Increased D1 dopamine receptor signaling in levodopa-induced dyskinesia
Involuntary movements, or dyskinesia, represent a debilitating complication of levodopa therapy for Parkinson's disease. Although changes affecting D1 and D2 dopamine receptors have been studied in association with this condition, no causal relationship has yet been established. Taking advantag...
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| Vydáno v: | Annals of neurology Ročník 57; číslo 1; s. 17 - 26 |
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| Jazyk: | angličtina |
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01.01.2005
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| ISSN: | 0364-5134, 1531-8249 |
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| Abstract | Involuntary movements, or dyskinesia, represent a debilitating complication of levodopa therapy for Parkinson's disease. Although changes affecting D1 and D2 dopamine receptors have been studied in association with this condition, no causal relationship has yet been established. Taking advantage of a monkey brain bank constituted to study levodopa‐induced dyskinesia, we report changes affecting D1 and D2 dopamine receptors within the striatum of normal, parkinsonian, nondyskinetic levodopa‐treated parkinsonian, and dyskinetic levodopa‐treated parkinsonian animals. Whereas D1 receptor expression itself is not related to dyskinesia, D1 sensitivity per D1 receptor measured by D1 agonist‐induced [35S]GTPγS binding is linearly related to dyskinesia. Moreover, the striata of dyskinetic animals show higher levels of cyclin‐dependent kinase 5 (Cdk5) and of the dopamine‐ and cAMP‐regulated phosphoprotein of 32kDa (DARPP‐32). Our data suggest that levodopa‐induced dyskinesia results from increased dopamine D1 receptor–mediated transmission at the level of the direct pathway. Ann Neurol 2004 |
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| AbstractList | Involuntary movements, or dyskinesia, represent a debilitating complication of levodopa therapy for Parkinson's disease. Although changes affecting D(1) and D(2) dopamine receptors have been studied in association with this condition, no causal relationship has yet been established. Taking advantage of a monkey brain bank constituted to study levodopa-induced dyskinesia, we report changes affecting D(1) and D(2) dopamine receptors within the striatum of normal, parkinsonian, nondyskinetic levodopa-treated parkinsonian, and dyskinetic levodopa-treated parkinsonian animals. Whereas D(1) receptor expression itself is not related to dyskinesia, D(1) sensitivity per D(1) receptor measured by D(1) agonist-induced [(35)S]GTPgammaS binding is linearly related to dyskinesia. Moreover, the striata of dyskinetic animals show higher levels of cyclin-dependent kinase 5 (Cdk5) and of the dopamine- and cAMP-regulated phosphoprotein of 32kDa (DARPP-32). Our data suggest that levodopa-induced dyskinesia results from increased dopamine D(1) receptor-mediated transmission at the level of the direct pathway.Involuntary movements, or dyskinesia, represent a debilitating complication of levodopa therapy for Parkinson's disease. Although changes affecting D(1) and D(2) dopamine receptors have been studied in association with this condition, no causal relationship has yet been established. Taking advantage of a monkey brain bank constituted to study levodopa-induced dyskinesia, we report changes affecting D(1) and D(2) dopamine receptors within the striatum of normal, parkinsonian, nondyskinetic levodopa-treated parkinsonian, and dyskinetic levodopa-treated parkinsonian animals. Whereas D(1) receptor expression itself is not