Impaired neuropathic pain and preserved acute pain in rats overexpressing voltage-gated potassium channel subunit Kv1.2 in primary afferent neurons

Molecular Pain

Volumn 10, Issue 1, 2014, Pages

  Fan, Longchang ^a,b   Guan, Xiaowei ^a   Wang, Wei ^a   Zhao, Jian Yuan ^a   Zhang, Hongkang ^a   Tiwari, Vinod ^a   Hoffman, Paul N ^a   Li, Min ^a   Tao, Yuan Xiang ^a,c  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

Distribution; Dorsal root ganglion; Kv1.2; Neuropathic pain; Potassium channels

Indexed keywords

ACUTE PAIN; ANIMALS; CAPSAICIN; GANGLIA, SPINAL; HEK293 CELLS; HUMANS; KV1.2 POTASSIUM CHANNEL; LIGATION; MALE; MOTOR ACTIVITY; NEURALGIA; NEURONS, AFFERENT; NOCICEPTION; PERIPHERAL NERVE INJURIES; PROTEIN TRANSPORT; RATS; RATS, SPRAGUE-DAWLEY; RNA, ANTISENSE; RNA, MESSENGER; SPINAL NERVES; TIME FACTORS; TRANSFECTION; UP-REGULATION;

EID: 84893016639     PISSN: None     EISSN: 17448069     Source Type: Journal    
DOI: 10.1186/1744-8069-10-8     Document Type: Article

References (43)

