Preloader

Production of human spinal-cord organoids recapitulating neural-tube morphogenesis

  • Smith, J. L. & Schoenwolf, G. C. Neurulation: coming to closure. Trends Neurosci. 20, 510–517 (1997).

    CAS 
    PubMed 

    Google Scholar 

  • Jankowska, E. Spinal interneuronal systems: identification, multifunctional character and reconfigurations in mammals. J. Physiol. 533, 31–40 (2001).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Lu, D. C., Niu, T. & Alaynick, W. A. Molecular and cellular development of spinal cord locomotor circuitry. Front. Mol. Neurosci. 8, 25 (2015).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Greene, N. D., Stanier, P. & Copp, A. J. Genetics of human neural tube defects. Hum. Mol. Genet. 18, R113–R129 (2009).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Loeken, M. R. Current perspectives on the causes of neural tube defects resulting from diabetic pregnancy. Am. J. Med. Genet. C 135, 77–87 (2005).

  • Matok, I. et al. Exposure to folic acid antagonists during the first trimester of pregnancy and the risk of major malformations. Br. J. Clin. Pharmacol. 68, 956–962 (2009).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Mølgaard-Nielsen, D. & Hviid, A. Newer-generation antiepileptic drugs and the risk of major birth defects. JAMA 305, 1996–2002 (2011).

    PubMed 

    Google Scholar 

  • Warmflash, A., Sorre, B., Etoc, F., Siggia, E. D. & Brivanlou, A. H. A method to recapitulate early embryonic spatial patterning in human embryonic stem cells. Nat. Methods 11, 847–854 (2014).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Haremaki, T. et al. Self-organizing neuruloids model developmental aspects of Huntington’s disease in the ectodermal compartment. Nat. Biotechnol. 37, 1198–1208 (2019).

    CAS 
    PubMed 

    Google Scholar 

  • Moris, N. et al. An in vitro model of early anteroposterior organization during human development. Nature 582, 410–415 (2020).

  • Kim, J., Koo, B.-K. & Knoblich, J. A. Human organoids: model systems for human biology and medicine. Nat. Rev. Mol. Cell Biol. 21, 571–584 (2020).

    CAS 
    PubMed 

    Google Scholar 

  • Lancaster, M. A. et al. Cerebral organoids model human brain development and microcephaly. Nature 501, 373 (2013).

    CAS 
    PubMed 

    Google Scholar 

  • Qian, X. et al. Brain-region-specific organoids using mini-bioreactors for modeling ZIKV exposure. Cell 165, 1238–1254 (2016).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Quadrato, G. et al. Cell diversity and network dynamics in photosensitive human brain organoids. Nature 545, 48 (2017).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Paşca, A. M. et al. Functional cortical neurons and astrocytes from human pluripotent stem cells in 3D culture. Nat. Methods 12, 671 (2015).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Kadoshima, T. et al. Self-organization of axial polarity, inside-out layer pattern, and species-specific progenitor dynamics in human ES cell–derived neocortex. Proc. Natl Acad. Sci. USA 110, 20284–20289 (2013).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Meinhardt, A. et al. 3D reconstitution of the patterned neural tube from embryonic stem cells. Stem Cell Rep. 3, 987–999 (2014).

    Google Scholar 

  • Ogura, T., Sakaguchi, H., Miyamoto, S. & Takahashi, J. Three-dimensional induction of dorsal, intermediate and ventral spinal cord tissues from human pluripotent stem cells. Development 145, dev162214 (2018).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Hor, J. H. et al. Cell cycle inhibitors protect motor neurons in an organoid model of spinal muscular atrophy. Cell Death Dis. 9, 1–12 (2018).

    CAS 

    Google Scholar 

  • Martins, J.-M. F. et al. Self-organizing 3D human trunk neuromuscular organoids. Cell Stem Cell 26, 172–186.e176 (2020).

    Google Scholar 

  • Rifes, P. et al. Modeling neural tube development by differentiation of human embryonic stem cells in a microfluidic WNT gradient. Nat. Biotechnol. 38, 1265–1273 (2020).

  • Quadrato, G., Brown, J. & Arlotta, P. The promises and challenges of human brain organoids as models of neuropsychiatric disease. Nat. Med. 22, 1220 (2016).

    CAS 
    PubMed 

    Google Scholar 

  • Velasco, S. et al. Individual brain organoids reproducibly form cell diversity of the human cerebral cortex. Nature 570, 523–527 (2019).

  • Denham, M. et al. Multipotent caudal neural progenitors derived from human pluripotent stem cells that give rise to lineages of the central and peripheral nervous system. Stem Cells 33, 1759–1770 (2015).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Anderson, M. J. et al. TCreERT2, a transgenic mouse line for temporal control of Cre-mediated recombination in lineages emerging from the primitive streak or tail bud. PLoS ONE 8, e62479 (2013).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Nagai, T. et al. The expression of the mouse Zic1, Zic2, and Zic3 gene suggests an essential role for Zic genes in body pattern formation. Dev. Biol. 182, 299–313 (1997).

    CAS 
    PubMed 

    Google Scholar 

  • Pyrgaki, C., Trainor, P., Hadjantonakis, A. K. & Niswander, L. Dynamic imaging of mammalian neural tube closure. Dev. Biol. 344, 941–947 (2010).

    CAS 
    PubMed 

    Google Scholar 

  • Aaku-Saraste, E., Hellwig, A. & Huttner, W. B. Loss of occludin and functional tight junctions, but not ZO-1, during neural tube closure—remodeling of the neuroepithelium prior to neurogenesis. Dev. Biol. 180, 664–679 (1996).

