Distinct Phenotypes of Shank2 Mouse Models Reflect Neuropsychiatric Spectrum Disorders of Human Patients With SHANK2 Variants

Amann, 2010, Mouse behavioral endophenotypes for schizophrenia, Brain Res. Bull., 83, 147, 10.1016/j.brainresbull.2010.04.008

Ammer, 2008, Cortactin branches out: roles in regulating protrusive actin dynamics, Cell Motil. Cytoskeleton, 65, 687, 10.1002/cm.20296

Angoa-Pérez, 2013, Marble burying and nestlet shredding as tests of repetitive, compulsive-like behaviors in mice, J. Vis. Exp., 82, 50978, 10.3791/50978

Baron, 2006, An architectural framework that may lie at the core of the postsynaptic density, Science, 311, 531, 10.1126/science.1118995

Ben Abdallah, 2011, The puzzle box as a simple and efficient behavioral test for exploring impairments of general cognition and executive functions in mouse models of schizophrenia, Exp. Neurol., 227, 42, 10.1016/j.expneurol.2010.09.008

Berkel, 2010, Mutations in the SHANK2 synaptic scaffolding gene in autism spectrum disorder and mental retardation, Nat. Genet., 42, 489, 10.1038/ng.589

Berkel, 2012, Inherited and de novo SHANK2 variants associated with autism spectrum disorder impair neuronal morphogenesis and physiology, Hum. Mol. Genet., 21, 344, 10.1093/hmg/ddr470

Boeckers, 2002, ProSAP/Shank proteins—a family of higher order organizing molecules of the postsynaptic density with an emerging role in human neurological disease, J. Neurochem., 81, 903, 10.1046/j.1471-4159.2002.00931.x

Boeckers, , Proline-rich synapse-associated protein-1/cortactin binding protein 1 (ProSAP1/CortBP1) is a PDZ-domain protein highly enriched in the postsynaptic density, J. Neurosci., 19, 6506, 10.1523/jneurosci.19-15-06506.1999

Boeckers, , Proline-rich synapse-associated proteins ProSAP1 and ProSAP2 interact with synaptic proteins of the SAPAP/GKAP family, Biochem. Biophys. Res. Commun., 264, 247, 10.1006/bbrc.1999.1489

Boeckers, 2005, C-terminal synaptic targeting elements for postsynaptic density proteins ProSAP1/Shank2 and ProSAP2/Shank3, J. Neurochem., 92, 519, 10.1111/j.1471-4159.2004.02910.x

Böckers, 2001, Synaptic scaffolding proteins in rat brain. Ankyrin repeats of the multidomain Shank protein family interact with the cytoskeletal protein α-fodrin, J. Biol. Chem., 276, 40104, 10.1074/jbc.m102454200

Böckers, 2004, Differential expression and dendritic transcript localization of Shank family members: identification of a dendritic targeting element in the 3′ untranslated region of Shank1 mRNA, Mol. Cell. Neurosci., 26, 182, 10.1016/j.mcn.2004.01.009

Borsini, 2002, Do animal models of anxiety predict anxiolytic-like effects of antidepressants?, Psychopharmacology, 163, 121, 10.1007/s00213-002-1155-6

Bowling, 2017, Genomic diagnosis for children with intellectual disability and/or developmental delay, Genome Med., 9, 43, 10.1186/s13073-017-0433-1

Bozdagi, 2010, Haploinsufficiency of the autism-associated Shank3 gene leads to deficits in synaptic function, social interaction and social communication, Mol. Autism, 1, 15, 10.1186/2040-2392-1-15

Braff, 1990, Sensorimotor gating and schizophrenia. Human and animal model studies, Arch. Gen. Psychiatry, 47, 181, 10.1001/archpsyc.1990.01810140081011

Broekkamp, 1986, Major tranquillizers can be distinguished from minor tranquillizers on the basis of effects on marble burying and swim-induced grooming in mice, Eur. J. Pharmacol., 126, 223, 10.1016/0014-2999(86)90051-8

Chadman, 2009, Criteria for validating mouse models of psychiatric diseases, Am. J. Med. Genet. B Neuropsychiatr. Genet., 1, 10.1002/ajmg.b.30777

