ArticleCell2022
Ensembles of endothelial and mural cells promote angiogenesis in prenatal human brain.
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Article in Cell, 2022. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 84 papers, 1 of them a synthesis that pooled it.
0numbers the graph read from it
0cells of the map it votes in
84citing papers in PubMed, 1 pooled it
9.6field-weighted citation impact, top 1% of its field
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Who cites it
84 citing papers in PubMed, 1 synthesis or guideline pooled it, 125 citations in OpenAlex.
- Deciphering cell-type-and temporally specific matrisome expression signatures in human cortical development and neurodevelopmental disorders via scRNA-seq meta-analysis.Nature communications · 2025Pooled it
- Engineered Microvascular Model of the Blood-Brain-Tumor Barrier Reveals Endothelial Remodeling in Diffuse Midline Glioma.Advanced healthcare materials · 2026Article
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- Cellular and signalling mechanisms that regulate the blood-brain barrier.Nature reviews. Molecular cell biology · 2026Review
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- TGF-β signaling promotes astroglial activation and TDP-43 proteinopathy in organoid models of frontotemporal lobar degeneration.The Journal of clinical investigation · 2026Article
- Distinct mural cells and fibroblasts drive fibrochondrogenesis in retrodiscal tissue following temporomandibular joint disc displacement.JCI insight · 2026Article
- Next-Generation Strategies for Neural Repair and Regeneration: Neural Organoid Transplantation in the CNS.Cell proliferation · 2026Review
- Hepatic cavernous hemangioma decellularized extracellular matrix/GelMA composite hydrogel promotes angiogenesis via the ITGA9-FAK-ERK1/2 axis.Materials today. Bio · 2026Article
- Simulation-guided chemical direct reprogramming informed by temporal cellular conversion processes at the single-cell level.Communications chemistry · 2026Article
- Towards precision medicine for brain arteriovenous malformations.The Journal of clinical investigation · 2026Review
- A Perturb-seq screen guided by species divergence uncovers pathways for collateral artery formation.bioRxiv : the preprint server for biology · 2026Article
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- Integrin β3 Promotes Retinal Neovascularization via Endoplasmic Reticulum Stress-Mediated Endothelial Cell Senescence.Investigative ophthalmology & visual science · 2026Article
- The Expanding Role of Gene Sequencing in Shaping Fetal Therapies: Clinical and Ethical Considerations.Prenatal diagnosis · 2026Review
- Single-cell transcriptomic analyses reveal angiogenic vascular responses to chronic cerebral hypoperfusion.iScience · 2026Article
- Article
- Targeting Arterial Dysfunction in Cardiovascular Disease Using Stem Cell-Based Therapies.FASEB journal : official publication of the Federation of American Societies for Experimental Biology · 2026Review
- Genetic insights on the mechanisms of human cortical folding.bioRxiv : the preprint server for biology · 2026Article
24 more citing papers are in PubMed but not listed here.
Corrections and comments
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Authors and funding
25 authors at 6 institutions in 2 countries.
Elizabeth E CrouchDepartment of Pediatrics, University of California San Francisco, San Francisco, CA 94143, USA; The Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, University of California, San Francisco, San Francisco, CA 94143, USA; Biomedical Science Graduate Program, University of California, San Francisco, San Francisco, CA 94143, USA; Developmental & Stem Cell Biology Graduate Program, University of California, San Francisco, San Francisco, CA 94143, USA. Electronic address: elizabeth.crouch@ucsf.edu.
Aparna BhaduriDepartment of Biological Chemistry, University of California, Los Angeles, Los Angeles, CA 90095, USA.
Madeline G AndrewsThe Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, University of California, San Francisco, San Francisco, CA 94143, USA; Department of Neurology, University of California, San Francisco, San Francisco, CA 94143, USA.
Arantxa Cebrian-SillaThe Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, University of California, San Francisco, San Francisco, CA 94143, USA; Department of Neurological Surgery, University of California, San Francisco, San Francisco, CA 94143, USA.
Loukas N DiafosDepartment of Pediatrics, University of California San Francisco, San Francisco, CA 94143, USA; The Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, University of California, San Francisco, San Francisco, CA 94143, USA.
Janeth Ochoa BirruetaDepartment of Pediatrics, University of California San Francisco, San Francisco, CA 94143, USA; The Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, University of California, San Francisco, San Francisco, CA 94143, USA.
Kaylee Wedderburn-PughThe Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, University of California, San Francisco, San Francisco, CA 94143, USA; Biomedical Science Graduate Program, University of California, San Francisco, San Francisco, CA 94143, USA; Medical Scientist Training Program, University of California, San Francisco, San Francisco, CA 94143, USA.
Edward J ValenzuelaDepartment of Pediatrics, University of California San Francisco, San Francisco, CA 94143, USA; The Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, University of California, San Francisco, San Francisco, CA 94143, USA.
Neal K BennettGladstone Institute of Neurological Disease, Gladstone Institutes, San Francisco, CA 94158, USA.
