Molecular diversity of midbrain development in mouse, human, and stem cells
Open accessAbstract
Understanding human embryonic ventral midbrain is of major interest for Parkinson's disease. However, the cell types, their gene expression dynamics, and their relationship to commonly used rodent models remain to be defined. We performed single-cell RNA sequencing to examine ventral midbrain development in human and mouse. We found 25 molecularly defined human cell types, including five subtypes of radial glia-like cells and four progenitors. In the mouse, two mature fetal dopaminergic neuron subtypes diversified into five adult classes during postnatal development. Cell types and gene expression were generally conserved across species, but with clear differences in cell proliferation, developmental timing, and dopaminergic neuron development. Additionally, we developed a method to quantitatively assess the fidelity of dopaminergic neurons derived from human pluripotent stem cells, at a single-cell level. Thus, our study provides insight into the molecular programs controlling human midbrain development and provides a foundation for the development of cell replacement therapies.
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Molecular heterogeneity within the murine dopaminergic system has been investigated by at least six independent groups, all attempting to classify dopamine neurons based on gene expression.
“Molecular heterogeneity within the murine DAergic system has been investigated by at least six independent groups, all attempting to classify DA neurons based on gene expression [13–18].”
From Classification of midbrain dopamine neurons using single-cell gene expression profiling approaches (2020) · cites this paper as [14]
The single-cell classification studies identified partially overlapping dopamine neuron subtypes, some of which were located in a manner agnostic to traditional anatomical boundaries.
“Although these studies differed significantly in their experimental parameters and analysis methods, they identified partially overlapping subtypes, some of which were located in a manner agnostic to traditional anatomical boundaries (SN, VTA, & RR).”
From Classification of midbrain dopamine neurons using single-cell gene expression profiling approaches (2020) · cites this paper as [14]
The Aldh1a1+, Sox6+ dopamine neuron subtype also displays Aldh1a7 and Ndnf mRNA expression.
“These cells also display Aldh1a7 [14,17] and Ndnf [13,14] mRNA expression.”
From Classification of midbrain dopamine neurons using single-cell gene expression profiling approaches (2020) · cites this paper as [14]
Aldh1a1 and Sox6 mRNAs are defining markers for a dopamine neuron subtype located in the ventral substantia nigra pars compacta.
“Aldh1a1 and Sox6 mRNAs are the defining markers for this DA neuron subtype, a population overtly represented in two studies: DA1A in [13] and DA-SNC in [14].”
From Classification of midbrain dopamine neurons using single-cell gene expression profiling approaches (2020) · cites this paper as [14]
Otx2+, Aldh1a1+ dopamine neurons are located in the ventromedial ventral tegmental area.
“Otx2+, Aldh1a1+ DA neurons in the ventromedial VTA”
From Classification of midbrain dopamine neurons using single-cell gene expression profiling approaches (2020) · cites this paper as [14]
A substantial SOX6+ ALDH1A1- population is located more dorsal to ALDH1A1+ neurons in the substantia nigra pars compacta, the parabrachial pigmented region of the ventral tegmental area, and the retrorubral area.
“In immunolabeling studies, there is a substantial SOX6+ population that is ALDH1A1- [13,14,26]; these cells are located more dorsal to the ALDH1A1+ neurons in the SNc, the parabrachial pigmented (PBP) region of the VTA and the RR.”
From Classification of midbrain dopamine neurons using single-cell gene expression profiling approaches (2020) · cites this paper as [14]
Vip+ dopamine neurons have an mRNA signature of Vip+, Gipr+, Calb1+, Sox6-, and Aldh1a1-.
“Based on the concordance of other genes co-expressed in Vip+ neurons [13–16], we developed the following mRNA signature for Vip neurons: Vip+ [13–16], Gipr+ [15], Calb1+ [13,14], Sox6- [13,14], Aldh1a1- [13,14].”
From Classification of midbrain dopamine neurons using single-cell gene expression profiling approaches (2020) · cites this paper as [14]
A dopamine subtype distinguished by Vgat mRNA expression is located mostly in the ventral tegmental area.
“Vgat+ DA subtype is located mostly in the VTA”
From Classification of midbrain dopamine neurons using single-cell gene expression profiling approaches (2020) · cites this paper as [14]
Sox6+, Aldh1a1- dopamine neurons co-express high levels of Ndnf, Igf1, and Sncg, and some also express Calb1, Lypd1, Tacr3, and Cyp26b1 mRNAs.
“These cells also co-express high levels of many of the mRNAs aforementioned in the previous population (Ndnf, Igf1 and Sncg), but in contrast, some of these neurons also express Calb1 [13,14], Lypd1 [14], Tacr3 [13,18], and Cyp26b1 [18] mRNAs.”
