Potential for targeting dopamine/DARPP-32 signaling in neuropsychiatric and neurodegenerative disorders

References

• Greengard P, Allen PB, Nairn AC. Beyond the dopamine receptor: the DARPP-32/protein phosphatase-1 cascade. Neuron. 1999;23:435–447.
   PubMed Web of Science ®Google Scholar
• Svenningsson P, Nishi A, Fisone G, et al. DARPP-32: an integrator of neurotransmission. Annu Rev Pharmacol Toxicol. 2004;44:269–296.
   PubMed Web of Science ®Google Scholar
• Walaas SI, Hemmings HC Jr., Greengard P, et al. Beyond the dopamine receptor: regulation and roles of serine/threonine protein phosphatases. Front Neuroanat. 2011;5:50.
   PubMed Web of Science ®Google Scholar
• Yger M, Girault JA. DARPP-32, Jack of all trades … Master of which? Front Behav Neurosci. 2011;5:56.
   PubMed Web of Science ®Google Scholar
• Bateup HS, Svenningsson P, Kuroiwa M, et al. Cell type-specific regulation of DARPP-32 phosphorylation by psychostimulant and antipsychotic drugs. Nat Neurosci. 2008;11:932–939.
   PubMed Web of Science ®Google Scholar
• Bibb JA, Snyder GL, Nishi A, et al. Phosphorylation of DARPP-32 by Cdk5 modulates dopamine signalling in neurons. Nature. 1999;402:669–671. P-Thr75.
   PubMed Web of Science ®Google Scholar
• Girault JA, Hemmings HC Jr., Williams KR, et al. Phosphorylation of DARPP-32, a dopamine- and cAMP-regulated phosphoprotein, by casein kinase II. J Biol Chem. 1989;264:21748–21759.
   PubMed Web of Science ®Google Scholar
• Desdouits F, Cohen D, Nairn AC, et al. Phosphorylation of DARPP-32, a dopamine- and cAMP-regulated phosphoprotein, by casein kinase I in vitro and in vivo. J Biol Chem. 1995;270:8772–8778.
   PubMed Web of Science ®Google Scholar
• Nishi A, Bibb JA, Snyder GL, et al. Amplification of dopaminergic signaling by a positive feedback loop. Proc Natl Acad Sci USA. 2000;97:12840–12845.
   PubMed Web of Science ®Google Scholar
• Ahn JH, McAvoy T, Rakhilin SV, et al. Protein kinase A activates protein phosphatase 2A by phosphorylation of the B56delta subunit. Proc Natl Acad Sci USA. 2007;104:2979–2984.
   PubMed Web of Science ®Google Scholar
• Stipanovich A, Valjent E, Matamales M, et al. A phosphatase cascade by which rewarding stimuli control nucleosomal response. Nature. 2008;453:879–884.
   PubMed Web of Science ®Google Scholar
• Engmann O, Giralt A, Gervasi N, et al. DARPP-32 interaction with adducin may mediate rapid environmental effects on striatal neurons. Nat Commun. 2015;6:10099.
   PubMed Web of Science ®Google Scholar
• Desdouits F, Siciliano JC, Greengard P, et al. Dopamine- and cAMP-regulated phosphoprotein DARPP-32: phosphorylation of Ser-137 by casein kinase I inhibits dephosphorylation of Thr-34 by calcineurin. Proc Natl Acad Sci USA. 1995;92:2682–2685.
   PubMed Web of Science ®Google Scholar
• Yamada K, Takahashi S, Karube F, et al. Neuronal circuits and physiological roles of the basal ganglia in terms of transmitters, receptors and related disorders. J Physiol Sci. 2016;66:435–446.
   PubMed Web of Science ®Google Scholar
• Nishi A, Snyder GL, Greengard P. Bidirectional regulation of DARPP-32 phosphorylation by dopamine. J Neurosci. 1997;17:8147–8155.
   PubMed Web of Science ®Google Scholar
• Hemmings HC Jr., Greengard P, Tung HY, et al. DARPP-32, a dopamine-regulated neuronal phosphoprotein, is a potent inhibitor of protein phosphatase-1. Nature. 1984;310:503–505.
   PubMed Web of Science ®Google Scholar
• King MM, Huang CY, Chock PB, et al. Mammalian brain phosphoproteins as substrates for calcineurin. J Biol Chem. 1984;259:8080–8083.
   PubMed Web of Science ®Google Scholar
• Desdouits F, Siciliano JC, Nairn AC, et al. Dephosphorylation of Ser-137 in DARPP-32 by protein phosphatases 2A and 2C: different roles in vitro and in striatonigral neurons. Biochem J. 1998;330(Pt 1):211–216.
   PubMed Web of Science ®Google Scholar
• Ahn JH, Sung JY, McAvoy T, et al. The B’’/PR72 subunit mediates Ca2+-dependent dephosphorylation of DARPP-32 by protein phosphatase 2A. Proc Natl Acad Sci USA. 2007;104:9876–9881.
   PubMed Web of Science ®Google Scholar
• Nishi A. Glutamate counteracts dopamine/PKA signaling via dephosphorylation of DARPP-32 Ser97 and alteration of its cytonuclear distribution. J Biol Chem. 2017. DOI:10.1074/jbc.M116.752402
   PubMed Web of Science ®Google Scholar
• Alexander GE, Crutcher MD. Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci. 1990;13:266–271.
