A human neurodevelopmental model for Williams syndrome
Open accessAbstract
Williams syndrome is a genetic neurodevelopmental disorder characterized by an uncommon hypersociability and a mosaic of retained and compromised linguistic and cognitive abilities. Nearly all clinically diagnosed individuals with Williams syndrome lack precisely the same set of genes, with breakpoints in chromosome band 7q11.23 (refs 1-5). The contribution of specific genes to the neuroanatomical and functional alterations, leading to behavioural pathologies in humans, remains largely unexplored. Here we investigate neural progenitor cells and cortical neurons derived from Williams syndrome and typically developing induced pluripotent stem cells. Neural progenitor cells in Williams syndrome have an increased doubling time and apoptosis compared with typically developing neural progenitor cells. Using an individual with atypical Williams syndrome, we narrowed this cellular phenotype to a single gene candidate, frizzled 9 (FZD9). At the neuronal stage, layer V/VI cortical neurons derived from Williams syndrome were characterized by longer total dendrites, increased numbers of spines and synapses, aberrant calcium oscillation and altered network connectivity. Morphometric alterations observed in neurons from Williams syndrome were validated after Golgi staining of post-mortem layer V/VI cortical neurons. This model of human induced pluripotent stem cells fills the current knowledge gap in the cellular biology of Williams syndrome and could lead to further insights into the molecular mechanism underlying the disorder and the human social brain.
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Williams syndrome is a rare NDD with a deletion of approximately 25 genes on chromosome 7 and characterized by an unusual sociability and cognitive deficits.
“Williams (WBS or WS) syndrome is a rare NDD with a deletion of approximately 25 genes on chromosome 7 and characterized by an unusual sociability and cognitive deficits [297].”
From Development of prefrontal cortex (2022) · cites this paper as [297]
The Abstract (page not provided) describes Williams syndrome as a genetic neurodevelopmental disorder with uncommon hypersociability and compromised cognitive abilities, and locates the typical deletion at chromosome band 7q11.23. Our copy does not establish that the syndrome is rare or that the deletion comprises approximately 25 genes. (LLM, conf=0.85)
Experimental — accuracy not yet measuredDeletion variants upstream of FZD9 had previously been associated with cell fraction changes related to Williams syndrome.
“deletion variants upstream of FZD9 had previously been associated with cell fraction changes related to Williams syndrome (40).”
From Comprehensive functional genomic resource and integrative model for the human brain (2018) · cites this paper as [40]
Increased dendrite length and synaptogenesis have been reported in neuron models of Williams syndrome and SHANK2, highlighting that different mutations of the same or different genes can have opposing effects on a cellular phenotype.
“An increase in dendrite length and synaptogenesis has also been reported in neuron models of Williams syndrome (Chailangkarn et al., 2016) and SHANK2 (Zaslavsky et al., 2019), further highlight how different mutations of the same gene or different genes can have opposing effects on a cellular phenotype”
From Getting to the cores of autism (2019) · cites this paper as Chailangkarn et al., 2016
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“Perhaps connected to this, deletion variants upstream of FZD9 had previously been associated with cell fraction changes related to Williams syndrome (40).”
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Cortical organoids model early brain development disrupted by 16p11.2 copy number variants in autism
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Self-citationNeuronal network dysfunction in a model for Kleefstra syndrome mediated by enhanced NMDAR signaling
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The role of TGF-β superfamily signaling in neurological disorders
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“Post-mortem layer V/VI cortical neurons in WS patients’ brain and iPSC-derived neurons show longer dendrites and an increased number of spines and synapses [115].”
BackgroundD’Souza, D., D’Souza, H., & Karmiloff‐Smith, A. (2017) · Journal of Child Language · doi:10.1017/s030500091700006x · Cited by 113 · see citing works
OTUD7A Regulates Neurodevelopmental Phenotypes in the 15q13.3 Microdeletion Syndrome
Uddin, M. J., Unda, B. K., Kwan, V., Holzapfel, N. T., White, S. H., Chalil, L., Woodbury‐Smith, M., Ho, K. S., Harward, E., Murtaza, N., et al. (2018) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2018.01.006 · Cited by 104 · see citing works
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“Calcium imaging in monolayer neurons Calcium imaging was performed as described (Chailangkarn et al, 2016).”
