Dopamine D1 Receptor-Dependent Trafficking of Striatal NMDA Glutamate Receptors to the Postsynaptic Membrane

Dunah, Anthone W.; Standaert, David G.

doi:10.1523/jneurosci.21-15-05546.2001

Cited by 351 publications

(289 citation statements)

References 61 publications

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“…Previously, our studies showed that stimulation of striatal slices with a D1 agonist or NMDA led to dephosphorylation of WAVE1 at Ser310, Ser397, and Ser441, indicating neuronal activity-mediated stimulation of WAVE1 (4, 7). We anticipated that WAVE1 would be dephosphorylated in response to cocaine administration in vivo, because cocaine increases synaptic levels of dopamine, and activation of D1 is known to increase NMDA-receptor-mediated signaling (13,28,29). However, there was no significant change in phosphorylation, or of the total protein level, of WAVE1 in the striatum in response to acute injection of cocaine (45 min after 15 mg/kg) or chronic injection of cocaine (15 mg/kg daily for 14 d; 45 min after the last injection).…”

Section: Resultsmentioning

confidence: 99%

WAVE1 in neurons expressing the D1 dopamine receptor regulates cellular and behavioral actions of cocaine

Ceglia

Lee

Cahill

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Wiskott-Aldrich syndrome protein (WASP) family verprolin homologous protein 1 (WAVE1) regulates actin-related protein 2/3 (Arp2/3) complex-mediated actin polymerization. Our previous studies have found WAVE1 to be inhibited by Cdk5-mediated phosphorylation in brain and to play a role in the regulation of dendritic spine morphology. Here we report that mice in which WAVE1 was knocked out (KO) in neurons expressing the D1 dopamine receptor (D1-KO), but not mice where WAVE1 was knocked out in neurons expressing the D2 dopamine receptor (D2-KO), exhibited a significant decrease in place preference associated with cocaine. In contrast to wild-type (WT) and WAVE1 D2-KO mice, cocaine-induced sensitized locomotor behavior was not maintained in WAVE1 D1-KO mice. After chronic cocaine administration and following withdrawal, an acute cocaine challenge induced WAVE1 activation in striatum, which was assessed by dephosphorylation. The cocaine-induced WAVE1 dephosphorylation was attenuated by coadministration of either a D1 dopamine receptor or NMDA glutamate receptor antagonist. Upon an acute challenge of cocaine following chronic cocaine exposure and withdrawal, we also observed in WT, but not in WAVE1 D1-KO mice, a decrease in dendritic spine density and a decrease in the frequency of excitatory postsynaptic AMPA receptor currents in medium spiny projection neurons expressing the D1 dopamine receptor (D1-MSNs) in the nucleus accumbens. These results suggest that WAVE1 is involved selectively in D1-MSNs in cocaine-evoked neuronal activitymediated feedback regulation of glutamatergic synapses.W iskott-Aldrich syndrome protein (WASP) family verprolin homologous protein (WAVE) initiates de novo actin polymerization through its ability to activate the actin-related protein 2/3 (Arp2/3) complex (1). Three members of the family (WAVE1-3) exist, with WAVE1 being highly expressed in brain (2). WAVE1 was purified from bovine or rat brain as part of a heteropentameric protein complex together with PIR121 [also called cytoplasmic FMR1-interacting protein 2, (Cyfip2)], Nck-associated protein 1 (Nckap1), Abl-interactor 2 (Abi2), and HSPC300 (3, 4). Whereas WAVE1 plays a key role in Arp2/3 complex binding and actin polymerization, other protein components in the complex are important for its subcellular localization and interaction with upstream ligands or activators (5, 6).In our initial study in striatum, the WAVE1 complex was found to interact with p35, the regulatory subunit of cyclin-dependent kinase 5 (Cdk5) (4). Phosphorylation of WAVE1 at Ser310, Ser397, and Ser441 by Cdk5/p35, in the complex purified from rat brain, or with recombinant WAVE1, resulted in inhibition of actin polymerization in vitro (4). We also observed that the stoichiometry of WAVE1 phosphorylation by Cdk5 is high in brain, suggestive of the protein being largely inactive under basal conditions (4). However, studies using mouse striatal slices indicated that WAVE1 can be dephosphorylated at all three Cdk5 sites and thereby activated upon stimulation of D1 dopa...

