Spinal 5-HT3 receptors facilitate behavioural hypersensitivity induced by elevated calcium channel alpha-2-delta-1 protein

European Journal of Pain (United Kingdom)

Volumn 17, Issue 4, 2013, Pages 505-513

  Chang, E Y ^a   Chen, X ^a,b   Sandhu, A ^a   Li, C Y ^a   Luo, Z D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CHINA MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA 2 DELTA 1 PROTEIN; CALCIUM CHANNEL; ONDANSETRON; PROTEIN; SEROTONIN 3 AGONIST; UNCLASSIFIED DRUG;

ALLODYNIA; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DOSE RESPONSE; DRUG EFFICACY; HYPERALGESIA; HYPERSENSITIVITY; MECHANICAL STIMULATION; MOUSE; NERVE INJURY; NONHUMAN; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; PROTEIN EXPRESSION; THERMAL STIMULATION;

ANIMALS; CALCIUM CHANNELS; HYPERALGESIA; INJECTIONS, INTRAPERITONEAL; INJECTIONS, SPINAL; MALE; MICE; MICE, TRANSGENIC; NEURALGIA; ONDANSETRON; PAIN MEASUREMENT; PHYSICAL STIMULATION; RECEPTORS, SEROTONIN, 5-HT3; SEROTONIN 5-HT3 RECEPTOR ANTAGONISTS; SPINAL CORD; UP-REGULATION;

EID: 84879573310     PISSN: 10903801     EISSN: 15322149     Source Type: Journal    
DOI: 10.1002/j.1532-2149.2012.00221.x     Document Type: Article

References (40)

