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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 (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]
Experimental — accuracy not yet measuredIn the citing paper
“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]
In the citing paper
“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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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
van den Hurk, M., & Bardy, C. (2019) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2019.108350 · Cited by 28
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
“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
“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 30
Self-citationPintacuda, G., Martín, J. M., & Eggan, K. C. (2021) · Molecular Autism · doi:10.1186/s13229-021-00417-x · Cited by 26
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
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 28
“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
“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
“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 26
“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
“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
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
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 25
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
“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
“…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 34
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 24
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
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 22
“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
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 15
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 21
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
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 20
“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 19
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
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
“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 18
“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
“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., Pehlivan, D., Suter, B., et al. (2024) · Human Molecular Genetics · doi:10.1093/hmg/ddae135 · Cited by 16
“…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
Modeling neurodevelopmental and psychiatric diseases with human iPSCs
Wen, Z. (2017) · Journal of Neuroscience Research · doi:10.1002/jnr.24031 · Cited by 15
“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
“…(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
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 16
Self-citation
Metadata
- 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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