Abstract
The cerebral cortex is a cellularly complex structure comprising a rich diversity of neuronal and glial cell types. Cortical neurons can be broadly categorized into two classes—excitatory neurons that use the neurotransmitter glutamate, and inhibitory interneurons that use γ-aminobutyric acid (GABA). Previous developmental studies in rodents have led to a prevailing model in which excitatory neurons are born from progenitors located in the cortex, whereas cortical interneurons are born from a separate population of progenitors located outside the developing cortex in the ganglionic eminences1,2,3,4,5. However, the developmental potential of human cortical progenitors has not been thoroughly explored. Here we show that, in addition to excitatory neurons and glia, human cortical progenitors are also capable of producing GABAergic neurons with the transcriptional characteristics and morphologies of cortical interneurons. By developing a cellular barcoding tool called ‘single-cell-RNA-sequencing-compatible tracer for identifying clonal relationships’ (STICR), we were able to carry out clonal lineage tracing of 1,912 primary human cortical progenitors from six specimens, and to capture both the transcriptional identities and the clonal relationships of their progeny. A subpopulation of cortically born GABAergic neurons was transcriptionally similar to cortical interneurons born from the caudal ganglionic eminence, and these cells were frequently related to excitatory neurons and glia. Our results show that individual human cortical progenitors can generate both excitatory neurons and cortical interneurons, providing a new framework for understanding the origins of neuronal diversity in the human cortex.
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Data availability
scRNA-seq transcriptomic data and STICR barcode data are available at the database of Genotypes and Phenotypes (dbGAP; https://www.ncbi.nlm.nih.gov/gap/) under accession number phs002624.v1.p1; and at the Gene Expression Omnibus (GEO; https://www.ncbi.nlm.nih.gov/geo/) under accession number GSE187875. An interactive browser of single-cell data can be found at the University of California, Santa Cruz (UCSC) cell browser49( https://human-cortical-lineage.cells.ucsc.edu). Publicly available reference genomes hg38 and mm10 were used for analysis. Source data are provided with this paper.
Code availability
Custom codes used in this study are available at the following GitHub repository: https://github.com/NOW-Lab/STICR.
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Acknowledgements
We thank A. Bhaduri for discussions regarding scRNA-seq analysis; B. Rabe and C. Cepko for discussions regarding viral vectors and sharing of reagents; C. Cadwell and M. Paredes for discussions regarding interneuron morphology; J. Rubenstein and R. Andersen for reading the manuscript; and M. Speir and B. Wick for data wrangling at the UCSC single-cell browser. This study was supported by the Psychiatric Cell Map Initiative Convergence Neuroscience award U01MH115747; an Innovation Award from the Broad Foundation (to T.J.N.); a New Frontiers Research Award from the Sandler Program for Breakthrough Biomedical Research (PBBR) (to T.J.N.); a National Science Foundation (NSF) Graduate Research Fellowship Program (GRFP) award (to D.E.A.); an Autism Speaks Predoctoral Fellowship (11874 to R.S.Z.); NIH K08 NS116161 and UCSF Physician Scientist Scholars Program to EEC; and gifts from Schmidt Futures and the William K. Bowes Jr Foundation (to T.J.N.). Work in the Alvarez-Buylla laboratory is supported by National Institutes of Health (NIH) grants R01NS028478 and R01EY025174, and a gift from the John G. Bowes Research Fund. A.A.-B. is the Heather and Melanie Muss Endowed Chair and Professor of Neurological Surgery at UCSF.
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Authors and Affiliations
Contributions
R.N.D conceived of the project, designed and generated the STICR barcode library, designed and conducted experiments, analysed the data, and wrote the manuscript. D.E.A. helped to design experiments, conducted experiments, analysed data, and helped to write the manuscript. M.G.K helped to design experiments, conducted experiments and helped to write the manuscript. W.R.M.L carried out xenograft transplantations. R.S.Z. helped to construct the STICR library. E.E.C. carried out PTPRZ1 FACS. A.A.-B. helped to supervise the research. T.J.N conceived of the project, helped to design experiments, assisted in the interpretation of data, and helped to write the manuscript.