Chilian, 2013, Dysfunction of SHANK2 and CHRNA7 in a patient with intellectual disability and language impairment supports genetic epistasis of the two loci, Clin. Genet., 84, 560, 10.1111/cge.12105

Cook, 2001, Anxiety-related behaviors in the elevated zero-maze are affected by genetic factors and retinal degeneration, Behav. Neurosci., 115, 468, 10.1037//0735-7044.115.2.468

Crawley, 1980, Preliminary report of a simple animal behavior model for the anxiolytic effects of benzodiazepines, Pharmacol. Biochem. Behav., 13, 167, 10.1016/0091-3057(80)90067-2

Crawley, 2007, Mouse behavioral assays relevant to the symptoms of autism, Brain Pathol., 17, 448, 10.1111/j.1750-3639.2007.00096.x

Deacon, 2012, Assessing burrowing, nest construction, and hoarding in mice, J. Vis. Exp., 59, e2607, 10.3791/2607

Deacon, 2006, Digging and marble burying in mice: simple methods for in vivo identification of biological impacts, Nat. Protoc., 1, 122, 10.1038/nprot.2006.20

de Sena Cortabitarte, 2017, Investigation of SHANK3 in schizophrenia, Am. J. Med. Genet. B Neuropsychiatr. Genet., 174, 390, 10.1002/ajmg.b.32528

Du, 1998, Identification of a novel cortactin SH3 domain-binding protein and its localization to growth cones of cultured neurons, Mol. Cell. Biol., 18, 5838, 10.1128/mcb.18.10.5838

Dunham, 1957, A note on a simple apparatus for detecting neurological deficit in rats and mice, J. Am. Pharm. Assoc. Am. Pharm. Assoc., 46, 208, 10.1002/jps.3030460322

Durand, 2007, Mutations in the gene encoding the synaptic scaffolding protein SHANK3 are associated with autism spectrum disorders, Nat. Genet., 39, 25, 10.1038/ng1933

Fridgeirsdottir, 2014, Escalated handling of young C57BL/6 mice results in altered Morris water maze performance, Ups. J. Med. Sci., 119, 1, 10.3109/03009734.2013.847511

Grabrucker, 2011, Concerted action of zinc and ProSAP/Shank in synaptogenesis and synapse maturation, EMBO J., 30, 569, 10.1038/emboj.2010.336

Gray, 2000, The Neuropsychology of Anxiety: An Enquiry into the Functions of the Septo-Hippocampal System.

Gundelfinger, 2006, A role for zinc in postsynaptic density asSAMbly and plasticity?, Trends Biochem. Sci., 31, 366, 10.1016/j.tibs.2006.05.007

Ha, 2016, Cerebellar Shank2 regulates excitatory synapse density, motor coordination and specific repetitive and anxiety-like behaviors, J. Neurosci., 36, 12129, 10.1523/jneurosci.1849-16.2016

Han, 2006, Shank2 associates with and regulates Na+/H+ exchanger 3, J. Biol. Chem., 281, 1461, 10.1074/jbc.M509786200

Handley, 1984, Effects of α-adrenoceptor agonists and antagonists in a maze-exploration model of ‘fear’-motivated behaviour, Naunyn Schmiedebergs Arch. Pharmacol., 327, 1, 10.1007/bf00504983

Hayashi, 2009, The postsynaptic density proteins Homer and Shank form a polymeric network structure, Cell, 137, 159, 10.1016/j.cell.2009.01.050

Heisler, 1998, Elevated anxiety and antidepressant-like responses in serotonin 5-HT1A receptor mutant mice, Proc. Natl. Acad. Sci. U S A, 95, 15049, 10.1073/pnas.95.25.15049

Homann, 2016, Whole-genome sequencing in multiplex families with psychoses reveals mutations in the SHANK2 and SMARCA1 genes segregating with illness, Mol. Psychiatry, 21, 1690, 10.1038/mp.2016.24

Hung, 2008, Smaller dendritic spines, weaker synaptic transmission, but enhanced spatial learning in mice lacking Shank1, J. Neurosci., 28, 1697, 10.1523/jneurosci.3032-07.2008

Immelmann, 1989, A Dictionary of Ethology.

