Loss of dysbindin-1 in mice impairs reward-based operant learning by increasing impulsive and compulsive behavior

Behavioural Brain Research

Volumn 241, Issue 1, 2013, Pages 173-184

  Carr, Gregory V ^a   Jenkins, Kimberly A ^a   Weinberger, Daniel R ^a,b,c   Papaleo, Francesco ^a,d,e  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^e UNIVERSITY OF PADOVA   (Italy)

Author keywords

Compulsivity; Dysbindin; Impulsivity; Operant learning; Schizophrenia; Timing

Indexed keywords

DYSBINDIN; MUTANT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; C57BL 6 MOUSE; COMPULSION; CONTROLLED STUDY; GENOTYPE; HETEROZYGOTE; IMPULSIVENESS; INSTRUMENTAL CONDITIONING; LEARNING DISORDER; MENTAL TASK; MOUSE; NONHUMAN; PERCEPTIVE DISCRIMINATION; PRIORITY JOURNAL; PROTEIN DEPLETION; RESPONSE TIME; VISUAL DISCRIMINATION; WILD TYPE;

ANIMALS; BEHAVIOR, ANIMAL; CARRIER PROTEINS; COMPULSIVE BEHAVIOR; CONDITIONING, OPERANT; IMPULSIVE BEHAVIOR; MEMORY; MICE; MICE, KNOCKOUT; MOTOR ACTIVITY; REACTION TIME; REWARD;

EID: 84872038495     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2012.12.021     Document Type: Article

References (51)

