The pattern of cortical dysfunction in a mouse model of a schizophrenia-related microdeletion

Journal of Neuroscience

Volumn 33, Issue 37, 2013, Pages 14825-14839

  Fénelon, Karine ^a   Xu, Bin ^a   Lai, Cora S ^e   Mukai, Jun ^a   Markx, Sander ^a   Stark, Kimberly L ^a   Hsu, Pei Ken ^a,b   Gan, Wen Biao ^e   Fischbach, Gerald D ^d   Macdermott, Amy B ^a   Karayiorgou, Maria ^a,c   Gogos, Joseph A ^a  

^a New York Presbyterian Morgan Stanley Children's Hospital   (United States)

^b Howard Hughes Medical Institute   (United States)

^c NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

^d FLATIRON INSTITUTE   (United States)

^e NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEURON SPECIFIC NUCLEAR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN DYSFUNCTION; BRAIN ELECTROPHYSIOLOGY; CHROMOSOME DELETION 22Q11; COGNITION; CONTROLLED STUDY; CYTOARCHITECTURE; DGCR8 GENE; EXON; FLUORESCENCE MICROSCOPY; GENE; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; LATENT INHIBITION; LONG TERM POTENTIATION; MALE; MICROARRAY ANALYSIS; MICRODELETION; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RNA SPLICING; SCHIZOPHRENIA; SYNAPTIC TRANSMISSION; WORKING MEMORY;

ANIMALS; COGNITION DISORDERS; DENDRITIC SPINES; DIGEORGE SYNDROME; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; LONG-TERM POTENTIATION; LONG-TERM SYNAPTIC DEPRESSION; MALE; MICE; MICE, INBRED C57BL; NEURONS; PHOSPHOPYRUVATE HYDRATASE; PREFRONTAL CORTEX; PROTEINS; RECOGNITION (PSYCHOLOGY); SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES;

EID: 84883736235     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1611-13.2013     Document Type: Article

References (78)

