Identification of direct connections between the dura and the brain

Leon C. D. Smyth (), Di Xu, Serhat V. Okar, Taitea Dykstra, Justin Rustenhoven, Zachary Papadopoulos, Kesshni Bhasiin, Min Woo Kim, Antoine Drieu, Tornike Mamuladze, Susan Blackburn, Xingxing Gu, María I. Gaitán, Govind Nair, Steffen E. Storck, Siling Du, Michael A. White, Peter Bayguinov, Igor Smirnov, Krikor Dikranian, Daniel S. Reich and Jonathan Kipnis ()
Additional contact information
Leon C. D. Smyth: Washington University in St Louis
Di Xu: Washington University in St Louis
Serhat V. Okar: National Institutes of Health
Taitea Dykstra: Washington University in St Louis
Justin Rustenhoven: Washington University in St Louis
Zachary Papadopoulos: Washington University in St Louis
Kesshni Bhasiin: Washington University in St Louis
Min Woo Kim: Washington University in St Louis
Antoine Drieu: Washington University in St Louis
Tornike Mamuladze: Washington University in St Louis
Susan Blackburn: Washington University in St Louis
Xingxing Gu: Washington University in St Louis
María I. Gaitán: National Institutes of Health
Govind Nair: National Institutes of Health
Steffen E. Storck: Washington University in St Louis
Siling Du: Washington University in St Louis
Michael A. White: Washington University School of Medicine, Washington University in St Louis
Peter Bayguinov: Washington University School of Medicine, Washington University in St Louis
Igor Smirnov: Washington University in St Louis
Krikor Dikranian: Washington University School of Medicine, Washington University in St Louis
Daniel S. Reich: National Institutes of Health
Jonathan Kipnis: Washington University in St Louis

Nature, 2024, vol. 627, issue 8002, 165-173

Abstract: Abstract The arachnoid barrier delineates the border between the central nervous system and dura mater. Although the arachnoid barrier creates a partition, communication between the central nervous system and the dura mater is crucial for waste clearance and immune surveillance1,2. How the arachnoid barrier balances separation and communication is poorly understood. Here, using transcriptomic data, we developed transgenic mice to examine specific anatomical structures that function as routes across the arachnoid barrier. Bridging veins create discontinuities where they cross the arachnoid barrier, forming structures that we termed arachnoid cuff exit (ACE) points. The openings that ACE points create allow the exchange of fluids and molecules between the subarachnoid space and the dura, enabling the drainage of cerebrospinal fluid and limited entry of molecules from the dura to the subarachnoid space. In healthy human volunteers, magnetic resonance imaging tracers transit along bridging veins in a similar manner to access the subarachnoid space. Notably, in neuroinflammatory conditions such as experimental autoimmune encephalomyelitis, ACE points also enable cellular trafficking, representing a route for immune cells to directly enter the subarachnoid space from the dura mater. Collectively, our results indicate that ACE points are a critical part of the anatomy of neuroimmune communication in both mice and humans that link the central nervous system with the dura and its immunological diversity and waste clearance systems.

Date: 2024
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DOI: 10.1038/s41586-023-06993-7

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