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    Area of Science:

    • Neuroscience
    • Developmental Biology
    • Genetics

    Background:

    • Sex steroids are crucial for human brain development.
    • The specific cellular and molecular effects of androgens require further investigation.
    • Human neural organoid models offer a platform to study these impacts.

    Purpose of the Study:

    • To model the impact of dihydrotestosterone (DHT) on human neural organoids derived from induced pluripotent stem cells (iPSCs).
    • To investigate the transcriptional, cellular, and epigenetic consequences of androgen signaling.
    • To explore how genetic background and sex influence androgen responses in the developing brain.

    Main Methods:

    • Utilized a brain microphysiological system (bMPS) model using nine iPSC lines.
    • Administered dihydrotestosterone (DHT) and analyzed organoid responses.
    • Employed bulk RNA-sequencing, cell-type expression profiling, immunohistochemistry, and DNA methylation analysis.
    • Used isogenic XX/XY lines to differentiate sex-chromosome effects from DHT effects.

    Main Results:

    • DHT was bioavailable, translocated the androgen receptor (AR), and activated mTOR and metabolic pathways.
    • Transcriptional responses varied by donor background, converging on mitochondrial energetics, lysosomal function, and apoptosis.
    • DHT induced a shift toward astrocytic profiles in male organoids, with reduced neuronal and oligodendrocyte signatures.
    • Androgen signaling altered neurodevelopmental pathways, with autism spectrum disorder (ASD) and seizure status moderating effects.
    • DHT induced extensive DNA methylation changes, including at HOX genes and synaptic genes.

    Conclusions:

    • Androgen signaling profoundly shapes neural organoid transcription, cell populations, and epigenetics in a genetic background-dependent manner.
    • DHT influences cell-type composition and neurodevelopmental pathways, with potential implications for neurodevelopmental disorders.
    • This study highlights the utility of in vitro models for understanding inter-individual variability in brain development and disorders.