Somatostatin receptor subtype 4 couples to the M-current to regulate seizures

Journal of Neuroscience

Volumn 28, Issue 14, 2008, Pages 3567-3576

  Qiu, Cuie ^a   Zeyda, Thomas ^b   Johnson, Brian ^a   Hochgeschwender, Ute ^c   De Lecea, Luis ^d   Tallent, Melanie K ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF HAWAII   (United States)

^c OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

^d STANFORD UNIVERSITY   (United States)

Author keywords

Electrophysiology; Epilepsy; KCNQ; Knock out mice; Kv7 channels; Somatostatin

Indexed keywords

LIGAND; RECEPTOR SUBTYPE; SOMATOSTATIN RECEPTOR 2; SOMATOSTATIN RECEPTOR 3; SOMATOSTATIN RECEPTOR 4; KAINIC ACID; MEMBRANE PROTEIN; PENTETRAZOLE; POTASSIUM; POTASSIUM CHANNEL; POTASSIUM CHANNEL BLOCKING AGENT; SOMATOSTATIN RECEPTOR; SOMATOSTATIN RECEPTOR SUBTYPE 4; SOMATOSTATIN RECEPTOR SUBTYPE-4;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; DISEASE SEVERITY; ELECTROPHYSIOLOGY; EPILEPTOGENESIS; FEMALE; HIPPOCAMPUS; KNOCKOUT MOUSE; LATENT PERIOD; MALE; MOUSE; NONHUMAN; POTASSIUM CURRENT; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RECEPTOR GENE; SEIZURE; SST2 GENE; SST3 GENE; SST4 GENE; WILD TYPE; ANALYSIS OF VARIANCE; ANIMAL; CELL MEMBRANE POTENTIAL; CHEMICALLY INDUCED DISORDER; CLASSIFICATION; CYTOLOGY; DISEASE MODEL; DRUG EFFECT; ELECTROSTIMULATION; GENETICS; IN VITRO STUDY; METHODOLOGY; MOUSE MUTANT; MUTATION; NERVE CELL; PATCH CLAMP; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; RADIATION EXPOSURE; RADIATION RESPONSE; RAT; REACTION TIME;

ANALYSIS OF VARIANCE; ANIMALS; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, RADIATION; ELECTRIC STIMULATION; HIPPOCAMPUS; KAINIC ACID; MEMBRANE POTENTIALS; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MUTATION; NEURONS; PATCH-CLAMP TECHNIQUES; PENTYLENETETRAZOLE; POTASSIUM; POTASSIUM CHANNEL BLOCKERS; POTASSIUM CHANNELS; RATS; REACTION TIME; RECEPTORS, SOMATOSTATIN; SEIZURES;

EID: 43649097985     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4679-07.2008     Document Type: Article

References (59)

