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Increasing evidence indicates that specific genomic regions each associate with these compartments. This genome compartmentalization has been linked to various functions, but these links are still poorly understood. Interestingly, Lamina Associated Domains (LADs) share specific heterochromatin marks, defining chromatin domains with distinct genetic and epigenetic properties. Genomic regions associating with other nuclear compartments may similarly define distinct classes of chromatin domains. One major bottleneck towards a deeper understanding of nuclear organization has been the inability to convert microscopy views of nuclear compartments into genome-wide maps that show which loci are associated with which compartment, and how the chromosomal fiber traverses between compartments. In addition, there is an urgent need for more efficient methods to dissect the mechanisms by which large genomic regions are targeted to specific nuclear compartments. Finally, there is an urgent need for high-throughput approaches that query the functional relevance of genome compartmentalization. For this Center grant, we propose to meet these needs through the following Aims: 1. Develop a strategy that connects microscopy views to genome-wide maps that, together with modeling, reveal the localization and dynamics of genomic regions relative to all major nuclear compartments. 2. Develop methods for efficient manipulation of the genome in order to elucidate mechanisms that target loci to specific compartments. 3. Develop methods to measure, model, and validate the functional relevance of nuclear compartments. The combined results of these approaches will reveal causal relationships now hidden among entangled genomic, epigenetic, and nuclear organization features. Deliverables of this proposal include a wide range of structural and functional maps of nuclear organization, reagents for visualizing endogenous chromosome loci, a powerful pipeline for synthesis of ~100kb DNA fragments, and cell lines facilitating repeated, high-fidelity insertio of these large fragments back into selected sites in the genome. These resources will provide a powerful complement to other 4D Nucleome Consortium efforts. A key strength of this Center proposal is the experience and complementary research capabilities of its five Investigators. 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We extended and validated Tyramide Signal Amplification (TSA)-seq to map genomic  regions near nucleoli and pericentric heterochromatin in four human cell lines.  Our study confirmed that smaller chromosomes localize closer to nucleoli but  further deconvolved this by revealing a preference for chromosome arms below  36-46 Mbp in length. We identified two lamina associated domain subsets through  their differential nuclear lamina versus nucleolar positioning in different cell  lines which showed distinctive patterns of DNA replication timing and gene  expression across all cell lines. Unexpectedly, active, nuclear  speckle-associated genomic regions were found near typically repressive nuclear  compartments, which is attributable to the close proximity of nuclear speckles  and nucleoli in some cell types, and association of centromeres with nuclear  speckles in human embryonic stem cells (hESCs). Our study points to a more  complex and variable nuclear genome organization than suggested by current  models, as revealed by our TSA-seq methodology.", "date_published": "2024-09-13", "title": "Nucleolus and centromere Tyramide Signal Amplification-Seq reveals variable  localization of heterochromatin in different cell types.", "authors": ["Kumar P", "Gholamalamdari O", "Zhang Y", "Zhang L", "Vertii A", "van Schaik T", "Peric-Hupkes D", "Sasaki T", "Gilbert DM", "van Steensel B", "Ma J", "Kaufman PD", "Belmont AS"], "ID": "PMID:39271748", "display_title": "Kumar P et al. (2024) PMID:39271748", "uuid": "22e02dc4-37b9-4891-9084-6d85f6683252", "@id": "/publications/22e02dc4-37b9-4891-9084-6d85f6683252/", "short_attribution": "Kumar P et al. (2024)", "status": "current", "journal": "Communications biology", "principals_allowed": {"view": ["system.Everyone"], "edit": ["group.admin"]}}, {"@type": ["Publication", "Item"], "abstract": "Cells undergo a major epigenome reconfiguration when reprogrammed to human  induced pluripotent stem cells (hiPS cells). However, the epigenomes of hiPS  cells and human embryonic stem (hES) cells differ significantly, which affects  hiPS cell function(1-8). These differences include epigenetic memory and  aberrations that emerge during reprogramming, for which the mechanisms remain  unknown. Here we characterized the persistence and emergence of these epigenetic  differences by performing genome-wide DNA methylation profiling throughout primed  and naive reprogramming of human somatic cells to hiPS cells. We found that  reprogramming-induced epigenetic aberrations emerge midway through primed  reprogramming, whereas DNA demethylation begins early in naive reprogramming.  