MethodInfluentialSelf-citationPlasticity of dendritic spines: Molecular function and dysfunction in neurodevelopmental disorders
Nishiyama, J. (2019) · Psychiatry and Clinical Neurosciences · doi:10.1111/pcn.12899 · Cited by 92 · see citing works
Li, L., Chao, J., & Shi, Y. (2018) · Cell and Tissue Research · doi:10.1007/s00441-017-2713-x · Cited by 89 · see citing works
“They found a novel phenotype in patient iPSCs-derived NSCs, which exhibited LRRK2 mutation-correlated nuclear-architecture defects and increased proteosomal stress.”
InfluentialWnt signalling in the development of axon, dendrites and synapses
He, C.-W., Liao, C., & Pan, C. (2018) · Open Biology · doi:10.1098/rsob.180116 · Cited by 82 · see citing works
Blocking Zika virus vertical transmission
Mesci, P., Macia, Á., Moore, S. M., Shiryaev, S. A., Pinto, A., Huang, C., Tejwani, L., Fernandes, I. R., Suarez, N. A., Kolar, M. J., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-19526-4 · Cited by 79 · see citing works
Self-citationNegraes, P. D., Trujillo, C. A., Yu, N., Wu, W., Yao, H., Liang, N., Lautz, J. D., Kwok, E., McClatchy, D. B., Diedrich, J. K., et al. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01104-2 · Cited by 77 · see citing works
“iPSCs were differentiated into NPCs as previously described [45, 46].”
Self-citationWard, J. M., Stoyas, C. A., Switonski, P. M., Ichou, F., Fan, W., Collins, B. L., Wall, C. E., Adanyeguh, I. M., Niu, C., Sopher, B. L., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.01.028 · Cited by 73 · see citing works
Self-citationThe 7q11.23 Protein DNAJC30 Interacts with ATP Synthase and Links Mitochondria to Brain Development
Tebbenkamp, A. T. N., Varela, L., Choi, J., Paredes, M. I., Giani, A. M., Song, J. E., Šestan-Peša, M., Franjic, D., Sousa, A. M. M., Liu, Z.-W., et al. (2018) · Cell · doi:10.1016/j.cell.2018.09.014 · Cited by 71 · see citing works
Multiplexed, image-based pooled screens in primary cells and tissues with PerturbView
Kudo, T., Meireles, A. M., Moncada, R., Chen, Y., Wu, P., Gould, J., Hu, X., Kornfeld, O., Jesudason, R., Foo, C., et al. (2025) · Nature Biotechnology · doi:10.1038/s41587-024-02391-0 · Cited by 74 · see citing works
“At day 18, cells were fixed for 30 min in 4% PFA in 1× PBS for ISS. iAstrocytes were generated from iPS cells (ALSTEM, iP11) based on a published protocol 69 .”
Branching mechanisms shaping dendrite architecture
Lanoue, V., & Cooper, H. M. (2018) · Developmental Biology · doi:10.1016/j.ydbio.2018.12.005 · Cited by 62 · see citing works
Kharbat, F. F., Alshawabkeh, A., & Woolsey, M. L. (2020) · Aslib Journal of Information Management · doi:10.1108/ajim-02-2020-0054 · Cited by 63 · see citing works
Recurrent reciprocal copy number variants: Roles and rules in neurodevelopmental disorders
Deshpande, A., & Weiss, L. A. (2018) · Developmental Neurobiology · doi:10.1002/dneu.22587 · Cited by 58 · see citing works
“23 deletion using carrier-derived iPSCs uncovered the role of frizzled9 (FZD9, a gene in the CNV) in decreasing neural progenitor viability, corroborating the reduced cortical thickness observed in carriers (Chailangkarn et al., 2016).”
BackgroundRaj, N., McEachin, Z. T., Harousseau, W., Zhou, Y., Zhang, F., Merritt-Garza, M. E., Taliaferro, J. M., Kalinowska, M., Marro, S. G., Hales, C. M., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.108991 · Cited by 54 · see citing works
“The EB-method used was similar to previously published methods, with minor modifications (Chailangkarn et al., 2016; Marchetto et al., 2010).”
Impact of alcohol exposure on neural development and network formation in human cortical organoids
Adams, J. W., Negraes, P. D., Truong, J., Tran, T. H., Szeto, R. A., Guerra, B. S., Herai, R. H., Teodorof‐Diedrich, C., Spector, S. A., Campo, M. D., et al. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01862-7 · Cited by 58 · see citing works
“Synaptic puncta quantification Pre (Vglut1+) and postsynaptic (PSD95+) puncta were quantified along MAP2+ neuronal processes, as previously described [29].”
MethodSelf-citationBodnar, B. H., Zhang, Y., Liu, J., Lin, Y., Wang, P., Wei, Z., Saribas, S., Zhu, Y., Li, F., Wang, X., et al. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.682272 · Cited by 56 · see citing works
“These applications include neurodevelopmental disorders such as autism spectrum disorders and related disorders (Mariani et al., 2015; Chailangkarn et al., 2016; Birey et al., 2017; Wang et al., 2017; Mellios et al., 2018; Gouder et al., 2019; Sun et al., 2019), neuropsychiatric disorders such as schizophrenia (Srikan…”
BackgroundMethodTwite, M. D., Stenquist, S., & Ing, R. J. (2019) · Pediatric Anesthesia · doi:10.1111/pan.13620 · Cited by 54 · see citing works
Sabitha, K. R., Shetty, A. K., & Upadhya, D. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.12.025 · Cited by 48 · see citing works
Serotonin in psychiatry: in vitro disease modeling using patient-derived neurons
Vadodaria, K. C., Stern, S., Marchetto, M. C., & Gage, F. H. (2017) · Cell and Tissue Research · doi:10.1007/s00441-017-2670-4 · Cited by 45 · see citing works
“Some of the first evidence leading to what came to be known as the Bmonoamine hypothesis of depression^ came from anecdotal evidence and from pharmacological studies that depleted or increased the concentration of brain monoamines (Charney 1998; Mosienko et al. 2015).”
BackgroundSelf-citationMoore, S. M., Seidman, J. S., Ellegood, J., Gao, R., Savchenko, A., Troutman, T. D., Abe, Y., Stender, J. D., Lee, D., Wang, S., et al. (2019) · Translational Psychiatry · doi:10.1038/s41398-018-0344-y · Cited by 45 · see citing works
Self-citationHuman Brain Organoid Models of Developmental Epilepsies
Nieto‐Estévez, V., & Hsieh, J. (2020) · Epiliepsy currents/Epilepsy currents · doi:10.1177/1535759720949254 · Cited by 44 · see citing works
Cutting‐Edge Nanomaterials for Advanced Multimodal Bioimaging Applications
Tsang, M., Wong, Y., & Hao, J. (2017) · Small Methods · doi:10.1002/smtd.201700265 · Cited by 42 · see citing works
Izsák, J., Seth, H., Andersson, M. X., Vizlin‐Hodzic, D., Theiss, S., Hanse, E., Ågren, H., Funa, K., & Illes, S. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00351 · Cited by 39 · see citing works
“Moreover, in some of the work calcium imaging was used, however, presented calcium traces clearly showed asynchronous calcium peaks and missed evidence for neuronal population wide synchronous network activity (Mertens et al., 2015; Chailangkarn et al., 2016; Monzel et al., 2017).”
BackgroundMethodInfluentialMolecular mechanisms that mediate dendrite morphogenesis
Lefebvre, J. L. (2021) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2020.12.008 · Cited by 42 · see citing works
Pavinato, L., Vedove, A. D., Carli, D., Ferrero, M., Carestiato, S., Howe, J., Agolini, E., Coviello, D. A., van de Laar, I. M. B. H., Au, P. Y. B., et al. (2022) · Brain · doi:10.1093/brain/awac278 · Cited by 41 · see citing works
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BrainPhys neuronal medium optimized for imaging and optogenetics in vitro
Zabolocki, M., McCormack, K., van den Hurk, M., Milky, B., Shoubridge, A. P., Adams, R., Tran, J., Mahadevan-Jansen, A. M., Reineck, P., Thomas, J., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-19275-x · Cited by 43 · see citing works
Self-citationWilliams Syndrome, Human Self-Domestication, and Language Evolution
Niego, A., & Benítez‐Burraco, A. (2019) · Frontiers in Psychology · doi:10.3389/fpsyg.2019.00521 · Cited by 35 · see citing works
meaRtools: An R package for the analysis of neuronal networks recorded on microelectrode arrays
Gelfman, S., Wang, Q., Lu, Y., Hall, D., Bostick, C. D., Dhindsa, R. S., Halvorsen, M., McSweeney, K. M., Cotterill, E., Edinburgh, T., et al. (2018) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1006506 · Cited by 35 · see citing works
“21 22 Introduction 23 24 The MEA platform is now increasingly being used to study the response of neuronal networks to 25 pharmacological manipulations and the spontaneous activity profiles of neural networks originating from 26 genetic mouse models and derived from human pluripotent stem cells[1-4].”
MethodHuman pluripotent stem cell (hPSC) and organoid models of autism: opportunities and limitations
Kilpatrick, S., Irwin, C. L., & Singh, K. K. (2023) · Translational Psychiatry · doi:10.1038/s41398-023-02510-6 · Cited by 34 · see citing works
Human SPG11 cerebral organoids reveal cortical neurogenesis impairment
Pérez‐Brangulí, F., Buchsbaum, I. Y., Pozner, T., Regensburger, M., Fan, W., Schray, A., Boerstler, T., Mishra, H., Gräf, D., Kohl, Z., et al. (2018) · Human Molecular Genetics · doi:10.1093/hmg/ddy397 · Cited by 32 · see citing works
“Induced pluripotent stem cell (iPSC)-derived neuronal models have been decisive for characterizing the cellular phenotypes of neurodevelopmental deficits in autism, Rett syndrome and Williams syndrome (6,22,23).”
BackgroundKnoll, A. T., Jiang, K., & Levitt, P. R. (2017) · Genes Brain & Behavior · doi:10.1111/gbb.12431 · Cited by 27 · see citing works
The Wnt receptor Ryk is a negative regulator of mammalian dendrite morphogenesis
Lanoue, V., Langford, M. B., White, A., Sempert, K., Fogg, L. G., & Cooper, H. M. (2017) · Scientific Reports · doi:10.1038/s41598-017-06140-z · Cited by 32 · see citing works
The Role of Wnt Signalling in Chronic Kidney Disease (CKD)
Malik, S. A., Modarage, K., & Goggolidou, P. (2020) · Genes · doi:10.3390/genes11050496 · Cited by 32 · see citing works
Integrative network analysis reveals biological pathways associated with Williams syndrome
Kimura, R., Swarup, V., Tomiwa, K., Gandal, M. J., Parikshak, N., Funabiki, Y., Nakata, M., Awaya, T., Kato, T., Iida, K., et al. (2018) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.12999 · Cited by 32 · see citing works
“…related to the diverse WS phenotypes using genomewide gene expression analyses, but these efforts have not yet provided conclusive results (Adamo et al., 2015; Antonell, Vilardell, & Perez Jurado, 2010; Chailangkarn et al., 2016; Henrichsen et al., 2011; Khattak et al., 2015; Lalli et al., 2016).”
BackgroundIn situ characterization of stem cells-like biomarkers in meningiomas
Alamir, H., Alomari, M., Salwati, A. A. A., Saka, M. Y., Bangash, M., Baeesa, S. S., Alghamdi, F. A., Carracedo, Á., Schulten, H.-J., Chaudhary, A., et al. (2018) · Cancer Cell International · doi:10.1186/s12935-018-0571-6 · Cited by 31 · see citing works
“Co-expression of FZD9 and Nestin has been observed in neural stem progenitor, derived from patients with Williams syndrome, a developmental disorder caused by mutations in chromosome 7 [89].”
Lewis, E. M. A., Meganathan, K., Baldridge, D., Gontarz, P. M., Zhang, B., Bonni, A., Constantino, J. N., & Kroll, K. L. (2019) · Molecular Autism · doi:10.1186/s13229-019-0306-0 · Cited by 31 · see citing works
“These findings are reminiscent of some observations made in prior work, in 520 which schizophrenia subject-derived iPSCs exhibited reduced neurosphere size (43) and 521 increased apoptosis was observed in Williams-Syndrome iPSC-derived NPCs (44).”
ResultHerai, R. H. (2019) · Gene · doi:10.1016/j.gene.2019.03.019 · Cited by 30 · see citing works
Self-citationConnacher, R., Williams, M., Prem, S., Yeung, P. L., Matteson, P. G., Mehta, M., Markov, A., Peng, C., Zhou, X., McDermott, C. R., et al. (2022) · Stem Cell Reports · doi:10.1016/j.stemcr.2022.04.019 · Cited by 29 · see citing works
Williams syndrome-specific neuroanatomical profile and its associations with behavioral features
Fan, C. C., Brown, T. T., Bartsch, H., Kuperman, J. M., Hagler, D. J., Schork, A. J., Searcy, Y. M., Bellugi, U., Halgren, E., & Dale, A. M. (2017) · NeuroImage Clinical · doi:10.1016/j.nicl.2017.05.011 · Cited by 28 · see citing works
Self-citationApplication of CRISPR/Cas9 to the study of brain development and neuropsychiatric disease
Powell, S. K., Gregory, J. K., Akbarian, S., & Brennand, K. (2017) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2017.05.007 · Cited by 28 · see citing works
“…may be overcome by studying hiPSCs only from individuals with well-defined genetic lesions and/or disease-relevant endophenotypes (e.g., Wen et al., 2014; Lee et al., 2015; Chailangkarn et al., 2016), such an approach necessarily limits the generalizability of any findings to the broader disorder.”
