Partial mitochondrial inhibition causes striatal dopamine release suppression and medium spiny neuron depolarization via H2O 2 elevation, not ATP depletion

Journal of Neuroscience

Volumn 25, Issue 43, 2005, Pages 10029-10040

  Bao, Li ^a   Avshalumov, Marat V ^a   Rice, Margaret E ^a  

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

Author keywords

Basal ganglia; KATP channels; Medium spiny neurons; Mitochondria; Parkinson's disease; Pesticide; Rotenone

Indexed keywords

3,4 DIHYDROXYPHENYLACETIC ACID; ADENOSINE TRIPHOSPHATE; DOPAMINE; GLIBENCLAMIDE; HYDROGEN PEROXIDE; PESTICIDE; POTASSIUM CHANNEL; POTASSIUM ION; ROTENONE; TOLBUTAMIDE;

ANIMAL TISSUE; ARTICLE; BRAIN MITOCHONDRION; BRAIN SLICE; CONTROLLED STUDY; DEGENERATIVE DISEASE; DOPAMINE RELEASE; DOPAMINERGIC NERVE CELL; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; NEUROLOGIC DISEASE; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL;

ADENOSINE TRIPHOSPHATE; ANALYSIS OF VARIANCE; ANIMALS; CATALASE; CORPUS STRIATUM; DOPAMINE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; ELECTRIC STIMULATION; FLUORESCEINS; GLYBURIDE; GUINEA PIGS; HYDROGEN PEROXIDE; HYPOGLYCEMIC AGENTS; MEMBRANE POTENTIALS; NEURONS; PATCH-CLAMP TECHNIQUES; ROTENONE; SODIUM CHANNEL BLOCKERS; TETRODOTOXIN; TIME FACTORS; TOLBUTAMIDE; UNCOUPLING AGENTS;

EID: 27344450419     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2652-05.2005     Document Type: Article

References (72)

