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It has recently been found that physiological stimuli including sensory experience or developmental signals remodel neuronal genome architecture in vivo. Strikingly, it's found that long-distance genome interactions massively increase in the developing cerebellum in mice. The discovery of these long-distance interactions formed between genes critical for neuronal differentiation unveils novel nuclear mechanisms by which genome architecture may play a role in the wiring of the brain. These findings raise fundamental questions on the mechanisms and biological functions of these interactions in the brain, which will be addressed in this grant. First, the organizing principles of long-distance genome interactions in the brain will be elucidated. Based on the in vivo findings, the hypothesis that long-distance genomic interactions are organized by specific epigenetic and transcriptional features will be tested. In addition, the study will also test the hypothesis that anchors of long-distance interactions assemble into higher-ordered subnuclear structures including nuclear speckles or Mediator condensates, which function as transcriptionally active hubs. Second, the projcet will define mechanisms by which long-distance interactions are formed in development. The BAF chromatin remodeling complex alters the genome environment to activate or repress transcription and is required for brain development in mice and humans, and its dysregulation results in human neurodevelopmental disorders, including Coffin\u2013Siris syndrome and autism. Based on our preliminary findings, the hypothesis that the BAF complex transiently inhibits formation of long-distance genome interactions in immature neurons of the developing brain will be tested. Following early development, the inhibition of the long-distance interactions might be relieved by the recruitment of specific sets of transcription factors that drive terminal neuron differentiation. This project will test the hypothesis that these transcription regulators, identified using DNA motif analyses, promote the formation of the long-distance genome interactions. Finally, this study will also test the hypothesis that the formation of long-distance genome interactions is necessary for the maturation of neurons in vivo, including making proper connections with their pre- and post-synaptic partners. The proposed research is significant as it will advance our understanding of the mechanisms regulating genome architecture to control neuronal differentiation in mammalian brain. 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\n In situ Hi-C is a method to detect and quantify the pairwise interactions between chromosome regions across the entire genome. It was developed in 2014 as an improvement over the dilution Hi-C method. Compared to standard dilution Hi-C, this technique reduces the frequency of random ligation because the ligation is performed in situ inside the nucleus, a constrained space, instead of in solution, where DNA fragments are floating freely. In addition, this protocol can be done more quickly in the lab and was the first to introduce the use of 4-cutter restriction enzymes as opposed to the previous 6-cutters, providing higher resolution.\n

\n

\nThe protocol involves cross-linking the cells with formaldehyde to form links between physically adjacent DNA regions. The cells are then permeabilized with their nuclei intact. A 4-cutter restriction enzyme is used to digest the chromatin into multiple DNA fragments. The resulting fragments are biotinylated by end filling of the fragments ends. The fragments are then ligated and the DNA is purified and sheared. The biotinylated fragments are pulled down from the solution with streptavidin beads and a library is constructed and sequenced. Analysis of the resulting paired-end short read sequences produces a matrix that shows the number of interactions between different DNA regions.\n

\n

\nSee Rao et al., 2014 for more details.\n

\n\n
\n\n

\n Image source: Rao et al., 2014, Figure 1A\n
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\n In situ Hi-C is a method to detect and quantify the pairwise interactions between chromosome regions across the entire genome. It was developed in 2014 as an improvement over the dilution Hi-C method. Compared to standard dilution Hi-C, this technique reduces the frequency of random ligation because the ligation is performed in situ inside the nucleus, a constrained space, instead of in solution, where DNA fragments are floating freely. In addition, this protocol can be done more quickly in the lab and was the first to introduce the use of 4-cutter restriction enzymes as opposed to the previous 6-cutters, providing higher resolution.\n

\n

\nThe protocol involves cross-linking the cells with formaldehyde to form links between physically adjacent DNA regions. The cells are then permeabilized with their nuclei intact. A 4-cutter restriction enzyme is used to digest the chromatin into multiple DNA fragments. The resulting fragments are biotinylated by end filling of the fragments ends. The fragments are then ligated and the DNA is purified and sheared. The biotinylated fragments are pulled down from the solution with streptavidin beads and a library is constructed and sequenced. Analysis of the resulting paired-end short read sequences produces a matrix that shows the number of interactions between different DNA regions.\n