1. Arguello PA, Gogos JA (2006) Modeling madness in mice: one piece at a time. Neuron 52:179-196. CrossRef Medline
2. Arguello PA, Gogos JA (2010) Cognition in mouse models of schizophrenia susceptibility genes. Schizophr Bull 36:289-300. CrossRef Medline
3. Arguello PA, Gogos JA (2012) Genetic and cognitive windows into circuit mechanisms of psychiatric disease. Trends Neurosci 35:3-13. CrossRef Medline
4. Bannister AP (2005) Inter- and intra-laminar connections of pyramidal cells in the neocortex. Neurosci Res 53:95-103. CrossRef Medline
5. Barañano DE, Ferris CD, Snyder SH (2001) Atypical neural messengers. Trends Neurosci 24:99-106. CrossRef Medline
6. Barch DM, Ceaser A (2012) Cognition in schizophrenia: core psychological and neural mechanisms. Trends Cogn Sci 16:27-34. CrossRef Medline
7. Bassett AS, Hodgkinson K, Chow EW, Correia S, Scutt LE, Weksberg R (1998) 22q11 deletion syndrome in adults with schizophrenia. AmJ Med Genet 81:328-337. CrossRef Medline
8. Bassett AS, Chow EW, AbdelMalik P, Gheorghiu M, Husted J, Weksberg R (2003) The schizophrenia phenotype in 22q11 deletion syndrome. Am J Psychiatry 160:1580-1586. CrossRef Medline
9. Bearden CE, van Erp TG, Dutton RA, Lee AD, Simon TJ, Cannon TD, Emanuel BS, McDonald-McGinn D, Zackai EH, Thompson PM (2009) Alterations in midline cortical thickness and gyrification patterns mapped in children with 22q11.2deletions. Cereb Cortex 19:115-126. CrossRef Medline
10. Beveridge NJ, Tooney PA, Carroll AP, Gardiner E, Bowden N, Scott RJ, Tran N, Dedova I, Cairns MJ (2008) Dysregulation of miRNA 181b in the temporal cortex in schizophrenia. Hum Mol Genet 17:1156-1168. CrossRef Medline
11. Bhatt DH, Zhang S, Gan WB (2009) Dendritic spine dynamics. Annu Rev Physiol 71:261-282. CrossRef Medline
12. Chong MM, Zhang G, Cheloufi S, Neubert TA, Hannon GJ, Littman DR (2010) Canonical and alternate functions of the microRNA biogenesis machinery. Genes Dev [Erratum (2010) 24:2228] 24:1951-1960. CrossRef Medline
13. De Roo M, Klauser P, Garcia PM, Poglia L, Muller D (2008) Spine dynamics and synapse remodeling during LTP and memory processes. Prog Brain Res 169:199-207. CrossRef Medline
14. Drew LJ, Stark KL, Fénelon K, Karayiorgou M, Macdermott AB, Gogos JA (2011) Evidence for altered hippocampal function in a mouse model of the human 22q11.2 microdeletion. Mol Cell Neurosci 47:293-305. CrossRef Medline
15. Earls LR, Fricke RG, Yu J, Berry RB, Baldwin LT, Zakharenko SS (2012) Age-dependent microRNA control of synaptic plasticity in 22q11 deletion syndrome and schizophrenia. J Neurosci 32:14132-14144. CrossRef Medline
16. Emig D, Salomonis N, Baumbach J, Lengauer T, Conklin BR, Albrecht M (2010) AltAnalyze and DomainGraph: analyzing and visualizing exon expression data. Nucleic Acids Res 2010 38(Web Server issue):W755-W762. CrossRef
17. Evans SF, Irmady K, Ostrow K, Kim T, Nykjaer A, Saftig P, Blobel C, Hempstead BL (2011) Neuronal brain-derived neurotrophic factor is synthesized in excess, with levels regulated by sortilin-mediated trafficking and lysosomal degradation. J Biol Chem 286:29556-29567. CrossRef Medline
18. Fénelon K, Mukai J, Xu B, Hsu PK, Drew LJ, Karayiorgou M, Fischbach GD, Macdermott AB, Gogos JA (2011) Deficiency of Dgcr8, a gene disrupted by the 22q11.2 microdeletion, results in altered short-term plasticity in the prefrontal cortex. Proc Natl Acad Sci U S A 108:4447-4452. CrossRef Medline
19. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, Wallace M, Nerbonne JM, Lichtman JW, Sanes JR (2000) Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28:41-51. CrossRef Medline
20. Fujisawa S, Amarasingham A, Harrison MT, Buzsáki G (2008) Behaviordependent short-term assembly dynamics in the medial prefrontal cortex. Nat Neurosci 11:823-833. CrossRef Medline
21. Fuster JM (1991) The prefrontal cortex and its relation to behavior. Prog Brain Res 87:201-211. CrossRef Medline