1. Alam M, Schmidt WJ (2004) L-DOPA reverses the hypokinetic behaviour and rigidity in rotenone-treated rats. Behav Brain Res 153:439-446.
2. + channels. Trends Neurosci 21:288-294.
3. 2 underlies glutamate-dependent inhibition of striatal dopamine release. Proc Natl Acad Sci USA 100:11729-11734.
4. 2. J Neurosci 23:2744-2750.
5. Avshalumov MV, Chen BT, Koos T, Tepper JM, Rice ME (2005) Endogenous hydrogen peroxide regulates the excitability of midbrain dopamine neurons via ATP-sensitive channels. J Neurosci 25:4222-4231.
6. Bengtson CP, Tozzi A, Bernardi G, Mercuri NB (2004) Transient receptor potential-like channels mediate metabotropic glutamate receptor EPSCs in rat dopamine neurones. J Physiol (Lond) 555:323-330.
7. Berman SB, Hastings TG (1999) Dopamine oxidation alters mitochondrial respiration and induces permeability transition in brain mitochondria: implications for Parkinson's disease. J Neurochem 73:1127-1137.
8. Betarbet R, Sherer TB, MacKenzie G, Garcia-Osuna M, Panov AV, Greenamyre JT (2000) Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nat Neurosci 3:1301-1306.
9. Bonsi P, Calabresi P, De Persis C, Papa M, Centonze D, Bernardi G, Pisani A (2004) Early ionic and membrane potential changes caused by the pesticide rotenone in striatal cholinergic interneurons. Exp Neurol 185:169-181.
10. Calabresi P, Ascone CM, Centonze D, Pisani A, Sancesario G, D'Angelo V, Bernardi G (1997) Opposite membrane potential changes induced by glucose deprivation in striatal spiny neurons and in large aspiny interneurons. J Neurosci 17:1940-1949.
11. Calabresi P, Marfia GA, Centonze D, Pisani A, Bernardi G (1999) Sodium influx plays a major role in the membrane depolarization induced by oxygen and glucose deprivation in rat striatal spiny neurons. Stroke 30:171-179.
12. Calabresi P, Centonze D, Bernardi G (2000) Cellular factors controlling neuronal vulnerability in the brain: a lesson from the striatum. Neurology 55:1249-1255.
13. Centonze D, Marfia GA, Pisani A, Picconi B, Giacomini P, Bernardi G, Calabresi P (2001) Ionic mechanisms underlying differential vulnerability to ischemia in striatal neurons. Prog Neurobiol 63:687-696.
14. 2 is a novel, endogenous modulator of synaptic dopamine release. J Neurophysiol 85:2468-2476.
15. + channels in pancreatic β-cells. Nature 311:271-273.
16. Cragg SJ (2003) Variable dopamine release probability and short-term plasticity between functional domains of the primate striatum. J Neurosci 23:4378-4385.
17. 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.
18. Dauer W, Przedborski S (2003) Parkinson's disease: mechanisms and models. Neuron 39:889-909.
19. Davey GP, Clark JB (1996) Threshold effects and control of oxidative phosphorylation in nonsynaptic rat brain mitochondria. J Neurochem 66:1617-1624.
20. Dawson TM, Dawson VL (2003) Molecular pathways of neurodegeneration in Parkinson's disease. Science 302:819-822.
21. Di Monte DA (2003) The environment and Parkinson's disease: is the nigrostriatal system preferentially targeted by neurotoxins? Lancet Neurol 2:531-538.
22. Ferrante RJ, Schulz JB, Kowall NW, Beal MF (1997) Systemic administration of rotenone produces selective damage in the striatum and globus pallidus, but not in the substantia nigra. Brain Res 753:157-162.
23. Fiskum G, Starkov A, Polster BM, Chinopoulos C (2003) Mitochondrial mechanisms of neural cell death and neuroprotective interventions in Parkinson's disease. Ann NY Acad Sci 991:111-119.
24. Fleming SM, Zhu C, Fernagut PO, Mehta A, DiCarlo CD, Seaman RL, Chesselet MF (2004) Behavioral and immunohistochemical effects of chronic intravenous and subcutaneous infusions of varying doses of rotenone. Exp Neurol 187:418-429.
25. + in rat brain synaptosomes and mitochondria. Brain Res 975:214-221.
26. Greenamyre JT, Sherer TB, Betarbet R, Panov AV (2001) Complex I and Parkinson's disease. IUBMB Life 52:135-141.
27. Greenamyre JT, Betarbet R, Sherer TB (2003) The rotenone model of Parkinson's disease: genes, environment and mitochondria. Parkinsonism Relat Disord 9 [Suppl 2]:S59-S64.
28. Gyulkhandanyan AV, Pennefather PS (2004) Shift in the localization of sites of hydrogen peroxide production in brain mitochondria by mitochondrial stress. J Neurochem 90:405-421.
29. Hill K, Benham CD, McNulty S, Randall AD (2004) Flufenamic acid is a pH-dependent antagonist of TRPM2 channels. Neuropharmacology 47:450-460.
30. Höglinger GU, Feger J, Prigent A, Michel PP, Parain K, Champy P, Ruberg M, Oertel WH, Hirsch EC (2003) Chronic systemic complex I inhibition induces a hypokinetic multisystem degeneration in rats. J Neurochem 84:491-502.
31. 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.
32. Kemp JM, Powell TP (1971) The structure of the caudate nucleus of the cat: light and electron microscopy. Philos Trans R Soc Lond B Biol Sci 262:383-401.
33. Koós T, Tepper JM (1999) Inhibitory control of neostriatal projection neurons by GABAergic interneurons. Nat Neurosci 2:467-472.
34. 2 with stimulus-secretion coupling in mouse pancreatic β-cells. J Physiol (Lond) 514:471-481.
35. Kudin AP, Bimpong-Buta NY, Vielhaber S, Elger CE, Kunz WS (2004) Characterization of superoxide-producing sites in isolated brain mitochondria. J Biol Chem 279:4127-4135.
36. Kwong LK, Sohal RS (1998) Substrate and site specificity of hydrogen peroxide generation in mouse mitochondria. Arch Biochem Biophys 350:118-126.
37. 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.
