Maturation and circuit integration of transplanted human cortical organoids.


Journal

Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462

Informations de publication

Date de publication:
10 2022
Historique:
received: 16 12 2021
accepted: 25 08 2022
entrez: 12 10 2022
pubmed: 13 10 2022
medline: 15 10 2022
Statut: ppublish

Résumé

Self-organizing neural organoids represent a promising in vitro platform with which to model human development and disease

Identifiants

pubmed: 36224417
doi: 10.1038/s41586-022-05277-w
pii: 10.1038/s41586-022-05277-w
pmc: PMC9556304
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

319-326

Subventions

Organisme : NINDS NIH HHS
ID : K08 NS123544
Pays : United States
Organisme : NIMH NIH HHS
ID : T32 MH019938
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH115012
Pays : United States
Organisme : NIDA NIH HHS
ID : K99 DA050662
Pays : United States

Commentaires et corrections

Type : CommentIn
Type : CommentIn

Informations de copyright

© 2022. The Author(s).

Références

Kelley, K. W. & Pașca, S. P. Human brain organogenesis: toward a cellular understanding of development and disease. Cell 185, 42–61 (2021).
pubmed: 34774127 doi: 10.1016/j.cell.2021.10.003
Pasca, A. M. et al. Functional cortical neurons and astrocytes from human pluripotent stem cells in 3D culture. Nat. Methods 12, 671–678 (2015).
pubmed: 26005811 pmcid: 4489980 doi: 10.1038/nmeth.3415
Valesco, S. et al. Individual brain organoids reproducibly form cell diversity of the human cerebral cortex. Nature 570, 523–527 (2019).
doi: 10.1038/s41586-019-1289-x
Qian, X. et al. Brain-region-specific organoids using mini-bioreactors for modeling ZIKV exposure. Cell 165, 1238–1254 (2016).
pubmed: 27118425 pmcid: 4900885 doi: 10.1016/j.cell.2016.04.032
Yoon, S. J. et al. Reliability of human cortical organoid generation. Nat. Methods 16, 75–78 (2019).
pubmed: 30573846 doi: 10.1038/s41592-018-0255-0
Birey, F. et al. Assembly of functionally integrated human forebrain spheroids. Nature 545, 54–59 (2017).
pubmed: 28445465 pmcid: 5805137 doi: 10.1038/nature22330
Espuny-Camacho, I. et al. Pyramidal neurons derived from human pluripotent stem cells integrate efficiently into mouse brain circuits in vivo. Neuron 77, 440–456 (2013).
pubmed: 23395372 doi: 10.1016/j.neuron.2012.12.011
Linaro, D. et al. Xenotransplanted human cortical neurons reveal species-specific development and functional integration into mouse visual circuits. Neuron 104, 972–986.e6 (2019).
pubmed: 31761708 pmcid: 6899440 doi: 10.1016/j.neuron.2019.10.002
Mansour, A. A. et al. An in vivo model of functional and vascularized human brain organoids. Nat. Biotechnol. 36, 432–441 (2018).
pubmed: 29658944 pmcid: 6331203 doi: 10.1038/nbt.4127
Real, R. et al. In vivo modeling of human neuron dynamics and down syndrome. Science 362, eaau1810 (2018).
pubmed: 30309905 pmcid: 6570619 doi: 10.1126/science.aau1810
Kitahara, T. et al. Axonal extensions along corticospinal tracts from transplanted human cerebral organoids. Stem Cell Rep. 15, 467–481 (2020).
doi: 10.1016/j.stemcr.2020.06.016
Xiong, M. et al. Human stem cell-derived neurons repair circuits and restore neural function. Cell Stem Cell 28, 112–126.e6 (2021).
pubmed: 32966778 doi: 10.1016/j.stem.2020.08.014
