Decreased striatal dopamine release underlies increased expression of long-term synaptic potentiation at corticostriatal synapses 24 h after 3-nitropropionic-acid-induced chemical hypoxia

Journal of Neuroscience

Volumn 28, Issue 38, 2008, Pages 9585-9597

  Akopian, Garnik ^a   Crawford, Cynthia ^c   Beal, M Flint ^d   Cappelletti, Maurand ^a   Jakowec, Michael W ^b   Petzinger, Giselle M ^b   Zheng, Ling ^b   Gheorghe, Stacey L ^c   Reichel, Carmela M ^c   Chow, Robert ^b   Walsh, John P ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c CALIFORNIA STATE UNIVERSITY   (United States)

^d WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

D1; D2; LTD; LTP; NMDA; Voltammetry

Indexed keywords

3 NITROPROPIONIC ACID; AMPA RECEPTOR; DIZOCILPINE; DOPAMINE; DOPAMINE RECEPTOR; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID; TYROSINE 3 MONOOXYGENASE;

ANIMAL TISSUE; ARTICLE; BEHAVIOR; BRAIN HYPOXIA; CONTROLLED STUDY; CYCLIC POTENTIOMETRY; DYSTONIA; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LONG TERM POTENTIATION; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SYNAPTIC POTENTIAL;

ANIMALS; CEREBRAL CORTEX; CONVULSANTS; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; DOPAMINE; DOPAMINE AGONISTS; DOWN-REGULATION; GLUTAMIC ACID; HYPOXIA, BRAIN; LONG-TERM POTENTIATION; MALE; MOVEMENT; NEURAL PATHWAYS; NEUROTOXINS; NITRO COMPOUNDS; PROPIONIC ACIDS; RATS; RATS, INBRED F344; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; SPECIES SPECIFICITY; SYNAPTIC TRANSMISSION; TIME FACTORS; UP-REGULATION;

EID: 58149339617     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5698-07.2008     Document Type: Article

References (82)

