Single-cell transcriptomic landscape of the developing human spinal cord
Abstract
Understanding spinal cord assembly is essential to elucidate how motor behavior is controlled and how disorders arise. The human spinal cord is exquisitely organized, and this complex organization contributes to the diversity and intricacy of motor behavior and sensory processing. But how this complexity arises at the cellular level in the human spinal cord remains unknown. Here we transcriptomically profiled the midgestation human spinal cord with single-cell resolution and discovered remarkable heterogeneity across and within cell types. Glia displayed diversity related to positional identity along the dorso-ventral and rostro-caudal axes, while astrocytes with specialized transcriptional programs mapped into white and gray matter subtypes. Motor neurons clustered at this stage into groups suggestive of alpha and gamma neurons. We also integrated our data with multiple existing datasets of the developing human spinal cord spanning 22 weeks of gestation to investigate the cell diversity over time. Together with mapping of disease-related genes, this transcriptomic mapping of the developing human spinal cord opens new avenues for interrogating the cellular basis of motor control in humans and guides human stem cell-based models of disease.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The cells projected on the UMAP space were annotated using canonical marker genes for neurons, progenitors, intermediate progenitors, astrocytes, other glial cells, and monocytes.
“The cells projected on the UMAP space were annotated using canonical marker genes for neurons, progenitors, intermediate progenitors, astrocytes, other glial cells, and monocytes (17, 84, 85).”
From Understanding monocyte-driven neuroinflammation in Alzheimer’s disease using human cortical organoid microphysiological systems (2025) · cites this paper as [85]
Cites
Comprehensive Integration of Single-Cell Data
Stuart, T., Butler, A., Hoffman, P., Hafemeister, C., Papalexi, E., Mauck, W. M., Hao, Y., Stoeckius, M., Smibert, P., & Satija, R. (2019) · Cell · doi:10.1016/j.cell.2019.05.031 · Cited by 15,453 · see citing works
Neurotoxic reactive astrocytes are induced by activated microglia
Liddelow, S. A., Guttenplan, K. A., Clarke, L. E., Bennett, F. C., Bohlen, C. J., Schirmer, L., Bennett, M. L., Münch, A. E., Chung, W.-S., Peterson, T. C., et al. (2017) · Nature · doi:10.1038/nature21029 · Cited by 7,971 · see citing works
La Manno, G., Soldatov, R., Zeisel, A., Braun, E., Hochgerner, H., Petukhov, V., Lidschreiber, K., Kastriti, M. E., Lönnerberg, P., Furlan, A., et al. (2018) · Nature · doi:10.1038/s41586-018-0414-6 · Cited by 4,118 · see citing works
Molecular Architecture of the Mouse Nervous System
Zeisel, A., Hochgerner, H., Lönnerberg, P., Johnsson, A., Memic, F., van der Zwan, J., Häring, M., Braun, E., Borm, L. E., La Manno, G., et al. (2018) · Cell · doi:10.1016/j.cell.2018.06.021 · Cited by 2,995 · see citing works
Generalizing RNA velocity to transient cell states through dynamical modeling
Bergen, V., Lange, M., Peidli, S., Wolf, F. A., & Theis, F. J. (2020) · Nature Biotechnology · doi:10.1038/s41587-020-0591-3 · Cited by 2,951 · see citing works
Neuronal specification in the spinal cord: inductive signals and transcriptional codes
Jessell, T. M. (2000) · Nature Reviews Genetics · doi:10.1038/35049541 · Cited by 2,089 · see citing works
Conserved cell types with divergent features in human versus mouse cortex
Hodge, R. D., Bakken, T. E., Miller, J. A., Smith, K. A., Barkan, E. R., Graybuck, L. T., Close, J. L., Long, B., Johansen, N., Penn, O., et al. (2019) · Nature · doi:10.1038/s41586-019-1506-7 · Cited by 1,775 · cited 5× · see citing works
“Therefore, the neuronal subcluster consists mainly of samples from GW4–21.”