Ugomma C EzeThe Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, University of California, San Francisco, San Francisco, CA 94143, USA; Medical Scientist Training Program, University of California, San Francisco, San Francisco, CA 94143, USA; Developmental & Stem Cell Biology Graduate Program, University of California, San Francisco, San Francisco, CA 94143, USA.
Carmen Sandoval-EspinosaThe Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, University of California, San Francisco, San Francisco, CA 94143, USA; Department of Neurology, University of California, San Francisco, San Francisco, CA 94143, USA; Biomedical Science Graduate Program, University of California, San Francisco, San Francisco, CA 94143, USA.
Jiapei ChenBiomedical Science Graduate Program, University of California, San Francisco, San Francisco, CA 94143, USA; Department of Pathology, University of California, San Francisco, San Francisco, CA 94143, USA.
Cristina MoraDepartment of Pathology, University of California, San Francisco, San Francisco, CA 94143, USA.
Jayden M RossThe Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, University of California, San Francisco, San Francisco, CA 94143, USA; Department of Neurology, University of California, San Francisco, San Francisco, CA 94143, USA.
Clare E HowardDepartment of Pediatrics, University of California San Francisco, San Francisco, CA 94143, USA.
Susana Gonzalez-GraneroLaboratorio de Neurobiología Comparada, Instituto Cavanilles de Biodiversidad y 21 Biología Evolutiva, Universitat de València - Centro de Investigación Biomédica en Red 22 sobre Enfermedades Neurodegenerativas, Valencia, Spain.
Jaime Ferrer LozanoDepartment of Pathology, Hospital Universitari i Politecnic La Fe, Valencia, Spain.
Maximo VentoNeonatal Research Group, Health Research Institute La Fe, Valencia, Spain; Division of Neonatology, University and Polytechnic Hospital La Fe, Valencia, Spain.
Maximilian HaeusslerGenomics Institute, University of California, Santa Cruz, Santa Cruz, CA 95060, USA.
Mercedes F ParedesThe Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, University of California, San Francisco, San Francisco, CA 94143, USA; Department of Neurology, University of California, San Francisco, San Francisco, CA 94143, USA; Biomedical Science Graduate Program, University of California, San Francisco, San Francisco, CA 94143, USA; Developmental & Stem Cell Biology Graduate Program, University of California, San Francisco, San Francisco, CA 94143, USA; Neuroscience Graduate Program, University of California San Francisco, San Francisco, CA 94143, USA.
Ken NakamuraDepartment of Neurology, University of California, San Francisco, San Francisco, CA 94143, USA; Biomedical Science Graduate Program, University of California, San Francisco, San Francisco, CA 94143, USA; Gladstone Institute of Neurological Disease, Gladstone Institutes, San Francisco, CA 94158, USA; Neuroscience Graduate Program, University of California San Francisco, San Francisco, CA 94143, USA.
Jose Manuel Garcia-VerdugoLaboratorio de Neurobiología Comparada, Instituto Cavanilles de Biodiversidad y 21 Biología Evolutiva, Universitat de València - Centro de Investigación Biomédica en Red 22 sobre Enfermedades Neurodegenerativas, Valencia, Spain.
Arturo Alvarez-BuyllaThe Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, University of California, San Francisco, San Francisco, CA 94143, USA; Department of Neurological Surgery, University of California, San Francisco, San Francisco, CA 94143, USA; Biomedical Science Graduate Program, University of California, San Francisco, San Francisco, CA 94143, USA; Developmental & Stem Cell Biology Graduate Program, University of California, San Francisco, San Francisco, CA 94143, USA; Neuroscience Graduate Program, University of California San Francisco, San Francisco, CA 94143, USA.
Arnold R KriegsteinThe Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, University of California, San Francisco, San Francisco, CA 94143, USA; Department of Neurology, University of California, San Francisco, San Francisco, CA 94143, USA; Biomedical Science Graduate Program, University of California, San Francisco, San Francisco, CA 94143, USA; Developmental & Stem Cell Biology Graduate Program, University of California, San Francisco, San Francisco, CA 94143, USA; Neuroscience Graduate Program, University of California San Francisco, San Francisco, CA 94143, USA.
Eric J HuangThe Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, University of California, San Francisco, San Francisco, CA 94143, USA; Biomedical Science Graduate Program, University of California, San Francisco, San Francisco, CA 94143, USA; Developmental & Stem Cell Biology Graduate Program, University of California, San Francisco, San Francisco, CA 94143, USA; Department of Pathology, University of California, San Francisco, San Francisco, CA 94143, USA; Neuroscience Graduate Program, University of California San Francisco, San Francisco, CA 94143, USA; Pathology Service 113B, San Francisco Veterans Affairs Healthcare System, San Francisco, CA 94121, USA. Electronic address: eric.huang2@ucsf.edu.
