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[Preprint]. 2025 Aug 22:2025.08.18.670951. [Version 1] doi: 10.1101/2025.08.18.670951

A long-lived Human Neurovascular PENTA Culture Model Reveals Incomplete Vascular Repair and Glial-Mediated Signaling After Traumatic Brain Injury

Daniel S Hinrichsen, Sunghyun Jun, Charitha C Anamala, Mitchell D Thielen, Anapaula Garcia, Volha Liaudanskaya
PMCID: PMC12393418  PMID: 40894680

Abstract

Traumatic brain injury (TBI) frequently leads to chronic neurovascular dysfunction, yet mechanistic insights into human-specific responses have been limited by the absence of long-term, multicellular in vitro models. Here, we report a five-cell-type human neurovascular culture system, comprising endothelial cells, astrocytes, pericytes, microglia, and neurons, engineered within a 3D scaffold to study injury-induced remodeling over multiple weeks. This PENTA-culture platform recapitulates hallmark features of the neurovascular unit and enables dissection of cell-specific contributions to vascular repair and degeneration. Upon mechanical trauma, cultures exhibit a biphasic response marked by acute endothelial disintegration, mitochondrial stress, and glial activation, followed by a delayed and incomplete repair. Confocal and proteomic analyses reveal persistent disruptions in tight junction organization, elevated TDP-43 and APP expression, and altered angiogenic and immunomodulatory signaling involving Tie2 and JAK/STAT pathways. Compared to simpler culture systems, the inclusion of microglia and neurons enhances post-injury cytokine resolution and junctional recovery, underscoring the importance of neuroimmune crosstalk. This system offers a mechanistically rich, human-relevant model for studying chronic neurovascular dysfunction and therapeutic revascularization.

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