Visceral hyperalgesia induced by forebrain-specific suppression of native Kv7/KCNQ/M-current in mice

Molecular Pain

Volumn 7, Issue , 2011, Pages

  Bi, Yeping ^a   Chen, Hui ^a   Su, Jun ^a   Cao, Xu ^a   Bian, Xiling ^a   Wang, KeWei ^a,b  

^a PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^b PEKING UNIVERSITY   (China)

Author keywords

Acetic acid; C fos; Capsaicin; Forebrain; Retigabine; Somatosensory cortex; Xe 991

Indexed keywords

10,10 BIS(4 PYRIDINYLMETHYL) 9(10H) ANTHRACENONE; ACETIC ACID; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CAPSAICIN; MAGNESIUM SULFATE; POTASSIUM CHANNEL KCNQ2; PROTEIN C FOS; RETIGABINE; 10,10-BIS(4-PYRIDINYLMETHYL)-9(10H)-ANTHRACENONE; ANTHRACENE DERIVATIVE; CARBAMIC ACID DERIVATIVE; PHENYLENEDIAMINE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINOCICEPTION; ARTICLE; CONTROLLED STUDY; FEMALE; FOREBRAIN; HIPPOCAMPAL CA1 REGION; HYPERALGESIA; IMMUNOHISTOLOGY; INSULA; LATERAL BRAIN VENTRICLE; MOUSE; NERVE CELL EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; SECONDARY SOMATOSENSORY CORTEX; TRANSGENIC MOUSE; VISCERAL PAIN; WRITHING TEST; ANIMAL; CHEMICALLY INDUCED DISORDER; DRUG ANTAGONISM; DRUG EFFECT; GENETICS; METABOLISM; SOMATOSENSORY CORTEX;

ANIMALS; ANTHRACENES; CAPSAICIN; CARBAMATES; HYPERALGESIA; KCNQ2 POTASSIUM CHANNEL; MAGNESIUM SULFATE; MICE; MICE, TRANSGENIC; PHENYLENEDIAMINES; PROSENCEPHALON; PROTO-ONCOGENE PROTEINS C-FOS; SOMATOSENSORY CORTEX; VISCERAL PAIN;

EID: 81255175511     PISSN: None     EISSN: 17448069     Source Type: Journal    
DOI: 10.1186/1744-8069-7-84     Document Type: Article

References (52)

