DISC1: A key lead in studying cortical development and associated brain disorders

Neuroscientist

Volumn 19, Issue 5, 2013, Pages 451-464

  Narayan, Soumya ^a   Nakajima, Kazunori ^b   Sawa, Akira ^a  

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

^b KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

cortex; corticogenesis; development; DISC1; probe

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; AMYLOID PRECURSOR PROTEIN; BARDET BIEDL SYNDROME PROTEIN; BETA CATENIN; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR 3; EPIDERMAL GROWTH FACTOR RECEPTOR 4; GLYCOGEN SYNTHASE KINASE 3BETA; LISSENCEPHALY PROTEIN; NEU DIFFERENTIATION FACTOR; NUCLEAR DISTRIBUTION ELEMENT 1; NUCLEAR DISTRIBUTION ELEMENT LIKE 1; PERICENTRIOLAR MATERIAL 1 PROTEIN; PROTEIN; REELIN; UNCLASSIFIED DRUG; WNT PROTEIN;

ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN DISEASE; CELL DIVISION; CELL INTERACTION; CELL MIGRATION; CENTROSOME; CYTOMEGALOVIRUS INFECTION; DENDRITE; ENVIRONMENTAL FACTOR; GENE MUTATION; HUMAN; INTERNEURON; LOCOMOTION; MICROENVIRONMENT; MICROTUBULE; MITOSIS; NERVE FIBER; NERVE FIBER GROWTH; NEURAL STEM CELL; NEWBORN HYPOXIA; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; WILD TYPE;

CORTEX; CORTICOGENESIS; DEVELOPMENT; DISC1; PROBE;

ANIMALS; BRAIN; BRAIN DISEASES; DISEASE MODELS, ANIMAL; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MENTAL DISORDERS; NERVE TISSUE PROTEINS;

EID: 84883702553     PISSN: 10738584     EISSN: 10894098     Source Type: Journal    
DOI: 10.1177/1073858412470168     Document Type: Article

References (153)

1. Abazyan B, Nomura J, Kannan G, Ishizuka K, Tamashiro KL, Nucifora F. Prenatal interaction of mutant DISC1 and immune activation produces adult psychopathology. Biol Psychiatry. 2010 ; 68 (12). 1172-81
2. Alkuraya FS, Cai X, Emery C, Mochida GH, Al-Dosari MS, Felie JM. Human mutations in NDE1 cause extreme microcephaly with lissencephaly [corrected]. Am J Hum Genet. 2011 ; 88 (5). 536-47
3. Anderson SA, Eisenstat DD, Shi L, Rubenstein JL. Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science. 1997 ; 278 (5337). 474-6
4. Assadi AH, Zhang G, Beffert U, McNeil RS, Renfro AL, Niu S. Interaction of reelin signaling and Lis1 in brain development. Nat Genet. 2003 ; 35 (3). 270-6
5. Ayala R, Shu T, Tsai LH. Trekking across the brain: the journey of neuronal migration. Cell.. 2007 ; 128 (1). 29-43
6. Badano JL, Teslovich TM, Katsanis N. The centrosome in human genetic disease. Nat Rev Genet. 2005 ; 6 (3). 194-205
7. Bar I, Lambert De Rouvroit C, Royaux I, Krizman DB, Dernoncourt C, Ruelle D. A YAC contig containing the reeler locus with preliminary characterization of candidate gene fragments. Genomics. 1995 ; 26 (3). 543-9
8. Barinaga M. Guiding neurons to the cortex. Science. 1996 ; 274 (5290). 1100-1
9. Blackwood DH, Fordyce A, Walker MT, St Clair DM, Porteous DJ, Muir WJ. Schizophrenia and affective disorders - cosegregation with a translocation at chromosome 1q42 that directly disrupts brain-expressed genes: clinical and P300 findings in a family. Am J Hum Genet. 2001 ; 69 (2). 428-33
10. Boycott KM, Bonnemann C, Herz J, Neuert S, Beaulieu C, Scott JN. Mutations in VLDLR as a cause for autosomal recessive cerebellar ataxia with mental retardation (dysequilibrium syndrome). J Child Neurol. 2009 ; 24 (10). 1310-5
11. Bradshaw NJ, Ogawa F, Antolin-Fontes B, Chubb JE, Carlyle BC, Christie S. DISC1, PDE4B, and NDE1 at the centrosome and synapse. Biochem Biophys Res Commun. 2008 ; 377 (4). 1091-6
12. Brandon NJ, Sawa A. Linking neurodevelopmental and synaptic theories of mental illness through DISC1. Nat Rev Neurosci. 2011 ; 12 (12). 707-22
13. Brauns S, Gollub RL, Roffman JL, Yendiki A, Ho BC, Wassink TH. DISC1 is associated with cortical thickness and neural efficiency. Neuroimage. 2011 ; 57 (4). 1591-600