   PubMed Web of Science ®Google Scholar
• DeLong MR. Primate models of movement disorders of basal ganglia origin. Trends Neurosci. 1990;13:281–285.
   PubMed Web of Science ®Google Scholar
• Smith RJ, Lobo MK, Spencer S, et al. Cocaine-induced adaptations in D1 and D2 accumbens projection neurons (a dichotomy not necessarily synonymous with direct and indirect pathways). Curr Opin Neurobiol. 2013;23:546–552.
   PubMed Web of Science ®Google Scholar
• Fienberg AA, Hiroi N, Mermelstein PG, et al. DARPP-32: regulator of the efficacy of dopaminergic neurotransmission. Science. 1998;281:838–842.
   PubMed Web of Science ®Google Scholar
• Svenningsson P, Tzavara ET, Carruthers R, et al. Diverse psychotomimetics act through a common signaling pathway. Science. 2003;302:1412–1415.
   PubMed Web of Science ®Google Scholar
• Bateup HS, Santini E, Shen W, et al. Distinct subclasses of medium spiny neurons differentially regulate striatal motor behaviors. Proc Natl Acad Sci USA. 2010;107:14845–14850.
   PubMed Web of Science ®Google Scholar
• Walaas SI, Aswad DW, Greengard P. A dopamine- and cyclic AMP-regulated phosphoprotein enriched in dopamine-innervated brain regions. Nature. 1983;301:69–71.
   PubMed Web of Science ®Google Scholar
• Nairn AC, Svenningsson P, Nishi A, et al. The role of DARPP-32 in the actions of drugs of abuse. Neuropharmacology. 2004;47(Suppl 1):14–23.
   PubMed Web of Science ®Google Scholar
• Benavides DR, Bibb JA. Role of Cdk5 in drug abuse and plasticity. Ann NY Acad Sci. 2004;1025:335–344.
   PubMed Web of Science ®Google Scholar
• Svenningsson P, Nairn AC, Greengard P. DARPP-32 mediates the actions of multiple drugs of abuse. AAPS J. 2005;7:E353–60.
   PubMed Web of Science ®Google Scholar
• Borgkvist A, Fisone G. Psychoactive drugs and regulation of the cAMP/PKA/DARPP-32 cascade in striatal medium spiny neurons. Neurosci Biobehav Rev. 2007;31:79–88.
   PubMed Web of Science ®Google Scholar
• Scheggi S, Raone A, De Montis MG, et al. Behavioral expression of cocaine sensitization in rats is accompanied by a distinct pattern of modifications in the PKA/DARPP-32 signaling pathway. J Neurochem. 2007;103:1168–1183.
   PubMed Web of Science ®Google Scholar
• Zachariou V, Sgambato-Faure V, Sasaki T, et al. Phosphorylation of DARPP-32 at Threonine-34 is required for cocaine action. Neuropsychopharmacology. 2006;31:555–562.
   PubMed Web of Science ®Google Scholar
• Hiroi N, Fienberg AA, Haile CN, et al. Neuronal and behavioural abnormalities in striatal function in DARPP-32-mutant mice. Eur J Neurosci. 1999;11:1114–1118.
   PubMed Web of Science ®Google Scholar
• Kelz MB, Chen J, Carlezon WA Jr., et al. Expression of the transcription factor deltaFosB in the brain controls sensitivity to cocaine. Nature. 1999;401:272–276.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Nestler EJ. Molecular basis of long-term plasticity underlying addiction. Nat Rev Neurosci. 2001;2:119–128.
   PubMed Web of Science ®Google Scholar
• Valjent E, Pascoli V, Svenningsson P, et al. Regulation of a protein phosphatase cascade allows convergent dopamine and glutamate signals to activate ERK in the striatum. Proc Natl Acad Sci USA. 2005;102:491–496.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Svenningsson P, Picetti R, et al. Cocaine self-administration in mice is inversely related to phosphorylation at Thr34 (protein kinase A site) and Ser130 (kinase CK1 site) of DARPP-32. J Neurosci. 2006;26:2645–2651.
   PubMed Web of Science ®Google Scholar
• Zachariou V, Benoit-Marand M, Allen PB, et al. Reduction of cocaine place preference in mice lacking the protein phosphatase 1 inhibitors DARPP 32 or Inhibitor 1. Biol Psychiatry. 2002;51:612–620.
   PubMed Web of Science ®Google Scholar
• Cervo L, Samanin R. Effects of dopaminergic and glutamatergic receptor antagonists on the acquisition and expression of cocaine conditioning place preference. Brain Res. 1995;673:242–250.
   PubMed Web of Science ®Google Scholar
• Graham DL, Hoppenot R, Hendryx A, et al. Differential ability of D1 and D2 dopamine receptor agonists to induce and modulate expression and reinstatement of cocaine place preference in rats. Psychopharmacology (Berl). 2007;191:719–730.
   PubMed Web of Science ®Google Scholar
• Tropea TF, Kosofsky BE, Rajadhyaksha AM. Enhanced CREB and DARPP-32 phosphorylation in the nucleus accumbens and CREB, ERK, and GluR1 phosphorylation in the dorsal hippocampus is associated with cocaine-conditioned place preference behavior. J Neurochem. 2008;106:1780–1790.
