Deletion of glutamate delta-1 receptor in mouse leads to aberrant emotional and social behaviors

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Yadav, Roopali ^a   Gupta, Subhash C ^a   Hillman, Brandon G ^a   Bhatt, Jay M ^a   Stairs, Dustin J ^b   Dravid, Shashank M ^a  

^a CREIGHTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CREIGHTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOSERINE; GLUTAMATE DELTA 1 RECEPTOR; GLUTAMATE RECEPTOR; LITHIUM; POSTSYNAPTIC DENSITY PROTEIN 95; PROTEIN GLUA1; PROTEIN GLUA2; PROTEIN GLUK2; RECEPTOR SUBUNIT; SYNAPSE RECEPTOR; UNCLASSIFIED DRUG; GLUTAMATE RECEPTOR DELTA 1;

AGGRESSION; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY DISORDER; ARTICLE; AUTISM; BIPOLAR DISORDER; CONTROLLED STUDY; DEPRESSION; EMOTIONAL DISORDER; FORCED SWIMMING TEST; GENE; GENE DELETION; GENETIC ASSOCIATION; GRID GENE; KNOCKOUT MOUSE; MAJOR DEPRESSION; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; PREFRONTAL CORTEX; PRESYNAPTIC NERVE; PROTEIN EXPRESSION; SCHIZOPHRENIA; SOCIAL INTERACTION; SOCIOPATHY; SYNAPTIC MEMBRANE; SYNAPTOSOME; 129 MOUSE; ANIMAL; ANIMAL BEHAVIOR; ANXIETY; C57BL MOUSE; GENE EXPRESSION; GENETICS; MALE; METABOLISM; MOUSE MUTANT;

MUS;

AFFECTIVE SYMPTOMS; AGGRESSION; AMYGDALA; ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; DEPRESSION; GENE DELETION; GENE EXPRESSION; LITHIUM; MALE; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; PREFRONTAL CORTEX; RECEPTORS, GLUTAMATE; SOCIAL BEHAVIOR DISORDERS;

EID: 84863279487     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0032969     Document Type: Article

References (109)

1. Lomeli H, Sprengel R, Laurie DJ, Kohr G, Herb A, et al. (1993) The rat delta-1 and delta-2 subunits extend the excitatory amino acid receptor family. FEBS Lett 315: 318-322.
2. Takayama C, Nakagawa S, Watanabe M, Mishina M, Inoue Y, (1996) Developmental changes in expression and distribution of the glutamate receptor channel delta 2 subunit according to the Purkinje cell maturation. Brain Res Dev Brain Res 92: 147-155.
3. Landsend AS, Amiry-Moghaddam M, Matsubara A, Bergersen L, Usami S, et al. (1997) Differential localization of delta glutamate receptors in the rat cerebellum: coexpression with AMPA receptors in parallel fiber-spine synapses and absence from climbing fiber-spine synapses. J Neurosci 17: 834-842.
4. Zhao HM, Wenthold RJ, Wang YX, Petralia RS, (1997) Delta-glutamate receptors are differentially distributed at parallel and climbing fiber synapses on Purkinje cells. J Neurochem 68: 1041-1052.
5. Kashiwabuchi N, Ikeda K, Araki K, Hirano T, Shibuki K, et al. (1995) Impairment of motor coordination, Purkinje cell synapse formation, and cerebellar long-term depression in GluR delta 2 mutant mice. Cell 81: 245-252.
6. Uemura T, Mishina M, (2008) The amino-terminal domain of glutamate receptor delta2 triggers presynaptic differentiation. Biochem Biophys Res Commun 377: 1315-1319.
7. Kakegawa W, Miyazaki T, Kohda K, Matsuda K, Emi K, et al. (2009) The N-terminal domain of GluD2 (GluRdelta2) recruits presynaptic terminals and regulates synaptogenesis in the cerebellum in vivo. J Neurosci 29: 5738-5748.
8. Kuroyanagi T, Yokoyama M, Hirano T, (2009) Postsynaptic glutamate receptor delta family contributes to presynaptic terminal differentiation and establishment of synaptic transmission. Proc Natl Acad Sci U S A 106: 4912-4916.
9. Safieddine S, Wenthold RJ, (1997) The glutamate receptor subunit delta1 is highly expressed in hair cells of the auditory and vestibular systems. J Neurosci 17: 7523-7531.
