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A molecular atlas of cell types and zonation in the brain vasculature
Open accessAbstract
Cerebrovascular disease is the third most common cause of death in developed countries, but our understanding of the cells that compose the cerebral vasculature is limited. Here, using vascular single-cell transcriptomics, we provide molecular definitions for the principal types of blood vascular and vessel-associated cells in the adult mouse brain. We uncover the transcriptional basis of the gradual phenotypic change (zonation) along the arteriovenous axis and reveal unexpected cell type differences: a seamless continuum for endothelial cells versus a punctuated continuum for mural cells. We also provide insight into pericyte organotypicity and define a population of perivascular fibroblast-like cells that are present on all vessel types except capillaries. Our work illustrates the power of single-cell transcriptomics to decode the higher organizational principles of a tissue and may provide the initial chapter in a molecular encyclopaedia of the mammalian vasculature.
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In the citing paper
“many of which were well documented61–66.”
From A high-resolution transcriptomic and spatial atlas of cell types in the whole mouse brain (2023) · cites this paper as [64]
In the citing paper
“We identified endothelial ICs (Figure 2E) with strong contributions from genes with arterial (IC 5 and 20) and veinous (IC 3 and 12) expression, suggesting heterogeneity related to vessel type”
From Molecular diversity and specializations among the cells of the adult mouse brain (2018) · cites this paper as Vanlandewijck et al., 2018
In the citing paper
“These genes (e.g. Tm4sf1 and Slc38a5) showed continuous, reciprocal expression (Data S4G), consistent with the smooth molecular transitions described for endothelial cells associated with arteries or veins”
From Molecular diversity and specializations among the cells of the adult mouse brain (2018) · cites this paper as Vanlandewijck et al., 2018
In the citing paper
“IC 19 represented this difference in a graded rather than categorical way, as Rgs5/Acta2 expression and IC cell scores were continuously, rather than bimodally, distributed across these cells”
From Molecular diversity and specializations among the cells of the adult mouse brain (2018) · cites this paper as Vanlandewijck et al., 2018
In the citing paper
“Among SMA cells, Acta2 expression correlates with a veinous versus arterial distribution”
From Molecular diversity and specializations among the cells of the adult mouse brain (2018) · cites this paper as Vanlandewijck et al., 2018
In the citing paper
“A single IC (IC 13) appeared to encode this distinction, with pericyte marker Vtn as the strongest loading gene”
From Molecular diversity and specializations among the cells of the adult mouse brain (2018) · cites this paper as Vanlandewijck et al., 2018
In the citing paper
“Like Vanlandewijck et al., we observed (Figure 5) distinct endothelial cell types carrying known arterial (e.g., Bmx; VECA) and venous (Slc38a5; VECV) markers, as well as capillary endothelial cells (VECC) expressing Meox1.”
From Molecular Architecture of the Mouse Nervous System (2018) · cites this paper as Vanlandewijck et al., 2018
In the citing paper
“Vanlandewijck et al. described two brain fibroblast-like cell types expressing fibril-forming collagens (e.g., Col1a1, Col1a2), collagen fiber crosslinking proteins (Lum, Dcn), and the platelet-derived growth factor receptor alpha, Pdgfra, which was interposed between astrocyte endfeet and vascular endothelial cells.”
From Molecular Architecture of the Mouse Nervous System (2018) · cites this paper as Vanlandewijck et al., 2018
In the citing paper
“In vivo, αSMA and calponin expression are restricted to mural cells along brain arterioles and arteries [38], however, these markers are often upregulated during culture [39], complicating identification of pericytes.”
From Role of iPSC-derived pericytes on barrier function of iPSC-derived brain microvascular endothelial cells in 2D and 3D (2019) · cites this paper as [38]
In the citing paper
“APOE in the brain is primarily synthesized by astrocytes and microglia, as indicated by a recent single cell RNA-seq study in the mouse (610).”
From Blood-Brain Barrier: From Physiology to Disease and Back (2019) · cites this paper as [610]
In the citing paper
“Pericytes, SMCs, and endothelial cells express thousands of transcripts encoding different transporters, receptors, active efflux pumps, ion channels, and regulatory molecules (28, 72, 86, 129, 242, 358, 359, 610, 675, 678), whose expression pattern varies by zonation along the arteriocapillary-venous axis and cell type (610).”
