Functional characterization of ether-à-go-go-related gene potassium channels in midbrain dopamine neurons - implications for a role in depolarization block

European Journal of Neuroscience

Volumn 36, Issue 7, 2012, Pages 2906-2916

  Ji, Huifang ^a   Tucker, Kristal R ^b   Putzier, Ilva ^b   Huertas, Marco A ^c   Horn, John P ^b   Canavier, Carmen C ^c   Levitan, Edwin S ^b   Shepard, Paul D ^a  

^a MARYLAND PSYCHIATRIC RESEARCH CENTER   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

Antipsychotic drugs; Bursting; HERG; KV11; KCNH2

Indexed keywords

1 [2 (6 METHYL 2 PYRIDYL)ETHYL] 4 (4 METHYLSULFONYLAMINOBENZOYL)PIPERIDINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; POTASSIUM CHANNEL BLOCKING AGENT; POTASSIUM CHANNEL HERG; RBEKM 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CELLULAR DISTRIBUTION; CHANNEL GATING; COMPUTER ANALYSIS; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DRUG TARGETING; FREQUENCY MODULATION; IN VITRO STUDY; IN VIVO STUDY; MALE; MESENCEPHALON; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE STEADY POTENTIAL; NEUROMODULATION; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; SPIKE WAVE; SYNAPTIC TRANSMISSION;

ANIMALS; DOPAMINERGIC NEURONS; ETHER-A-GO-GO POTASSIUM CHANNELS; MALE; MEMBRANE POTENTIALS; MESENCEPHALON; PIPERIDINES; POTASSIUM CHANNEL BLOCKERS; PYRIDINES; RATS; RATS, SPRAGUE-DAWLEY; SCORPION VENOMS;

EID: 84866984063     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2012.08190.x     Document Type: Article

References (68)