14. Burdick KE, Kamiya A, Hodgkinson CA, Lencz T, DeRosse P, Ishizuka K. Elucidating the relationship between DISC1, NDEL1 and NDE1 and the risk for schizophrenia: evidence of epistasis and competitive binding. Hum Mol Genet. 2008 ; 17 (16). 2462-73
15. Bystron I, Blakemore C, Rakic P. Development of the human cerebral cortex: Boulder Committee revisited. Nat Rev Neurosci. 2008 ; 9 (2). 110-22
16. Callicott JH, Straub RE, Pezawas L, Egan MF, Mattay VS, Hariri AR. Variation in DISC1 affects hippocampal structure and function and increases risk for schizophrenia. Proc Natl Acad Sci U S A. 2005 ; 102 (24). 8627-32
17. Camargo LM, Collura V, Rain JC, Mizuguchi K, Hermjakob H, Kerrien S. Disrupted in Schizophrenia 1 Interactome: evidence for the close connectivity of risk genes and a potential synaptic basis for schizophrenia. Mol Psychiatry. 2007 ; 12 (1). 74-86
18. Cannon TD, Hennah W, van Erp TG, Thompson PM, Lonnqvist J, Huttunen M. Association of DISC1/TRAX haplotypes with schizophrenia, reduced prefrontal gray matter, and impaired short- and long-term memory. Arch Gen Psychiatry. 2005 ; 62 (11). 1205-13
19. Carless MA, Glahn DC, Johnson MP, Curran JE, Bozaoglu K, Dyer TD. Impact of DISC1 variation on neuroanatomical and neurocognitive phenotypes. Mol Psychiatry. 2011 ; 16 (11). 1096-104
20. Cassidy F, Roche S, Claffey E, McKeon P. First family-based test for association of neuregulin with bipolar affective disorder. Mol Psychiatry. 2006 ; 11 (8). 706-7
21. Chang BS, Duzcan F, Kim S, Cinbis M, Aggarwal A, Apse KA. The role of RELN in lissencephaly and neuropsychiatric disease. Am J Med Genet B Neuropsychiatr Genet. 2007 ; 144B (1). 58-63
22. Cheeran MC, Lokensgard JR, Schleiss MR. Neuropathogenesis of congenital cytomegalovirus infection: disease mechanisms and prospects for intervention. Clin Microbiol Rev. 2009 ; 22 (1). 99-126
23. Chen PL, Avramopoulos D, Lasseter VK, McGrath JA, Fallin MD, Liang KY. Fine mapping on chromosome 10q22-q23 implicates Neuregulin 3 in schizophrenia. Am J Hum Genet. 2009 ; 84 (1). 21-34
24. Chenn A, Walsh CA. Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science. 2002 ; 297 (5580). 365-9
25. Clapcote SJ, Lipina TV, Millar JK, Mackie S, Christie S, Ogawa F. Behavioral phenotypes of Disc1 missense mutations in mice. Neuron. 2007 ; 54 (3). 387-402
26. Clevers H, Nusse R. Wnt/beta-catenin signaling and disease. Cell. 2012 ; 149 (6). 1192-205
27. Corfas G, Roy K, Buxbaum JD. Neuregulin 1-erbB signaling and the molecular/cellular basis of schizophrenia. Nat Neurosci. 2004 ; 7 (6). 575-80
28. D'Arcangelo G, Miao GG, Chen SC, Soares HD, Morgan JI, Curran T. A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature. 1995 ; 374 (6524). 719-23
29. Datta SR, McQuillin A, Rizig M, Blaveri E, Thirumalai S, Kalsi G. A threonine to isoleucine missense mutation in the pericentriolar material 1 gene is strongly associated with schizophrenia. Mol Psychiatry. 2010 ; 15 (6). 615-28
30. Dehay C, Kennedy H. Cell-cycle control and cortical development. Nat Rev Neurosci. 2007 ; 8 (6). 438-50
31. Derrick M, Drobyshevsky A, Ji X, Tan S. A model of cerebral palsy from fetal hypoxia-ischemia. Stroke. 2007 ; 38: 731-5
32. Dohner K, Nagel CH, Sodeik B. Viral stop-and-go along microtubules: taking a ride with dynein and kinesins. Trends Microbiol. 2005 ; 13 (7). 320-7
33. Dohner K, Sodeik B. The role of the cytoskeleton during viral infection. Curr Top Microbiol Immunol. 2005 ; 285: 67-108
34. Fatemi SH, Earle JA, McMenomy T. Reduction in Reelin immunoreactivity in hippocampus of subjects with schizophrenia, bipolar disorder and major depression. Mol Psychiatry. 2000 ; 5 (6). 654-63