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Section: Resultsmentioning

confidence: 99%

WAVE1 in neurons expressing the D1 dopamine receptor regulates cellular and behavioral actions of cocaine

Ceglia

Lee

Cahill

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…4B). Synaptophysin is enriched in the LP2 fraction, representing a synaptic vesicle-enriched fraction (31). In addition to LP2, synapsin I was also detected in the LP1 fraction, a fraction enriched with synaptosomal membranes (32).…”

Section: Resultsmentioning

confidence: 99%

The Interaction between Cytoplasmic Prion Protein and the Hydrophobic Lipid Core of Membrane Correlates with Neurotoxicity

Wang

Arterburn

et al. 2006

Journal of Biological Chemistry

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Prion protein (PrP), normally a cell surface protein, has been detected in the cytosol of a subset of neurons. The appearance of PrP in the cytosol could result from either retro-translocation of misfolded PrP from the endoplasmic reticulum (ER) or impaired import of PrP into the ER. Transgenic mice expressing cytoplasmic PrP (cyPrP) developed neurodegeneration in cerebellar granular neurons, although no detectable pathology was observed in other brain regions. In order to understand why granular neurons in the cerebellum were most susceptible to cyPrP-induced degeneration, we investigated the subcellular localization of cyPrP. Interestingly, we found that cyPrP is membrane-bound. In transfected cells, it binds to the ER and plasma/endocytic vesicular membranes. In transgenic mice, it is associated with synaptic and microsomal membranes. Furthermore, the cerebellar neurodegeneration in transgenic mice correlates with the interaction between cyPrP and the hydrophobic lipid core of the membrane but not with either the aggregation status or the dosage of cyPrP. These results suggest that lipid membrane perturbation could be a cellular mechanism for cyPrP-induced neurotoxicity and explain the seemingly conflicting results concerning cyPrP.Prion diseases are a group of fatal neurodegenerative disorders that are sporadic, inherited, or transmissible (1). The resistance of PrP 2 knock-out mice to prion disease revealed the essential role of endogenous PrP in developing the two characteristics of prion disease, infectivity and neurodegeneration (2). In prion disease, a portion of PrP converts from its normal conformation, PrP C , to an insoluble and protease-resistant pathogenic conformation, PrP Sc (1). Compelling evidence supports that PrP Sc is the transmissible element in prion disease (3-5).Newly synthesized PrP contains an N-terminal signal sequence, which directs PrP to be co-translationally imported into the lumen of the ER. The signal sequence is cleaved within the ER, along with a C-terminal glycosylphosphatidylinositol signal sequence that is responsible for glycosylphosphatidylinositol anchor addition (6). Once folded correctly, PrP passes through the ER quality control machinery, maturing along the secretory pathway en route to the cell surface. In addition to cell surface and luminal localizations, cytosolic localized PrP has also been detected (7,8). Recent studies revealed that the cytosolic appearance of PrP could result from two independent but not mutually exclusive pathways. In a variety of cell lines, including primary neurons expressing endogenous PrP, it has been found that some PrP molecules misfold in the ER and are retro-translocated to the cytosol for proteasome degradation via the ER-associated degradation pathway (9 -13). Disease-associated PrP mutants have an increased tendency to misfold and are subjected to ER-associated degradation (9,10,12). An alternative pathway, the unsuccessful import of PrP because of the insufficiency of the PrP signal sequence, was revealed by an elegant study in...

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“…It remains to be determined whether an abnormal upregulation of these postsynaptic second messenger cascade events could result in exaggerated pyramidal cell excitability in response to D 1 and NMDA, as observed in the PFC of NVHL animals. A D 1 receptor activation also induces NMDA receptor trafficking to the postsynaptic membrane (Dunah and Standaert 2001), increasing surface expression of NMDA receptors. This interaction could selectively enhance pyramidal neurons' response to NMDA and not to AMPA in the adult PFC.…”

Section: Discussionmentioning

confidence: 99%

Post-Pubertal Disruption of Medial Prefrontal Cortical Dopamine–Glutamate Interactions in a Developmental Animal Model of Schizophrenia

Tseng

Lewis

Lipska³

et al. 2007

Biological Psychiatry

116

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Background-A neonatal ventral hippocampal lesion (NVHL) induces behavioral and physiological anomalies mimicking pathophysiological changes of schizophrenia. Because prefrontal cortical (PFC) pyramidal neurons recorded from adult NVHL rats exhibit abnormal responses to activation of the mesocortical dopaminergic (DA) system, we explored whether these changes are due to an altered DA modulation of pyramidal neurons.

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Dopamine D1 Receptor-Dependent Trafficking of Striatal NMDA Glutamate Receptors to the Postsynaptic Membrane

Cited by 351 publications

References 61 publications

WAVE1 in neurons expressing the D1 dopamine receptor regulates cellular and behavioral actions of cocaine

WAVE1 in neurons expressing the D1 dopamine receptor regulates cellular and behavioral actions of cocaine

The Interaction between Cytoplasmic Prion Protein and the Hydrophobic Lipid Core of Membrane Correlates with Neurotoxicity

Post-Pubertal Disruption of Medial Prefrontal Cortical Dopamine–Glutamate Interactions in a Developmental Animal Model of Schizophrenia

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