1. Anand P, Aziz Q, Willert R, van Oudenhove L. Peripheral and central mechanisms of visceral sensitization in man. Neurogastroenterol Motil 2007, 19:29-46. 10.1111/j.1365-2982.2006.00873.x, 17280584.
2. Woolf CJ. Central sensitization: implications for the diagnosis and treatment of pain. Pain 2011, 152:S2-15. 10.1016/j.pain.2010.09.030, 20961685.
3. 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.
4. Mayer EA, Tillisch K. The brain-gut axis in abdominal pain syndromes. Annu Rev Med 2011, 62:381-396. 10.1146/annurev-med-012309-103958, 21090962.
5. Moisset X, Bouhassira D, Denis D, Dominique G, Benoit C, Sabate JM. Anatomical connections between brain areas activated during rectal distension in healthy volunteers: a visceral pain network. Eur J Pain 2010, 14:142-148. 10.1016/j.ejpain.2009.04.011, 19473859.
6. Derbyshire SW. A systematic review of neuroimaging data during visceral stimulation. Am J Gastroenterol 2003, 98:12-20. 10.1111/j.1572-0241.2003.07168.x, 12526930.
7. Strigo IA, Duncan GH, Boivin M, Bushnell MC. Differentiation of visceral and cutaneous pain in the human brain. J Neurophysiol 2003, 89:3294-3303. 10.1152/jn.01048.2002, 12611986.
8. Wang Z, Guo Y, Bradesi S, Labus JS, Maarek JM, Lee K, Winchester WJ, Mayer EA, Holschneider DP. Sex differences in functional brain activation during noxious visceral stimulation in rats. Pain 2009, 145:120-128. 10.1016/j.pain.2009.05.025, 2756542, 19560270.
9. Zhuo M. Molecular mechanisms of pain in the anterior cingulate cortex. J Neurosci Res 2006, 84:927-933. 10.1002/jnr.21003, 16862566.
10. Wei F, Wang GD, Kerchner GA, Kim SJ, Xu HM, Chen ZF, Zhuo M. Genetic enhancement of inflammatory pain by forebrain NR2B overexpression. Nat Neurosci 2001, 4:164-169. 10.1038/83993, 11175877.
11. Stepanovic-Petrovic RM, Tomic MA, Vuckovic SM, Paranos S, Ugresic ND, Prostran MS, Milovanovic S, Boskovic B. The antinociceptive effects of anticonvulsants in a mouse visceral pain model. Anesth Analg 2008, 106:1897-1903. 10.1213/ane.0b013e318172b993, 18499629.
12. Hirano K, Kuratani K, Fujiyoshi M, Tashiro N, Hayashi E, Kinoshita M. Kv7.2-7.5 voltage-gated potassium channel (KCNQ2-5) opener, retigabine, reduces capsaicin-induced visceral pain in mice. Neurosci Lett 2007, 413:159-162. 10.1016/j.neulet.2006.11.043, 17184917.
13. Lang PM, Fleckenstein J, Passmore GM, Brown DA, Grafe P. Retigabine reduces the excitability of unmyelinated peripheral human axons. Neuropharmacology 2008, 54:1271-1278. 10.1016/j.neuropharm.2008.04.006, 18474382.
14. Roza C, Lopez-Garcia JA. Retigabine, the specific KCNQ channel opener, blocks ectopic discharges in axotomized sensory fibres. Pain 2008, 138:537-545. 10.1016/j.pain.2008.01.031, 18331780.
15. Cooper EC, Jan LY. M-channels: neurological diseases, neuromodulation, and drug development. Arch Neurol 2003, 60:496-500. 10.1001/archneur.60.4.496, 12707061.
16. Brown BS, Yu SP. Modulation and genetic identification of the M channe. Progress in Biophysics & Molecular Biology 2000, 73:135-166. 10.1016/S0079-6107(00)00004-3, 22020120.
17. Armand V, Rundfeldt C, Heinemann U. Effects of retigabine (D-23129) on different patterns of epileptiform activity induced by low magnesium in rat entorhinal cortex hippocampal slices. Epilepsia 2000, 41:28-33.
18. Blackburn-Munro G, Jensen BS. The anticonvulsant retigabine attenuates nociceptive behaviours in rat models of persistent and neuropathic pain. Euro J Pharmacol 2003, 460:109-116.
