Spinal astrocytic activation is involved in a virally-induced rat model of neuropathic pain

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Zhang, Gui He ^a,b   Lv, Miao Miao ^b   Wang, Shuang ^b   Chen, Lei ^c   Qian, Nian Song ^d   Tang, Yu ^e   Zhang, Xu Dong ^a   Ren, Peng Cheng ^a   Gao, Chang Jun ^a   Sun, Xu De ^a   Xu, Li Xian ^b  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^c NAVY GENERAL HOSPITAL   (China)

^d CHINESE PLA GENERAL HOSPITAL   (China)

^e BEIJING 302 HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

2 (4 CARBOXYPHENYL) 4,4,5,5 TETRAMETHYLIMIDAZOLINE 1 OXYL 3 OXIDE; 2 AMINOADIPIC ACID; 5 AMINOPHOSPHONOVALERIC ACID; 7 NITROINDAZOLE; DIZOCILPINE; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 1BETA; MINOCYCLINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; N6 (1 IMINOETHYL)LYSINE; NITRIC OXIDE; PENTOXIFYLLINE; UNCLASSIFIED DRUG; VALACICLOVIR;

ALLODYNIA; ANALGESIC ACTIVITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL ACTIVATION; CHRONIC PAIN; CONTROLLED STUDY; HERPES ZOSTER; MALE; MICROGLIA; NONHUMAN; PATHOGENESIS; POSTHERPETIC NEURALGIA; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SENSITIZATION; SPINAL CORD DORSAL HORN; SPINE; TREATMENT FAILURE; TREATMENT RESPONSE; VIRUS TRANSMISSION; ANIMAL; CYTOLOGY; DISEASE MODEL; ELECTROPHYSIOLOGY; FLUORESCENCE MICROSCOPY; GENE EXPRESSION REGULATION; HYPERALGESIA; METABOLISM; METHODOLOGY; NEURALGIA; PATHOLOGY; TIME; VARICELLA ZOSTER VIRUS; WISTAR RAT;

HERPES ZOSTER; HUMAN HERPESVIRUS 3; RATTUS;

ANIMALS; ASTROCYTES; DISEASE MODELS, ANIMAL; ELECTROPHYSIOLOGY; GENE EXPRESSION REGULATION; HERPES ZOSTER; HERPESVIRUS 3, HUMAN; HYPERALGESIA; INTERLEUKIN-1BETA; MALE; MICROSCOPY, FLUORESCENCE; NEURALGIA; NITRIC OXIDE; RATS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE; TIME FACTORS;

EID: 80053274963     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023059     Document Type: Article

References (53)