35. Faulkner NE, Dujardin DL, Tai CY, Vaughan KT, O'Connell CB, Wang Y. A role for the lissencephaly gene LIS1 in mitosis and cytoplasmic dynein function. Nat Cell Biol. 2000 ; 2 (11). 784-91
36. Feng Y, Walsh CA. Mitotic spindle regulation by Nde1 controls cerebral cortical size. Neuron. 2004 ; 44 (2). 279-93
37. Flames N, Long JE, Garratt AN, Fischer TM, Gassmann M, Birchmeier C. Short- and long-range attraction of cortical GABAergic interneurons by neuregulin-1. Neuron. 2004 ; 44 (2). 251-61
38. Francis F, Meyer G, Fallet-Bianco C, Moreno S, Kappeler C, Socorro AC. Human disorders of cortical development: from past to present. Eur J Neurosci. 2006 ; 23 (4). 877-93
39. Ge X, Frank CL, Calderon de, Anda F, Tsai LH. Hook3 interacts with PCM1 to regulate pericentriolar material assembly and the timing of neurogenesis. Neuron. 2010 ; 65 (2). 191-203
40. Gelman DM, Martini FJ, Nobrega-Pereira S, Pierani A, Kessaris N, Marin O. The embryonic preoptic area is a novel source of cortical GABAergic interneurons. J Neurosci. 2009 ; 29 (29). 9380-9
41. Ghashghaei HT, Weber J, Pevny L, Schmid R, Schwab MH, Lloyd KC. The role of neuregulin-ErbB4 interactions on the proliferation and organization of cells in the subventricular zone. Proc Natl Acad Sci U S A. 2006 ; 103 (6). 1930-5
42. Grabham PW, Seale GE, Bennecib M, Goldberg DJ, Vallee RB. Cytoplasmic dynein and LIS1 are required for microtubule advance during growth cone remodeling and fast axonal outgrowth. J Neurosci. 2007 ; 27 (21). 5823-34
43. Guerrini R, Dobyns WB, Barkovich AJ. Abnormal development of the human cerebral cortex: genetics, functional consequences and treatment options. Trends Neurosci. 2008 ; 31 (3). 154-62
44. Guidotti A, Auta J, Davis JM, Di-Giorgi-Gerevini V, Dwivedi Y, Grayson DR. Decrease in reelin and glutamic acid decarboxylase67 (GAD67) expression in schizophrenia and bipolar disorder: a postmortem brain study. Arch Gen Psychiatry. 2000 ; 57 (11). 1061-9
45. Gupta A, Tsai LH, Wynshaw-Boris A. Life is a journey: a genetic look at neocortical development. Nat Rev Genet. 2002 ; 3 (5). 342-55
46. Gurling HM, Critchley H, Datta SR, McQuillin A, Blaveri E, Thirumalai S. Genetic association and brain morphology studies and the chromosome 8p22 pericentriolar material 1 (PCM1) gene in susceptibility to schizophrenia. Arch Gen Psychiatry. 2006 ; 63 (8). 844-54
47. Hashimoto R, Numakawa T, Ohnishi T, Kumamaru E, Yagasaki Y, Ishimoto T. Impact of the DISC1 Ser704Cys polymorphism on risk for major depression, brain morphology and ERK signaling. Hum Mol Genet. 2006 ; 15 (20). 3024-33
48. Hayashi MA, Guerreiro JR, Charych E, Kamiya A, Barbosa RL, Machado MF. Assessing the role of endooligopeptidase activity of Ndel1 (nuclear-distribution gene E homolog like-1) in neurite outgrowth. Mol Cell Neurosci. 2010 ; 44 (4). 353-61
49. Heng JI, Chariot A, Nguyen L. Molecular layers underlying cytoskeletal remodelling during cortical development. Trends Neurosci. 2010 ; 33 (1). 38-47
50. Higginbotham HR, Gleeson JG. The centrosome in neuronal development. Trends Neurosci. 2007 ; 30 (6). 276-83
51. Hikida T, Jaaro-Peled H, Seshadri S, Oishi K, Hookway C, Kong S. Dominant-negative DISC1 transgenic mice display schizophrenia-associated phenotypes detected by measures translatable to humans. Proc Natl Acad Sci U S A. 2007 ; 104 (36). 14501-6
52. Hirabayashi Y, Itoh Y, Tabata H, Nakajima K, Akiyama T, Masuyama N. The Wnt/beta-catenin pathway directs neuronal differentiation of cortical neural precursor cells. Development. 2004 ; 131 (12). 2791-801
53. Hirotsune S, Takahara T, Sasaki N, Hirose K, Yoshiki A, Ohashi T. The reeler gene encodes a protein with an EGF-like motif expressed by pioneer neurons. Nat Genet. 1995 ; 10 (1). 77-83
