Dopamine receptor activation reveals a novel, kynurenate-sensitive component of striatal N-methyl-d-aspartate neurotoxicity

Neuroscience

Volumn 148, Issue 1, 2007, Pages 188-197

  Poeggeler, B ^a   Rassoulpour, A ^a   Wu, H Q ^a   Guidetti, P ^a   Roberts, R C ^a   Schwarcz, R ^a  

^a MARYLAND PSYCHIATRIC RESEARCH CENTER   (United States)

Author keywords

amphetamine; astrocyte; basal ganglia; dopamine; kynurenine 3 hydroxylase; quinolinic acid

Indexed keywords

APOMORPHINE; DEXAMPHETAMINE; DOPAMINE RECEPTOR; DOPAMINE RECEPTOR STIMULATING AGENT; GLUTAMATE RECEPTOR; KYNURENIC ACID; KYNURENINE; N METHYL DEXTRO ASPARTIC ACID; OXYGENASE INHIBITOR; RECEPTOR SUBTYPE; TRYPTOPHAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CONTROLLED STUDY; CORPUS STRIATUM; FEMALE; IN VIVO STUDY; METABOLITE; NERVE CELL EXCITABILITY; NERVE CELL LESION; NERVE CELL NECROSIS; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; RAT; SEIZURE;

ANIMALS; ASTROCYTES; CELL DEATH; CORPUS STRIATUM; DOPAMINE; DOPAMINE AGONISTS; EXCITATORY AMINO ACID AGONISTS; FEMALE; GLUTAMIC ACID; HUMANS; KYNURENIC ACID; N-METHYLASPARTATE; NERVE DEGENERATION; NEUROTOXINS; QUINOLINIC ACID; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, DOPAMINE; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 34547669100     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2007.05.033     Document Type: Article

References (81)

