Selective overexpression of dopamine D3 receptors in the striatum disrupts motivation but not cognition

Biological Psychiatry

Volumn 76, Issue 10, 2014, Pages 823-831

  Simpson, Eleanor H ^a,b   Winiger, Vanessa ^b   Biezonski, Dominik K ^b   Haq, Iram ^b   Kandel, Eric R ^b,c   Kellendonk, Christoph ^a,b  

^a NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

^b Howard Hughes Medical Institute ^*  (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Cognition; Dopamine D3 receptor; Motivation; Schizophrenia; Striatum; Transgenic model

Indexed keywords

DOPAMINE 1 RECEPTOR; DOPAMINE 3 RECEPTOR; MESSENGER RNA; TETRACYCLINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COGNITION; CONTROLLED STUDY; CORPUS STRIATUM; DOWN REGULATION; EXPERIMENTAL BEHAVIORAL TEST; GENE EXPRESSION SYSTEM; GENE OVEREXPRESSION; GENE SWITCHING; LIGAND BINDING; MALE; MOTIVATION; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; QUANTITATIVE STUDY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCHIZOPHRENIA; SPATIAL MEMORY; STATE DEPENDENT LEARNING; TRANSGENE; WILD TYPE; WORKING MEMORY; ANIMAL; ANXIETY; DISEASE MODEL; GENETICS; LEARNING; METABOLISM; MOTOR ACTIVITY; PHYSIOLOGY; SENSORY GATING; TRANSGENIC MOUSE;

ANIMALS; ANXIETY; COGNITION; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; DOWN-REGULATION; LEARNING; MICE; MICE, TRANSGENIC; MOTIVATION; MOTOR ACTIVITY; RECEPTORS, DOPAMINE D1; RECEPTORS, DOPAMINE D3; RNA, MESSENGER; SCHIZOPHRENIA; SENSORY GATING;

EID: 84920626997     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2013.11.023     Document Type: Article

References (50)