Using this knowledge, we developed a transient-naive-treatment (TNT)  reprogramming strategy that emulates the embryonic epigenetic reset. We show that  the epigenetic memory in hiPS cells is concentrated in cell of origin-dependent  repressive chromatin marked by H3K9me3, lamin-B1 and aberrant CpH methylation.  TNT reprogramming reconfigures these domains to a hES cell-like state and does  not disrupt genomic imprinting. Using an isogenic system, we demonstrate that TNT  reprogramming can correct the transposable element overexpression and  differential gene expression seen in conventional hiPS cells, and that  TNT-reprogrammed hiPS and hES cells show similar differentiation efficiencies.  Moreover, TNT reprogramming enhances the differentiation of hiPS cells derived  from multiple cell types. Thus, TNT reprogramming corrects epigenetic memory and  aberrations, producing hiPS cells that are molecularly and functionally more  similar to hES cells than conventional hiPS cells. We foresee TNT reprogramming  becoming a new standard for biomedical and therapeutic applications and providing  a novel system for studying epigenetic memory.", "date_published": "2023-08", "title": "Transient naive reprogramming corrects hiPS cells functionally and  epigenetically.", "authors": ["Buckberry S", "Liu X", "Poppe D", "Tan JP", "Sun G", "Chen J", "Nguyen TV", "de Mendoza A", "Pflueger J", "Frazer T", "Vargas-Landin DB", "Paynter JM", "Smits N", "Liu N", "Ouyang JF", "Rossello FJ", "Chy HS", "Rackham OJL", "Laslett AL", "Breen J", "Faulkner GJ", "Nefzger CM", "Polo JM", "Lister R"], "ID": "PMID:37587336", "display_title": "Buckberry S et al. (2023) PMID:37587336", "uuid": "0d4af084-38e2-4a91-aa63-b170ffbe252b", "@id": "/publications/0d4af084-38e2-4a91-aa63-b170ffbe252b/", "short_attribution": "Buckberry S et al. (2023)", "status": "current", "journal": "Nature", "principals_allowed": {"view": ["system.Everyone"], "edit": ["group.admin"]}}, {"@type": ["Publication", "Item"], "abstract": "Models of nuclear genome organization often propose a binary division into active  versus inactive compartments yet typically overlook nuclear bodies. Here we  integrated analysis of sequencing and image-based data to compare genome  organization in four human cell types relative to three different nuclear  locales: the nuclear lamina, nuclear speckles, and nucleoli. Whereas gene  expression correlates mostly with nuclear speckle proximity, DNA replication  timing correlates with proximity to multiple nuclear locales. Speckle attachment  regions emerge as DNA replication initiation zones whose replication timing and  gene composition vary with their attachment frequency. Most facultative LADs  retain a partially repressed state as iLADs, despite their positioning in the  nuclear interior. Knock out of two lamina proteins, Lamin A and LBR, causes a  shift of H3K9me3-enriched LADs from lamina to nucleolus, and a reciprocal  relocation of H3K27me3-enriched partially repressed iLADs from nucleolus to  lamina. Thus, these partially repressed iLADs appear to compete with LADs for  nuclear lamina attachment with consequences for replication timing. The nuclear  organization in adherent cells is polarized with nuclear bodies and genomic  regions segregating both radially and relative to the equatorial plane. Together,  our results underscore the importance of considering genome organization relative  to nuclear locales for a more complete understanding of the spatial and  functional organization of the human genome.", "date_published": "2025-02-26", "title": "Beyond A and B Compartments: how major nuclear locales define nuclear genome  organization and function.", "authors": ["Gholamalamdari O", "van Schaik T", "Wang Y", "Kumar P", "Zhang L", "Zhang Y", "Gonzalez GAH", "Vouzas AE", "Zhao PA", "Gilbert DM", "Ma J", "van Steensel B", "Belmont AS"], "ID": "PMID:38712201", "display_title": "Gholamalamdari O et al. (2025) PMID:38712201", "uuid": "f2b3b3fb-e9af-484d-abeb-fe4316ffdc1a", "@id": "/publications/f2b3b3fb-e9af-484d-abeb-fe4316ffdc1a/", "short_attribution": "Gholamalamdari O et al. (2025)", "status": "current", "journal": "bioRxiv : the preprint server for biology", "principals_allowed": {"view": ["system.Everyone"], "edit": ["group.admin"]}}], "experiment_categorizer": {"field": "Target", "value": "LMNB1 protein", "combined": "Target: LMNB1 protein"}, "experiment_summary": "DamID-seq with DAM-LMNB1 on HFFc6 (Tier 1)", "@context": "/terms/", "aggregated-items": {"badges": [{"parent": "/biosamples/4DNBSTQ7LRR9/", "embedded_path": "biosample.badges", "item": {"messages": ["Biosample receives gold status for being a 4DN Tier 1 or Tier 2 cell line that follows the approved SOP and contains all of the pertinent metadata information as required by the 4DN Samples working group."], "badge": {"commendation": "Gold Biosample", "warning": null, "uuid": "6c2b7409-4478-4e15-aabc-1a0df6b883e9", "@id": "/badges/gold-biosample/", "badge_icon": "/static/img/badges/biosample-badge-gold-star.svg", "description": "Gold biosample"}}}]}, "validation-errors": []}