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A.A.-B. is co-founder and on the Scientific Advisory Board of Neurona Therapeutics.
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Extended data figures and tables
Extended Data Fig. 1 Validation of the STICR barcode design.
a, Histogram showing pairwise hamming distances between every sequence in each STICR fragment pool. b, Barcode diversity extrapolations derived from sequencing a representative STICR plasmid or lentiviral library. Mean ± 95% confidence range for each library is shown. c, Simulated barcode collision frequencies (mean ± s.d.) for a range of starting cell numbers, based on the barcode diversity estimated in b. Barcode sampling was performed with replacement using measured proportions of barcodes within the representative plasmid and lentiviral libraries depicted in b. Each simulation was performed 20,000 times. Most error bars (depicting standard deviations) are not visible as they are smaller than the dots (depicting mean values). d, The ‘barnyard’ species-mixing experiment. e, Plot depicting species-specific transcript counts from barnyard experiment. Each dot depicts a single cell and the dot colour indicates whether the cell was determined to be a 3T3 cell (mouse), cortex cell (human), or mixed droplet (multiplet). f, Violin plots depicting the number of unique STICR barcode molecules recovered from droplets identified as either mouse, human, or multiplet. ND, not detected.
Extended Data Fig. 2 Cluster analysis of in vitro STICR data sets.
a, UMAP plots of each individual biological sample highlighted. b, Top marker-gene expression for each cluster. The size of each dot corresponds to the proportion of cells in the cluster that express the gene, while the colour of the dot corresponds to the average expression level per cluster. c, d, Heatmap depicting pairwise transcriptional cluster correlation of in vitro cultured cells with itself (c) and the 2017 Nowakowski scRNA-seq atlas (d)14. The principal cell-type designation is depicted next to each column and row. The dendrogram depicts hierarchical clustering distance.
Extended Data Fig. 3 Transcriptional analysis of in vitro STICR data sets.
a–f, Feature plots depicting expression of genes corresponding to cell cycle (a), glia (b), oligodendroglia (c), excitatory neurons (d), interneurons (e), and regional markers (f). g, Bar plot depicting the proportion of cells within each cluster with a recovered STICR barcode. h, Heatmap depicting the percentage of STICR barcodes shared between biological samples. GW15 (Rep1) and all GW18 samples were labelled with the same viral stock, while GW15 (Rep2) was labelled with a different stock (see Methods). i, Stacked barplot depicting relative proportions of principal cell types within each sample, restricted to cells that are members of multicellular clones.
Extended Data Fig. 4 Clonal analysis of cortical clones containing excitatory neurons.
a, Histogram of excitatory neuron (EN) counts within each multicellular cortical clone. Left, clone sizes from 1–25 cells in single-cell bins. Right, clone sizes of more than 25 cells in the indicated bin sizes. b, Box-and-whisker plot depicting the proportion of EN cells within individual multicellular clones for each biological sample. Maxima and minima of boxes depict third and first quartiles, while box centres depict medians. Whiskers depict 1.5× the interquartile distance. Individual clone values are shown as dots. The number of clones is listed below each sample group. c, Ternary plots depicting the relative proportions of inhibitory neurons, excitatory neurons and all other cell types (‘Other’) within individual clones. d, e, Immunohistochemistry of in vitro cultures derived from GW15 germinal zone cells labelled with STICR. d, Low-magnification image to show distribution; scale bar, 25 μm. e, High-magnification image showing a cluster of ENs; scale bar, 250 μm.