1. Akopian G, Walsh JP (2006) Reduced expression of short- and long-term facilitation at aged corticostriatal synapses. Synapse 60:223-238.
2. Akopian G, Musleh W, Smith R, Walsh JP (2000) Functional state of presynaptic terminals influences the expression of short- and long-term plasticity at corticostriatal synapses. Synapse 38:271-280.
3. Ariano MA, Monsma FJ Jr, Barton AC, Kang HC, Haugland RP, Sibley DR (1989) Direct visualization and cellular localization of D1 and D2 dopamine receptors in rat forebrain by use of fluorescent ligands. Proc Natl Acad Sci U S A 86:8570-8574.
4. Aspey BS, Cohen S, Patel Y, Terruli M, Harrison MJ (1998) Middle cerebral artery occlusion in the rat: consistent protocol for a model of stroke. Neuropathol Appl Neurobiol 24:487-497.
5. Aspey BS, Taylor FL, Terruli M, Harrison MJ (2000) Temporary middle cerebral artery occlusion in the rat: consistent protocol for a model of stroke and reperfusion. Neuropathol Appl Neurobiol 26:232-242.
6. Beal MF (1994) Neurochemistry and toxin models in Huntington's disease. Curr Opin Neurol 7:542-547.
7. Beal MF, Brouillet E, Jenkins B, Henshaw R, Rosen B, Hyman BT (1993a) Age-dependent striatal excitotoxic lesions produced by the endogenous mitochondrial inhibitor malonate. J Neurochem 61:1147-1150.
8. Beal MF, Brouillet E, Jenkins BG, Ferrante RJ, Kowall NW, Miller JM, Storey E, Srivastava R, Rosen BR, Hyman BT (1993b) Neurochemical and histologic characterization of striatal excitotoxic lesions produced by the mitochondrial toxin 3-nitropropionic acid. J Neurosci 13:4181-4192.
9. Blum D, Galas MC, Gall D, Cuvelier L, Schiffmann SN (2002) Striatal and cortical neurochemical changes induced by chronic metabolic compromise in the 3-nitropropionic model of Huntington's disease. Neurobiol Dis 10:410-426.
10. Blum D, Galas MC, Cuvelier L, Schiffmann SN (2004) Chronic intoxication with 3-nitropropionic acid in rats induces the loss of striatal dopamine terminals without affecting nigral cell viability. Neurosci Lett 354:234-238.
11. Bogdanov MB, Ferrante RJ, Kuemmerle S, Klivenyi P, Beal MF (1998) Increased vulnerability to 3-nitropropionic acid in an animal model of Huntington's disease. J Neurochem 71:2642-2644.
12. Borgland SL, Malenka RC, Bonci A (2004) Acute and chronic cocaine-induced potentiation of synaptic strength in the ventral tegmental area: electrophysiological and behavioral correlates in individual rats. J Neurosci 24:7482-7490.
13. Borlongan CV, Koutouzis TK, Randall TS, Freeman TB, Cahill DW, Sanberg PR (1995) Systemic 3-nitropropionic acid: behavioral deficits and striatal damage in adult rats. Brain Res Bull 36:549-556.
14. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 72:248-254.
15. Burke RE, Franklin SO, Inturrisi CE (1994) (1994) Acute and persistent suppression of preproenkephalin mRNA expression in the striatum following developmental hypoxic-ischemic injury. J Neurochem 62:1878-1886.
16. Calabresi P, Maj R, Pisani A, Mercuri NB, Bernardi G (1992) Long-term synaptic depression in the striatum: physiological and pharmacological characterization. J Neurosci 12:4224-4233.
17. Calabresi P, Centonze D, Gubellini P, Bernardi G (1999) Activation of M1-like muscarinic receptors is required for the induction of corticostriatal LTP. Neuropharmacology 38:323-326.
18. Calabresi P, Gubellini P, Picconi B, Centonze D, Pisani A, Bonsi P, Greengard P, Hipskind RA, Borrelli E, Bernardi G (2001) Inhibition of mitochondrial complex II induces a long-term potentiation of NMDA-mediated synaptic excitation in the striatum requiring endogenous dopamine. J Neurosci 21:5110-5120.
19. Calabresi P, Centonze D, Pisani A, Cupini L, Bernardi G (2003) Synaptic plasticity in the ischaemic brain. Lancet Neurol 2:622-629.
20. Callaway JK, Lawrence AJ, Jarrott B (2003) AM-36, a novel neuroprotective agent, profoundly reduces reactive oxygen species formation and dopamine release in the striatum of conscious rats after endothelin-1-induced middle cerebral artery occlusion. Neuropharmacol 44:787-800.