InfluentialUniquely Hominid Features of Adult Human Astrocytes
Oberheim, N. A., Takano, T., Han, X., He, W., Lin, J. H. C., Wang, F., Xu, Q., Wyatt, J. D., Pilcher, W., Ojemann, J. G., et al. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.4707-08.2009 · Cited by 1,488 · see citing works
Single-cell profiling of the developing mouse brain and spinal cord with split-pool barcoding
Rosenberg, A. B., Roco, C. M., Muscat, R. A., Kuchina, A., Sample, P., Yao, Z., Graybuck, L. T., Peeler, D. J., Mukherjee, S., Chen, W., et al. (2018) · Science · doi:10.1126/science.aam8999 · Cited by 1,422 · see citing works
Astrocytes mediate synapse elimination through MEGF10 and MERTK pathways
Chung, W.-S., Clarke, L. E., Wang, G. X., Stafford, B. K., Sher, A., Chakraborty, C., Joung, J., Foo, L. C., Thompson, A., Chen, C., et al. (2013) · Nature · doi:10.1038/nature12776 · Cited by 1,377 · see citing works
Cell Biology of Astrocyte-Synapse Interactions
Allen, N. J., & Eroğlu, Ç. (2017) · Neuron · doi:10.1016/j.neuron.2017.09.056 · Cited by 1,031 · see citing works
Non–cell autonomous toxicity in neurodegenerative disorders: ALS and beyond
Ilieva, H., Polymenidou, M., & Cleveland, D. W. (2009) · Journal of Cell Biology · doi:10.1083/jcb.200908164 · Cited by 1,008 · see citing works
Exome sequencing in amyotrophic lateral sclerosis identifies risk genes and pathways
Cirulli, E. T., Lasseigne, B. N., Petrovski, S., Sapp, P. C., Dion, P. A., Leblond, C. S., Couthouis, J., Lu, Y.-F., Wang, Q., Krueger, B. J., et al. (2015) · Science · doi:10.1126/science.aaa3650 · Cited by 966 · see citing works
Molecular Identity of Human Outer Radial Glia during Cortical Development
Pollen, A. A., Nowakowski, T. J., Chen, J., Retallack, H., Sandoval-Espinosa, C., Nicholas, C. R., Shuga, J., Liu, S. J., Oldham, M. C., Diaz, A., et al. (2015) · Cell · doi:10.1016/j.cell.2015.09.004 · Cited by 908 · see citing works
Glia — more than just brain glue
Allen, N. J., & Barres, B. A. (2009) · Nature · doi:10.1038/457675a · Cited by 856 · see citing works
Mutations in GFAP, encoding glial fibrillary acidic protein, are associated with Alexander disease
Brenner, M., Johnson, T., Boespflug‐Tanguy, O., Rodriguez, D., Goldman, J. E., & Messing, A. (2001) · Nature Genetics · doi:10.1038/83679 · Cited by 689 · see citing works
Genome-Wide Analyses Identify KIF5A as a Novel ALS Gene
Nicolas, A., Kenna, K. P., Renton, A. E., Ticozzi, N., Faghri, F., Chia, R., Dominov, J. A., Kenna, B., Nalls, M. A., Keagle, P. J., et al. (2018) · Neuron · doi:10.1016/j.neuron.2018.02.027 · Cited by 670 · see citing works
Genetic identification of brain cell types underlying schizophrenia
Major Depressive Disorder Working Group of the Psychiatric Genomics Consortium, Skene, N. G., Bryois, J., Bakken, T. E., Breen, G., Crowley, J. J., Gaspar, H. A., Giusti-Rodriguez, P., Hodge, R. D., Miller, J. A., et al. (2018) · Nature Genetics · doi:10.1038/s41588-018-0129-5 · Cited by 651 · see citing works
Functional diversity of astrocytes in neural circuit regulation
Haim, L. B., & Rowitch, D. H. (2017) · Nature Reviews Neuroscience · doi:10.1038/nrn.2016.159 · Cited by 618 · see citing works
Single-nucleus and single-cell transcriptomes compared in matched cortical cell types
Bakken, T. E., Hodge, R. D., Miller, J. A., Yao, Z., Nguyen, T. N., Aevermann, B., Barkan, E., Bertagnolli, D., Casper, T., Dee, N., et al. (2018) · PLoS ONE · doi:10.1371/journal.pone.0209648 · Cited by 608 · see citing works
PARALS Registry, van Rheenen, W., SLALOM Group, SLAP Registry, NNIPPS Study Group, Shatunov, A., Dekker, A. M., McLaughlin, R. L., Diekstra, F. P., Pulit, S. L., et al. (2016) · Nature Genetics · doi:10.1038/ng.3622 · Cited by 574 · see citing works
Regional Astrocyte Allocation Regulates CNS Synaptogenesis and Repair
Tsai, H., Li, H., Fuentealba, L. C., Molofsky, A. V., Taveira‐Marques, R., Zhuang, H., Tenney, A., Murnen, A. T., Fancy, S. P. J., Merkle, F. T., et al. (2012) · Science · doi:10.1126/science.1222381 · Cited by 529 · see citing works
Evolution of the Human Nervous System Function, Structure, and Development
Sousa, A. M. M., Meyer, K. A., Santpere, G., Gulden, F. O., & Sestan, N. (2017) · Cell · doi:10.1016/j.cell.2017.06.036 · Cited by 517 · see citing works
Generation and assembly of human brain region-specific three-dimensional cultures
Sloan, S. A., Andersen, J., Pașca, A. M., Birey, F., & Pașca, S. P. (2018) · Nature Protocols · doi:10.1038/s41596-018-0032-7 · Cited by 490 · see citing works
Self-citationThe Emerging Nature of Astrocyte Diversity
Khakh, B. S., & Deneen, B. (2019) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-070918-050443 · Cited by 485 · see citing works
Trevino, A. E., Müller, F., Andersen, J., Sundaram, L., Kathiria, A., Shcherbina, A., Farh, K., Chang, H. Y., Pașca, A. M., Kundaje, A., et al. (2021) · Cell · doi:10.1016/j.cell.2021.07.039 · Cited by 478 · see citing works
Self-citationHäring, M., Zeisel, A., Hochgerner, H., Rinwa, P., Jakobsson, J. E. T., Lönnerberg, P., La Manno, G., Sharma, N., Borgius, L., Kiehn, O., et al. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0141-1 · Cited by 470 · see citing works
Transcriptional neoteny in the human brain
Somel, M., Franz, H., Zheng, Y., Lorenc, A., Guo, S., Giger, T., Kelso, J. F., Nickel, B., Dannemann, M., Bahn, S., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0900544106 · Cited by 409 · see citing works