10. Gao J, Maison SF, Wu X, Hirose K, Jones SM, et al. (2007) Orphan glutamate receptor delta1 subunit required for high-frequency hearing. Mol Cell Biol 27: 4500-4512.
11. Mayat E, Petralia RS, Wang YX, Wenthold RJ, (1995) Immunoprecipitation, immunoblotting, and immunocytochemistry studies suggest that glutamate receptor delta subunits form novel postsynaptic receptor complexes. J Neurosci 15: 2533-2546.
12. Matsuda K, Miura E, Miyazaki T, Kakegawa W, Emi K, et al. (2010) Cbln1 is a ligand for an orphan glutamate receptor delta2, a bidirectional synapse organizer. Science 328: 363-368.
13. Uemura T, Lee SJ, Yasumura M, Takeuchi T, Yoshida T, et al. (2010) Trans-synaptic interaction of GluRdelta2 and Neurexin through Cbln1 mediates synapse formation in the cerebellum. Cell 141: 1068-1079.
14. Fallin MD, Lasseter VK, Avramopoulos D, Nicodemus KK, Wolyniec PS, et al. (2005) Bipolar I disorder and schizophrenia: a 440-single-nucleotide polymorphism screen of 64 candidate genes among Ashkenazi Jewish case-parent trios. Am J Hum Genet 77: 918-936.
15. Guo SZ, Huang K, Shi YY, Tang W, Zhou J, et al. (2007) A case-control association study between the GRID1 gene and schizophrenia in the Chinese Northern Han population. Schizophr Res 93: 385-390.
16. Venken T, Alaerts M, Souery D, Goossens D, Sluijs S, et al. (2008) Chromosome 10q harbors a susceptibility locus for bipolar disorder in Ashkenazi Jewish families. Mol Psychiatry 13: 442-450.
17. Treutlein J, Muhleisen TW, Frank J, Mattheisen M, Herms S, et al. (2009) Dissection of phenotype reveals possible association between schizophrenia and Glutamate Receptor Delta 1 (GRID1) gene promoter. Schizophr Res 111: 123-130.
18. Zhu Y, Kalbfleisch T, Brennan MD, Li Y, (2009) A MicroRNA gene is hosted in an intron of a schizophrenia-susceptibility gene. Schizophr Res 109: 86-89.
19. Greenwood TA, Lazzeroni LC, Murray SS, Cadenhead KS, Calkins ME, et al. (2011) Analysis of 94 candidate genes and 12 endophenotypes for schizophrenia from the consortium on the genetics of schizophrenia. Am J Psychiatry 168: 930-946.
20. Orsetti M, Di Brisco F, Canonico PL, Genazzani AA, Ghi P, (2008) Gene regulation in the frontal cortex of rats exposed to the chronic mild stress paradigm, an animal model of human depression. Eur J Neurosci 27: 2156-2164.
21. Orsetti M, Di Brisco F, Rinaldi M, Dallorto D, Ghi P, (2009) Some molecular effectors of antidepressant action of quetiapine revealed by DNA microarray in the frontal cortex of anhedonic rats. Pharmacogenet Genomics 19: 600-612.
22. Glessner JT, Wang K, Cai G, Korvatska O, Kim CE, et al. (2009) Autism genome-wide copy number variation reveals ubiquitin and neuronal genes. Nature 459: 569-573.
23. Smith M, Spence MA, Flodman P, (2009) Nuclear and mitochondrial genome defects in autisms. Ann N Y Acad Sci 1151: 102-132.
24. Cooper GM, Coe BP, Girirajan S, Rosenfeld JA, Vu TH, et al. (2011) A copy number variation morbidity map of developmental delay. Nat Genet 43: 838-846.
25. Balciuniene J, Feng N, Iyadurai K, Hirsch B, Charnas L, et al. (2007) Recurrent 10q22-q23 deletions: a genomic disorder on 10q associated with cognitive and behavioral abnormalities. Am J Hum Genet 80: 938-947.
26. van Bon BW, Balciuniene J, Fruhman G, Nagamani SC, Broome DL, et al. (2011) The phenotype of recurrent 10q22q23 deletions and duplications. Eur J Hum Genet 19: 400-408.
27. Shaltiel G, Maeng S, Malkesman O, Pearson B, Schloesser RJ, et al. (2008) Evidence for the involvement of the kainate receptor subunit GluR6 (GRIK2) in mediating behavioral displays related to behavioral symptoms of mania. Mol Psychiatry 13: 858-872.