1. Benson M.A., Newey S.E., Martin-Rendon E., Hawkes R., Blake D.J. Dysbindin, a novel coiled-coil-containing protein that interacts with the dystrobrevins in muscle and brain. Journal of Biological Chemistry 2001, 276:24232-24241.
2. Chen X.W., Feng Y.Q., Hao C.J., Guo X.L., He X., Zhou Z.Y., et al. DTNBP1, a schizophrenia susceptibility gene, affects kinetics of transmitter release. Journal of Cell Biology 2008, 181:791-801.
3. Li W., Zhang Q., Oiso N., Novak E.K., Gautam R., O'Brien E.P., et al. Hermansky-Pudlak syndrome type 7 (HPS-7) results from mutant dysbindin, a member of the biogenesis of lysosome-related organelles complex 1 (BLOC-1). Nature Genetics 2003, 35:84-89.
4. Ghiani C.A., Starcevic M., Rodriguez-Fernandez I.A., Nazarian R., Cheli V.T., Chan L.N., et al. The dysbindin-containing complex (BLOC-1) in brain: developmental regulation, interaction with SNARE proteins and role in neurite outgrowth. Molecular Psychiatry 2010, 15(115):204-215.
5. Burdick K.E., Lencz T., Funke B., Finn C.T., Szeszko P.R., Kane J.M., et al. Genetic variation in DTNBP1 influences general cognitive ability. Human Molecular Genetics 2006, 15:1563-1568.
6. Fallgatter A.J., Herrmann M.J., Hohoff C., Ehlis A.C., Jarczok T.A., Freitag C.M., et al. DTNBP1 (dysbindin) gene variants modulate prefrontal brain function in healthy individuals. Neuropsychopharmacology 2006, 31:2002-2010.
7. Wolf C., Jackson M.C., Kissling C., Thome J., Linden D.E. Dysbindin-1 genotype effects on emotional working memory. Molecular Psychiatry 2011, 16:145-155.
8. Straub R.E., Jiang Y., MacLean C.J., Ma Y., Webb B.T., Myakishev M.V., et al. Genetic variation in the 6p22.3 gene DTNBP1, the human ortholog of the mouse dysbindin gene, is associated with schizophrenia. American Journal of Human Genetics 2002, 71:337-348.
9. Schwab S.G., Knapp M., Mondabon S., Hallmayer J., Borrmann-Hassenbach M., Albus M., et al. Support for association of schizophrenia with genetic variation in the 6p22.3 gene, dysbindin, in sib-pair families with linkage and in an additional sample of triad families. American Journal of Human Genetics 2003, 72:185-190.
10. Van Den Bogaert A., Schumacher J., Schulze T.G., Otte A.C., Ohlraun S., Kovalenko S., et al. The DTNBP1 (dysbindin) gene contributes to schizophrenia, depending on family history of the disease. American Journal of Human Genetics 2003, 73:1438-1443.
11. Allen N.C., Bagade S., McQueen M.B., Ioannidis J.P., Kavvoura F.K., Khoury M.J., et al. Systematic meta-analyses and field synopsis of genetic association studies in schizophrenia: the SzGene database. Nature Genetics 2008, 40:827-834.
12. Weickert C.S., Rothmond D.A., Hyde T.M., Kleinman J.E., Straub R.E. Reduced DTNBP1 (dysbindin-1) mRNA in the hippocampal formation of schizophrenia patients. Schizophrenia Research 2008, 98:105-110.
13. Talbot K., Eidem W.L., Tinsley C.L., Benson M.A., Thompson E.W., Smith R.J., et al. Dysbindin-1 is reduced in intrinsic, glutamatergic terminals of the hippocampal formation in schizophrenia. Journal of Clinical Investigation 2004, 113:1353-1363.
14. Tang J., LeGros R.P., Louneva N., Yeh L., Cohen J.W., Hahn C.G., et al. Dysbindin-1 in dorsolateral prefrontal cortex of schizophrenia cases is reduced in an isoform-specific manner unrelated to dysbindin-1 mRNA expression. Human Molecular Genetics 2009, 18:3851-3863.
15. Weickert C.S., Straub R.E., McClintock B.W., Matsumoto M., Hashimoto R., Hyde T.M., et al. Human dysbindin (DTNBP1) gene expression in normal brain and in schizophrenic prefrontal cortex and midbrain. Archives of General Psychiatry 2004, 61:544-555.
16. Jentsch J.D., Trantham-Davidson H., Jairl C., Tinsley M., Cannon T.D., Lavin A. Dysbindin modulates prefrontal cortical glutamatergic circuits and working memory function in mice. Neuropsychopharmacology 2009, 34:2601-2608.
17. Takao K., Toyama K., Nakanishi K., Hattori S., Takamura H., Takeda M., et al. Impaired long-term memory retention and working memory in sdy mutant mice with a deletion in Dtnbp1, a susceptibility gene for schizophrenia. Molecular Brain 2008, 1:11.
18. Nguyen P.V., Abel T., Kandel E.R., Bourtchouladze R. Strain-dependent differences in LTP and hippocampus-dependent memory in inbred mice. Learning & Memory 2000, 7:170-179.
19. D'Este L., Casini A., Puglisi-Allegra S., Cabib S., Renda T.G. Comparative immunohistochemical study of the dopaminergic systems in two inbred mouse strains (C57BL/6J and DBA/2J). Journal of Chemical Neuroanatomy 2007, 33:67-74.
20. Cox M.M., Tucker A.M., Tang J., Talbot K., Richer D.C., Yeh L., et al. Neurobehavioral abnormalities in the dysbindin-1 mutant, sandy, on a C57BL/6J genetic background. Genes, Brain and Behavior 2009, 8:390-397.
21. Papaleo F., Yang F., Garcia S., Chen J., Lu B., Crawley J.N., et al. Dysbindin-1 modulates prefrontal cortical activity and schizophrenia-like behaviors via dopamine/D2 pathways. Molecular Psychiatry 2012, 17:85-98.
22. Karlsgodt K.H., Robleto K., Trantham-Davidson H., Jairl C., Cannon T.D., Lavin A., et al. Reduced dysbindin expression mediates N-methyl-D-aspartate receptor hypofunction and impaired working memory performance. Biological Psychiatry 2011, 69:28-34.
23. Dickman D.K., Davis G.W. The schizophrenia susceptibility gene dysbindin controls synaptic homeostasis. Science 2009, 326:1127-1130.
24. Papaleo F., Weinberger D.R. Dysbindin and Schizophrenia: it's dopamine and glutamate all over again. Biological Psychiatry 2011, 69:2-4.
