A human neurodevelopmental model for Williams syndrome

Nature

Volumn 536, Issue 7616, 2016, Pages 338-343

  Chailangkarn, Thanathom ^a,b,c,d   Trujillo, Cleber A ^a,b,c   Freitas, Beatriz C ^a,b,c   Hrvoj Mihic, Branka ^e   Herai, Roberto H ^a,b,c,f   Yu, Diana X ^g   Brown, Timothy T ^b,e,h   Marchetto, Maria C ^g   Bardy, Cedric ^g,i   McHenry, Lauren ^g   Stefanacci, Lisa ^a,b,c,e   Järvinen, Anna ^g   Searcy, Yvonne M ^g   Dewitt, Michelle ^g   Wong, Wenny ^g   Lai, Philip ^g   Ard, M Colin ^b   Hanson, Kari L ^e   Romero, Sarah ^a,b,c   Jacobs, Bob ^j   Dale, Anders M ^b,e,k   Dai, Li ^l,m   Korenberg, Julie R ^l,m   Gage, Fred H ^g,n   Bellugi, Ursula ^g   Halgren, Eric ^b,e,n   Semendeferi, Katerina ^b,e,n   Muotri, Alysson R ^a,b,c,n   more..

^a RADY CHILDREN'S HOSPITAL   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c San Diego   (United States)

^d NATIONAL SCIENCE AND TECHNOLOGY DEVELOPMENT AGENCY   (Thailand)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f PONTIFICAL CATHOLIC UNIVERSITY OF PARANÁ   (Brazil)

^g SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^h University of California   (United States)

ⁱ SOUTH AUSTRALIAN HEALTH AND MEDICAL RESEARCH INSTITUTE   (Australia)

^j University of Colorado College of Nursing   (United States)

^k UNIVERSITY OF CALIFORNIA   (United States)

^l UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^m UNIVERSITY OF UTAH   (United States)

ⁿ UNIVERSITY OF CALIFORNIA   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

FRIZZLED 9 PROTEIN; FRIZZLED PROTEIN; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; CALCIUM; FZD9 PROTEIN, HUMAN;

APOPTOSIS; BRAIN; CALCIUM; CELLS AND CELL COMPONENTS; CHROMOSOME; NERVOUS SYSTEM DISORDER; NUMERICAL MODEL; PHENOTYPE;

APOPTOSIS; ARTICLE; BRAIN CELL; CHROMOSOME 7Q; CHROMOSOME BAND; CONTROLLED STUDY; DENDRITE; DENDRITIC SPINE; GENE EXPRESSION PROFILING; HUMAN; HUMAN TISSUE; INDUCED PLURIPOTENT STEM CELL; MAJOR CLINICAL STUDY; NERVE CELL DIFFERENTIATION; NERVE CELL NETWORK; NEURAL STEM CELL; PRIORITY JOURNAL; SYNAPSE; WILLIAMS BEUREN SYNDROME; ADOLESCENT; ADULT; BIOLOGICAL MODEL; BRAIN; BRAIN CORTEX; CELL DIFFERENTIATION; CELL SHAPE; CHROMOSOME 7; DEFICIENCY; FEMALE; GENETICS; HAPLOINSUFFICIENCY; MALE; METABOLISM; NERVE CELL; NUCLEAR REPROGRAMMING; PATHOLOGY; PHENOTYPE; REPRODUCIBILITY; YOUNG ADULT;

ADOLESCENT; ADULT; APOPTOSIS; BRAIN; CALCIUM; CELL DIFFERENTIATION; CELL SHAPE; CELLULAR REPROGRAMMING; CEREBRAL CORTEX; CHROMOSOMES, HUMAN, PAIR 7; DENDRITES; FEMALE; FRIZZLED RECEPTORS; HAPLOINSUFFICIENCY; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MALE; MODELS, NEUROLOGICAL; NEURAL STEM CELLS; NEURONS; PHENOTYPE; REPRODUCIBILITY OF RESULTS; SYNAPSES; WILLIAMS SYNDROME; YOUNG ADULT;

EID: 84983372661     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature19067     Document Type: Article

References (59)

