, Kwon P, Hickey WF (1997). Dissociation of microglial activation and neuropathic pain behaviors following peripheral nerve injury in the rat. J Neuroimmunol 79:163-175. (Pubitemid 27502035)
11. Colburn RW, Rickman AJ, DeLeo JA (1999). The effect of site and type of nerve injury on spinal glial activation and neuropathic pain behavior. Exp Neurol 157:289-304. (Pubitemid 29260737)
12. Coyle DE (1998). Partial peripheral nerve injury leads to activation of astroglia and microglia which parallels the development of allodynic behavior. Glia 23:75-83. (Pubitemid 28174047)
13. Cui Y, Chen Y, Zhi JL, Guo RX, Feng JQ, Chen PX (2006). Activation of p38 mitogen-activated protein kinase in spinal microglia mediates morphine antinociceptive tolerance. Brain Res 1069:235-243. (Pubitemid 43145918)
14. Cui Y, Liao XX, Liu W, Guo RX, Wu ZZ, Zhao CM, et al. (2008). A novel role of minocycline: attenuating morphine antinociceptive tolerance by inhibition of p38 MAPK in the activated spinal microglia. Brain Behav Immun 22: 114-123. (Pubitemid 350216368)
15. DeLeo JA, Yezierski RP (2001). The role of neuroinflammation and neuroimmune activation in persistent pain. Pain 90:1-6. (Pubitemid 32146552)
16. DeLeo JA, Colburn RW, Rickman AJ (1997). Cytokine and growth factor immunohistochemical spinal profiles in two animal models of mononeuro-pathy. Brain Res 759:50-57. (Pubitemid 27286343)
17. Duh CY, El-Gamal AA, Song PY, Wang SK, Dai CF (2004). Steroids and sesquiterpenoids from the soft corals Dendronephthya gigantea and Lemnalia cervicorni. J Nat Prod 67:1650-1653. (Pubitemid 39426116)
18. Finnerup NB, Sindrup SH, Jensen TS (2010). The evidence for pharmacological treatment of neuropathic pain. Pain 150:573-581.
19. Garrison CJ, Dougherty PM, Kajander KC, Carlton SM (1991). Staining of glial fibrillary acidic protein (GFAP) in lumbar spinal cord increases following a sciatic nerve constriction injury. Brain Res 565:1-7.
20. Giulian D, Li J, Leara B, Keenen C (1994). Phagocytic microglia release cytokines and cytotoxins that regulate the survival of astrocytes and neurons in culture. Neurochem Int 25:227-233. (Pubitemid 24282424)
21. Hains BC, Waxman SG (2006). Activated microglia contribute to the maintenance of chronic pain after spinal cord injury. J Neurosci 26: 4308-4317. (Pubitemid 44315390)
22. Hargreaves K, Dubner R, Brown F, Flores C, Joris J (1988). A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32:77-88.
23. Hofstetter CP, Holmström NA, Lilja JA, Schweinhardt P, Hao J, Spenger C, et al. (2005). Allodynia limits the usefulness of intraspinal neural stem cell grafts; directed differentiation improves outcome. Nat Neurosci 8: 346-353. (Pubitemid 40300192)
24. Jean YH, Chen WF, Duh CY, Huang SY, Hsu CH, Lin CS, et al. (2008). Inducible nitric oxide synthase and cyclooxygenase-2 participate in anti-inflammatory and analgesic effects of the natural marine compound lemnalol from Formosan soft coral Lemnalia cervicorni. Eur J Pharmacol 578: 323-331.
25. Jean YH, Chen WF, Sung CS, Duh CY, Huang SY, Lin CS, et al. (2009). Capnellene, a natural marine compound derived from soft coral, attenuates chronic constriction injury-induced neuropathic pain in rats. Br J Pharmacol 158:713-725.
26. Ji RR, Suter MR (2007). p38 MAPK, microglial signaling, and neuropathic pain. Mol Pain 3:33.
27. Jo D, Chapman CR, Light AR (2009). Glial mechanisms of neuropathic pain and emerging interventions. Korean J Pain 22:1-15.
28. Kijjoa A, Sawangwong P (2004). Drugs and cosmetics from the sea. Mar Drugs 2:73-82.
29. Kreutzberg GW (1996). Microglia: a sensor for pathological events in the CNS. Trends Neurosci 19:312-318. (Pubitemid 26349059)
30. Kulmatycki KM, Jamali F (2007). Drug disease interactions: role of inflammatory mediators in pain and variability in analgesic drug response. J Pharm Pharm Sci 10:554-566.
