Reopening of ATP-sensitive potassium channels reduces neuropathic pain and regulates astroglial gap junctions in the rat spinal cord

Pain

Volumn 152, Issue 11, 2011, Pages 2605-2615

  Wu, Xue Feng ^a,b   Liu, Wen Tao ^a   Liu, Yue Peng ^a   Huang, Zhi Jiang ^a   Zhang, Yan Kai ^a   Song, Xue Jun ^a  

^a Parker University   (United States)

^b NANJING UNIVERSITY   (China)

Author keywords

Carbenoxolone; Connexin 43; Cromakalim; Nerve injury; Spinal cord

Indexed keywords

ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM ION; CARBENOXOLONE; CONNEXIN 43; CROMAKALIM; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GAP JUNCTION PROTEIN; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR6.1; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR6.2; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; SULFONYLUREA RECEPTOR; SULFONYLUREA RECEPTOR 1; SULFONYLUREA RECEPTOR 2; UNCLASSIFIED DRUG;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; HYPERALGESIA; MACROGLIA; MALE; NEUROPATHIC PAIN; NONHUMAN; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SCIATIC NERVE; SCIATIC NERVE INJURY; SIGNAL TRANSDUCTION; SPINAL CORD;

ANIMALS; ASTROCYTES; ATP-BINDING CASSETTE TRANSPORTERS; CROMAKALIM; GAP JUNCTIONS; HYPERALGESIA; KATP CHANNELS; MALE; NEURALGIA; POTASSIUM CHANNELS, INWARDLY RECTIFYING; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, DRUG; SCIATICA; SPINAL CORD;

EID: 80054971706     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1016/j.pain.2011.08.003     Document Type: Article

References (43)