54. Hodgkinson CA, Goldman D, Jaeger J, Persaud S, Kane JM, Lipsky RH. Disrupted in schizophrenia 1 (DISC1): association with schizophrenia, schizoaffective disorder, and bipolar disorder. Am J Hum Genet. 2004 ; 75 (5). 862-72
55. Hong SE, Shugart YY, Huang DT, Shahwan SA, Grant PE, Hourihane JO. Autosomal recessive lissencephaly with cerebellar hypoplasia is associated with human RELN mutations. Nat Genet. 2000 ; 26 (1). 93-6
56. Ibi D, Nagai T, Koike H, Kitahara Y, Mizoguchi H, Niwa M. Combined effect of neonatal immune activation and mutant DISC1 on phenotypic changes in adulthood. Behav Brain Res. 2010 ; 206 (1). 32-7
57. Ikonomidou C, Bittigau P, Ishimaru MJ, Wozniak DF, Koch C, Genz K. Ethanol-induced apoptotic neurodegeneration and fetal alcohol syndrome. Science. 2000 ; 287 (5455). 1056-60
58. Inkster B, Nichols TE, Saemann PG, Auer DP, Holsboer F, Muglia P. Association of GSK3beta polymorphisms with brain structural changes in major depressive disorder. Arch Gen Psychiatry. 2009 ; 66 (7). 721-8
59. Inkster B, Nichols TE, Saemann PG, Auer DP, Holsboer F, Muglia P. Pathway-based approaches to imaging genetics association studies: Wnt signaling, GSK3beta substrates and major depression. Neuroimage. 2010 ; 53 (3). 908-17
60. Ishizuka K, Kamiya A, Oh EC, Kanki H, Seshadri S, Robinson JF. DISC1-dependent switch from progenitor proliferation to migration in the developing cortex. Nature. 2011 ; 473 (7345). 92-6
61. Johnstone M, Thomson PA, Hall J, McIntosh AM, Lawrie SM, Porteous DJ. DISC1 in schizophrenia: genetic mouse models and human genomic imaging. Schizophr Bull. 2011 ; 37 (1). 14-20
62. Kahler AK, Rimol LM, Brown AA, Djurovic S, Hartberg CB, Melle I. Effect of DISC1 SNPs on brain structure in healthy controls and patients with a history of psychosis. Am J Med Genet B Neuropsychiatr Genet. 2012 ; 159B (6). 722-30
63. Kamiya A, Kubo K, Tomoda T, Takaki M, Youn R, Ozeki Y. A schizophrenia-associated mutation of DISC1 perturbs cerebral cortex development. Nat Cell Biol. 2005 ; 7 (12). 1167-78
64. Kamiya A, Tan PL, Kubo K, Engelhard C, Ishizuka K, Kubo A. Recruitment of PCM1 to the centrosome by the cooperative action of DISC1 and BBS4: a candidate for psychiatric illnesses. Arch Gen Psychiatry. 2008 ; 65 (9). 996-1006
65. Kamiya A, Tomoda T, Chang J, Takaki M, Zhan C, Morita M. DISC1-NDEL1/NUDEL protein interaction, an essential component for neurite outgrowth, is modulated by genetic variations of DISC1. Hum Mol Genet. 2006 ; 15 (22). 3313-23
66. Kanatani S, Yozu M, Tabata H, Nakajima K. COUP-TFII is preferentially expressed in the caudal ganglionic eminence and is involved in the caudal migratory stream. J Neurosci. 2008 ; 28 (50). 13582-91
67. Kardon JR, Vale RD. Regulators of the cytoplasmic dynein motor. Nat Rev Mol Cell Biol. 2009 ; 10 (12). 854-65
68. Katsanis N, Lupski JR, Beales PL. Exploring the molecular basis of Bardet-Biedl syndrome. Hum Mol Genet. 2001 ; 10 (20). 2293-9
69. Kim JC, Badano JL, Sibold S, Esmail MA, Hill J, Hoskins BE. The Bardet-Biedl protein BBS4 targets cargo to the pericentriolar region and is required for microtubule anchoring and cell cycle progression. Nat Genet. 2004 ; 36 (5). 462-70
70. Koike H, Arguello PA, Kvajo M, Karayiorgou M, Gogos JA. Disc1 is mutated in the 129S6/SvEv strain and modulates working memory in mice. Proc Natl Acad Sci U S A. 2006 ; 103 (10). 3693-7
71. Kosugi I, Shinmura Y, Kawasaki H, Arai Y, Li RY, Baba S. Cytomegalovirus infection of the central nervous system stem cells from mouse embryo: a model for developmental brain disorders induced by cytomegalovirus. Lab Invest. 2000 ; 80 (9). 1373-83
72. Kuroda K, Yamada S, Tanaka M, Iizuka M, Yano H, Mori D. Behavioral alterations associated with targeted disruption of exons 2 and 3 of the Disc1 gene in the mouse. Hum Mol Genet. 2011 ; 20 (23). 4666-83