1. Apud, J.A., Zhang, F., Decot, H., Bigos, K.L. & Weinberger, D.R. (2011) Genetic variation in KCNH2 associated with expression in brain of a unique hERG isoform modulates antipsychotic response in patients with schizophrenia. Society for Neuroscience Meeting. Society for Neuroscience, Washington, DC, pp. CC14.
2. Bradaia, A., Trube, G., Stalder, H., Norcross, R.D., Ozmen, L., Wettstein, J.G., Pinard, A., Buchy, D., Gassmann, M., Hoener, M.C. & Bettler, B. (2009) The selective antagonist EPPTB reveals TAAR1-mediated regulatory mechanisms in dopaminergic neurons of the mesolimbic system. Proc. Natl Acad. Sci. USA, 106, 20081-20086.
3. Bunney, B.S., Walters, J.R., Roth, R.H. & Aghajanian, G.K. (1973) Dopaminergic neurons: effect of antipsychotic drugs and amphetamine on single cell activity. J. Pharmacol. Exp. Ther., 185, 560-571.
4. Canavier, C.C., Oprisan, S., Callaway, J., Ji, H. & Shepard, P.D. (2007) Computational model predicts a role for ERG current in repolarizing plateau potentials in dopamine neurons: implications for modulation of neuronal activity. J. Neurophysiol., 98, 3006-3022.
5. + channels: spike-frequency adaptation. J. Physiol., 501 (Pt 2), 313-318.
6. Deister, C.A., Teagarden, M.A., Wilson, C.J. & Paladini, C.A. (2009) An intrinsic neuronal oscillator underlies dopaminergic neuron bursting. J. Neurosci., 29, 15888-15897.
7. Ding, S., Matta, S.G. & Zhou, F.M. (2011a) Kv3-like potassium channels are required for sustained high-frequency firing in basal ganglia output neurons. J. Neurophysiol., 105, 554-570.
8. Ding, S., Wei, W. & Zhou, F.M. (2011b) Molecular and functional differences in voltage-activated sodium currents between GABA projection neurons and dopamine neurons in the substantia nigra. J. Neurophysiol., 106, 3019-3034.
9. Drion, G., Bonjean, M., Waroux, O., Scuvee-Moreau, J., Liegeois, J.F., Sejnowski, T.J., Sepulchre, R. & Seutin, V. (2010) M-type channels selectively control bursting in rat dopaminergic neurons. Eur. J. Neurosci., 31, 827-835.
10. Durante, P., Cardenas, C.G., Whittaker, J.A., Kitai, S.T. & Scroggs, R.S. (2004) Low-threshold L-type calcium channels in rat dopamine neurons. J. Neurophysiol., 91, 1450-1454.
11. Ekins, S., Crumb, W.J., Sarazan, R.D., Wikel, J.H. & Wrighton, S.A. (2002) Three-dimensional quantitative structure-activity relationship for inhibition of human ether-a-go-go-related gene potassium channel. J. Pharmacol. Exp. Ther., 301, 427-434.
12. Fernandez, F.R. & White, J.A. (2010) Gain control in CA1 pyramidal cells using changes in somatic conductance. J. Neurosci., 30, 230-241.
13. Ferreira, N.R., Mitkovski, M., Stuhmer, W., Pardo, L.A. & Del Bel, E.A. (2012) Ether-a-go-go 1 (Eag1) potassium channel expression in dopaminergic neurons of basal ganglia is modulated by 6-hydroxydopamine lesion. Neurotox. Res., 21, 317-333.
14. + channels. Circ. Res., 82, 386-395.
15. Fujimura, K. & Matsuda, Y. (1989) Autogenous oscillatory potentials in neurons of the guinea pig substantia nigra pars compacta in vitro. Neurosc. Lett., 104, 53-57.
16. Grace, A.A. & Bunney, B.S. (1983) Intracellular and extracellular electrophysiology of nigral dopaminergic neurons-1. Identification and characterization. Neuroscience, 10, 301-315.
17. Grace, A.A. & Bunney, B.S. (1984a) The control of firing pattern in nigral dopamine neurons: burst firing. J. Neurosci., 4, 2877-2890.
18. Grace, A.A. & Bunney, B.S. (1984b) The control of firing pattern in nigral dopamine neurons: single spike firing. J. Neurosci., 4, 2866-2876.
19. Grace, A.A. & Bunney, B.S. (1986) Induction of depolarization block in midbrain dopamine neuron by repeated administration of haloperidol: analysis using in vivo intracellular recording. J. Pharmacol. Exp. Ther., 238, 1092-1100.
20. + channels contribute to threshold excitability of mouse auditory brainstem neurons. J. Physiol., 587, 2487-2497.
21. Harris, N.C., C. Webb & Greenfield, S.A. (1989) A possible pacemaker mechanism in pars compacta neurons of the guinea-pig substantia nigra revealed by various ion channel blocking agents. Neuroscience, 31, 355-362.