related to dyskinesia, D(1) sensitivity per D(1) receptor measured by D(1) agonist-induced [(35)S]GTPgammaS binding is linearly related to dyskinesia. Moreover, the striata of dyskinetic animals show higher levels of cyclin-dependent kinase 5 (Cdk5) and of the dopamine- and cAMP-regulated phosphoprotein of 32kDa (DARPP-32). Our data suggest that levodopa-induced dyskinesia results from increased dopamine D(1) receptor-mediated transmission at the level of the direct pathway. Involuntary movements, or dyskinesia, represent a debilitating complication of levodopa therapy for Parkinson's disease. Although changes affecting D1 and D2 dopamine receptors have been studied in association with this condition, no causal relationship has yet been established. Taking advantage of a monkey brain bank constituted to study levodopa‐induced dyskinesia, we report changes affecting D1 and D2 dopamine receptors within the striatum of normal, parkinsonian, nondyskinetic levodopa‐treated parkinsonian, and dyskinetic levodopa‐treated parkinsonian animals. Whereas D1 receptor expression itself is not related to dyskinesia, D1 sensitivity per D1 receptor measured by D1 agonist‐induced [35S]GTPγS binding is linearly related to dyskinesia. Moreover, the striata of dyskinetic animals show higher levels of cyclin‐dependent kinase 5 (Cdk5) and of the dopamine‐ and cAMP‐regulated phosphoprotein of 32kDa (DARPP‐32). Our data suggest that levodopa‐induced dyskinesia results from increased dopamine D1 receptor–mediated transmission at the level of the direct pathway. Ann Neurol 2004 Involuntary movements, or dyskinesia, represent a debilitating complication of levodopa therapy for Parkinson's disease. Although changes affecting D(1) and D(2) dopamine receptors have been studied in association with this condition, no causal relationship has yet been established. Taking advantage of a monkey brain bank constituted to study levodopa-induced dyskinesia, we report changes affecting D(1) and D(2) dopamine receptors within the striatum of normal, parkinsonian, nondyskinetic levodopa-treated parkinsonian, and dyskinetic levodopa-treated parkinsonian animals. Whereas D(1) receptor expression itself is not related to dyskinesia, D(1) sensitivity per D(1) receptor measured by D(1) agonist-induced [(35)S]GTPgammaS binding is linearly related to dyskinesia. Moreover, the striata of dyskinetic animals show higher levels of cyclin-dependent kinase 5 (Cdk5) and of the dopamine- and cAMP-regulated phosphoprotein of 32kDa (DARPP-32). Our data suggest that levodopa-induced dyskinesia results from increased dopamine D(1) receptor-mediated transmission at the level of the direct pathway. |
| Author | Dovero, Sandra Aubert, Incarnation Bioulac, Bernard H. Guigoni, Céline Barthe, Nicole Håkansson, Kerstin Bloch, Bertrand Li, Qin Bezard, Erwan Gross, Christian E. Fisone, Gilberto |
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| Keywords | Signal transduction Nervous system diseases Central nervous system disease D1 Dopamine receptor Levodopa Neurological disorder Antiparkinson agent Motor control Cerebral disorder Extrapyramidal syndrome Involuntary movement Dyskinesia |
