Characteristics of blood-brain barrier heterogeneity between brain regions revealed by profiling vascular and perivascular cells.

TitleCharacteristics of blood-brain barrier heterogeneity between brain regions revealed by profiling vascular and perivascular cells.
Publication TypeJournal Article
Year of Publication2024
AuthorsPfau SJ, Langen UH, Fisher TM, Prakash I, Nagpurwala F, Lozoya RA, Lee W-CAllen, Wu Z, Gu C
JournalNat Neurosci
Volume27
Issue10
Pagination1892-1903
Date Published2024 Oct
ISSN1546-1726
KeywordsAnimals, Astrocytes, Blood-Brain Barrier, Brain, Cerebral Cortex, Endothelial Cells, Fibroblasts, Male, Median Eminence, Mice, Mice, Inbred C57BL, Pericytes, Single-Cell Analysis
Abstract

The blood-brain barrier (BBB) protects the brain and maintains neuronal homeostasis. BBB properties can vary between brain regions to support regional functions, yet how BBB heterogeneity occurs is poorly understood. Here, we used single-cell and spatial transcriptomics to compare the mouse median eminence, one of the circumventricular organs that has naturally leaky blood vessels, with the cortex. We identified hundreds of molecular differences in endothelial cells (ECs) and perivascular cells, including astrocytes, pericytes and fibroblasts. Using electron microscopy and an aqueous-based tissue-clearing method, we revealed distinct anatomical specializations and interaction patterns of ECs and perivascular cells in these regions. Finally, we identified candidate regionally enriched EC-perivascular cell ligand-receptor pairs. Our results indicate that both molecular specializations in ECs and unique EC-perivascular cell interactions contribute to BBB functional heterogeneity. This platform can be used to investigate BBB heterogeneity in other regions and may facilitate the development of central nervous system region-specific therapeutics.

DOI10.1038/s41593-024-01743-y
Alternate JournalNat Neurosci
PubMed ID39210068
PubMed Central IDPMC11452347
Grant ListDP1 NS092473 / NS / NINDS NIH HHS / United States
RF1DA048786 / / U.S. Department of Health & Human Services | NIH | National Institute on Drug Abuse (NIDA) /
P30 NS072030 / NS / NINDS NIH HHS / United States
R01 NS108410 / NS / NINDS NIH HHS / United States
R35NS116820 / / U.S. Department of Health & Human Services | NIH | National Institute on Drug Abuse (NIDA) /
RF1 DA048786 / DA / NIDA NIH HHS / United States
Investigator / / Howard Hughes Medical Institute (HHMI) /
R35 NS116820 / NS / NINDS NIH HHS / United States
R21 NS085320 / NS / NINDS NIH HHS / United States
DRG-2289-17 / / Damon Runyon Cancer Research Foundation (Cancer Research Fund of the Damon Runyon-Walter Winchell Foundation) /
DP1NS092473 / / U.S. Department of Health & Human Services | NIH | National Cancer Institute (NCI) /
ALTF 42-2017 / / European Molecular Biology Organization (EMBO) /
Faculty Scholar / / Howard Hughes Medical Institute (HHMI) /