22. Herzberg, I.M., Trudeau, M.C. & Robertson, G.A. (1998) Transfer of rapid inactivation and sensitivity to the class III antiarrhythmic drug E-4031 from HERG to M-eag channels. J. Physiol., 511 (Pt 1), 3-14.
23. Hines, M.L. & Carnevale, N.T. (1997) The NEURON simulation environment. Neural Comput., 9, 1179-1209.
24. Huffaker, S.J., Chen, J., Nicodemus, K.K., Sambataro, F., Yang, F., Mattay, V., Lipska, B.K., Hyde, T.M., Song, J., Rujescu, D., Giegling, I., Mayilyan, K., Proust, M.J., Soghoyan, A., Caforio, G., Callicott, J.H., Bertolino, A., Meyer-Lindenberg, A., Chang, J., Ji, Y., Egan, M.F., Goldberg, T.E., Kleinman, J.E., Lu, B. & Weinberger, D.R. (2009) A primate-specific, brain isoform of KCNH2 affects cortical physiology, cognition, neuronal repolarization and risk of schizophrenia. Nat. Med., 15, 509-518.
25. Jahr, C.E. & Stevens, C.F. (1990) Voltage dependence of NMDA-activated macroscopic conductances predicted by single-channel kinetics. J. Neurosci., 10, 3178-3182.
26. + channel ligands alter the firing pattern of dopamine-containing neurons in vivo. Neuroscience, 140, 623-633.
27. 2+ sensitivity of SK channels. Eur. J. Neurosci., 29, 1883-1895.
28. Johnson, S.W. & Wu, Y.N. (2004) Multiple mechanisms underlie burst firing in rat midbrain dopamine neurons in vitro. Brain Res., 1019, 293-296.
29. Johnson, S.W., Seutin, V. & North, R.A. (1992) Burst firing in dopamine neurons induced by N-methyl-d-aspartate: role of electrogenic sodium pump. Science, 258, 665-667.
30. Kamiya, K., Niwa, R., Mitcheson, J.S. & Sanguinetti, M.C. (2006) Molecular determinants of HERG channel block. Mol. Pharmacol., 69, 1709-1716.
31. Kang, Y. & Kitai, S.T. (1993) Calcium spike underlying rhythmic firing in dopaminergic neurons on the rat substantia nigra. Neurosci. Res., 18, 195-207.
32. Khaliq, Z.M. & Bean, B.P. (2010) Pacemaking in dopaminergic ventral tegmental area neurons: depolarizing drive from background and voltage-dependent sodium conductances. J. Neurosci., 30, 7401-7413.
33. Kongsamut, S., Kang, J., Chen, X.L., Roehr, J. & Rampe, D. (2002) A comparison of the receptor binding and HERG channel affinities for a series of antipsychotic drugs. Eur. J. Pharmacol., 450, 37-41.
34. Korolkova, Y.V., Kozlov, S.A., Lipkin, A.V., Pluzhnikov, K.A., Hadley, J.K., Filippov, A.K., Brown, D.A., Angelo, K., Strobaek, D., Jespersen, T., Olesen, S.P., Jensen, B.S. & Grishin, E.V. (2001) An ERG channel inhibitor from the scorpion Buthus eupeus. J. Biol. Chem., 276, 9868-9876.
35. Kullmann, P.H., Wheeler, D.W., Beacom, J. & Horn, J.P. (2004) Implementation of a fast 16-Bit dynamic clamp using LabVIEW-RT. J. Neurophysiol., 91, 542-554.
36. Kuznetsova, A.Y., Huertas, M.A., Kuznetsov, A.S., Paladini, C.A. & Canavier, C.C. (2010) Regulation of firing frequency in a computational model of a midbrain dopaminergic neuron. J. Comput. Neurosci., 28, 389-403.
37. Ljungberg, T., Apicella, P. & Schultz, W. (1992) Responses of monkey dopamine neurons during learning of behavioral reactions. J. Neurophysiol., 67, 145-163.
38. Montague, P.R., Dayan, P. & Sejnowski, T.J. (1996) A framework for mesencephalic dopamine systems based on predictive Hebbian learning. J. Neurosci., 16, 1936-1947.
39. Morikawa, H. & Paladini, C.A. (2011) Dynamic regulation of midbrain dopamine neuron activity: intrinsic, synaptic, and plasticity mechanisms. Neuroscience, 198, 95-111.
40. 2+ mobilization in dopamine neurons. J. Neurosci., 23, 149-157.
41. 2+-independent slow afterhyperpolarization in substantia nigra compacta neurons. Neuroscience, 125, 841-852.
42. 2+ conductances in guinea-pig substantia nigra pars compacta neurones. J. Physiol., 466, 727-747.
43. Overton, P.G. & Clark, D. (1997) Burst firing in midbrain dopaminergic neurons. Brain Res. Rev., 25, 312-334.
44. Pan, W.X., Schmidt, R., Wickens, J.R. & Hyland, B.I. (2005) Dopamine cells respond to predicted events during classical conditioning: evidence for eligibility traces in the reward-learning network. J. Neurosci., 25, 6235-6242.
45. + channel-encoding genes ERG1, ERG2, and ERG3 in the adult rat central nervous system. J. Comp. Neurol., 466, 119-135.