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Arch Neurol 2001; 58: 249-254. Bezard E, Dovero S, Prunier C, et al. Relationship between the appearance of symptoms and the level of nigrostriatal degeneration in a progressive MPTP-lesioned macaque model of Parkinson's disease. J Neurosci 2001; 21: 6853-6861. Graham WC, Sambrook MA, Crossman AR. Differential effect of chronic dopaminergic treatment on dopamine D1 and D2 receptors in the monkey brain in MPTP-induced parkinsonism. Brain Res 1993; 602: 290-303. Picconi B, Centonze D, Hakansson K, et al. Loss of bidirectional striatal synaptic plasticity in L-dopa-induced dyskinesia. Nat Neurosci 2003; 6: 501-506. Rascol O, Brooks DJ, Korczyn AD, et al. A five-year study of the incidence of dyskinesia in patients with early Parkinson's disease who were treated with ropinirole or levodopa. N Engl J Med 2000; 342: 1484-1491. Grandy DK, Marchionni MA, Makam H, et al. Cloning of the cDNA and gene for a human D2 dopamine receptor. Proc Natl Acad Sci U S A 1989; 86: 9762-9766. Aubert I, Ghorayeb I, Normand E, Bloch B. Phenotypical characterization of the neurons expressing the D1 and D2 dopamine receptors in the monkey striatum. J Comp Neurol 2000; 418: 22-32. Craven SE, Bredt DS. PDZ proteins organize synaptic signaling pathways. Cell 1998; 93: 495-498. Muriel MP, Bernard V, Levey AI, et al. Levodopa induces a cytoplasmic localization of D1 dopamine receptors in striatal neurons in Parkinson's disease. Ann Neurol 1999; 46: 103-111. Yahr MD, Duvoisin RC, Hoehn MM, et al. L-Dopa (L-3,4-dihydroxyphenylanine): its clinical effects in parkinsonism. Trans Am Neurol Assoc 1968; 93: 56-63. Walaas SI, Aswaad SW, Greengard P. A dopamine- and cyclic AMP-regulated phosphoprotein enriched in dopamine-innervated brain regions. Nature 1984; 301: 69-71. Gerfen CR, Engber TM, Mahan LC, et al. D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons. Science 1990; 250: 1429-1432. Charpak G, Dominik W, Zaganidis N. Optical imaging of the spatial distribution of β-particles emerging from surfaces. Proc Natl Acad Sci U S A 1989; 86: 1741-1745. Chergui K, Svenningsson P, Greengard P. Cyclin-dependent kinase 5 regulates dopaminergic and glutamatergic transmission in the striatum. Proc Natl Acad Sci USA 2004; 101: 2191-2196. Theler JM, Lakhdar-Ghazal N, Pevet P, et al. Mapping of [3H]vasopressin binding sites in the brain of jerboa (Jaculus orientalis) by an high resolution β-radio imager. J Neurosci Methods 1993; 49: 231-240. Creese I, Burt DR, Snyder SH. Dopamine receptor binding enhancement accompanies lesion-induced behavioral supersensitivity. Science 1977; 197: 596-598. Gross CE, Ravenscroft P, Dovero S, et al. Pattern of levodopa-induced striatal changes is different in normal and MPTP-lesioned mice. J Neurochem 2003; 84: 1246-1255. Shinotoh H, Inoue O, Hirayama K, et al. Dopamine D1 receptors in Parkinson's disease and striatonigral degeneration: a positron emission tomography study. J Neurol Neurosurg Psychiatry 1993; 56: 467-472. Bibb JA, Snyder GL, Nishi A, et al. Phosphorylation of DARPP-32 by Cdk5 modulates dopamine signalling in neurons. Nature 1999; 402: 669-671. Birkmayer W, Hornykiewicz O. The L-dihydroxyphenylalanine (L-dopa) effect in Parkinson's syndrome in man: on the pathogenesis and treatment of Parkinson akinesis. Arch Psychiat Nervenkr 1962; 203: 560-574. Bezard E, Ferry S, Mach U, et al. Attenuation of levodopa-induced dyskinesia by normalizing dopamine D3 receptor function. Nat Med 2003; 9: 762-767. Boraud T, Bezard E, Bioulac B, Gross C. Dopamine agonist-induced dyskinesias are correlated to both firing pattern and frequency alteration of pallidal neurons in the MPTP-treated monkey. Brain 2001; 124: 546-557. Dearry A, Gingrich JA, Falardeau P, et al. Molecular cloning and expression of the gene for a human D1 dopamine receptor. Nature 1990; 347: 72-76. Lee T, Seeman P, Rajput A, et al. Receptor basis for dopaminergic supersensitivity in Parkinson's disease. Nature 1978; 273: 150-151. Bibb JA, Chen J, Taylor JR, et al. Effects of chronic exposure to cocaine are regulated by the neuronal protein Cdk5. Nature 2001; 410: 376-380. Gerfen CR. Molecular effects of dopamine