Germline Chd8 haploinsufficiency alters brain development in mouse

Gompers, Andrea L.; Su-Feher, Linda; Ellegood, Jacob; Copping, Nycole A.; Riyadh, M. Asrafuzzaman; Stradleigh, Tyler W.; Pride, Michael C.; Schaffler, Melanie D.; Wade, A. Ayanna; Catta-Preta, Rinaldo; Zdilar, Iva; Louis, Shreya; Kaushik, Gaurav; Mannion, Brandon J.; Plajzer-Frick, Ingrid; Afzal, Veena; Visel, Axel; Pennacchio, Len A.; Dickel, Diane E.; Lerch, Jason P.; Crawley, Jacqueline N.; Zarbalis, Konstantinos S.; Silverman, Jill L.; Nord, Alex S.

doi:10.1038/nn.4592

Title: Germline Chd8 haploinsufficiency alters brain development in mouse

Journal Article · Mon Jun 26 00:00:00 EDT 2017 · Nature Neuroscience

DOI:https://doi.org/10.1038/nn.4592· OSTI ID:1436635

Gompers, Andrea L. ^[1];

^[1]; Ellegood, Jacob ^[2]; Copping, Nycole A. ^[3]; Riyadh, M. Asrafuzzaman ^[4]; Stradleigh, Tyler W. ^[1]; Pride, Michael C. ^[3]; Schaffler, Melanie D. ^[3];

^[1];

^[1]; Zdilar, Iva ^[1];

^[1]; Kaushik, Gaurav ^[4]; Mannion, Brandon J. ^[5]; Plajzer-Frick, Ingrid ^[5]; Afzal, Veena ^[5];

^[6]; Pennacchio, Len A. ^[7]; Dickel, Diane E. ^[5]; Lerch, Jason P. ^[8] more »

Univ. of California, Davis, CA (United States). Dept. of Psychiatry and Behavioral Sciences. Dept. of Neurobiology, Physiology and Behavior
The Hospital for Sick Children, Toronto, ON (Canada). Mouse Imaging Centre
Univ. of California, Davis, CA (United States). Dept. of Psychiatry and Behavioral Sciences. MIND Inst. School of Medicine
Univ. of California, Davis, Sacramento, CA (United States). Dept. of Pathology and Laboratory Medicine. Shriners Hospitals for Children. Inst. for Pediatric Regenerative Medicine
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Functional Genomics Dept.
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Functional Genomics Dept.; USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Merced, CA (United States). School of Natural Sciences
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Functional Genomics Dept.; USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
The Hospital for Sick Children, Toronto, ON (Canada). Mouse Imaging Centre; Univ. of Toronto, ON (Canada). Dept. of Medical Biophysics

The chromatin remodeling gene CHD8 represents a central node in neurodevelopmental gene networks implicated in autism. In this paper, we examined the impact of germline heterozygous frameshift Chd8 mutation on neurodevelopment in mice. Chd8⁺/^del5 mice displayed normal social interactions with no repetitive behaviors but exhibited cognitive impairment correlated with increased regional brain volume, validating that phenotypes of Chd8⁺/^del5 mice overlap pathology reported in humans with CHD8 mutations. We applied network analysis to characterize neurodevelopmental gene expression, revealing widespread transcriptional changes in Chd8⁺/^del5 mice across pathways disrupted in neurodevelopmental disorders, including neurogenesis, synaptic processes and neuroimmune signaling. We identified a co-expression module with peak expression in early brain development featuring dysregulation of RNA processing, chromatin remodeling and cell-cycle genes enriched for promoter binding by Chd8, and we validated increased neuronal proliferation and developmental splicing perturbation in Chd8⁺/^del5 mice. Finally, this integrative analysis offers an initial picture of the consequences of Chd8 haploinsufficiency for brain development.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE; Univ. of California, Davis (United States); National Inst. of Health (NIH) (United States); National Council for Scientific and Technological Development (CNPq) (Brazil); Canadian Inst. for Health Research (CIHR)

Grant/Contract Number:: AC02-05CH11231; U54 HD079125; NIGMS R35 GM119831; T32-GM008799; T32-GM007377; R24HL123879; U01DE024427; R01HG003988; U54HG006997; UM1HL098166

OSTI ID:: 1436635

Journal Information:: Nature Neuroscience, Vol. 20, Issue 8; ISSN 1097-6256

Publisher:: Springer NatureCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 136 works

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featureCounts: An efficient general-purpose program for assigning sequence reads to genomic features Liao, Yang; Smyth, Gordon K.; Shi, Wei arXiv https://doi.org/10.48550/arxiv.1305.3347	text	January 2013
Thresholding of Statistical Maps in Functional Neuroimaging Using the False Discovery Rate Genovese, Christopher R.; Lazar, Nicole A.; Nichols, Thomas figshare https://doi.org/10.6084/m9.figshare.5572453	text	January 2017
Insights into Autism Spectrum Disorder Genomic Architecture and Biology from 71 Risk Loci State, Mw; Roeder, K.; Devlin, B. NIMH Data Archive https://doi.org/10.15154/1334312	dataset	January 2016

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Setd5 haploinsufficiency alters neuronal network connectivity and leads to autistic-like behaviors in mice Moore, Spencer M.; Seidman, Jason S.; Ellegood, Jacob Translational Psychiatry, Vol. 9, Issue 1 https://doi.org/10.1038/s41398-018-0344-y	journal	January 2019
Sexually dimorphic behavior, neuronal activity, and gene expression in Chd8-mutant mice Jung, Hwajin; Park, Haram; Choi, Yeonsoo Nature Neuroscience, Vol. 21, Issue 9 https://doi.org/10.1038/s41593-018-0208-z	journal	August 2018
Sex bias in autism: new insights from Chd8 mutant mice? Andreae, Laura C.; Basson, M. Albert Nature Neuroscience, Vol. 21, Issue 9 https://doi.org/10.1038/s41593-018-0217-y	journal	August 2018
A perturbed gene network containing PI3K–AKT, RAS–ERK and WNT–β-catenin pathways in leukocytes is linked to ASD genetics and symptom severity Gazestani, Vahid H.; Pramparo, Tiziano; Nalabolu, Srinivasa Nature Neuroscience, Vol. 22, Issue 10 https://doi.org/10.1038/s41593-019-0489-x	journal	September 2019
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The clinical presentation caused by truncating CHD8 variants Douzgou, Sofia; Liang, Hui Wen; Metcalfe, Kay Clinical Genetics, Vol. 96, Issue 1 https://doi.org/10.1111/cge.13554	journal	April 2019
Epigenetic cues modulating the generation of cell‐type diversity in the cerebral cortex Amberg, Nicole; Laukoter, Susanne; Hippenmeyer, Simon Journal of Neurochemistry, Vol. 149, Issue 1 https://doi.org/10.1111/jnc.14601	journal	November 2018
Autism-linked CHD gene expression patterns during development predict multi-organ disease phenotypes Kasah, Sahrunizam; Oddy, Christopher; Basson, M. Albert Journal of Anatomy, Vol. 233, Issue 6 https://doi.org/10.1111/joa.12889	journal	October 2018
Autism-associated CHD8 deficiency impairs axon development and migration of cortical neurons Xu, Qiong; Liu, Yuan-yuan; Wang, Xiaoming Molecular Autism, Vol. 9, Issue 1 https://doi.org/10.1186/s13229-018-0244-2	journal	December 2018
Arid1b Haploinsufficiency Causes Abnormal Brain Gene Expression and Autism-Related Behaviors in Mice Shibutani, Mihiro; Horii, Takuro; Shoji, Hirotaka International Journal of Molecular Sciences, Vol. 18, Issue 9 https://doi.org/10.3390/ijms18091872	journal	August 2017
Developmental social communication deficits in the Shank3 rat model of phelan-mcdermid syndrome and autism spectrum disorder: Social communication in the Shank3 rat Berg, Elizabeth L.; Copping, Nycole A.; Rivera, Josef K. Autism Research, Vol. 11, Issue 4 https://doi.org/10.1002/aur.1925	journal	January 2018
Molecular causes of sex‐specific deficits in rodent models of neurodevelopmental disorders Mossa, Adele; Manzini, M. Chiara Journal of Neuroscience Research, Vol. 99, Issue 1 https://doi.org/10.1002/jnr.24577	journal	December 2019
The ASD Living Biology: from cell proliferation to clinical phenotype Courchesne, Eric; Pramparo, Tiziano; Gazestani, Vahid H. Molecular Psychiatry, Vol. 24, Issue 1 https://doi.org/10.1038/s41380-018-0056-y	journal	June 2018
Pten haploinsufficiency disrupts scaling across brain areas during development in mice Clipperton-Allen, Amy E.; Cohen, Ori S.; Aceti, Massimiliano Translational Psychiatry, Vol. 9, Issue 1 https://doi.org/10.1038/s41398-019-0656-6	journal	December 2019
Molecular dissection of CHARGE syndrome highlights the vulnerability of neural crest cells to problems with alternative splicing and other transcription-related processes Bérubé-Simard, Félix-Antoine; Pilon, Nicolas Transcription, Vol. 10, Issue 1 https://doi.org/10.1080/21541264.2018.1521213	journal	September 2018
Neuronal overexpression of Ube3a isoform 2 causes behavioral impairments and neuroanatomical pathology relevant to 15q11.2-q13.3 duplication syndrome Copping, Nycole A.; Christian, Sarah G. B.; Ritter, Dylan J. Human Molecular Genetics, Vol. 26, Issue 20 https://doi.org/10.1093/hmg/ddx289	journal	July 2017
Observational fear behavior in rodents as a model for empathy Kim, Arie; Keum, Sehoon; Shin, Hee-Sup Genes, Brain and Behavior, Vol. 18, Issue 1 https://doi.org/10.1111/gbb.12521	journal	October 2018
Genetic mutations in Ca ²⁺ signaling alter dendrite morphology and social approach in juvenile mice Keil, Kimberly P.; Sethi, Sunjay; Wilson, Machelle D. Genes, Brain and Behavior, Vol. 18, Issue 1 https://doi.org/10.1111/gbb.12526	journal	November 2018
Volumes of brain structures in captive wild-type and laboratory rats: 7T magnetic resonance in vivo automatic atlas-based study Welniak–Kaminska, Marlena; Fiedorowicz, Michal; Orzel, Jaroslaw PLOS ONE, Vol. 14, Issue 4 https://doi.org/10.1371/journal.pone.0215348	journal	April 2019
Pleiotropic Meta-Analysis of Cognition, Education, and Schizophrenia Differentiates Roles of Early Neurodevelopmental and Adult Synaptic Pathways Lam, Max; Hill, W. David; Trampush, Joey W. The American Journal of Human Genetics, Vol. 105, Issue 2 https://doi.org/10.1016/j.ajhg.2019.06.012	journal	August 2019
The potential association of psychoactive pharmaceuticals in the environment with human neurological disorders Kaushik, Gaurav; Thomas, Michael A. Sustainable Chemistry and Pharmacy, Vol. 13 https://doi.org/10.1016/j.scp.2019.100148	journal	September 2019
Translational outcomes in a full gene deletion of ubiquitin protein ligase E3A rat model of Angelman syndrome Berg, E. L.; Pride, M. C.; Petkova, S. P. Translational Psychiatry, Vol. 10, Issue 1 https://doi.org/10.1038/s41398-020-0720-2	journal	January 2020
Pathogenic POGZ mutation causes impaired cortical development and reversible autism-like phenotypes Matsumura, Kensuke; Seiriki, Kaoru; Okada, Shota Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-14697-z	journal	February 2020
The CHD Protein, Kismet, is Important for the Recycling of Synaptic Vesicles during Endocytosis Latcheva, Nina K.; Delaney, Taylor L.; Viveiros, Jennifer M. Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-55900-6	journal	December 2019

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