From Blood-Brain Barrier: From Physiology to Disease and Back (2019) · cites this paper as [610]
In the citing paper
“In contrast to the BBB endothelium's gradual phenotypic change along the arteriovenous axis, mural cells formed two distinct groups comprising pericyte and venous SMCs, and arterial and arteriole SMCs (610).”
From Blood-Brain Barrier: From Physiology to Disease and Back (2019) · cites this paper as [610]
In the citing paper
“Briefly, this study is the first to report that at the BBB endothelium transcription factors predominated at arteries and arterioles, transporters predominated capillaries and veins, and ribosomal proteins indicative of protein synthesis were spread along the arteriovenous axis (610), yielding important insights to biological functions and endothelial specialization along the brain vasculature”
From Blood-Brain Barrier: From Physiology to Disease and Back (2019) · cites this paper as [610]
In the citing paper
“According to a transcriptomic analysis of cells in the vasculature, Plcg2 seems to be expressed in certain subtypes of endothelial cells, although at lower level than compared to microglia (http://betsholtzlab.org/VascularSingleCells/database.html [43]).”
From Alzheimer’s disease phospholipase C-gamma-2 (PLCG2) protective variant is a functional hypermorph (2019) · cites this paper as [43]
In the citing paper
“we used an siRNA sequence targeting Ppib because this gene is abundantly and ubiquitously expressed across CNS cell types [27].”
From Elucidating brain transport pathways and cell type-dependent gene silencing of a durable lipid–siRNA conjugate administered into cerebrospinal fluid (2025) · cites this paper as [27]
In the citing paper
“Here, we used an siRNA sequence targeting Ppib because this gene is abundantly and ubiquitously expressed across CNS cell types.34”
From Lipid-siRNA conjugate accesses a perivascular transport mechanism and achieves widespread and durable knockdown in the central nervous system (2024) · cites this paper as [34]
In the citing paper
“WAVE2 is expressed at high levels in microglia and vascular endothelial cells14,15.”
From The WAVE complex in developmental and adulthood brain disorders (2025) · cites this paper as [14]
In the citing paper
“In addition to astrocytes and microglia, other cell types in the brain have been reported to produce ApoE under different conditions. These cells include oligodendrocytes, pericytes, vascular smooth muscle cells, perivascular fibroblasts, and perivascular macrophages [107–109].”
From ApoE lipoproteins in the central nervous system under homeostasis and role in Alzheimer’s disease and related disorders (2026) · cites this paper as [108]
In the citing paper
“PDGFRβ expression in pericytes is noticeably higher than in SMCs18,25,26.”
From Blood–brain barrier breakdown is an early biomarker of human cognitive dysfunction (2019) · cites this paper as [25]
In the citing paper
“Based on marker gene enrichment (Table S1), Endo.1 may correspond to endothelial capillary cells, Endo.2 to venous endothelial cells, and Endo.3 to arterial endothelial cells (Vanlandewijck et al., 2018).”
From Single-Cell Analysis of Regional Differences in Adult V-SVZ Neural Stem Cell Lineages (2019) · cites this paper as Vanlandewijck et al., 2018
In the citing paper
“We spatially mapped the developing arterio-venous zonation in the embryonic LV ChP in whole explants by combining the pan-endothelial marker PECAM1 with markers for arteries (Acta2+, Vwf+) and veins (Acta2−, Vwf+) (Vanlandewijck et al., 2018).”
From A cellular and spatial map of the choroid plexus across brain ventricles and ages (2021) · cites this paper as Vanlandewijck et al., 2018
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“BECs express major histocompatibility complex class I (MHC I) proteins, a key group of immune system receptors 14,40 .”