on striatal-projection pathways. Trends Neurosci 1995; 23: S64-S70. Luttrell LM, Lefkowitz RJ. The role of β-arrestins in the termination and transduction of G-protein-coupled receptor signals. J Cell Sci 2002; 115: 455-465. Abercrombie E. Estimation of nuclear population from microtome sections. Anat Rec 1946; 94: 239-247. Brooks DJ, Ibanez V, Sawle GV, et al. Striatal D2 receptor status in patients with Parkinson's disease, striatonigral degeneration, and progressive supranuclear palsy, measured with 11C-raclopride and positron emission tomography. Ann Neurol 1992; 31: 184-192. Birkmayer W, Hornykiewicz O. The L-3,4-dioxyphenylalanine (dopa)-effect in Parkinson-akinesia. Wien klin Wschr 1961; 73: 787-788. Lees AJ. Levodopa substitution: the gold standard. Clin Neuropharmacol 1994; 17: S1-S6 Greengard P, Allen PB, Nairn AC. Beyond the dopamine receptor: the DARPP-32/protein phosphatase-1 cascade. Neuron 1999; 23: 435-447. 2000; 418 2004; 101 1962; 203 2001; 124 1990; 347 1993; 602 1989; 86 1993; 49 1984; 301 1993; 60 1999; 46 1978; 273 1999; 45 1999; 23 2002; 115 1961; 73 1992; 31 1999; 402 2001; 21 1998; 18 2001; 410 1993; 56 1946; 94 2000; 12 2003; 6 1995; 23 2003; 9 2001; 2 2000; 342 1994; 17 1998; 93 2003; 84 1968; 93 2001; 58 1977; 197 1990; 250 |
| References_xml | – reference: Chergui K, Svenningsson P, Greengard P. Cyclin-dependent kinase 5 regulates dopaminergic and glutamatergic transmission in the striatum. Proc Natl Acad Sci USA 2004; 101: 2191-2196. – reference: Lee T, Seeman P, Rajput A, et al. Receptor basis for dopaminergic supersensitivity in Parkinson's disease. Nature 1978; 273: 150-151. – reference: Craven SE, Bredt DS. PDZ proteins organize synaptic signaling pathways. Cell 1998; 93: 495-498. – reference: Birkmayer W, Hornykiewicz O. The L-dihydroxyphenylalanine (L-dopa) effect in Parkinson's syndrome in man: on the pathogenesis and treatment of Parkinson akinesis. Arch Psychiat Nervenkr 1962; 203: 560-574. – reference: Charpak G, Dominik W, Zaganidis N. Optical imaging of the spatial distribution of β-particles emerging from surfaces. Proc Natl Acad Sci U S A 1989; 86: 1741-1745. – reference: Aubert I, Ghorayeb I, Normand E, Bloch B. Phenotypical characterization of the neurons expressing the D1 and D2 dopamine receptors in the monkey striatum. J Comp Neurol 2000; 418: 22-32. – reference: Grandy DK, Marchionni MA, Makam H, et al. Cloning of the cDNA and gene for a human D2 dopamine receptor. Proc Natl Acad Sci U S A 1989; 86: 9762-9766. – reference: Gross CE, Ravenscroft P, Dovero S, et al. Pattern of levodopa-induced striatal changes is different in normal and MPTP-lesioned mice. J Neurochem 2003; 84: 1246-1255. – reference: Graham WC, Sambrook MA, Crossman AR. Differential effect of chronic dopaminergic treatment on dopamine D1 and D2 receptors in the monkey brain in MPTP-induced parkinsonism. Brain Res 1993; 602: 290-303. – reference: Birkmayer W, Hornykiewicz O. The L-3,4-dioxyphenylalanine (dopa)-effect in Parkinson-akinesia. Wien klin Wschr 1961; 73: 787-788. – reference: Bordet R, Ridray S, Schwartz JC, Sokoloff P. Involvement of the direct striatonigral pathway in levodopa-induced sensitization in 6-OHDA-lesioned rats. Eur J Neurosci 2000; 12: 2117-2123. – reference: Rascol O, Brooks DJ, Korczyn AD, et al. A five-year study of the incidence of dyskinesia in patients with early Parkinson's disease who were treated with ropinirole or levodopa. N Engl J Med 2000; 342: 1484-1491. – reference: Brooks DJ, Ibanez V, Sawle GV, et al. Striatal D2 receptor status in patients with Parkinson's disease, striatonigral degeneration, and progressive supranuclear palsy, measured with 11C-raclopride and positron emission tomography. Ann Neurol 1992; 31: 184-192. – reference: Shinotoh H, Inoue O, Hirayama K, et al. Dopamine D1 receptors in Parkinson's disease and striatonigral degeneration: a positron emission tomography study. J Neurol Neurosurg Psychiatry 1993; 56: 467-472. – reference: Abercrombie E. Estimation of nuclear population from microtome sections. 