bioRxiv Science⌕ Search

Biology subjects

Giacich, M.

Publications and source records attributed to Giacich, M..

2 recordsLinked to original sources

Pathological variants in HPDL cause collapse of the neuro-glial unit during human cortical maturation

Biallelic variants in HPDL cause a severe neurological disorder in childhood, but the mechanisms linking early developmental abnormalities to later cortical degeneration remain unclear. Here, using long-term iPSC-derived human cortical cultures derived from four patients, we investigated the late consequences of HPDL deficiency through quantitative immunofluorescence and bulk RNA-seq. We found that HPDL-deficient cortical cultures undergo progressive synaptic impairment, with marked loss of PSD95-positive postsynaptic puncta despite largely preserved general neuronal maturation markers. This phenotype is accompanied by a profound reduction in astrocytes and oligodendrocytes, together with increased neuronal apoptosis and transcriptional dysregulation of genes linked to extracellular matrix organization, cellular stress, and neurodegeneration. Unexpectedly, late-stage mutant cultures also show reactivation of early developmental programs, including aberrant expression of NEUROD4 and other proneural regulators, suggesting instability of cell identity during cortical maturation. Together, these findings support a model in which HPDL deficiency first perturbs cortical developmental timing and later drives collapse of the neuro-glial unit, linking premature neurogenesis to synaptic failure, glial loss, and progressive neurodegeneration.

neuroscience↗

HPDL is critical in human cortical development via regulation of mitochondrial functional properties

Human brain development is highly regulated by several spatiotemporal processes, which disruption can result in severe neurological disorders. Emerging evidence highlights the pivotal role of mitochondrial function as one of these fundamental pathways involved in neurodevelopment. Our study investigates the role of 4-hydroxyphenylpyruvate dioxygenase-like (HPDL) protein in cortical neurogenesis and mitochondrial activity, since mutations in the HPDL gene are associated with SPG83, a childhood-onset form of hereditary spastic paraplegia characterized by corticospinal tract degeneration and cortical abnormalities. Starting from mutant neuroblastoma cells, we demonstrated that HPDL is essential to mitochondrial respiratory chain supercomplex assembly and cellular redox balance. Moreover, transcriptomic analyses revealed dysregulated pathways related to neurogenesis, implicating HPDL role in early cortical development. To further elucidate the role of HPDL, we generated cortical neurons and organoids from SPG83 patient-derived induced pluripotent stem cells. Mutant cells exhibited premature neurogenesis at early differentiation stages, likely leading to depletion of cortical progenitors, as evidenced by decreased proliferation, slight increase of apoptosis, and unbalanced cortical type composition at later stages. Furthermore, cortical organoids derived from SPG83 patients showed impaired growth, reminding microcephaly observed in severe cases. In addition, mitochondrial morpho-functional characterization in mutant neurons confirmed disruption of OxPhos chain functionality and increased ROS generation rate. Treatment of cortical cells with two antioxidant compounds, could partially revert premature neurogenesis. In conclusion, our findings reveal a critical role for HPDL in coordinating cortical progenitor proliferation, neurogenesis, and mitochondrial function. These insights shed light on a mechanistical understanding of SPG83 pathology and underscore the therapeutic potential of targeting oxidative stress in this and related neurological disorders.

neuroscience↗