1. Basbaum, A.I., Fields, H.L. (1984). Endogenous pain control systems: Brainstem spinal pathways and endorphin circuitry. Annu Rev Neurosci 7, 309-338.
2. Bauer, C.S., Nieto-Rostro, M., Rahman, W., Tran-Van-Minh, A., Ferron, L., Douglas, L., Kadurin, I., Sri Ranjan, Y., Fernandez- Alacid, L., Millar, N.S., Dickenson, A.H., Lujan, R., Dolphin, A.C. (2009). The increased trafficking of the calcium channel subunit alpha2delta-1 to presynaptic terminals in neuropathic pain is inhibited by the alpha2delta ligand pregabalin. J Neurosci 29, 4076-4088.
3. Bee, L.A., Dickenson, A.H. (2008). Descending facilitation from the brainstem determines behavioural and neuronal hypersensitivity following nerve injury and efficacy of pregabalin. Pain 140, 209-223.
4. Boroujerdi, A., Kim, H.K., Lyu, Y.S., Kim, D.S., Figueroa, K.W., Chung, J.M., Luo, Z.D. (2008). Injury discharges regulate calcium channel alpha-2-delta-1 subunit upregulation in the dorsal horn that contributes to initiation of neuropathic pain. Pain 139, 358-366.
5. Chesler, E.J., Wilson, S.G., Lariviere, W.R., Rodriguez-Zas, S.L., Mogil, J.S. (2002). Identification and ranking of genetic and laboratory environment factors influencing a behavioral trait, thermal nociception, via computational analysis of a large data archive. Neurosci Biobehav Rev 26, 907-923.
6. Conte, D., Legg, E.D., McCourt, A.C., Silajdzic, E., Nagy, G.G., Maxwell, D.J. (2005). Transmitter content, origins and connections of axons in the spinal cord that possess the serotonin (5-hydroxytryptamine) 3 receptor. Neuroscience 134, 165- 173.
7. Costigan, M., Befort, K., Karchewski, L., Griffin, R.S., D'Urso, D., Allchorne, A., Sitarski, J., Mannion, J.W., Pratt, R.E., Woolf, C.J. (2002). Replicate high-density rat genome oligonucleotide microarrays reveal hundreds of regulated genes in the dorsal root ganglion after peripheral nerve injury. BMC Neurosci 3, 16.
8. Derbent, A., Uyar, M., Demirag, K., Uyer, M., Kurtoglu, E., Goktay, A. (2005). Can antiemetics really relieve pain? Adv Ther 22, 307-312.
9. Dixon, W.J. (1980). Efficient analysis of experimental observations. Annu Rev Pharmacol Toxicol 20, 441-462.
10. Dogrul, A., Ossipov, M.H., Porreca, F. (2009). Differential mediation of descending pain facilitation and inhibition by spinal 5HT-3 and 5HT-7 receptors. Brain Res 1280, 52-59.
11. Farber, L., Haus, U., Spath, M., Drechsler, S. (2004). Physiology and pathophysiology of the 5-HT3 receptor. Scand J Rheumatol Suppl 119, 2-8.
12. Fozard, J.R. (1984). Neuronal 5-HT receptors in the periphery. Neuropharmacology 23, 1473-1486.
13. Gee, N.S., Brown, J.P., Dissanayake, V.U., Offord, J., Thurlow, R., Woodruff, G.N. (1996). The novel anticonvulsant drug, gabapentin (Neurontin), binds to the alpha2delta subunit of a calcium channel. J Biol Chem 271, 5768-5776.
14. Green, G.M., Scarth, J., Dickenson, A. (2000). An excitatory role for 5-HT in spinal inflammatory nociceptive transmission; state-dependent actions via dorsal horn 5-HT(3) receptors in the anaesthetized rat. Pain 89, 81-88.
15. 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.
16. Kidd, E.J., Laporte, A.M., Langlois, X., Fattaccini, C.M., Doyen, C., Lombard, M.C., Gozlan, H., Hamon, M. (1993). 5-HT3 receptors in the rat central nervous system are mainly located on nerve fibres and terminals. Brain Res 612, 289-298.
17. Kim, D.S., Figueroa, K.W., Li, K.W., Boroujerdi, A., Yolo, T., Luo, Z.D. (2009). Profiling of dynamically changed gene expression in dorsal root ganglia post peripheral nerve injury and a critical role of injury-induced glial fibrillary acidic protein in maintenance of pain behaviors [corrected]. Pain 143, 114-122.
18. Kim, S.H., Chung, J.M. (1992). An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 50, 355-363.
19. Leong, M.L., Gu, M., Speltz-Paiz, R., Stahura, E.I., Mottey, N., Steer, C.J., Wessendorf, M. (2011). Neuronal loss in the rostral ventromedial medulla in a rat model of neuropathic pain. J Neurosci 31, 17028-17039.
20. Li, C.Y., Song, Y.H., Higuera, E.S., Luo, Z.D. (2004). Spinal dorsal horn calcium channel alpha2delta-1 subunit upregulation contributes to peripheral nerve injury-induced tactile allodynia. J Neurosci 24, 8494-8499.
21. Li, C.Y., Zhang, X.L., Matthews, E.A., Li, K.W., Kurwa, A., Boroujerdi, A., Gross, J., Gold, M.S., Dickenson, A.H., Feng, G., Luo, Z.D. (2006). Calcium channel alpha2delta1 subunit mediates spinal hyperexcitability in pain modulation. Pain 125, 20-34.