Extended Data Fig. 5 Clonal and transcriptional analysis of inhibitory neurons and DLX2+ IPCs in vitro.
a, UMAP embedding and Leiden subclustering of GABAergic inhibitory neuron (IN) trajectory cells. b, Feature plots depicting expression of MKI67, STMN2, CENPF and ERBB4. c, Heatmap depicting pairwise transcriptional cluster correlation of this data set with itself. d, Stacked barplot depicting relative proportion of multicellular clones from each sample that comprise each IN trajectory. e, Stacked barplot depicting the relative proportions of different IN trajectory cells within multicellular clones of each sample. f, Feature plots depicting MGE-derived cells (red) and expression of NKX2-1, LHX6, ACKR3, MAF and PDE1A. The enlarged insets below show IN.1 trajectory cells. g, Heat plot depicting differential expression of IN.2 and IN.3 marker genes in the developing human cortex, olfactory bulb/rostral migratory stream and basal ganglia. Data are derived from the Allen BrainSpan Laser Capture Microdissection database. Dendrograms reflect hierarchical clustering of genes and samples while colours represent quantile-normalized z-scores. h, Paired violin plots and in situ hybridization (ISH) images of P60 mouse brains from the Allen Brain Atlas for select genes. The log2 fold difference between IN.2 (olfactory-bulb-like) and IN.3 (cortical-interneuron-like) cells is depicted above each violin plot. i, Stacked barplots depicting relative proportions of IN.1, IN.2, IN.3, EN and glia trajectory cells within multicellular clones. The number of clones is listed below each sample. j, Venn diagram depicting the number of EN-containing multicellular cortical clones that also contain IN.2 and/or IN.3 cells.
Extended Data Fig. 6 Clonal and transcriptional analysis of excitatory neurons and EOMES+ IPCs in vitro.
a, UMAP embedding and Leiden subclustering of excitatory neuron (EN) trajectory cells. b, c, Heatmap depicting pairwise transcriptional cluster correlation of subclustered EN trajectory cells with self (b) and with the 2017 Nowakowski developing human brain scRNA-seq atlas (c)14. d, Feature plots depicting the expression of genes corresponding to labelled subclustered EN trajectory subtypes. e, Stacked barplot depicting relative proportions of EN subtypes within EN trajectory cells of multicellular clones. f, Venn diagram depicting the number of multicellular cortical clones containing deep-like ENs, upper-like ENs, and IN.3 cells.
Extended Data Fig. 7 Characterization of human cortical progenitor xenografts at six weeks.
a, b, Representative images of transplanted human cortical cells analysed by IHC for principal cell-type markers six weeks after transplantation. EGFP expression from STICR is in green, with NEUROD2 or GABA expression in red. Scale bars: a, 50 μm; b,10 μm. c, Barplot depicting the proportion (mean ± s.d.) of transplanted cells expressing principal cell-type markers as assessed by IHC. n = 7 sections derived from 6 xenografted mice, 3 of which were transplanted with donor cells from GW15 Rep1 and 3 with cells from GW15 Rep2. d, Top marker-gene expression for each cluster from xenografted cells. Sizes of dots correspond to the proportion of cells in the cluster expressing the gene, while dot colours correspond to the average expression level per cluster. e, UMAP embedding of xenografted cells and feature plots depicting expression of NEUROD2, EOMES, DLX2, MKI67 and GFAP. f, Heatmap depicting pairwise transcriptional cluster correlation of subclustered excitatory neuron (EN) trajectory cells with the 2017 Nowakowski developing human cortex scRNA-seq atlas14. g, Comparison of principal cell-type quantification (mean) in transplanted cells by analysis method (IHC versus scRNA-seq) and biological replicate.
Extended Data Fig. 8 Transcriptional analysis of excitatory and inhibitory neurons from xenografts.
a, UMAP embedding and Leiden subclustering of inhibitory neuron (IN) trajectory cells from xenografts. b, Feature plots depicting expression of CENPF, MKI67, ERBB4, NR2F1, NFIX, SP8, SCGN and KLHL35. c, Heatmap depicting pairwise transcriptional cluster correlation of subclustered xenograft IN and DXL2+ IPC trajectory cells with the 2017 Nowakowski developing human cortex scRNA-seq atlas14. d, UMAP embedding depicting cells in multicellular clones from xenograft IN subclusters 1 (salmon) and 2 (lime), integrated with an in vitro cultured STICR IN subset. e, UMAP embedding depicting individual interneuron trajectory cells from multicellular clones from xenograft experiments integrated with interneuron trajectory cells from in vitro cultures, split by biological replicate. Members of such clones are highlighted in red. f, UMAP embedding and Leiden subclustering of excitatory neuron (EN) and EOMES+ IPC trajectory cells from xenografts. g, Heatmap depicting pairwise transcriptional cluster correlation of subclustered xenograft EN and EOMES+ IPC trajectory cells with the 2017 Nowakowski developing human cortex scRNA-seq atlas14.
