Over-expression of P2X7 receptors in spinal glial cells contributes to the development of chronic postsurgical pain induced by skin/muscle incision and retraction (SMIR) in rats

Experimental Neurology

Volumn 261, Issue , 2014, Pages 836-843

  Ying, Yan Lu ^a   Wei, Xu Hong ^b   Xu, Xue Bing ^c   She, Shou Zhang ^a   Zhou, Li Jun ^b   Lv, Jing ^a   Li, Dai ^b   Zheng, Bin ^a   Liu, Xian Guo ^b  

^a GUANGZHOU MEDICAL UNIVERSITY   (China)

^b SUN YAT SEN UNIVERSITY   (China)

^c THE UNIVERSITY OF HONG KONG SHENZHEN HOSPITAL   (China)

Author keywords

Chronic postsurgical pain; Microglia; P2X7 receptor; Tumor necrosis factor alpha

Indexed keywords

3 [[5 (2,3 DICHLOROPHENYL) 1H TETRAZOL 1 YL]METHYL]PYRIDINE; BRILLIANT BLUE; PURINERGIC P2X7 RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; 3-(5-(2,3-DICHLOROPHENYL)-1H-TETRAZOL-1-YL)METHYLPYRIDINE; GLIAL FIBRILLARY ACIDIC PROTEIN; PURINERGIC P2X RECEPTOR ANTAGONIST; PYRIDINE DERIVATIVE; TETRAZOLE DERIVATIVE;

ALLODYNIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CHRONIC PAIN; CHRONIC POSTSURGICAL PAIN; CONTROLLED STUDY; DISEASE COURSE; GLIA CELL; IMMUNOFLUORESCENCE TEST; IMMUNOREACTIVITY; INCISION; MALE; MICROGLIA; MUSCLE INCISION; NERVE CELL LESION; NERVE CELL STIMULATION; NERVOUS SYSTEM PARAMETERS; NONHUMAN; POSTOPERATIVE PAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PSYCHOPHYSIOLOGY; RAT; RECEPTOR UPREGULATION; SAPHENOUS NERVE; SCHWANN CELL; SKIN INCISION; SPINAL CORD DORSAL HORN; SPINAL CORD NERVE CELL; SPINAL GANGLION; ANIMAL; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; GLIA; HEMISPHERIC DOMINANCE; METABOLISM; MUSCLE; PAIN, POSTOPERATIVE; PATHOLOGY; PHYSIOLOGY; SKIN; SKIN SURGERY; SPINAL CORD; SPRAGUE DAWLEY RAT; SURGERY; TIME; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; UPREGULATION;

ANIMALS; DERMATOLOGIC SURGICAL PROCEDURES; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; FUNCTIONAL LATERALITY; GLIAL FIBRILLARY ACIDIC PROTEIN; MALE; MICROSCOPY, ELECTRON, TRANSMISSION; MUSCLES; NEUROGLIA; PAIN, POSTOPERATIVE; PURINERGIC P2X RECEPTOR ANTAGONISTS; PYRIDINES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, PURINERGIC P2X7; SKIN; SPINAL CORD; TETRAZOLES; TIME FACTORS; UP-REGULATION;

EID: 84908373979     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2014.09.007     Document Type: Article

References (38)