73. Lachman HM, Pedrosa E, Petruolo OA, Cockerham M, Papolos A, Novak T. Increase in GSK3beta gene copy number variation in bipolar disorder. Am J Med Genet B Neuropsychiatr Genet. 2007 ; 144B (3). 259-65
74. Li J, Lee WL, Cooper JA. NudEL targets dynein to microtubule ends through LIS1. Nat Cell Biol. 2005 ; 7 (7). 686-90
75. Li W, Zhou Y, Jentsch JD, Brown RA, Tian X, Ehninger D. Specific developmental disruption of disrupted- in-schizophrenia-1 function results in schizophrenia-related phenotypes in mice. Proc Natl Acad Sci U S A. 2007 ; 104 (46). 18280-5
76. Libbey JE, Sweeten TL, McMahon WM, Fujinami RS. Autistic disorder and viral infections. J Neurovirol. 2005 ; 11 (1). 1-10
77. Lipina TV, Kaidanovich-Beilin O, Patel S, Wang M, Clapcote SJ, Liu F. Genetic and pharmacological evidence for schizophrenia-related Disc1 interaction with GSK-3. Synapse. 2011 ; 65 (3). 234-48
78. Lipina TV, Wang M, Liu F, Roder JC. Synergistic interactions between PDE4B and GSK-3: DISC1 mutant mice. Neuropharmacology. 2012 ; 62 (3). 1252-62
79. Liu Y, Ford BD, Mann MA, Fischbach GD. Neuregulin-1 increases the proliferation of neuronal progenitors from embryonic neural stem cells. Dev Biol. 2005 ; 283 (2). 437-45
80. Lo Nigro C, Chong CS, Smith AC, Dobyns WB, Carrozzo R, Ledbetter DH. Point mutations and an intragenic deletion in LIS1, the lissencephaly causative gene in isolated lissencephaly sequence and Miller-Dieker syndrome. Hum Mol Genet. 1997 ; 6 (2). 157-64
81. LoTurco JJ, Bai J. The multipolar stage and disruptions in neuronal migration. Trends Neurosci. 2006 ; 29 (7). 407-13
82. Mahmood S, Ahmad W, Hassan MJ. Autosomal recessive primary microcephaly (MCPH): clinical manifestations, genetic heterogeneity and mutation continuum. Orphanet J Rare Dis. 2011 ; 6: 39
83. Malavasi EL, Ogawa F, Porteous DJ, Millar JK. DISC1 variants 37W and 607F disrupt its nuclear targeting and regulatory role in ATF4-mediated transcription. Hum Mol Genet. 2012 ; 21 (12). 2779-92
84. Manzini MC, Walsh CA. What disorders of cortical development tell us about the cortex: one plus one does not always make two. Curr Opin Genet Dev. 2011 ; 21 (3). 333-9
85. Mao Y, Ge X, Frank CL, Madison JM, Koehler AN, Doud MK. Disrupted in schizophrenia 1 regulates neuronal progenitor proliferation via modulation of GSK3beta/beta-catenin signaling. Cell. 2009 ; 136 (6). 1017-31
86. Maricich SM, Gilmore EC, Herrup K. The role of tangential migration in the establishment of mammalian cortex. Neuron. 2001 ; 31 (2). 175-8
87. Marin O, Rubenstein JL. A long, remarkable journey: tangential migration in the telencephalon. Nat Rev Neurosci. 2001 ; 2 (11). 780-90
88. Marin O, Valiente M, Ge X, Tsai LH. Guiding neuronal cell migrations. Cold Spring Harb Perspect Biol. 2010 ; 2 (2). a001834
89. Matigian N, Windus L, Smith H, Filippich C, Pantelis C, McGrath J. Expression profiling in monozygotic twins discordant for bipolar disorder reveals dysregulation of the WNT signalling pathway. Mol Psychiatry. 2007 ; 12 (9). 815-25
90. Mei L, Xiong WC. Neuregulin 1 in neural development, synaptic plasticity and schizophrenia. Nat Rev Neurosci. 2008 ; 9 (6). 437-52
91. Millar JK, Wilson-Annan JC, Anderson S, Christie S, Taylor MS, Semple CA. Disruption of two novel genes by a translocation co-segregating with schizophrenia. Hum Mol Genet. 2000 ; 9 (9). 1415-23
92. Miyoshi K, Honda A, Baba K, Taniguchi M, Oono K, Fujita T. Disrupted-In-Schizophrenia 1, a candidate gene for schizophrenia, participates in neurite outgrowth. Mol Psychiatry. 2003 ; 8 (7). 685-94
93. Mochida GH, Walsh CA. Genetic basis of developmental malformations of the cerebral cortex. Arch Neurol. 2004 ; 61 (5). 637-40
94. Morris JA, Kandpal G, Ma L, Austin CP. DISC1 (Disrupted-In-Schizophrenia 1) is a centrosome-associated protein that interacts with MAP1A, MIPT3, ATF4/5 and NUDEL: regulation and loss of interaction with mutation. Hum Mol Genet. 2003 ; 12 (13). 1591-608
95. Nadarajah B, Brunstrom JE, Grutzendler J, Wong RO, Pearlman AL. Two modes of radial migration in early development of the cerebral cortex. Nat Neurosci. 2001 ; 4 (2). 143-50
96. Nagai T, Kitahara Y, Ibi D, Nabeshima T, Sawa A, Yamada K. Effects of antipsychotics on the behavioral deficits in human dominant-negative DISC1 transgenic mice with neonatal polyI:C treatment. Behav Brain Res. 2011 ; 225 (1). 305-10
97. Nakajima K. Control of tangential/non-radial migration of neurons in the developing cerebral cortex. Neurochem Int. 2007 ; 51 (2-4). 121-31
98. Nigg EA, Stearns T. The centrosome cycle: centriole biogenesis, duplication and inherent asymmetries. Nat Cell Biol. 2011 ; 13 (10). 1154-60
99. Niwa M, Kamiya A, Murai R, Kubo K, Gruber AJ, Tomita K. Knockdown of DISC1 by in utero gene transfer disturbs postnatal dopaminergic maturation in the frontal cortex and leads to adult behavioral deficits. Neuron. 2010 ; 65 (4). 480-9
100. Noctor SC, Martinez-Cerdeno V, Ivic L, Kriegstein AR. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci. 2004 ; 7 (2). 136-44
101. Ogawa M, Miyata T, Nakajima K, Yagyu K, Seike M, Ikenaka K. The reeler gene-associated antigen on Cajal-Retzius neurons is a crucial molecule for laminar organization of cortical neurons. Neuron. 1995 ; 14 (5). 899-912
102. Okerlund ND, Cheyette BN. Synaptic Wnt signaling - a contributor to major psychiatric disorders?. J Neurodev Disord. 2011 ; 3 (2). 162-74
103. Ozeki Y, Tomoda T, Kleiderlein J, Kamiya A, Bord L, Fujii K. Disrupted-in-Schizophrenia-1 (DISC-1): mutant truncation prevents binding to NudE-like (NUDEL) and inhibits neurite outgrowth. Proc Natl Acad Sci U S A. 2003 ; 100 (1). 289-94
104. Pan CL, Garriga G. Fresh air is good for nerves: hypoxia disturbs axon guidance. Nat Neurosci. 2008 ; 11 (8). 859-61
105. Pearce BD. Schizophrenia and viral infection during neurodevelopment: a focus on mechanisms. Mol Psychiatry. 2001 ; 6 (6). 634-46
106. Persico AM, D'Agruma L, Maiorano N, Totaro A, Militerni R, Bravaccio C. Reelin gene alleles and haplotypes as a factor predisposing to autistic disorder. Mol Psychiatry. 2001 ; 6 (2). 150-9
107. Pletnikov MV, Ayhan Y, Nikolskaia O, Xu Y, Ovanesov MV, Huang H. Inducible expression of mutant human DISC1 in mice is associated with brain and behavioral abnormalities reminiscent of schizophrenia. Mol Psychiatry. 2008 ; 13 (2). 173-86
108. Pocock R, Hobert O. Oxygen levels affect axon guidance and neuronal migration in Caenorhabditis elegans. Nat Neurosci. 2008 ; 11 (8). 894-900
109. Porteous DJ, Millar JK, Brandon NJ, Sawa A. DISC1 at 10: connecting psychiatric genetics and neuroscience. Trends Mol Med.. 2011 ; 17 (12). 699-706
110. Rakic P. Mode of cell migration to the superficial layers of fetal monkey neocortex. J Comp Neurol. 1972 ; 145 (1). 61-83
111. Rees S, Breen S, Loeliger M, McCrabb G, Harding R. Hypoxemia near mid-gestation has long-term effects on fetal brain development. J Neuropathol Exp Neurol. 1999 ; 58 (9). 932-45
112. Rees S, Inder T. Fetal and neonatal origins of altered brain development. Early Hum Dev. 2005 ; 81 (9). 753-61
113. Reiner O, Carrozzo R, Shen Y, Wehnert M, Faustinella F, Dobyns WB. Isolation of a Miller-Dieker lissencephaly gene containing G protein beta-subunit-like repeats. Nature. 1993 ; 364 (6439). 717-21
114. Rice DS, Curran T. Role of the reelin signaling pathway in central nervous system development. Annu Rev Neurosci. 2001 ; 24: 1005-39
115. Rio C, Rieff HI, Qi P, Khurana TS, Corfas G. Neuregulin and erbB receptors play a critical role in neuronal migration. Neuron. 1997 ; 19 (1). 39-50
116. Sawamura N, Ando T, Maruyama Y, Fujimuro M, Mochizuki H, Honjo K. Nuclear DISC1 regulates CRE-mediated gene transcription and sleep homeostasis in the fruit fly. Mol Psychiatry. 2008 ; 13 (12). 1138-48
117. Schmid RS, McGrath B, Berechid BE, Boyles B, Marchionni M, Sestan N. Neuregulin 1-erbB2 signaling is required for the establishment of radial glia and their transformation into astrocytes in cerebral cortex. Proc Natl Acad Sci U S A. 2003 ; 100 (7). 4251-6
118. Schurov IL, Handford EJ, Brandon NJ, Whiting PJ. Expression of disrupted in schizophrenia 1 (DISC1) protein in the adult and developing mouse brain indicates its role in neurodevelopment. Mol Psychiatry. 2004 ; 9 (12). 1100-10
119. Sekine K, Honda T, Kawauchi T, Kubo K, Nakajima K. The outermost region of the developing cortical plate is crucial for both the switch of the radial migration mode and the Dab1-dependent "inside-out" lamination in the neocortex. J Neurosci. 2011 ; 31 (25). 9426-39
120. Sekine K, Kawauchi T, Kubo K, Honda T, Herz J, Hattori M. Reelin controls neuronal positioning by promoting cell-matrix adhesion via inside-out activation of integrin α5β1. Neuron. 2012 ; 76 (2). 353-69
121. Seshadri S, Kamiya A, Yokota Y, Prikulis I, Kano S, Hayashi-Takagi A. Disrupted-in-schizophrenia-1 expression is regulated by beta-site amyloid precursor protein cleaving enzyme-1-neuregulin cascade. Proc Natl Acad Sci U S A. 2010 ; 107 (12). 5622-7
122. Shen S, Lang B, Nakamoto C, Zhang F, Pu J, Kuan SL. Schizophrenia-related neural and behavioral phenotypes in transgenic mice expressing truncated Disc1. J Neurosci. 2008 ; 28 (43). 10893-904
123. Shinmura Y, Kosugi I, Aiba-Masago S, Baba S, Yong LR, Tsutsui Y. Disordered migration and loss of virus-infected neuronal cells in developing mouse brains infected with murine cytomegalovirus. Acta Neuropathol. 1997 ; 93 (6). 551-7
124. Shu T, Ayala R, Nguyen MD, Xie Z, Gleeson JG, Tsai LH. Ndel1 operates in a common pathway with LIS1 and cytoplasmic dynein to regulate cortical neuronal positioning. Neuron. 2004 ; 44 (2). 263-77
125. Singh KK, De Rienzo G, Drane L, Mao Y, Flood Z, Madison J. Common DISC1 polymorphisms disrupt Wnt/GSK3beta signaling and brain development. Neuron. 2011 ; 72 (4). 545-58
126. Sprooten E, Sussmann JE, Moorhead TW, Whalley HC, Ffrench-Constant C, Blumberg HP. Association of white matter integrity with genetic variation in an exonic DISC1 SNP. Mol Psychiatry. 2011 ; 16 685 (7). 688-9
127. Stefansson H, Sigurdsson E, Steinthorsdottir V, Bjornsdottir S, Sigmundsson T, Ghosh S. Neuregulin 1 and susceptibility to schizophrenia. Am J Hum Genet. 2002 ; 71 (4). 877-92
128. Stolp H, Neuhaus A, Sundramoorthi R, Molnar Z. The long and the short of it: Gene and environment interactions during early cortical development and consequences for long-term neurological disease. Front Psychiatry. 2012 ; 3: 50
129. Szeszko PR, Hodgkinson CA, Robinson DG, Derosse P, Bilder RM, Lencz T. DISC1 is associated with prefrontal cortical gray matter and positive symptoms in schizophrenia. Biol Psychol. 2008 ; 79 (1). 103-10
130. Tabata H, Kanatani S, Nakajima K. Differences of migratory behavior between direct progeny of apical progenitors and basal progenitors in the developing cerebral cortex. Cereb Cortex. 2009 ; 19 (9). 2092-105
131. Tabata H, Nakajima K. Multipolar migration: the third mode of radial neuronal migration in the developing cerebral cortex. J Neurosci. 2003 ; 23 (31). 9996-10001
132. Takahashi T, Suzuki M, Tsunoda M, Maeno N, Kawasaki Y, Zhou SY. The Disrupted-in-Schizophrenia-1 Ser704Cys polymorphism and brain morphology in schizophrenia. Psychiatry Res. 2009 ; 172 (2). 128-35
133. Tamamaki N, Fujimori KE, Takauji R. Origin and route of tangentially migrating neurons in the developing neocortical intermediate zone. J Neurosci. 1997 ; 17 (21). 8313-23