1. Dworkin RH, Portenoy RK, (1996) Pain and its persistence in herpes zoster. Pain 67: 241-251.
2. Bowsher D, (1997) The management of postherpetic neuralgia. Postgrad Med J 73: 623-629.
3. Lydick E, Epstein RS, Himmelberger D, White CJ, (1995) Herpes zoster and quality of life: a self-limited disease with severe impact. Neurology 45: S52-53.
4. Bowsher D, (1995) Pathophysiology of postherpetic neuralgia: towards a rational treatment. Neurology 45 (Suppl. 8): S56-S57.
5. Gilden DH, (1994) Herpes zoster with postherpetic neuralgia: persisting pain and frustration. N Engl J Med 330: 932-934.
6. Delaney A, Colvin LA, Fallon MT, Dalziel RG, Mitchell R, et al. (2009) Postherpetic Neuralgia: From Preclinical Models to the Clinic. Neurotherapeutics 6: 630-637.
7. Garry EM, Delaney A, Anderson HA, Sirinathsinghji EC, Clapp RH, et al. (2005) Varicella zoster virus induces neuropathic changes in rat dorsal root ganglia and behavioral reflex sensitisation that is attenuated by gabapentin or sodium channel blocking drugs. Pain 118: 97-111.
8. Christoph T, Schiene K, Englberger W, Parsons CG, Chizh BA, (2006) The antiallodynic effect of NMDA antagonists in neuropathic pain outlasts the duration of the in vivo NMDA antagonism. Neuropharmacology 51: 12-17.
9. Woolf CJ, Salter MW, (2000) Neuronal plasticity: increasing the gain in pain. Science 288: 1765-1769.
10. Brenner GJ, Ji RR, Shaffer S, Woolf CJ, (2004) Peripheral noxious stimulation induces phosphorylation of the NMDA receptor NR1 subunit at the PKC-dependent site, serine-896, in spinal cord dorsal horn neurons. Eur J Neurosci 20: 375-384.
11. Ultenius C, Linderoth B, Meyerson BA, Wallin J, (2006) Spinal NMDA receptor phosphorylation correlates with the presence of neuropathic signs following peripheral nerve injury in the rat. Neurosci Lett 399: 85-90.
12. DeLeo JA, Yezierski RP, (2001) The role of neuroinflammation and neuroimmune activation in persistent pain. Pain 90: 1-6.
13. Watkins LR, Milligan ED, Maier SF, (2001) Spinal cord glia: new players in pain. Pain 93: 201-205.
14. Watkins LR, Milligan ED, Maier SF, (2001) Glial activation: a driving force for pathological pain. Trends Neurosci 24: 450-455.
15. Watkins LR, Milligan ED, Maier SF, (2003) Glial proinflammatory cytokines mediate exaggerated pain states: implications for clinical pain. Adv Exp Med Biol 521: 1-21.
16. Viviani B, Bartesaghi S, Gardoni F, Vezzani A, Behrens MM, et al. (2003) Interleukin-1β enhances NMDA receptor-mediated intracellular calcium increase through activation of the Src family of kinases. J Neurosci 23: 8692-8700.
17. Wei F, Dubner R, Ren K, (2007) Glial-cytokine-neuronal interactions underlying the mechanisms of persistent pain. J Neurosci 27: 6006-6018.
18. Fleetwood-Walker SM, Quinn JP, Wallace C, Blackburn-Munro G, Kelly BG, et al. (1999) Behavioural changes in the rat following infection with varicella zoster virus. J Gen Virol 80: 2433-2436.
19. Sadzot-Delvaux C, Merville-Louis MP, Delree P, Marc P, Piette J, et al. (1990) An in vivo model of varicella-zoster virus latent infection of dorsal root ganglia. J Neurosci Res 26: 83-89.
20. Medhurst SJ, Collins SD, Billinton A, Bingham S, Dalziel RG, et al. (2008) Novel histamine H3 receptor antagonists GSK189254 and GSK334429 are efficacious in surgically-induced and virally-induced rat models of neuropathic pain. Pain 138: 61-69.
21. Dalziel RG, Bingham S, Sutton D, Grant D, Champion JM, et al. (2004) Allodynia in rats infected with varicella zoster virus-a small animal model for post-herpetic neuralgia. Brain Res Rev 46: 234-242.
22. Khurgel M, Koo AC, Ivy GO, (1996) Selective ablation of astrocytes by intracerebral injections of alpha-aminoadipate. Glia 16: 351-358.
23. Zimmermann M, (1983) Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16: 109-110.
24. Storkson RV, Kjorsvik A, Tjolsen A, Hole K, (1996) Lumbar catheterization of the spinal subarachnoid space in the rat. J Neurosci Methods 65: 167-172.
25. Wang W, Mei X, Huang J, Wei Y, Wang Y, et al. (2009) Crosstalk between spinal astrocytes and neurons in nerve injury-induced neuropathic pain. PLoS One 4: e6973.
26. Hua XY, Svensson CI, Matsui T, Fitzsimmons B, Yaksh TL, et al. (2005) Intrathecal minocycline attenuates peripheral inflammation-induced hyperalgesia by inhibiting p38 MAPK in spinal microglia. Eur J Neurosci 22: 2431-2440.
27. Zanchet EM, Longo I, Cury Y, (2004) Involvement of spinal neurokinins, excitatory amino acids, proinflammatory cytokines, nitric oxide and prostanoids in pain facilitation induced by Phoneutria nigriventer spider venom. Brain Res 1021: 101-111.