22. Gardina PJ, Clark TA, Shimada B, Staples MK, Yang Q, Veitch J, Schweitzer A, Awad T, Sugnet C, Dee S, Davies C, Williams A, Turpaz Y (2006) Alternative splicing and differential gene expression in colon cancer detected by a whole genome exon array. BMCGenomics 27:325. CrossRef Medline
23. Gardiner E, Beveridge NJ, Wu JQ, Carr V, Scott RJ, Tooney PA, Cairns MJ (2012) Imprinted DLK1-DIO3 region of 14q32 defines a schizophreniaassociated miRNA signature in peripheral blood mononuclear cells. Mol Psychiatry 17:827-840. CrossRef Medline
24. Gemperle AY, Enz A, Pozza MF, Luthi A, Olpe HR (2003) Effects of clozapine, haloperidol and iloperidone on neurotransmission and synaptic plasticity in prefrontal cortex and their accumulation in brain tissue: an in vitro study. Neuroscience 117:681-695. CrossRef Medline
25. Gilman SR, Chang J, Xu B, Bawa TS, Gogos JA, Karayiorgou M, Vitkup D (2012) Diverse types of genetic variation converge on functional gene networks involved in schizophrenia. Nat Neurosci 15:1723-1728. CrossRef Medline
26. Goldman-Rakic PS (1995) Architecture of the prefrontal cortex and the central executive. Ann N Y Acad Sci 769:71-83. CrossRef Medline
27. Gustafsson B, Wigström H (1990) Long-term potentiation in the hippocampal CA1 region: its induction and early temporal development. Prog Brain Res 83:223-232. CrossRef Medline
28. Hanse E, Gustafsson B (1994) Onset and stabilization of NMDA receptordependent hippocampal long-term potentiation. Neurosci Res 20:15-25. CrossRef Medline
29. Hempel CM, Hartman KH, Wang XJ, Turrigiano GG, Nelson SB (2000) Multiple forms of short-term plasticity at excitatory synapses in rat medial prefrontal cortex. J Neurophysiol 83:3031-3041. Medline
30. Hirsch JC, Crepel F (1990) Use-dependent changes in synaptic efficacy in rat prefrontal neurons in vitro. J Physiol 427:31-49. Medline
31. Janas MM, Khaled M, Schubert S, Bernstein JG, Golan D, Veguilla RA, Fisher DE, Shomron N, Levy C, Novina CD (2011) Feed-forward microprocessing and splicing activities at a microRNA-containing intron. PLoS Genet 7:e1002330. CrossRef Medline
32. Joel D, Weiner I, Feldon J (1997) Electrolytic lesions of the medial prefrontal cortex in rats disrupt performance on an analog of the Wisconsin Card Sorting Test, but do not disrupt latent inhibition: implications for animal models of schizophrenia. Behav Brain Res 85:187-201. CrossRef Medline
33. Jurica MS, Licklider LJ, Gygi SR, Grigorieff N, Moore MJ (2002) Purification and characterization of native spliceosomes suitable for threedimensional structural analysis. RNA 8:426-439. CrossRef Medline
34. Karayiorgou M, Morris MA, Morrow B, Shprintzen RJ, Goldberg R, Borrow J, Gos A, Nestadt G, Wolyniec PS, Lasseter VK, Eisen H, Childs B, Kazazian HH, Kucherlapati R, Antonarakis SE, Pulver AE, Housman DE (1995) Schizophrenia susceptibility associated with interstitial deletions of chromosome 22q11. Proc Natl Acad SciU S A 92:7612-7616. CrossRef Medline
35. Karayiorgou M, Simon TJ, Gogos JA (2010) 22q11.2 microdeletions: linkingDNAstructural variation to brain dysfunction and schizophrenia. Nat Rev Neurosci 11:402-416. CrossRef Medline
36. Karayiorgou M, Flint J, Gogos JA, Malenka RC; Genetic and Neural Complexity in Psychiatry 2011 Working Group (2012) The best of times, the worst of times for psychiatric disease. Nat Neurosci 15:811-812. CrossRef Medline
37. Kasai H, Fukuda M, Watanabe S, Hayashi-Takagi A, Noguchi J (2010) Structural dynamics of dendritic spines in memory and cognition. Trends Neurosci 33:121-129. CrossRef Medline
38. Kates WR, Krauss BR, Abdulsabur N, Colgan D, Antshel KM, Higgins AM, Shprintzen RJ (2007) The neural correlates of non-spatial working memory in velocardiofacial syndrome (22q11.2deletion syndrome). Neuropsychologia 45:2863-2873. CrossRef Medline
39. Knuckles P, Vogt MA, Lugert S, Milo M, Chong MM, Hautbergue GM, Wilson SA, Littman DR, Taylor V (2012) Drosha regulates neurogenesis by controlling neurogenin 2 expression independent of microRNAs. Nat Neurosci 15:962-969. CrossRef Medline