Quantity as a Fish Views It: Behavior and Neurobiology
Messina, A., Potrich, D., Perrino, M., Sheardown, E., Petrazzini, M. E. M., Luu, P., Nadtochiy, A., Truong, T. V., Sovrano, V. A., Fraser, S. E., et al. (2022) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2022.943504 · Cited by 28 · see citing works
van den Hurk, M., & Bardy, C. (2019) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2019.108350 · Cited by 27 · see citing works
Self-citationNutrient regulation of the islet epigenome controls adaptive insulin secretion
Wortham, M., Liu, F., Harrington, A. R., Fleischman, J. Y., Wallace, M., Mulas, F., Mallick, M., Vinckier, N. K., Cross, B. R., Chiou, J., et al. (2023) · Journal of Clinical Investigation · doi:10.1172/jci165208 · Cited by 27 · see citing works
“Fluorescence was monitored and analyzed as described (64).”
Gracia-Diaz, C., Zhou, Y., Yang, Q., Maroofian, R., Espana-Bonilla, P., Lee, C., Zhang, S., Padilla, N., Fueyo, R., Waxman, E. A., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-39645-5 · Cited by 27 · see citing works
“To test whether EZH1 LOF and GOF variants affect cortical neurogenesis, we took advantage of hPSC derived neurodevelopmental models, which provide unique and versatile resources to study mechanisms of neurodevelopmental disorders 54 – 56 .”
BackgroundModeling anorexia nervosa: transcriptional insights from human iPSC-derived neurons
Negraes, P. D., Cugola, F. R., Herai, R. H., Trujillo, C. A., Cristino, A. S., Chailangkarn, T., Muotri, A. R., & Duvvuri, V. (2017) · Translational Psychiatry · doi:10.1038/tp.2017.37 · Cited by 27 · see citing works
Self-citationPintacuda, G., Martín, J. M., & Eggan, K. C. (2021) · Molecular Autism · doi:10.1186/s13229-021-00417-x · Cited by 26 · see citing works
Cavallo, F., Troglio, F., Fagà, G., Fancelli, D., Shyti, R., Trattaro, S., Zanella, M., D’Agostino, G., Hughes, J. M., Cera, M. R., et al. (2020) · Molecular Autism · doi:10.1186/s13229-020-00387-6 · Cited by 23 · see citing works
The molecular basis of music-induced neuroplasticity in humans: A systematic review
Kunikullaya, K. U., Pranjić, P., Rigby, A. M., Pallás-Ferrer, I., Anand, H. J., Kunnavil, R., & Jaschke, A. C. (2025) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2025.106219 · Cited by 25 · see citing works
“The study by Dai et al. involved individuals with Williams Syndrome (WS) (Dai et al., 2012), a genetic neurodevelopmental disorder marked by intellectual disability (Chailangkarn et al., 2016).”
Milky, B., Zabolocki, M., Al‐Bataineh, S. A., van den Hurk, M., Greenberg, Z., Turner, L., Mazzachi, P., Williams, A., Illeperuma, I., Adams, R., et al. (2022) · Stem Cell Reports · doi:10.1016/j.stemcr.2022.01.013 · Cited by 24 · see citing works
“Applications of glass-DAP coverslips Patient-derived iPSCs are increasingly popular pre-clinical models of neurological and psychiatric disorders (Bardy et al., 2020; Chailangkarn et al., 2016; Israel et al., 2012; Mertens et al., 2016; Sarkar et al., 2018; Tran et al., 2020; van den Hurk and Bardy, 2019).”
BackgroundSelf-citationAtypical deletion of Williams–Beuren syndrome reveals the mechanism of neurodevelopmental disorders
Zhou, J., Zheng, Y., Liang, G., Qin, X., Yang, H., Chen, S., Ge, T., Huang, S., Zhang, Y., Zhou, X., et al. (2022) · BMC Medical Genomics · doi:10.1186/s12920-022-01227-7 · Cited by 23 · see citing works
“By increasing the doubling time and apoptosis of nerve cells, the deletion of the FZD9 gene can affect the development of the nervous system and cause cognitive impairment [9].”
