Functional Upregulation of Ca2+ -Activated K+ Channels in the Development of Substantia Nigra Dopamine Neurons

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Ramírez Latorre, José A ^a,b  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b UNIVERSIDAD DEL ROSARIO   (Colombia)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ACTIVATED POTASSIUM CHANNEL; LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; SMALL CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL;

ANIMAL TISSUE; ARTICLE; BASAL GANGLION; CELL ACTIVITY; CELL KINETICS; CELL SELECTION; CLUSTER ANALYSIS; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; ENZYME ACTIVITY; ENZYME REGULATION; HUMAN; HUMAN CELL; NERVE CELL DIFFERENTIATION; NERVE STIMULATION; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SUBSTANTIA NIGRA; SYNAPSE;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; BRAIN; CALCIUM; DOPAMINE; DOPAMINERGIC NEURONS; ELECTROPHYSIOLOGY; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNOENZYME TECHNIQUES; KINETICS; LARGE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; MODELS, THEORETICAL; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNEL BLOCKERS; RATS; RATS, SPRAGUE-DAWLEY; SMALL-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; SUBSTANTIA NIGRA; TYROSINE 3-MONOOXYGENASE; UP-REGULATION;

ANIMALIA;

EID: 84871457948     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0051610     Document Type: Article

References (80)

1. Shi WX (2009) Electrophysiological Characteristics of Dopamine Neurons: A 35-Year Update. In: Giovanni G, Di Matteo V, Esposito E, editors, Birth, Life and Death of Dopaminergic Neurons in the Substantia Nigra, Springer Vienna, volume 73 of Journal of Neural Transmission. Supplementa. pp. 103-119.
2. Albin RL, Young AB, Penney JB, (1995) The functional anatomy of disorders of the basal ganglia. Trends Neurosci 18: 63-64.
3. Alexander GE, DeLong MR, Strick PL, (1986) Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annual Review of Neuroscience 9: 357-381.
4. Gerfen CR, Engber TM, Mahan LC, Susel Z, Chase TN, et al. (1990) D1 and D2 dopamine receptorregulated gene expression of striatonigral and striatopallidal neurons. Science 250: 1429-1432.
5. Smith Y, Bevan MD, Shink E, Bolam JP, (1998) Microcircuitry of the direct and indirect pathways of the basal ganglia. Neuroscience 86: 353-387.
6. Redgrave P, Rodriguez M, Smith Y, Rodriguez-Oroz MC, Lehericy S, et al. (2010) Goal-directed and habitual control in the basal ganglia: implications for Parkinson's disease. Nature Reviews Neuroscience 11: 760-772.
7. Gonon F, (1988) Nonlinear relationship between impulse flow and dopamine released by rat midbrain dopaminergic neurons as studied by in vivo electrochemistry. Neuroscience 24: 19-28.
8. Manley LD, Kuczenski R, Segal DS, Young SJ, Groves PM, (1992) Effects of frequency and pattern of medial forebrain bundle stimulation on caudate dialysate dopamine and serotonin. Journal of Neurochemistry 58: 1491-1498.
9. Chergui K, Charlty PJ, Akaoka H, Saunier CF, Brunet JL, et al. (1993) Tonic activation of NMDA receptors causes spontaneous burst discharge of rat midbrain dopamine neurons in vivo. European Journal of Neuroscience 5: 137-144.
10. Garris PA, Ciolkowski EL, Pastore P, Wightman RM, (1994) Efflux of dopamine from the synaptic cleft in the nucleus accumbens of the rat brain. J Neurosci 14: 6084-6093.
11. Shen W, Flajolet M, Greengard P, Surmeier DJ, (2008) Dichotomous dopaminergic control of striatal synaptic plasticity. Science (New York, NY) 321: 848-851.
12. Lee CR, Tepper JM (2009) Basal ganglia control of substantia nigra dopaminergic neurons. In: Giovanni G, Di Matteo V, Esposito E, editors, Birth, Life and Death of Dopaminergic Neurons in the Substantia Nigra, Springer Vienna, volume 73 of Journal of Neural Transmission. Supplementa. pp. 71-90.
13. Harris N, Webb C, Greenfield S, (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.
14. Lacey M, Mercuri N, North R, (1989) Two cell types in rat substantia nigra zona compacta distinguished by membrane properties and the actions of dopamine and opioids. The Journal of Neuroscience 9: 1233-1241.
15. Yung WH, Husser MA, Jack JJ, (1991) Electrophysiology of dopaminergic and non-dopaminergic neurones of the guinea-pig substantia nigra pars compacta in vitro. The Journal of Physiology 436: 643-667.