1. Allen JP, Hathway GJ, Clarke NJ, Jowett MI, Topps S, Kendrick KM, Humphrey PPA, Wilkinson LS, Emson PC (2003) Somatostatin receptor 2 knock-out/LacZ knockin mice show impaired motor coordination and reveal sites of somatostatin action within the striatum. Eur J Neurosci 17:1881-1895.
2. Armand V, Rundfeldt C, Heinemann U (1999) Effects of retigabine (D-23129) on different patterns of epileptiform activity induced by 4-aminopyridine in rat entorhinal cortex hippocampal slices. Naunyn Schmiedebergs Arch Pharmacol 359:33-39.
3. Armand V, Rundfeldt C, Heinemann U (2000) Effects of retigabine (D-23129) on different patterns of epileptiform activity induced by low magnesium in rat entorhinal cortex hippocampal slices. Epilepsia 41:28-33.
4. 2+ signaling in mouse dentate gyrus. J Neurophysiol 88:3078-3086.
5. Biervert C, Schroeder BC, Kubisch C, Berkovic SF, Propping P, Jentsch TJ, Steinlein OK (1998) A potassium channel mutation in neonatal human epilepsy. Science 279:403-406.
6. Boehm S, Betz H (1997) Somatostatin inhibits excitatory transmission at rat hippocampal synapses via presynaptic receptors. J Neurosci 17:4066-4075.
7. Brevard ME, Kulkarni P, King JA, Ferris CF (2006) Imaging the neural substrates involved in the genesis of pentylenetetrazol-induced seizures. Epilepsia 47:745-754.
8. Cammalleri M, Cervia D, Langenegger D, Liu Y, Monte MD, Hoyer D, Bagnoli P (2004) Somatostatin receptors differentially affect spontaneous epileptiform activity in mouse hippocampal slices. Eur J Neurosci 20:2711-2721.
9. Charlier C, Singh NA, Ryan SG, Lewis TB, Reus BE, Leach RJ, Leppert M (1998) A pore mutation in a novel KQT-like potassium channel gene in an idiopathic epilepsy family. Nat Genet 18:53-55.
10. Cooper EC, Aldape KD, Abosch A, Barbaro NM, Berger MS, Peacock WS, Jan YN, Jan LY (2000) Colocalization and coassembly of two human brain M-type potassium channel subunits that are mutated in epilepsy. Proc Natl Acad Sci USA 97:4914-4919.
11. Delmas P, Brown DA (2005) Pathways modulating neural KCNQ/M (Kv7) potassium channels. Nat Rev Neurosci 6:850-862.
12. Dost R, Rundfeldt C (2000) The anticonvulsant retigabine potently suppresses epileptiform discharges in the low Ca++ and low Mg++ model in the hippocampal slice preparation. Epilepsy Res 38:53-66.
13. 2A in rat brain using a specific anti-peptide antibody. J Neurosci 16:4468-4478.
14. Dutar P, Vaillend C, Viollet C, Billard JM, Potier B, Carlo AS, Ungerer A, Epelbaum J (2002) Spatial learning and synaptic hippocampal plasticity in type 2 somatostatin receptor knock-out mice. Neuroscience 112:455-466.
15. Engstrom M, Savola JM, Wurster S (2006) Differential efficacies of somatostatin receptor agonists for G-protein activation and desensitization of somatostatin receptor subtype 4-mediated responses. J Pharmacol Exp Ther 316:1262-1268.
16. Freund TF, Buzsaki G (1996) Interneurons of the hippocampus. Hippocampus 6:347-470.
17. Fuchs JL, Schwark HD (2004) Neuronal primary cilia: a review. Cell Biol Int 28:111-118.
18. Handel M, Schulz S, Stanarius A, Schreff M, Erdtmann-Vourliotis M, Schmidt H, Wolf G, Hollt V (1999) Selective targeting of somatostatin receptor 3 to neuronal cilia. Neuroscience 89:909-926.
19. Hervieu G, Emson PC (1998) The localization of somatostatin receptor 1 (sst1) immunoreactivity in the rat brain using an N-terminal specific antibody. Neuroscience 85:1263-1284.
20. Hicks GA, Feniuk W, Humphrey PP (1998) Outward current produced by somatostatin (SRIF) in rat anterior cingulate pyramidal cells in vitro. Br J Pharmacol 124:252-258.
21. Hoyer D, Perez J, Schoeffter P, Langenegger D, Schuepbach E, Kaupmann K, Luebbert H, Bruns C, Reubi JC (1995) Pharmacological identity between somatostatin SS-2 binding sites and SSTR-1 receptors. Eur J Pharmacol Mol Pharmacol 289:151-161.