28. Deutsch SI, Burket JA, Jacome LF, Cannon WR, Herndon AL, (2011) D-Cycloserine improves the impaired sociability of the Balb/c mouse. Brain Res Bull 84: 8-11.
29. McAllister KH, (1994) D-cycloserine enhances social behaviour in individually-housed mice in the resident-intruder test. Psychopharmacology (Berl) 116: 317-325.
30. Yang M, Crawley JN, (2009) Simple behavioral assessment of mouse olfaction. Curr Protoc Neurosci Chapter 8: Unit 8 24.
31. Hillman BG, Gupta SC, Stairs DJ, Buonanno A, Dravid SM, (2011) Behavioral analysis of NR2C knockout mouse reveals deficit in acquisition of conditioned fear and working memory. Neurobiol Learn Mem 95: 404-414.
32. Deacon RM, (2006) Digging and marble burying in mice: simple methods for in vivo identification of biological impacts. Nat Protoc 1: 122-124.
33. Walf AA, Frye CA, (2007) The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nat Protoc 2: 322-328.
34. Liu GX, Cai GQ, Cai YQ, Sheng ZJ, Jiang J, et al. (2007) Reduced anxiety and depression-like behaviors in mice lacking GABA transporter subtype 1. Neuropsychopharmacology 32: 1531-1539.
35. Strekalova T, Spanagel R, Bartsch D, Henn FA, Gass P, (2004) Stress-induced anhedonia in mice is associated with deficits in forced swimming and exploration. Neuropsychopharmacology 29: 2007-2017.
36. Saudou F, Amara DA, Dierich A, LeMeur M, Ramboz S, et al. (1994) Enhanced aggressive behavior in mice lacking 5-HT1B receptor. Science 265: 1875-1878.
37. Moy SS, Nadler JJ, Perez A, Barbaro RP, Johns JM, et al. (2004) Sociability and preference for social novelty in five inbred strains: an approach to assess autistic-like behavior in mice. Genes Brain Behav 3: 287-302.
38. Crawley JN, (2007) Mouse behavioral assays relevant to the symptoms of autism. Brain Pathol 17: 448-459.
39. Villasana LE, Klann E, Tejada-Simon MV, (2006) Rapid isolation of synaptoneurosomes and postsynaptic densities from adult mouse hippocampus. J Neurosci Methods 158: 30-36.
40. Goodwin FK, Jamison KR, (1990) Manic-Depressive Illness New York Oxford University Press.
41. Baldessarini RJ, Tondo L, (2000) Does lithium treatment still work? Evidence of stable responses over three decades. Arch Gen Psychiatry 57: 187-190.
42. Manji HK, Moore GJ, Chen G, (2001) Bipolar disorder: leads from the molecular and cellular mechanisms of action of mood stabilizers. Br J Psychiatry Suppl 41: s107-119.
43. Goodwin FKJK, (1990) Manic-Depressive Illness New York Oxford University Press.
44. Stevens KE, Johnson RG, Rose GM, (1997) Rats reared in social isolation show schizophrenia-like changes in auditory gating. Pharmacol Biochem Behav 58: 1031-1036.
45. Stilo SA, Murray RM, (2010) The epidemiology of schizophrenia: replacing dogma with knowledge. Dialogues Clin Neurosci 12: 305-315.
46. Sheinkopf SJ, (2005) Hot topics in autism: cognitive deficits, cognitive style, and joint attention dysfunction. Med Health R I 88: 152-153, 157-158.
47. Guo H, Hu Z, Zhao J, Xia K, (2011) Genetics of autism spectrum disorders. Zhong Nan Da Xue Xue Bao Yi Xue Ban 36: 703-711.
48. Crawley JN, (2004) Designing mouse behavioral tasks relevant to autistic-like behaviors. Ment Retard Dev Disabil Res Rev 10: 248-258.
49. Dravid SM, Burger PB, Prakash A, Geballe MT, Yadav R, et al. (2010) Structural determinants of D-cycloserine efficacy at the NR1/NR2C NMDA receptors. J Neurosci 30: 2741-2754.
50. Modi ME, Young LJ, (2011) D-cycloserine facilitates socially reinforced learning in an animal model relevant to autism spectrum disorders. Biol Psychiatry 70: 298-304.