1. Simpson EH, Kellendonk C, Kandel E (2010): A possible role for the striatum in the pathogenesis of the cognitive symptoms of schizophrenia. Neuron 65:585-596
2. Howes OD, Kambeitz J, Kim E, Stahl D, Slifstein M, Abi-Dargham A, Kapur S (2012): The nature of dopamine dysfunction in schizophrenia and what this means for treatment. Arch Gen Psychiatry 69:776-786
3. Seeman P, Lee T (1975): Antipsychotic drugs: Direct correlation between clinical potency and presynaptic action on dopamine neurons. Science 188:1217-1219
4. Creese I, Burt DR, Snyder SH (1976): Dopamine receptor binding predicts clinical and pharmacological potencies of antischizophrenic drugs. Science 192:481-483
5. Schwartz JC, Diaz J, Pilon C, Sokoloff P (2000): Possible implications of the dopamine D(3) receptor in schizophrenia and in antipsychotic drug actions. Brain Res Brain Res Rev 31:277-287
6. Weinberger DR, Laruelle M (2001): Neurochemical and neuropharmacological imaging in schizophrenia. In: Davis KL, Charney D, Coyle JT, Nemeroff CB, editors. Neuropharmacology: The Fifth Generation of Progress. Philadelphia: Lippincott, Williams, and Wilkins
7. Sibley DR (1991): Cloning of a 'D3' receptor subtype expands dopamine receptor family. Trends Pharmacol Sci 12:7-9
8. Prante O, Dorfler M, Gmeiner P (2010): Dopamine receptor subtypeselective drugs: D2-like receptors. In: Neve KA, editor. The Dopamine Receptors, 2nd ed. New York: Humana Press, 101-136
9. Gallezot JD, Beaver JD, Gunn RN, Nabulsi N, Weinzimmer D, Singhal T, et al. (2012): Affinity and selectivity of [(1)(1)C]-(+)-PHNO for the D3 and D2 receptors in the rhesus monkey brain in vivo. Synapse 66:489-500
10. Tziortzi AC, Searle GE, Tzimopoulou S, Salinas C, Beaver JD, Jenkinson M, et al. (2011): Imaging dopamine receptors in humans with [11C]- (+)-PHNO: Dissection of D3 signal and anatomy. Neuroimage 54:264-277
11. Searle G, Beaver JD, Comley RA, Bani M, Tziortzi A, Slifstein M, et al. (2010): Imaging dopamine D3 receptors in the human brain with positron emission tomography, [11C]PHNO, and a selective D3 receptor antagonist. Biol Psychiatry 68:392-399
12. Graff-Guerrero A, Mizrahi R, Agid O, Marcon H, Barsoum P, Rusjan P, et al. (2009): The dopamine D2 receptors in high-affinity state and D3 receptors in schizophrenia: A clinical [11C]-(+)-PHNO PET study. Neuropsychopharmacology 34:1078-1086
13. Kung MP, Kung HF, Chumpradit S, Foulon C (1993): In vitro binding of a novel dopamine D3 receptor ligand: [125I]trans-7-OH-PIPAT-A. Eur J Pharmacol 235:165-166
14. Gurevich EV, Bordelon Y, Shapiro RM, Arnold SE, Gur RE, Joyce JN (1997): Mesolimbic dopamine D3 receptors and use of antipsychotics in patients with schizophrenia. A postmortem study. Arch Gen Psychiatry 54:225-232
15. Kellendonk C, Simpson EH, Polan HJ, Malleret G, Vronskaya S, Winiger V, et al. (2006): Transient and selective overexpression of dopamine D2 receptors in the striatum causes persistent abnormalities in prefrontal cortex functioning. Neuron 49:603-615
16. Mayford M, Bach ME, Huang YY, Wang L, Hawkins RD, Kandel ER (1996): Control of memory formation through regulated expression of a CaMKII transgene. Science 274:1678-1683
17. Schaeren-Wiemers N, Gerfin-Moser A (1993): A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: In situ hybridization using digoxigeninlabelled cRNA probes. Histochemistry 100:431-440
18. Biezonski DK, Meyer JS (2010): Effects of 3,4-methylenedioxymethamphetamine (MDMA) on serotonin transporter and vesicular monoamine transporter 2 protein and gene expression in rats: Implications for MDMA neurotoxicity. J Neurochem 112:951-962
19. Simpson EH, Kellendonk C, Ward RD, Richards V, Lipatova O, Fairhurst S, et al. (2011): Pharmacologic rescue of motivational deficit in an animal model of the negative symptoms of schizophrenia. Biol Psychiatry 69:928-935
20. Muller PY, Janovjak H, Miserez AR, Dobbie Z (2002): Processing of gene expression data generated by quantitative real-time RT-PCR. Biotechniques 32:1372-1374, 1376, 1378-1379
21. Pittenger C, Fasano S, Mazzocchi-Jones D, Dunnett SB, Kandel ER, Brambilla R (2006): Impaired bidirectional synaptic plasticity and procedural memory formation in striatum-specific cAMP response element-binding protein-deficient mice. J Neurosci 26:2808-2813
22. Bach ME, Simpson EH, Kahn L, Marshall JJ, Kandel ER, Kellendonk C (2008): Transient and selective overexpression of D2 receptors in the striatum causes persistent deficits in conditional associative learning. Proc Natl Acad Sci U S A 105:16027-16032
23. Drew MR, Simpson EH, Kellendonk C, Herzberg WG, Lipatova O, Fairhurst S, et al. (2007): Transient overexpression of striatal D2 receptors impairs operant motivation and interval timing. J Neurosci 27:7731-7739
24. Cazorla M, Shegda M, Ramesh B, Harrison NL, Kellendonk C (2012): Striatal D2 receptors regulate dendritic morphology of medium spiny neurons via Kir2 channels. J Neurosci 32:2398-2409