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L-Dopa (L-3,4-dihydroxyphenylanine): its clinical effects in parkinsonism. Trans Am Neurol Assoc 1968; 93: 56-63. – reference: Bezard E, Dovero S, Prunier C, et al. Relationship between the appearance of symptoms and the level of nigrostriatal degeneration in a progressive MPTP-lesioned macaque model of Parkinson's disease. J Neurosci 2001; 21: 6853-6861. – reference: Luttrell LM, Lefkowitz RJ. The role of β-arrestins in the termination and transduction of G-protein-coupled receptor signals. J Cell Sci 2002; 115: 455-465. – reference: Gerfen CR. Molecular effects of dopamine on striatal-projection pathways. Trends Neurosci 1995; 23: S64-S70. – reference: Greengard P, Allen PB, Nairn AC. Beyond the dopamine receptor: the DARPP-32/protein phosphatase-1 cascade. Neuron 1999; 23: 435-447. – reference: Lees AJ. Levodopa substitution: the gold standard. Clin Neuropharmacol 1994; 17: S1-S6 – reference: Picconi B, Centonze D, Hakansson K, et al. 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| Snippet | Involuntary movements, or dyskinesia, represent a debilitating complication of levodopa therapy for Parkinson's disease. Although changes affecting D1 and D2... Involuntary movements, or dyskinesia, represent a debilitating complication of levodopa therapy for Parkinson's disease. Although changes affecting D(1) and... |
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| SubjectTerms | 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine - pharmacology 2,3,4,5-Tetrahydro-7,8-dihydroxy-1-phenyl-1H-3-benzazepine - pharmacology Analysis of Variance Animals Antiparkinson Agents - adverse effects Autoradiography - methods Behavior, Animal Biological and medical sciences Blotting, Western - methods Cyclin-Dependent Kinase 5 Cyclin-Dependent Kinases Degenerative and inherited degenerative diseases of the nervous system. Leukodystrophies. Prion diseases Disease Models, Animal Dopamine and cAMP-Regulated Phosphoprotein 32 Dopamine Plasma Membrane Transport Proteins Dose-Response Relationship, Drug Drug Interactions Drug toxicity and drugs side effects treatment Dyskinesia, Drug-Induced - etiology Dyskinesia, Drug-Induced - metabolism Female Guanosine 5'-O-(3-Thiotriphosphate) - pharmacokinetics Immunohistochemistry - methods In Situ Hybridization - methods Isotopes - pharmacokinetics Levodopa - adverse effects Macaca fascicularis Medical sciences Membrane Glycoproteins - metabolism Membrane Transport Proteins - metabolism Motor Activity - drug effects Nerve Tissue Proteins - metabolism Neurology Nortropanes - pharmacokinetics Parkinsonian Disorders - drug therapy Parkinsonian Disorders - metabolism Parkinsonian Disorders - physiopathology Pharmacology. Drug treatments Phosphoproteins - metabolism Radioligand Assay - methods Receptors, Dopamine D1 - agonists Receptors, Dopamine D1 - genetics Receptors, Dopamine D1 - metabolism Receptors, Dopamine D2 - genetics Receptors, Dopamine D2 - metabolism Signal Transduction - drug effects Substantia Nigra - drug effects Substantia Nigra - metabolism Time Factors Toxicity: nervous system and muscle Tyrosine 3-Monooxygenase - metabolism |
| Title | Increased D1 dopamine receptor signaling in levodopa-induced dyskinesia |
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