InfluentialDLL1/NOTCH1 signaling pathway maintain angiogenesis in meniscus development and degeneration
Liu, F., Sun, H. X., Deng, L., et al. (2024) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2024.106589 · Cited by 1
Modern view on the role of pericytes in the microcirculation
Михайлов, П. В., Муравьев, А. В., Tikhomirova, I. A., & Osetrov, I. A. (2024) · Regional blood circulation and microcirculation · doi:10.24884/1682-6655-2024-23-2-4-14 · Cited by 2
Immunology of cell and gene therapy approaches for neurologic diseases
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Species-specific blood–brain barrier permeability in amphibians
Antesberger, S., Stiening, B., Forsthofer, M., Joven, A., Eroğlu, E., Huber, J., Heß, M., Straka, H., & Sánchez-González, R. (2025) · BMC Biology · doi:10.1186/s12915-025-02145-7 · Cited by 1
“Despite the apparent morphological homogeneity, different subpopulations of ECs might allow regionally different regulatory schemes of the BBB [14].”
Voluntary locomotion induces an early and remote hemodynamic decrease in the large cerebral veins
Eyre, B., Shaw, K., Francis, S., Howarth, C., & Berwick, J. (2025) · Neurophotonics · doi:10.1117/1.nph.12.s1.s14609 · Cited by 1
“…et al. 38 reported the observation of pulsatility within small cerebral veins, and veins are thought to play a role in the exchange of nutrients, 39,40 the regulation of immune cell infiltration, 41 and clearance pathways, with research suggesting that solutes empty along the venous circulation.”
Pericytes under pressure: TRPC3 channels as gatekeepers of capillary flow
Earley, S. (2025) · Science Signaling · doi:10.1126/scisignal.adw7185 · Cited by 1
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“Neurosphere markers [49–53], chemokine receptor genes [54–56], and pericyte markers [57, 58] were chosen from a selection of prior studies.”
Koh, Y., Noterman, M. F., Bangalore, A., Kandjoze, U. P., Bud, Z., Noel, K. L., Lee, H., Franke, K., Cintrón-Pérez, C. J., Rajadhyaksha, A. M., et al. (2025) · Channels · doi:10.1080/19336950.2025.2523788 · Cited by 1
Research Progress on MET, Tip Link, and Stereocilia Complex with Special Reference to Zebrafish
Wang, X., Shen, Y., & Liu, D. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26178480 · Cited by 1
“…in the apical cell branches of cerebrovascular endothelium determines the fate of apical cell branch contraction or elongation, which in turn determines the choice of pathways for blood vessel growth and the pattern of formation of the three-dimensional network of cerebrovascular vessels [49].”
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The Multifaceted Roles of Pituitary Pericytes in Health and Disease
Chen, X., Ke, X., Lu, Y., Miao, H., Duan, L., Yang, H., Pan, H., Gong, F., Wang, L., & Zhu, H. (2025) · Endocrinology · doi:10.1210/endocr/bqaf152 · Cited by 1
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Fibrinogen triggers perivascular fibroblast activation in a mouse model of cortical ischemic stroke
Santamaría, J. C. M., Fehlberg, C., Conforti, P., Ness, J. N., Justiniano, F. G., Manzitti, P., Bucher, F., Lee, J. K., & Schachtrup, C. (2025) · iScience · doi:10.1016/j.isci.2025.113834 · Cited by 2
“2,6,7,9,12 Morphometric analysis and 3–”
Wazhi, K., Lam, F. C., Guru, S., Hori, Y. S., AbuReesh, D., Shoemaker, L. D., Park, D. J., & Chang, S. D. (2025) · Brain Sciences · doi:10.3390/brainsci15111145 · Cited by 1
“Other genes that were enriched in human endothelial AVM zonations included VEGF in the arteries, MFSD2A in the capillaries, and ACKR1 in the veins [13–15].”
Type-I nNOS neurons orchestrate cortical neural activity and vasomotion
Turner, K., Brockway, D. F., Hossain, M. S., Griffith, K. R., Greenawalt, D. I., Zhang, Q., Gheres, K. W., Crowley, N. A., & Drew, P. J. (2025) · eLife · doi:10.7554/elife.105649.3 · Cited by 4
Neuronal stress promotes Cre recombinase transfer from oligodendroglia to neurons
Xu, T., Yang, K., Feng, Y., Wu, Y., Zhang, L., Yang, Z., Yuan, F., & Lyu, H. (2025) · Acta Histochemica · doi:10.1016/j.acthis.2025.152300 · Cited by 1
Kurz, L., Lütge, M., Martin, A. D., et al. (2025) · The Journal of Experimental Medicine · doi:10.1084/jem.20242300 · Cited by 1
“…all organs, including lymph nodes, is separated from the bloodstream by an endothelial barrier that is under-pinned by concentric layers of mural cells (i.e., pericytes and vascular smooth muscle cells [VSMCs]) (Lütge et al., 2025; Muhl et al., 2020; Muhl et al., 2022; Vanlandewijck et al., 2018).”
