Deletion of GSK3β in D2R-expressing neurons reveals distinct roles for β-arrestin signaling in antipsychotic and lithium action

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 50, 2012, Pages 20732-20737

  Urs, Nikhil M ^a   Snyder, Joshua C ^a   Jacobsen, Jacob P R ^a   Peterson, Sean M ^a   Caron, Marc G ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Bipolar disorder; Frontal cortex; Functional selectivity; Schizophrenia; Striatum

Indexed keywords

ARIPIPRAZOLE; BETA ARRESTIN; BETA CATENIN; DOPAMINE 2 RECEPTOR; GLYCOGEN SYNTHASE KINASE 3BETA; HALOPERIDOL; LITHIUM; CATNB PROTEIN, MOUSE; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; NEUROLEPTIC AGENT; PIPERAZINE DERIVATIVE; QUINOLONE DERIVATIVE; RETINA S ANTIGEN;

AFFECT; ANIMAL EXPERIMENT; ANTIDEPRESSANT ACTIVITY; ARTICLE; CONTROLLED STUDY; DEPRESSION; DOPAMINERGIC NERVE CELL; GENE DELETION; HALOPERIDOL-INDUCED CATALEPSY; LIGHT DARK CYCLE; LOCOMOTION; MANIA; MOUSE; NONHUMAN; PLACE PREFERENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; SCHIZOPHRENIA; SIGNAL TRANSDUCTION; TAIL SUSPENSION TEST; 129 MOUSE; ANIMAL; ANIMAL BEHAVIOR; C57BL MOUSE; DRUG EFFECT; GENE INACTIVATION; GENETICS; MOTOR ACTIVITY; MOUSE MUTANT; PHYSIOLOGY;

ANIMALS; ANTIPSYCHOTIC AGENTS; ARRESTINS; BEHAVIOR, ANIMAL; BETA CATENIN; DOPAMINERGIC NEURONS; GENE KNOCKOUT TECHNIQUES; GLYCOGEN SYNTHASE KINASE 3; LITHIUM; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MOTOR ACTIVITY; PIPERAZINES; QUINOLONES; RECEPTORS, DOPAMINE D2; SIGNAL TRANSDUCTION;

EID: 84874407555     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1215489109     Document Type: Article

References (60)