Extended Data Fig. 9 Analysis of PTPRZ1-sorted STICR+ cells in the cortex, subventricular zone, rostral migratory stream and olfactory bulb at 12 weeks.
a, Representative FACS plots depicting isolation of PTPRZ1+ cells from the cortical germinal zone. b, Representative image of transplanted human cortical cells in the cortex of a 12-week-old host mouse. EGFP expression from STICR is in green, with DAPI in blue. Scale bar, 50 μm. CC, corpus callosum. c, Representative images of PTPRZ1-sorted, STICR-labelled cells in the dorsolateral corner of the lateral ventricle of a 12-week-old host mouse analysed by IHC. EGFP from STICR is in green, DCX in red, and DAPI in blue. Scale bar, 100 μm. d, High-magnification inset of the region boxed in c. Scale bar, 10 μm. SVZ, subventricular zone. e, Representative images of PTPRZ1-sorted, STICR-labelled cells in the rostral forebrain, analysed by IHC. The rostral migratory stream (RMS) is outlined by the white box labelled f. GFP expression is in green, DCX expression in red, and DAPI in blue. Scale bar, 100 μm. f, High-magnification insets of the RMS depicted in the white box in e. Scale bar, 10 μm. The cell outlined by the white box is magnified below. g, Representative images of PTPRZ1-sorted, STICR-labelled cells that migrated from the transplantation site in the cortex to the olfactory bulb, analysed by IHC. EGFP expression is in green and DAPI in magenta. GCL, granule cell layer; MCL, mitral cell layer. Scale bar, 10 μm.
Extended Data Fig. 10 Immunohistochemistry of STICR-labelled cortical INs from xenografts at 12 weeks.
Representative images of STICR-labelled GABA+ cells throughout the cortical plate, analysed by IHC. EGFP from STICR is in green, GABA in red, and DAPI in blue. Same cells from Fig. 4d. Arrows point to STICR-labelled GABA+ cells. Scale bar, 10 μm.
Supplementary information
Supplemental Table 1
Table describing clone composition from in vitro culture experiments. Columns: Clone Barcode (“Full_VBC”), clone size (“Total Cells”), sample of origin (“Library”), as well as the number of cells within that clone assigned to principal cell types (“EN”, “IN”, “glia”, “DLX.IPC”, “EOMES.IPC”), cluster 34 (“Unknown”), the excitatory neuron subclustering cell types (“Upper”, “Deep”, “EN.Newborn”, “EN.other”), and the inhibitory neuron/DLX.IPC subclustering cell types (“DLX2.IPC”, “IN.early”, “IN.1”,”IN.2”,”IN.3”). Principal cell type designations reflect subclustering results.
Supplemental Table 2
Table describing clone composition from xenograft experiments (GW15 Reps 3, 4, and 5). Columns: Clone Barcode (“Full_VBC”), clone size (“Total Cells”), sample of origin (“Library”), as well as the number of cells within that clone assigned to principal cell types (“EN”, “IN”, “glia”, “DLX.IPC”, “EOMES.IPC”), “microglia”, “Undetermined” and the inhibitory neuron/DLX.IPC subclustering cell types (“DLX2.IPC”, “IN.early”, “IN.2”,”IN.3”). Principal cell type designations reflect subclustering results.
Supplemental Table 3
Table of STICR ssDNA oligomers used to create barcode fragment sequences.
Supplemental Table 4
Table of primers used to amplify STICR barcodes from plasmid and lentiviral libraries as well as from 10X genomics cDNA libraries.
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Delgado, R.N., Allen, D.E., Keefe, M.G. et al. Individual human cortical progenitors can produce excitatory and inhibitory neurons. Nature 601, 397–403 (2022). https://doi.org/10.1038/s41586-021-04230-7
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DOI: https://doi.org/10.1038/s41586-021-04230-7
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