   PubMed Web of Science ®Google Scholar
• Brami-Cherrier K, Valjent E, Herve D, et al. Parsing molecular and behavioral effects of cocaine in mitogen- and stress-activated protein kinase-1-deficient mice. J Neurosci. 2005;25:11444–11454.
   PubMed Web of Science ®Google Scholar
• Girault JA, Valjent E, Caboche J, et al. ERK2: a logical AND gate critical for drug-induced plasticity? Curr Opin Pharmacol. 2007;7:77–85.
   PubMed Web of Science ®Google Scholar
• Miller CA, Marshall JF. Molecular substrates for retrieval and reconsolidation of cocaine-associated contextual memory. Neuron. 2005;47:873–884.
   PubMed Web of Science ®Google Scholar
• Bertran-Gonzalez J, Bosch C, Maroteaux M, et al. Opposing patterns of signaling activation in dopamine D1 and D2 receptor-expressing striatal neurons in response to cocaine and haloperidol. J Neurosci. 2008;28:5671–5685.
   PubMed Web of Science ®Google Scholar
• Sulzer D. How addictive drugs disrupt presynaptic dopamine neurotransmission. Neuron. 2011;69:628–649.
   PubMed Web of Science ®Google Scholar
• Sitte HH, Freissmuth M. Amphetamines, new psychoactive drugs and the monoamine transporter cycle. Trends Pharmacol Sci. 2015;36:41–50.
   PubMed Web of Science ®Google Scholar
• Chen PC, Chen JC. Enhanced Cdk5 activity and p35 translocation in the ventral striatum of acute and chronic methamphetamine-treated rats. Neuropsychopharmacology. 2005;30:538–549.
   PubMed Web of Science ®Google Scholar
• Ehrman LA, Williams MT, Schaefer TL, et al. Phosphodiesterase 1B differentially modulates the effects of methamphetamine on locomotor activity and spatial learning through DARPP32-dependent pathways: evidence from PDE1B-DARPP32 double-knockout mice. Genes Brain Behav. 2006;5:540–551.
   PubMed Web of Science ®Google Scholar
• Gerfen CR, Paletzki R, Worley P. Differences between dorsal and ventral striatum in Drd1a dopamine receptor coupling of dopamine- and cAMP-regulated phosphoprotein-32 to activation of extracellular signal-regulated kinase. J Neurosci. 2008;28:7113–7120.
   PubMed Web of Science ®Google Scholar
• Johnson SW, North RA. Opioids excite dopamine neurons by hyperpolarization of local interneurons. J Neurosci. 1992;12:483–488.
   PubMed Web of Science ®Google Scholar
• Bourdy R, Barrot M. A new control center for dopaminergic systems: pulling the VTA by the tail. Trends Neurosci. 2012;35:681–690.
   PubMed Web of Science ®Google Scholar
• Borgkvist A, Usiello A, Greengard P, et al. Activation of the cAMP/PKA/DARPP-32 signaling pathway is required for morphine psychomotor stimulation but not for morphine reward. Neuropsychopharmacology. 2007;32:1995–2003.
   PubMed Web of Science ®Google Scholar
• Lindskog M, Svenningsson P, Fredholm B, et al. Mu- and delta-opioid receptor agonists inhibit DARPP-32 phosphorylation in distinct populations of striatal projection neurons. Eur J Neurosci. 1999;11:2182–2186.
   PubMed Web of Science ®Google Scholar
• Valjent E, Bertran-Gonzalez J, Aubier B, et al. Mechanisms of locomotor sensitization to drugs of abuse in a two-injection protocol. Neuropsychopharmacology. 2010;35:401–415.
   PubMed Web of Science ®Google Scholar
• Scheggi S, Rauggi R, Gambarana C, et al. Dopamine and cyclic AMP-regulated phosphoprotein-32 phosphorylation pattern in cocaine and morphine-sensitized rats. J Neurochem. 2004;90:792–799.
   PubMed Web of Science ®Google Scholar
• Nye HE, Nestler EJ. Induction of chronic Fos-related antigens in rat brain by chronic morphine administration. Mol Pharmacol. 1996;49:636–645.
   PubMed Web of Science ®Google Scholar
• Zachariou V, Bolanos CA, Selley DE, et al. An essential role for DeltaFosB in the nucleus accumbens in morphine action. Nat Neurosci. 2006;9:205–211.
   PubMed Web of Science ®Google Scholar
• Pareek TK, Kulkarni AB. Cdk5: a new player in pain signaling. Cell Cycle. 2006;5:585–588.
   PubMed Web of Science ®Google Scholar
• Beaudry H, Mercier-Blais AA, Delaygue C, et al. Regulation of mu and delta opioid receptor functions: involvement of cyclin-dependent kinase 5. Br J Pharmacol. 2015;172:2573–2587.
   PubMed Web of Science ®Google Scholar
• Kuribara H, Uchihashi Y. Dopamine antagonists can inhibit methamphetamine sensitization, but not cocaine sensitization, when assessed by ambulatory activity in mice. J Pharm Pharmacol. 1993;45:1042–1045.
   PubMed Web of Science ®Google Scholar
• Kuribara H, Uchihashi Y. Effects of dopamine antagonism on methamphetamine sensitization: evaluation by ambulatory activity in mice. Pharmacol Biochem Behav. 1994;47:101–106.