25. Surmeier DJ, Eberwine J, Wilson CJ, Cao Y, Stefani A, Kitai ST (1992): Dopamine receptor subtypes colocalize in rat striatonigral neurons. Proc Natl Acad Sci U S A 89:10178-10182
26. Surmeier DJ, Song WJ, Yan Z (1996): Coordinated expression of dopamine receptors in neostriatal medium spiny neurons. J Neurosci 16: 6579-6591
27. Aleman A, Hijman R, de Haan EH, Kahn RS (1999): Memory impairment in schizophrenia: A meta-analysis. Am J Psychiatry 156: 1358-1366
28. Fioravanti M, Carlone O, Vitale B, Cinti ME, Clare L (2005): A metaanalysis of cognitive deficits in adults with a diagnosis of schizophrenia. Neuropsychol Rev 15:73-95
29. Spieker EA, Astur RS, West JT, Griego JA, Rowland LM (2012): Spatial memory deficits in a virtual reality eight-arm radial maze in schizophrenia. Schizophr Res 135:84-89
30. Goldman-Rakic PS (1994): Working memory dysfunction in schizophrenia. J Neuropsychiatry Clin Neurosci 6:348-357
31. Lee J, Park S (2005): Working memory impairments in schizophrenia: A meta-analysis. J Abnorm Psychol 114:599-611
32. Park S, Holzman PS (1992): Schizophrenics show spatial working memory deficits. Arch Gen Psychiatry 49:975-982
33. Gold JM, Bish JA, Iannone VN, Hobart MP, Queern CA, Buchanan RW (2000): Effects of contextual processing on visual conditional associative learning in schizophrenia. Biol Psychiatry 48:406-414
34. Kemali D, Maj M, Galderisi S, Monteleone P, Mucci A (1987): Conditional associative learning in drug-free schizophrenic patients. Neuropsychobiology 17:30-34
35. Rushe TM, Woodruff PW, Murray RM, Morris RG (1999): Episodic memory and learning in patients with chronic schizophrenia. Schizophr Res 35:85-96
36. Salamone JD (2006): Will the last person who uses the term 'reward' please turn out the lights? Comments on processes related to reinforcement, learning, motivation and effort. Addict Biol 11:43-44
37. Aberman JE, Ward SJ, Salamone JD (1998): Effects of dopamine antagonists and accumbens dopamine depletions on time-constrained progressive-ratio performance. Pharmacol Biochem Behav 61: 341-348
38. Cousins MS, Salamone JD (1994): Nucleus accumbens dopamine depletions in rats affect relative response allocation in a novel cost/ benefit procedure. Pharmacol Biochem Behav 49:85-91
39. Salamone JD, Arizzi MN, Sandoval MD, Cervone KM, Aberman JE (2002): Dopamine antagonists alter response allocation but do not suppress appetite for food in rats: Contrast between the effects of SKF 83566, raclopride, and fenfluramine on a concurrent choice task. Psychopharmacology (Berl) 160:371-380
40. Kosaka J, Takahashi H, Ito H, Takano A, Fujimura Y, Matsumoto R, et al. (2010): Decreased binding of [11C]NNC112 and [11C]SCH23390 in patients with chronic schizophrenia. Life Sci 86:814-818
41. Abi-Dargham A, Xu X, Thompson JL, Gil R, Kegeles LS, Urban N, et al. (2012): Increased prefrontal cortical D(1) receptors in drug naive patients with schizophrenia: A PET study with [(1)(1)C]NNC112. J Psychopharmacol 26:794-805
42. Napolitano F, Bonito-Oliva A, Federici M, Carta M, Errico F, Magara S, et al. (2010): Role of aberrant striatal dopamine D1 receptor/cAMP/ protein kinase A/DARPP32 signaling in the paradoxical calming effect of amphetamine. J Neurosci 30:11043-11056
43. van Tol HH, Riva M, Civelli O, Creese I (1990): Lack of effect of chronic dopamine receptor blockade on D2 dopamine receptor mRNA level. Neurosci Lett 111:303-308
44. Bouthenet ML, Souil E, Martres MP, Sokoloff P, Giros B, Schwartz JC (1991): Localization of dopamine D3 receptor mRNA in the rat brain using in situ hybridization histochemistry: Comparison with dopamine D2 receptor mRNA. Brain Res 564:203-219
45. Guillin O, Diaz J, Carroll P, Griffon N, Schwartz JC, Sokoloff P (2001): BDNF controls dopamine D3 receptor expression and triggers behavioural sensitization. Nature 411:86-89
46. Sokoloff P, Diaz J, Le Foll B, Guillin O, Leriche L, Bezard E, Gross C (2006): The dopamine D3 receptor: A therapeutic target for the treatment of neuropsychiatric disorders. CNS Neurol Disord Drug Targets 5:25-43
47. Fiorentini C, Busi C, Gorruso E, Gotti C, Spano P, Missale C (2008): Reciprocal regulation of dopamine D1 and D3 receptor function and trafficking by heterodimerization. Mol Pharmacol 74:59-69
48. Berridge KC (2007): The debate over dopamine's role in reward: The case for incentive salience. Psychopharmacology (Berl) 191:391-431
49. Flagel SB, Clark JJ, Robinson TE, Mayo L, Czuj A, Willuhn I, et al. (2011): A selective role for dopamine in stimulus-reward learning. Nature 469: 53-57
50. Adham N, Gyertyan I, Kiss B, Pasztor G, Gupta S, Szombathelyi Z, et al. (2007): Antidepressant activity of RGH-188, a potential antipsychotic with D3/D2 antagonist/partial agonist properties in a chronic mild stress-induced anhedonia model. Presented at the Society for Neuroscience Annual Meeting, November 12-17, San Diego, California. San Diego, CA: Society for Neuroscience.