31. Ledeboer A, Sloane EM, Milligan ED, Frank MG, Mahony JH, Maier SF, et al. (2005). Minocycline attenuates mechanical allodynia and proinflamma-tory cytokine expression in rat models of pain facilitation. Pain 115: 71-83.
32. Lee CH, Wen ZH, Chang YC, Huang SY, Tang CC, Chen WF, et al. (2009). Intra-articular magnesium sulfate (MgSO4) reduces experimental osteoarthritis and nociception: association with attenuation of N-methyl-D-aspartate (NMDA) receptor subunit 1 phosphorylation and apoptosis in rat chondro-cytes. Osteoarthritis Cartilage 17:1485-1493.
33. Marchand F, Perretti M, McMahon SB (2005). Role of the immune system in chronic pain. Nat Rev Neurosci 6:521-532. (Pubitemid 40942819)
34. Mika J, Osikowicz M, Makuch W, Przewlocka B (2007). Minocycline and pentoxifylline attenuate allodynia and hyperalgesia and potentiate the effects of morphine in rat and mouse models of neuropathic pain. Eur J Pharmacol 560:142-149. (Pubitemid 46341303)
35. Mika J, Wawrzczak-Bargiela A, Osikowicz M, Makuch W, Przewlocka B (2009). Attenuation of morphine tolerance by minocycline and pentoxifylline in naive and neuropathic mice. Brain Behav Immun 23:75-84.
36. Milligan ED, Watkins LR (2009). Pathological and protective roles of glia in chronic pain. Nat Rev Neurosci 10:23-36.
37. Milligan ED, Sloane EM, Watkins LR (2008). Glia in pathological pain: a role for fractalkine. J Neuroimmunol 198:113-120.
38. Myers RR, Campana WM, Shubayev VI (2006). The role of neuroinflammation in neuropathic pain: mechanisms and therapeutic targets. Drug Discov Today 11:8-20. (Pubitemid 43227847)
39. Nickander R, McMahon FG, Ridolfo AS (1979). Nonsteroidal anti-inflammatory agents. Annu Rev Pharmacol Toxicol 9:469-490. (Pubitemid 9156587)
40. Obara I, Przewlocki R, Przewlocka B (2005). Spinal and local peripheral antiallodynic activity of Ro64-6198 in neuropathic pain in the rat. Pain 116:17-25. (Pubitemid 40828496)
41. Obara I, Makuch W, Spetea M, Schütz J, Schmidhammer H, Przewlocki R, et al. (2007). Local peripheral antinociceptive effects of 14-O- methyloxymorphone derivatives in inflammatory and neuropathic pain in the rat. Eur J Pharmacol 558:60-67. (Pubitemid 46328870)
42. Obara I, Parkitna JR, Korostynski M, Makuch W, Kaminska D, Przewlocka B, et al. (2009). Local peripheral opioid effects and expression of opioid genes in the spinal cord and dorsal root ganglia in neuropathic and inflammatory pain. Pain 141:283-291.
43. Padi SS, Kulkarni SK (2008). Minocycline prevents the development of neuropathic pain, but not acute pain: possible anti-inflammatory and antioxidant mechanisms. Eur J Pharmacol 601:79-87.
44. Patte-Mensah C, Mensah-Nyagan AG (2008). Peripheral neuropathy and neurosteroid formation in the central nervous system. Brain Res Rev 57:454-459. (Pubitemid 351391957)
45. Pitcher GM, Henry JL (2000). Cellular mechanisms of hyperalgesia and spontaneous pain in a spinalized rat model of peripheral neuropathy: changes in myelinated afferent inputs implicated. Eur J Neurosci 12: 2006-2020. (Pubitemid 30348838)
46. 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. (Pubitemid 36886161)
47. Romero-Sandoval EA, Horvath RJ, DeLeo JA (2008). Neuroimmune interactions and pain: focus on glial-modulating targets. Curr Opin Investig Drugs 9: 726-734. (Pubitemid 351950869)
48. Rowland M, Tozer TN (1995). Assessment of AUC. In: Balado D, editor. Clinical pharmacokinetics: concepts and applications. 3rd edition Philadelphia: Lippincott William and Wilkins. pp. 469-470.
49. Scholz J, Woolf CJ (2007). The neuropathic pain triad: neurons, immune cells and glia. Nat Neurosci 10:1361-1368. (Pubitemid 350014681)
50. Song P, Zhao ZQ (2001). The involvement of glial cells in the development of morphine tolerance. Neurosci Res 39:281-286. (Pubitemid 32186379)
51. Streit WJ, Mrak RE, Griffin WS (2004). Microglia and neuroinflammation: a pathological perspective. J Neuroinflammation 1:14.