   PubMed Web of Science ®Google Scholar
• Moro H, Sato H, Ida I, et al. Effects of SKF-38393, a dopamine D1 receptor agonist on expression of amphetamine-induced behavioral sensitization and expression of immediate early gene arc in prefrontal cortex of rats. Pharmacol Biochem Behav. 2007;87:56–64.
   PubMed Web of Science ®Google Scholar
• Hirabayashi M, Tadokoro S. Effect of chlorpromazine on mouse ambulatory activity sensitization caused by (+)-amphetamine. J Pharm Pharmacol. 1993;45:481–483.
   PubMed Web of Science ®Google Scholar
• Futamura T, Akiyama S, Sugino H, et al. Aripiprazole attenuates established behavioral sensitization induced by methamphetamine. Prog Neuropsychopharmacol Biol Psychiatry. 2010;34:1115–1119.
   PubMed Web of Science ®Google Scholar
• Li Y, White FJ, Wolf ME. Pharmacological reversal of behavioral and cellular indices of cocaine sensitization in the rat. Psychopharmacology (Berl). 2000;151:175–183.
   PubMed Web of Science ®Google Scholar
• Shuto T, Kuroiwa M, Hamamura M, et al. Reversal of methamphetamine-induced behavioral sensitization by repeated administration of a dopamine D1 receptor agonist. Neuropharmacology. 2006;50:991–997.
   PubMed Web of Science ®Google Scholar
• Shuto T, Seeman P, Kuroiwa M, et al. Repeated administration of a dopamine D1 receptor agonist reverses the increased proportions of striatal dopamine D1High and D2High receptors in methamphetamine-sensitized rats. Eur J Neurosci. 2008;27:2551–2557.
   PubMed Web of Science ®Google Scholar
• Barrett AC, Miller JR, Dohrmann JM, et al. Effects of dopamine indirect agonists and selective D1-like and D2-like agonists and antagonists on cocaine self-administration and food maintained responding in rats. Neuropharmacology. 2004;47(Suppl 1):256–273.
   PubMed Web of Science ®Google Scholar
• Caine SB, Negus SS, Mello NK, et al. Effects of dopamine D(1-like) and D(2-like) agonists in rats that self-administer cocaine. J Pharmacol Exp Ther. 1999;291:353–360.
   PubMed Web of Science ®Google Scholar
• Self DW, Barnhart WJ, Lehman DA, et al. Opposite modulation of cocaine-seeking behavior by D1- and D2-like dopamine receptor agonists. Science. 1996;271:1586–1589.
   PubMed Web of Science ®Google Scholar
• Pascoli V, Turiault M, Luscher C. Reversal of cocaine-evoked synaptic potentiation resets drug-induced adaptive behaviour. Nature. 2012;481:71–75.
   Web of Science ®Google Scholar
• Bonito-Oliva A, DuPont C, Madjid N, et al. Involvement of the striatal medium spiny neurons of the direct pathway in the motor stimulant effects of phencyclidine. Int J Neuropsychopharmacol. 2016;16:pyv134.
   PubMed Web of Science ®Google Scholar
• Levesque D, Rouillard C. Nur77 and retinoid X receptors: crucial factors in dopamine-related neuroadaptation. Trends Neurosci. 2007;30:22–30.
   PubMed Web of Science ®Google Scholar
• Sanchez N, Coura R, Engmann O, et al. Haloperidol-induced Nur77 expression in striatopallidal neurons is under the control of protein phosphatase 1 regulation by DARPP-32. Neuropharmacology. 2014;79:559–566.
   PubMed Web of Science ®Google Scholar
• Albert KA, Hemmings HC Jr., Adamo AI, et al. Evidence for decreased DARPP-32 in the prefrontal cortex of patients with schizophrenia. Arch Gen Psychiatry. 2002;59:705–712.
   PubMed Web of Science ®Google Scholar
• Ishikawa M, Mizukami K, Iwakiri M, et al. Immunohistochemical and immunoblot analysis of Dopamine and cyclic AMP-regulated phosphoprotein, relative molecular mass 32,000 (DARPP-32) in the prefrontal cortex of subjects with schizophrenia and bipolar disorder. Prog Neuropsychopharmacol Biol Psychiatry. 2007;31:1177–1181.
   PubMed Web of Science ®Google Scholar
• Kunii Y, Ikemoto K, Wada A, et al. Detailed DARPP-32 expression profiles in postmortem brains from patients with schizophrenia: an immunohistochemical study. Med Mol Morphol. 2011;44:190–199.
   PubMed Web of Science ®Google Scholar
• Feldcamp LA, Souza RP, Romano-Silva M, et al. Reduced prefrontal cortex DARPP-32 mRNA in completed suicide victims with schizophrenia. Schizophr Res. 2008;103:192–200.
   PubMed Web of Science ®Google Scholar
• Torres KC, Souza BR, Miranda DM, et al. The leukocytes expressing DARPP-32 are reduced in patients with schizophrenia and bipolar disorder. Prog Neuropsychopharmacol Biol Psychiatry. 2009;33:214–219.
   PubMed Web of Science ®Google Scholar
• Zhan L, Kerr JR, Lafuente MJ, et al. Altered expression and coregulation of dopamine signalling genes in schizophrenia and bipolar disorder. Neuropathol Appl Neurobiol. 2011;37:206–219.