22. Li E, Bestor TH, Jaenisch R (1992) Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69:915-926.
23. Mazarati AM, Telegdy G (1992) Effects of somatostatin and anti-somatostatin serum on picrotoxin-kindled seizures. Neuropharmacology 31:793-797.
24. Meis S, Sosulina L, Schulz S, Hollt V, Pape HC (2005) Mechanisms of somatostatin-evoked responses in neurons of the rat lateral amygdala. Eur J Neurosci 21:755-762.
25. Moneta D, Richichi C, Aliprandi M, Dournaud P, Dutar P, Billard JM, Carlo AS, Viollet C, Hannon JP, Fehlmann D, Nunn C, Hoyer D, Epelbaum J, Vezzani A (2002) Somatostatin receptor subtypes 2 and 4 affect seizure susceptibility and hippocampal excitatory neurotransmission in mice. Eur J Neurosci 16:843-849.
26. Moore SD, Madamba SG, Joels M, Siggins GR (1988) Somatostatin augments the M-current in hippocampal neurons. Science 239:278-280.
27. Moore SD, Madamba SG, Schweitzer P, Siggins GR (1994) Voltage-dependent effects of opioid peptides on hippocampal CA3 pyramidal neurons in vitro. J Neurosci 14:809-820.
28. Otto JF, Yang Y, Frankel WN, White HS, Wilcox KS (2006) A spontaneous mutation involving Kcnq2 (Kv7.2) reduces M-current density and spike frequency adaptation in mouse CA1 neurons. J Neurosci 26:2053-2059.
29. Perez J, Vezzani A, Civenni G, Tutka P, Rizzi M, Schuepbach E, Hoyer D (1995) Functional effects of D-Phe-c[Cys-Tyr-D-Trp-Lys-Val-Cys]-Trp-NH2 and differential changes in somatostatin receptor messenger RNAs, binding sites and somatostatin release in kainic acid-treated rats. Neuroscience 65:1087-1097.
30. Porter RJ, Nohria V, Rundfeldt C (2007a) Retigabine. Neurotherapeutics 4:149-154.
31. Porter RJ, Partiot A, Sachdeo R, Nohria V, Alves WM (2007b) Randomized, multicenter, dose-ranging trial of retigabine for partial-onset seizures. Neurology 68:1197-1204.
32. Qiu C, Johnson BN, Tallent MK (2007) K(+) M-current regulates the transition to seizures in immature and adult hippocampus. Epilepsia 48:2047-2058.
33. Racine RJ (1972) Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 32:281-294.
34. Ramirez JL, Mouchantaf R, Kumar U, Otero Corchon V, Rubinstein M, Low MJ, Patel YC (2002) Brain somatostatin receptors are up-regulated in somatostatin-deficient mice. Mol Endocrinol 16:1951-1963.
35. Rohrer SP, Birzin ET, Mosley RT, Berk SC, Hutchins SM, Shen DM, Xiong Y, Hayes EC, Parmar RM, Foor F, Mitra SW, Degrado SJ, Shu M, Klopp JM, Cai SJ, Blake A, Chan WW, Pasternak A, Yang L, Patchett AA, et al. (1998) Rapid identification of subtype-selective agonists of the somatostatin receptor through combinatorial chemistry. Science 282:737-740.
36. Sarkisian MR (2001) Overview of the current animal models for human seizure and epileptic disorders. Epilepsy Behav 2:201-216.
37. Schoeffter P, Perez J, Langenegger D, Schuepbach E, Bobirnac I, Luebbert H, Bruns C, Hoyer D (1995) Characterization and distribution of somatostatin SS-1 and SRIF-1 binding sites in rat brain: Identity with SSTR-2 receptors. Eur J Pharmacol Mol Pharmacol 289:163-173.
38. Schreff M, Schulz S, Handel M, Keilhoff G, Braun H, Pereira G, Klutzny M, Schmidt H, Wolf G, Hollt V (2000) Distribution, targeting, and internalization of the sst4 somatostatin receptor in rat brain. J Neurosci 20:3785-3797.
39. Schulz S, Handel M, Schreff M, Schmidt H, Hollt V (2000) Localization of five somatostatin receptors in the rat central nervous system using subtype-specific antibodies. J Physiol Paris 94:259-264.
40. Schwabe W, Brennan MB, Hochgeschwender U (1996) Isolation and characterization of the mouse (Mus musculus) somatostatin receptor type-4-encoding gene (mSSTR4). Gene 168:233-235.
41. Schweitzer P, Madamba S, Siggins GR (1990) Arachidonic acid metabolites as mediators of somatostatin-induced increase of neuronal M-current. Nature 346:464-467.