van der Knaap, M. S., & Bugiani, M. (2017) · Acta Neuropathologica · doi:10.1007/s00401-017-1739-1 · Cited by 403 · see citing works
Sathyamurthy, A., Johnson, K. R., Matson, K. J. E., Dobrott, C. I., Li, L., Ryba, A. R., Bergman, T. B., Kelly, M. C., Kelley, M. W., & Levine, A. J. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.02.003 · Cited by 370 · see citing works
Self-citationExome-wide Rare Variant Analysis Identifies TUBA4A Mutations Associated with Familial ALS
Smith, B. N., Ticozzi, N., Fallini, C., Gkazi, S. A., Topp, S. D., Kenna, K. P., Scotter, E. L., Kost, J., Keagle, P. J., Miller, J. W., et al. (2014) · Neuron · doi:10.1016/j.neuron.2014.09.027 · Cited by 368 · see citing works
Delile, J., Rayon, T., Melchionda, M., Edwards, A., Briscoe, J., & Sagner, A. (2019) · Development · doi:10.1242/dev.173807 · Cited by 356 · see citing works
Spinal Muscular Atrophy: A Deficiency in a Ubiquitous Protein; a Motor Neuron-Specific Disease
Monani, U. R. (2005) · Neuron · doi:10.1016/j.neuron.2005.12.001 · Cited by 352 · see citing works
Astrocyte regulation of synaptic behavior
Allen, N. J. (2014) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100913-013053 · Cited by 343 · see citing works
Hochstim, C., Deneen, B., Lukaszewicz, A., Zhou, Q., & Anderson, D. J. (2008) · Cell · doi:10.1016/j.cell.2008.02.046 · Cited by 331 · see citing works
Astrocyte-encoded positional cues maintain sensorimotor circuit integrity
Molofsky, A. V., Kelley, K. W., Tsai, H., Redmond, S., Chang, S., Madireddy, L., Chan, J. R., Baranzini, S. E., Ullian, E. M., & Rowitch, D. H. (2014) · Nature · doi:10.1038/nature13161 · Cited by 312 · see citing works
Regulation of motor neuron pool sorting by differential expression of type II cadherins
Price, S. R., De Marco Garcia, N. V., Ranscht, B., & Jessell, T. M. (2002) · Cell · doi:10.1016/s0092-8674(02)00695-5 · Cited by 304 · see citing works
Establishing neuronal diversity in the spinal cord: a time and a place
Sagner, A., & Briscoe, J. (2019) · Development · doi:10.1242/dev.182154 · Cited by 282 · see citing works
NEK1 variants confer susceptibility to amyotrophic lateral sclerosis
Kenna, K. P., van Doormaal, P. T. C., Dekker, A. M., Ticozzi, N., Kenna, B., Diekstra, F. P., van Rheenen, W., van Eijk, K. R., Jones, A. R., Keagle, P. J., et al. (2016) · Nature Genetics · doi:10.1038/ng.3626 · Cited by 281 · see citing works
Conservation and divergence of cortical cell organization in human and mouse revealed by MERFISH
Fang, R., Xia, C., Close, J. L., Zhang, M., He, J., Huang, Z., Halpern, A. R., Long, B., Miller, J. A., Lein, E. S., et al. (2022) · Science · doi:10.1126/science.abm1741 · Cited by 277 · see citing works
Lavialle, M., Aumann, G., Anlauf, E., Pröls, F., Arpin, M., & Derouiche, A. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1100957108 · Cited by 267 · see citing works
A harmonized atlas of mouse spinal cord cell types and their spatial organization
Russ, D. E., Cross, R. B. P., Li, L., Koch, S. C., Matson, K. J. E., Yadav, A., Alkaslasi, M. R., Lee, D. I., Le Pichon, C. E., Menon, V., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-25125-1 · Cited by 255 · see citing works
Self-citationChromatin accessibility dynamics in a model of human forebrain development
Trevino, A. E., Sinnott-Armstrong, N., Andersen, J., Yoon, S.-J., Huber, N., Pritchard, J. K., Chang, H. Y., Greenleaf, W. J., & Pașca, S. P. (2020) · Science · doi:10.1126/science.aay1645 · Cited by 251 · see citing works
Self-citationSrinivasan, J., Schachner, M., & Catterall, W. A. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.26.15753 · Cited by 249 · see citing works
Olig2 Directs Astrocyte and Oligodendrocyte Formation in Postnatal Subventricular Zone Cells
Marshall, C. A. G., Novitch, B. G., & Goldman, J. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1924-05.2005 · Cited by 249 · see citing works
Smith, B. N., Topp, S. D., Fallini, C., Shibata, H., Chen, H.-J., Troakes, C., King, A., Ticozzi, N., Kenna, K. P., Gkazi, S. A., et al. (2017) · Science Translational Medicine · doi:10.1126/scitranslmed.aad9157 · Cited by 249 · see citing works
Blum, J. A., Klemm, S., Shadrach, J. L., Guttenplan, K. A., Nakayama, L., Kathiria, A., Hoang, P. T., Gautier, O., Kaltschmidt, J. A., Greenleaf, W. J., et al. (2021) · Nature Neuroscience · doi:10.1038/s41593-020-00795-0 · Cited by 210 · see citing works
Self-citationRewiring of human neurodevelopmental gene regulatory programs by human accelerated regions
Girskis, K. M., Stergachis, A. B., DeGennaro, E. M., Doan, R. N., Qian, X., Johnson, M. B., Wang, P. P., Sejourne, G. M., Nagy, M. A., Pollina, E. A., et al. (2021) · Neuron · doi:10.1016/j.neuron.2021.08.005 · Cited by 193 · see citing works
Masahira, N., Takebayashi, H., Ono, K., Watanabe, K., Ding, L., Furusho, M., Ogawa, Y., Nabeshima, Y., Álvarez-Buylla, A., Shimizu, K., et al. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.02.029 · Cited by 182 · see citing works
Depienne, C., Bugiani, M., Dupuits, C., Damien Galanaud, E., Touitou, V., Postma, N. L., van Berkel, C. G. M., Polder, E., Tollard, É., Darios, F. D., et al. (2013) · The Lancet Neurology · doi:10.1016/s1474-4422(13)70053-x · Cited by 181 · see citing works
Analysis of early human neural crest development
Betters, E., Liu, Y., Kjaeldgaard, A., Sundström, E., & García-Castro, M. I. (2010) · Developmental Biology · doi:10.1016/j.ydbio.2010.05.012 · Cited by 181 · see citing works
Glial control of neuronal development.