22. Luo, Z.D., Calcutt, N.A., Higuera, E.S., Valder, C.R., Song, Y.H., Svensson, C.I., Myers, R.R. (2002). Injury type-specific calcium channel alpha 2 delta-1 subunit up-regulation in rat neuropathic pain models correlates with antiallodynic effects of gabapentin. J Pharmacol Exp Ther 303, 1199-1205.
23. Luo, Z.D., Chaplan, S.R., Higuera, E.S., Sorkin, L.S., Stauderman, K.A., Williams, M.E., Yaksh, T.L. (2001). Upregulation of dorsal root ganglion (alpha)2(delta) calcium channel subunit and its correlation with allodynia in spinal nerve-injured rats. J Neurosci 21, 1868-1875.
24. McCleane, G.J., Suzuki, R., Dickenson, A.H. (2003). Does a single intravenous injection of the 5HT3 receptor antagonist ondansetron have an analgesic effect in neuropathic pain? A double-blinded, placebo-controlled cross-over study. Anesth Analg 97, 1474-1478.
25. Newton, R.A., Bingham, S., Case, P.C., Sanger, G.J., Lawson, S.N. (2001). Dorsal root ganglion neurons show increased expression of the calcium channel alpha2delta-1 subunit following partial sciatic nerve injury. Brain Res Mol Brain Res 95, 1-8.
26. Nguyen, D., Deng, P., Matthews, E.A., Kim, D.S., Feng, G., Dickenson, A.H., Xu, Z.C., Luo, Z.D. (2009). Enhanced presynaptic glutamate release in deep-dorsal horn contributes to calcium channel alpha-2-delta-1 protein-mediated spinal sensitization and behavioral hypersensitivity. Mol Pain 5, 6.
27. Peters, C.M., Hayashida, K., Ewan, E.E., Nakajima, K., Obata, H., Xu, Q., Yaksh, T.L., Eisenach, J.C. (2010). Lack of analgesic efficacy of spinal ondansetron on thermal and mechanical hypersensitivity following spinal nerve ligation in the rat. Brain Res 1352, 83-93.
28. Rahman, W., Bauer, C.S., Bannister, K., Vonsy, J.L., Dolphin, A.C., Dickenson, A.H. (2009). Descending serotonergic facilitation and the antinociceptive effects of pregabalin in a rat model of osteoarthritic pain. Mol Pain 5, 45.
29. Rahman, W., Suzuki, R., Rygh, L.J., Dickenson, A.H. (2004). Descending serotonergic facilitation mediated through rat spinal 5HT3 receptors is unaltered following carrageenan inflammation. Neurosci Lett 361, 229-231.
30. Rigaud, M., Gemes, G., Barabas, M.E., Chernoff, D.I., Abram, S.E., Stucky, C.L., Hogan, Q.H. (2008). Species and strain differences in rodent sciatic nerve anatomy: Implications for studies of neuropathic pain. Pain 136, 188-201.
31. Suzuki, R., Morcuende, S., Webber, M., Hunt, S.P., Dickenson, A.H. (2002). Superficial NK1-expressing neurons control spinal excitability through activation of descending pathways. Nat Neurosci 5, 1319-1326.
32. Suzuki, R., Rahman, W., Hunt, S.P., Dickenson, A.H. (2004). Descending facilitatory control of mechanically evoked responses is enhanced in deep dorsal horn neurones following peripheral nerve injury. Brain Res 1019, 68-76.
33. Suzuki, R., Rahman, W., Rygh, L.J., Webber, M., Hunt, S.P., Dickenson, A.H. (2005). Spinal-supraspinal serotonergic circuits regulating neuropathic pain and its treatment with gabapentin. Pain 117, 292-303.
34. Taylor, C.P. (2009). Mechanisms of analgesia by gabapentin and pregabalin - calcium channel alpha2-delta [Cavalpha2-delta] ligands. Pain 142, 13-16.
35. Tuveson, B., Leffler, A.S., Hansson, P. (2011). Ondansetron, a 5HT3-antagonist, does not alter dynamic mechanical allodynia or spontaneous ongoing pain in peripheral neuropathy. Clin J Pain 27, 323-329.
36. Valder, C.R., Liu, J.J., Song, Y.H., Luo, Z.D. (2003). Coupling gene chip analyses and rat genetic variances in identifying potential target genes that may contribute to neuropathic allodynia development. J Neurochem 87, 560-573.
37. Wang, H., Sun, H., Della Penna, K., Benz, R.J., Xu, J., Gerhold, D.L., Holder, D.J., Koblan, K.S. (2002). Chronic neuropathic pain is accompanied by global changes in gene expression and shares pathobiology with neurodegenerative diseases. Neuroscience 114, 529-546.
38. Yakel, J.L., Jackson, M.B. (1988). 5-HT3 receptors mediate rapid responses in cultured hippocampus and a clonal cell line. Neuron 1, 615-621.
39. Zeitz, K.P., Guy, N., Malmberg, A.B., Dirajlal, S., Martin, W.J., Sun, L., Bonhaus, D.W., Stucky, C.L., Julius, D., Basbaum, A.I. (2002). The 5-HT3 subtype of serotonin receptor contributes to nociceptive processing via a novel subset of myelinated and unmyelinated nociceptors. J Neurosci 22, 1010-1019.
40. Zhuo, M., Gebhart, G.F. (1991). Spinal serotonin receptors mediate descending facilitation of a nociceptive reflex from the nuclei reticularis gigantocellularis and gigantocellularis pars alpha in the rat. Brain Res 550, 35-48. Development