42. Schweitzer P, Madamba S, Champagnat J, Siggins GR (1993) Somatostatin inhibition of hippocampal CA1 pyramidal neurons: mediation by arachidonic acid and its metabolites. J Neurosci 13:2033-2049.
43. Schweitzer P, Madamba SG, Siggins GR (1998) Somatostatin increases a voltage-insensitive K+ conductance in rat CA1 hippocampal neurons. J Neurophysiol 79:1230-1238.
44. Sharifi N, Diehl N, Yaswen L, Brennan MB, Hochgeschwender U (2001) Generation of dynorphin knock-out mice. Brain Res Mol Brain Res 86:70-75.
45. Silva AJ, Simpson EM, Takahashi JS, Lipp H, Nakanishi S, Wehner JM, Giese KP, Tully T, Abel T, Chapman PF, Fox K, Grant S, Itohara S, Lathe R, Mayford M, McNamara JO, Morris RJ, Picciotto M, Roder M, Shin H, et al. (1997) Mutant mice and neuroscience: recommendations concerning genetic background. Banbury Conference on genetic background in mice. Neuron 19:755-759.
46. Singh NA, Charlier C, Stauffer D, DuPont BR, Leach RJ, Melis R, Ronen GM, Bjerre I, Quattlebaum T, Murphy JV, McHarg ML, Gagnon D, Rosales TO, Peiffer A, Anderson VE, Leppert M (1998) A novel potassium channel gene, KCNQ2, is mutated in an inherited epilepsy of newborns. Nat Genet 18:25-29.
47. Singh NA, Westenskow P, Charlier C, Pappas C, Leslie J, Dillon J, Anderson VE, Sanguinetti MC, Leppert MF (2003) KCNQ2 and KCNQ3 potassium channel genes in benign familial neonatal convulsions: expansion of the functional and mutation spectrum. Brain 126:2726-2737.
48. Starzl TE, Niemer WT, Dell M, Forgrave PR (1953) Cortical and subcortical electrical activity in experimental seizures induced by metrazol. J Neuropathol Exp Neurol 12:262-276.
49. Suh BC, Hille B (2007) Regulation of KCNQ channels by manipulation of phosphoinositides. J Physiol 582:911-916.
50. Tallent MK, Siggins GR (1997) Somatostatin depresses excitatory but not inhibitory neurotransmission in rat CA1 hippocampus. J Neurophysiol 78:3008-3018.
51. Tallent MK, Madamba SG, Siggins GR (2001) Nociceptin reduces epileptiform events in CA3 hippocampus via presynaptic and postsynaptic mechanisms. J Neurosci 21:6940-6948.
52. Traub RD, Wong RK (1983) Synchronized burst discharge in disinhibited hippocampal slice. II. Model of cellular mechanism. J Neurophysiol 49:459-471.
53. Traub RD, Miles R, Jefferys JG (1993) Synaptic and intrinsic conductances shape picrotoxin-induced synchronized after-discharges in the guinea-pig hippocampal slice. J Physiol (Lond) 461:525-547.
54. Vezzani A, Hoyer D (1999) Brain somatostatin: a candidate inhibitory role in seizures and epileptogenesis. Eur J Neurosci 11:3767-3776.
55. Vezzani A, Serafini R, Stasi MA, Vigano G, Rizzi M, Samanin R (1991) A peptidase-resistant cyclic octapeptide analogue of somatostatin (SMS 201-995) modulates seizures induced by quinolic acid and kainic acid differently in the rat hippocampus. Neuropharmacology 30:345-352.
56. Videau C, Hochgeschwender U, Kreienkamp HJ, Brennan MB, Viollet C, Richter D, Epelbaum J (2003) Characterisation of [125I]-Tyr0DTrp8-somatostatin binding in sst1- to sst4- and SRIF-gene-invalidated mouse brain. Naunyn Schmiedebergs Arch Pharmacol 367:562-571.
57. Viollet C, Vaillend C, Videau C, Bluet-Pajot MT, Ungerer A, L'Heritier A, Kopp C, Potier B, Billard J, Schaeffer J, Smith RG, Rohrer SP, Wilkinson H, Zheng H, Epelbaum J (2000) Involvement of sst2 somatostatin receptor in locomotor, exploratory activity and emotional reactivity in mice. Eur J Neurosci 12:3761-3770.
58. Whitfield JF (2004) The neuronal primary cilium - an extrasynaptic signaling device. Cell Signal 16:763-767.
59. Zeyda T, Diehl N, Paylor R, Brennan MB, Hochgeschwender U (2001) Impairment in motor learning of somatostatin null mutant mice. Brain Res 906:107-114.