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Coexpression Networks Implicate Human Midfetal Deep Cortical Projection Neurons in the Pathogenesis of Autism
Open accessAbstract
Autism spectrum disorder (ASD) is a complex developmental syndrome of unknown etiology. Recent studies employing exome- and genome-wide sequencing have identified nine high-confidence ASD (hcASD) genes. Working from the hypothesis that ASD-associated mutations in these biologically pleiotropic genes will disrupt intersecting developmental processes to contribute to a common phenotype, we have attempted to identify time periods, brain regions, and cell types in which these genes converge. We have constructed coexpression networks based on the hcASD "seed" genes, leveraging a rich expression data set encompassing multiple human brain regions across human development and into adulthood. By assessing enrichment of an independent set of probable ASD (pASD) genes, derived from the same sequencing studies, we demonstrate a key point of convergence in midfetal layer 5/6 cortical projection neurons. This approach informs when, where, and in what cell types mutations in these specific genes may be productively studied to clarify ASD pathophysiology.
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“Prior analyses have implicated excitatory glutamatergic neurons in the cortex and medium spiny neurons in the striatum in ASD (Chang et al., 2015; Parikshak et al., 2013; Willsey et al., 2013; Xu et al., 2014).”
From Large-Scale Exome Sequencing Study Implicates Both Developmental and Functional Changes in the Neurobiology of Autism (2020) · cites this paper as Willsey et al., 2013
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
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“Thus, in keeping with prior analyses (Chang et al., 2015; Parikshak et al., 2013; Willsey et al., 2013; Xuet al., 2014), ASD genes are expressed at high levels in the human cortex and early in development.”
From Large-Scale Exome Sequencing Study Implicates Both Developmental and Functional Changes in the Neurobiology of Autism (2020) · cites this paper as Willsey et al., 2013
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Because the microarray probes for CHD8 , one of the genes with the lowest p values for ASD association (De Rubeis et al., 2014), do not perform well (Willsey et al., 2013; Cotney et al., 2015)”
From Large-Scale Exome Sequencing Study Implicates Both Developmental and Functional Changes in the Neurobiology of Autism (2020) · cites this paper as Willsey et al., 2013
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“It has been described that the PFC of individuals with ASD show structural and functional changes, specifically in the ACC, oFC and lPFC [367, 368].”
From Development of prefrontal cortex (2022) · cites this paper as [367]
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“several studies have supported a nexus in mid-fetal, glutamatergic neurons during cortical development, with modestly divergent findings regarding deep 56 versus”
From Autism spectrum disorder (2020) · cites this paper as [56]
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“We extracted the subset of the data for a spatio-temporal window that was previously implicated for ASD risk: midfetal development in the prefrontal cortex (PFC) (Willsey et al., 2013).”
From Large-Scale Exome Sequencing Study Implicates Both Developmental and Functional Changes in the Neurobiology of Autism (2020) · cites this paper as Willsey et al., 2013
The cited source says what the claim attributes to it.
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“Moreover, coexpression network analyses of ASD genes indicate that the developmental defects associated with ASD may arise during fetal stages5,6, periods that are difficult to investigate.”
From Single-cell brain organoid screening identifies developmental defects in autism (2023) · cites this paper as [5]
In the citing paper
“Recent studies integrating ASD candidate genes with spatiotemporal coexpression networks demonstrate that gene expression converge on the transcriptional regulation in pyramidal, glutamatergic cortical neurons during mid-fetal human development8, 9.”
From Altered proliferation and networks in neural cells derived from idiopathic autistic individuals (2017) · cites this paper as [9]
In the citing paper
“Some of these networks are particularly involved during pre-natal cortical development (Willsey et al., 2013) while others were associated with post-natal down-regulation of synaptic density (Tsai et al., 2013).”
From From early markers to neuro-developmental mechanisms of autism (2014) · cites this paper as Willsey et al., 2013
In the citing paper
“ASD risk variants are enriched in cortical glutamatergic neurons expressed during neurogenesis and neuronal migration during fetal cortical development in human and mouse (Parikshak et al., 2013; Willsey et al., 2013).”
From Defining the genetic, genomic, cellular, and diagnostic architectures of psychiatric disorders (2019) · cites this paper as Willsey et al., 2013
In the citing paper
“Analysis of spatiotemporal expression of genes has revealed that ASD genes as a group are preferentially expressed in late mid-fetal prefrontal cortex, with a concentration in layer 5/6 cortical projection neurons (Willsey et al., 2013).”
From Getting to the cores of autism (2019) · cites this paper as Willsey et al., 2013
In the citing paper
“Remarkably, CTX.M24 was significantly enriched for lncRNAs, genes expressed highly during fetal cortical development, and genes harbouring protein-disrupting mutations found in ASD, suggesting that lncRNAs will be important targets for investigation in ASD10,25 (FDR < 0.05, Extended Data Fig. 9a, g).”
From Genome-wide changes in lncRNA, splicing, and regional gene expression patterns in autism (2016) · cites this paper as [25]
In the citing paper
“A complementary study identified developmental co-expression networks enriched for ASD risk genes seeded around nine genes with the highest ASD association signal from whole-exome sequencing112.”
