Systemic administration of an alpha-7 nicotinic acetylcholine agonist reverses neuropathic pain in male sprague dawley rats

Journal of Pain

Volumn 13, Issue 12, 2012, Pages 1162-1171

  Loram, Lisa C ^a   Taylor, Frederick R ^a   Strand, Keith A ^a   Maier, Steven F ^a   Speake, Jason D ^b   Jordan, Kristen G ^b   James, John W ^b   Wene, Steven P ^b   Pritchard, Robert C ^b   Green, Heather ^b   Van Dyke, Katherine ^b   Mazarov, Anatoly ^b   Letchworth, Sharon R ^b   Watkins, Linda R ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b TARGACEPT INC   (United States)

Author keywords

7 nAchR agonist; allodynia; antinociception; chronic constriction injury; dorsal root ganglia; Glial activation

Indexed keywords

BUNGAROTOXIN RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; NICOTINIC AGENT; TC 7020; TRANSCRIPTION FACTOR 3; UNCLASSIFIED DRUG;

ALLODYNIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; CELL DENSITY; CONTROLLED STUDY; DOWN REGULATION; DRUG PENETRATION; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MALE; MICROGLIA; NERVE CELL LESION; NEUROPATHIC PAIN; NONHUMAN; RAT; SATELLITE CELL; SPINAL CORD; SPINAL GANGLION;

ANIMALS; GANGLIA, SPINAL; MALE; NEURALGIA; NICOTINIC AGONISTS; QUINUCLIDINES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, NICOTINIC; THIOPHENES;

EID: 84870209841     PISSN: 15265900     EISSN: 15288447     Source Type: Journal    
DOI: 10.1016/j.jpain.2012.08.009     Document Type: Article

References (67)