21. Carmichael ST (2005) Rodent models of focal stroke: size, mechanism, and purpose. NeuroRx 2:396-409.
22. Centonze D, Gubellini P, Picconi B, Calabresi P, Giacomini P, Bernardi G (1999) Unilateral dopamine denervation blocks corticostriatal LTP. J Neurophysiol 82:3575-3579.
23. Centonze D, Picconi B, Gubellini P, Bernardi G, Calabresi P (2001a) Dopaminergic control of synaptic plasticity in the dorsal striatum. Eur J Neurosci 13:1071-1077.
24. Centonze D, Saulle E, Bernardi G, Calabresi P (2001b) Receptor and postreceptor mechanisms of ischemic long-term potentiation in the striatum. Functional Neurology 16:149-152.
25. Coleman GL, Barthold W, Osbaldiston GW, Foster SJ, Jonas AM (1977) Pathological changes during aging in barrier-reared Fischer 344 male rats. J Gerontol 32:258-278.
26. Cragg SJ, Greenfield SA (1997) Differential autoreceptor control of somatodendritic and axon terminal dopamine release in substantia nigra, ventral tegmental area, and striatum. J Neurosci 17:5738-5746.
27. Crawford CA, Zavala AR, Karper PE, McDougall SA (2000) Long-term effects of postnatal amphetamine treatment on striatal protein kinase A activity, dopamine D(1)-like and D(2)-like binding sites, and dopamine content. Neurotoxicol Teratol 22:799-804.
28. Dalbem A, Silveira CV, Pedroso MF, Breda RV, Werne Baes CV, Bartmann AP, da Costa JC (2005) Altered distribution of striatal activity-dependent synaptic plasticity in the 3-nitropropionic acid model of Huntington's disease. Brain Res 1047:148-158.
29. Dos Santos Villar F, Walsh JP (1999) Modulation of long-term synaptic plasticity at corticostriatal synapses. Neuroscience 90:1031-1041.
30. Fancellu R, Armentero MT, Nappi G, Blandini F (2003) Neuroprotective effects mediated by dopamine receptor agonists against malonate-induced lesion in the rat striatum. Neurol Sci 24:180-181.
31. Fernagut PO, Diguet E, Jaber M, Bioulac B, Tison F (2002) Dopamine transporter knock-out mice are hypersensitive to 3-nitropropionic acid-induced striatal damage. Eur J Neurosci 15:2053-2056.
32. Ferriero DM, Arcavi LJ, Sagar SM, McIntosh TK, Simon RP (1988) Selective sparing of NADPH-diaphorase neurons in neonatal hypoxia-ischemia. Ann Neurol 24:670-676.
33. Flores-Hernández J, Cepeda C, Hernández-Echeagaray E, Calvert CR, Jokel ES, Fienberg AA, Greengard P, Levine MS (2002) Dopamine enhancement of NMDA currents in dissociated medium-sized striatal neurons: role of D1 receptors and DARPP-32. J Neurophysiol 88:3010-3020.
34. Friedemann MN, Gerhardt GA (1992) Regional effects of aging on dopaminergic function in the Fisher-344 rat. Neurobiol Aging 13:325-332.
35. Golden WC, Brambrink AM, Traystman RJ, Shaffner DH, Martin LJ (2003) Nitration of the striatal Na,K-ATPase alpha3 isoform occurs in normal brain development but is not increased during hypoxia-ischemia in newborn piglets. Neurochem Res 28:1883-1889.
36. Gu W, Zhao H, Yenari MA, Sapolsky RM, Steinberg GK (2004) Catalase over-expression protects striatal neurons from transient focal cerebral ischemia. Neuroreport 15:413-416.
37. Gubellini P, Centonze D, Tropepi D, Bernardi G, Calabresi P (2004) Induction of corticostriatal LTP by 3-nitropropionic acid requires the activation of mGluR1/PKC pathway. Neuropharmacol 46:761-769.
38. Gurden H, Takita M, Jay TM (2000) Essential role of D1 but not D2 receptors in the NMDA receptor-dependent long-term potentiation at hippocampal-prefrontal cortex synapses in vivo. J Neurosci 20:RC106.
39. Hamilton BF, Gould DH (1987) Nature and distribution of brain lesions in rats intoxicated with 3-nitropropionic acid: a type of hypoxic (energy deficient) brain damage. Acta Neuropathol 72:286-297.
40. Hashimoto N, Matsumoto T, Mabe H, Hashitani T, Nishino H (1994) Dopamine has inhibitory and accelerating effects on ischemia-induced neuronal cell damage in the rat striatum. Brain Res Bull 33:281-288.
41. Huang YY, Kandel ER (1995) D1/D5 receptor agonists induce a protein synthesis-dependent late potentiation in the CA1 region of the hippocampus. Proc Natl Acad Sci U S A 92:2446-2450.
