Altered Cortical Dynamics and Cognitive Function upon Haploinsufficiency of the Autism-Linked Excitatory Synaptic Suppressor MDGA2

Neuron - Tập 91 - Trang 1052-1068 - 2016
Steven A. Connor1,2, Ina Ammendrup-Johnsen1, Allen W. Chan1,2, Yasushi Kishimoto3, Chiaki Murayama4,5, Naokazu Kurihara3, Atsushi Tada3, Yuan Ge1, Hong Lu1, Ryan Yan1, Jeffrey M. LeDue1, Hirotaka Matsumoto5, Hiroshi Kiyonari6,7, Yutaka Kirino3, Fumio Matsuzaki8, Toshiharu Suzuki5, Timothy H. Murphy1, Yu Tian Wang2, Tohru Yamamoto4, Ann Marie Craig1
1Brain Research Centre and Department of Psychiatry, University of British Columbia, Vancouver, BC V6T 2B5, Canada
2Brain Research Centre and Department of Medicine, University of British Columbia, Vancouver, BC V6T 2B5, Canada
3Department of Neurobiophysics, Kagawa School of Pharmaceutical Sciences, Tokushima Bunri University, Sanuki, Kagawa 769-2101, Japan
4Department of Molecular Neurobiology, Faculty of Medicine, Kagawa University, Miki-cho, Kagawa 761-0793, Japan
5Laboratory of Neuroscience, Faculty of Pharmaceutical Sciences, Hokkaido University, Sapporo, Hokkaido 060-0812, Japan
6Animal Resource Development Unit, RIKEN Center for Developmental Biology, Kobe, Hyogo 650-0047, Japan
7Genetic Engineering Team, RIKEN Center for Developmental Biology, Kobe, Hyogo 650-0047, Japan
8Laboratory for Cell Asymmetry, RIKEN Center for Developmental Biology, Kobe, Hyogo 650-0047, Japan

Tài liệu tham khảo

Abel, 1997, Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory, Cell, 88, 615, 10.1016/S0092-8674(00)81904-2 2000 Amiet, 2008, Epilepsy in autism is associated with intellectual disability and gender: evidence from a meta-analysis, Biol. Psychiatry, 64, 577, 10.1016/j.biopsych.2008.04.030 Béna, 2013, Molecular and clinical characterization of 25 individuals with exonic deletions of NRXN1 and comprehensive review of the literature, Am. J. Med. Genet. B. Neuropsychiatr. Genet., 162B, 388, 10.1002/ajmg.b.32148 Blundell, 2010, Neuroligin-1 deletion results in impaired spatial memory and increased repetitive behavior, J. Neurosci., 30, 2115, 10.1523/JNEUROSCI.4517-09.2010 Bourgeron, 2015, From the genetic architecture to synaptic plasticity in autism spectrum disorder, Nat. Rev. Neurosci., 16, 551, 10.1038/nrn3992 Bucan, 2009, Genome-wide analyses of exonic copy number variants in a family-based study point to novel autism susceptibility genes, PLoS Genet., 5, e1000536, 10.1371/journal.pgen.1000536 Chamma, 2016, Mapping the dynamics and nanoscale organization of synaptic adhesion proteins using monomeric streptavidin, Nat. Commun., 7, 10773, 10.1038/ncomms10773 Chan, 2015, Mesoscale infraslow spontaneous membrane potential fluctuations recapitulate high-frequency activity cortical motifs, Nat. Commun., 6, 7738, 10.1038/ncomms8738 Chen, 2015, The emerging picture of autism spectrum disorder: genetics and pathology, Annu. Rev. Pathol., 10, 111, 10.1146/annurev-pathol-012414-040405 Cohen, 2015, Assessing rodent hippocampal involvement in the novel object recognition task. A review, Behav. Brain Res., 285, 105, 10.1016/j.bbr.2014.08.002 Costa-Mattioli, 2005, Translational control of hippocampal synaptic plasticity and memory by the eIF2alpha kinase GCN2, Nature, 436, 1166, 10.1038/nature03897 Dahlhaus, 2010, Overexpression of the cell adhesion protein neuroligin-1 induces learning deficits and impairs synaptic plasticity by altering the ratio of excitation to inhibition in the hippocampus, Hippocampus, 20, 305, 10.1002/hipo.20630 Di Martino, 2014, The autism brain imaging data exchange: towards a large-scale evaluation of the intrinsic brain architecture in autism, Mol. Psychiatry, 19, 659, 10.1038/mp.2013.78 Dodero, 2013, Neuroimaging evidence of major morpho-anatomical and functional abnormalities in the BTBR T+TF/J mouse model of autism, PLoS ONE, 8, e76655, 10.1371/journal.pone.0076655 Etherton, 2009, Mouse neurexin-1alpha deletion causes correlated electrophysiological and behavioral changes consistent with cognitive impairments, Proc. Natl. Acad. Sci. USA, 106, 17998, 10.1073/pnas.0910297106 Giannone, 2013, Neurexin-1β binding to neuroligin-1 