1. A.P. Babenko, L. Aguilar-Bryan, and J. Bryan A view of sur/KIR6.X, KATP channels Annu Rev Physiol 60 1998 667 687
2. X. Bao, L. Reuss, and G.A. Altenberg Regulation of purified and reconstituted connexin 43 hemichannels by protein kinase C-mediated phosphorylation of Serine 368 J Biol Chem 279 2004 20058 20066 (Pubitemid 38623450)
3. V.M. Berthoud, M.L. Ledbetter, E.L. Hertzberg, and J.C. Saez Connexin 43 in MDCK cells: regulation by a tumor-promoting phorbol ester and Ca2+ Eur J Cell Biol 57 1992 40 50
4. J.L. Brissette, N.M. Kumar, N.B. Gilula, and G.P. Dotto The tumor promoter 12-O-tetradecanoylphorbol-13-acetate and the ras oncogene modulate expression and phosphorylation of gap junction proteins Mol Cell Biol 11 1991 5364 5371 (Pubitemid 21895300)
5. R. Dermietzel Diversification of gap junction proteins (connexins) in the central nervous system and the concept of functional compartments Cell Biol Int 22 1998 719 730 (Pubitemid 29509301)
6. B.N. Giepmans, T. Hengeveld, F.R. Postma, and W.H. Moolenaar Interaction of c-Src with gap junction protein connexin 43. Role in the regulation of cell-cell communication J Biol Chem 276 2001 8544 8549
7. J. Gilleron, C. Fiorini, D. Carette, C. Avondet, M.M. Falk, D. Segretain, and G. Pointis Molecular reorganization of Cx43, Zo-1 and Src complexes during the endocytosis of gap junction plaques in response to a non-genomic carcinogen J Cell Sci 121 2008 4069 4078
8. D. Gosejacob, P. Dublin, P. Bedner, K. Huttmann, J. Zhang, O. Tress, K. Willecke, F. Pfrieger, C. Steinhauser, and M. Theis Role of astroglial connexin30 in hippocampal gap junction coupling Glia 59 2011 511 519
9. M. Hanani, T.Y. Huang, P.S. Cherkas, M. Ledda, and E. Pannese Glial cell plasticity in sensory ganglia induced by nerve damage Neuroscience 114 2002 279 283 (Pubitemid 35245408)
10. N. Inagaki, T. Gonoi, J.P. Clement, C.Z. Wang, L. Aguilar-Bryan, J. Bryan, and S. Seino A family of sulfonylurea receptors determines the pharmacological properties of ATP-sensitive K+ channels Neuron 16 1996 1011 1017 (Pubitemid 26171205)
11. N. Inagaki, Y. Tsuura, N. Namba, K. Masuda, T. Gonoi, M. Horie, Y. Seino, M. Mizuta, and S. Seino Cloning and functional characterization of a novel ATP-sensitive potassium channel ubiquitously expressed in rat tissues, including pancreatic islets, pituitary, skeletal muscle, and heart J Biol Chem 270 1995 5691 5694
12. A. Jahangir, and S.C. Hammill Parasympathetics and atrial fibrillation J Cardiovasc Electrophysiol 16 2005 885 887 (Pubitemid 41623781)
13. L. Jasmin, J.P. Vit, A. Bhargava, and P.T. Ohara Can satellite glial cells be therapeutic targets for pain control? Neuron Glia Biol 6 2010 63 71
14. R.R. Ji, Y. Kawasaki, Z.Y. Zhuang, Y.R. Wen, and I. Decosterd Possible role of spinal astrocytes in maintaining chronic pain sensitization: review of current evidence with focus on bFGF/JNK pathway Neuron Glia Biol 2 2006 259 269 (Pubitemid 47074743)
15. H. Katsura, K. Obata, T. Mizushima, J. Sakurai, K. Kobayashi, H. Yamanaka, Y. Dai, T. Fukuoka, M. Sakagami, and K. Noguchi Activation of Src-family kinases in spinal microglia contributes to mechanical hypersensitivity after nerve injury J Neurosci 26 2006 8680 8690 (Pubitemid 44319403)
16. T. Kawano, V. Zoga, G. Gemes, J.B. McCallum, H.E. Wu, D. Pravdic, M.Y. Liang, W.M. Kwok, Q. Hogan, and C. Sarantopoulos Suppressed Ca2+/CaM/CaMKII- dependent K(ATP) channel activity in primary afferent neurons mediates hyperalgesia after axotomy Proc Natl Acad Sci USA 106 2009 8725 8730
17. T. Kawano, V. Zoga, M. Kimura, M.Y. Liang, H.E. Wu, G. Gemes, J.B. McCallum, W.M. Kwok, Q.H. Hogan, and C.D. Sarantopoulos Nitric oxide activates ATP-sensitive potassium channels in mammalian sensory neurons: action by direct S-nitrosylation Mol Pain 5 2009 12
18. C. Koster-Patzlaff, S.M. Hosseini, and B. Reuss Layer specific changes of astroglial gap junctions in the rat cerebellar cortex by persistent Borna disease virus infection Brain Res 1219 2008 143 158
19. P.D. Lampe Analyzing phorbol ester effects on gap junctional communication: a dramatic inhibition of assembly J Cell Biol 127 1994 1895 1905
20. P.D. Lampe, E.M. TenBroek, J.M. Burt, W.E. Kurata, R.G. Johnson, and A.F. Lau Phosphorylation of connexin 43 on serine368 by protein kinase C regulates gap junctional communication J Cell Biol 149 2000 1503 1512 (Pubitemid 30437622)
21. R. Lin, B.J. Warn-Cramer, W.E. Kurata, and A.F. Lau v-Src phosphorylation of connexin 43 on Tyr247 and Tyr265 disrupts gap junctional communication J Cell Biol 154 2001 815 827 (Pubitemid 34292962)