Kichula, E. A. & Huntley, G. W. Developmental and comparative aspects of posterior medial thalamocortical innervation of the barrel cortex in mice and rats. J. Comp. Neurol. 509, 239–258 (2008).
pubmed: 18496871 pmcid: 4913357 doi: 10.1002/cne.21690
Ebert, D. H. & Greenberg, M. E. Activity-dependent neuronal signalling and autism spectrum disorder. Nature 493, 327–337 (2013).
pubmed: 23325215 pmcid: 3576027 doi: 10.1038/nature11860
Trujillo, C. A. et al. Complex oscillatory waves emerging from cortical organoids model early human brain network development. Cell Stem Cell 25, 558–569.e7 (2019).
pubmed: 31474560 pmcid: 6778040 doi: 10.1016/j.stem.2019.08.002
Hrvatin, S. et al. Single-cell analysis of experience-dependent transcriptomic states in the mouse visual cortex. Nat. Neurosci. 21, 120–129 (2018).
pubmed: 29230054 doi: 10.1038/s41593-017-0029-5
Ataman, B. et al. Evolution of osteocrin as an activity-regulated factor in the primate brain. Nature 539, 120–129 (2016).
doi: 10.1038/nature20111
Hong, E. J., McCord, A. E. & Greenberg, M. E. A biological function for the neuronal activity-dependent component of Bdnf transcription in the development of cortical inhibition. Neuron 60, 610–624 (2008).
pubmed: 19038219 pmcid: 2873221 doi: 10.1016/j.neuron.2008.09.024
Polioudakis, D. et al. A single-cell transcriptomic atlas of human neocortical development during mid-gestation. Neuron 103, 785–801.e8 (2019).
pubmed: 31303374 pmcid: 6831089 doi: 10.1016/j.neuron.2019.06.011
Trevino, A. E. et al. Chromatin and gene-regulatory dynamics of the developing human cerebral cortex at single-cell resolution. Cell 184, 5053–5069.e23 (2021).
pubmed: 34390642 doi: 10.1016/j.cell.2021.07.039
Hodge, R. D. et al. Conserved cell types with divergent features in human versus mouse cortex. Nature 573, 61–68 (2019).
pubmed: 31435019 pmcid: 6919571 doi: 10.1038/s41586-019-1506-7
Bakken, T. E. et al. Comparative cellular analysis of motor cortex in human, marmoset and mouse. Nature 598, 111–119 (2021).
pubmed: 34616062 pmcid: 8494640 doi: 10.1038/s41586-021-03465-8
Li, M. et al. Integrative functional genomic analysis of human brain development and neuropsychiatric risks. Science 362, eaat7615 (2018).
pubmed: 30545854 pmcid: 6413317 doi: 10.1126/science.aat7615
Gordon, A. et al. Long-term maturation of human cortical organoids matches key early postnatal transitions. Nat. Neurosci. 24, 331–342 (2021).
pubmed: 33619405 pmcid: 8109149 doi: 10.1038/s41593-021-00802-y
Krey, J. F. et al. Timothy syndrome is associated with activity-dependent dendritic retraction in rodent and human neurons. Nat. Neurosci. 16, 201–209 (2013).
pubmed: 23313911 pmcid: 3568452 doi: 10.1038/nn.3307
Agmon, A. & Connors, B. W. Thalamocortical responses of mouse somatosensory (barrel) cortex in vitro. Neuroscience 41, 365–379 (1991).
pubmed: 1870696 doi: 10.1016/0306-4522(91)90333-J
Petreanu, L., Mao, T., Sternson, S. M. & Svoboda, K. The subcellular organization of neocortical excitatory connections. Nature 457, 1142–1145 (2009).
pubmed: 19151697 pmcid: 2745650 doi: 10.1038/nature07709
Kalmbach, B. E. et al. h-Channels contribute to divergent intrinsic membrane properties of supragranular pyramidal neurons in human versus mouse cerebral cortex. Neuron 100, 1194–1208.e5 (2018).