From Systems biology and gene networks in neurodevelopmental and neurodegenerative disorders (2015) · cites this paper as [112]
In the citing paper
“Importantly, both of these studies found convergence for rare de novo ASD-associated mutations during early fetal and mid-fetal development, with the greatest enrichment for risk in genes found in cortical glutamatergic neurons.”
From Systems biology and gene networks in neurodevelopmental and neurodegenerative disorders (2015) · cites this paper as [112]
In the citing paper
“They identified three spatiotemporal combinations that passed stringent correction for multiple testing: frontal cortical regions during the fetal period, and thalamic and cerebellar regions from birth to 6 years of postnatal age.”
From Systems biology and gene networks in neurodevelopmental and neurodegenerative disorders (2015) · cites this paper as [112]
In the citing paper
“This suggests involvement of autism risk factors in early development of excitatory cortical neurons, consistent with other recent studies39,40.”
From Transcriptional landscape of the prenatal human brain (2014) · cites this paper as [40]
In the citing paper
“ANK2 has been consistently associated with ASD (22,26,80) and also with cardiac arrhythmia (OMIM no.600919) (78).”
From Genetics and genomics of autism spectrum disorder: embracing complexity (2015) · cites this paper as [80]
In the citing paper
“Recent evidence11, 12, 13, 14, 15, 16, 17, 18, 19, 20 has also catalyzed the concept that genetic and non-genetic factors and their interaction, may act at very early periods of fetal brain development and potentially alter protein or gene expression regulation leading to shared pathways for complex ASD-related phenotypes.”
From Maternal immune activation dysregulation of the fetal brain transcriptome and relevance to the pathophysiology of autism spectrum disorder (2018) · cites this paper as [13]
In the citing paper
“Ank2, necessary for neuronal migration (Kordeli and Bennett, 1991; Willsey et al., 2013), exhibited decreased inclusion of a MXE in the STR of oASD mice, compared to oTD controls (Figure 3F).”
From Human Gut Microbiota from Autism Spectrum Disorder Promote Behavioral Symptoms in Mice (2019) · cites this paper as Willsey et al., 2013
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“of ASD both individually (Ben-Shalom et al., 2017; Bernier et al., 2014) and en masse (De Rubeis et al., 2014; Ruzzo et al., 2019; Sanders et al., 2015; Willsey et al., 2013).”
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Metadata
- Authors
- Willsey, A. J., Sanders, S. J., Li, M., Dong, S., Tebbenkamp, A. T., Muhle, R. A., Reilly, S. K., Lin, L., Fertuzinhos, S., Miller, J. A., Murtha, M. T., Bichsel, C., Niu, W., Cotney, J., Ercan-Sencicek, A. G., Gockley, J., Gupta, A. R., Han, W., He, X., Hoffman, E. J., Klei, L., Lei, J., Liu, W., Liu, L., Lu, C., Xu, X., Zhu, Y., Mane, S. M., Lein, E. S., Wei, L., Noonan, J. P., Roeder, K., Devlin, B., Sestan, N., & State, M. W.
- Affiliations
- University of California, San Francisco (US)
- Yale University (US)
- Peking University (CN)
- Allen Institute for Brain Science (US)
- Carnegie Mellon University (US)
- University of Pittsburgh (US)
- Corresponding author
- Devlin, Bernie
- State, Matthew W.
- ORCID
- Willsey, A. Jeremy
- Sanders, Stephan J.
- Li, Mingfeng
- Dong, Shan
- Tebbenkamp, Andrew T.
- Muhle, Rebecca A.
- Reilly, Steven K.
- Lin, Leon
- Fertuzinhos, Sofia
- Miller, Jeremy A.
- Niu, Wei
- Cotney, Justin
- Gockley, Jake
- Gupta, Abha R.
- He, Xin
- Hoffman, Ellen J.
- Klei, Lambertus
- Lei, Jing
- Liu, Wenzhong
- Liu, Li
- Lu, Cong
- Xu, Xuming
- Zhu, Ying
- Mane, Shrikant M.
- Lein, Ed S.
- Wei, Liping
- Noonan, James P.
- Roeder, Kathryn
- Devlin, Bernie
- State, Matthew W.
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2013-11
- Volume
- 155
- Issue
- 5
- Pages
- 997-1007
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC3995413
- OpenAlex
- W2009742334
- Cited by
- 934
- References
- 35
- Citations by year
- 2026: 48 · 2025: 59 · 2024: 61 · 2023: 57 · 2022: 69 · 2021: 77 · 2020: 112 · 2019: 83 · 2018: 76 · 2017: 82 · 2016: 81 · 2015: 66 · 2014: 59 · 2013: 2
- FWCI
- 37.35
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- Simons Foundation Autism Research Initiative
- Canadian Institutes of Health Research
- National Institute of Mental Health (RC2MH089956, R37MH057881, U01MH081896, R25MH077823, T32MH018268)
- National Institute of General Medical Sciences (R01GM094780)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bioinformatics and Genomic Networks
- Keywords
- autism spectrum disorder, co-expression network, ASD pathogenesis
- MeSH terms
- Animals, Brain, Child Development Disorders, Pervasive, Female, Fetus, Humans, Male, Mutation, Neurons, Prefrontal Cortex, Sequence Analysis, DNA, Genetic Predisposition to Disease, Gene Expression Profiling, Mice, Genome-Wide Association Study, Exome
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