1. C. Abbadie Chemokines, chemokine receptors and pain Trends Immunol 26 2005 529 534
2. M.J. Abdin, N. Morioka, K. Morita, T. Kitayama, S. Kitayama, T. Nakashima, and T. Dohi Analgesic action of nicotine on tibial nerve transection (TNT)-induced mechanical allodynia through enhancement of the glycinergic inhibitory system in spinal cord Life Sci 80 2006 9 16
3. P.J. Austin, and G. Moalem-Taylor The neuro-immune balance in neuropathic pain: Involvement of inflammatory immune cells, immune-like glial cells and cytokines J Neuroimmunol 229 2010 26 50
4. M. Bencherif, P.M. Lippiello, R. Lucas, and M.B. Marrero Alpha7 nicotinic receptors as novel therapeutic targets for inflammation-based diseases Cell Mol Life Sci 68 2011 931 949
5. G.J. Bennett, and Y.K. Xie A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man Pain 33 1988 87 107
6. L.V. Borovikova, S. Ivanova, D. Nardi, M. Zhang, H. Yang, M. Ombrellino, and K.J. Tracey Role of vagus nerve signaling in CNI-1493-mediated suppression of acute inflammation Auton Neurosci 85 2000 141 147
7. L.V. Borovikova, S. Ivanova, M. Zhang, H. Yang, G.I. Botchkina, L.R. Watkins, H. Wang, N. Abumrad, J.W. Eaton, and K.J. Tracey Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin Nature 405 2000 458 462
8. W. Bruck The role of macrophages in Wallerian degeneration Brain Pathol 7 1997 741 752
9. R.J. Cady, J.R. Glenn, K.M. Smith, and P.L. Durham Calcitonin gene-related peptide promotes cellular changes in trigeminal neurons and glia implicated in peripheral and central sensitization Mol Pain 7 2011 94
10. M. Chacur, E.D. Milligan, L.S. Gazda, C. Armstrong, H. Wang, K.J. Tracey, S.F. Maier, and L.R. Watkins A new model of sciatic inflammatory neuritis (SIN): Induction of unilateral and bilateral mechanical allodynia following acute unilateral peri-sciatic immune activation in rats Pain 94 2001 231 244
11. P.K. Chatterjee, Y. Al-Abed, B. Sherry, and C.N. Metz Cholinergic agonists regulate JAK2/STAT3 signaling to suppress endothelial cell activation Am J Physiol Cell Physiol 297 2009 C1294 C1306
12. M. Costigan, J. Scholz, and C.J. Woolf Neuropathic pain: A maladaptive response of the nervous system to damage Annu Rev Neurosci 32 2009 1 32
13. M.I. Damaj, E.M. Meyer, and B.R. Martin The antinociceptive effects of alpha7 nicotinic agonists in an acute pain model Neuropharmacology 39 2000 2785 2791
14. J.A. De Leo, V.L. Tawfik, and M.L. LaCroix-Fralish The tetrapartite synapse: Path to CNS sensitization and chronic pain Pain 122 2006 17 21
15. R.D. Fields New culprits in chronic pain Sci Am 301 2009 50 57
16. Y.J. Gao, and R.R. Ji Chemokines, neuronal-glial interactions, and central processing of neuropathic pain Pharmacol Ther 126 2010 56 68
17. P.M. Grace, P.E. Rolan, and M.R. Hutchinson Peripheral immune contributions to the maintenance of central glial activation underlying neuropathic pain Brain Behav Immun 25 2011 1322 1332
18. M. Grybko, G. Sharma, and S. Vijayaraghavan Functional distribution of nicotinic receptors in CA3 region of the hippocampus J Mol Neurosci 40 2010 114 120
19. M.S. Gurun, R. Parker, J.C. Eisenach, and M. Vincler The effect of peripherally administered CDP-choline in an acute inflammatory pain model: The role of alpha7 nicotinic acetylcholine receptor Anesth Analg 108 2009 1680 1687
20. T. Hai, C.D. Wolfgang, D.K. Marsee, A.E. Allen, and U. Sivaprasad ATF3 and stress responses Gene Expr 7 1999 321 335
21. R. Hamano, H.K. Takahashi, H. Iwagaki, T. Yoshino, M. Nishibori, and N. Tanaka Stimulation of alpha7 nicotinic acetylcholine receptor inhibits CD14 and the toll-like receptor 4 expression in human monocytes Shock 26 2006 358 364
22. L.O. Harvey Efficient estimation of sensory thresholds Behav Res Methods Instrum Comput 18 1986 623 632
23. K. Inoue, T. Zama, T. Kamimoto, R. Aoki, Y. Ikeda, H. Kimura, and M. Hagiwara TNFalpha-induced ATF3 expression is bidirectionally regulated by the JNK and ERK pathways in vascular endothelial cells Genes Cells 9 2004 59 70
24. R. Jancalek, P. Dubovy, I. Svizenska, and I. Klusakova Bilateral changes of TNF-alpha and IL-10 protein in the lumbar and cervical dorsal root ganglia following a unilateral chronic constriction injury of the sciatic nerve J Neuroinflammation 7 2010 11
25. S.M. Jeon, K.M. Lee, and H.J. Cho Expression of monocyte chemoattractant protein-1 in rat dorsal root ganglia and spinal cord in experimental models of neuropathic pain Brain Res 1251 2009 103 111
26. H. Jung, P.T. Toth, F.A. White, and R.J. Miller Monocyte chemoattractant protein-1 functions as a neuromodulator in dorsal root ganglia neurons J Neurochem 104 2008 254 263
27. I.M. Khan, T.L. Yaksh, and P. Taylor Ligand specificity of nicotinic acetylcholine receptors in rat spinal cord: Studies with nicotine and cytisine J Pharmacol Exp Ther 270 1994 159 166
28. N. Kiguchi, T. Maeda, Y. Kobayashi, Y. Fukazawa, and S. Kishioka Macrophage inflammatory protein-1alpha mediates the development of neuropathic pain following peripheral nerve injury through interleukin-1beta up-regulation Pain 149 2010 305 315
29. M. Kox, J.C. Pompe, M.C. Gordinou de Gouberville, J.G. van der Hoeven, C.W. Hoedemaekers, and P. Pickkers Effects of the alpha7nAChR Agonist GTS-21 on the Innate Immune Response in Humans Shock 36 2011 5 11
30. L.C. Loram, J.A. Harrison, L. Chao, F.R. Taylor, A. Reddy, C.L. Travis, R. Giffard, Y. Al-Abed, K. Tracey, S.F. Maier, and L.R. Watkins Intrathecal injection of an alpha seven nicotinic acetylcholine receptor agonist attenuates gp120-induced mechanical allodynia and spinal pro-inflammatory cytokine profiles in rats Brain Behav Immun 24 2010 959 967
31. L.C. Loram, J.A. Harrison, E.M. Sloane, M.R. Hutchinson, P. Sholar, F.R. Taylor, D. Berkelhammer, B.D. Coats, S. Poole, E.D. Milligan, S.F. Maier, J. Rieger, and L.R. Watkins Enduring reversal of neuropathic pain by a single intrathecal injection of adenosine 2A receptor agonists: A novel therapy for neuropathic pain J Neurosci 29 2009 14015 14025
32. M.B. Marrero, R. Lucas, C. Salet, T.A. Hauser, A. Mazurov, P.M. Lippiello, and M. Bencherif An alpha7 nicotinic acetylcholine receptor-selective agonist reduces weight gain and metabolic changes in a mouse model of diabetes J Pharmacol Exp Ther 332 2010 173 180
33. S.J. Medhurst, J.P. Hatcher, C.J. Hille, S. Bingham, N.M. Clayton, A. Billinton, and I.P. Chessell Activation of the alpha7-nicotinic acetylcholine receptor reverses complete freund adjuvant-induced mechanical hyperalgesia in the rat via a central site of action J Pain 9 2008 580 587
34. P. Miao, K. Madec, Y. Gong, H. Shen, D. Eisenstat, M. Melanson, X. Gu, C. Leong, M. Klowak, and M. Namaka Axotomy-induced up-regulation of tumor necrosis factor-alpha in the dorsal root ganglia Neurol Res 30 2008 623 631
35. E.D. Milligan, S.F. Maier, and L.R. Watkins Sciatic inflammatory neuropathy in the rat: Surgical procedures, induction of inflammation, and behavioral testing Methods Mol Med 99 2004 67 89
36. E.D. Milligan, K.K. Mehmert, J.L. Hinde, L.O. Harvey, D. Martin, K.J. Tracey, S.F. Maier, and L.R. Watkins Thermal hyperalgesia and mechanical allodynia produced by intrathecal administration of the human immunodeficiency virus-1 (HIV-1) envelope glycoprotein, gp120 Brain Res 861 2000 105 116
37. E.D. Milligan, R.G. Soderquist, S.M. Malone, J.H. Mahoney, T.S. Hughes, S.J. Langer, E.M. Sloane, S.F. Maier, L.A. Leinwand, L.R. Watkins, and M.J. Mahoney Intrathecal polymer-based interleukin-10 gene delivery for neuropathic pain Neuron Glia Biol 2 2006 293 308
38. E.D. Milligan, C. Twining, M. Chacur, J. Biedenkapp, K. O'Connor, S. Poole, K. Tracey, D. Martin, S.F. Maier, and L.R. Watkins Spinal glia and proinflammatory cytokines mediate mirror-image neuropathic pain in rats J Neurosci 23 2003 1026 1040
39. E.D. Milligan, and L.R. Watkins Pathological and protective roles of glia in chronic pain Nat Rev Neurosci 10 2009 23 36
40. R. Myers, R. Wagner, and L. Sorkin Hyperalgesic actions of cytokines on peripheral nerves L. Watkins, S. Maier, Cytokines and Pain 1999 Birkhauser Verlag Basel, CH 133 156
41. R. Nirogi, V. Kandikere, K. Mudigonda, G. Bhyrapuneni, N. Muddana, R. Saralaya, and V. Benade A simple and rapid method to collect the cerebrospinal fluid of rats and its application for the assessment of drug penetration into the central nervous system J Neurosci Methods 178 2009 116 119
42. K. Obata, H. Yamanaka, T. Fukuoka, D. Yi, A. Tokunaga, N. Hashimoto, H. Yoshikawa, and K. Noguchi Contribution of injured and uninjured dorsal root ganglion neurons to pain behavior and the changes in gene expression following chronic constriction injury of the sciatic nerve in rats Pain 101 2003 65 77
43. K. Obata, H. Yamanaka, K. Kobayashi, Y. Dai, T. Mizushima, H. Katsura, T. Fukuoka, A. Tokunaga, and K. Noguchi Role of mitogen-activated protein kinase activation in injured and intact primary afferent neurons for mechanical and heat hypersensitivity after spinal nerve ligation J Neurosci 24 2004 10211 10222
44. F.E. Perrin, S. Lacroix, M. Aviles-Trigueros, and S. David Involvement of monocyte chemoattractant protein-1, macrophage inflammatory protein-1alpha and interleukin-1beta in Wallerian degeneration Brain 128 2005 854 866
45. C.M. Peters, J.R. Ghilardi, C.P. Keyser, K. Kubota, T.H. Lindsay, N.M. Luger, D.B. Mach, M.J. Schwei, M.A. Sevcik, and P.W. Mantyh Tumor-induced injury of primary afferent sensory nerve fibers in bone cancer pain Exp Neurol 193 2005 85 100
46. M.H. Rashid, and H. Ueda Neuropathy-specific analgesic action of intrathecal nicotinic agonists and its spinal GABA-mediated mechanism Brain Res 953 2002 53 62
47. E.A. Romero-Sandoval, R.J. Horvath, and J.A. DeLeo Neuroimmune interactions and pain: Focus on glial-modulating targets Curr Opin Investig Drugs 9 2008 726 734
48. M. Rosas-Ballina, R.S. Goldstein, M. Gallowitsch-Puerta, L. Yang, S.I. Valdes-Ferrer, N.B. Patel, S. Chavan, Y. Al-Abed, H. Yang, and K.J. Tracey The selective alpha7 agonist GTS-21 attenuates cytokine production in human whole blood and human monocytes activated by ligands for TLR2, TLR3, TLR4, TLR9, and RAGE Mol Med 15 2009 195 202
49. M. Rosas-Ballina, M. Ochani, W.R. Parrish, K. Ochani, Y.T. Harris, J.M. Huston, S. Chavan, and K.J. Tracey Splenic nerve is required for cholinergic antiinflammatory pathway control of TNF in endotoxemia Proc Natl Acad Sci U S A 105 2008 11008 11013
50. T.J. Rowley, A. McKinstry, E. Greenidge, W. Smith, and P. Flood Antinociceptive and anti-inflammatory effects of choline in a mouse model of postoperative pain Br J Anaesth 105 2010 201 207
51. T.J. Rowley, J. Payappilly, J. Lu, and P. Flood The antinociceptive response to nicotinic agonists in a mouse model of postoperative pain Anesth Analg 107 2008 1052 1057
52. J. Scholz, and C.J. Woolf The neuropathic pain triad: Neurons, immune cells and glia Nat Neurosci 10 2007 1361 1368
53. I.V. Shelukhina, E.V. Kryukova, K.S. Lips, V.I. Tsetlin, and W. Kummer Presence of alpha7 nicotinic acetylcholine receptors on dorsal root ganglion neurons proved using knockout mice and selective alpha-neurotoxins in histochemistry J Neurochem 109 2009 1087 1095
54. R.D. Shytle, T. Mori, K. Townsend, M. Vendrame, N. Sun, J. Zeng, J. Ehrhart, A.A. Silver, P.R. Sanberg, and J. Tan Cholinergic modulation of microglial activation by alpha 7 nicotinic receptors J Neurochem 89 2004 337 343
55. S. Sweitzer, D. Martin, and J.A. DeLeo 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 2001 529 539
56. H.K. Takahashi, H. Iwagaki, R. Hamano, T. Yoshino, N. Tanaka, and M. Nishibori alpha7 Nicotinic acetylcholine receptor stimulation inhibits lipopolysaccharide-induced interleukin-18 and -12 production in monocytes J Pharmacol Sci 102 2006 143 146
57. N. Takahashi, S. Kikuchi, V.I. Shubayev, W.M. Campana, and R.R. Myers TNF-alpha and phosphorylation of ERK in DRG and spinal cord: Insights into mechanisms of sciatica Spine (Phila Pa 1976) 31 2006 523 529
58. R.S. Taylor Epidemiology of refractory neuropathic pain Pain Pract 6 2006 22 26
59. M.A. Thacker, A.K. Clark, T. Bishop, J. Grist, P.K. Yip, L.D. Moon, S.W. Thompson, F. Marchand, and S.B. McMahon CCL2 is a key mediator of microglia activation in neuropathic pain states Eur J Pain 13 2009 263 272
60. K. Tsuzuki, E. Kondo, T. Fukuoka, D. Yi, H. Tsujino, M. Sakagami, and K. Noguchi Differential regulation of P2X(3) mRNA expression by peripheral nerve injury in intact and injured neurons in the rat sensory ganglia Pain 91 2001 351 360
61. C.M. Twining, E.M. Sloane, E.D. Milligan, M. Chacur, D. Martin, S. Poole, H. Marsh, S.F. Maier, and L.R. Watkins Peri-sciatic proinflammatory cytokines, reactive oxygen species, and complement induce mirror-image neuropathic pain in rats Pain 110 2004 299 309
62. H. Wang, M. Yu, M. Ochani, C.A. Amella, M. Tanovic, S. Susarla, J.H. Li, H. Yang, L. Ulloa, Y. Al-Abed, C.J. Czura, and K.J. Tracey Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation Nature 421 2003 384 388
63. Y. Wang, D.M. Su, R.H. Wang, Y. Liu, and H. Wang Antinociceptive effects of choline against acute and inflammatory pain Neuroscience 132 2005 49 56
64. L.R. Watkins, M.R. Hutchinson, E.D. Milligan, and S.F. Maier "Listening" and "talking" to neurons: Implications of immune activation for pain control and increasing the efficacy of opioids Brain Res Rev 56 2007 148 169
65. L.R. Watkins, and S.F. Maier Beyond neurons: Evidence that immune and glial cells contribute to pathological pain states Physiol Rev 82 2002 981 1011
66. F.A. White, P. Feldman, and R.J. Miller Chemokine signaling and the management of neuropathic pain Mol Interv 9 2009 188 195
67. T. Young, S. Wittenauer, R. Parker, and M. Vincler Peripheral nerve injury alters spinal nicotinic acetylcholine receptor pharmacology Eur J Pharmacol 590 2008 163 169