Distinguishing subtypes of endothelial cells in the mouse aorta
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EHD4 and ASAP2 are critical negative regulators of the claudin‐5‐based endothelial barrier
Hashimoto, Y., Porkoláb, G., Hudson, N., O’Callaghan, J., Hanley, N., Delaney, C. P., Deli, M. A., Westenskow, P. D., & Campbell, M. (2025) · FEBS Journal · doi:10.1111/febs.70357 · Cited by 1
Mechanisms of parasite‐mediated disruption of brain vessels
Loira, L., Arroz‐Madeira, S., Franco, C. A., & Pereira, S. S. (2025) · FEBS Letters · doi:10.1002/1873-3468.70255 · Cited by 1
“At these vessels, glial cells modulate EC expression of adhesion molecules, such as VCAM-1, ICAM-1 or P-glycoprotein [51,85,86], promoting immune cell recruitment and crossing into the perivascular space, thus contributing to immune cell surveillance of the brain [87].”
Janton, C., Nichols, A., & Hadjiargyrou, M. (2025) · JBMR Plus · doi:10.1093/jbmrpl/ziaf193 · Cited by 1
“In a separate neuronal atlas, constructed by Vanlandewijck et al. 48 and He et al. 49 examining neuronal cell types that have been enriched for vasculature and vessel-associated cell types, Mustn1 (Figure 1B) and Acta2 (Figure 1C) were highly coexpressed in arterial and venous SMCs.”
Tian, Y., Liu, L., Ma, C., et al. (2025) · Microchemical Journal · doi:10.1016/j.microc.2025.114581 · Cited by 1
Distribution and Levels of Insulin-like Growth Factor 2 Receptor Across Mouse Brain Cell Types
Gaunt, J. R., Manoj, G., & Alberini, C. M. (2025) · Receptors · doi:10.3390/receptors5010001 · Cited by 2
“Our mRNA analyses of previously published transcriptomic data confirmed that Igf2r expression is highest in neurons, particularly in cholinergic populations, and in mural cells relative to vascular endothelial cells [33–36].”
InfluentialTargeting KAT8 alleviates vascular senescence by modulating the INHBA/TGF-β pathway
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“67,97 Fibroblasts are a highly heterogeneous cell type with different functions and gene expression depending on the tissue of origin.”
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“We characterized the endothelial subclusters and assigned identity using known markers of endothelial zonation [66–71] (Table 2).”
Lin, J., Liao, K., & Lewandowski, S. A. (2026) · Acta Neuropathologica Communications · doi:10.1186/s40478-026-02236-8 · Cited by 2
“Subsequent single cell sequencing studies showed that the expression of Glast / Slc1a3 is present in other brain cell types including fibroblasts and astrocytes [58].”
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“Using the single-cell transcriptome database of mouse cerebrovascular cells from previous reports [33, 34], we analyzed the expression level of Pkhd1 in each cell type.”
Vascular basement membrane laminins modulate functional zonation of cerebral microvessels
Deshpande, T., Kapupara, K., Hannocks, M., Huppert, J., Samawar, S.-K., Thulichery, D. R., Budny, S., Ghavampour, S., Song, J., Meng, L., et al. (2026) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x251410040 · Cited by 1
“18,828 single cell transcriptomes were clustered and annotated based on previous studies 31,32 (sFigure 1(B)).”
Thaysen, M., Ørum, L. T., Pedersen, A. B. V., Svane, N., Frazier, S. E. D., Saaby, L., Brodin, B., & Kristensen, M. (2026) · Fluids and Barriers of the CNS · doi:10.1186/s12987-026-00781-x · Cited by 1
“However, in contrast to GLUT1 and TfR, BCRP is not expressed in pericytes and astrocytes [45, 46], thus excluding the possibility from obtaining a BCRP signal from contaminating cells of the capillary preparations.”