134. Taniguchi Y, Young-Pearse T, Sawa A, Kamiya A. In utero electroporation as a tool for genetic manipulation in vivo to study psychiatric disorders: from genes to circuits and behaviors. Neuroscientist. 2012 ; 18 (2). 169-79
135. Taya S, Shinoda T, Tsuboi D, Asaki J, Nagai K, Hikita T. DISC1 regulates the transport of the NUDEL/LIS1/14-3-3epsilon complex through kinesin-1. J Neurosci. 2007 ; 27 (1). 15-26
136. Thomson PA, Macintyre DJ, Hamilton G, Dominiczak A, Smith BH, Morris A. Association of DISC1 variants with age of onset in a population-based sample of recurrent major depression. Mol Psychiatry. Epub ahead of print. 2012 ;:
137. Thornton GK, Woods CG. Primary microcephaly: do all roads lead to Rome?. Trends Genet. 2009 ; 25 (11). 501-10
138. Tsai JW, Bremner KH, Vallee RB. Dual subcellular roles for LIS1 and dynein in radial neuronal migration in live brain tissue. Nat Neurosci. 2007 ; 10 (8). 970-9
139. Tsai LH, Gleeson JG. Nucleokinesis in neuronal migration. Neuron. 2005 ; 46 (3). 383-8
140. Tsutsui Y, Kosugi I, Kawasaki H, Arai Y, Han GP, Li L. Roles of neural stem progenitor cells in cytomegalovirus infection of the brain in mouse models. Pathol Int. 2008 ; 58 (5). 257-67
141. Vallee RB, Seale GE, Tsai JW. Emerging roles for myosin II and cytoplasmic dynein in migrating neurons and growth cones. Trends Cell Biol. 2009 ; 19 (7). 347-55
142. Walsh T, McClellan JM, McCarthy SE, Addington AM, Pierce SB, Cooper GM. Rare structural variants disrupt multiple genes in neurodevelopmental pathways in schizophrenia. Science. 2008 ; 320 (5875). 539-43
143. Whalley HC, Sussmann JE, Johnstone M, Romaniuk L, Redpath H, Chakirova G. Effects of a mis-sense DISC1 variant on brain activation in two cohorts at high risk of bipolar disorder or schizophrenia. Am J Med Genet B Neuropsychiatr Genet. 2012 ; 159B (3). 343-53
144. Wonders CP, Anderson SA. The origin and specification of cortical interneurons. Nat Rev Neurosci. 2006 ; 7 (9). 687-96
145. Woodhead GJ, Mutch CA, Olson EC, Chenn A. Cell-autonomous beta-catenin signaling regulates cortical precursor proliferation. J Neurosci. 2006 ; 26 (48). 12620-30
146. Wynshaw-Boris A. Lissencephaly and LIS1: insights into the molecular mechanisms of neuronal migration and development. Clin Genet. 2007 ; 72 (4). 296-304
147. Xu Q, Cobos I, De La, Cruz E, Rubenstein JL, Anderson SA. Origins of cortical interneuron subtypes. J Neurosci. 2004 ; 24 (11). 2612-22
148. Yingling J, Youn YH, Darling D, Toyo-Oka K, Pramparo T, Hirotsune S. Neuroepithelial stem cell proliferation requires LIS1 for precise spindle orientation and symmetric division. Cell. 2008 ; 132 (3). 474-86
149. Young-Pearse TL, Suth S, Luth ES, Sawa A, Selkoe DJ. Biochemical and functional interaction of disrupted-in-schizophrenia 1 and amyloid precursor protein regulates neuronal migration during mammalian cortical development. J Neurosci. 2010 ; 30 (31). 10431-40
150. Yozu M, Tabata H, Nakajima K. The caudal migratory stream: a novel migratory stream of interneurons derived from the caudal ganglionic eminence in the developing mouse forebrain. J Neurosci. 2005 ; 25 (31). 7268-77
151. Zandi PP, Belmonte PL, Willour VL, Goes FS, Badner JA, Simpson SG. Association study of Wnt signaling pathway genes in bipolar disorder. Arch Gen Psychiatry. 2008 ; 65 (7). 785-93
152. Zechel JL, Gamboa JL, Peterson AG, Puchowicz MA, Selman WR, Lust WD. Neuronal migration is transiently delayed by prenatal exposure to intermittent hypoxia. Birth Defects Res B Dev Reprod Toxicol. 2005 ; 74 (4). 287-99
153. Zhu LL, Wu LY, Yew DT, Fan M. Effects of hypoxia on the proliferation and differentiation of NSCs. Mol Neurobiol. 2005 ; 31 (1-3). 231-42