BackgroundFink, J. J., & Levine, E. S. (2018) · Frontiers in Neurology · doi:10.3389/fneur.2018.00237 · Cited by 23 · see citing works
“Other studies have shown increases in spiking and calcium transients in Williams syndrome-derived neurons complemented by gene expression and morphological studies, and that neurons derived from Alzheimer’s patients mature into functional neurons, as measured by the presence of AP firing and synaptic activity, despite…”
BackgroundHu, C., Kanellopoulos, A. K., Richter, M., Petersen, M., Konietzny, A., Tenedini, F. M., Hoyer, N., Cheng, L., Poon, C. L. C., Harvey, K. F., et al. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.1846-19.2020 · Cited by 20 · see citing works
“Abnormal dendritic morphogenesis is thought to be a major contributing factor to the pathology of psychiatric and neurological disorders (Kulkarni and Firestein, 2012; Koleske, 2013; Chailangkarn et al., 2016).”
BackgroundSedmak, D., Hrvoj-Mihić, B., Džaja, D., Habek, N., Uylings, H. B. M., & Petanjek, Z. (2018) · Croatian Medical Journal · doi:10.3325/cmj.2018.59.189 · Cited by 22 · see citing works
Upconversion Luminescence Sandwich Assay For Detection of Influenza H7 Subtype
Tsang, M., Wong, Y., Tsoi, T., Wong, W., & Hao, J. (2019) · Advanced Healthcare Materials · doi:10.1002/adhm.201900575 · Cited by 22 · see citing works
Self-citationZhang, S., Zhang, X., Purmann, C., Ma, S., Shrestha, A., Davis, K. N., Ho, M., Huang, Y., Pattni, R., Wong, W. H., et al. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2020.06.021 · Cited by 22 · see citing works
Self-citationThe contribution of GTF2I haploinsufficiency to Williams syndrome
Chailangkarn, T., Noree, C., & Muotri, A. R. (2018) · Molecular and Cellular Probes · doi:10.1016/j.mcp.2017.12.005 · Cited by 22 · see citing works
“morphology comparable to those observed in postmortem neurons as well as increases in calcium transient frequency when compared to NPCs and neurons derived from typical developing (TD) subjects’ iPSCs, respectively [29].”
BackgroundResultSelf-citationHrvoj-Mihic, B., Hanson, K. L., Lew, C. H., Stefanacci, L., Jacobs, B., Bellugi, U., & Semendeferi, K. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00419 · Cited by 21 · see citing works
“…length of basal dendrites compared to supra-granular layers (Figures 6, 7), more complex morphology of apical and basal dendrites compared to TD in layer V/VI (Chailangkarn et al., 2016), and longer and more branched dendrites in layer V/VI ofMSV compared to layer V/VI in PFC (Figures 7A,B).”
InfluentialSelf-citationPetanjek, Z., Banovac, I., Sedmak, D., & Hladnik, A. (2023) · Advances in neurobiology · doi:10.1007/978-3-031-36159-3_4 · Cited by 23 · see citing works
Autism spectrum disorders and disease modeling using stem cells
Brito, A., Russo, F. B., Muotri, A. R., & Beltrão-Braga, P. C. B. (2017) · Cell and Tissue Research · doi:10.1007/s00441-017-2685-x · Cited by 21 · see citing works
Self-citationDruggable transcriptomic pathways revealed in Parkinson’s patient-derived midbrain neurons
van den Hurk, M., Lau, S., Marchetto, M. C., Mertens, J., Stern, S., Corti, O., Brice, A., Winner, B., Winkler, J., Gage, F. H., et al. (2022) · npj Parkinson s Disease · doi:10.1038/s41531-022-00400-0 · Cited by 21 · see citing works
Self-citationThe promise of induced pluripotent stem cells for neurodevelopmental disorders
Linda, K., Fiuza, C., & Kasri, N. N. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.11.009 · Cited by 21 · see citing works
“showed the potential of patient iPSCs as model for polygenic disorders (Chailangkarn et al., 2016).”
Guan, M., Han, X., Liao, B., Han, W., Chen, L., Zhang, B., Peng, X., Tian, Y., Xiao, G., Li, X., et al. (2025) · Advanced Science · doi:10.1002/advs.202413930 · Cited by 19 · see citing works
Comparative Analysis of Multiple Neurodegenerative Diseases Based on Advanced Epigenetic Aging Brain
Shi, F., He, Y., Chen, Y., Yin, X., Sha, X., & Wang, Y. (2021) · Frontiers in Genetics · doi:10.3389/fgene.2021.657636 · Cited by 19 · see citing works
van Rhijn, J.-R., Shi, Y., Bormann, M., Mossink, B., Frega, M., Recaioglu, H., Hakobjan, M., Gunnewiek, T. M. K., Schoenmaker, C., Palmer, E. E., et al. (2021) · Neurobiology of Disease · doi:10.1016/j.nbd.2021.105587 · Cited by 19 · see citing works
Neuron density is decreased in the prefrontal cortex in Williams syndrome
Lew, C. H., Brown, C., Bellugi, U., & Semendeferi, K. (2017) · Autism Research · doi:10.1002/aur.1677 · Cited by 18 · see citing works
Self-citationYuan, F., Li, Y., Hu, R., Gong, M., Chai, M., Ma, X., Cha, J., Guo, P., Yang, K., Li, M., et al. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-01987-3 · Cited by 18 · see citing works
“To evaluate WFS1 ’ s role in neurons and astrocytes, we differentiated WT and WFS1 − / − HuES8 into NPCs using previously reported 2D culture methods [18, 44], which could be maintained and subsequently differentiated into neurons and astrocytes separately.”
MethodMiao, N., Bian, S., Lee, T., Mubarak, T., Huang, S., Wen, Z., Hussain, G., & Sun, T. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00247 · Cited by 18 · see citing works
Izsák, J., Seth, H., Iljin, M., Theiss, S., Ågren, H., Funa, K., Aigner, L., Hanse, E., & Illes, S. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01399-3 · Cited by 18 · see citing works
Stem cell contributions to neurological disease modeling and personalized medicine
Liang, N., Trujillo, C. A., Negraes, P. D., Muotri, A. R., Lameu, C., & Ulrich, H. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.05.025 · Cited by 18 · see citing works
“After characterizing neuronal morphology, Williams syndrome (WS) iPSC-derived neurons showed increased dendritic length and arborization (Chailangkarn et al. 2016).”
Self-citationModeling Williams syndrome with induced pluripotent stem cells
Chailangkarn, T., & Muotri, A. R. (2017) · Neurogenesis · doi:10.1080/23262133.2017.1283187 · Cited by 17 · see citing works
“have demonstrated that iPSC-derived neurons with morphological changes largely comparable to the ones in the postmortem cortex, displayed differences in doubling time of NPCs and calcium transients in response to activity, both of which may underlie morphological changes observed in individual neurons.(27)”
ResultSelf-citationSerrano‐Juárez, C. A., Prieto‐Corona, B., Rodríguez-Camacho, M. A., Sandoval-Lira, L., Villalva-Sánchez, Á. F., Yáñez-Téllez, M. G., & López, M. F. R. (2022) · Neuropsychology Review · doi:10.1007/s11065-022-09571-2 · Cited by 16 · see citing works
“Chailangkarn et al. (2016) found that blocking of this gene is accompanied by apoptosis of neural progenitor cells.”
Bajikar, S. S., Sztainberg, Y., Trostle, A. J., Tirumala, H. P., Wan, Y., Harrop, C. L., Bengtsson, J. D., Carvalho, C. M. B., Pehli̇van, D., Suter, B., et al. (2024) · Human Molecular Genetics · doi:10.1093/hmg/ddae135 · Cited by 16 · see citing works
“…cell type, which allows the generation of in vitro neuronal avatars of disease to understand disease mechanism and test potential therapeutics [35, 36]. iPSCs and iPSC-derived neurons have been used to study MECP2 loss-of-function and RTT and to study MDS, though the effects of altered MeCP2…”
Altered Neocortical Dynamics in a Mouse Model of Williams–Beuren Syndrome
Dasilva, M., Navarro-Guzman, A., Ortiz‐Romero, P., Camassa, A., Muñoz, A., Campuzano, V., & Sanchez-Vives, M. V. (2019) · Molecular Neurobiology · doi:10.1007/s12035-019-01732-4 · Cited by 16 · see citing works
Modeling neurodevelopmental and psychiatric diseases with human iPSCs
Wen, Z. (2017) · Journal of Neuroscience Research · doi:10.1002/jnr.24031 · Cited by 15 · see citing works
“Furthermore, NPCs from Williams syndrome display a decreased growth rate and increased cell death, while layer V/VI cortical neurons derived from Williams syndrome showed morphological alterations, abnormal synapse formation, aberrant calcium oscillation, and altered network connectivity (Table I) (Chailangkarn et al.…”
BackgroundCardiovascular findings in Williams–Beuren Syndrome : Experience of a single center with 127 cases
Honjo, R. S., Monteleone, V. F., Aiello, V. D., Wagenführ, J., Issa, V. S., Pomerantzeff, P. M. A., Furusawa, É. A., Zanardo, É. A., Kulikowski, L. D., Bertola, D. R., et al. (2021) · American Journal of Medical Genetics Part A · doi:10.1002/ajmg.a.62542 · Cited by 15 · see citing works
“…(Merla et al., 2010; Peoples, Peres-Jurado, Wang, Kaplan, & Francke, 1996; Tomida et al., 2008)]; STX1 [impaired glucose tolerance (Lam et al., 2005; Merla et al., 2010)]; FZD9 [osteopenia and the neurodevelopmental aspects of WBS (Chailangkarn et al., 2016; Merla et al., 2010; Pober, 2010)].”