Jacob, 2015, The organization of AMPA receptor subunits at the postsynaptic membrane, Hippocampus, 25, 798, 10.1002/hipo.22404

Jaramillo, 2017, Novel Shank3 mutant exhibits behaviors with face validity for autism and altered striatal and hippocampal function, Autism Res., 10, 42, 10.1002/aur.1664

Jaramillo, 2016, Altered striatal synaptic function and abnormal behaviour in Shank3 Exon4–9 deletion mouse model of autism, Autism Res., 9, 350, 10.1002/aur.1529

Jiang, 2013, Modeling autism by SHANK gene mutations in mice, Neuron, 78, 8, 10.1016/j.neuron.2013.03.016

Kamakura, 2016, The effects of group and single housing and automated animal monitoring on urinary corticosterone levels in male C57BL/6 mice, Physiol. Rep., 4, e12703, 10.14814/phy2.12703

Kim, 2001, Interaction of the AMPA receptor subunit GluR2/3 with PDZ domains regulates hippocampal long-term depression, Proc. Natl. Acad. Sci. U S A, 98, 11725, 10.1073/pnas.211132798

Kim, 2018, Cell-type-specific shank2 deletion in mice leads to differential synaptic and behavioral phenotypes, J. Neurosci., 38, 4076, 10.1523/jneurosci.2684-17.2018

Kolarova, 2015, Array-based DNA methylation analysis in individuals with developmental delay/intellectual disability and normal molecular karyotype, Eur. J. Med. Genet., 58, 419, 10.1016/j.ejmg.2015.05.001

Kornau, 1995, Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95, Science, 269, 1737, 10.1126/science.7569905

Kouser, 2013, Loss of predominant Shank3 isoforms results in hippocampus-dependent impairments in behavior and synaptic transmission, J. Neurosci., 33, 18448, 10.1523/jneurosci.3017-13.2013

Kudryavtseva, 2003, Use of the “partition” test in behavioral and pharmacological experiments, Neurosci. Behav. Physiol., 33, 461, 10.1023/A:1023411217051

Leblond, 2012, Genetic and functional analyses of SHANK2 mutations suggest a multiple hit model of autism spectrum disorders, PLoS Genet., 8, e1002521, 10.1371/journal.pgen.1002521

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, 2015, Shank3-mutant mice lacking exon 9 show altered excitation/inhibition balance, enhanced rearing, and spatial memory deficit, Front. Cell. Neurosci., 9, 94, 10.3389/fncel.2015.00094

Lee, 2015, Trans-synaptic zinc mobilization improves social interaction in two mouse models of autism through NMDAR activation, Nat. Commun., 6, 7168, 10.1038/ncomms8168

Lim, 1999, Characterization of the Shank family of synaptic proteins. Multiple genes, alternative splicing, and differential expression in brain and development, J. Biol. Chem., 274, 29510, 10.1074/jbc.274.41.29510

Lim, 2017, Enhancing inhibitory synaptic function reverses spatial memory deficits in Shank2 mutant mice, Neuropharmacology, 112, 104, 10.1016/j.neuropharm.2016.08.016

Lister, 1987, The use of a plus-maze to measure anxiety in the mouse, Psychopharmacology, 92, 180, 10.1007/bf00177912

Lu, 2005, PICK1 interacts with ABP/GRIP to regulate AMPA receptor trafficking, Neuron, 47, 407, 10.1016/j.neuron.2005.07.006

Luong, 2011, Assessment of motor balance and coordination in mice using the balance beam, J. Vis. Exp., 49, 2376, 10.3791/2376

Manzerra, 2001, Zinc induces a Src family kinase-mediated up-regulation of NMDA receptor activity and excitotoxicity, Proc. Natl. Acad. Sci. U S A, 98, 11055, 10.1073/pnas.191353598

Maren, 2001, Neurobiology of Pavlovian fear conditioning, Annu. Rev. Neurosci., 24, 897, 10.1146/annurev.neuro.24.1.897

Mei, 2016, Adult restoration of Shank3 expression rescues selective autistic-like phenotypes, Nature, 530, 481, 10.1038/nature16971

Monteiro, 2017, SHANK proteins: roles at the synapse and in autism spectrum disorder, Nat. Rev. Neurosci., 18, 147, 10.1038/nrn.2016.183