52. Stuesse SL, Cruce WL, Lovell JA, McBurney DL, Crisp T (2000). Microglial proliferation in the spinal cord of aged rats with a sciatic nerve injury. Neurosci Lett 287:121-124. (Pubitemid 30353062)
53. Stuesse SL, Crisp T, McBurney DL, Schechter JB, Lovell JA, Cruce WL (2001). Neuropathic pain in aged rats: behavioral responses and astrocytic activation. Exp Brain Res 137:219-227. (Pubitemid 32250034)
54. Sung B, Lim G, Mao J (2003). Altered expression and uptake activity of spinal glutamate transporters after nerve injury contribute to the pathogenesis of neuropathic pain in rats. J Neurosci 23:2899-2910. (Pubitemid 36418626)
55. Suter MR,Wen YR, Decosterd I, Ji RR (2007). Do glial cells control pain? Neuron Glia Biol 3:255-268. (Pubitemid 351594231)
56. Svensson M, Eriksson P, Persson JK, Molander C, Arvidsson J, Aldskogius H (1993). The response of central glia to peripheral nerve injury. Brain Res Bull 30:499-506. (Pubitemid 23072762)
57. Sweitzer SM, Schubert P, DeLeo JA (2001). Propentofylline, a glial modulating agent, exhibits antiallodynic properties in a rat model of neuropathic pain. J Pharmacol Exp Ther 297:1210-1217. (Pubitemid 32472523)
58. Tawfik VL, Nutile-McMenemy N, Lacroix-Fralish ML, Deleo JA (2007). Efficacy of propentofylline, a glial modulating agent, on existing mechanical allodynia following peripheral nerve injury. Brain Behav Immun 21:238-246. (Pubitemid 46038912)
59. Toda S, Sakai A, Ikeda Y, Sakamoto A, Suzuki H (2011). A local anesthetic, ropivacaine, suppresses activated microglia via a nerve growth factor-dependent mechanism and astrocytes via a nerve growth factor-independent mechanism in neuropathic pain. Mol Pain 7:2.
60. Uceyler N, Schafers M, Sommer C (2009). Mode of action of cytokines on nociceptive neurons. Exp Brain Res 196:67-78.
61. Vitkovic L, Bockaert J, Jacque C (2000). "Inflammatory" cytokines: neuromodu-lators in normal brain? J Neurochem 74:457-471.
62. Warfield CA, Fausett HJ (2002). Manual of pain management. Philadelphia: Lippincott Williams and Wilkins.
63. Watkins LR, Maier SF (2003). Glia: a novel drug discovery target for clinical pain. Nat Rev Drug Discov 2:973-985. (Pubitemid 37540579)
64. Watkins LR, Milligan ED, Maier SF (2001). Glial activation: a driving force for pathological pain. Trends Neurosci 24:450-455. (Pubitemid 32695356)
65. Wen ZH, Tang CC, Chang YC, Huang SY, Hsieh SP, Lee CH, et al. (2010). Glucosamine sulfate reduces experimental osteoarthritis and nociception in rats: association with changes of mitogen-activated protein kinase in chondrocytes. Osteoarthritis Cartilage 18:1192-1202.
66. Winkelstein BA, Rutkowski MD, Sweitzer SM, Pahl JL, DeLeo JA (2001). Nerve injury proximal or distal to the DRG induces similar spinal glial activation and selective cytokine expression but differential behavioral responses to pharmacologic treatment. J Comp Neurol 439:127-139. (Pubitemid 32906017)
67. Xu JT, Xin WJ, Zang Y, Wu CY, Liu XG (2006). The role of tumor necrosis factor-alpha in the neuropathic pain induced by Lumbar 5 ventral root transection in rat. Pain 123:306-321.
68. Xu L, Huang Y, Yu X, Yue J, Yang N, Zuo P (2007). The influence of p38 mitogen-activated protein kinase inhibitor on synthesis of inflammatory cytokine tumor necrosis factor alpha in spinal cord of rats with chronic constriction injury. Anesth Analg 105:1838-1844. (Pubitemid 350190586)
69. Yaksh TL, Rudy TA (1976). Chronic catheterization of the spinal subarachnoid space. Physiol Behav 17:1031-1036. (Pubitemid 8063691)
70. Youn DH, Wang H, Jeong SJ (2008). Exogenous tumor necrosis factor-alpha rapidly alters synaptic and sensory transmission in the adult rat spinal cord dorsal horn. J Neurosci Res 86:2867-2875.
71. 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. (Pubitemid 40279096)
72. Zhuang ZY, Wen YR, Zhang DR, Borsello T, Bonny C, Strichartz GR, et al. (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.