Lemke, G. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.87 · Cited by 157 · see citing works
Farhan, S. M. K., Howrigan, D. P., Abbott, L. E., Klim, J. R., Topp, S. D., Byrnes, A., Churchhouse, C. L., Phatnani, H. P., Smith, B. N., Rampersaud, E., et al. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0530-0 · Cited by 151 · see citing works
A latent lineage potential in resident neural stem cells enables spinal cord repair
Llorens-Bobadilla, E., Chell, J. M., Merre, P. L., Wu, Y.-C., Zamboni, M., Bergenstråhle, J., Stenudd, M., Sopova, E., Lundeberg, J., Shupliakov, O., et al. (2020) · Science · doi:10.1126/science.abb8795 · Cited by 143 · see citing works
GluA2-lacking, calcium-permeable AMPA receptors--inducers of plasticity?
Man, H.-Y. (2011) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.01.001 · Cited by 142 · see citing works
Roles of axon guidance molecules in neuronal wiring in the developing spinal cord
Chédotal, A. (2019) · Nature reviews. Neuroscience · doi:10.1038/s41583-019-0168-7 · Cited by 138 · see citing works
Rayón, T., Maizels, R. J., Barrington, C., & Briscoe, J. (2021) · Development · doi:10.1242/dev.199711 · Cited by 132 · see citing works
Neuronal Nuclei Isolation from Human Postmortem Brain Tissue
Matevossian, A., & Akbarian, S. (2008) · Journal of Visualized Experiments · doi:10.3791/914 · Cited by 126 · see citing works
Gap junctions in inherited human disorders of the central nervous system
Abrams, C. K., & Scherer, S. S. (2011) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2011.08.015 · Cited by 120 · see citing works
Osseward, P. J., Amin, N. D., Moore, J. D., Temple, B. A., Barriga, B. K., Bachmann, L. C., Beltran, F., Gullo, M., Clark, R. C., Driscoll, S. P., et al. (2021) · Science · doi:10.1126/science.abe0690 · Cited by 115 · see citing works
Self-citationControl of species-dependent cortico-motoneuronal connections underlying manual dexterity
Gu, Z., Kalambogias, J., Yoshioka, S., Han, W., Li, Z., Kawasawa, Y. I., Pochareddy, S., Li, Z., Liu, F., Xu, X., et al. (2017) · Science · doi:10.1126/science.aan3721 · Cited by 114 · see citing works
FOCAL LOSS OF ANTERIOR HORN CELLS IN THE CERVICAL CORD IN MOTOR NEURON DISEASE
Swash, M., LEADER, M., BROWN, A., & Swettenham, K. V. (1986) · Brain · doi:10.1093/brain/109.5.939 · Cited by 81 · see citing works
Single-cell analysis reveals dynamic changes of neural cells in developing human spinal cord
Zhang, Q., Wu, X., Fan, Y., Jiang, P., Zhao, Y., Yang, Y., Han, S., Bai, X., Chen, B., Han, J., et al. (2021) · EMBO Reports · doi:10.15252/embr.202152728 · Cited by 69 · see citing works
Hypomyelinating leukodystrophies — a molecular insight into the white matter pathology
Charzewska, A., Wierzba, J., Iżycka‐Świeszewska, E., Bekiesińska‐Figatowska, M., Jurek, M., Gintowt, A., Kłosowska, A., Bal, J., & Hoffman‐Zacharska, D. (2016) · Clinical Genetics · doi:10.1111/cge.12811 · Cited by 60 · see citing works
Isolation of Adult Spinal Cord Nuclei for Massively Parallel Single-nucleus RNA Sequencing
Matson, K. J. E., Sathyamurthy, A., Johnson, K. R., Kelly, M. C., Kelley, M. W., & Levine, A. J. (2018) · Journal of Visualized Experiments · doi:10.3791/58413 · Cited by 57 · see citing works
Region-specific distribution of Olig2-expressing astrocytes in adult mouse brain and spinal cord
Wang, H., Xu, L., Lai, C., Hou, K., Chen, J., Guo, Y., Sambangi, A., Swaminathan, S., Xie, C., Wu, Z., et al. (2021) · Molecular Brain · doi:10.1186/s13041-021-00747-0 · Cited by 57 · see citing works
Vue, T. Y., Kim, E. J., Parras, C. M., Guillemot, F., & Johnson, J. E. B. (2014) · Development · doi:10.1242/dev.105270 · Cited by 48 · see citing works
Ghazale, H., Ripoll, C., Leventoux, N., Jacob, L., Azar, S., Mamaeva, D. V., Glasson, Y., Calvo, C., Thomas, J., Meneceur, S., et al. (2019) · Stem Cell Reports · doi:10.1016/j.stemcr.2019.04.001 · Cited by 42 · see citing works
Ashrafi, S., Lalancette–Hébert, M., Friese, A., Sigrist, M., Arber, S., Shneider, N. A., & Kaltschmidt, J. A. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.1160-12.2012 · Cited by 39 · see citing works
