Endogenous hydrogen peroxide regulates the excitability of midbrain dopamine neurons via ATP-sensitive potassium channels

Journal of Neuroscience

Volumn 25, Issue 17, 2005, Pages 4222-4231

  Avshalumov, Marat V ^a   Chen, Billy T ^a,c   Koos, Tibor ^b,d   Tepper, James M ^b   Rice, Margaret E ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b RUTGERS UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA SAN FRANCISCO   (United States)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Basal ganglia; DCF fluorescence imaging; Dopamine; KATP channels; Parkinson's disease; Peroxide; Potassium (K+) channels; Substantia nigra

Indexed keywords

ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; AMITROLE; CATALASE; CROMAKALIM; DIAZOXIDE; DICHLOROFLUORESCEIN; GLIBENCLAMIDE; GLUTATHIONE PEROXIDASE; HYDROGEN PEROXIDE; PEROXIDASE; POTASSIUM CHANNEL; POTASSIUM CHANNEL AFFECTING AGENT; POTASSIUM CHANNEL BLOCKING AGENT; RECEPTOR SUBUNIT; SULFONYLUREA RECEPTOR; SULFONYLUREA RECEPTOR 1; SULFONYLUREA RECEPTOR 2; THIOMALIC ACID; UNCLASSIFIED DRUG;

AEROBIC METABOLISM; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN METABOLISM; BRAIN SLICE; CHANNEL GATING; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; ENZYME INHIBITION; FLUORESCENCE; GLIA; GUINEA PIG; HYPERPOLARIZATION; MALE; MESENCEPHALON; NERVE CELL EXCITABILITY; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; SUBSTANTIA NIGRA;

ADENOSINE TRIPHOSPHATE; ANALYSIS OF VARIANCE; ANIMALS; CROMAKALIM; DIAZOXIDE; DOPAMINE; DOSE-RESPONSE RELATIONSHIP, DRUG; DOSE-RESPONSE RELATIONSHIP, RADIATION; DRUG INTERACTIONS; ELECTRIC STIMULATION; GLUTATHIONE PEROXIDASE; GLYBURIDE; GUINEA PIGS; HYDROGEN PEROXIDE; HYPOGLYCEMIC AGENTS; ISOQUINOLINES; MEMBRANE POTENTIALS; MESENCEPHALON; NEURONS; ORGANOPLATINUM COMPOUNDS; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNELS; TETRODOTOXIN; THIOMALATES; TIME FACTORS; VASODILATOR AGENTS;

EID: 18244386217     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4701-04.2005     Document Type: Article

References (66)