1. Campbell JN, Meyer RA. Mechanisms of neuropathic pain. Neuron 2006, 52:77-92. 10.1016/j.neuron.2006.09.021, 1810425, 17015228.
2. Baron R, Binder A, Wasner G. Neuropathic pain: diagnosis, pathophysiological mechanisms, and treatment. Lancet Neurol 2010, 9:807-819. 10.1016/S1474-4422(10)70143-5, 20650402.
3. Finnerup NB, Sindrup SH, Jensen TS. The evidence for pharmacological treatment of neuropathic pain. Pain 2010, 150:573-581. 10.1016/j.pain.2010.06.019, 20705215.
4. Ji RR, Woolf CJ. Neuronal plasticity and signal transduction in nociceptive neurons: implications for the initiation and maintenance of pathological pain. Neurobiol Dis 2001, 8:1-10. 10.1006/nbdi.2000.0360, 11162235.
5. Latremoliere A, Woolf CJ. Central sensitization: a generator of pain hypersensitivity by central neural plasticity. J Pain 2009, 10:895-926. 10.1016/j.jpain.2009.06.012, 2750819, 19712899.
6. Altier C, Zamponi GW. Targeting Ca2+ channels to treat pain: T-type versus N-type. Trends Pharmacol Sci 2004, 25:465-470. 10.1016/j.tips.2004.07.004, 15559248.
7. Shieh CC. Ion channels as therapeutic targets for neuropathic pain. Curr Pharm Des 2009, 15:1709-1710. 10.2174/138161209788186317, 19442184.
8. Wang W, Gu J, Li YQ, Tao YX. Are voltage-gated sodium channels on the dorsal root ganglion involved in the development of neuropathic pain?. Mol Pain 2011, 7:16. 10.1186/1744-8069-7-16, 3052185, 21345196.
9. Coetzee WA, Amarillo Y, Chiu J, Chow A, Lau D, McCormack T, Moreno H, Nadal MS, Ozaita A, Pountney D, Saganich M, de Vega-Saenz ME, Rudy B. Molecular diversity of K + channels. Ann N Y Acad Sci 1999, 868:233-285. 10.1111/j.1749-6632.1999.tb11293.x, 10414301.
10. Ocana M, Cendan CM, Cobos EJ, Entrena JM, Baeyens JM. Potassium channels and pain: present realities and future opportunities. Eur J Pharmacol 2004, 500:203-219. 10.1016/j.ejphar.2004.07.026, 15464034.
11. Pongs O. Regulation of excitability by potassium channels. Results Probl Cell Differ 2008, 44:145-161. 10.1007/400_2007_032, 17579818.
12. Yang EK, Takimoto K, Hayashi Y, de Groat WC, Yoshimura N. Altered expression of potassium channel subunit mRNA and alpha-dendrotoxin sensitivity of potassium currents in rat dorsal root ganglion neurons after axotomy. Neuroscience 2004, 123:867-874. 10.1016/j.neuroscience.2003.11.014, 14751280.
13. Ishikawa K, Tanaka M, Black JA, Waxman SG. Changes in expression of voltage-gated potassium channels in dorsal root ganglion neurons following axotomy. Muscle Nerve 1999, 22:502-507. 10.1002/(SICI)1097-4598(199904)22:4<502::AID-MUS12>3.0.CO;2-K, 10204786.
14. Rasband MN, Park EW, Vanderah TW, Lai J, Porreca F, Trimmer JS. Distinct potassium channels on pain-sensing neurons. Proc Natl Acad Sci USA 2001, 98:13373-13378. 10.1073/pnas.231376298, 60878, 11698689.
15. Kim DS, Choi JO, Rim HD, Cho HJ. Downregulation of voltage-gated potassium channel alpha gene expression in dorsal root ganglia following chronic constriction injury of the rat sciatic nerve. Brain Res Mol Brain Res 2002, 105:146-152. 10.1016/S0169-328X(02)00388-1, 12399117.
16. Zhao X, Tang Z, Zhang H, Atianjoh FE, Zhao JY, Liang L, Wang W, Guan X, Kao SC, Tiwari V, Gao YJ, Hoffman PN, Cui H, Li M, Dong X, Tao YX. A long noncoding RNA contributes to neuropathic pain by silencing Kcna2 in primary afferent neurons. Nat Neurosci 2013, 16:1024-1031. 10.1038/nn.3438, 23792947.
17. Han PJ, Shukla S, Subramanian PS, Hoffman PN. Cyclic AMP elevates tubulin expression without increasing intrinsic axon growth capacity. Exp Neurol 2004, 189:293-302. 10.1016/j.expneurol.2004.03.010, 15380480.
18. Xu Y, Gu Y, Wu P, Li GW, Huang LY. Efficiencies of transgene expression in nociceptive neurons through different routes of delivery of adeno-associated viral vectors. Hum Gene Ther 2003, 14:897-906. 10.1089/104303403765701187, 12828860.
19. Xu Y, Gu Y, Xu GY, Wu P, Li GW, Huang LY. Adeno-associated viral transfer of opioid receptor gene to primary sensory neurons: a strategy to increase opioid antinociception. Proc Natl Acad Sci USA 2003, 100:6204-6209. 10.1073/pnas.0930324100, 156350, 12719538.
20. Guan X, Zhu X, Tao YX. Peripheral nerve injury up-regulates expression of interactor protein for cytohesin exchange factor 1 (IPCEF1) mRNA in rat dorsal root ganglion. Naunyn Schmiedebergs Arch Pharmacol 2009, 380:459-463. 10.1007/s00210-009-0451-7, 2771885, 19756519.
21. Lee CY, Perez FM, Wang W, Guan X, Zhao X, Fisher JL, Guan Y, Sweitzer SM, Raja SN, Tao YX. Dynamic temporal and spatial regulation of mu opioid receptor expression in primary afferent neurons following spinal nerve injury. Eur J Pain 2011, 15:669-675. 10.1016/j.ejpain.2010.11.018, 3129388, 21310637.
22. Singh OV, Yaster M, Xu JT, Guan Y, Guan X, Dharmarajan AM, Raja SN, Zeitlin PL, Tao YX. Proteome of synaptosome-associated proteins in spinal cord dorsal horn after peripheral nerve injury. Proteomics 2009, 9:1241-1253. 10.1002/pmic.200800636, 2768229, 19206110.