16. Hainsworth A, Röper J, Kapoor R, Ashcroft F, (1991) Identification and electrophysiology of isolated pars compacta neurons from guinea-pig substantia nigra. Neuroscience 43: 81-93.
17. Blythe SN, Atherton JF, Bevan MD, (2007) Synaptic activation of dendritic AMPA and NMDA receptors generates transient high-frequency firing in substantia nigra dopamine neurons in vitro. Journal of Neurophysiology 97: 2837-2850.
18. Blythe SN, Wokosin D, Atherton JF, Bevan MD, (2009) Cellular mechanisms underlying burst firing in substantia nigra dopamine neurons. The Journal of Neuroscience 29: 15531-15541.
19. Grace A, Bunney B, (1984) The control of firing pattern in nigral dopamine neurons: burst firing. The Journal of Neuroscience 4: 2877-2890.
20. Hyland B, Reynolds J, Hay J, Perk C, Miller R, (2002) Firing modes of midbrain dopamine cells in the freely moving rat. Neuroscience 114: 475-492.
21. Lobb CJ, Wilson CJ, Paladini CA, (2011) High-frequency, short-latency disinhibition bursting of midbrain dopaminergic neurons. Journal of Neurophysiology 105: 2501-2511.
22. Iribe Y, Moore K, Pang KCH, Tepper JM, (1999) Subthalamic stimulation-induced synaptic responses in substantia nigra pars compacta dopaminergic neurons in vitro. Journal of Neurophysiology 82: 925-933.
23. Lokwan S, Overton P, Berry M, Clark D, (1999) Stimulation of the pedunculopontine tegmental nucleus in the rat produces burst firing in A9 dopaminergic neurons. Neuroscience 92: 245-254.
24. Cohen B, Mackey E, Grady S, Mckinney S, Patzlaff N, et al. (2012) Nicotinic cholinergic mechanisms causing elevated dopamine release and abnormal locomotor behavior. Neuroscience 200: 31-41.
25. Tepper J, Trent F, Nakamura S, (1990) Postnatal development of the electrical activity of rat nigrostriatal dopaminergic neurons. Developmental Brain Research 54: 21-33.
26. Ferrari DC, Mdzomba BJ, Dehorter N, Lopez C, Michel FJ, et al. (2012) Midbrain dopaminergic neurons generate calcium and sodium currents and release dopamine in the striatum of pups. Frontiers in Cellular Neuroscience 6 No. 7: 1-9.
27. Marty A, (1981) Ca-dependent K channels with large unitary conductance in chromaffin cell membranes. Nature 291: 497-500.
28. Elkins T, Ganetzky B, Wu CF, (1986) A drosophila mutation that eliminates a calcium-dependent potassium current. Proceedings of the National Academy of Sciences 83: 8415-8419.
29. Du W, Bautista JF, Yang H, Diez-Sampedro A, You SA, et al. (2005) Calcium-sensitive potassium channelopathy in human epilepsy and paroxysmal movement disorder. Nature Genetics 37: 733-738.
30. Guzman JN, Snchez-Padilla J, Chan CS, Surmeier DJ, (2009) Robust pacemaking in substantia nigra dopaminergic neurons. The Journal of Neuroscience 29: 11011-11019.
31. Wisgirda ME, Dryer SE, (1994) Functional dependence of Ca(2+)-activated K+ current on L- and N-type Ca2+ channels: differences between chicken sympathetic and parasympathetic neurons suggest different regulatory mechanisms. Proceedings of the National Academy of Sciences 91: 2858-2862.
32. Vandael D, Marcantoni A, Mahapatra S, Caro A, Ruth P, et al. (2010) Cav1.3 and BK channels for timing and regulating cell firing. Molecular Neurobiology 42: 185-198.
33. Hille B, (1984) Ionic channels of excitable membranes. Sinauer Associates, Sunderland, Mass.
34. Su W, Song X, Ji JJ, (2010) Functional expression of a large-conductance Ca2+-activated K+ channel in mouse substantia nigra pars compacta dopaminergic neurons. Neuroscience Letters 471: 1-5.
35. Cardozo DL, Bean BP, (1995) Voltage-dependent calcium channels in rat midbrain dopamine neurons: modulation by dopamine and GABAB receptors. Journal of Neurophysiology 74: 1137-1148.
36. Katayama J, Akaike N, Nabekura J, (2003) Characterization of pre- and post-synaptic metabotropic glutamate receptor-mediated inhibitory responses in substantia nigra dopamine neurons. Neuroscience Research 45: 101-115.
37. Neuhoff H, Neu A, Liss B, Roeper J, (2002) Ih channels contribute to the different functional properties of identified dopaminergic subpopulations in the midbrain. The Journal of Neuroscience 22: 1290-1302.