1. Albin RL, Young AB, Penney JB (1989) The functional anatomy of basal ganglia disorders. Trends Neurosci 12:366-375.
2. + channels. Science 247:852-854.
3. + channels. Trends Neurosci 21:288-294.
4. Ashcroft SJ, Ashcroft FM (1990) Properties and functions of ATP-sensitive K-channels. Cell Signal 2:197-214.
5. 2 underlies glutamate-dependent inhibition of striatal dopamine release. Proc Natl Acad Sci USA 100:11729-11734.
6. 2. J Neurosci 23:2744-2750.
7. ATP channels. Annu Rev Physiol 60:667-687.
8. Boveris A, Chance B (1973) The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen. Biochem J 134:707-716.
9. 2 is a novel, endogenous modulator of synaptic dopamine release. J Neurophysiol 85:2468-2476.
10. 2: susceptibility in substantia nigra but resistance in VTA. J Neurophysiol 87:1155-1158.
11. ATP channels in guinea pig ventricular cells. Am J Physiol 269:H1625-H1633.
12. Cohen G (1994) Enzymatic/nonenzymatic sources of oxyradicals and regulation of antioxidant defenses. Ann NY Acad Sci 738:8-14.
13. + channels in pancreatic β-cells. Nature 311:271-273.
14. Crepel V, Krnjevic K, Ben-Ari Y (1993) Sulphonylureas reduce the slowly inactivating D-type outward current in rat hippocampal neurons. J Physiol (Lond) 466:39-54.
15. Dahlstrom A, Fuxe K (1964) Localization of monoamines in the lower brain stem. Experientia 20:398-399.
16. Damier P, Hirsch EC, Zhang P, Agid Y, Javoy-Agid F (1993) Glutathione peroxidase, glial cells and Parkinson's disease. Neuroscience 52:1-6.
17. Desagher S, Glowinski J, Premont J (1996) Astrocytes protect neurons from hydrogen peroxide toxicity. J Neurosci 16:2553-2562.
18. Dringen R, Kussmaul L, Hamprecht B (1998) Rapid clearance of tertiary butyl hydroperoxide by cultured astroglial cells via oxidation of glutathione. Glia 23:139-145.
19. Dugan LL, Sensi SL, Canzoniero LM, Handran SD, Rothman SM, Lin TS, Goldberg MP, Choi DW (1995) Mitochondrial production of reactive oxygen species in cortical neurons following exposure to N-methyl-D-aspartate. J Neurosci 15:6377-6388.
20. Forbes RA, Steenbergen C, Murphy E (2001) Diazoxide-induced cardioprotection requires signaling through a redox-sensitive mechanism. Circ Res 88:802-809.
21. Gerfen CR, Baimbridge KG, Thibault J (1987) The neostriatal mosaic: III. Biochemical and developmental dissociation of patch-matrix mesostriatal systems. J Neurosci 7:3935-3944.
22. Gonon FG, Buda M (1985) Regulation of dopamine release by impulse flow and by autoreceptors as studied by in vivo voltammetry in the rat striatum. Neuroscience 14:765-774.
23. Grace AA, Onn S-P (1989) Morphology and electrophysiological properties of immunocytochemically identified rat dopamine neurons recorded in vitro. J Neurosci 9:3463-3481.
24. Guatteo E, Federici M, Siniscalchi A, Knopfel T, Mercuri NB, Bernardi G (1998) Whole cell patch-clamp recordings of rat midbrain dopaminergic neurons isolate a sulphonylurea- and ATP-sensitive component of potassium currents activated by hypoxia. J Neurophysiol 79:1239-1245.
25. Hanley JJ, Bolam JP (1997) Synaptology of the nigrostriatal projection in relation to the compartmental organization of the neostriatum in the rat. Neuroscience 81:353-370.
26. + channels in substantia nigra. Biochem Biophys Res Commun 174:909-914.
27. Hung HC, Lee EH (1998) MPTP produces differential oxidative stress and antioxidative responses in the nigrostriatal and mesolimbic dopaminergic pathways. Free Radic Biol Med 24:76-84.
28. Ichinari K, Kakei M, Matsuoka T, Nakashima H, Tanaka H (1996) Direct activation of the ATP-sensitive potassium channel by oxygen free radicals in guinea-pig ventricular cells: its potentiation by MgADP. J Mol Cell Cardiol 28:1867-1877.
29. + channels. Neuron 16:1011-1017.
30. + channel. J Biol Chem 271:24321-24324.
31. + channel in substantia nigra neurons. J Neurosci 14:5590-5602.
32. Kamsler A, Segal M (2004) Hydrogen peroxide as a diffusible signal molecule in synaptic plasticity. Mol Neurobiol 29:167-178.
33. Kang Y, Kitai ST (1993) Calcium spike underlying rhythmic firing in dopaminergic neurons of the rat substantia nigra. Neurosci Res 18:195-207.
34. Koós T, Tepper JM (1999) Inhibitory control of neostriatal projection neurons by GABAergic interneurons. Nat Neurosci 2:467-472.
35. 2 with stimulus-secretion coupling in mouse pancreatic β-cells. J Physiol (Lond) 514:471-481.
36. Lee K, Dixon AK, Freeman TC, Richardson PJ (1998) Identification of an ATP-sensitive potassium channel current in rat striatal cholinergic interneurones. J Physiol (Lond) 510:441-453.
37. Levesque D, Greenfield SA (1991) Psychopharmacological evidence for a role of the ATP-sensitive potassium channel in the substantia nigra of the rat. Neuropharmacology 30:359-365.