pubmed: 30392798 pmcid: 6447369 doi: 10.1016/j.neuron.2018.10.012
Molnár, Z., Luhmann, H. J. & Kanold, P. O. Transient cortical circuits match spontaneous and sensory-driven activity during development. Science 370, eabb2153 (2020).
pubmed: 33060328 pmcid: 8050953 doi: 10.1126/science.abb2153
Jabaudon, D. Fate and freedom in developing neocortical circuits. Nat. Commun. 8, 16042 (2017).
pubmed: 28671189 pmcid: 5500875 doi: 10.1038/ncomms16042
Matson, K. J. et al. Isolation of adult spinal cord nuclei for massively parallel single-nucleus RNA sequencing. J. Vis. Exp. 140, 58413 (2018).
Stuart, T. et al. Comprehensive integration of single-cell data. Cell 177, 1888–1902.e21 (2019).
pubmed: 31178118 pmcid: 6687398 doi: 10.1016/j.cell.2019.05.031
McGinnis, C. S., Murrow, L. M. & Gartner, Z. J. DoubletFinder: doublet detection in single-cell RNA sequencing data using artificial nearest neighbors. Cell Syst. 8, 329–337.e4 (2019).
pubmed: 30954475 pmcid: 6853612 doi: 10.1016/j.cels.2019.03.003
Becht, E. et al. Dimensionality reduction for visualizing single-cell data using UMAP. Nat. Biotechnol. 37, 38–44 (2019).
doi: 10.1038/nbt.4314
Nowakowski, T. J. et al. Spatiotemporal gene expression trajectories reveal developmental hierarchies of the human cortex. Science 358, 1318–1323 (2017).
pubmed: 29217575 pmcid: 5991609 doi: 10.1126/science.aap8809
Squair, J. W. et al. Confronting false discoveries in single-cell differential expression. Nat. Commun. 12, 5692 (2021).
pubmed: 34584091 pmcid: 8479118 doi: 10.1038/s41467-021-25960-2
Chen, J., Bardes, E. E., Aronow, B. J. & Jegga, A. G. ToppGene Suite for gene list enrichment analysis and candidate gene prioritization. Nucleic Acids Res. 37, W305–W311 (2009).
pubmed: 19465376 pmcid: 2703978 doi: 10.1093/nar/gkp427
Zhu, Y. et al. Spatiotemporal transcriptomic divergence across human and macaque brain development. Science 362, eaat8077 (2018).
pubmed: 30545855 pmcid: 6900982 doi: 10.1126/science.aat8077
Huguenard, J. R. & Prince, D. A. Intrathalamic rhythmicity studied in vitro: nominal T-current modulation causes robust antioscillatory effects. J. Neurosci. 14, 5485–5502 (1994).
pubmed: 8083749 pmcid: 6577071 doi: 10.1523/JNEUROSCI.14-09-05485.1994
Feng, L., Zhao, T. & Kim, J. Neutube 1.0: a new design for efficient neuron reconstruction software based on the SWC format. eNeuro 2, ENEURO.0049-14.2014 (2015).
pubmed: 26464967 pmcid: 4586918 doi: 10.1523/ENEURO.0049-14.2014
Arshadi, C., Günther, U., Eddison, M., Harrington, K. I. S. & Ferreira, T. A. SNT: a unifying toolbox for quantification of neuronal anatomy. Nat. Methods 18, 374–377 (2021).
pubmed: 33795878 doi: 10.1038/s41592-021-01105-7
Steinberg, E. E. et al. Amygdala–midbrain connections modulate appetitive and aversive learning. Neuron 106, 1026–1043.e9 (2020).
pubmed: 32294466 doi: 10.1016/j.neuron.2020.03.016
Zhou, P. et al. Efficient and accurate extraction of in vivo calcium signals from microendoscopic video data. eLife 7, e28728 (2018).
pubmed: 29469809 pmcid: 5871355 doi: 10.7554/eLife.28728
Stringer, C., Pachitariu, M., Steinmetz, N., Carandini, M. & Harris, K. D. High-dimensional geometry of population responses in visual cortex. Nature 571, 361–365 (2019).
pubmed: 31243367 pmcid: 6642054 doi: 10.1038/s41586-019-1346-5