1. Aoyama R., Okada Y., Yokota S., Yasui Y., Fukuda K., Shinozaki Y., et al. Spatiotemporal and anatomical analyses of P2X receptor-mediated neuronal and glial processing of sensory signals in the rat dorsal horn. Pain 2011, 152:2085-2097.
2. Chacur M., Milligan E.D., Gazda L.S., Armstrong C., Wang H., Tracey K.J., et al. A new model of sciatic inflammatory neuritis (SIN): induction of unilateral and bilateral mechanical allodynia following acute unilateral perisciatic immune activation in rats. Pain 2001, 94:231-244.
3. Chaplan S.R., Bach F.W., Pogrel J.W., Chung J.M., Yaksh T.L. Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 1994, 53:55-63.
4. Chessell I.P., Hatcher J.P., Bountra C., Michel A.D., Hughes J.P., Green P., et al. Disruption of the P2X7 purinoceptor gene abolishes chronic inflammatory and neuropathic pain. Pain 2005, 114:386-396.
5. Chu Y.X., Zhang Y., Zhang Y.Q., Zhao Z.Q. Involvement of microglial P2X7 receptors and downstream signaling pathways in long-term potentiation of spinal nociceptive responses. Brain Behav Immun 2010, 24:1176-1189.
6. Ferrari D., Pizzirani C., Adinolfi E., Lemoli R.M., Curti A., Idzko M., et al. The P2X7 receptor: a key player in IL-1 processing and release. J Immunol 2006, 176:3877-3883.
7. Flatters S.J. Characterization of a model of persistent postoperative pain evoked by skin/muscle incision and retraction (SMIR). Pain 2008, 135:119-130.
8. Guo L.H., Schluesener H.J. Acute but not chronic stimulation of glial cells in rat spinal cord by systemic injection of lipopolysaccharide is associated with hyperalgesia. Acta Neuropathol 2006, 112:703-713.
9. Honda S., Sasaki Y., Ohsawa K., Imai Y., Nakamura Y., Inoue K., et al. Extracellular ATP and ADP induce chemotaxis of cultured microglia through Gi/o-coupled P2Y receptors. J Neurosci 2001, 21:1975-1982.
10. Honore P., Donnelly-Roberts D., Namovic M.T., Hsieh G., Zhu C.Z., Mikusa J.P., et al. A-740003 [N-(1-{[(cyanoimino)(5-quinolinylamino) methyl]amino}-2,2-dimethylpropyl)-2-(3,4-dimethoxyphenyl)acetamide], a novel and selective P2X7 receptor antagonist, dose-dependently reduces neuropathic pain in the rat. J Pharmacol Exp Ther 2006, 319:1376-1385.
11. Huang L., Gao Y.J., Wang J., Strichartz G. Shifts in cell-type expression accompany a diminishing role of spinal p38-mapkinase activation over time during prolonged postoperative pain. Anesthesiology 2011, 115:1281-1290.
12. Ji R.R., Suter M.R. p38 MAPK, microglial signaling, and neuropathic pain. Mol Pain 2007, 3:33.
13. Kawasaki Y., Zhang L., Cheng J.K., Ji R.R. Cytokine mechanisms of central sensitization: distinct and overlapping role of interleukin-1beta, interleukin-6, and tumor necrosis factor-alpha in regulating synaptic and neuronal activity in the superficial spinal cord. J Neurosci 2008, 28:5189-5194.
14. Kehlet H., Jensen T.S., Woolf C.J. Persistent postsurgical pain: risk factors and prevention. Lancet 2006, 367:1618-1625.
15. Khakh B.S., North R.A. P2X receptors as cell-surface ATP sensors in health and disease. Nature 2006, 442:527-532.
16. Lazarowski E.R., Boucher R.C., Harden T.K. Constitutive release of ATP and evidence for major contribution of ecto-nucleotide pyrophosphatase and nucleoside diphosphokinase to extracellular nucleotide concentrations. J Biol Chem 2000, 275:31061-31068.
17. Leung L., Cahill C.M. TNF-α and neuropathic pain - a review. J Neuroinflammation 2010, 7:27.
18. Ma J.Y., Zhao Z.Q. The involvement of glia in long-term plasticity in the spinal dorsal horn of the rat. Neuroreport 2002, 13:1781-1784.