1. Missale C, Nash SR, Robinson SW, Jaber M, Caron MG (1998) Dopamine receptors: From structure to function. Physiol Rev 78(1):189–225.
2. Svenningsson P, et al. (1998) Activation of adenosine A2A and dopamine D1 receptors stimulates cyclic AMP-dependent phosphorylation of DARPP-32 in distinct populations of striatal projection neurons. Neuroscience 84(1):223–228.
3. Bateup HS, et al. (2008) Cell type-specific regulation of DARPP-32 phosphorylation by psychostimulant and antipsychotic drugs. Nat Neurosci 11(8):932–939.
4. Greengard P (2001) The neurobiology of slow synaptic transmission. Science 294 (5544):1024–1030.
5. Beaulieu JM, et al. (2005) An Akt/beta-arrestin 2/PP2A signaling complex mediates dopaminergic neurotransmission and behavior. Cell 122(2):261–273.
6. Beaulieu JM, et al. (2007) Regulation of Akt signaling by D2 and D3 dopamine receptors in vivo. J Neurosci 27(4):881–885.
7. Lovestone S, Killick R, Di Forti M, Murray R (2007) Schizophrenia as a GSK-3 dysre-gulation disorder. Trends Neurosci 30(4):142–149.
8. Du J, et al. (2010) A kinesin signaling complex mediates the ability of GSK-3beta to affect mood-associated behaviors. Proc Natl Acad Sci USA 107(25):11573–11578.
9. Emamian ES, Hall D, Birnbaum MJ, Karayiorgou M, Gogos JA (2004) Convergent evidence for impaired AKT1-GSK3beta signaling in schizophrenia. Nat Genet 36(2): 131–137.
10. Jope RS (2011) Glycogen synthase kinase-3 in the etiology and treatment of mood disorders. Front Mol Neurosci 4:16.
11. Beaulieu JM, et al. (2004) Lithium antagonizes dopamine-dependent behaviors mediated by an AKT/glycogen synthase kinase 3 signaling cascade. Proc Natl Acad Sci USA 101(14):5099–5104.
12. Gould TD, Manji HK (2005) Glycogen synthase kinase-3: A putative molecular target for lithium mimetic drugs. Neuropsychopharmacology 30(7):1223–1237.
13. Sutton LP, Rushlow WJ (2011) The effects of neuropsychiatric drugs on glycogen synthase kinase-3 signaling. Neuroscience 199:116–124.
14. Gould TD, Picchini AM, Einat H, Manji HK (2006) Targeting glycogen synthase kinase-3 in the CNS: Implications for the development of new treatments for mood disorders. Curr Drug Targets 7(11):1399–1409.
15. Beaulieu JM, et al. (2008) A beta-arrestin 2 signaling complex mediates lithium action on behavior. Cell 132(1):125–136.
16. Patel S, et al. (2008) Tissue-specific role of glycogen synthase kinase 3beta in glucose homeostasis and insulin action. Mol Cell Biol 28(20):6314–6328.
17. Levey AI, et al. (1993) Localization of D1 and D2 dopamine receptors in brain with subtype-specific antibodies. Proc Natl Acad Sci USA 90(19):8861–8865.
18. Holmes A, Lachowicz JE, Sibley DR (2004) Phenotypic analysis of dopamine receptor knockout mice; recent insights into the functional specificity of dopamine receptor subtypes. Neuropharmacology 47(8):1117–1134.
19. van den Buuse M (2010) Modeling the positive symptoms of schizophrenia in genetically modified mice: Pharmacology and methodology aspects. Schizophr Bull 36 (2):246–270.
20. Lieberman JA, et al. (2008) Antipsychotic drugs: Comparison in animal models of efficacy, neurotransmitter regulation, and neuroprotection. Pharmacol Rev 60(3): 358–403.
21. Ramsey AJ, et al. (2008) Genetic NMDA receptor deficiency disrupts acute and chronic effects of cocaine but not amphetamine. Neuropsychopharmacology 33(11): 2701–2714.
22. Giros B, Jaber M, Jones SR, Wightman RM, Caron MG (1996) Hyperlocomotion and indifference to cocaine and amphetamine in mice lacking the dopamine transporter. Nature 379(6566):606–612.
23. O’Brien WT, et al. (2011) Glycogen synthase kinase-3 is essential for β-arrestin-2 complex formation and lithium-sensitive behaviors in mice. J Clin Invest 121(9): 3756–3762.
24. Masri B, et al. (2008) Antagonism of dopamine D2 receptor/beta-arrestin 2 interaction is a common property of clinically effective antipsychotics. Proc Natl Acad Sci USA 105 (36):13656–13661.
25. Stambolic V, Ruel L, Woodgett JR (1996) Lithium inhibits glycogen synthase kinase-3 activity and mimics wingless signalling in intact cells. Curr Biol 6(12):1664–1668.
26. Klein PS, Melton DA (1996) A molecular mechanism for the effect of lithium on development. Proc Natl Acad Sci USA 93(16):8455–8459.
27. Freyberg Z, Ferrando SJ, Javitch JA (2010) Roles of the Akt/GSK-3 and Wnt signaling pathways in schizophrenia and antipsychotic drug action. Am J Psychiatry 167(4): 388–396.
28. Sutton LP, Honardoust D, Mouyal J, Rajakumar N, Rushlow WJ (2007) Activation of the canonical Wnt pathway by the antipsychotics haloperidol and clozapine involves dishevelled-3. J Neurochem 102(1):153–169.
29. Alimohamad H, Rajakumar N, Seah YH, Rushlow W (2005) Antipsychotics alter the protein expression levels of beta-catenin and GSK-3 in the rat medial prefrontal cortex and striatum. Biol Psychiatry 57(5):533–542.
30. Gould TD, et al. (2007) Beta-catenin overexpression in the mouse brain phenocopies lithium-sensitive behaviors. Neuropsychopharmacology 32(10):2173–2183.
31. Prickaerts J, et al. (2006) Transgenic mice overexpressing glycogen synthase kinase 3beta: A putative model of hyperactivity and mania. J Neurosci 26(35):9022–9029.