38. Liss B, Bruns R, Roeper J (1999) Alternative sulfonylurea receptor expression defines sensitivity to K-ATP channels in dopaminergic midbrain neurons. EMBO J 18:833-846.
39. Liu Y, Fiskum G, Schubert D (2002) Generation of reactive oxygen species by the mitochondrial electron transport chain. J Neurochem 80:780-787.
40. Mercuri NB, Bond A, Johnson SW, Stratta F, Calabresi P, Bernardi G (1994) Effects of anoxia on rat midbrain dopamine neurons. J Neurophysiol 71:1165-1173.
41. Mourre C, Ben Ari Y, Bernardi H, Fosset M, Lazdunski M (1989) Antidiabetic sulfonylureas: localization of binding sites in the brain and effects on the hyperpolarization induced by anoxia in hippocampal slices. Brain Res 486:159-164.
42. Murphy KP, Greenfield SA (1992) Neuronal selectivity of ATP-sensitive potassium channels in guinea-pig substantia nigra revealed by responses to anoxia. J Physiol (Lond) 453:167-183.
43. h channels contribute to the different functional properties of identified dopaminergic subpopulations in the midbrain. J Neurosci 22:1290-1302.
44. o are target proteins of reactive oxygen species. Nature 408:492-495.
45. + channels in cardiac muscle. Nature 305:147-148.
46. Olanow CW, Tatton WG (1999) Etiology and pathogenesis of Parkinson's disease. Annu Rev Neurosci 22:123-144.
47. Oyama Y, Hayashi A, Ueha T, Maekawa K (1994) Characterization of 2′,7′-dichlorofluorescin fluorescence in dissociated mammalian brain neurons: estimation on intracellular content of hydrogen peroxide. Brain Res 635:113-117.
48. A receptor stimulation blocks NMDA-induced bursting of dopaminergic neurons in vitro by decreasing input resistance. Brain Res 832:145-151.
49. Prensa L, Parent A (2001) The nigrostriatal pathway in the rat: a single-axon study of the relationship between dorsal and ventral tier nigral neurons and the striosome/matrix striatal compartments. J Neurosci 21:7247-7260.
50. Rae J, Cooper K, Gates P, Watsky M (1991) Low access resistance perforated patch recordings using amphotericin B. J Neurosci Methods 37:15-26.
51. Reynolds IJ, Hastings TG (1995) Glutamate induces the production of reactive oxygen species in cultured forebrain neurons following NMDA receptor activation. J Neurosci 15:3318-3327.
52. Rice ME, Cragg SJ, Greenfield SA (1997) Characteristics of electrically evoked somatodendritic dopamine release in substantia nigra and ventral tegmental area in vitro. J Neurophysiol 77:853-862.
53. Roeper J, Ashcroft FM (1995) Metabolic inhibition and low internal ATP activate K-ATP channels in rat dopaminergic substantia nigra neurones. Pflügers Arch 430:44-54.
54. Sah R, Schwartz-Bloom RD (1999) Optical imaging reveals elevated intracellular chloride in hippocampal pyramidal cells after oxidative stress. J Neurosci 19:9209-9217.
55. Schaffer P, Pelzmann B, Bernhart E, Lang P, Machler H, Rigler B, Koidl B (1999) The sulphonylurea glibenclamide inhibits voltage dependent potassium currents in human atrial and ventricular myocytes. Br J Pharmacol 128:1175-1180.
56. Scuvee-Moreau J, Seutin V, Vrijens B, Pirotte B, De Tullio P, Massotte L, Albert A, Delarge J, Dresse A (1997) Effect of potassium channel openers on the firing rate of hippocampal pyramidal cells and A10 dopaminergic neurons in vitro. Arch Physiol Biochem 105:421-428.
57. Seutin V, Scuvee-Moreau J, Masotte L, Dresse A (1995) Hydrogen peroxide hyperpolarizes rat CA1 pyramidal neurons by inducing an increase in potassium conductance. Brain Res 683:275-278.
58. Stanford IM, Lacey MG (1995) Regulation of a potassium conductance in rat midbrain dopamine neurons by intracellular adenosine triphosphate (ATP) and the sulfonylureas tolbutamide and glibenclamide. J Neurosci 15:4651-4657.
59. 2 for platelet-derived growth factor signal transduction. Science 270:296-299.
60. ATP channels in guinea-pig ventricular myocytes. Pflügers Arch 437:155-157.
61. Trépanier G, Furling D, Puymirat J, Mirault ME (1996) Immunocytochemical localization of seleno-glutathione peroxidase in the adult mouse brain. Neuroscience 75:231-243.
62. Wilson CJ, Callaway JC (2000) Coupled oscillator model of the dopaminergic neuron of the substantia nigra. J Neurophysiol 83:3084-3100.
63. Witkovsky P, Gabriel R, Haycock JW, Meller E (2000) Influence of light and neural circuitry on tyrosine hydroxylase phosphorylation in the rat retina. J Chem Neuroanat 19:105-116.
64. Xia Y, Haddad GG (1991) Major differences in CNS sulfonylurea receptor distribution between the rat (newborn, adult) and turtle. J Comp Neurol 314:278-289.
65. Yung WH, Häusser MA, Jack JJ (1991) Electrophysiology of dopaminergic and non-dopaminergic neurones of the guinea-pig substantia nigra pars compacta in vitro. J Physiol (Lond) 436:643-667.
66. Zini S, Tremblay E, Pollard H, Moreau J, Ben-Ari Y (1993) Regional distribution of sulfonylurea receptors in the brain of rodent and primate. Neuroscience 55:1085-1091.