51. Posey DJ, Kem DL, Swiezy NB, Sweeten TL, Wiegand RE, et al. (2004) A pilot study of D-cycloserine in subjects with autistic disorder. Am J Psychiatry 161: 2115-2117.
52. Adolphs R, Tranel D, Damasio AR, (1998) The human amygdala in social judgment. Nature 393: 470-474.
53. Franzen EA, Myers RE, (1973) Neural control of social behavior: prefrontal and anterior temporal cortex. Neuropsychologia 11: 141-157.
54. Anderson SW, Bechara A, Damasio H, Tranel D, Damasio AR, (1999) Impairment of social and moral behavior related to early damage in human prefrontal cortex. Nat Neurosci 2: 1032-1037.
55. Wood JN, (2003) Social cognition and the prefrontal cortex. Behav Cogn Neurosci Rev 2: 97-114.
56. Hall FS, Ghaed S, Pert A, Xing G, (2002) The effects of isolation rearing on glutamate receptor NMDAR1A mRNA expression determined by in situ hybridization in Fawn hooded and Wistar rats. Pharmacol Biochem Behav 73: 185-191.
57. Hermes G, Li N, Duman C, Duman R, (2011) Post-weaning chronic social isolation produces profound behavioral dysregulation with decreases in prefrontal cortex synaptic-associated protein expression in female rats. Physiol Behav 104: 354-359.
58. Prather MD, Lavenex P, Mauldin-Jourdain ML, Mason WA, Capitanio JP, et al. (2001) Increased social fear and decreased fear of objects in monkeys with neonatal amygdala lesions. Neuroscience 106: 653-658.
59. Amaral DG, (2002) The primate amygdala and the neurobiology of social behavior: implications for understanding social anxiety. Biol Psychiatry 51: 11-17.
60. Coccaro EF, McCloskey MS, Fitzgerald DA, Phan KL, (2007) Amygdala and orbitofrontal reactivity to social threat in individuals with impulsive aggression. Biol Psychiatry 62: 168-178.
61. Baumann N, Turpin JC, (2010) Neurochemistry of stress. An overview. Neurochem Res 35: 1875-1879.
62. Hofmann SG, Meuret AE, Smits JA, Simon NM, Pollack MH, et al. (2006) Augmentation of exposure therapy with D-cycloserine for social anxiety disorder. Arch Gen Psychiatry 63: 298-304.
63. Guastella AJ, Richardson R, Lovibond PF, Rapee RM, Gaston JE, et al. (2008) A randomized controlled trial of D-cycloserine enhancement of exposure therapy for social anxiety disorder. Biol Psychiatry 63: 544-549.
64. Sheinin A, Shavit S, Benveniste M, (2001) Subunit specificity and mechanism of action of NMDA partial agonist D-cycloserine. Neuropharmacology 41: 151-158.
65. Li N, Lee B, Liu RJ, Banasr M, Dwyer JM, et al. (2010) mTOR-dependent synapse formation underlies the rapid antidepressant effects of NMDA antagonists. Science 329: 959-964.
66. Garbett K, Ebert PJ, Mitchell A, Lintas C, Manzi B, et al. (2008) Immune transcriptome alterations in the temporal cortex of subjects with autism. Neurobiol Dis 30: 303-311.
67. Hirai H, Launey T, Mikawa S, Torashima T, Yanagihara D, et al. (2003) New role of delta2-glutamate receptors in AMPA receptor trafficking and cerebellar function. Nat Neurosci 6: 869-876.
68. Kohda K, Kamiya Y, Matsuda S, Kato K, Umemori H, et al. (2003) Heteromer formation of delta2 glutamate receptors with AMPA or kainate receptors. Brain Res Mol Brain Res 110: 27-37.
69. Kakegawa W, Yuzaki M, (2005) A mechanism underlying AMPA receptor trafficking during cerebellar long-term potentiation. Proc Natl Acad Sci U S A 102: 17846-17851.
70. Karolewicz B, Szebeni K, Gilmore T, Maciag D, Stockmeier CA, et al. (2009) Elevated levels of NR2A and PSD-95 in the lateral amygdala in depression. Int J Neuropsychopharmacol 12: 143-153.
71. Sheline YI, Gado MH, Price JL, (1998) Amygdala core nuclei volumes are decreased in recurrent major depression. Neuroreport 9: 2023-2028.
72. Davidson RJ, Pizzagalli D, Nitschke JB, Putnam K, (2002) Depression: perspectives from affective neuroscience. Annu Rev Psychol 53: 545-574.
73. Drevets WC, (2000) Neuroimaging studies of mood disorders. Biol Psychiatry 48: 813-829.
74. Klimek V, Schenck JE, Han H, Stockmeier CA, Ordway GA, (2002) Dopaminergic abnormalities in amygdaloid nuclei in major depression: a postmortem study. Biol Psychiatry 52: 740-748.
75. Bremner JD, Vythilingam M, Vermetten E, Nazeer A, Adil J, et al. (2002) Reduced volume of orbitofrontal cortex in major depression. Biol Psychiatry 51: 273-279.
76. Koenigs M, Huey ED, Calamia M, Raymont V, Tranel D, et al. (2008) Distinct regions of prefrontal cortex mediate resistance and vulnerability to depression. J Neurosci 28: 12341-12348.
77. Padberg F, George MS, (2009) Repetitive transcranial magnetic stimulation of the prefrontal cortex in depression. Exp Neurol 219: 2-13.
78. Sanacora G, Fenton LR, Fasula MK, Rothman DL, Levin Y, et al. (2006) Cortical gamma-aminobutyric acid concentrations in depressed patients receiving cognitive behavioral therapy. Biol Psychiatry 59: 284-286.
79. Hashimoto K, Sawa A, Iyo M, (2007) Increased levels of glutamate in brains from patients with mood disorders. Biol Psychiatry 62: 1310-1316.
80. Feyissa AM, Woolverton WL, Miguel-Hidalgo JJ, Wang Z, Kyle PB, et al. (2010) Elevated level of metabotropic glutamate receptor 2/3 in the prefrontal cortex in major depression. Prog Neuropsychopharmacol Biol Psychiatry 34: 279-283.
81. Taylor MJ, Mannie ZN, Norbury R, Near J, Cowen PJ, (2011) Elevated cortical glutamate in young people at increased familial risk of depression. Int J Neuropsychopharmacol 14: 255-259.
82. Schmitt A, Hasan A, Gruber O, Falkai P, (2011) Schizophrenia as a disorder of disconnectivity. Eur Arch Psychiatry Clin Neurosci.
83. Hines RM, Wu L, Hines DJ, Steenland H, Mansour S, et al. (2008) Synaptic imbalance, stereotypies, and impaired social interactions in mice with altered neuroligin 2 expression. J Neurosci 28: 6055-6067.
84. Yizhar O, Fenno LE, Prigge M, Schneider F, Davidson TJ, et al. (2011) Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature 477: 171-178.
85. Harrison PJ, McLaughlin D, Kerwin RW, (1991) Decreased hippocampal expression of a glutamate receptor gene in schizophrenia. Lancet 337: 450-452.
86. Eastwood SL, McDonald B, Burnet PW, Beckwith JP, Kerwin RW, et al. (1995) Decreased expression of mRNAs encoding non-NMDA glutamate receptors GluR1 and GluR2 in medial temporal lobe neurons in schizophrenia. Brain Res Mol Brain Res 29: 211-223.
87. Eastwood SL, Burnet PW, Harrison PJ, (1997) GluR2 glutamate receptor subunit flip and flop isoforms are decreased in the hippocampal formation in schizophrenia: a reverse transcriptase-polymerase chain reaction (RT-PCR) study. Brain Res Mol Brain Res 44: 92-98.
88. Porter RH, Eastwood SL, Harrison PJ, (1997) Distribution of kainate receptor subunit mRNAs in human hippocampus, neocortex and cerebellum, and bilateral reduction of hippocampal GluR6 and KA2 transcripts in schizophrenia. Brain Res 751: 217-231.
89. Scarr EPG, Sundram S, MacKinnon A, Dean B, (2003) Decreased hippocampal NMDA, but not kainate or AMPA receptors in bipolar disorder. Bipolar Disord 5: 257-264.
90. Beneyto M, Kristiansen LV, Oni-Orisan A, McCullumsmith RE, Meador-Woodruff JH, (2007) Abnormal glutamate receptor expression in the medial temporal lobe in schizophrenia and mood disorders. Neuropsychopharmacology 32: 1888-1902.
91. Ng WX, Lau IY, Graham S, Sim K, (2009) Neurobiological evidence for thalamic, hippocampal and related glutamatergic abnormalities in bipolar disorder: a review and synthesis. Neurosci Biobehav Rev 33: 336-354.
92. Du J, Gray NA, Falke C, Yuan P, Szabo S, et al. (2003) Structurally dissimilar antimanic agents modulate synaptic plasticity by regulating AMPA glutamate receptor subunit GluR1 synaptic expression. Ann N Y Acad Sci 1003: 378-380.
93. Du J, Creson TK, Wu LJ, Ren M, Gray NA, et al. (2008) The role of hippocampal GluR1 and GluR2 receptors in manic-like behavior. J Neurosci 28: 68-79.
94. Fallin MD, Lasseter VK, Wolyniec PS, McGrath JA, Nestadt G, et al. (2003) Genomewide linkage scan for schizophrenia susceptibility loci among Ashkenazi Jewish families shows evidence of linkage on chromosome 10q22. Am J Hum Genet 73: 601-611.
95. Lerer B, Segman RH, Hamdan A, Kanyas K, Karni O, et al. (2003) Genome scan of Arab Israeli families maps a schizophrenia susceptibility gene to chromosome 6q23 and supports a locus at chromosome 10q24. Mol Psychiatry 8: 488-498.
96. Carter CS, (2007) Some rewarding insights into the cognitive and neurobiological basis of negative symptoms in schizophrenia. Biol Psychiatry 62: 709-710.
97. Carroll LS, Owen MJ, (2009) Genetic overlap between autism, schizophrenia and bipolar disorder. Genome Med 1: 102.
98. Lachman HM, Stopkova P, Papolos DF, Pedrosa E, Margolis B, et al. (2006) Analysis of synapsin III-196 promoter mutation in schizophrenia and bipolar disorder. Neuropsychobiology 53: 57-62.
99. Gauthier J, Champagne N, Lafreniere RG, Xiong L, Spiegelman D, et al. (2010) De novo mutations in the gene encoding the synaptic scaffolding protein SHANK3 in patients ascertained for schizophrenia. Proc Natl Acad Sci U S A 107: 7863-7868.
100. Tabuchi K, Blundell J, Etherton MR, Hammer RE, Liu X, et al. (2007) A neuroligin-3 mutation implicated in autism increases inhibitory synaptic transmission in mice. Science 318: 71-76.
101. Kim S, Webster MJ, (2010) Correlation analysis between genome-wide expression profiles and cytoarchitectural abnormalities in the prefrontal cortex of psychiatric disorders. Mol Psychiatry 15: 326-336.
102. Jamain S, Quach H, Betancur C, Rastam M, Colineaux C, et al. (2003) Mutations of the X-linked genes encoding neuroligins NLGN3 and NLGN4 are associated with autism. Nat Genet 34: 27-29.
103. Durand CM, Betancur C, Boeckers TM, Bockmann J, Chaste P, et al. (2007) Mutations in the gene encoding the synaptic scaffolding protein SHANK3 are associated with autism spectrum disorders. Nat Genet 39: 25-27.
104. Shah AK, Tioleco NM, Nolan K, Locker J, Groh K, et al. (2010) Rare NRXN1 promoter variants in patients with schizophrenia. Neurosci Lett 475: 80-84.
105. Muhleisen TW, Basmanav FB, Forstner AJ, Mattheisen M, Priebe L, et al. (2011) Resequencing and follow-up of neurexin 1 (NRXN1) in schizophrenia patients. Schizophr Res 127: 35-40.
106. Yue W, Yang Y, Zhang Y, Lu T, Hu X, et al. (2011) A case-control association study of NRXN1 polymorphisms with schizophrenia in Chinese Han population. Behav Brain Funct 7: 7.
107. Nestler EJ, Gould E, Manji H, Buncan M, Duman RS, et al. (2002) Preclinical models: status of basic research in depression. Biol Psychiatry 52: 503-528.
108. Prickaerts J, Moechars D, Cryns K, Lenaerts I, van Craenendonck H, et al. (2006) Transgenic mice overexpressing glycogen synthase kinase 3beta: a putative model of hyperactivity and mania. J Neurosci 26: 9022-9029.
109. Roybal K, Theobold D, Graham A, DiNieri JA, Russo SJ, et al. (2007) Mania-like behavior induced by disruption of CLOCK. Proc Natl Acad Sci U S A 104: 6406-6411.