Lee, N. J., Bozdag, F. Z., Leong, J. X., Parab, S., Lam, A. E., Thakur, V., & Matsuoka, R. L. (2026) · Journal of Neuroscience · doi:10.1523/jneurosci.2204-25.2026 · Cited by 2
“Current evidence suggests that cerebrovascular endothelial cells (ECs) play a central role in regulating brain region-speci fi c vessel permeability by exhibiting phenotypic diversity (Vanlandewijck et al., 2018; Kalucka et al., 2020).”
Junctions, Transporters, and Interactions of Endothelial Cells: Regulation by Ethanol
Mandyam, C. D., Vandekerkhoff, A., Jung, S., Kharidia, D., Ponomarev, I., & Kisby, B. R. (2026) · International Journal of Molecular Sciences · doi:10.3390/ijms27062695 · Cited by 3
Function and Modulation of Sphingosine-1-Phosphate Receptors in the Central Nervous System
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“Although pericyte-specific S1PR expression patterns are less comprehensively defined than those of endothelial cells, available evidence supports functional expression of S1PR1 and S1PR2, with S1P signaling influencing pericyte survival, contractility, and endothelial–pericyte crosstalk [76].”
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Zhang, X., Li, C., Wang, Y., Liu, Y., Han, Y., Jing, Y., & Deng, F. (2026) · Journal of Neurology · doi:10.1007/s00415-026-13783-4 · Cited by 3
Sensing of shear stress in vascular endothelial cells – from physiology to pathology
Chuntharpursat‐Bon, E., Serbanovic‐Canic, J., Alfaidi, M., Jones, E. A. V., Cheng, C., White, S. J., Hsiai, T. K., Jo, H., Baeyens, N., Fang, Y., et al. (2026) · Journal of Cell Science · doi:10.1242/jcs.264456 · Cited by 2
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Benchmarking component choices for unpaired single cell RNA and epigenomic integration
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A neurovascular survival axis for adult sympathetic neurons
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Calcium‐activated chloride channels in pericytes and their role in regulating organ blood flow
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Metadata
- Authors
- Vanlandewijck, M., He, L., Mäe, M. A., Andrae, J., Ando, K., Del Gaudio, F., Nahar, K., Lebouvier, T., Laviña, B., Gouveia, L., Sun, Y., Raschperger, E., Räsänen, M., Zarb, Y., Mochizuki, N., Keller, A., Lendahl, U., & Betsholtz, C.
- Affiliations
- Uppsala University (SE)
- Tianjin Medical University General Hospital (CN)
- Karolinska Institutet (SE)
- University of Zurich (CH)
- Japan Agency for Medical Research and Development (JP)
- Corresponding author
- Betsholtz, Christer
- ORCID
- Venue
- Nature
- Published
- 2018-02-14
- Volume
- 554
- Issue
- 7693
- Pages
- 475-480
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2786318872
- Semantic Scholar
- 237e37a314d2faef1d389b147614e8fa550a3087
- Cited by
- 1,892
- References
- 65
- Citations by year
- 2026: 197 · 2025: 244 · 2024: 275 · 2023: 234 · 2022: 258 · 2021: 271 · 2020: 222 · 2019: 125 · 2018: 65
- FWCI
- 74.80
- Type
- journal article
- Language
- en
- Update notices
- correction (2018-06-20)
- Open access
- green
- hdl.handle.net
- Licence
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Työväentutkimus Vuosikirja (submittedVersion, other-oa)
- Funders
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (159514)
- Topics
- Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Single-cell and spatial transcriptomics
- Health Sciences › Medicine › Clinical Neurology › Cerebrovascular and genetic disorders
- Keywords
- cerebral vasculature, blood-brain barrier, endothelial cells, mural cells, pericytes, smooth muscle cells, perivascular cells, single-cell transcriptomics, cerebrovascular disease, mouse brain
- MeSH terms
- Animals, Arteries, Arterioles, Blood Vessels, Brain, Capillaries, Female, Fibroblasts, Male, Organ Specificity, Veins, Pericytes, Myocytes, Smooth Muscle, Endothelial Cells, Mice, Single-Cell Analysis, Transcriptome
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