\n

\nSee Rao et al., 2014 for more details.\n

\n\n
\n\n

\n Image source: Rao et al., 2014, Figure 1A\n
", "filetype": "html", "content_as_html": "
In Situ Hi-C\n

\n In situ Hi-C is a method to detect and quantify the pairwise interactions between chromosome regions across the entire genome. It was developed in 2014 as an improvement over the dilution Hi-C method. Compared to standard dilution Hi-C, this technique reduces the frequency of random ligation because the ligation is performed in situ inside the nucleus, a constrained space, instead of in solution, where DNA fragments are floating freely. In addition, this protocol can be done more quickly in the lab and was the first to introduce the use of 4-cutter restriction enzymes as opposed to the previous 6-cutters, providing higher resolution.\n

\n

\nThe protocol involves cross-linking the cells with formaldehyde to form links between physically adjacent DNA regions. The cells are then permeabilized with their nuclei intact. A 4-cutter restriction enzyme is used to digest the chromatin into multiple DNA fragments. The resulting fragments are biotinylated by end filling of the fragments ends. The fragments are then ligated and the DNA is purified and sheared. The biotinylated fragments are pulled down from the solution with streptavidin beads and a library is constructed and sequenced. Analysis of the resulting paired-end short read sequences produces a matrix that shows the number of interactions between different DNA regions.\n

\n

\nSee Rao et al., 2014 for more details.\n

\n
\n\n

\nImage source: Rao et al., 2014, Figure 1A\n
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Post-mitotic neurons undergo conserved changes in genome organization, such as the inward radial repositioning of heterochromatin-rich chromosomes as they differentiate. Additionally, transcriptionally active but heterochromatin-associated gene-dense (hGD) regions significantly strengthen their long-distance interactions during cerebellar development. However, the specific developmental stages during which these nuclear changes take place have remained poorly defined. Here, we report that hGD regions relocalize toward the nuclear interior and strengthen their chromosomal interactions as immature granule neurons transition from active cell migration to subsequent stages of neuronal differentiation. During this period, hGD genomic regions are coordinately repositioned in the nucleus alongside their physically tethered heterochromatic chromocenters. Despite these major changes in nuclear organization, the hGD subcompartment remains distinct from other transcriptionally active or repressive nuclear bodies, including heterochromatic chromocenters, throughout development. Notably, these nuclear changes appear to be independent of transcriptional changes that occur during granule neuron differentiation. Together, our results provide insights into the developmental timing of structural changes in the chromosomes of post-mitotic neurons.", "uuid": "6e38470d-c0e1-4824-ba6b-ce5b905f94e3", "date_published": "2025-05-15", "url": "https://www.ncbi.nlm.nih.gov/pubmed/40353744", "journal": "Biology open", "title": "Reorganization of the heterochromatin-associated gene-dense subcompartment in early neuronal development.", "status": "current", "short_attribution": "Scrutton Alvarado NJ et al. (2025)", "ID": "PMID:40353744", "display_title": "Scrutton Alvarado NJ et al. 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However, the specific developmental stages during which these nuclear changes take place have remained poorly defined. Here, we report that hGD regions relocalize toward the nuclear interior and strengthen their chromosomal interactions as immature granule neurons transition from active cell migration to subsequent stages of neuronal differentiation. During this period, hGD genomic regions are coordinately repositioned in the nucleus alongside their physically tethered heterochromatic chromocenters. Despite these major changes in nuclear organization, the hGD subcompartment remains distinct from other transcriptionally active or repressive nuclear bodies, including heterochromatic chromocenters, throughout development. Notably, these nuclear changes appear to be independent of transcriptional changes that occur during granule neuron differentiation. 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