23. Zhang B, Tao F, Liaw WJ, Bredt DS, Johns RA, Tao YX. Effect of knock down of spinal cord PSD-93/chapsin-110 on persistent pain induced by complete Freund's adjuvant and peripheral nerve injury. Pain 2003, 106:187-196. 10.1016/j.pain.2003.08.003, 14581127.
24. Lu YC, Chen CW, Wang SY, Wu FS. 17Beta-estradiol mediates the sex difference in capsaicin-induced nociception in rats. J Pharmacol Exp Ther 2009, 331:1104-1110. 10.1124/jpet.109.158402, 19773532.
25. Jankowski MP, Lawson JJ, McIlwrath SL, Rau KK, Anderson CE, Albers KM, Koerber HR. Sensitization of cutaneous nociceptors after nerve transection and regeneration: possible role of target-derived neurotrophic factor signaling. J Neurosci 2009, 29:1636-1647. 10.1523/JNEUROSCI.3474-08.2009, 2768416, 19211871.
26. Park JS, Voitenko N, Petralia RS, Guan X, Xu JT, Steinberg JP, Takamiya K, Sotnik A, Kopach O, Huganir RL, Tao YX. Persistent inflammation induces GluR2 internalization via NMDA receptor-triggered PKC activation in dorsal horn neurons. J Neurosci 2009, 29:3206-3219. 10.1523/JNEUROSCI.4514-08.2009, 2664544, 19279258.
27. Park JS, Yaster M, Guan X, Xu JT, Shih MH, Guan Y, Raja SN, Tao YX. Role of spinal cord alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors in complete Freund's adjuvant-induced inflammatory pain. Mol Pain 2008, 4:67. 10.1186/1744-8069-4-67, 2628655, 19116032.
28. Tao F, Liaw WJ, Zhang B, Yaster M, Rothstein JD, Johns RA, Tao YX. Evidence of neuronal excitatory amino acid carrier 1 expression in rat dorsal root ganglion neurons and their central terminals. Neuroscience 2004, 123:1045-1051. 10.1016/j.neuroscience.2003.11.026, 14751295.
29. Xu JT, Zhao X, Yaster M, Tao YX. Expression and distribution of mTOR, p70S6K, 4E-BP1, and their phosphorylated counterparts in rat dorsal root ganglion and spinal cord dorsal horn. Brain Res 2010, 1336:46-57. 2874637, 20399760.
30. Douglas CL, Vyazovskiy V, Southard T, Chiu SY, Messing A, Tononi G, Cirelli C. Sleep in Kcna2 knockout mice. BMC Biol 2007, 5:42. 10.1186/1741-7007-5-42, 2151933, 17925011.
31. Castle NA, London DO, Creech C, Fajloun Z, Stocker JW, Sabatier JM. Maurotoxin: a potent inhibitor of intermediate conductance Ca2 + -activated potassium channels. Mol Pharmacol 2003, 63:409-418. 10.1124/mol.63.2.409, 12527813.
32. Fulton S, Thibault D, Mendez JA, Lahaie N, Tirotta E, Borrelli E, Bouvier M, Tempel BL, Trudeau LE. Contribution of Kv1.2 voltage-gated potassium channel to D2 autoreceptor regulation of axonal dopamine overflow. J Biol Chem 2011, 286:9360-9372. 10.1074/jbc.M110.153262, 3059064, 21233214.
33. Visan V, Fajloun Z, Sabatier JM, Grissmer S. Mapping of maurotoxin binding sites on hKv1.2, hKv1.3, and hIKCa1 channels. Mol Pharmacol 2004, 66:1103-1112. 10.1124/mol.104.002774, 15286210.
34. Bradbury EJ, Burnstock G, McMahon SB. The expression of P2X3 purinoreceptors in sensory neurons: effects of axotomy and glial-derived neurotrophic factor. Mol Cell Neurosci 1998, 12:256-268. 10.1006/mcne.1998.0719, 9828090.
35. Ji RR, Shi TJ, Xu ZQ, Zhang Q, Sakagami H, Tsubochi H, Kondo H, Hokfelt T. Ca2+/calmodulin-dependent protein kinase type IV in dorsal root ganglion: colocalization with peptides, axonal transport and effect of axotomy. Brain Res 1996, 721:167-173. 10.1016/0006-8993(95)01316-4, 8793097.
36. Papka RE, McNeill DL. Coexistence of calcitonin gene-related peptide and galanin immunoreactivity in female rat pelvic and lumbosacral dorsal root ganglia. Peptides 1992, 13:761-767. 10.1016/0196-9781(92)90184-5, 1279631.
37. Aoki Y, Takahashi Y, Ohtori S, Moriya H, Takahashi K. Distribution and immunocytochemical characterization of dorsal root ganglion neurons innervating the lumbar intervertebral disc in rats: a review. Life Sci 2004, 74:2627-2642. 10.1016/j.lfs.2004.01.008, 15041445.
38. Kim DS, Lee SJ, Cho HJ. Differential usage of multiple brain-derived neurotrophic factor promoter in rat dorsal root ganglia following peripheral nerve injuries and inflammation. Brain Res Mol Brain Res 2001, 92:167-171. 10.1016/S0169-328X(01)00154-1, 11483253.
39. Park SY, Choi JY, Kim RU, Lee YS, Cho HJ, Kim DS. Downregulation of voltage-gated potassium channel alpha gene expression by axotomy and neurotrophins in rat dorsal root ganglia. Mol Cells 2003, 16:256-259.
40. Liu CN, Michaelis M, Amir R, Devor M. Spinal nerve injury enhances subthreshold membrane potential oscillations in DRG neurons: relation to neuropathic pain. J Neurophysiol 2000, 84:205-215.
41. Liu CN, Wall PD, Ben-Dor E, Michaelis M, Amir R, Devor M. Tactile allodynia in the absence of C-fiber activation: altered firing properties of DRG neurons following spinal nerve injury. Pain 2000, 85:503-521. 10.1016/S0304-3959(00)00251-7, 10781925.
42. Tal M, Wall PD, Devor M. Myelinated afferent fiber types that become spontaneously active and mechanosensitive following nerve transection in the rat. Brain Res 1999, 824:218-223. 10.1016/S0006-8993(99)01190-7, 10196451.
43. Devor M. Ectopic discharge in Abeta afferents as a source of neuropathic pain. Exp Brain Res 2009, 196:115-128. 10.1007/s00221-009-1724-6, 19242687.