38. Voorn P, Kalsbeek A, Jorritsma-Byham B, Groenewegen HJ, (1988) The pre- and postnatal development of the dopaminergic cell groups in the ventral mesencephalon and the dopaminergic innervation of the striatum of the rat. Neuroscience 25: 857-887.
39. Tepper J, Damlama M, Trent F, (1994) Postnatal changes in the distribution and morphology of rat substantia nigra dopaminergic neurons. Neuroscience 60: 469-477.
40. Gerfen CR, (1992) The neostriatal mosaic: Multiple levels of compartmental organization in the basal ganglia. Annual Review of Neuroscience 15: 285-320.
41. Solaro C, Prakriya M, Ding J, Lingle C, (1995) Inactivating and noninactivating Ca2+- and voltagedependent K+ current in rat adrenal chromaffin cells. The Journal of Neuroscience 15: 6110-6123.
42. Pyott SJ, Glowatzki E, Trimmer JS, Aldrich RW, (2004) Extrasynaptic localization of inactivating calcium-activated potassium channels in mouse inner hair cells. The Journal of Neuroscience 24: 9469-9474.
43. Hicks GA, Marrion NV, (1998) Ca2+-dependent inactivation of large conductance Ca2+-activated K+ (BK) channels in rat hippocampal neurones produced by pore block from an associated particle. The Journal of Physiology 508: 721-734.
44. Faber ESL, Sah P, (2003) Ca2+-activated K+ (BK) channel inactivation contributes to spike broadening during repetitive firing in the rat lateral amygdala. The Journal of Physiology 552: 483-497.
45. Sun X, Gu XQ, Haddad GG, (2003) Calcium influx via L- and N-Type calcium channels activates a transient large-conductance Ca2+-activated K+ current in mouse neocortical pyramidal neurons. The Journal of Neuroscience 23: 3639-3648.
46. Lee US, Cui J, (2009) β subunit-specific modulations of BK channel function by a mutation associated with epilepsy and dyskinesia. The Journal of Physiology 587: 1481-1498.
47. Lee US, Cui J, (2010) BK channel activation: structural and functional insights. Trends in Neurosciences 33: 415-423.
48. Durante P, Cardenas CG, Whittaker JA, Kitai ST, Scroggs RS, (2004) Low-threshold L-type calcium channels in rat dopamine neurons. Journal of Neurophysiology 91: 1450-1454.
49. Puopolo M, Raviola E, Bean BP, (2007) Roles of subthreshold calcium current and sodium current in spontaneous firing of mouse midbrain dopamine neurons. The Journal of Neuroscience 27: 645-656.
50. Kang Y, Kitai ST, (1993) A whole cell patch-clamp study on the pacemaker potential in dopaminergic neurons of rat substantia nigra compacta. Neuroscience Research 18: 209-221.
51. Wolfart J, Roeper J, (2002) Selective coupling of T-type calcium channels to SK potassium channels prevents intrinsic bursting in dopaminergic midbrain neurons. The Journal of Neuroscience 22: 3404-3413.
52. Cui G, Okamoto T, Morikawa H, (2004) Spontaneous opening of T-type Ca2+channels contributes to the irregular firing of dopamine neurons in neonatal rats. The Journal of Neuroscience 24: 11079-11087.
53. Cueni L, Canepari M, Adelman J, Lthi A, (2009) Ca2+signaling by T-tpe Ca2+channels in neurons. Pflgers Archiv European Journal of Physiology 457: 1161-1172.
54. Sherman A, Keizer J, Rinzel J, (1990) Domain model for Ca2+-inactivation of Ca2+channels at low channel density. Biophysical Journal 58: 985-995.
55. Fakler B, Adelman JP, (2008) Control of KCa channels by calcium nano/microdomains. Neuron 59: 873-881.
56. Smith G, Wagner J, Keizer J, (1996) Validity of the rapid buffering approximation near a point source of calcium ions. Biophysical Journal 70: 2527-2539.
57. Smith G (2001) Modeling local and global calcium signals. In: De Schutter E, editor, Computational Neuroscience, Boca Ratn: CRC Press. pp. 49-85.
58. Shults C, Hashimoto R, Brady R, Gage F, (1990) Dopaminergic cells align along radial glia in the developing mesencephalon of the rat. Neuroscience 38: 427-436.
59. Marchand R, Poirier L, (1983) Isthmic origin of neurons of the rat substantia nigra. Neuroscience 9: 373-381.
60. Cameron JS, Dryer L, Dryer SE, (2001) β-neuregulin-1 is required for the in vivo development of functional Ca2+-activated K+ channels in parasympathetic neurons. Proceedings of the National Academy of Sciences 98: 2832-2836.