38. McNulty S, Fonfria E (2005) The role of TRPM channels in cell death. Pflügers Arch, in press.
39. Moran MM, Xu H, Clapham DE (2004) TRP ion channels in the nervous system. Curr Opin Neurobiol 14:362-369.
40. Nirenberg MJ, Chan J, Liu Y, Edwards RH, Pickel VM (1997) Vesicular monoamine transporter-2: immunogold localization in striatal axons and terminals. Synapse 26:194-198.
41. Nisenbaum ES, Wilson CJ (1995) Potassium currents responsible for inward and outward rectification in rat neostriatal spiny projection neurons. J Neurosci 15:4449-4463.
42. + channels in cardiac muscle. Nature 305:147-148.
43. Olanow CW, Tatton WG (1999) Etiology and pathogenesis of Parkinson's disease. Annu Rev Neurosci 22:123-144.
44. Orth M, Schapira AH (2002) Mitochondrial involvement in Parkinson's disease. Neurochem Int 40:533-541.
45. Parker Jr WD, Boyson SJ, Parks JK (1989) Abnormalities of the electron transport chain in idiopathic Parkinson's disease. Ann Neurol 26:719-723.
46. 2+ permeable cation channels: from gene to biological function. Cell Calcium 33:519-531.
47. 2 in biomembranes. Biochem Biophys Acta 694:69-93.
48. 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.
49. Rice ME, Cragg SJ (2004) Nicotine amplifies reward-related dopamine signals in striatum. Nat Neurosci 7:583-584.
50. Rice ME, Nicholson C (1991) Diffusion characteristics and extracellular volume fraction during normoxia and hypoxia in slices of rat neostriatum. J Neurophysiol 65:264-272.
51. Rice ME, Russo-Menna I (1998) Differential compartmentalization of brain ascorbate and glutathione between neurons and glia. Neuroscience 82:1213-1223.
52. Sah R, Schwartz-Bloom RD (1999) Optical imaging reveals elevated intracellular chloride in hippocampal pyramidal cells after oxidative stress. J Neurosci 19:9209-9217.
53. Saulle E, Gubellini P, Picconi B, Centonze D, Tropepi D, Pisani A, Morari M, Marti M, Rossi L, Papa M, Bernardi G, Calabresi P (2004) Neuronal vulnerability following inhibition of mitochondrial complex II: a possible ionic mechanism for Huntington's disease. Mol Cell Neurosci 25:9-20.
54. 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.
55. Schapira AH, Cooper JM, Dexter D, Clark JB, Jenner P, Marsden CD (1990) Mitochondrial complex I deficiency in Parkinson's disease. J Neurochem 54:823-827.
56. ATP-channel on the somata of spiny neurones in rat caudate nucleus: regulation by drugs and nucleotides. Br J Pharmacol 121:193-198.
57. + channel in spiny neurons of rat caudate nucleus. Pflügers Arch 427:187-189.
58. Sherer TB, Kim JH, Betarbet R, Greenamyre JT (2003a) Subcutaneous rote-none exposure causes highly selective dopaminergic degeneration and alpha-synuclein aggregation. Exp Neurol 179:9-16.
59. Sherer TB, Betarbet R, Testa CM, Seo BB, Richardson JR, Kim JH, Miller GW, Yagi T, Matsuno-Yagi A, Greenamyre JT (2003b) Mechanism of toxicity in rotenone models of Parkinson's disease. J Neurosci 23:10756-10764.
60. Sipos I, Tretter L, Adam-Vizi V (2003) Quantitative relationship between inhibition of respiratory complexes and formation of reactive oxygen species in isolated nerve terminals. J Neurochem 84:112-118.
61. Smith AD, Bolam JP (1990) The neural network of the basal ganglia as revealed by the study of synaptic connections of identified neurons. Trends Neurosci 13:259-265.
62. Smith MA, Herson PS, Lee K, Pinnock RD, Ashford ML (2003) Hydrogen-peroxide-induced toxicity of rat striatal neurones involves activation of a non-selective cation channel. J Physiol (Lond) 547:417-425.
63. Sonsalla PK, Manzino L, Sinton CM, Liang CL, German DC, Zeevalk GD (1997) Inhibition of striatal energy metabolism produces cell loss in the ipsilateral substantia nigra. Brain Res 773:223-226.
64. Testa CM, Sherer TB, Greenamyre JT (2005) Rotenone induces oxidative stress and dopaminergic neuron damage in organotypic substantia nigra cultures. Mol Brain Res 134:109-118.
65. Tretter L, Sipos I, Adam-Vizi V (2004) Initiation of neuronal damage by complex I deficiency and oxidative stress in Parkinson's disease. Neurochem Res 29:569-577.
66. Valente EM, Abou-Sleiman PM, Caputo V, Muqit MM, Harvey K, Gispert S, Ali Z, Del Turco D, Bentivoglio AR, Healy DG, Albanese A, Nussbaum R, Gonzalez-Maldonado R, Deller T, Salvi S, Cortelli P, Gilks WP, Latchman DS, Harvey RJ, Dallapiccola B, et al. (2004) Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science 304:1158-1160.
67. m-Dependent and -independent production of reactive oxygen species by rat brain mitochondria. J Neurochem 79:266-277.
68. Witkovsky P, Nicholson C, Rice ME, Bohmaker K, Meller E (1993) Extracellular dopamine concentration in the retina of the clawed frog, Xenopus laevis. Proc Natl Acad Sci USA 90:5667-5671.
69. Zeevalk GD, Bernard LP, Song C, Gluck M, Ehrhart J (2005) Mitochondrial inhibition and oxidative stress: reciprocating players in neurodegeneration. Antioxid Redox Signal 7:1117-1139.
70. Zhang Y, Dawson VL, Dawson TM (2000) Oxidative stress and genetics in the pathogenesis of Parkinson's disease. Neurobiol Dis 7:240-250.
71. Zhu ZT, Munhall A, Shen KZ, Johnson SW (2005) NMDA enhances a depolarization-activated inward current in subthalamic neurons. Neuropharmacology 49:317-327.
72. Zigmond MJ, Abercrombie ED, Berger TW, Grace AA, Stricker EM (1990) Compensations after lesions of central dopaminergic neurons: some clinical and basic implications. Trends Neurosci 13:290-296.