Self-citationCa2+-permeable AMPA receptors in mouse olfactory bulb astrocytes
Droste, D., Seifert, G., Seddar, L., Jädtke, O., Steinhäuser, C., & Lohr, C. (2017) · Scientific Reports · doi:10.1038/srep44817 · Cited by 37 · see citing works
A translational model to determine rodent’s age from human foetal age
Ohmura, Y., & Kuniyoshi, Y. (2017) · Scientific Reports · doi:10.1038/s41598-017-17571-z · Cited by 32 · see citing works
Cañizares, M. A., Albors, A. R., Singer, G. A., Suttie, N., Gorkic, M., Felts, P. A., & Storey, K. G. (2019) · Journal of Anatomy · doi:10.1111/joa.13094 · Cited by 29 · see citing works
Electrical maturation of spinal neurons in the human fetus: comparison of ventral and dorsal horn
Tadros, M. A., Lim, R., Hughes, D. I., Brichta, A. M., & Callister, R. (2015) · Journal of Neurophysiology · doi:10.1152/jn.00682.2015 · Cited by 23 · see citing works
Weidenheim, K. M., Epshteyn, I., Rashbaum, W. K., & Lyman, W. D. (1994) · Journal of Neurocytology · doi:10.1007/bf01666524 · Cited by 22 · see citing works
Motor pools organization depends on the combined function of N-cadherin and type II cadherins
Dewitz, C., Duan, X., & Zampieri, N. (2019) · Development · doi:10.1242/dev.180422 · Cited by 17 · see citing works
Morphological and Functional Changes of Roof Plate Cells in Spinal Cord Development
Shinozuka, T., & Takada, S. (2021) · Journal of Developmental Biology · doi:10.3390/jdb9030030 · Cited by 16 · see citing works
A census of cell types in the brain’s motor cortex
Winnubst, J., & Arber, S. (2021) · Nature · doi:10.1038/d41586-021-02493-8 · Cited by 12 · see citing works
Zardadi, S., Rayat, S., Doabsari, M. H., Alishiri, A., Keramatipour, M., Shahri, Z. J., & Morovvati, S. (2021) · BMC Pediatrics · doi:10.1186/s12887-021-02521-6 · Cited by 6 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Human assembloid model of the ascending neural sensory pathway
Kim, J., Imaizumi, K., Jurjuţ, O. F., Kelley, K. W., Wang, D., Thete, M. V., Hudáčová, Z., Amin, N. D., Levy, R. J., Scherrer, G., et al. (2025) · Nature · doi:10.1038/s41586-025-08808-3 · Cited by 144 · see citing works
Self-citationXie, J., Yang, A., Liu, Q., Deng, X., Lv, G., Ou, X., Zheng, S., Situ, M., Yu, Y., Liang, J., et al. (2024) · Cell Proliferation · doi:10.1111/cpr.13697 · Cited by 53 · see citing works
Fan, Y., Wu, X., Han, S., Zhang, Q., Sun, Z., Chen, B., Xue, X., Zhang, H., Chen, Z., Yin, M., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-40513-5 · Cited by 54 · see citing works
Challenges of profiling motor neuron transcriptomes from human spinal cord
Gautier, O., Blum, J. A., Maksymetz, J., Chen, D. C., Schweingruber, C., Mei, I., Hermann, A., Hackos, D. H., Hedlund, E., Ravits, J., et al. (2023) · Neuron · doi:10.1016/j.neuron.2023.10.035 · Cited by 42 · see citing works
Decoding the spatiotemporal regulation of transcription factors during human spinal cord development
Shi, Y., Huang, L., Dong, H., Yang, M., Ding, W., Zhou, X., Lu, T., Liu, Z., Zhou, X., Wang, M., et al. (2024) · Cell Research · doi:10.1038/s41422-023-00897-x · Cited by 33 · see citing works
Spinal Cord Organoids to Study Motor Neuron Development and Disease
Buchner, F., Dokuzluoglu, Z., Graß, T., & Rodríguez‐Muela, N. (2023) · Life · doi:10.3390/life13061254 · Cited by 27 · see citing works
Kussick, E., Johansen, N., Taskin, N., Chowdhury, A., Quinlan, M. A., Fraser, A., Clark, A. G., Wynalda, B., Martinez, R. A., Groce, E. L., et al. (2025) · Cell Reports · doi:10.1016/j.celrep.2025.115730 · Cited by 27 · see citing works
Grass, T., Dokuzluoglu, Z., Büchner, F., Rosignol, I., Thomas, J., Caldarelli, A., Dalinskaya, A., Becker, J., Rost, F., Marass, M., et al. (2024) · Cell Reports Medicine · doi:10.1016/j.xcrm.2024.101659 · Cited by 30 · see citing works
Pietrogrande, G., Shaker, M. R., Stednitz, S. J., Soheilmoghaddam, M., Aguado, J., Morrison, S. D., Zambrano, S., Tabassum, T., Javed, I., Cooper-White, J. J., et al. (2024) · Molecular Psychiatry · doi:10.1038/s41380-024-02732-0 · Cited by 22 · see citing works