   PubMed Web of Science ®Google Scholar
• Baracskay KL, Haroutunian V, Meador-Woodruff JH. Dopamine receptor signaling molecules are altered in elderly schizophrenic cortex. Synapse. 2006;60:271–279.
   PubMed Web of Science ®Google Scholar
• Cui Y, Prabhu V, Nguyen TB, et al. The mRNA expression status of dopamine receptor D2, dopamine receptor D3 and DARPP-32 in T lymphocytes of patients with early psychosis. Int J Mol Sci. 2015;16:26677–26686.
   PubMed Web of Science ®Google Scholar
• Souza BR, Motta BS, Rosa DV, et al. DARPP-32 and NCS-1 expression is not altered in brains of rats treated with typical or atypical antipsychotics. Neurochem Res. 2008;33:533–538.
   PubMed Web of Science ®Google Scholar
• Grebb JA, Girault JA, Ehrlich M, et al. Chronic treatment of rats with SCH-23390 or raclopride does not affect the concentrations of DARPP-32 or its mRNA in dopamine-innervated brain regions. J Neurochem. 1990;55:204–207.
   PubMed Web of Science ®Google Scholar
• Souza BR, Torres KC, Miranda DM, et al. Lack of effects of typical and atypical antipsychotics in DARPP-32 and NCS-1 levels in PC12 cells overexpressing NCS-1. J Negat Results Biomed. 2010;9:4.
   PubMedGoogle Scholar
• Romero E, Ali C, Molina-Holgado E, et al. Neurobehavioral and immunological consequences of prenatal immune activation in rats. Influence of antipsychotics. Neuropsychopharmacology. 2007;32:1791–1804.
   PubMed Web of Science ®Google Scholar
• Paterlini M, Zakharenko SS, Lai WS, et al. Transcriptional and behavioral interaction between 22q11.2 orthologs modulates schizophrenia-related phenotypes in mice. Nat Neurosci. 2005;8:1586–1594.
   PubMed Web of Science ®Google Scholar
• Cantrup R, Sathanantham K, Rushlow WJ, et al. Chronic hyperdopaminergic activity of schizophrenia is associated with increased DeltaFosB levels and cdk-5 signaling in the nucleus accumbens. Neuroscience. 2012;222:124–135.
   PubMed Web of Science ®Google Scholar
• Powell KJ, Binder TL, Hori S, et al. Neonatal ventral hippocampal lesions produce an elevation of DeltaFosB-like protein(s) in the rodent neocortex. Neuropsychopharmacology. 2006;31:700–711.
   PubMed Web of Science ®Google Scholar
• Yabuki Y, Nakagawasai O, Moriguchi S, et al. Decreased CaMKII and PKC activities in specific brain regions are associated with cognitive impairment in neonatal ventral hippocampus-lesioned rats. Neuroscience. 2013;234:103–115.
   PubMed Web of Science ®Google Scholar
• Le Pen G, Moreau JL. Disruption of prepulse inhibition of startle reflex in a neurodevelopmental model of schizophrenia: reversal by clozapine, olanzapine and risperidone but not by haloperidol. Neuropsychopharmacology. 2002;27:1–11.
   PubMed Web of Science ®Google Scholar
• Alquicer G, Silva-Gomez AB, Peralta F, et al. Neonatal ventral hippocampus lesion alters the dopamine content in the limbic regions in postpubertal rats. Int J Dev Neurosci. 2004;22:103–111.
   PubMed Web of Science ®Google Scholar
• Kuroiwa M, Snyder GL, Shuto T, et al. Phosphodiesterase 4 inhibition enhances the dopamine D1 receptor/PKA/DARPP-32 signaling cascade in frontal cortex. Psychopharmacology (Berl). 2012;219:1065–1079.
   PubMed Web of Science ®Google Scholar
• Nishi A, Kuroiwa M, Miller DB, et al. Distinct roles of PDE4 and PDE10A in the regulation of cAMP/PKA signaling in the striatum. J Neurosci. 2008;28:10460–10471.
   PubMed Web of Science ®Google Scholar
• Heckman PR, Van Duinen MA, Bollen EP, et al. Phosphodiesterase inhibition and regulation of dopaminergic frontal and striatal functioning: clinical implications. Int J Neuropsychopharmacol. 2016;19:pyw030.
   PubMed Web of Science ®Google Scholar
• Robichaud A, Stamatiou PB, Jin SL, et al. Deletion of phosphodiesterase 4D in mice shortens alpha(2)-adrenoceptor-mediated anesthesia, a behavioral correlate of emesis. J Clin Invest. 2002;110:1045–1052.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Brown AM, Deutch AY, Colbran RJ. Dopamine depletion alters phosphorylation of striatal proteins in a model of Parkinsonism. Eur J Neurosci. 2005;22:247–256.
   PubMed Web of Science ®Google Scholar
• Kuroiwa M, Hamada M, Hieda E, et al. Muscarinic receptors acting at pre- and post-synaptic sites differentially regulate dopamine/DARPP-32 signaling in striatonigral and striatopallidal neurons. Neuropharmacology. 2012;63:1248–1257.
   PubMed Web of Science ®Google Scholar
• Santini E, Feyder M, Gangarossa G, et al. Dopamine- and cAMP-regulated phosphoprotein of 32-kDa (DARPP-32)-dependent activation of extracellular signal-regulated kinase (ERK) and mammalian target of rapamycin complex 1 (mTORC1) signaling in experimental parkinsonism. J Biol Chem. 2012;287:27806–27812.
   PubMed Web of Science ®Google Scholar
• Meurers BH, Dziewczapolski G, Shi T, et al. Dopamine depletion induces distinct compensatory gene expression changes in DARPP-32 signal transduction cascades of striatonigral and striatopallidal neurons. J Neurosci. 2009;29:6828–6839.
   PubMed Web of Science ®Google Scholar
• Yamamura Y, Morigaki R, Kasahara J, et al. Dopamine signaling negatively regulates striatal phosphorylation of Cdk5 at tyrosine 15 in mice. Front Cell Neurosci. 2013;7:12.
   PubMed Web of Science ®Google Scholar
• Yabuki Y, Ohizumi Y, Yokosuka A, et al. Nobiletin treatment improves motor and cognitive deficits seen in MPTP-induced Parkinson model mice. Neuroscience. 2014;259:126–141.
   PubMed Web of Science ®Google Scholar
• Fabbrini G, Brotchie JM, Grandas F, et al. Levodopa-induced dyskinesias. Mov Disord. 2007;22:1379-89; quiz 523.
   Web of Science ®Google Scholar
• Aubert I, Guigoni C, Hakansson K, et al. Increased D1 dopamine receptor signaling in levodopa-induced dyskinesia. Ann Neurol. 2005;57:17–26.
   PubMed Web of Science ®Google Scholar
• Murer MG, Moratalla R. Striatal signaling in L-DOPA-induced dyskinesia: common mechanisms with drug abuse and long term memory involving D1 dopamine receptor stimulation. Front Neuroanat. 2011;5:51.
   PubMed Web of Science ®Google Scholar
• Feyder M, Bonito-Oliva A, Fisone G. L-DOPA-induced dyskinesia and abnormal signaling in striatal medium spiny neurons: focus on dopamine D1 receptor-mediated transmission. Front Behav Neurosci. 2011;5:71.
   PubMed Web of Science ®Google Scholar
• Santini E, Valjent E, Usiello A, et al. Critical involvement of cAMP/DARPP-32 and extracellular signal-regulated protein kinase signaling in L-DOPA-induced dyskinesia. J Neurosci. 2007;27:6995–7005.
   PubMed Web of Science ®Google Scholar
• Santini E, Valjent E, Fisone G. Parkinson’s disease: levodopa-induced dyskinesia and signal transduction. FEBS J. 2008;275:1392–1399.
   PubMed Web of Science ®Google Scholar
• Santini E, Valjent E, Fisone G. mTORC1 signaling in Parkinson’s disease and L-DOPA-induced dyskinesia: a sensitized matter. Cell Cycle. 2010;9:2713–2718.
   PubMed Web of Science ®Google Scholar
• Guigoni C, Doudnikoff E, Li Q, et al. Altered D(1) dopamine receptor trafficking in parkinsonian and dyskinetic non-human primates. Neurobiol Dis. 2007;26:452–463.
   PubMed Web of Science ®Google Scholar
• Herve D, Levi-Strauss M, Marey-Semper I, et al. G(olf) and Gs in rat basal ganglia: possible involvement of G(olf) in the coupling of dopamine D1 receptor with adenylyl cyclase. J Neurosci. 1993;13:2237–2248.
   PubMed Web of Science ®Google Scholar
• Corvol JC, Muriel MP, Valjent E, et al. Persistent increase in olfactory type G-protein alpha subunit levels may underlie D1 receptor functional hypersensitivity in Parkinson disease. J Neurosci. 2004;24:7007–7014.
   PubMed Web of Science ®Google Scholar
• Alcacer C, Santini E, Valjent E, et al. Galpha(olf) mutation allows parsing the role of cAMP-dependent and extracellular signal-regulated kinase-dependent signaling in L-3,4-dihydroxyphenylalanine-induced dyskinesia. J Neurosci. 2012;32:5900–5910.
   PubMed Web of Science ®Google Scholar
• Berthet A, Porras G, Doudnikoff E, et al. Pharmacological analysis demonstrates dramatic alteration of D1 dopamine receptor neuronal distribution in the rat analog of L-DOPA-induced dyskinesia. J Neurosci. 2009;29:4829–4835.
   PubMed Web of Science ®Google Scholar
• Bordet R, Ridray S, Carboni S, et al. Induction of dopamine D3 receptor expression as a mechanism of behavioral sensitization to levodopa. Proc Natl Acad Sci USA. 1997;94:3363–3367.
   PubMed Web of Science ®Google Scholar
• Guillin O, Diaz J, Carroll P, et al. BDNF controls dopamine D3 receptor expression and triggers behavioural sensitization. Nature. 2001;411:86–89.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Rangel-Barajas C, Silva I, Lopez-Santiago LM, et al. L-DOPA-induced dyskinesia in hemiparkinsonian rats is associated with up-regulation of adenylyl cyclase type V/VI and increased GABA release in the substantia nigra reticulata. Neurobiol Dis. 2011;41:51–61.
   PubMed Web of Science ®Google Scholar
• Lebel M, Chagniel L, Bureau G, et al. Striatal inhibition of PKA prevents levodopa-induced behavioural and molecular changes in the hemiparkinsonian rat. Neurobiol Dis. 2010;38:59–67.
   PubMed Web of Science ®Google Scholar
• Pavon N, Martin AB, Mendialdua A, et al. ERK phosphorylation and FosB expression are associated with L-DOPA-induced dyskinesia in hemiparkinsonian mice. Biol Psychiatry. 2006;59:64–74.
   PubMed Web of Science ®Google Scholar
• Santini E, Alcacer C, Cacciatore S, et al. L-DOPA activates ERK signaling and phosphorylates histone H3 in the striatonigral medium spiny neurons of hemiparkinsonian mice. J Neurochem. 2009;108:621–633.
   PubMed Web of Science ®Google Scholar
• Oh JD, Chartisathian K, Ahmed SM, et al. Cyclic AMP responsive element binding protein phosphorylation and persistent expression of levodopa-induced response alterations in unilateral nigrostriatal 6-OHDA lesioned rats. J Neurosci Res. 2003;72:768–780.
   PubMed Web of Science ®Google Scholar
• Sodersten E, Feyder M, Lerdrup M, et al. Dopamine signaling leads to loss of Polycomb repression and aberrant gene activation in experimental parkinsonism. Plos Genet. 2014;10:e1004574.
   PubMed Web of Science ®Google Scholar
• Schuster S, Nadjar A, Guo JT, et al. The 3-hydroxy-3-methylglutaryl-CoA reductase inhibitor lovastatin reduces severity of L-DOPA-induced abnormal involuntary movements in experimental Parkinson’s disease. J Neurosci. 2008;28:4311–4316.
   PubMed Web of Science ®Google Scholar
• Fasano S, Bezard E, D’Antoni A, et al. Inhibition of Ras-guanine nucleotide-releasing factor 1 (Ras-GRF1) signaling in the striatum reverts motor symptoms associated with L-dopa-induced dyskinesia. Proc Natl Acad Sci USA. 2010;107:21824–21829.
   PubMed Web of Science ®Google Scholar
• Crittenden JR, Cantuti-Castelvetri I, Saka E, et al. Dysregulation of CalDAG-GEFI and CalDAG-GEFII predicts the severity of motor side-effects induced by anti-parkinsonian therapy. Proc Natl Acad Sci USA. 2009;106:2892–2896.
   PubMed Web of Science ®Google Scholar
• Nagai T, Nakamuta S, Kuroda K, et al. Phosphoproteomics of the dopamine pathway enables discovery of Rap1 activation as a reward signal in vivo. Neuron. 2016;89:550–565.
   PubMed Web of Science ®Google Scholar
• Nagai T, Yoshimoto J, Kannon T, et al. Phosphorylation signals in striatal medium spiny neurons. Trends Pharmacol Sci. 2016;37:858–871.
   PubMed Web of Science ®Google Scholar
• Santini E, Heiman M, Greengard P, et al. Inhibition of mTOR signaling in Parkinson’s disease prevents L-DOPA-induced dyskinesia. Sci Signal. 2009;2:ra36.
   PubMed Web of Science ®Google Scholar
• Calabresi P, Gubellini P, Centonze D, et al. Dopamine and cAMP-regulated phosphoprotein 32 kDa controls both striatal long-term depression and long-term potentiation, opposing forms of synaptic plasticity. J Neurosci. 2000;20:8443–8451.
   PubMed Web of Science ®Google Scholar
• Centonze D, Gubellini P, Picconi B, et al. Unilateral dopamine denervation blocks corticostriatal LTP. J Neurophysiol. 1999;82:3575–3579.
   PubMed Web of Science ®Google Scholar
• Calabresi P, Di Filippo M, Ghiglieri V, et al. Levodopa-induced dyskinesias in patients with Parkinson’s disease: filling the bench-to-bedside gap. Lancet Neurol. 2010;9:1106–1117.
   PubMed Web of Science ®Google Scholar
• Fiorentini C, Savoia P, Bono F, et al. The D3 dopamine receptor: from structural interactions to function. Eur Neuropsychopharmacol. 2015;25:1462–1469.
   PubMed Web of Science ®Google Scholar
• Bordet R, Ridray S, Schwartz JC, et al. Involvement of the direct striatonigral pathway in levodopa-induced sensitization in 6-hydroxydopamine-lesioned rats. Eur J Neurosci. 2000;12:2117–2123.
   PubMed Web of Science ®Google Scholar
• Visanji NP, Fox SH, Johnston T, et al. Dopamine D3 receptor stimulation underlies the development of L-DOPA-induced dyskinesia in animal models of Parkinson’s disease. Neurobiol Dis. 2009;35:184–192.
   PubMed Web of Science ®Google Scholar
• Kumar R, Riddle L, Griffin SA, et al. Evaluation of the D3 dopamine receptor selective antagonist PG01037 on L-dopa-dependent abnormal involuntary movements in rats. Neuropharmacology. 2009;56:944–955.
   PubMed Web of Science ®Google Scholar
• van Kampen JM, Stoessl AJ. Effects of oligonucleotide antisense to dopamine D3 receptor mRNA in a rodent model of behavioural sensitization to levodopa. Neuroscience. 2003;116:307–314.