triggers the preferential recruitment of PSD-95 versus gephyrin through tyrosine phosphorylation of neuroligin-1, Cell Rep., 3, 1996, 10.1016/j.celrep.2013.05.013 Glessner, 2009, Autism genome-wide copy number variation reveals ubiquitin and neuronal genes, Nature, 459, 569, 10.1038/nature07953 Gogolla, 2014, Sensory integration in mouse insular cortex reflects GABA circuit maturation, Neuron, 83, 894, 10.1016/j.neuron.2014.06.033 Gonçalves, 2013, Circuit level defects in the developing neocortex of fragile X mice, Nat. Neurosci., 16, 903, 10.1038/nn.3415 Hahamy, 2015, The idiosyncratic brain: distortion of spontaneous connectivity patterns in autism spectrum disorder, Nat. Neurosci., 18, 302, 10.1038/nn.3919 Hammer, 2015, Perturbed hippocampal synaptic inhibition and γ-oscillations in a neuroligin-4 knockout mouse model of autism, Cell Rep., 13, 516, 10.1016/j.celrep.2015.09.011 He, 2008, Electrophysiological correlates of the brain’s intrinsic large-scale functional architecture, Proc. Natl. Acad. Sci. USA, 105, 16039, 10.1073/pnas.0807010105 Hiltunen, 2014, Infra-slow EEG fluctuations are correlated with resting-state network dynamics in fMRI, J. Neurosci., 34, 356, 10.1523/JNEUROSCI.0276-13.2014 Huang, 1994, Recruitment of long-lasting and protein kinase A-dependent long-term potentiation in the CA1 region of hippocampus requires repeated tetanization, Learn. Mem., 1, 74, 10.1101/lm.1.1.74 Huang, 2013, mTORC2 controls actin polymerization required for consolidation of long-term memory, Nat. Neurosci., 16, 441, 10.1038/nn.3351 Irie, 1997, Binding of neuroligins to PSD-95, Science, 277, 1511, 10.1126/science.277.5331.1511 Ishikawa, 2011, IgSF molecule MDGA1 is involved in radial migration and positioning of a subset of cortical upper-layer neurons, Dev. Dyn., 240, 96, 10.1002/dvdy.22496 Jiang, 2013, Modeling autism by SHANK gene mutations in mice, Neuron, 78, 8, 10.1016/j.neuron.2013.03.016 Kane, 2012, Mice genetically depleted of brain serotonin display social impairments, communication deficits and repetitive behaviors: possible relevance to autism, PLoS ONE, 7, e48975, 10.1371/journal.pone.0048975 Keown, 2013, Local functional overconnectivity in posterior brain regions is associated with symptom severity in autism spectrum disorders, Cell Rep., 5, 567, 10.1016/j.celrep.2013.10.003 Kishimoto, 2015, Task-specific enhancement of hippocampus-dependent learning in mice deficient in monoacylglycerol lipase, the major hydrolyzing enzyme of the endocannabinoid 2-arachidonoylglycerol, Front. Behav. Neurosci., 9, 134, 10.3389/fnbeh.2015.00134 Komiyama, 2002, SynGAP regulates ERK/MAPK signaling, synaptic plasticity, and learning in the complex with postsynaptic density 95 and NMDA receptor, J. Neurosci., 22, 9721, 10.1523/JNEUROSCI.22-22-09721.2002 Krueger, 2012, The role of neurexins and neuroligins in the formation, maturation, and function of vertebrate synapses, Curr. Opin. Neurobiol., 22, 412, 10.1016/j.conb.2012.02.012 Leblond, 2014, Meta-analysis of SHANK mutations in autism spectrum disorders: a gradient of severity in cognitive impairments, PLoS Genet., 10, e1004580, 10.1371/journal.pgen.1004580 Lee, 2004, Differential contributions of dorsal hippocampal subregions to memory acquisition and retrieval in contextual fear-conditioning, Hippocampus, 14, 301, 10.1002/hipo.10177 Lee, 2013, MDGAs interact selectively with neuroligin-2 but not other neuroligins to regulate inhibitory synapse development, Proc. Natl. Acad. Sci. USA, 110, 336, 10.1073/pnas.1219987110 Lesca, 2012, Epileptic encephalopathies of the Landau-Kleffner and continuous spike and waves during slow-wave sleep types: genomic dissection makes the link with autism, Epilepsia, 53, 1526, 10.1111/j.1528-1167.2012.03559.x Lim, 2015, Network analysis of mesoscale optical recordings to assess regional, functional connectivity, Neurophotonics, 2, 041405, 10.1117/1.NPh.2.4.041405 Linhoff, 2009, An unbiased expression screen for synaptogenic proteins identifies the LRRTM protein family as synaptic organizers, Neuron, 61, 734, 10.1016/j.neuron.2009.01.017 Litwack, 2004, Identification