1. Korenberg, J. R. et al. VI. Genome structure and cognitive map of Williams syndrome. J. Cogn. Neurosci. 12 (Suppl. 1), 89-107 (2000).
2. Meyer-Lindenberg, A. et al. Neural basis of genetically determined visuospatial construction deficit in Williams syndrome. Neuron 43, 623-631 (2004).
3. Bellugi, U., Lichtenberger, L., Mills, D., Galaburda, A. & Korenberg, J. R. Bridging cognition, the brain and molecular genetics: evidence from Williams syndrome. Trends Neurosci. 22, 197-207 (1999).
4. Bellugi, U., Lichtenberger, L., Jones, W., Lai, Z. & St George, M. I. The neurocognitive profile of Williams syndrome: a complex pattern of strengths and weaknesses. J. Cogn. Neurosci. 12 (Suppl. 1), 7-29 (2000).
5. Doyle, T. F., Bellugi, U., Korenberg, J. R. & Graham, J. "Everybody in the world is my friend" hypersociability in young children with Williams syndrome. Am. J. Med. Genet. A 124, 263-273 (2004).
6. Dai, L. et al. Is it Williams syndrome? GTF2IRD1 implicated in visual-spatial construction and GTF2I in sociability revealed by high resolution arrays. Am. J. Med. Genet. A 149A, 302-314 (2009).
7. Edelmann, L. et al. An atypical deletion of the Williams-Beuren syndrome interval implicates genes associated with defective visuospatial processing and autism. J. Med. Genet. 44, 136-143 (2007).
8. Chailangkarn, T., Acab, A. & Muotri, A. R. Modeling neurodevelopmental disorders using human neurons. Curr. Opin. Neurobiol. 22, 785-790 (2012).
9. Ewart, A. K. et al. Hemizygosity at the elastin locus in a developmental disorder, Williams syndrome. Nature Genet. 5, 11-16 (1993).
10. Järvinen-Pasley, A. et al. Defining the social phenotype in Williams syndrome: a model for linking gene, the brain, and behavior. Dev. Psychopathol. 20, 1-35 (2008).
11. Marchetto, M. C. et al. A model for neural development and treatment of Rett syndrome using human induced pluripotent stem cells. Cell 143, 527-539 (2010).
12. Beltrão-Braga, P. C. B. et al. Feeder-free derivation of induced pluripotent stem cells from human immature dental pulp stem cells. Cell Transplant. 20, 1707-1719 (2011).
13. Adamo, A. et al. 7q11.23 dosage-dependent dysregulation in human pluripotent stem cells affects transcriptional programs in disease-relevant lineages. Nature Genet. 47, 132-141 (2015).
14. Van Raay, T. J. et al. frizzled 9 is expressed in neural precursor cells in the developing neural tube. Dev. Genes Evol. 211, 453-457 (2001).
15. Zhao, C. et al. Hippocampal and visuospatial learning defects in mice with a deletion of frizzled 9, a gene in the Williams syndrome deletion interval. Development 132, 2917-2927 (2005).
16. Fujimoto, T., Tomizawa, M. & Yokosuka, O. SiRNA of frizzled-9 suppresses proliferation and motility of hepatoma cells. Int. J. Oncol. 35, 861-866 (2009).
17. Lian, X. et al. Efficient differentiation of human pluripotent stem cells to endothelial progenitors via small-molecule activation of WNT signaling. Stem Cell Rep. 3, 804-816 (2014).
18. Jho, E. H. et al. Wnt/beta-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol. Cell. Biol. 22, 1172-1183 (2002).
19. Fujimura, N. et al. Wnt-mediated down-regulation of Sp1 target genes by a transcriptional repressor Sp5. J. Biol. Chem. 282, 1225-1237 (2007).
20. Srinivasan, K. et al. A network of genetic repression and derepression specifies projection fates in the developing neocortex. Proc. Natl Acad. Sci. USA 109, 19071-19078 (2012).
21. Chen, B. et al. The Fezf2-Ctip2 genetic pathway regulates the fate choice of subcortical projection neurons in the developing cerebral cortex. Proc. Natl Acad. Sci. USA 105, 11382-11387 (2008).
22. Leone, D. P., Srinivasan, K., Chen, B., Alcamo, E. & McConnell, S. K. The determination of projection neuron identity in the developing cerebral cortex. Curr. Opin. Neurobiol. 18, 28-35 (2008).
23. Hutsler, J. J. & Zhang, H. Increased dendritic spine densities on cortical projection neurons in autism spectrum disorders. Brain Res. 1309, 83-94 (2010).
24. Spitzer, N. C., Root, C. M. & Borodinsky, L. N. Orchestrating neuronal differentiation: patterns of Ca2+ spikes specify transmitter choice. Trends Neurosci. 27, 415-421 (2004).
25. Chiang, M. C. et al. 3D pattern of brain abnormalities in Williams syndrome visualized using tensor-based morphometry. Neuroimage 36, 1096-1109 (2007).
26. Lawless, J. F. & Fredette, M. Frequentist prediction intervals and predictive distributions. Biometrika 92, 529-542 (2005).
27. Chen, J. et al. Transcriptome comparison of human neurons generated using induced pluripotent stem cells derived from dental pulp and skin fibroblasts. PLoS ONE 8, e75682 (2013).