19. Passmore GM, Selyanko AA, Mistry M, Al-Qatari M, Marsh SJ, Matthews EA, Dickenson AH, Brown TA, Burbidge SA, Main M, Brown DA. KCNQ/M currents in sensory neurons: significance for pain therapy. J Neurosci 2003, 23:7227-7236.
20. Dost R, Rostock A, Rundfeldt C. The anti-hyperalgesic activity of retigabine is mediated by KCNQ potassium channel activation. Naunyn Schmiedebergs Arch Pharmacol 2004, 369:382-390. 10.1007/s00210-004-0881-1, 15007538.
21. Nielsen AN, Mathiesen C, Blackburn-Munro G. Pharmacological characterisation of acid-induced muscle allodynia in rats. Eur J Pharmacol 2004, 487:93-103. 10.1016/j.ejphar.2004.01.017, 15033380.
22. Peters HC, Hu H, Pongs O, Storm JF, Isbrandt D. Conditional transgenic suppression of M channels in mouse brain reveals functions in neuronal excitability, resonance and behavior. Nat Neurosci 2005, 8:51-60. 10.1038/nn1375, 15608631.
23. Kim D, Park D, Choi S, Lee S, Sun M, Kim C, Shin HS. Thalamic control of visceral nociception mediated by T-type Ca2+ channels. Science 2003, 302:117-119. 10.1126/science.1088886, 14526084.
24. Ringel Y. New directions in brain imaging research in functional gastrointestinal disorders. Dig Dis 2006, 24:278-285. 10.1159/000092881, 16849855.
25. Wang H, Shimizu E, Tang YP, Cho M, Kyin M, Zuo W, Robinson DA, Alaimo PJ, Zhang C, Morimoto H, et al. Inducible protein knockout reveals temporal requirement of CaMKII reactivation for memory consolidation in the brain. Proc Natl Acad Sci USA 2003, 100:4287-4292. 10.1073/pnas.0636870100, 153085, 12646704.
26. Cui Z, Wang H, Tan Y, Zaia KA, Zhang S, Tsien JZ. Inducible and reversible NR1 knockout reveals crucial role of the NMDA receptor in preserving remote memories in the brain. Neuron 2004, 41:781-793. 10.1016/S0896-6273(04)00072-8, 15003177.
27. Tsien JZ, Chen DF, Gerber D, Tom C, Mercer EH, Anderson DJ, Mayford M, Kandel ER, Tonegawa S. Subregion- and cell type-restricted gene knockout in mouse brain. Cell 1996, 87:1317-1326. 10.1016/S0092-8674(00)81826-7, 8980237.
28. Tang YP, Shimizu E, Dube GR, Rampon C, Kerchner GA, Zhuo M, Liu G, Tsien JZ. Genetic enhancement of learning and memory in mice. Nature 1999, 401:63-69. 10.1038/43432, 10485705.
29. Charlier C, Singh NA, Ryan SG, Lewis TB, Reus BE, Leach RJ, Leppert M. A pore mutation in a novel KQT-like potassium channel gene in an idiopathic epilepsy family [see comments]. Nature Genetics 1998, 18:53-55. 10.1038/ng0198-53, 9425900.
30. Biervert C, Schroeder BC, Kubisch C, Berkovic SF, Propping P, Jentsch TJ, Steinlein OK. A potassium channel mutation in neonatal human epilepsy. Science 1998, 279:403-406. 10.1126/science.279.5349.403, 9430594.
31. Wang HS, Pan Z, Shi W, Brown BS, Wymore RS, Cohen IS, Dixon JE, McKinnon D. KCNQ2 and KCNQ3 potassium channel subunits: molecular correlates of the M-channel. Science 1998, 282:1890-1893.
32. Ouimet CC, McGuinness TL, Greengard P. Immunocytochemical localization of calcium/calmodulin-dependent protein kinase II in rat brain. Proc Natl Acad Sci USA 1984, 81:5604-5608. 10.1073/pnas.81.17.5604, 391755, 6591208.
33. Erondu NE, Kennedy MB. Regional distribution of type II Ca2+/calmodulin-dependent protein kinase in rat brain. J Neurosci 1985, 5:3270-3277.
34. Burgin KE, Waxham MN, Rickling S, Westgate SA, Mobley WC, Kelly PT. In situ hybridization histochemistry of Ca2+/calmodulin-dependent protein kinase in developing rat brain. J Neurosci 1990, 10:1788-1798.
35. Cooper EC, Harrington E, Jan YN, Jan LY. M channel KCNQ2 subunits are localized to key sites for control of neuronal network oscillations and synchronization in mouse brain. J Neurosci 2001, 21:9529-9540.