61. MacDonald S, Ruth P, Knaus HG, Shipston M, (2006) Increased large conductance calciumactivated potassium (BK) channel expression accompanied by strex variant downregulation in the developing mouse CNS. BMC Developmental Biology 6: 37.
62. Olsen M, Weaver A, Ritch P, Sontheimer H, (2005) Modulation of glioma BK channels via ErbB2. Journal of Neuroscience Research 81: 179-189.
63. Abe Y, Namba H, Zheng Y, Nawa H, (2009) In situ hybridization reveals developmental regulation of ErbB1-4 mRNA expression in mouse midbrain: Implication of ErbB receptors for dopaminergic neurons. Neuroscience 161: 95-110.
64. Meyer D, Yamaai T, Garratt A, Riethmacher-Sonnenberg E, Kane D, et al. (1997) Isoform-specific expression and function of neuregulin. Development 124: 3575-3586.
65. Yurek DM, Zhang L, Fletcher-Turner A, Seroogy KB, (2004) Supranigral injection of neuregulin1-β induces striatal dopamine overflow. Brain Research 1028: 116-119.
66. Carlsson T, Schindler FR, Hllerhage M, Depboylu C, Arias-Carrin O, et al. (2011) Systemic administration of neuregulin-1β1 protects dopaminergic neurons in a mouse model of parkinsons disease. Journal of Neurochemistry 117: 1066-1074.
67. Zhang L, Li X, Zhou R, Xing G, (2006) Possible role of potassium channel, big K in etiology of schizophrenia. Medical hypotheses 67: 41-43.
68. Jaaro-Peled H, Hayashi-Takagi A, Seshadri S, Kamiya A, Brandon NJ, et al. (2009) Neurodevelopmental mechanisms of schizophrenia: understanding disturbed postnatal brain maturation through neuregulin-1erbb4 and disc1. Trends in Neurosciences 32: 485-495.
69. Gu N, Vervaeke K, Storm JF, (2007) BK potassium channels facilitate high-frequency firing and cause early spike frequency adaptation in rat CA1 hippocampal pyramidal cells. The Journal of Physiology 580: 859-882.
70. Schultz W, Dayan P, Montague PR, (1997) A neural substrate of prediction and reward. Science 275: 1593-1599.
71. Ben-Ari Y, Spitzer NC, (2010) Phenotypic checkpoints regulate neuronal development. Trends in Neurosciences 33: 485-492.
72. Trent F, Shoji N, Tepper JM, (1991) Amphetamine exerts anomalous effects on dopaminergic neurons in neonatal rats in vivo. European Journal of Pharmacology 204: 265-272.
73. Watmuff B, Pouton CW, Haynes JM, (2012) In vitro maturation of dopaminergic neurons derived from mouse embryonic stem cells: Implications for transplantation. PLoS ONE 7: e31999.
74. Imlach WL, Finch SC, Dunlop J, Meredith AL, Aldrich RW, et al. (2008) The molecular mechanism of "ryegrass staggers", a neurological disorder of K+ channels. Journal of Pharmacology and Experimental Therapeutics 327: 657-664.
75. Liu J, Vaithianathan T, Manivannan K, Parrill A, Dopico AM, (2008) Ethanol modulates BKCa channels by acting as an adjuvant of calcium. Molecular Pharmacology 74: 628-640.
76. Ebihara S, Shirato K, Harata N, Akaike N, (1995) Gramicidin-perforated patch recording: GABA response in mammalian neurones with intact intracellular chloride. The Journal of Physiology 484: 77-86.
77. McGuigan JAS, Lthi D, Buri A, (1991) Calcium buffer solutions and how to make them: A do it yourself guide. Canadian Journal of Physiology and Pharmacology 69: 1733-1749.
78. Thomas D, Tovey S, Collins T, Bootman M, Berridge M, et al. (2000) A comparison of fluorescent Ca2+indicator properties and their use in measuring elementary and global Ca2+signals. Cell Calcium 28: 213-223.
79. Franciolini F, Hogg R, Catacuzzeno L, Petris A, Trequattrini C, et al. (2001) Large-conductance calcium-activated potassium channels in neonatal rat intracardiac ganglion neurons. Pflgers Archiv European Journal of Physiology 441: 629-638.
80. Pouvreau S, Berthier C, Blaineau S, Amsellem J, Coronado R, et al. (2004) Membrane cholesterol modulates dihydropyridine receptor function in mice fetal skeletal muscle cells. The Journal of Physiology 555: 365-381.