   PubMed Web of Science ®Google Scholar
• Cote SR, Chitravanshi VC, Bleickardt C, et al. Overexpression of the dopamine D3 receptor in the rat dorsal striatum induces dyskinetic behaviors. Behav Brain Res. 2014;263:46–50.
   PubMed Web of Science ®Google Scholar
• Fiorentini C, Busi C, Gorruso E, et al. Reciprocal regulation of dopamine D1 and D3 receptor function and trafficking by heterodimerization. Mol Pharmacol. 2008;74:59–69.
   PubMed Web of Science ®Google Scholar
• Marcellino D, Ferre S, Casado V, et al. Identification of dopamine D1-D3 receptor heteromers. Indications for a role of synergistic D1-D3 receptor interactions in the striatum. J Biol Chem. 2008;283:26016–26025.
   PubMed Web of Science ®Google Scholar
• Guitart X, Navarro G, Moreno E, et al. Functional selectivity of allosteric interactions within G protein-coupled receptor oligomers: the dopamine D1-D3 receptor heterotetramer. Mol Pharmacol. 2014;86:417–429.
   PubMed Web of Science ®Google Scholar
• Bernard V, Normand E, Bloch B. Phenotypical characterization of the rat striatal neurons expressing muscarinic receptor genes. J Neurosci. 1992;12:3591–3600.
   PubMed Web of Science ®Google Scholar
• Yan Z, Flores-Hernandez J, Surmeier DJ. Coordinated expression of muscarinic receptor messenger RNAs in striatal medium spiny neurons. Neuroscience. 2001;103:1017–1024.
   PubMed Web of Science ®Google Scholar
• Shen W, Plotkin JL, Francardo V, et al. M4 muscarinic receptor signaling ameliorates striatal plasticity deficits in models of L-DOPA-induced dyskinesia. Neuron. 2015;88:762–773.
   PubMed Web of Science ®Google Scholar
• Hara M, Fukui R, Hieda E, et al. Role of adrenoceptors in the regulation of dopamine/DARPP-32 signaling in neostriatal neurons. J Neurochem. 2010;113:1046–1059.
   PubMed Web of Science ®Google Scholar
• Dekundy A, Lundblad M, Danysz W, et al. Modulation of L-DOPA-induced abnormal involuntary movements by clinically tested compounds: further validation of the rat dyskinesia model. Behav Brain Res. 2007;179:76–89.
   PubMed Web of Science ®Google Scholar
• Gomez-Mancilla B, Bedard PJ. Effect of nondopaminergic drugs on L-dopa-induced dyskinesias in MPTP-treated monkeys. Clin Neuropharmacol. 1993;16:418–427.
   PubMed Web of Science ®Google Scholar
• Nishikawa T, Tanaka M, Tsuda A, et al. Clonidine therapy for tardive dyskinesia and related syndromes. Clin Neuropharmacol. 1984;7:239–245.
   PubMed Web of Science ®Google Scholar
• Grondin R, Hadj Tahar A, Doan VD, et al. Noradrenoceptor antagonism with idazoxan improves L-dopa-induced dyskinesias in MPTP monkeys. Naunyn Schmiedebergs Arch Pharmacol. 2000;361:181–186.
   PubMed Web of Science ®Google Scholar
• Hemmings HC Jr., Nairn AC, Elliott JI, et al. Synthetic peptide analogs of DARPP-32 (Mr 32,000 dopamine- and cAMP-regulated phosphoprotein), an inhibitor of protein phosphatase-1. Phosphorylation, dephosphorylation, and inhibitory activity. J Biol Chem. 1990;265:20369–20376.
   PubMed Web of Science ®Google Scholar
• Kwon YG, Huang HB, Desdouits F, et al. Characterization of the interaction between DARPP-32 and protein phosphatase 1 (PP-1): DARPP-32 peptides antagonize the interaction of PP-1 with binding proteins. Proc Natl Acad Sci USA. 1997;94:3536–3541.
   PubMed Web of Science ®Google Scholar
• Sotoud H, Borgmeyer U, Schulze C, et al. Development of phosphatase inhibitor-1 peptides acting as indirect activators of phosphatase 1. Naunyn Schmiedebergs Arch Pharmacol. 2015;388:283–293.
   PubMed Web of Science ®Google Scholar
• Heiman M, Schaefer A, Gong S, et al. A translational profiling approach for the molecular characterization of CNS cell types. Cell. 2008;135:738–748.
   PubMed Web of Science ®Google Scholar
• Heiman M, Kulicke R, Fenster RJ, et al. Cell type-specific mRNA purification by translating ribosome affinity purification (TRAP). Nat Protoc. 2014;9:1282–1291.
   PubMed Web of Science ®Google Scholar
• Heiman M, Heilbut A, Francardo V, et al. Molecular adaptations of striatal spiny projection neurons during levodopa-induced dyskinesia. Proc Natl Acad Sci USA. 2014;111:4578–4583.
   PubMed Web of Science ®Google Scholar
• Nishi A, Snyder GL. Advanced research on dopamine signaling to develop drugs for the treatment of mental disorders: biochemical and behavioral profiles of phosphodiesterase inhibition in dopaminergic neurotransmission. J Pharmacol Sci. 2010;114:6–16.
   PubMed Web of Science ®Google Scholar