32. Miller JS, Tallarida RJ, Unterwald EM (2010) Inhibition of GSK3 attenuates dopamine D1 receptor agonist-induced hyperactivity in mice. Brain Res Bull 82(3-4):184–187.
33. Lefkowitz RJ, Shenoy SK (2005) Transduction of receptor signals by beta-arrestins. Science 308(5721):512–517.
34. Ralph RJ, Paulus MP, Fumagalli F, Caron MG, Geyer MA (2001) Prepulse inhibition deficits and perseverative motor patterns in dopamine transporter knock-out mice: Differential effects of D1 and D2 receptor antagonists. J Neurosci 21(1):305–313.
35. Ralph RJ, et al. (1999) The dopamine D2, but not D3 or D4, receptor subtype is essential for the disruption of prepulse inhibition produced by amphetamine in mice. J Neurosci 19(11):4627–4633.
36. Ralph-Williams RJ, Lehmann-Masten V, Otero-Corchon V, Low MJ, Geyer MA (2002) Differential effects of direct and indirect dopamine agonists on prepulse inhibition: A study in D1 and D2 receptor knock-out mice. J Neurosci 22(21):9604–9611.
37. Kapfhamer D, et al. (2010) Protein Phosphatase 2a and glycogen synthase kinase 3 signaling modulate prepulse inhibition of the acoustic startle response by altering cortical M-Type potassium channel activity. J Neurosci 30(26):8830–8840.
38. Kozlovsky N, Belmaker RH, Agam G (2001) Low GSK-3 activity in frontal cortex of schizophrenic patients. Schizophr Res 52(1-2):101–105.
39. Abi-Dargham A, Laruelle M (2005) Mechanisms of action of second generation antipsychotic drugs in schizophrenia: Insights from brain imaging studies. Eur Psychiatry 20(1):15–27.
40. Lieberman JA, et al.; Clinical Antipsychotic Trials of Intervention Effectiveness (CATIE) Investigators (2005) Effectiveness of antipsychotic drugs in patients with chronic schizophrenia. N Engl J Med 353(12):1209–1223.
41. Li X, Rosborough KM, Friedman AB, Zhu W, Roth KA (2007) Regulation of mouse brain glycogen synthase kinase-3 by atypical antipsychotics. Int J Neuro-psychopharmacol 10(1):7–19.
42. Bateup HS, et al. (2010) Distinct subclasses of medium spiny neurons differentially regulate striatal motor behaviors. Proc Natl Acad Sci USA 107(33):14845–14850.
43. Allen JA, et al. (2011) Discovery of β-arrestin-biased dopamine D2 ligands for probing signal transduction pathways essential for antipsychotic efficacy. Proc Natl Acad Sci USA 108(45):18488–18493.
44. Li YC, Xi D, Roman J, Huang YQ, Gao WJ (2009) Activation of glycogen synthase kinase-3 beta is required for hyperdopamine and D2 receptor-mediated inhibition of synaptic NMDA receptor function in the rat prefrontal cortex. J Neurosci 29(49): 15551–15563.
45. Kellendonk C, et al. (2006) Transient and selective overexpression of dopamine D2 receptors in the striatum causes persistent abnormalities in prefrontal cortex functioning. Neuron 49(4):603–615.
46. Li YC, Kellendonk C, Simpson EH, Kandel ER, Gao WJ (2011) D2 receptor overexpression in the striatum leads to a deficit in inhibitory transmission and dopamine sensitivity in mouse prefrontal cortex. Proc Natl Acad Sci USA 108(29):12107–12112.
47. Kellendonk C, Simpson EH, Kandel ER (2009) Modeling cognitive endophenotypes of schizophrenia in mice. Trends Neurosci 32(6):347–358.
48. Chalecka-Franaszek E, Chuang DM (1999) Lithium activates the serine/threonine kinase Akt-1 and suppresses glutamate-induced inhibition of Akt-1 activity in neurons. Proc Natl Acad Sci USA 96(15):8745–8750.
49. Belmaker RH, Bersudsky Y, Agam G, Levine J, Kofman O (1996) How does lithium work on manic depression? Clinical and psychological correlates of the inositol theory. Annu Rev Med 47:47–56.
50. Williams RS, Cheng L, Mudge AW, Harwood AJ (2002) A common mechanism of action for three mood-stabilizing drugs. Nature 417(6886):292–295.
51. Gould TD, et al. (2008) Involvement of AMPA receptors in the antidepressant-like effects of lithium in the mouse tail suspension test and forced swim test. Neuropharmacology 54(3):577–587.
52. Scotti MA, et al. (2011) Behavioral and pharmacological assessment of a potential new mouse model for mania. Physiol Behav 103(3-4):376–383.
53. Mines MA, Jope RS (2012) Brain region differences in regulation of Akt and GSK3 by chronic stimulant administration in mice. Cell Signal 24(7):1398–1405.
54. Chou JC, et al. (1996) Neuroleptics in acute mania: A pharmacoepidemiologic study. Ann Pharmacother 30(12):1396–1398.
55. Cookson J (2001) Use of antipsychotic drugs and lithium in mania. Br J Psychiatry Suppl 41:s148–s156.
56. Kalinichev M, Dawson LA (2011) Evidence for antimanic efficacy of glycogen synthase kinase-3 (GSK3) inhibitors in a strain-specific model of acute mania. Int J Neuro-psychopharmacol 14(8):1051–1067.
57. Einat H, Manji HK, Belmaker RH (2003) New approaches to modeling bipolar disorder. Psychopharmacol Bull 37(1):47–63.
58. Gould TD, Einat H, Bhat R, Manji HK (2004) AR-A014418, a selective GSK-3 inhibitor, produces antidepressant-like effects in the forced swim test. Int J Neuro-psychopharmacol 7(4):387–390.
59. Urs NM, Daigle TL, Caron MG (2011) A dopamine D1 receptor-dependent β-arrestin signaling complex potentially regulates morphine-induced psychomotor activation but not reward in mice. Neuropsychopharmacology 36(3):551–558.
60. Wang X, et al. (2011) Synaptic dysfunction and abnormal behaviors in mice lacking major isoforms of Shank3. Hum Mol Genet 20(15):3093–3108.