19. Ma L., Uchida H., Nagai J., Inoue M., Aoki J., Ueda H. Evidence for de novo synthesis of lysophosphatidic acid in the spinal cord through phospholipase A2 and autotaxin in nerve injury-induced neuropathic pain. J Pharmacol Exp Ther 2010, 333:540-546.
20. McGaraughty S., Chu K.L., Namovic M.T., Donnelly-Roberts D.L., Harris R.R., Zhang X.F., et al. P2X7-related modulation of pathological nociception in rats. Neuroscience 2007, 146:1817-1828.
21. Monif M., Reid C.A., Powell K.L., Smart M.L., Williams D.A. The P2X7 receptor drives microglial activation and proliferation: a trophic role for P2X7R pore. J Neurosci 2009, 29:3781-3791.
22. Nieber K., Eschke D., Brand E. Brain hypoxia: effects of ATP and adenosine. Prog Brain Res 1999, 120:287-297.
23. North R.A. Molecular physiology of P2X receptors. Physiol Rev 2002, 82:1013-1067.
24. Oliveira J.F., Riedel T., Leichsenring A., Heine C., Franke H., Krugel U., et al. Rodent cortical astroglia express in situ functional P2X7 receptors sensing pathologically high ATP concentrations. Cereb Cortex 2011, 21:806-820.
25. Shieh C.H., Heinrich A., Serchov T., van C.D., Biber K. P2X7-dependent, but differentially regulated release of IL-6, CCL2, and TNF-alpha in cultured mouse microglia. Glia 2014, 62:592-607.
26. Skaper S.D., Debetto P., Giusti P. The P2X7 purinergic receptor: from physiology to neurological disorders. FASEB J 2010, 24:337-345.
27. Sperlagh B., Vizi E.S., Wirkner K., Illes P. P2X7 receptors in the nervous system. Prog Neurobiol 2006, 78:327-346.
28. Steyaert A., De K.M. Chronic postsurgical pain. Curr Opin Anaesthesiol 2012, 25:584-588.
29. Volanté C., Amadio S., Cavaliere F., D'Ambrosi N., Vacca F., Bernardi G. Extracellular ATP and neurodegeneration. Curr Drug Targets CNS Neurol Disord 2003, 2:403-412.
30. Wang H., Bloom O., Zhang M., Vishnubhakat J.M., Ombrellino M., Che J., et al. HMG-1 as a later mediator of endotoxin lethality in mice. Science 1999, 285:248-251.
31. Wei X.H., Zang Y., Wu C.Y., Xu J.T., Xin W.J., Liu X.G. Peri-sciatic administration of recombinant rat TNF-α induces mechanical allodynia via upregulation of TNF-α in dorsal root ganglia and in spinal dorsal horn: the role of NF-kappa B pathway. Exp Neurol 2007, 205:471-484.
32. Wei X.H., Yang T., Wu Q., Xin W.J., Wu J.L., Wang Y.Q., et al. Peri-sciatic administration of recombinant rat IL-1beta induces mechanical allodynia by activation of src-family kinases in spinal microglia in rats. Exp Neurol 2012, 234:389-397.
33. Wei X.H., Na X.D., Liao G.J., Chen Q.Y., Cui Y., Chen F.Y., et al. The up-regulation of IL-6 in DRG and spinal dorsal horn contributes to neuropathic pain following L5 ventral root transection. Exp Neurol 2013, 241:159-168.
34. Xu J.T., Xin W.J., Zang Y., Wu C.Y., Liu X.G. The role of tumor necrosis factor-alpha in the neuropathic pain induced by Lumbar 5 ventral root transection in rat. Pain 2006, 123:306-321.
35. Ying B., Lu N., Zhang Y.Q., Zhao Z.Q. Involvement of spinal glia in tetanically sciatic stimulation-induced bilateral mechanical allodynia in rats. Biochem Biophys Res Commun 2006, 340:1264-1272.
36. Zhuang Z.Y., Gerner P., Woolf C.J., Ji R.R. ERK is sequentially activated in neurons, microglia, and astrocytes by spinal nerve ligation and contributes to mechanical allodynia in this neuropathic pain model. Pain 2005, 114:149-159.
37. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 1983, 16:109-110.
38. Zimmermann M. Pathobiology of neuropathic pain. Eur J Pharmacol 2001, 429:23-37.