Modeling blood-brain barrier formation and cerebral cavernous malformations in human PSC-derived organoids

Lan Dao, Zhen You, Lu Lu, Tianyang Xu, Avijite Kumer Sarkar, Hui Zhu, Miao Liu, Riccardo Calandrelli, George Yoshida, Pei Lin, Yifei Miao, Sarah Mierke, Srijan Kalva, Haining Zhu, Mingxia Gu, Sudhakar Vadivelu, Sheng Zhong, L. Frank Huang, Ziyuan Guo

Research output: Contribution to journalArticlepeer-review

11 Scopus citations

Abstract

The human blood-brain barrier (hBBB) is a highly specialized structure that regulates passage across blood and central nervous system (CNS) compartments. Despite its critical physiological role, there are no reliable in vitro models that can mimic hBBB development and function. Here, we constructed hBBB assembloids from brain and blood vessel organoids derived from human pluripotent stem cells. We validated the acquisition of blood-brain barrier (BBB)-specific molecular, cellular, transcriptomic, and functional characteristics and uncovered an extensive neuro-vascular crosstalk with a spatial pattern within hBBB assembloids. When we used patient-derived hBBB assembloids to model cerebral cavernous malformations (CCMs), we found that these assembloids recapitulated the cavernoma anatomy and BBB breakdown observed in patients. Upon comparison of phenotypes and transcriptome between patient-derived hBBB assembloids and primary human cavernoma tissues, we uncovered CCM-related molecular and cellular alterations. Taken together, we report hBBB assembloids that mimic the core properties of the hBBB and identify a potentially underlying cause of CCMs.

Original languageEnglish (US)
Pages (from-to)818-833.e11
JournalCell Stem Cell
Volume31
Issue number6
DOIs
StatePublished - Jun 6 2024

Keywords

  • assembloids
  • cerebral cavernous malformations
  • human PSC-derived organoids
  • human blood-brain barrier
  • neuro-vascular development
  • neuro-vascular interactions
  • single-cell transcriptomics
  • spatial transcriptomics

ASJC Scopus subject areas

  • Molecular Medicine
  • Genetics
  • Cell Biology

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