36. Schnitzler A, Volkmann J, Enck P, Frieling T, Witte OW, Freund HJ. Different cortical organization of visceral and somatic sensation in humans. Eur J Neurosci 1999, 11:305-315. 10.1046/j.1460-9568.1999.00429.x, 9987033.
37. Lotze M, Wietek B, Birbaumer N, Ehrhardt J, Grodd W, Enck P. Cerebral activation during anal and rectal stimulation. Neuroimage 2001, 14:1027-1034. 10.1006/nimg.2001.0901, 11697934.
38. Aziz Q, Thompson DG, Ng VW, Hamdy S, Sarkar S, Brammer MJ, Bullmore ET, Hobson A, Tracey I, Gregory L, et al. Cortical processing of human somatic and visceral sensation. J Neurosci 2000, 20:2657-2663.
39. Ladabaum U, Roberts TP, McGonigle DJ. Gastric fundic distension activates fronto-limbic structures but not primary somatosensory cortex: a functional magnetic resonance imaging study. Neuroimage 2007, 34:724-732. 10.1016/j.neuroimage.2006.07.033, 17110130.
40. Hobday DI, Aziz Q, Thacker N, Hollander I, Jackson A, Thompson DG. A study of the cortical processing of ano-rectal sensation using functional MRI. Brain 2001, 124:361-368. 10.1093/brain/124.2.361, 11157563.
41. Xu CM, Wang J, Wu P, Zhu WL, Li QQ, Xue YX, Zhai HF, Shi J, Lu L. Glycogen synthase kinase 3beta in the nucleus accumbens core mediates cocaine-induced behavioral sensitization. J Neurochem 2009, 111:1357-1368. 10.1111/j.1471-4159.2009.06414.x, 19799712.
42. Laird JM, Martinez-Caro L, Garcia-Nicas E, Cervero F. A new model of visceral pain and referred hyperalgesia in the mouse. Pain 2001, 92:335-342. 10.1016/S0304-3959(01)00275-5, 11376906.
43. Mogil JS, Breese NM, Witty MF, Ritchie J, Rainville ML, Ase A, Abbadi N, Stucky CL, Seguela P. Transgenic expression of a dominant-negative ASIC3 subunit leads to increased sensitivity to mechanical and inflammatory stimuli. J Neurosci 2005, 25:9893-9901. 10.1523/JNEUROSCI.2019-05.2005, 16251436.
44. Mogil JS, Wilson SG, Bon K, Lee SE, Chung K, Raber P, Pieper JO, Hain HS, Belknap JK, Hubert L, et al. Heritability of nociception I: responses of 11 inbred mouse strains on 12 measures of nociception. Pain 1999, 80:67-82. 10.1016/S0304-3959(98)00197-3, 10204719.
45. Wilson SG, Mogil JS. Measuring pain in the (knockout) mouse: big challenges in a small mammal. Behav Brain Res 2001, 125:65-73. 10.1016/S0166-4328(01)00281-9, 11682095.
46. Bannon AW, Malmberg AB. Models of nociception: hot-plate, tail-flick, and formalin tests in rodents. Curr Protoc Neurosci 2007, Chapter 8. Unit 8 9.
47. Haley TJ, McCormick WG. Pharmacological effects produced by intracerebral injection of drugs in the conscious mouse. Br J Pharmacol Chemother 1957, 12:12-15. 1509635, 13413144.
48. Xu W, Wu Y, Bi Y, Tan L, Gan Y, Wang K. Activation of voltage-gated KCNQ/Kv7 channels by anticonvulsant retigabine attenuates mechanical allodynia of inflammatory temporomandibular joint in rats. Mol Pain 2010, 6:49. 10.1186/1744-8069-6-49, 2936374, 20796319.
49. Hefner K, Whittle N, Juhasz J, Norcross M, Karlsson RM, Saksida LM, Bussey TJ, Singewald N, Holmes A. Impaired fear extinction learning and cortico-amygdala circuit abnormalities in a common genetic mouse strain. Journal of Neuroscience 2008, 28:8074-8085. 10.1523/JNEUROSCI.4904-07.2008, 2547848, 18685032.
50. Chen ZS, Gu J. Immunoglobulin G expression in carcinomas and cancer cell lines. Faseb Journal 2007, 21:2931-2938. 10.1096/fj.07-8073com, 17475920.
51. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408. 10.1006/meth.2001.1262, 11846609.
52. Paxinos G, Franklin KBJ. The mouse brain in stereotaxic coordinates 2001, San Diego: Academic Press, 2.