25. Kumamoto N., Matsuzaki S., Inoue K., Hattori T., Shimizu S., Hashimoto R., et al. Hyperactivation of midbrain dopaminergic system in schizophrenia could be attributed to the down-regulation of dysbindin. Biochemical and Biophysical Research Communications 2006, 345:904-909.
26. Ji Y., Yang F., Papaleo F., Wang H.X., Gao W.J., Weinberger D.R., et al. Role of dysbindin in dopamine receptor trafficking and cortical GABA function. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:19593-19598.
27. Numakawa T., Yagasaki Y., Ishimoto T., Okada T., Suzuki T., Iwata N., et al. Evidence of novel neuronal functions of dysbindin, a susceptibility gene for schizophrenia. Human Molecular Genetics 2004, 13:2699-2708.
28. Drew M.R., Simpson E.H., Kellendonk C., Herzberg W.G., Lipatova O., Fairhurst S., et al. Transient overexpression of striatal D2 receptors impairs operant motivation and interval timing. Journal of Neuroscience 2007, 27:7731-7739.
29. Kellendonk C., Simpson E.H., Polan H.J., Malleret G., Vronskaya S., Winiger V., et al. Transient and selective overexpression of dopamine D2 receptors in the striatum causes persistent abnormalities in prefrontal cortex functioning. Neuron 2006, 49:603-615.
30. Nagai T., Kitahara Y., Shiraki A., Hikita T., Taya S., Kaibuchi K., et al. Dysfunction of dopamine release in the prefrontal cortex of dysbindin deficient sandy mice: an in vivo microdialysis study. Neuroscience Letters 2010, 470:134-138.
31. Winterer G., Weinberger D.R. Genes, dopamine and cortical signal-to-noise ratio in schizophrenia. Trends in Neurosciences 2004, 27:683-690.
32. Dalton G.L., Ma L.M., Phillips A.G., Floresco S.B. Blockade of NMDA GluN2B receptors selectively impairs behavioral flexibility but not initial discrimination learning. Psychopharmacology (Berlin, Germany) 2011, 216:525-535.
33. Floresco S.B., Block A.E., Tse M.T. Inactivation of the medial prefrontal cortex of the rat impairs strategy set-shifting, but not reversal learning, using a novel, automated procedure. Behavioural Brain Research 2008, 190:85-96.
34. Kato S., Kuramochi M., Kobayashi K., Fukabori R., Okada K., Uchigashima M., et al. Selective neural pathway targeting reveals key roles of thalamostriatal projection in the control of visual discrimination. Journal of Neuroscience 2011, 31:17169-17179.
35. Robinson S., Rainwater A.J., Hnasko T.S., Palmiter R.D. Viral restoration of dopamine signaling to the dorsal striatum restores instrumental conditioning to dopamine-deficient mice. Psychopharmacology (Berlin, Germany) 2007, 191:567-578.
36. Ward R.D., Kellendonk C., Kandel E.R., Balsam P.D. Timing as a window on cognition in schizophrenia. Neuropharmacology 2012, 62:1175-1181. 10.1016/j.neuropharm.2011.04.014.
37. Narayanan N.S., Laubach M. Top-down control of motor cortex ensembles by dorsomedial prefrontal cortex. Neuron 2006, 52:921-931.
38. McBain C.J., Fisahn A. Interneurons unbound. Nature Reviews Neuroscience 2001, 2:11-23.
39. Spencer K.M., Nestor P.G., Niznikiewicz M.A., Salisbury D.F., Shenton M.E., McCarley R.W. Abnormal neural synchrony in schizophrenia. Journal of Neuroscience 2003, 23:7407-7411.
40. Whittington M.A., Traub R.D. Interneuron diversity series: inhibitory interneurons and network oscillations in vitro. Trends in Neurosciences 2003, 26:676-682.
41. Graybiel A.M. Habits, rituals, and the evaluative brain. Annual Review of Neuroscience 2008, 31:359-387.
42. Li Y.C., Kellendonk C., Simpson E.H., Kandel E.R., Gao W.J. D2 receptor overexpression in the striatum leads to a deficit in inhibitory transmission and dopamine sensitivity in mouse prefrontal cortex. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:12107-12112.
43. Iizuka Y., Sei Y., Weinberger D.R., Straub R.E. Evidence that the BLOC-1 protein dysbindin modulates dopamine D2 receptor internalization and signaling but not D1 internalization. Journal of Neuroscience 2007, 27:12390-12395.
44. Ito H., Morishita R., Shinoda T., Iwamoto I., Sudo K., Okamoto K., et al. Dysbindin-1, a schizophrenia-related molecule, is involved in the regulation of neuronal dendritic development. Molecular Psychiatry 2010, 15:969.
45. Elvevåg B., McCormack T., Gilbert A., Brown G.D., Weinberger D.R., Goldberg T.E. Duration judgements in patients with schizophrenia. Psychological Medicine 2003, 33:1249-1261.
46. Wong D.F., Wagner H.N., Tune L.E., Dannals R.F., Pearlson G.D., Links J.M., et al. Positron emission tomography reveals elevated D2 dopamine receptors in drug-naive schizophrenics. Science 1986, 234:1558-1563.
47. Papaleo F., Lipska B.K., Weinberger D.R. Mouse models of genetic effects on cognition: relevance to schizophrenia. Neuropharmacology 2012, 62:1204-1220.
48. Brigman J.L., Feyder M., Saksida L.M., Bussey T.J., Mishina M., Holmes A. Impaired discrimination learning in mice lacking the NMDA receptor NR2A subunit. Learning & Memory 2008, 15:50-54.
49. Karlsson R.M., Tanaka K., Saksida L.M., Bussey T.J., Heilig M., Holmes A. Assessment of glutamate transporter GLAST (EAAT1)-deficient mice for phenotypes relevant to the negative and executive/cognitive symptoms of schizophrenia. Neuropsychopharmacology 2009, 34:1578-1589.
50. Brigman J.L., Ihne J., Saksida L.M., Bussey T.J., Holmes A. Effects of subchronic phencyclidine (PCP) treatment on social behaviors, and operant discrimination and reversal learning in C57BL/6J mice. Frontiers in Behavioral Neuroscience 2009, 3:2.
51. Barkus C., Feyder M., Graybeal C., Wright T., Wiedholz L., Izquierdo A., et al. Do GluA1 knockout mice exhibit behavioral abnormalities relevant to the negative or cognitive symptoms of schizophrenia and schizoaffective disorder. Neuropharmacology 2012, 62:1263-1272.