Moy, 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, 10.1111/j.1601-1848.2004.00076.x

Naisbitt, 1999, Shank, a novel family of postsynaptic density proteins that binds to the NMDA receptor/PSD-95/GKAP complex and cortactin, Neuron, 23, 569, 10.1016/s0896-6273(00)80809-0

Naisbitt, 1997, Characterization of guanylate kinase-associated protein, a postsynaptic density protein at excitatory synapses that interacts directly with postsynaptic density-95/synapse-associated protein 90, J. Neurosci., 17, 5687, 10.1523/JNEUROSCI.17-15-05687.1997

Neves, 2008, Synaptic plasticity, memory and the hippocampus: a neural network approach to causality, Nat. Rev. Neurosci., 9, 65, 10.1038/nrn2303

Papp, 1991, An animal model of anhedonia: attenuation of sucrose consumption and place preference conditioning by chronic unpredictable mild stress, Psychopharmacology, 104, 255, 10.1007/bf02244188

Pappas, 2017, Deficiency of Shank2 causes mania-like behavior that responds to mood stabilizers, JCI Insight, 2, e92052, 10.1172/jci.insight.92052

Peca, 2011, Shank3 mutant mice display autistic-like behaviours and striatal dysfunction, Nature, 472, 437, 10.1038/nature09965

Pellow, 1985, Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat, J. Neurosci. Methods, 14, 149, 10.1016/0165-0270(85)90031-7

Peter, 2016, Dysfunctional cerebellar Purkinje cells contribute to autism-like behaviour in Shank2-deficient mice, Nat. Commun., 7, 12627, 10.1038/ncomms12627

Peykov, 2015, Identification and functional characterization of rare SHANK2 variants in schizophrenia, Mol. Psychiatry, 20, 1489, 10.1038/mp.2014.172

Pinto, 2010, Functional impact of global rare copy number variation in autism spectrum disorders, Nature, 466, 368, 10.1038/nature09146

Porsolt, 1977, Behavioral despair in mice: a primary screening test for antidepressants, Arch. Int. Pharmacodyn. Ther., 229, 327

Prasad, 2012, A discovery resource of rare copy number variations in individuals with autism spectrum disorder, G3, 2, 1665, 10.1534/g3.112.004689

Rauch, 2012, Range of genetic mutations associated with severe non-syndromic sporadic intellectual disability: an exome sequencing study, Lancet, 380, 1674, 10.1016/S0140-6736(12)61480-9

Sala, 2001, Regulation of dendritic spine morphology and synaptic function by Shank and Homer, Neuron, 31, 115, 10.1016/s0896-6273(01)00339-7

Sala, 2015, Shank synaptic scaffold proteins: keys to understanding the pathogenesis of autism and other synaptic disorders, J. Neurochem., 135, 849, 10.1111/jnc.13232

Schellinck, 2010, Chapter 7—how many ways can mouse behavioral experiments go wrong? Confounding variables in mouse models of neurodegenerative diseases and how to control them, Advances in the Study of Behavior, 255

Schluth-Bolard, 2013, Breakpoint mapping by next generation sequencing reveals causative gene disruption in patients carrying apparently balanced chromosome rearrangements with intellectual deficiency and/or congenital malformations, J. Med. Genet., 50, 144, 10.1136/jmedgenet-2012-101351

Schmeisser, 2012, Autistic-like behaviours and hyperactivity in mice lacking ProSAP1/Shank2, Nature, 486, 256, 10.1038/nature11015

Schmeisser, 2016, Chapter 10—SHANK mutations in intellectual disability and autism spectrum disorder, Neuronal and Synaptic Dysfunction in Autism Spectrum Disorder and Intellectual Disability, 151, 10.1016/B978-0-12-800109-7.00010-8

Sheng, 2011, The postsynaptic organization of synapses, Cold Spring Harb. Perspect. Biol., 3, a005678, 10.1101/cshperspect.a005678

Shepherd, 1994, Behavioural and pharmacological characterisation of the elevated “zero-maze” as an animal model of anxiety, Psychopharmacology, 116, 56, 10.1007/bf02244871

Shi, 2017, Shank proteins differentially regulate synaptic transmission, eNeuro, 4, ENEURO.0163-15.2017, 10.1523/ENEURO.0163-15.2017

Silverman, 2010, Behavioural phenotyping assays for mouse models of autism, Nat. Rev. Neurosci., 11, 490, 10.1038/nrn2851

Speed, 2015, Autism-associated insertion mutation (InsG) of Shank3 exon 21 causes impaired synaptic transmission and behavioral deficits, J. Neurosci., 35, 9648, 10.1523/JNEUROSCI.3125-14.2015

Steru, 1985, The tail suspension test: a new method for screening antidepressants in mice, Psychopharmacology, 85, 367, 10.1007/bf00428203

Swerdlow, 1994, Assessing the validity of an animal model of deficient sensorimotor gating in schizophrenic patients, Arch. Gen. Psychiatry, 51, 139, 10.1001/archpsyc.1994.03950020063007

Thomas, 2009, Marble burying reflects a repetitive and perseverative behavior more than novelty-induced anxiety, Psychopharmacology, 204, 361, 10.1007/s00213-009-1466-y

Tordjman, 2007, Animal models relevant to schizophrenia and autism: validity and limitations, Behav. Genet., 37, 61, 10.1007/s10519-006-9120-5

Tu, 1999, Coupling of mGluR/Homer and PSD-95 complexes by the Shank family of postsynaptic density proteins, Neuron, 23, 583, 10.1016/s0896-6273(00)80810-7

Tye, 2013, Dopamine neurons modulate neural encoding and expression of depression-related behaviour, Nature, 493, 537, 10.1038/nature11740

Uemura, 2004, Direct interaction of GluRdelta2 with Shank scaffold proteins in cerebellar Purkinje cells, Mol. Cell. Neurosci., 26, 330, 10.1016/j.mcn.2004.02.007

Van Der Giessen, 2008, Role of olivary electrical coupling in cerebellar motor learning, Neuron, 58, 599, 10.1016/j.neuron.2008.03.016

Vandeputte, 2010, Automated quantitative gait analysis in animal models of movement disorders, BMC Neurosci., 11, 92, 10.1186/1471-2202-11-92

Verpelli, 2012, Scaffold proteins at the postsynaptic density, Adv. Exp. Med. Biol., 970, 29, 10.1007/978-3-7091-0932-8_2

Wang, 2016, Altered mGluR5-Homer scaffolds and corticostriatal connectivity in a Shank3 complete knockout model of autism, Nat. Commun., 7, 11459, 10.1038/ncomms11459

Wang, 2011, Synaptic dysfunction and abnormal behaviors in mice lacking major isoforms of Shank3, Hum. Mol. Genet., 20, 3093, 10.1093/hmg/ddr212

Wang, 2015, Genome-wide differential expression of synaptic long noncoding RNAs in autism spectrum disorder, Transl. Psychiatry, 5, e660, 10.1038/tp.2015.144

Wesson, 2008, Sniffing behavior of mice during performance in odor-guided tasks, Chem. Senses, 33, 581, 10.1093/chemse/bjn029

Wischmeijer, 2011, Olfactory receptor-related duplicons mediate a microdeletion at 11q13.2q13.4 associated with a syndromic phenotype, Mol. Syndromol., 1, 176, 10.1159/000322054

Won, 2012, Autistic-like social behaviour in Shank2-mutant mice improved by restoring NMDA receptor function, Nature, 486, 261, 10.1038/nature11208

Wrenn, 2004, Social transmission of food preference in mice, Curr. Protoc. Neurosci., 8, 8.5G, 10.1002/0471142301.ns0805gs28

Yang, 2012, Reduced excitatory neurotransmission and mild autism-relevant phenotypes in adolescent Shank3 null mutant mice, J. Neurosci., 32, 6525, 10.1523/JNEUROSCI.6107-11.2012

Yuen, 2017, Whole genome sequencing resource identifies 18 new candidate genes for autism spectrum disorder, Nat. Neurosci., 20, 602, 10.1038/nn.4524

Zhou, 2016, Mice with Shank3 mutations associated with ASD and schizophrenia display both shared and distinct defects, Neuron, 89, 147, 10.1016/j.neuron.2015.11.023