28. Chen SR, Eisenach JC, Pan HL, (2000) Intrathecal S-nitroso-N-acetylpenicillamine and L-cysteine attenuate nerve injury-induced allodynia through noradrenergic activation in rats. Neuroscience 101: 759-765.
29. Liu J, Feng XM, Yu M, Xie WY, Zhao X, et al. (2007) Pentoxifylline attenuates the development of hyperalgesia in a rat model of neuropathic pain. Neurosci Lett 412: 268-272.
30. Zhang RX, Li A, Liu B, Wang L, Ren K, et al. (2008) IL-1ra alleviates inflammatory hyperalgesia through preventing phosphorylation of NMDA receptor NR-1 subunit in rats. Pain 135: 232-239.
31. Hao JX, Xu IS, Xu XJ, Wiesenfeld-Hallin Z, (1999) Effects of intrathecal morphine, clonidine and baclofen on allodynia after partial sciatic nerve injury in the rat. Acta Anaesthesiol Scand 43: 1027-1034.
32. Rowbotham MC, Fields HL, (1996) The relationship of pain, allodynia and thermal sensation in post-herpetic neuralgia. Brain 119: 347-354.
33. 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.
34. 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.
35. Cho IH, Chung YM, Park CK, Park SH, Li HY, et al. (2006) Systemic administration of minocycline inhibits formalin-induced inflammatory pain in rat. Brain Res 1072: 208-214.
36. Hains BC, Waxman SG, (2006) Activated microglia contribute to the maintenance of chronic pain after spinal cord injury. J Neurosci 26: 4308-4317.
37. Raghavendra V, Tanga FY, DeLeo JA, (2004) Complete Freunds adjuvant-induced peripheral inflammation evokes glial activation and proinflammatory cytokine expression in the CNS. Eur J Neurosci 20: 467-473.
38. Feng QX, Wang W, Feng XY, Mei XP, Zhu C, et al. (2010) Astrocytic activation in thoracic spinal cord contributes to persistent pain in rat model of chronic pancreatitis. Neuroscience 167: 501-509.
39. Liao YH, Zhang GH, Jia D, Wang P, Qian NS, et al. (2011) Spinal astrocytic activation contributes to mechanical allodynia in a mouse model of type 2 diabetes. Brain Res 1368: 324-335.
40. Mika J, Osikowicz M, Rojewska E, Korostynski M, Wawrzczak-Bargiela A, et al. (2009) Differential activation of spinal microglial and astroglial cells in a mouse model of peripheral neuropathic pain. Eur J Pharmacol 623: 65-72.
41. 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.
42. Basbaum AI, Bautista DM, Scherrer G, Julius D, (2009) Cellular and Molecular Mechanisms of Pain. Cell 139: 267-284.
43. Zimmermann M, (2001) Pathobiology of neuropathic pain. Eur J Pharmacol 429: 23-37.
44. Brahmachari S, Fung YK, Pahan K, (2006) Induction of glial fibrillary acidic protein expression in astrocytes by nitric oxide. J Neurosci 26: 4930-4939.
45. Holguin A, O'Connor KA, Biedenkapp J, Campisi J, Wieseler-Frank J, et al. (2004) HIV-1 gp120 stimulates proinflammatory cytokine-mediated pain facilitation via activation of nitric oxide synthase-I (nNOS). Pain 110: 517-530.
46. Meller ST, Gebhart GF, (1993) Nitric oxide (NO) and nociceptive processing in the spinal cord. Pain 52: 127-136.
47. Zhang RX, Liu B, Wang L, Ren K, Qiao JT, et al. (2005) Spinal glial activation in a new rat model of bone cancer pain produced by prostate cancer cell inoculation of the tibia. Pain 118: 125-136.
48. Safieh-Garabedian B, Poole S, Allchorne A, Winter J, Woolf CJ, (1995) Contribution of interleukin-1β to the inflammation-induced increase in nerve growth factor levels and inflammatory hyperalgesia. Brit J Pharmacol 115: 1265-1275.
49. Sweitzer S, Martin D, DeLeo JA, (2001) Intrathecal interleukin-1 receptor antagonist in combination with soluble tumor necrosis factor receptor exhibits an anti-allodynic action in a rat model of neuropathic pain. Neuroscience 103: 529-539.
50. Guo W, Wang H, Watanabe M, Shimizu K, Zou S, et al. (2007) Glial-cytokine-neuronal interactions underlying the mechanisms of persistent pain. J Neurosci 27: 6006-6018.
51. Dayer JM, (2003) The pivotal role of interleukin-1 in the clinical manifestations of rheumatoid arthritis. Rheumatology (Oxford) 42: ii3-i10.
52. Samad TA, Moore KA, Sapirstein A, Billet S, Allchorne A, et al. (2001) Interleukin-1beta-mediated induction of Cox-2 in the CNS contributes to inflammatory pain hypersensitivity. Nature 410: 471-475.
53. Mei XP, Wang W, Wang W, Zhu C, Chen L, et al. (2010) Combining ketamine with astrocytic inhibitor as a potential analgesic strategy for neuropathic pain. ketamine, astrocytic inhibitor and pain. Mol Pain 6: 50.