Lall, D., Workman, M. J., Sances, S., Ondatje, B. N., Bell, S., Lawless, G. M., Woodbury, A., West, D., Meyer, A. S., Matlock, A. D., et al. (2025) · Cell stem cell · doi:10.1016/j.stem.2025.05.015 · Cited by 24 · see citing works
Human neuron subtype programming via single-cell transcriptome-coupled patterning screens
Lin, H., Janssens, J., Eisinger, B. N., Hornauer, P., Kroell, A.-S. H., Santel, M., Pascual-Garcia, M., Okamoto, R., Karava, K., He, Z., et al. (2025) · Science · doi:10.1126/science.adn6121 · Cited by 19 · see citing works
Zhang, D., Chen, Y., Wei, Y., Chen, H., Wu, Y., Wu, L., Li, J., Ren, Q., Miao, C., Zhu, T., et al. (2024) · eLife · doi:10.7554/elife.92046.2 · Cited by 19 · see citing works
Engineered thoracic spinal cord organoids for transplantation after spinal cord injury
Zhu, Y., Huang, R., Yu, L., Liu, Z., Liu, Y., Fan, W., Lin, G., Wang, Z., He, X., Xu, X., et al. (2025) · Nature Biomedical Engineering · doi:10.1038/s41551-025-01549-8 · Cited by 17 · see citing works
Gliomas: a reflection of temporal gliogenic principles
Sojka, C., & Sloan, S. A. (2024) · Communications Biology · doi:10.1038/s42003-024-05833-2 · Cited by 18 · see citing works
Zhang, D., Chen, Y., Wei, Y., Chen, H., Wu, Y., Wu, L., Li, J., Ren, Q., Miao, C., Zhu, T., et al. (2023) · eLife · doi:10.7554/elife.92046 · Cited by 14 · see citing works
Injury and therapy in a human spinal cord organoid
Takata, N., Li, Z., Metlushko, A., Chen, F., Sather, N. A., Lin, X., Schipma, M. J., Carballo-Molina, O. A., Jamroz, C., Strong, M. E., et al. (2026) · Nature Biomedical Engineering · doi:10.1038/s41551-025-01606-2 · Cited by 10 · see citing works
Tian, C., Ao, Z., Cerneckis, J., Cai, H., Chen, L., Niu, H., Takayama, K., Kim, J., Shi, Y., Gu, M., et al. (2025) · Science Advances · doi:10.1126/sciadv.adu2708 · Cited by 9 · see citing works
Chen, Y., Liao, Y., Wu, Z., Wan, A., Cai, H., Wong, S. S. C., Feng, X., Fan, C., Zhan, D., Hui, C.-C., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-65092-5 · Cited by 9 · see citing works
Dábilla, N., Maya, S., McNinch, C. M., Eddens, T. J., Dolan, P., & Freeman, M. C. (2025) · Frontiers in Microbiology · doi:10.3389/fmicb.2025.1698639 · Cited by 8 · see citing works
Neural stem/progenitor cell transplantation therapy for chronic spinal cord injury
Zhang, J., Zheng, X., Wu, Z., Wang, Y., & Chen, H. (2025) · Journal of Neurorestoratology · doi:10.1016/j.jnrt.2025.100223 · Cited by 7 · see citing works
Spatiotemporal disarray of inflammatory microenvironment following spinal cord injury
Di, J., Lu, Y., Yao, S., Zhang, H., Tian, Z., Xiao, L., Shang, Z., He, L., Pang, M., Yang, Y., et al. (2025) · Neural Regeneration Research · doi:10.4103/nrr.nrr-d-25-00822 · Cited by 8 · see citing works
Glial cells in neuropathic pain
Berta, T., Khoutorsky, A., Xu, J., & Ji, R. (2026) · Physiological Reviews · doi:10.1152/physrev.00034.2025 · Cited by 7 · see citing works
hECA v2.0: an AI-ready ensemble cell atlas of single-cell RNA and ATAC sequencing data
Xi, X., Chen, Y., Wu, X., Hao, M., Li, J., Bian, H., Meng, Q., Li, F., Li, C., Xiao, C., et al. (2025) · Scientific Data · doi:10.1038/s41597-025-06426-2 · Cited by 6 · see citing works
Self-citationEpigenetic regulation in spinal muscular atrophy: emerging areas and future directions
Li, H., Yu, B., Yuan, Y., Chen, N., Wu, J., & Zhang, Z. (2025) · Orphanet Journal of Rare Diseases · doi:10.1186/s13023-025-03857-3 · Cited by 5 · see citing works
Timing mechanisms: insights from comparative neural differentiation systems
Azzi, C., & Rayón, T. (2024) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2024.102197 · Cited by 5 · see citing works
Yang, Y., Chen, B.-R., Ye, X.-C., Ni, L., Zhang, X.-Y., Liu, Y.-Z., Lyu, T., Tian, Y., Fu, Y.-J., & Wang, Y. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114814 · Cited by 5 · see citing works
Revealing the roles of TLR7, a nucleic acid sensor for COVID-19 in pan-cancer