Auteurs

Omer Revah (O)

Department of Psychiatry and Behavioral Sciences, Stanford University, Stanford, CA, USA.
Stanford Brain Organogenesis, Wu Tsai Neurosciences Institute and Bio-X, Stanford University, Stanford, CA, USA.

Felicity Gore (F)

Department of Psychiatry and Behavioral Sciences, Stanford University, Stanford, CA, USA.
Department of Bioengineering, Stanford University, Stanford, CA, USA.

Kevin W Kelley (KW)

Department of Psychiatry and Behavioral Sciences, Stanford University, Stanford, CA, USA.
Stanford Brain Organogenesis, Wu Tsai Neurosciences Institute and Bio-X, Stanford University, Stanford, CA, USA.

Jimena Andersen (J)

Department of Psychiatry and Behavioral Sciences, Stanford University, Stanford, CA, USA.
Stanford Brain Organogenesis, Wu Tsai Neurosciences Institute and Bio-X, Stanford University, Stanford, CA, USA.

Noriaki Sakai (N)

Department of Psychiatry and Behavioral Sciences, Stanford University, Stanford, CA, USA.

Xiaoyu Chen (X)

Department of Psychiatry and Behavioral Sciences, Stanford University, Stanford, CA, USA.
Stanford Brain Organogenesis, Wu Tsai Neurosciences Institute and Bio-X, Stanford University, Stanford, CA, USA.

Min-Yin Li (MY)

Department of Psychiatry and Behavioral Sciences, Stanford University, Stanford, CA, USA.
Stanford Brain Organogenesis, Wu Tsai Neurosciences Institute and Bio-X, Stanford University, Stanford, CA, USA.

Fikri Birey (F)

Department of Psychiatry and Behavioral Sciences, Stanford University, Stanford, CA, USA.
Stanford Brain Organogenesis, Wu Tsai Neurosciences Institute and Bio-X, Stanford University, Stanford, CA, USA.

Xiao Yang (X)

Department of Psychiatry and Behavioral Sciences, Stanford University, Stanford, CA, USA.
Stanford Brain Organogenesis, Wu Tsai Neurosciences Institute and Bio-X, Stanford University, Stanford, CA, USA.
Department of Chemistry, Stanford University, Stanford, CA, USA.

Nay L Saw (NL)

Stanford Behavioral and Functional Neuroscience Laboratory, Wu Tsai Neurosciences Institute, Stanford University, Stanford, CA, USA.

Samuel W Baker (SW)

Department of Comparative Medicine, Stanford University, Stanford, CA, USA.

Neal D Amin (ND)

Department of Psychiatry and Behavioral Sciences, Stanford University, Stanford, CA, USA.
Stanford Brain Organogenesis, Wu Tsai Neurosciences Institute and Bio-X, Stanford University, Stanford, CA, USA.

Shravanti Kulkarni (S)

Department of Psychiatry and Behavioral Sciences, Stanford University, Stanford, CA, USA.
Stanford Brain Organogenesis, Wu Tsai Neurosciences Institute and Bio-X, Stanford University, Stanford, CA, USA.

Rachana Mudipalli (R)

Department of Psychiatry and Behavioral Sciences, Stanford University, Stanford, CA, USA.
Department of Bioengineering, Stanford University, Stanford, CA, USA.

Bianxiao Cui (B)

Department of Chemistry, Stanford University, Stanford, CA, USA.

Seiji Nishino (S)

Department of Psychiatry and Behavioral Sciences, Stanford University, Stanford, CA, USA.

Gerald A Grant (GA)

Department of Neurosurgery, Stanford University, Stanford, CA, USA.

Juliet K Knowles (JK)

Department of Neurology and Neurological Sciences, Stanford, CA, USA.

Mehrdad Shamloo (M)

Stanford Behavioral and Functional Neuroscience Laboratory, Wu Tsai Neurosciences Institute, Stanford University, Stanford, CA, USA.
Department of Neurosurgery, Stanford University, Stanford, CA, USA.

John R Huguenard (JR)

Department of Neurology and Neurological Sciences, Stanford, CA, USA.

Karl Deisseroth (K)

Department of Psychiatry and Behavioral Sciences, Stanford University, Stanford, CA, USA.
Department of Bioengineering, Stanford University, Stanford, CA, USA.
Howard Hughes Medical Institute, Stanford University, Stanford, CA, USA.

Sergiu P Pașca (SP)

Department of Psychiatry and Behavioral Sciences, Stanford University, Stanford, CA, USA. spasca@stanford.edu.
Stanford Brain Organogenesis, Wu Tsai Neurosciences Institute and Bio-X, Stanford University, Stanford, CA, USA. spasca@stanford.edu.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH