Mosaic midbrain organoids: a new tool to study Progressive Supranuclear Palsy and advancing clinical neurology research

Author:

Parrotta Elvira ImmacolataORCID,Lucchino Valeria,Zannino Clara,Valente Desirèe,Scalise Stefania,Benedetto Giorgia Lucia,Iazzetta Maria Roberta,Talarico Mariagrazia,Conforti Francesco,Di Agostino Silvia,Fiorenzano Alessandro,Quattrone Aldo,Cuda Giovanni,Quattrone Andrea

Abstract

AbstractProgressive supranuclear palsy (PSP) is a severe neurodegenerative disease pathologically characterized by intracellular tangles of hyperphosphorylated tau protein, widely distributed across the neocortex, basal ganglia, and midbrain. Developing effective drugs for PSP presents challenges due to its complex underpinning mechanism and the absence of robust human models that accurately recapitulate biochemical and pathological features of the disease phenotype. Brain organoids have recently emerged as a three-dimensional tissue culture platform to study brain development and pathology. Here, we present a novel induced pluripotent stem cell (iPSC)-derived mosaic midbrain organoid (mMOs) system from four patients with progressive supranuclear palsy-Richardson syndrome (PSP-RS), aimed at reproducing key molecular disease features while reducing variability across organoids derived from different iPSC donors. The PSP-RS 3D model exhibited accumulation of hyperphosphorylated tau protein, predominance of 4R-tau, increased GFAP-positive cells, and PSP-associated histological alterations compared to organoids derived from healthy donors. Pathologically, diseased mMOs showed typical neurofibrillary tangles and tufted-shaped astrocytes, and poorly branched processes of Tyrosine Hydroxylase-immunoreactive cells with thin terminal branches. Our results suggest that mMOs represent a valuable experimental model for PSP research and hold great promise for future identification of new therapeutic targets for progressive supranuclear palsy.

Publisher

Cold Spring Harbor Laboratory

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