22. W.T. Liu, Y. Han, Y.P. Liu, A.A. Song, B. Barnes, and X.J. Song Spinal matrix metalloproteinase-9 contributes to physical dependence on morphine in mice J Neurosci 30 2010 7613 7623
23. W.T. Liu, H.C. Li, X.S. Song, Z.J. Huang, and X.J. Song EphB receptor signaling in mouse spinal cord contributes to physical dependence on morphine FASEB J 23 2008 90 98
24. X.J. Liu, J.R. Gingrich, M. Vargas-Caballero, Y.N. Dong, A. Sengar, S. Beggs, S.H. Wang, H.K. Ding, P.W. Frankland, and M.W. Salter Treatment of inflammatory and neuropathic pain by uncoupling Src from the NMDA receptor complex Nat Med 14 2008 1325 1332
25. L.M. Magnotti, D.A. Goodenough, and D.L. Paul Deletion of oligodendrocyte Cx32 and astrocyte Cx43 causes white matter vacuolation, astrocyte loss and early mortality Glia 59 2011 1064 1074
26. J. Mika, E. Rojewska, W. Makuch, M. Korostynski, S. Luvisetto, S. Marinelli, F. Pavone, and B. Przewlocka The effect of botulinum neurotoxin A on sciatic nerve injury-induced neuroimmunological changes in rat dorsal root ganglia and spinal cord Neuroscience 175 2010 358 366
27. D. Mor, A.L. Bembrick, P.J. Austin, P.M. Wyllie, N.J. Creber, G.S. Denyer, and K.A. Keay Anatomically specific patterns of glial activation in the periaqueductal gray of the sub-population of rats showing pain and disability following chronic constriction injury of the sciatic nerve Neuroscience 166 2010 1167 1184
28. P.T. Ohara, J.P. Vit, A. Bhargava, and L. Jasmin Evidence for a role of connexin 43 in trigeminal pain using RNA interference in vivo J Neurophysiol 100 2008 3064 3073
29. K. Procida, L. Jorgensen, N. Schmitt, M. Delmar, S.M. Taffet, N.H. Holstein-Rathlou, M.S. Nielsen, and T.H. Braunstein Phosphorylation of connexin 43 on serine 306 regulates electrical coupling Heart Rhythm 6 2009 1632 1638
30. K. Ren, and R. Dubner Neuron-glia crosstalk gets serious: role in pain hypersensitivity Curr Opin Anaesthesiol 21 2008 570 579
31. J.K. Reynhout, P.D. Lampe, and R.G. Johnson An activator of protein kinase C inhibits gap junction communication between cultured bovine lens cells Exp Cell Res 198 1992 337 342
32. D.H. Roh, S.Y. Yoon, H.S. Seo, S.Y. Kang, H.J. Han, A.J. Beitz, and J.H. Lee Intrathecal injection of carbenoxolone, a gap junction decoupler, attenuates the induction of below-level neuropathic pain after spinal cord injury in rats Exp Neurol 224 2010 123 132
33. S. Seino ATP-sensitive potassium channels: a model of heteromultimeric potassium channel/receptor assemblies Annu Rev Physiol 61 1999 337 362 (Pubitemid 29143174)
34. S. Seino, and T. Miki Physiological and pathophysiological roles of ATP-sensitive K+ channels Prog Biophys Mol Biol 81 2003 133 176 (Pubitemid 36141258)
35. X.J. Song, C. Vizcarra, D.S. Xu, R.L. Rupert, and Z.N. Wong Hyperalgesia and neural excitability following injuries to central and peripheral branches of axons and somata of dorsal root ganglion neurons J Neurophysiol 89 2003 2185 2193 (Pubitemid 36444271)
36. X.J. Song, Z.B. Wang, Q. Gan, and E.T. Walters cAMP and cGMP contribute to sensory neuron hyperexcitability and hyperalgesia in rats with dorsal root ganglia compression J Neurophysiol 95 2006 479 492 (Pubitemid 44698949)
37. L.E. Spataro, E.M. Sloane, E.D. Milligan, J. Wieseler-Frank, D. Schoeniger, B.M. Jekich, R.M. Barrientos, S.F. Maier, and L.R. Watkins Spinal gap junctions: potential involvement in pain facilitation J Pain 5 2004 392 405 (Pubitemid 39410108)
38. J.P. Vit, L. Jasmin, A. Bhargava, and P.T. Ohara Satellite glial cells in the trigeminal ganglion as a determinant of orofacial neuropathic pain Neuron Glia Biol 2 2006 247 257 (Pubitemid 47074744)
39. Z.B. Wang, Q. Gan, R.L. Rupert, Y.M. Zeng, and X.J. Song Thiamine, pyridoxine, cyanocobalamin and their combination inhibit thermal, but not mechanical hyperalgesia in rats with primary sensory neuron injury Pain 114 2005 266 277 (Pubitemid 40279109)
40. Wu XF, Liu WT, Liu YP, Song XJ. Reopening of ATP-sensitive potassium channels reduces neuropathic hyperalgesia via improving spinal astroglial gap junctional communication. Soc Neurosci Abstracts 2010;376.14/SS14.
41. T. Yamamoto, A. Ochalski, E.L. Hertzberg, and J.I. Nagy LM and EM immunolocalization of the gap junctional protein connexin 43 in rat brain Brain Res 508 1990 313 319 (Pubitemid 20063469)
42. M.L. Zhuo, Y. Huang, D.P. Liu, and C.C. Liang KATP channel: relation with cell metabolism and role in the cardiovascular system Int J Biochem Cell Biol 37 2005 751 764 (Pubitemid 40202997)
43. V. Zoga, T. Kawano, M.Y. Liang, M. Bienengraeber, D. Weihrauch, B. McCallum, G. Gemes, Q. Hogan, and C. Sarantopoulos KATP channel subunits in rat dorsal root ganglia: alterations by painful axotomy Mol Pain 6 2010 6