Huang, Z., Gao, Y., Han, Y., Yang, J., Yang, C., Li, S., Zhou, D., Huang, Q., & Yang, J. (2023) · Biosafety and Health · doi:10.1016/j.bsheal.2023.05.004 · Cited by 5 · see citing works
Zheng, X., Liu, Z., He, Z., Xu, J., Wang, Y., Gong, C.-Z., Zhang, R., Zhang, S., Chen, H., & Wang, W. (2023) · iScience · doi:10.1016/j.isci.2023.108306 · Cited by 3 · see citing works
Lou, Z., Post, A., Nagoshi, N., Hong, J., Hejrati, N., Chio, J. C. T., Khazaei, M., & Fehlings, M. G. (2024) · Stem Cells Translational Medicine · doi:10.1093/stcltm/szae090 · Cited by 5 · see citing works
Mueller, S., Kline, C., Franson, A. T., van der Lugt, J., Prados, M. D., Waszak, S. M., Plasschaert, S. L. A., Molinaro, A. M., Koschmann, C. J., & Nazarian, J. (2023) · Neuro-Oncology · doi:10.1093/neuonc/noad181 · Cited by 3 · see citing works
From neural tube to spinal cord: The dynamic journey of the dorsal neuroepithelium
Ventriglia, S., & Kalcheim, C. (2024) · Developmental Biology · doi:10.1016/j.ydbio.2024.04.001 · Cited by 3 · see citing works
Tian, C., Ao, Z., Cerneckis, J., Cai, H., Chen, L., Niu, H., Takayama, K., Kim, J., Shi, Y., Gu, M., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.02.16.638539 · Cited by 3 · see citing works
Innovations in spinal cord cell type heterogeneity across vertebrate evolutionPreprint
Ignatyev, Y., Papadopoulos, S., Soretić, M., Yeung, J., Lin, T., Tanaka, E. M., Peshkin, L., Levine, A. J., Gabitto, M. I., & Sweeney, L. B. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.10.09.680955 · Cited by 3 · see citing works
Ferrer, R. M., Jaspers, Y. R. J., Coveña, N., Breeuwsma, N., Dijkstra, I. M. E., Kempff, J. M., van Klinken, J. B., Wortel, J., van Weering, J. R. T., Engelen, M., et al. (2025) · iScience · doi:10.1016/j.isci.2025.114339 · Cited by 2 · see citing works
Miao, N., Lee, T., Chen, L., Zhang, H., Wang, J. H., Sun, J., Sun, J., Sha, Y., Huang, S., & Sun, T. (2026) · iScience · doi:10.1016/j.isci.2026.115399 · Cited by 3 · see citing works
Defining multipotent intermediate progenitors in cortical development
Kebede, N., & Sloan, S. A. (2026) · Trends in Neurosciences · doi:10.1016/j.tins.2026.03.005 · Cited by 2 · see citing works
Azbukina, N. V., He, Z., Lin, H., Santel, M., Kashanian, B., Maynard, A., Török, T., Okamoto, R., Nikolova, M. T., Seimiya, M., et al. (2026) · Nature Neuroscience · doi:10.1038/s41593-026-02316-x · Cited by 2 · see citing works
Neuron-Astrocyte Interactions: A Human Perspective
Pio, T., Hill, E. J., Kebede, N., Andersen, J., & Sloan, S. A. (2024) · Advances in neurobiology · doi:10.1007/978-3-031-64839-7_4 · Cited by 2 · see citing works
Self-citationSingle-Cell Transcriptomics in Spinal Cord Studies: Progress and Perspectives
Maihemuti, M., Mimi, M. A., Sohag, S. M., & Hasan, M. M. (2025) · BioChem · doi:10.3390/biochem5020016 · Cited by 4 · see citing works
Spatiotemporal dynamics of neuron differentiation and migration in the developing human spinal cord
Yu, Y., Pan, M., Cai, Q., Feng, Z., Cai, B., Lin, K., Cao, S., Lin, L., Lin, L., Ma, Y., et al. (2025) · Journal of genetics and genomics/Journal of Genetics and Genomics · doi:10.1016/j.jgg.2025.08.004 · Cited by 2 · see citing works
Zhang, D., Chen, Y., Wei, Y., Chen, H., Wu, Y., Wu, L., Li, J., Ren, Q., Miao, C., Zhu, T., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.09.26.559582 · Cited by 2 · see citing works
Gupta, S., Heinrichs, E., Rodriguez, C., Friedman, E., Gallardo, S., Demirjie, T., Panosian, T., Phan, K. D., Tahmasian, A., Verdin, Y., et al. (2025) · SSRN Electronic Journal · doi:10.64898/2025.12.22.696129 · Cited by 2 · see citing works
Yu, H., Liu, Y., Xu, F., Fu, Y., Yang, M., Ding, L., Wu, Y., Tang, F., Qiao, J., & Wen, L. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114586 · Cited by 1 · see citing works
Single-nucleus transcriptomics of spinal ependymoma subtypes recognizes intratumoral heterogeneity
Hack, K., Jauch-Speer, S.-L., Kresbach, C., Schoof, M., Thomas, C., & Schüller, U. (2025) · Neuro-Oncology · doi:10.1093/neuonc/noaf210 · Cited by 1 · see citing works