BackgroundA postmortem stereological study of the amygdala in Williams syndrome
Lew, C. H., Groeniger, K. M., Bellugi, U., Stefanacci, L., Schumann, C. M., & Semendeferi, K. (2017) · Brain Structure and Function · doi:10.1007/s00429-017-1592-y · Cited by 15 · see citing works
Self-citationDirect Generation of Human Cortical Organoids from Primary Cells
Schukking, M., Miranda, H. C., Trujillo, C. A., Negraes, P. D., & Muotri, A. R. (2018) · Stem Cells and Development · doi:10.1089/scd.2018.0112 · Cited by 14 · see citing works
Self-citation
- Authors
- Chailangkarn, T., Trujillo, C. A., Freitas, B. C., Hrvoj-Mihic, B., Herai, R. H., Yu, D. X., Brown, T. T., Marchetto, M. C., Bardy, C., McHenry, L., Stefanacci, L., Järvinen, A., Searcy, Y. M., DeWitt, M., Wong, W., Lai, P., Ard, M. C., Hanson, K. L., Romero, S., Jacobs, B., Dale, A. M., Dai, L., Korenberg, J. R., Gage, F. H., Bellugi, U., Halgren, E., Semendeferi, K., & Muotri, A. R.
- Affiliations
- University of California San Diego (US)
- Pontifícia Universidade Católica do Paraná (BR)
- Salk Institute for Biological Studies (US)
- Colorado College (US)
- University of Utah (US)
- Corresponding author
- Semendeferi, Katerina
- Muotri, Alysson R.
- ORCID
- Venue
- Nature
- Published
- 2016-08
- Volume
- 536
- Issue
- 7616
- Pages
- 338-343
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC4995142
- OpenAlex
- W2510152931
- Cited by
- 195
- References
- 60
- Citations by year
- 2026: 8 · 2025: 11 · 2024: 14 · 2023: 15 · 2022: 16 · 2021: 20 · 2020: 23 · 2019: 27 · 2018: 30 · 2017: 27 · 2016: 4
- FWCI
- 14.97
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Institutes of Health (1dp2od006495-01)
- U.S. Public Health Service (P01 NICHD033113)
- National Institute of Mental Health (T32MH020002, R01MH095741, R01MH103134, U19MH107367, U19MH106434, R01MH094753, R56MH109587, R01MH100175)
- National Institute on Deafness and Other Communication Disorders (T32DC007361)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Williams Syndrome Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Keywords
- Williams syndrome, induced pluripotent stem cells, neural progenitor cells, cortical neurons, FZD9, haploinsufficiency, apoptosis, dendritic morphology, synapses, calcium oscillations, neuronal network connectivity, social brain, neurodevelopmental disorders, 7q11.23 deletion
- MeSH terms
- Adolescent, Adult, Brain, Calcium, Cell Differentiation, Cerebral Cortex, Chromosomes, Human, Pair 7, Dendrites, Female, Humans, Male, Models, Neurological, Neurons, Phenotype, Synapses, Reproducibility of Results, Apoptosis, Williams Syndrome, Cell Shape, Frizzled Receptors, Young Adult, Induced Pluripotent Stem Cells, Haploinsufficiency, Neural Stem Cells, Cellular Reprogramming
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