46. + channels regulate excitability and discharge dynamics of the medial vestibular nucleus neurons. J. Physiol., 586 (Pt 20), 4877-4890.
47. + channels regulate pacemaker activity in nigral dopamine neurons. NeuroReport, 8, 809-814.
48. 2+ selectivity, drives pacemaker activity and amplifies bursts in nigral dopamine neurons. J. Neurosci., 29, 15414-15419.
49. Putzier, I., Kullmann, P.H., Horn, J.P. & Levitan, E.S. (2009b) Dopamine neuron responses depend exponentially on pacemaker interval. J. Neurophysiol., 101, 926-933.
50. Roesch, M.R., Calu, D.J. & Schoenbaum, G. (2007) Dopamine neurons encode the better option in rats deciding between differently delayed or sized rewards. Nat. Neurosci., 10, 1615-1624.
51. Sacco, T., Bruno, A., Wanke, E. & Tempia, F. (2003) Functional roles of an ERG current isolated in cerebellar Purkinje neurons. J. Neurophysiol., 90, 1817-1828.
52. + channels in brain. J. Neurosci., 21, 4609-4624.
53. Sanghera, M.K., Trulson, M.E. & German, D.C. (1984) Electrophysiological properties of mouse dopamine neurons: in vivo and in vitro studies. Neuroscience, 12, 793-801.
54. + channels. Eur. J. Neurosci., 11, 753-760.
55. Seutin, V. & Engel, D. (2010) Differences in Na+ conductance density and Na+ channel functional properties between dopamine and GABA neurons of the rat substantia nigra. J. Neurophysiol., 103, 3099-3114.
56. Seutin, V., Johnson, S.W. & North, R.A. (1993) Apamin increases NMDA-induced burst-firing of rat mesencephalic dopamine neurons. Brain Res., 630, 341-344.
57. Shepard, P.D. & Stump, D. (1999) Nifedipine blocks apamin-induced bursting activity in nigral dopamine-containing neurons. Brain Res., 817, 104-109.
58. Shepard, P.D., Canavier, C.C. & Levitan, E.S. (2007) Ether-a-go-go-related gene potassium channels: what's all the buzz about?Schizophr. Bull., 33, 1263-1269.
59. Steward, O., Tomasulo, R. & Levy, W.B. (1990) Blockade of inhibition in a pathway with dual excitatory and inhibitory action unmasks a capability for LTP that is otherwise not expressed. Brain Res., 516, 292-300.
60. Tepper, J.M., Martin, L.P. & Anderson, D.R. (1995) GABAA receptor-mediated inhibition of rat substantia nigra dopaminergic neurons by pars reticulata projection neurons. J. Neurosci., 15, 3092-3103.
61. Titier, K., Canal, M., Deridet, E., Abouelfath, A., Gromb, S., Molimard, M. & Moore, N. (2004) Determination of myocardium to plasma concentration ratios of five antipsychotic drugs: comparison with their ability to induce arrhythmia and sudden death in clinical practice. Toxicol. Appl. Pharmacol., 199, 52-60.
62. Titier, K., Girodet, P.O., Verdoux, H., Molimard, M., Begaud, B., Haverkamp, W., Lader, M. & Moore, N. (2005) Atypical antipsychotics: from potassium channels to torsade de pointes and sudden death. Drug Saf., 28, 35-51.
63. Valenti, O., Cifelli, P., Gill, K.M. & Grace, A.A. (2011) Antipsychotic drugs rapidly induce dopamine neuron depolarization block in a developmental rat model of schizophrenia. J. Neurosci., 31, 12330-12338.
64. Vilums, M., Overman, J., Klaasse, E., Scheel, O., Brussee, J. & Ijzerman, A.P. (2011) Understanding of molecular substructures that contribute to hERG K(+) channel blockade: synthesis and biological evaluation of E-4031 analogues. ChemMedChem., 7, 107-113.
65. Wang, R.Y. (1981) Dopaminergic neurons in the rat ventral tegmental area. I. Identification and characterization. Brain Res. Rev., 3, 123-140.
66. Waroux, O., Massotte, L., Alleva, L., Graulich, A., Thomas, E., Liegeois, J.F., Scuvee-Moreau, J. & Seutin, V. (2005) SK channels control the firing pattern of midbrain dopaminergic neurons in vivo. Eur. J. Neurosci., 22, 3111-3121.
67. Wilson, C.J., Young, S.J. & Groves, P.M. (1977) Statistical properties of neuronal spike trains in the substantia nigra: cell types and their interactions. Brain Res., 136, 243-260.
68. Yung, W.H., Hausser, M.A. & Jack, J.J.B. (1991) Electrophysiology of dopaminergic and non-dopaminergic neurones of the guinea-pig substantia nigra pars compacta in vitro. J. Physiol., 436, 643-667.