42. Kerr JN, Wickens JR (2001) Dopamine D-1/D-5 receptor activation is required for long-term potentiation in the rat neostriatum in vitro. J Neurophysiol 85:117-124.
43. Kim GW, Chan PH (2002) Involvement of superoxide in excitotoxicity and DNA fragmentation in striatal vulnerability in mice after treatment with the mitochondrial toxin, 3-nitropropionic acid. J Cereb Blood Flow Metab 22:798-809.
44. Kim GW, Copin JC, Kawase M, Chen SF, Sato S, Gobbel GT, Chan PH (2000) Excitotoxicity is required for induction of oxidative stress and apoptosis in mouse striatum by the mitochondrial toxin, 3-nitropropionic acid. J Cereb Blood Flow Metab 20:119-129.
45. Klivenyi P, Andreassen OA, Ferrante RJ, Dedeoglu A, Mueller G, Lancelot E, Bogdanov M, Andersen JK, Jiang D, Beal MF (2000) Mice deficient in cellular glutathione peroxidase show increased vulnerability to malonate, 3-nitropropionic acid, and 1-methyl-4-phenyl-1,2,5,6-tetrahydropyridine. J Neurosci 20:1-7.
46. Koutouzis TK, Borlongan CV, Scorcia T, Creese I, Cahill DW, Freeman TB, Sanberg PR (1994) Systemic 3-nitropropionic acid: long-term effects on locomotor behavior. Brain Res 646:242-246.
47. Kreitzer AC, Malenka RC (2007) Endocannabinoid-mediated rescue of striatal LTD and motor deficits in Parkinson's disease models. Nature 445:643-647.
48. Lancelot E, Callebert J, Revaud ML, Boulu RG, Plotkine M (1995) Detection of hydroxyl radicals in rat striatum during transient focal cerebral ischemia: possible implication in tissue damage. Neurosci Lett 197:85-88.
49. Liu X, Luo X, Hu W (1992) Studies on the epidemiology and etiology of moldy sugarcane poisoning in China. Biomed Environ Sci 5:161-177.
50. Lowry OH, Rosenbrough NG, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 93:265-275.
51. Ludolph AC, He F, Spencer PS, Hammerstad J, Sabri M (1991) 3-Nitropropionic acid-exogenous animal neurotoxin and possible human striatal toxin. Can J Neurolog Sci 18:492-498.
52. Maeno H (1982) Dopamine receptors in canine caudate nucleus. Mol Cell Biochem 43:65-80.
53. Marti M, Mela F, Ulazzi L, Hanau S, Stocchi S, Paganini F, Beani L, Bianchi C, Morari M (2003) Differential responsiveness of rat striatal nerve endings to the mitochondrial toxin 3-nitropropionic acid: implications for Huntington's disease. Eur J Neurosci 18:759-767.
54. McLin JP, Thompson LM, Steward O (2006) Differential susceptibility to striatal neurodegeneration induced by quinolinic acid and kainate in inbred, outbred and hybrid mouse strains. Eur J Neurosci 24:3134-3140.
55. Miles PR, Mundorf ML, Wightman RM (2002) Release and uptake of catecholamines in the bed nucleus of the stria terminalis measured in the mouse brain slice. Synapse 44:188-197.
56. Ming L (1995) Moldy sugarcane poisoning - a case report with a brief review. J Toxicol Clin Toxicol 33:363-367.
57. Nakao N, Nakai E, Nakai K, Itakura T (1999) Ablation of the subthalamic nucleus supports the survival of nigral dopaminergic neurons after nigrostriatal lesions induced by the mitochondrial toxin 3-nitropropionic acid. Ann Neurol 45:640-651.
58. Newcomb JD, Brown WD, Rodriguez AI, Garbuzova-Davis S, Saporta S, Sanberg PR, Willing AE (2005) Behavioral alterations in Lewis rats following two-day continuous 3-nitropropionic acid administration. Neurotox Res 8:259-266.
59. Nishino H, Hida H, Kumazaki M, Shimano Y, Nakajima K, Shimizu H, Ooiwa T, Baba H (2000) The striatum is the most vulnerable region in the brain to mitochondrial energy compromise: a hypothesis to explain its specific vulnerability. J Neurotrauma 17:251-260.
60. Otani S, Daniel H, Roisin MP, Crepel F (2003) Dopaminergic modulation of long-term synaptic plasticity in rat prefrontal neurons. Cereb Cortex 13:1251-1256.
61. Otmakhova NA, Lisman JE (1996) D1/D5 dopamine receptor activation increases the magnitude of early long-term potentiation at CA1 hippocampal synapses. J Neurosci 16:7478-7486.
62. Ouary S, Bizat N, Altairac S, Ménétrat H, Mittoux V, Condé F, Hantraye P, Brouillet E (2000) Major strain differences in response to chronic systemic administration of the mitochondrial toxin 3-nitropropionic acid in rats: implications for neuroprotection studies. Neuroscience 97:521-530.
63. Pang ZP, Ling GY, Gajendiran M, Xu ZC (2002) Asymmetrical changes of excitatory synaptic transmission in dopamine-denervated striatum after transient forebrain ischemia. Neuroscience 114:317-326.
64. Partridge JG, Tang KC, Lovinger DM (2000) Regional and postnatal heterogeneity of activity-dependent long-term changes in synaptic efficacy in the dorsal striatum. J Neurophysiol 84:1422-1429.
65. Patel J, Rice ME (2006) Monitoring dopamine release in brain slices. In: Encyclopedia of sensors (Grimes CA, Dickey EC, Pishko MV, eds), pp 313-334. Stevenson Ranch, CA: American Scientific.
66. Petzinger GM, Walsh JP, Akopian G, Hogg E, Abernathy A, Arevalo P, Turnquist P, Vucković M, Fisher BE, Togasaki DM, Jakowec MW (2007) Effects of treadmill exercise on dopaminergic transmission in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-(MPTP)-lesioned mouse model of basal ganglia injury. J Neurosci 27:5291-5300.
67. Picconi B, Passino E, Sgobio C, Bonsi P, Barone I, Ghiglieri V, Pisani A, Bernardi G, Ammassari-Teule M, Calabresi P (2006) Plastic and behavioral abnormalities in experimental Huntington's disease: a crucial role for cholinergic interneurons. Neurobiol Dis 22:143-152.
68. Reynolds DS, Carter RJ, Morton AJ (1998) Dopamine modulates the susceptibility of striatal neurons to 3-nitropropionic acid in the rat model of Huntington's disease. J Neurosci 18:10116-10127.
69. Reynolds JN, Wickens JR (2002) Dopamine-dependent plasticity of corticostriatal synapses. Neural Netw 15:507-521.
70. Reynolds JN, Hyland BI, Wickens JR (2001) A cellular mechanism of reward-related learning. Nature 413:67-70.
71. Rice ME, Cragg SJ, Greenfield SA (1997) Characteristics of electrically evoked somatodendritic release in substanitia nigra and ventral tegmental area in vitro. J Neurophysiol 77:853-862.
72. Schauwecker PE (2005) Susceptibility to excitotoxic and metabolic striatal neurodegeneration in the mouse is genotype dependent. Brain Res 1040:112-120.
73. Schulte A, Chow RH (1996) A simple method for insulating carbon-fiber microelectrodes using anodic electrophoretic deposition of paint. Anal Chem 68:3054-3058.
74. Simpson JR, Isacson O (1993) Mitochondrial impairment reduces the threshold for in vivo NMDA-mediated neuronal death in the striatum. Exp Neurol 121:57-64.
75. Smith R, Musleh W, Akopian W, Buckwalter G, Walsh JP (2001) Regional differences in the expression of corticostriatal synaptic plasticity. Neuroscience 106:95-101.
76. Ste-Marie L, Vachon P, Vachon L, Bémeur C, Guertin MC, Montgomery J (2000) Hydroxyl radical production in the cortex and striatum in a rat model of focal cerebral ischemia. Can J Neurol Sci 27:152-159.
77. Thomas MJ, Beurrier C, Bonci A, Malenka RC (2001) Long-term depression in the nucleus accumbens: a neural correlate of behavioral sensitization to cocaine. Nature Neurosci 4:1217-1223.
78. Toner CC, Stamford JA (1999) Effects of metabolic alterations on dopamine release in an in vitro model of neostriatal ischaemia. Brain Res Bull 48:395-399.
79. Tozzi A, Costa C, Di Filippo M, Tantucci M, Siliquini S, Belcastro V, Parnetti L, Picconi B, Calabresi P (2007) Memantine reduces neuronal dysfunctions triggered by in vitro ischemia and 3-nitropropionic acid. Exp Neurol 207:218-226.
80. Trantham-Davidson H, Neely LC, Lavin A, Seamans JK (2004) Mechanisms underlying differential D1 versus D2 dopamine receptor regulation of inhibition in prefrontal cortex. J Neurosci 24:10652-10659.
81. Wang Z, Kai L, Day M, Ronesi J, Yin HH, Ding J, Tkatch T, Lovinger DM, Surmeier DJ (2006) Dopaminergic control of corticostriatal long-term synaptic depression in medium spiny neurons is mediated by cholinergic interneurons. Neuron 50:443-452.
82. Wüllner U, Young AB, Penney JB, Beal MF (1994) 3-Nitropropionic acid toxicity in the striatum. J Neurochem 63:1772-1781