From Classification of midbrain dopamine neurons using single-cell gene expression profiling approaches (2020) · cites this paper as [14]
Sox6+, Aldh1a1- dopamine neurons are located in the substantia nigra pars compacta, the parabrachial ventral tegmental area, and the retrorubral area.
“Sox6+, Aldh1a1- DA neurons are located in the SNc, parabrachial VTA, and RR”
From Classification of midbrain dopamine neurons using single-cell gene expression profiling approaches (2020) · cites this paper as [14]
Vgat+ dopamine neurons are enriched for Vgat, Calb1, Crhbp, Gad2, and Wnt7b mRNAs.
“This group of cells is enriched for Vgat [13–15,18], Calb1 [13,14], Crhbp [15,18], Gad2 [15,18] and Wnt7b [15,18] mRNAs.”
From Classification of midbrain dopamine neurons using single-cell gene expression profiling approaches (2020) · cites this paper as [14]
Vip+ dopamine neurons are the most caudally located population, found in the periaqueductal gray and dorsal raphe, where they account for about 49% of dopamine neurons, but are sparser in the ventral tegmental area.
“Vip+ DA neurons are the most caudally located population”
From Classification of midbrain dopamine neurons using single-cell gene expression profiling approaches (2020) · cites this paper as [14]
Sox6+, Aldh1a1- dopamine neurons lack Aldh1a1, Anxa1, and Aldh1a7 expression.
“In addition to lacking Aldh1a1 mRNA, they also do not express Anxa1 [14,17,18] and Aldh1a7 [14,17,18].”
From Classification of midbrain dopamine neurons using single-cell gene expression profiling approaches (2020) · cites this paper as [14]
In mouse embryos from E11.5 to E18.5, La Manno et al. identified an immature DA neuron type that expresses Th and other key DA markers.
“identified three types of embryonic DA neurons (E11.5-E18.5) in the mouse: 1) an immature type expressing Th and other key markers of DA neurons”
From Classification of midbrain dopamine neurons using single-cell gene expression profiling approaches (2020) · cites this paper as [14]
La Manno et al. identified a third embryonic DA neuron type whose signature resembled the mature type but additionally included Aldh1a1 and Lmo3.
“3) neurons with a similar signature but also expressing Aldh1a1 and Lmo3”
From Classification of midbrain dopamine neurons using single-cell gene expression profiling approaches (2020) · cites this paper as [14]
La Manno et al. identified a more mature embryonic DA neuron type that expresses both Th and Dat.
“2) a more mature neuron type expressing both Th and Dat”
From Classification of midbrain dopamine neurons using single-cell gene expression profiling approaches (2020) · cites this paper as [14]
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Single-Cell RNA Sequencing: Unraveling the Brain One Cell at a Time
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- Authors
- La Manno, G., Gyllborg, D., Codeluppi, S., Nishimura, K., Salto, C., Zeisel, A., Borm, L. E., Stott, S. R. W., Toledo, E. M., Villaescusa, J. C., Lönnerberg, P., Ryge, J., Barker, R. A., Arenas, E., & Linnarsson, S.
- Affiliations
- Karolinska Institutet (SE)
- Science for Life Laboratory (SE)
- University of Cambridge (GB)
- Karolinska University Hospital (SE)
- École Polytechnique Fédérale de Lausanne (CH)
- Corresponding author
- Arenas, Ernest
- Linnarsson, Sten
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2016-10
- Volume
- 167
- Issue
- 2
- Pages
- 566-580.e19
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC5055122
- OpenAlex
- W2528543174
- Cited by
- 835
- References
- 71
- Citations by year
- 2026: 60 · 2025: 81 · 2024: 84 · 2023: 87 · 2022: 100 · 2021: 103 · 2020: 111 · 2019: 87 · 2018: 72 · 2017: 44 · 2016: 3
- FWCI
- 35.87
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Cell (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion)
- Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion, cc-by-nc-nd)
- Lund University Publications (Lund University) (submittedVersion)
- Apollo (University of Cambridge) (submittedVersion, cc-by)
- Apollo (cc-by)
- Funders
- Medical Research Council (MC_PC_12009)
- 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 › Pluripotent Stem Cells Research
- Keywords
- Parkinson's disease, dopaminergic neurons, radial glia-like cells, neural progenitor cells, cell type diversity, species conservation, postnatal development, human pluripotent stem cell-derived neurons, cell replacement therapy, single-cell transcriptomics
- MeSH terms
- Cellular Reprogramming Techniques, Machine Learning, Animals, Cell Line, Humans, Mesencephalon, Neuroglia, Sequence Analysis, RNA, Pluripotent Stem Cells, Mice, Neurogenesis, Neural Stem Cells, Single-Cell Analysis, Dopaminergic Neurons
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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.
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