40. Kvajo M, McKellar H, Arguello PA, Drew LJ, Moore H, MacDermott AB, Karayiorgou M, Gogos JA (2008) A mutation in mouse Disc1 that models a schizophrenia risk allele leads to specific alterations in neuronal architecture and cognition. Proc Natl Acad Sci U S A 105:7076-7081. CrossRef Medline
41. Kvajo M, McKellar H, Gogos JA (2010) Molecules, signaling, and schizophrenia. Curr Top Behav Neurosci 4:629-656. CrossRef Medline
42. Kvajo M, McKellar H, Drew LJ, Lepagnol-Bestel AM, Xiao L, Levy RJ, Blazeski R, Arguello PA, Lacefield CO, Mason CA, Simonneau M, O'Donnell JM, MacDermott AB, Karayiorgou M, Gogos JA (2011) Altered axonal targeting and short-term plasticity in the hippocampus of Disc1 mutant mice. Proc Natl Acad Sci U S A 108:E1349-E1358. CrossRef Medline
43. Lai CS, Franke TF, Gan WB (2012) Opposite effects of fear conditioning and extinction on dendritic spine remodelling. Nature 483:87-91. CrossRef Medline
44. Lai CY, Yu SL, Hsieh MH, Chen CH, Chen HY, Wen CC, Huang YH, Hsiao PC, Hsiao CK, Liu CM, Yang PC, Hwu HG, Chen WJ (2011) MicroRNA expression aberration as potential peripheral blood biomarkers for schizophrenia. PLoS One 6:e21635. CrossRef Medline
45. Lai WS, Xu B, Westphal KG, Paterlini M, Olivier B, Pavlidis P, Karayiorgou M, Gogos JA (2006) Akt1 deficiency affects neuronal morphology and predisposes to abnormalities in prefrontal cortex functioning. Proc Natl Acad Sci U S A 103:16906-16911. CrossRef Medline
46. Langfelder P, Horvath S (2007) Eigengene networks for studying the relationships between co-expression modules. BMC Syst Biol 1:54. CrossRef Medline
47. Lerner I, Bentin S, Shriki O (2012) Excessive attractor instability accounts for semantic priming in schizophrenia. PLoS One 7:e40663. CrossRef Medline
48. Litterman N, Ikeuchi Y, Gallardo G, O'Connell BC, Sowa ME, Gygi SP, Harper JW, Bonni A (2011) An OBSL1-Cul7Fbxw8 ubiquitin ligase signaling mechanism regulates Golgi morphology and dendrite patterning. PLoS Biol 9:e1001060. CrossRef Medline
49. Lockstone HE (2011) Exon array data analysis using Affymetrix power tools and R statistical software. Brief Bioinform 12:634-644. CrossRef Medline
50. Lodder-Gadaczek J, Becker I, Gieselmann V, Wang-Eckhardt L, Eckhardt M (2011) N-acetylaspartylglutamate synthetase II synthesizes N-acetylaspartylglutamylglutamate. J Biol Chem 286:16693-16706. CrossRef Medline
51. Macias S, Plass M, Stajuda A, Michlewski G, Eyras E, Cáceres JF (2012) DGCR8 HITS-CLIP reveals novel functions for the Microprocessor. Nat Struct Mol Biol 19:760-766. CrossRef Medline
52. Miller BH, Zeier Z, Xi L, Lanz TA, Deng S, Strathmann J, Willoughby D, Kenny PJ, Elsworth JD, Lawrence MS, Roth RH, Edbauer D, Kleiman RJ, Wahlestedt C (2012) MicroRNA-132 dysregulation in schizophrenia has implications for both neurodevelopment and adult brain function. Proc Natl Acad Sci U S A 109:3125-3130. CrossRef Medline
53. Miller EK, Erickson CA, Desimone R (1996) Neural mechanisms of visual working memory in prefrontal cortex of the macaque. J Neurosci 16: 5154-5167. Medline
54. Morciano M, Beckhaus T, Karas M, Zimmermann H, Volknandt W (2009) The proteome of the presynaptic active zone: from docked synaptic vesicles to adhesion molecules and maxi-channels. J Neurochem 108:662-675. CrossRef Medline
55. Moreau MP, Bruse SE, David-Rus R, Buyske S, Brzustowicz LM (2011) Altered microRNA expression profiles in postmortem brain samples from individuals with schizophrenia and bipolar disorder. Biol Psychiatry 69: 188-193. CrossRef Medline
56. Mukai J, Dhilla A, Drew LJ, Stark KL, Cao L, MacDermott AB, Karayiorgou M, Gogos JA (2008) Palmitoylation-dependent neurodevelopmental deficits in a mouse model of 22q11 microdeletion. Nat Neurosci 11:1302-1310. CrossRef Medline
57. Pan F, Gan WB (2008) Two-photon imaging of dendritic spine development in the mouse cortex. Dev Neurobiol 68:771-778. CrossRef Medline
58. Perkins DO, Jeffries CD, Jarskog LF, Thomson JM, Woods K, Newman MA, Parker JS, Jin J, Hammond SM (2007) microRNA expression in the prefrontal cortex of individuals with schizophrenia and schizoaffective disorder. Genome Biol 8:R27. CrossRef Medline