University of California, San Francisco · USGladstone Institutes · USHospital Universitari i Politècnic La Fe · ESUniversitat de València · ESUniversity of California, Los Angeles · USUniversity of California, Santa Cruz · US
Funding
Pediatric Scientist Development Program (PSDP) [K12]K12HD000850 · NICHD · YALE UNIVERSITY · PI Sallie R. Permar · 1987 to 2026
$44.1MThe UCSC Genome BrowserU41HG002371 · NHGRI · UNIVERSITY OF CALIFORNIA SANTA CRUZ · PI KENT, WILLIAM JAMES · 2012 to 2021
$36.6MResearch BaseP30DK063720 · NIDDK · UNIVERSITY OF CALIFORNIA, SAN FRANCISCO · PI KRUMMEL, MATTHEW F · 2003 to 2019
$21.8MThe UCSC Genome BrowserU24HG002371 · NHGRI · UNIVERSITY OF CALIFORNIA SANTA CRUZ · PI Maximilian Haeussler · 2022 to 2026
$17.6MRegulation of Cellular Pathwaysin Human Brain DevelopmentP01NS083513 · NINDS · UNIVERSITY OF CALIFORNIA, SAN FRANCISCO · PI FANCY, STEPHEN PHILIP JAMES · 2014 to 2024
$12.6MMedical Scientist Training Program (T32 NRSA Training Grant)T32GM141323 · NIGMS · UNIVERSITY OF CALIFORNIA, SAN FRANCISCO · PI Aimee Kao · 2021 to 2026
$10.5MDevelopment and Expansion of the Human Cerebral CortexR35NS097305 · NINDS · UNIVERSITY OF CALIFORNIA, SAN FRANCISCO · PI KRIEGSTEIN, ARNOLD · 2017 to 2024
$8.5MMapping the Developing Human Neocortex by Massively Parallel Single Cell AnalysisU01MH105989 · NIMH · UNIVERSITY OF CALIFORNIA, SAN FRANCISCO · PI KRIEGSTEIN, ARNOLD · 2014 to 2016
$5.1MDefining Strategies to Target Energy Failure in Metabolically Vulnerable Human CellsR01AG065428 · NIA · J. DAVID GLADSTONE INSTITUTES · PI NAKAMURA, KEN · 2020 to 2024
$3.7MGyrencephalic Model for Neurodevelopmental Disease and Postnatal Cortical Therapeutic InterventionsDP2NS122550 · NINDS · UNIVERSITY OF CALIFORNIA, SAN FRANCISCO · PI PAREDES, MERCEDES · 2020 to 2020
$2.4MVascular mural cells in the development of the blood brain barrierDP2MH136391 · NIMH · UNIVERSITY OF CALIFORNIA, SAN FRANCISCO · PI Elizabeth Erin Crouch · 2023 to 2026
$2.4MMural stem cells in normal development and germinal matrix hemorrhage in the preterm human brainK08NS116161 · NINDS · UNIVERSITY OF CALIFORNIA, SAN FRANCISCO · PI CROUCH, ELIZABETH ERIN · 2021 to 2025
$1.1MNHGRI NIH HHS U24 HG002371NHGRI NIH HHS U41 HG002371NIA NIH HHS R01 AG065428NICHD NIH HHS K12 HD000850NIDDK NIH HHS P30 DK063720NIMH NIH HHS DP2 MH136391NIMH NIH HHS K99 MH125329NIMH NIH HHS R00 MH125329NIMH NIH HHS RF1 MH132662NIMH NIH HHS U01 MH105989NINDS NIH HHS DP2 NS122550NINDS NIH HHS F31 NS117121NINDS NIH HHS K08 NS091537NINDS NIH HHS K08 NS116161NINDS NIH HHS K99 NS111731NINDS NIH HHS P01 NS083513NINDS NIH HHS R00 NS111731NINDS NIH HHS R35 NS097305
Abstract
Interactions between angiogenesis and neurogenesis regulate embryonic brain development. However, a comprehensive understanding of the stages of vascular cell maturation is lacking, especially in the prenatal human brain. Using fluorescence-activated cell sorting, single-cell transcriptomics, and histological and ultrastructural analyses, we show that an ensemble of endothelial and mural cell subtypes tile the brain vasculature during the second trimester. These vascular cells follow distinct developmental trajectories and utilize diverse signaling mechanisms, including collagen, laminin, and midkine, to facilitate cell-cell communication and maturation. Interestingly, our results reveal that tip cells, a subtype of endothelial cells, are highly enriched near the ventricular zone, the site of active neurogenesis. Consistent with these observations, prenatal vascular cells transplanted into cortical organoids exhibit restricted lineage potential that favors tip cells, promotes neurogenesis, and reduces cellular stress. Together, our results uncover important mechanisms into vascular maturation during this critical period of human brain development.
Indexed as
Endothelial CellsNeovascularization, PhysiologicBrainCollagenHumansLamininMidkineNeovascularization, PathologicPericytesCollagenLamininMidkineangiogenesisarterial endothelial cellsblood brain barriercortical organoidsendothelial cellshuman prenatal brain developmentmural cellspericytessmooth muscle cellstip cellsvenous and capillary endothelial cellsventricular zone
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