and characterization of two novel brain-derived immunoglobulin superfamily members with a unique structural organization, Mol. Cell. Neurosci., 25, 263, 10.1016/j.mcn.2003.10.016 Logothetis, 2008, What we can do and what we cannot do with fMRI, Nature, 453, 869, 10.1038/nature06976 Lu, 2012, Rat brains also have a default mode network, Proc. Natl. Acad. Sci. USA, 109, 3979, 10.1073/pnas.1200506109 Margolis, 2010, EphB-mediated degradation of the RhoA GEF Ephexin5 relieves a developmental brake on excitatory synapse formation, Cell, 143, 442, 10.1016/j.cell.2010.09.038 Mohajerani, 2013, Spontaneous cortical activity alternates between motifs defined by regional axonal projections, Nat. Neurosci., 16, 1426, 10.1038/nn.3499 Mondin, 2011, Neurexin-neuroligin adhesions capture surface-diffusing AMPA receptors through PSD-95 scaffolds, J. Neurosci., 31, 13500, 10.1523/JNEUROSCI.6439-10.2011 Nelson, 2015, Excitatory/inhibitory balance and circuit homeostasis in autism spectrum disorders, Neuron, 87, 684, 10.1016/j.neuron.2015.07.033 Ogden, 2016, Prioritizing the development of mouse models for childhood brain disorders, Neuropharmacology, 100, 2, 10.1016/j.neuropharm.2015.07.029 Peça, 2012, Cellular and synaptic network defects in autism, Curr. Opin. Neurobiol., 22, 866, 10.1016/j.conb.2012.02.015 Perez-Garcia, 2016, Formation of the cortical subventricular zone requires MDGA1-mediated aggregation of basal progenitors, Cell Rep., 14, 560, 10.1016/j.celrep.2015.12.066 Pettem, 2013, The specific α-neurexin interactor calsyntenin-3 promotes excitatory and inhibitory synapse development, Neuron, 80, 113, 10.1016/j.neuron.2013.07.016 Pettem, 2013, Interaction between autism-linked MDGAs and neuroligins suppresses inhibitory synapse development, J. Cell Biol., 200, 321, 10.1083/jcb.201206028 Reymann, 2007, The late maintenance of hippocampal LTP: requirements, phases, ‘synaptic tagging’, ‘late-associativity’ and implications, Neuropharmacology, 52, 24, 10.1016/j.neuropharm.2006.07.026 Rubenstein, 2003, Model of autism: increased ratio of excitation/inhibition in key neural systems, Genes Brain Behav., 2, 255, 10.1034/j.1601-183X.2003.00037.x Schnell, 2012, Neuroligin-1 overexpression in newborn granule cells in vivo, PLoS ONE, 7, e48045, 10.1371/journal.pone.0048045 Shipman, 2012, A subtype-specific function for the extracellular domain of neuroligin 1 in hippocampal LTP, Neuron, 76, 309, 10.1016/j.neuron.2012.07.024 Siddiqui, 2013, An LRRTM4-HSPG complex mediates excitatory synapse development on dentate gyrus granule cells, Neuron, 79, 680, 10.1016/j.neuron.2013.06.029 Silverman, 2010, Behavioural phenotyping assays for mouse models of autism, Nat. Rev. Neurosci., 11, 490, 10.1038/nrn2851 Supekar, 2013, Brain hyperconnectivity in children with autism and its links to social deficits, Cell Rep., 5, 738, 10.1016/j.celrep.2013.10.001 Takeuchi, 2006, Radial migration of superficial layer cortical neurons controlled by novel Ig cell adhesion molecule MDGA1, J. Neurosci., 26, 4460, 10.1523/JNEUROSCI.4935-05.2006 Takeuchi, 2013, The synaptic plasticity and memory hypothesis: encoding, storage and persistence, Philos. Trans. R. Soc. Lond. B Biol. Sci., 369, 20130288, 10.1098/rstb.2013.0288 Tsien, 1996, The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory, Cell, 87, 1327, 10.1016/S0092-8674(00)81827-9 Uddin, 2013, Reconceptualizing functional brain connectivity in autism from a developmental perspective, Front. Hum. Neurosci., 7, 458, 10.3389/fnhum.2013.00458 Wilkerson, 2014, A role for dendritic mGluR5-mediated local translation of Arc/Arg3.1 in MEF2-dependent synapse elimination, Cell Rep., 7, 1589, 10.1016/j.celrep.2014.04.035 Wills, 2012, The nogo receptor family restricts synapse number in the developing hippocampus, Neuron, 73, 466, 10.1016/j.neuron.2011.11.029 Yizhar, 2011, Neocortical excitation/inhibition balance in information processing and social dysfunction, Nature, 477, 171, 10.1038/nature10360 Zhang, 2014, Dendritic channelopathies contribute to neocortical and sensory hyperexcitability in Fmr1(-/y) mice, Nat. Neurosci., 17, 1701, 10.1038/nn.3864