59. Rodriguez-Murillo L, Gogos JA, Karayiorgou M (2012) The genetic architecture of schizophrenia: new mutations and emerging paradigms. Annu Rev Med 63:63-80. CrossRef Medline
60. Rosso SB, Sussman D, Wynshaw-Boris A, Salinas PC (2005) Wnt signaling through Dishevelled, Rac and JNK regulates dendritic development. Nat Neurosci 8:34-42. CrossRef Medline
61. Schor IE, Llères D, Risso GJ, Pawellek A, Ule J, Lamond AI, Kornblihtt AR (2012) Perturbation of chromatin structure globally affects localization and recruitment of splicing factors. PLoS One 7:e48084. CrossRef Medline
62. Schulz PE, Fitzgibbons JC (1997) Differing mechanisms of expression for short- and long-term potentiation. J Neurophysiol 78:321-334. Medline
63. Shuvaev AN, Horiuchi H, Seki T, Goenawan H, Irie T, Iizuka A, Sakai N, Hirai H (2011) Mutant PKCγ in spinocerebellar ataxia type 14 disrupts synapse elimination and long-term depression in Purkinje cells in vivo. J Neurosci 31:14324-14334. CrossRef Medline
64. Sigurdsson T, Stark KL, Karayiorgou M, Gogos JA, Gordon JA (2010) Impaired hippocampal-prefrontal synchrony in a genetic mouse model of schizophrenia. Nature 464:763-767. CrossRef Medline
65. Stark KL, Xu B, Bagchi A, Lai WS, Liu H, Hsu R, Wan X, Pavlidis P, Mills AA, Karayiorgou M, Gogos JA (2008) Altered brain microRNA biogenesis contributes to phenotypic deficits in a 22q11-deletion mouse model. Nat Genet 40:751-760. CrossRef Medline
66. Szentágothai J (1978) The Ferrier Lecture, 1977. The neuron network of the cerebral cortex: a functional interpretation. Proc R Soc Lond B Biol Sci 201:219-248. CrossRef Medline
67. Volianskis A, Jensen MS (2003) Transient and sustained types of long-term potentiation in the CA1 area of the rat hippocampus. J Physiol 550:459-492. CrossRef Medline
68. Wearne SL, Rodriguez A, Ehlenberger DB, Rocher AB, Henderson SC, Hof PR (2005) New techniques for imaging, digitization and analysis of three-dimensional neural morphology on multiple scales. Neuroscience 136:661-680. CrossRef Medline
69. Xu B, Roos JL, Levy S, van Rensburg EJ, Gogos JA, Karayiorgou M (2008) Strong association of de novo copy number mutations with sporadic schizophrenia. Nat Genet 40:880-885. CrossRef Medline
70. Xu B, Karayiorgou M, Gogos JA (2010) MicroRNAs in psychiatric and neurodevelopmental disorders. Brain Res 1338:78-88. CrossRef Medline
71. Xu B, Ionita-Laza I, Roos JL, Boone B, Woodrick S, Sun Y, Levy S, Gogos JA, Karayiorgou M (2012a) De novo gene mutations highlight patterns of genetic and neural complexity in schizophrenia. Nat Genet 44:1365-1369. CrossRef Medline
72. Xu B, Hsu PK, Karayiorgou M, Gogos JA (2012b) MicroRNA dysregulation in neuropsychiatric disorders and cognitive dysfunction. Neurobiol Dis 46:291-301. CrossRef Medline
73. Xu B, Hsu PK, Stark KL, Karayiorgou M, Gogos JA (2013) Derepression of a neuronal inhibitor due to miRNA dysregulation in a schizophrenia related microdeletion. Cell 152:262-275. CrossRef Medline
74. Yang G, Pan F, Gan WB (2009) Stably maintained dendritic spines are associated with lifelong memories. Nature 462:920-924. CrossRef Medline
75. Yang G, Pan F, Parkhurst CN, Grutzendler J, Gan WB (2010) Thinned-skull cranial window technique for long-term imaging of the cortex in live mice. Nat Protoc 5:201-208. CrossRef Medline
76. Yang JH, Li JH, Shao P, Zhou H, Chen YQ, Qu LH (2011) starBase: a database for exploring microRNA-mRNA interaction maps from Argonaute CLIP-Seq andDegradome-Seq data. Nucleic Acids Res 39(Database issue): D202-D209. CrossRef
77. Yee BK, Balic E, Singer P, Schwerdel C, Grampp T, Gabernet L, Knuesel I, Benke D, Feldon J, Mohler H, Boison D (2006) Disruption of a glycine transporter 1 restricted to forebrain neurons is associated with a procognitive and antipsychotic phenotypic profile. J Neurosci 26:3169-3181. CrossRef Medline
78. Zhang B, Horvath S (2005) A general framework for weighted gene coexpression network analysis. Stat Appl Genet Mol Biol 4:Article 17. CrossRef Medline