Temporally distinct 3D multi-omic dynamics in the developing human brain.

Heffel, Matthew G; Zhou, Jingtian; Zhang, Yi; Lee, Dong-Sung; Hou, Kangcheng; Pastor-Alonso, Oier; Abuhanna, Kevin D; Galasso, Joseph et al. · Nature · 2024

basic_science · Level V

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Abstract

The human hippocampus and prefrontal cortex play critical roles in learning and cognition<sup>1,2</sup>, yet the dynamic molecular characteristics of their development remain enigmatic. Here we investigated the epigenomic and three-dimensional chromatin conformational reorganization during the development of the hippocampus and prefrontal cortex, using more than 53,000 joint single-nucleus profiles of chromatin conformation and DNA methylation generated by single-nucleus methyl-3C sequencing (snm3C-seq3)<sup>3</sup>. The remodelling of DNA methylation is temporally separated from chromatin conformation dynamics. Using single-cell profiling and multimodal single-molecule imaging approaches, we have found that short-range chromatin interactions are enriched in neurons, whereas long-range interactions are enriched in glial cells and non-brain tissues. We reconstructed the regulatory programs of cell-type development and differentiation, finding putatively causal common variants for schizophrenia strongly overlapping with chromatin loop-connected, cell-type-specific regulatory regions. Our data provide multimodal resources for studying gene regulatory dynamics in brain development and demonstrate that single-cell three-dimensional multi-omics is a powerful approach for dissecting neuropsychiatric risk loci.

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