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Cited by 233Barrier Structure and Function StudiesNeuroinflammation and Neurodegeneration MechanismsAngiogenesis and VEGF in Cancer

Analysis of the brain mural cell transcriptome

Open access
He, Liqun, Vanlandewijck, Michael, Raschperger, Elisabeth, Andaloussi Mäe, Maarja, Jung, Bongnam, Lebouvier, Thibaud, Ando, Koji, Hofmann, Jennifer +2 more·2016·Scientific Reports
DOI 10.1038/srep35108PMC PMC5057134
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Abstract

Pericytes, the mural cells of blood microvessels, regulate microvascular development and function and have been implicated in many brain diseases. However, due to a paucity of defining markers, pericyte identification and functional characterization remain ambiguous and data interpretation problematic. In mice carrying two transgenic reporters, Pdgfrb-eGFP and NG2-DsRed, we found that double-positive cells were vascular mural cells, while the single reporters marked additional, but non-overlapping, neuroglial cells. Double-positive cells were isolated by fluorescence-activated cell sorting (FACS) and analyzed by RNA sequencing. To reveal defining patterns of mural cell transcripts, we compared the RNA sequencing data with data from four previously published studies. The meta-analysis provided a conservative catalogue of 260 brain mural cell-enriched gene transcripts. We validated pericyte-specific expression of two novel markers, vitronectin (Vtn) and interferon-induced transmembrane protein 1 (Ifitm1), using fluorescent in situ hybridization and immunohistochemistry. We further analyzed signaling pathways and interaction networks of the pericyte-enriched genes in silico. This work provides novel insight into the molecular composition of brain mural cells. The reported gene catalogue facilitates identification of brain pericytes by providing numerous new candidate marker genes and is a rich source for new hypotheses for future studies of brain mural cell physiology and pathophysiology.

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  • Pericytes, SMCs, and endothelial cells express thousands of transcripts encoding different transporters, receptors, active efflux pumps, ion channels, and regulatory molecules, whose expression pattern varies by zonation along the arteriocapillary-venous axis and cell type.

    “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 [242]

    The Results (pages not available in our copy) describe differences in mural-cell marker expression between capillaries, arterioles, and venules, and the Discussion reports genes expressed more strongly in pericytes than in other vascular cells. But the paper’s catalogue is of 260 mural-cell-enriched transcripts; these passages do not establish the claimed thousands of transcripts across pericytes, SMCs, and endothelial cells, or zonation of the listed functional categories along the full arteriocapillary–venous axis. (LLM, conf=0.83)

    Experimental — accuracy not yet measured

  • Organic anions are transported via the organic anion transporter OATP3A1 in pericytes.

    “Organic anions are transported via the organic anion transporter OATP3A1 (28, 129, 242).”

    From Blood-Brain Barrier: From Physiology to Disease and Back (2019) · cites this paper as [242]

    The Results section (Enriched pathway and interaction networks among the pericyte-enriched gene catalogue; page unavailable) identifies SLCO3A1, also called OATP-D, in a discussion of pericyte-enriched genes. It does not show that OATP3A1 transports organic anions in pericytes; it says the proteins’ functional roles in pericytes in vivo await investigation. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

  • Pericytes express LRP-3, which internalizes and transports lipophilic molecules.

    “Additionally, pericytes express LRP-3 (242) which internalizes and transports lipophilic molecules.”

    From Blood-Brain Barrier: From Physiology to Disease and Back (2019) · cites this paper as [242]

    The Results sections on brain mural-cell transcripts and pericyte-enriched genes do not identify LRP-3 as expressed in pericytes. Searches for Lrp3 and for lipophilic-molecule transport found no passage addressing either point in our copy. (LLM, conf=0.72)

    Experimental — accuracy not yet measured

  • Pericytes express sodium-dependent SLC13A3 for dicarboxylic acids.

    “and sodium-dependent SLC13A3 for dicarboxylic acids (242).”

    From Blood-Brain Barrier: From Physiology to Disease and Back (2019) · cites this paper as [242]

    The Results section on pericyte-enriched genes discusses SLC9A3R1, a different transporter-related protein, but does not identify SLC13A3. Searches for SLC13A3 and sodium-dependent dicarboxylate transport found no passage in our copy establishing its expression in pericytes. (LLM, conf=0.73)

    Experimental — accuracy not yet measured

  • Pericytes express carbohydrate transporters such as insulin-regulated glucose transporter GLUT4, facilitative glucose transporter GLUT10, and the sodium/myo-inositol cotransporter SMIT.

    “Pericytes express carbohydrate transporters such as insulin-regulated glucose transporter GLUT4 (242), facilitative glucose transporter GLUT10(242), and the sodium/myo-inositol cotransporter SMIT (28).”

    From Blood-Brain Barrier: From Physiology to Disease and Back (2019) · cites this paper as [242]

    The Results section describes a catalogue of brain mural-cell-enriched transcripts, but the passages in our copy do not identify GLUT4 or GLUT10 as expressed by pericytes (searched: GLUT4, GLUT10, SLC2A4, and SLC2A10). The citing sentence attaches a different citation to SMIT, so that part is not attributed to this paper. (LLM, conf=0.75)

    Experimental — accuracy not yet measured

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Research works printed but not linked: 68

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Authors
He, L., Vanlandewijck, M., Raschperger, E., Andaloussi Mäe, M., Jung, B., Lebouvier, T., Ando, K., Hofmann, J., Keller, A., & Betsholtz, C.
Affiliations
  • Uppsala University (SE)
  • University of Zurich (CH)
Corresponding author
Betsholtz, Christer
ORCID
Venue
Scientific Reports
Publisher
Springer Science and Business Media LLC
Published
2016-10-11
Volume
6
Issue
1
Pages
35108-35108
ISSN
2045-2322 (ISSN-L)
DOI
10.1038/srep35108
PMC
PMC5057134
OpenAlex
W2531568380
Cited by
233
References
75
Citations by year
2026: 6 · 2025: 18 · 2024: 32 · 2023: 18 · 2022: 30 · 2021: 36 · 2020: 29 · 2019: 18 · 2018: 36 · 2017: 8 · 2016: 1
FWCI
11.51
Type
journal article
Language
en
Open access
Licence
Locations
  • Scientific Reports (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Zurich Open Repository and Archive (University of Zurich) (acceptedVersion, cc-by)
  • Uppsala University Publications (Uppsala University) (submittedVersion, other-oa)
  • Zurich Open Repository and Archive (University of Zurich) (submittedVersion, cc-by)
  • Zurich Open Repository and Archive (University of Zurich)
Funders
  • National Science Foundation
  • Swedish Cancer Foundation
  • Fondation Leducq
  • Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (159514)
  • Knut och Alice Wallenbergs Stiftelse
  • Vetenskapsrådet
  • Uppsala Universitet
  • Science for Life Laboratory
  • Uppsala Multidisciplinary Center for Advanced Computational Science
  • FP7 Ideas: European Research Council (294556)
Topics
  • Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
  • Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
Keywords
pericytes, transcriptome, pericyte markers, vitronectin, IFITM1, signaling pathways, neuroglial cells
MeSH terms
Animals, Brain, Flow Cytometry, Staining and Labeling, Sequence Analysis, RNA, Pericytes, Gene Expression Profiling, Mice, Microvessels

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