28. Marinho, P. A., Chailangkarn, T. & Muotri, A. R. Systematic optimization of human pluripotent stem cells media using Design of Experiments. Sci. Rep. 5, 9834 (2015).
29. Gautier, L., Cope, L., Bolstad, B. M. & Irizarry, R. A. affy-analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20, 307-315 (2004).
30. Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔC T method. Methods 25, 402-408 (2001).
31. Marchetto, M. C. et al. Differential L1 regulation in pluripotent stem cells of humans and apes. Nature 503, 525-529 (2013).
32. Zhang, B., Kirov, S. & Snoddy, J. WebGestalt: an integrated system for exploring gene sets in various biological contexts. Nucleic Acids Res. 33, W741-W748 (2005).
33. Shannon, P. et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498-2504 (2003).
34. Llorens-Bobadilla, E. et al. Single-cell transcriptomics reveals a population of dormant neural stem cells that become activated upon brain injury. Cell Stem Cell 17, 329-340 (2015).
35. Livak, K. J. et al. Methods for qPCR gene expression profiling applied to 1440 lymphoblastoid single cells. Methods 59, 71-79 (2013).
36. Hermann, B. P. et al. Transcriptional and translational heterogeneity among neonatal mouse spermatogonia. Biol. Reprod. 92, 54 (2015).
37. Jacobs, B. et al. Regional dendritic and spine variation in human cerebral cortex: a quantitative golgi study. Cereb. Cortex 11, 558-571 (2001).
38. Semendeferi, K. et al. Spatial organization of neurons in the frontal pole sets humans apart from great apes. Cereb. Cortex 21, 1485-1497 (2011).
39. Marin-Padilla, M. Structural abnormalities of the cerebral cortex in human chromosomal aberrations: a Golgi study. Brain Res. 44, 625-629 (1972).
40. Takashima, S., Becker, L. E., Armstrong, D. L. & Chan, F. Abnormal neuronal development in the visual cortex of the human fetus and infant with down's syndrome. A quantitative and qualitative Golgi study. Brain Res. 225, 1-21 (1981).
41. Jay, V., Chan, F. W. & Becker, L. E. Dendritic arborization in the human fetus and infant with the trisomy 18 syndrome. Brain Res. Dev. Brain Res. 54, 291-294 (1990).
42. Marin-Padilla, M. Prenatal and early postnatal ontogenesis of the human motor cortex: a golgi study. II. The basket-pyramidal system. Brain Res. 23, 185-191 (1970).
43. Vukšić, M., Petanjek, Z., Rasin, M. R. & Kostović, I. Perinatal growth of prefrontal layer III pyramids in Down syndrome. Pediatr. Neurol. 27, 36-38 (2002).
44. Jacobs, B. et al. Quantitative analysis of cortical pyramidal neurons after corpus callosotomy. Ann. Neurol. 54, 126-130 (2003).
45. Riley, J. N. A reliable Golgi-Kopsch modification. Brain Res. Bull. 4, 127-129 (1979).
46. Williams, R. S., Ferrante, R. J. & Caviness, V. S., Jr. The Golgi rapid method in clinical neuropathology: the morphologic consequences of suboptimal fixation. J. Neuropathol. Exp. Neurol. 37, 13-33 (1978).
47. Jacobs, B. & Scheibel, A. B. A quantitative dendritic analysis of Wernicke's area in humans. I. Lifespan changes. J. Comp. Neurol. 327, 83-96 (1993).
48. Uylings, H. B., Ruiz-Marcos, A. & van Pelt, J. The metric analysis of threedimensional dendritic tree patterns: a methodological review. J. Neurosci. Methods 18, 127-151 (1986).
49. White, N. et al. PROMO: Real-time prospective motion correction in MRI using image-based tracking. Magn. Reson. Med. 63, 91-105 (2010).
50. Brown, T. T. et al. Prospective motion correction of high-resolution magnetic resonance imaging data in children. Neuroimage 53, 139-145 (2010).
51. Kuperman, J. M. et al. Prospective motion correction improves diagnostic utility of pediatric MRI scans. Pediatr. Radiol. 41, 1578-1582 (2011).
52. Jovicich, J. et al. Reliability in multi-site structural MRI studies: effects of gradient non-linearity correction on phantom and human data. Neuroimage 30, 436-443 (2006).
53. Dale, A. M., Fischl, B. & Sereno, M. I. Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 9, 179-194 (1999).
54. Fischl, B., Sereno, M. I. & Dale, A. M. Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. Neuroimage 9, 195-207 (1999).
55. Fischl, B. et al. Sequence-independent segmentation of magnetic resonance images. Neuroimage 23 (Suppl 1), S69-S84 (2004).
56. Fischl, B. et al. Automatically parcellating the human cerebral cortex. Cereb. Cortex 14, 11-22 (2004).
57. Fischl, B. & Dale, A. M. Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc. Natl Acad. Sci. USA 97, 11050-11055 (2000).
58. Desikan, R. S. et al. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 31, 968-980 (2006).
59. Destrieux, C., Fischl, B., Dale, A. & Halgren, E. Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature. Neuroimage 53, 1-15 (2010).