Malka-Gibor, E., Oliver, K. M., Chen, S., Garcia-Diaz, A., Williams, D. J., Henry, J. A., Akcan, B. T., Corneo, B., & de Nooij, J. C. (2026) · Stem Cell Reports · doi:10.1016/j.stemcr.2025.102753 · Cited by 1 · see citing works
Gibbons, G. M., Fuchsberger, T., Abdelgawad, M., Giandomenico, S. L., Szebényi, K., Petrova, V., Wenger, L. M. D., Olschewski, D. N., Chabros, J., Mureşan, L., et al. (2026) · Cell Reports · doi:10.1016/j.celrep.2026.117399 · Cited by 1 · see citing works
Pio, T., Bettaiah, M., Zhao, R., Wariyar, S. S., Mouhi, S., Hill, E. J., Sloan, S. A., Ou, Z., Yu, A. J. R., Adams, C., et al. (2026) · Stem Cell Reports · doi:10.1016/j.stemcr.2026.103114 · Cited by 1 · see citing works
Self-citationIt’s me, hi, I solved the problem, it’s TF-seqFISH
Gautier, O., & Gitler, A. D. (2024) · Cell Research · doi:10.1038/s41422-023-00901-4 · Cited by 1 · see citing works
Zhang, D., Chen, Y., Wei, Y., Chen, H., Wu, Y., Wu, L., Li, J., Ren, Q., Miao, C., Zhu, T., et al. (2023) · eLife · doi:10.7554/elife.92046.1 · Cited by 1 · see citing works
Pietrogrande, G., Shaker, M. R., Stednitz, S. J., Soheilmoghaddam, M., Aguado, J., Morrison, S. D., Zambrano, S., Tabassum, T., Javed, I., Cooper-White, J. J., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.08.29.555421
Single nucleus RNA-sequencing study revealed expansion of Gpnmb+ microglia in aged mouse spinal cordPreprint
Gao, Y., Zhang, Z., Guo, W., Qian, P., & Xie, G. (2023) · Research Square · doi:10.21203/rs.3.rs-3333031/v1
Iwasaki, R., Kohro, Y., & Tsuda, M. (2024) · Molecular Brain · doi:10.1186/s13041-024-01097-3
Synchronous 3D patterning of diverse CNS progenitors generates motor neurons of broad axial identityPreprint
Buchner, F., Dokuzluoglu, Z., Thomas, J. D., Caldarelli, A., Kavali, S., Rost, F., Graß, T., & Rodríguez‐Muela, N. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.12.13.628384
Han, B., Chen, Y., Ouyang, W., Chen, D., Li, J., Liang, W., Zhang, X., Wei, C., Liu, L., Yan, S., et al. (2026) · Scientific Data · doi:10.1038/s41597-026-06882-4
Deng, Z., Zhang, H., Li, X., Feng, Y., Liu, Y., Shang, H., Wang, L. M., Zhou, X., & Wei, X. (2026) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-026-01711-z
Blauth, O., Sławińska, U., & Zawadzka, M. (2026) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2026.1819322
Using human 3D organoid models to gain mechanistic insight in motor neuron diseases
Frizzi, B., Correia, A. M. B., Faravelli, I., Bosch, L. V. D., & Corti, S. P. (2026) · Nature reviews. Neuroscience · doi:10.1038/s41583-026-01057-x
Shu, X., Zhang, J., & Qin, Z. (2026) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2026.1857896
Kong, S. K., Shin, A., Song, M., Lee, J., Ju, A., Choi, K., Koh, I. G., An, J., Choi, N., Yoo, Y., et al. (2026) · SSRN Electronic Journal · doi:10.2139/ssrn.7347056
- Authors
- Andersen, J., Thom, N., Shadrach, J. L., Chen, X., Onesto, M. M., Amin, N. D., Yoon, S.-J., Li, L., Greenleaf, W. J., Müller, F., Pașca, A. M., Kaltschmidt, J. A., & Pașca, S. P.
- Affiliations
- Emory University (US)
- Stanford Medicine (US)
- Stanford University (US)
- Saarland University (DE)
- Corresponding author
- Pașca, Sergiu P.
- ORCID
- Venue
- Nature Neuroscience
- Published
- 2023-04-24
- Volume
- 26
- Issue
- 5
- Pages
- 902-914
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- OpenAlex
- W4366823419
- Cited by
- 61
- References
- 78
- Citations by year
- 2026: 14 · 2025: 19 · 2024: 15 · 2023: 13
- FWCI
- 5.44
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Single-cell and spatial transcriptomics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- single-cell transcriptomics, midgestation, motor neurons, astrocytes, glial heterogeneity, dorsal-ventral axis, rostrocaudal axis, cell type diversity, disease-related genes, motor control
- MeSH terms
- Humans, Motor Neurons, Neuroglia, Spinal Cord, Transcriptome, Gray Matter
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review