1. 3H]SCH 23390 binding to dopamine receptors in vivo in mouse brain. Eur J Pharmacol 146 (1988) 113-120
2. Becquet D., Faudon M., and Hery F. In vivo evidence for an inhibitory glutamatergic control of serotonin release in the cat caudate nucleus: involvement of GABA neurons. Brain Res 519 (1990) 82-88
3. Bernard V., and Bolam J.P. Subcellular and subsynaptic distribution of the NR1 subunit of the NMDA receptor in the neostriatum and globus pallidus of the rat: co-localization at synapses with the GluR2/3 subunit of the AMPA receptor. Eur J Neurosci 10 (1998) 3721-3736
4. Buisson A., Pateau V., Plotkine M., and Boulu R.G. Nigrostriatal pathway modulates striatum vulnerability to quinolinic acid. Neurosci Lett 131 (1991) 257-259
5. Carpenedo R., Pittaluga A., Cozzi A., Attucci S., Galli A., Raiteri M., and Moroni F. Presynaptic kynurenate-sensitive receptors inhibit glutamate release. Eur J Neurosci 13 (2001) 2141-2147
6. Carroll R.C., and Zukin R.S. NMDA-receptor trafficking and targeting: implications for synaptic transmission and plasticity. Trends Neurosci 25 (2002) 571-577
7. Centonze D., Usiello A., Costa C., Picconi B., Erbs E., Bernardi G., Borrelli E., and Calabresi P. Chronic haloperidol promotes corticostriatal long-term potentiation by targeting dopamine D2L receptors. J Neurosci 24 (2004) 8214-8222
8. Choi D.W., Koh J.Y., and Peters S. Pharmacology of glutamate neurotoxicity in cortical cell culture: attenuation by NMDA antagonists. J Neurosci 8 (1988) 185-196
9. Coyle J., and Tsai G. The NMDA receptor glycine modulatory site: a therapeutic target for improving cognition and reducing negative symptoms in schizophrenia. Psychopharmacology (Berl) 174 (2004) 32-38
10. Coyle J.T. Glial metabolites of tryptophan and excitotoxicity: Coming unglued. Exp Neurol 197 (2006) 4-7
11. Dang M.T., Yokoi F., Yin H.H., Lovinger D.M., Wang Y., and Li Y. Disrupted motor learning and long-term synaptic plasticity in mice lacking NMDAR1 in the striatum. Proc Natl Acad Sci U S A 103 (2006) 15254-15259
12. Dunah A.W., and Standaert D.G. Subcellular segregation of distinct heteromeric NMDA glutamate receptors in the striatum. J Neurochem 85 (2003) 935-943
13. Eastman C.L., and Guilarte T.R. The role of hydrogen peroxide in the in vitro cytotoxicity of 3-hydroxykynurenine. Neurochem Res 15 (1990) 1101-1107
14. Fan M.M., and Raymond L.A. N-methyl-d-aspartate (NMDA) receptor function and excitotoxicity in Huntington's disease. Prog Neurobiol 81 (2006) 272-293
15. Fiskum G., Murphy A.N., and Beal M.F. Mitochondria in neurodegeneration: acute ischemia and chronic neurodegenerative diseases. J Cereb Blood Flow Metab 19 (1999) 351-369
16. Foster A.C., Vezzani A., French E.D., and Schwarcz R. Kynurenic acid blocks neurotoxicity and seizures induced in rats by the related brain metabolite quinolinic acid. Neurosci Lett 48 (1984) 273-278
17. Galvan A., Kuwajima M., and Smith Y. Glutamate and GABA receptors and transporters in the basal ganglia: what does their subsynaptic localization reveal about their function?. Neuroscience 143 (2006) 351-375
18. Ganong A.H., and Cotman C.W. Kynurenic acid and quinolinic acid act at N-methyl-D-aspartate receptors in the rat hippocampus. J Pharmacol Exp Ther 236 (1986) 293-299
19. Gardoni F., Picconi B., Ghiglieri V., Polli F., Bagetta V., Bernardi G., Cattabeni F., Di Luca M., and Calabresi P. A critical interaction between NR2B and MAGUK in L-DOPA induced dyskinesia. J Neurosci 26 (2006) 2914-2922
20. Greengard P. The neurobiology of dopamine signaling. Biosci Rep 21 (2001) 247-269
21. Grilli M., Raiteri L., Patti L., Parodi M., Robino F., Raiteri M., and Marchi M. Modulation of the function of presynaptic alpha7 and non-alpha7 nicotinic receptors by the tryptophan metabolites, 5-hydroxyindole and kynurenate in mouse brain. Br J Pharmacol 149 (2006) 724-732
22. Guidetti P., Bates G.P., Graham R.K., Hayden M.R., Leavitt B.R., MacDonald M.E., Slow E.J., Wheeler V.C., Woodman B., and Schwarcz R. Elevated brain 3-hydroxykynurenine and quinolinate levels in Huntington disease mice. Neurobiol Dis 23 (2006) 190-197
23. Guidetti P., and Schwarcz R. 3-Hydroxykynurenine potentiates quinolinate but not NMDA toxicity in the rat striatum. Eur J Neurosci 11 (1999) 3857-3863
24. Guidetti P., and Schwarcz R. 3-Hydroxykynurenine and quinolinate: pathogenic synergism in early grade Huntington's disease?. In: Allegri G., et al. (Ed). Developments in tryptophan and serotonin metabolism (2003), Kluwer Academic Publishers, New York 137-145
25. Hallett P.J., Dunah A.W., Ravenscroft P., Zhou S., Bezard E., Crossman A.R., Brotchie J.M., and Standaert D.G. Alterations of striatal NMDA receptor subunits associated with the development of dyskinesia in the MPTP-lesioned primate model of Parkinson's disease. Neuropharmacology 48 (2005) 503-516
26. Harris C.A., Miranda A.F., Tanguay J.J., Boegman R.J., Beninger R.J., and Jhamandas K. Modulation of striatal quinolinate neurotoxicity by elevation of endogenous brain kynurenic acid. Br J Pharmacol 124 (1998) 391-399
27. Hathway G.J., Humphrey P.P., and Kendrick K.M. Somatostatin release by glutamate in vivo is primarily regulated by AMPA receptors. Br J Pharmacol 134 (2001) 1155-1158
28. Haydon P.G. Glia: listening and talking to the synapse. Nat Rev Neurosci 2 (2001) 185-193
29. Hilmas C., Pereira E.F., Alkondon M., Rassoulpour A., Schwarcz R., and Albuquerque E.X. The brain metabolite kynurenic acid inhibits alpha7 nicotinic receptor activity and increases non-alpha7 nicotinic receptor expression: physiopathological implications. J Neurosci 21 (2001) 7463-7473
30. Jakel R.J., and Maragos W.F. Neuronal cell death in Huntington's disease: a potential role for dopamine. Trends Neurosci 23 (2000) 239-245
31. Kaiser S., and Wonnacott S. Alpha-bungarotoxin-sensitive nicotinic receptors indirectly modulate [(3)H]dopamine release in rat striatal slices via glutamate release. Mol Pharmacol 58 (2000) 312-318
32. Kessler M., Terramani T., Lynch G., and Baudry M. A glycine site associated with N-methyl-D-aspartic acid receptors: characterization and identification of a new class of antagonists. J Neurochem 52 (1989) 1319-1328
33. Khan Z.U., Koulen P., Rubinstein M., Grandy D.K., and Goldman-Rakic P.S. An astroglia-linked dopamine D2-receptor action in prefrontal cortex. Proc Natl Acad Sci U S A 98 (2001) 1964-1969
34. Kiss C., Ceresoli-Borroni G., Guidetti P., Zielke C.L., Zielke H.R., and Schwarcz R. Kynurenate production by cultured human astrocytes. J Neural Transm 110 (2003) 1-14
35. Knauber J., Kischka U., Roth M., Schmidt W.J., Hennerici M., and Fassbender K. Modulation of striatal acetylcholine concentrations by NMDA and the competitive NMDA receptor-antagonist AP-5: an in vivo microdialysis study. J Neural Transm 106 (1999) 35-45
36. Leeson P.D., Baker R., Carling R.W., Curtis N.R., Moore K.W., Williams B.J., Foster A.C., Donald A.E., Kemp J.A., and Marshall G.R. Kynurenic acid derivatives. Structure-activity relationships for excitatory amino acid antagonism and identification of potent and selective antagonists at the glycine site on the N-methyl-D-aspartate receptor. J Med Chem 34 (1991) 1243-1252
37. Lowry O.H., Rosebrough N.J., Farr A.L., and Randall R.J. Protein measurement with the Folin phenol reagent. J Biol Chem 193 (1951) 265-275
38. Marchi M., Risso F., Viola C., Cavazzani P., and Raiteri M. Direct evidence that release-stimulating alpha7* nicotinic cholinergic receptors are localized on human and rat brain glutamatergic axon terminals. J Neurochem 80 (2002) 1071-1078
39. Marti M., Manzalini M., Fantin M., Bianchi C., Della Corte L., and Morari M. Striatal glutamate release evoked in vivo by NMDA is dependent upon ongoing neuronal activity in the substantia nigra, endogenous striatal substance P and dopamine. J Neurochem 93 (2005) 195-205
40. Martineau M., Baux G., and Mothet J.P. D-serine signalling in the brain: friend and foe. Trends Neurosci 29 (2006) 481-491
41. Massieu L., Gomez-Roman N., and Montiel T. In vivo potentiation of glutamate-mediated neuronal damage after chronic administration of the glycolysis inhibitor iodoacetate. Exp Neurol 165 (2000) 257-267
42. Meldrum A., Dunnett S.B., and Everitt B.J. Role of corticostriatal and nigrostriatal inputs in malonate-induced striatal toxicity. Neuroreport 12 (2001) 89-93
43. Moncada S., and Bolanos J.P. Nitric oxide, cell bioenergetics and neurodegeneration. J Neurochem 97 (2006) 1676-1689
44. Monnerie H., Shashidhara S., and Le Roux P.D. Effect of excess extracellular glutamate on dendrite growth from cerebral cortical neurons at 3 days in vitro: Involvement of NMDA receptors. J Neurosci Res 74 (2003) 688-700
45. Moroni F., Russi P., Lombardi G., Beni M., and Carla V. Presence of kynurenic acid in the mammalian brain. J Neurochem 51 (1988) 177-180
46. Nakazawa K., McHugh T.J., Wilson M.A., and Tonegawa S. NMDA receptors, place cells and hippocampal spatial memory. Nat Rev Neurosci 5 (2004) 361-372
47. Nishikawa T. A molecular pharmacological approach to the vulnerability to schizophrenia. Biol Psychiatry 57 (2005) 145S
48. Obrenovitch T.P., and Urenjak J. In vivo assessment of kynurenate neuroprotective potency and quinolinate excitotoxicity. Amino Acids 19 (2000) 299-309
49. Okuda S., Nishiyama N., Saito H., and Katsuki H. Hydrogen peroxide-mediated neuronal cell death induced by an endogenous neurotoxin, 3-hydroxykynurenine. Proc Natl Acad Sci U S A 93 (1996) 12553-12558
50. Olney J.W. The toxic effects of glutamate and related compounds in the retina and the brain. Retina 2 (1982) 341-359
51. Orlando L.R., Alsdorf S.A., Penney Jr. J.B., and Young A.B. The role of group I and group II metabotropic glutamate receptors in modulation of striatal NMDA and quinolinic acid toxicity. Exp Neurol 167 (2001) 196-204
52. Parsons C.G., Danysz W., Quack G., Hartmann S., Lorenz B., Wollenburg C., Baran L., Przegalinski E., Kostowski W., Krzascik P., Chizh B., and Headley P.M. Novel systemically active antagonists of the glycine site of the N-methyl-D-aspartate receptor: electrophysiological, biochemical and behavioral characterization. J Pharmacol Exp Ther 283 (1997) 1264-1275
53. Pittaluga A., Vaccari D., and Raiteri M. The "kynurenate test," a biochemical assay for putative cognition enhancers. J Pharmacol Exp Ther 283 (1997) 82-90
54. Poeggeler B., Pappolla M.A., Hardeland R., Rassoulpour A., Hodgkins P.S., Guidetti P., and Schwarcz R. Indole-3-propionate: a potent hydroxyl radical scavenger in rat brain. Brain Res 815 (1999) 382-388
55. Poeggeler B., Rassoulpour A., Guidetti P., Wu H.Q., and Schwarcz R. Dopaminergic control of kynurenate levels and N-methyl-D-aspartate toxicity in the developing rat striatum. Dev Neurosci 20 (1998) 146-153
56. Radke J.M., Owens M.J., and Nemeroff C.B. The effects of glutamate receptor agonists on neurotensin release using in vivo microdialysis. Eur J Pharmacol 411 (2001) 129-134
57. Rashid A.J., So C.H., Kong M.M., Furtak T., El-Ghundi M., Cheng R., O'Dowd B.F., and George S.R. D1-D2 dopamine receptor heterooligomers with unique pharmacology are coupled to rapid activation of Gq/11 in the striatum. Proc Natl Acad Sci U S A 104 (2007) 654-659
58. Rassoulpour A., Wu H.Q., Ferré S., and Schwarcz R. Nanomolar concentrations of kynurenic acid reduce extracellular dopamine levels in the striatum. J Neurochem 93 (2005) 762-765
59. Rassoulpour A., Wu H.Q., Poeggeler B., and Schwarcz R. Systemic d-amphetamine administration causes a reduction of kynurenic acid levels in rat brain. Brain Res 802 (1998) 111-118
60. Reuss B., Lorenzen A., and Unsicker K. Dopamine and epinephrine, but not serotonin, downregulate dopamine sensitivity in cultured cortical and striatal astroglial cells. Receptors Channels 7 (2001) 441-451
61. Reynolds I.J., and Hastings T.G. Glutamate induces the production of reactive oxygen species in cultured forebrain neurons following NMDA receptor activation. J Neurosci 15 (1995) 3318-3327
62. Rousseau S.J., Jones I.W., Pullar I.A., and Wonnacott S. Presynaptic alpha7 and non-alpha7 nicotinic acetylcholine receptors modulate [3H]d-aspartate release from rat frontal cortex in vitro. Neuropharmacology 49 (2005) 59-72
63. Röver S., Cesura A.M., Huguenin P., Kettler R., and Szente A. Synthesis and biochemical evaluation of N-(4-phenylthiazol-2-yl)benzenesulfonamides as high-affinity inhibitors of kynurenine 3-hydroxylase. J Med Chem 40 (1997) 4378-4385
64. Ryan L.J., Linder J.C., Martone M.E., and Groves P.M. Histological and ultrastructural evidence that D-amphetamine causes degeneration in neostriatum and frontal cortex of rats. Brain Res 518 (1990) 67-77
65. Santamaria A., Jimenez-Capdeville M.E., Camacho A., Rodriguez-Martinez E., Flores A., and Galvan-Arzate S. In vivo hydroxyl radical formation after quinolinic acid infusion into rat corpus striatum. Neuroreport 12 (2001) 2693-2696
66. Sapko M.T., Guidetti P., Yu P., Tagle D.A., Pellicciari R., and Schwarcz R. Endogenous kynurenate controls the vulnerability of striatal neurons to quinolinate: Implications for Huntington's disease. Exp Neurol 197 (2006) 31-40
67. Sauer D., Allegrini P.R., Cosenti A., Pataki A., Amacker H., and Fagg G.E. Characterization of the cerebroprotective efficacy of the competitive NMDA receptor antagonist CGP40116 in a rat model of focal cerebral ischemia: an in vivo magnetic resonance imaging study. J Cereb Blood Flow Metab 13 (1993) 595-602
68. Schell M.J. The N-methyl D-aspartate receptor glycine site and D-serine metabolism: an evolutionary perspective. Philos Trans R Soc Lond B Biol Sci 359 (2004) 943-964
69. Schrattenholz A., and Soskic V. NMDA receptors are not alone: dynamic regulation of NMDA receptor structure and function by neuregulins and transient cholesterol-rich membrane domains leads to disease-specific nuances of glutamate-signalling. Curr Top Med Chem 6 (2006) 663-686
70. Schwarcz R. The kynurenine pathway of tryptophan degradation as a drug target. Curr Opin Pharmacol 4 (2004) 12-17
71. Schwarcz R., Ceresoli-Borroni G., Wu H.Q., Rassoulpour A., Poeggeler B., Hodgkins P.S., and Guidetti P. Modulation and function of kynurenic acid in the immature rat brain. In: Huether G., et al. (Ed). Tryptophan, serotonin, melatonin: Basic aspects and applications (1999), Plenum, New York 113-123
72. Schwarcz R., Fuxe K., Agnati L.F., Hökfelt T., and Coyle J.T. Rotational behaviour in rats with unilateral striatal kainic acid lesions: a behavioural model for studies on intact dopamine receptors. Brain Res 170 (1979) 485-495
73. Schwarcz R., and Pellicciari R. Manipulation of brain kynurenines: glial targets, neuronal effects, and clinical opportunities. J Pharmacol Exp Ther 303 (2002) 1-10
74. So C.H., Varghese G., Curley K.J., Kong M.M., Alijaniaram M., Ji X., Nguyen T., O'Dowd B.F., and George S.R. D1 and D2 dopamine receptors form heterooligomers and cointernalize after selective activation of either receptor. Mol Pharmacol 68 (2005) 568-578
75. Sonsalla P.K., Albers D.S., and Zeevalk G.D. Role of glutamate in neurodegeneration of dopamine neurons in several animal models of parkinsonism. Amino Acids 14 (1998) 69-74
76. Stone T.W., and Perkins M.N. Quinolinic acid: a potent endogenous excitant at amino acid receptors in CNS. Eur J Pharmacol 72 (1981) 411-412
77. Swartz K.J., Matson W.R., MacGarvey U., Ryan E.A., and Beal M.F. Measurement of kynurenic acid in mammalian brain extracts and cerebrospinal fluid by high-performance liquid chromatography with fluorometric and coulometric electrode array detection. Anal Biochem 185 (1990) 363-376
78. Turski W.A., Nakamura M., Todd W.P., Carpenter B.K., Whetsell Jr. W.O., and Schwarcz R. Identification and quantification of kynurenic acid in human brain tissue. Brain Res 454 (1988) 164-169
79. Wang H., and Pickel V.M. Presence of NMDA-type glutamate receptors in cingulate corticostriatal terminals and their postsynaptic targets. Synapse 35 (2000) 300-310
80. Waxman E.A., and Lynch D.R. N-methyl-D-aspartate receptor subtypes: multiple roles in excitotoxicity and neurological disease. Neuroscientist 11 (2005) 37-49
81. Young A.M., and Bradford H.F. N-methyl-D-aspartate releases gamma-aminobutyric acid from rat striatum in vivo: a microdialysis study using a novel preloading method. J Neurochem 60 (1993) 487-492