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Key epigenetic and signaling factors in the formation and maintenance of the blood-brain barrier

by Sadanandan, Jayanarayanan , Lokhande, Hrishikesh , Dash, Pramod K , Bresnick, Emery H , Huang, Zhen , Zeineddine, Hussein A , Hong, Sungha , Thomas, Sithara , Tandon, Nitin , Blackburn, Spiros L , McCrea, Pierre D , Ahirwar, Lalit K , Kumar T, Peeyush , Dienel, Ari C , Mathew, Iny Elizabeth , McBride, Devin W , Harmanci, Arif , Jose, Dania

in Analysis / Animals / beta-catenin / blood-brain barrier / Blood-Brain Barrier - metabolism / Endothelial Cells - metabolism / Epigenesis, Genetic / Epigenetic inheritance / epigenetics / Female / Gene expression / Gene Expression Profiling / Genes / HDAC2 / Histone Deacetylase 2 - genetics / Histone Deacetylase 2 - metabolism / Mice / Polycomb Repressive Complex 2 - genetics / Polycomb Repressive Complex 2 - metabolism / PRC2 / Signal Transduction / Wnt Signaling Pathway / wnt signalling

2024

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2024

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2024

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Journal Article

Key epigenetic and signaling factors in the formation and maintenance of the blood-brain barrier

Sadanandan, Jayanarayanan,

Lokhande, Hrishikesh,

Dash, Pramod K,

Bresnick, Emery H,

Huang, Zhen,

Zeineddine, Hussein A,

Hong, Sungha,

Thomas, Sithara,

Tandon, Nitin,

Blackburn, Spiros L,

McCrea, Pierre D,

Ahirwar, Lalit K,

Kumar T, Peeyush,

Dienel, Ari C,

Mathew, Iny Elizabeth,

McBride, Devin W,

Harmanci, Arif,

Jose, Dania

2024

Overview

The blood-brain barrier (BBB) controls the movement of molecules into and out of the central nervous system (CNS). Since a functional BBB forms by mouse embryonic day E15.5, we reasoned that gene cohorts expressed in CNS endothelial cells (EC) at E13.5 contribute to BBB formation. In contrast, adult gene signatures reflect BBB maintenance mechanisms. Supporting this hypothesis, transcriptomic analysis revealed distinct cohorts of EC genes involved in BBB formation and maintenance. Here, we demonstrate that epigenetic regulator’s histone deacetylase 2 (HDAC2) and polycomb repressive complex 2 (PRC2) control EC gene expression for BBB development and prevent Wnt/β-catenin (Wnt) target genes from being expressed in adult CNS ECs. Low Wnt activity during development modifies BBB genes epigenetically for the formation of functional BBB. As a Class-I HDAC inhibitor induces adult CNS ECs to regain Wnt activity and BBB genetic signatures that support BBB formation, our results inform strategies to promote BBB repair.

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Publisher

eLife Science Publications, Ltd,eLife Sciences Publications Ltd

Subject

Analysis

/ Animals

/ beta-catenin

/ blood-brain barrier

/ Blood-Brain Barrier - metabolism

/ Endothelial Cells - metabolism

/ Epigenesis, Genetic