    CAS 
    PubMed 

    Google Scholar 

  • Nishimura, T., Honda, H. & Takeichi, M. Planar cell polarity links axes of spatial dynamics in neural-tube closure. Cell 149, 1084–1097 (2012).

    CAS 
    PubMed 

    Google Scholar 

  • Stuart, T. et al. Comprehensive integration of single-cell data. Cell 177, 1888–1902.e1821 (2019).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Delile, J. et al. Single cell transcriptomics reveals spatial and temporal dynamics of gene expression in the developing mouse spinal cord. Development 146, dev173807 (2019).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Floyd, T. L., Dai, Y. & Ladle, D. R. Characterization of calbindin D28k expressing interneurons in the ventral horn of the mouse spinal cord. Dev. Dyn. 247, 185–193 (2018).

    CAS 
    PubMed 

    Google Scholar 

  • Dale, N. Reciprocal inhibitory interneurones in the Xenopus embryo spinal cord. J. Physiol. 363, 61–70 (1985).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Shin, H. et al. Multifunctional multi-shank neural probe for investigating and modulating long-range neural circuits in vivo. Nat. Commun. 10, 3777 (2019).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Hanson, M. G. & Landmesser, L. T. Characterization of the circuits that generate spontaneous episodes of activity in the early embryonic mouse spinal cord. J. Neurosci. 23, 587–600 (2003).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Zafeiriou, M.-P. et al. Developmental GABA polarity switch and neuronal plasticity in bioengineered neuronal organoids. Nat. Commun. 11, 3791 (2020).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Greene, N. D. & Copp, A. J. Neural tube defects. Annu. Rev. Neurosci. 37, 221–242 (2014).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Agopian, A., Tinker, S. C., Lupo, P. J., Canfield, M. A. & Mitchell, L. E. Proportion of neural tube defects attributable to known risk factors. Birth Defects Res. A 97, 42–46 (2013).

    CAS 

    Google Scholar 

  • Weston, J. et al. Monotherapy treatment of epilepsy in pregnancy: congenital malformation outcomes in the child. Cochrane Database Syst. Rev. 11, CD010224 (2016).

  • Hughes, A., Greene, N. D., Copp, A. J. & Galea, G. L. Valproic acid disrupts the biomechanics of late spinal neural tube closure in mouse embryos. Mech. Dev. 149, 20–26 (2018).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Sahni, G. et al. A micropatterned human-specific neuroepithelial tissue for modeling gene and drug‐induced neurodevelopmental defects. Adv. Sci. 8, 2001100 (2021).

    CAS 

    Google Scholar 

  • Kawada, J. et al. Generation of a motor nerve organoid with human stem cell-derived neurons. Stem Cell Rep. 9, 1441–1449 (2017).

    Google Scholar 

  • Sternfeld, M. J. et al. Speed and segmentation control mechanisms characterized in rhythmically-active circuits created from spinal neurons produced from genetically-tagged embryonic stem cells. eLife 6, e21540 (2017).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Zheng, Y. et al. Dorsal-ventral patterned neural cyst from human pluripotent stem cells in a neurogenic niche. Sci. Adv. 5, eaax5933 (2019).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Davidson, B. P., Kinder, S. J., Steiner, K., Schoenwolf, G. C. & Tam, P. P. Impact of node ablation on the morphogenesis of the body axis and the lateral asymmetry of the mouse embryo during early organogenesis. Dev. Biol. 211, 11–26 (1999).

    CAS 
    PubMed 

    Google Scholar 

  • Stemple, D. L. Structure and function of the notochord: an essential organ for chordate development. Development 132, 2503–2512 (2005).

    CAS 

    Google Scholar 

  • Moury, J. D. & Schoenwolf, G. C. Cooperative model of epithelial shaping and bending during avian neurulation: autonomous movements of the neural plate, autonomous movements of the epidermis, and interactions in the neural plate/epidermis transition zone. Dev. Dyn. 204, 323–337 (1995).

    CAS 
    PubMed 

    Google Scholar 

  • Sato, T. et al. Single Lgr5 stem cells build crypt–villus structures in vitro without a mesenchymal niche. Nature 459, 262 (2009).

    CAS 
    PubMed 

    Google Scholar 

  • Lowery, L. A. & Sive, H. Strategies of vertebrate neurulation and a re-evaluation of teleost neural tube formation. Mech. Dev. 121, 1189–1197 (2004).

    CAS 
    PubMed 

    Google Scholar 

  • Yoon, S.-J. et al. Reliability of human cortical organoid generation. Nat. Met. 16, 75–78 (2019).

    CAS 

    Google Scholar 

  • Bakkum, D. J. et al. Parameters for burst detection. Front. Comput. Neurosci. 7, 193 (2014).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Butler, A., Hoffman, P., Smibert, P., Papalexi, E. & Satija, R. Integrating single-cell transcriptomic data across different conditions, technologies, and species. Nat. Biotechnol. 36, 411–420 (2018).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hafemeister, C. & Satija, R. Normalization and variance stabilization of single-cell RNA-seq data using regularized negative binomial regression. Genome Biol. 20, 1–15 (2019).

    Google Scholar 

  • Sakar, M. S. et al. Formation and optogenetic control of engineered 3D skeletal muscle bioactuators. Lab Chip 12, 4976–4985 (2012).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Source link