bims-crepig Biomed News
on Chromatin regulation and epigenetics in cell fate and cancer
Issue of 2023–10–15
twenty papers selected by
Connor Rogerson, University of Cambridge



  1. Nat Commun. 2023 10 09. 14(1): 6314
      Transcription reprogramming during cell differentiation involves targeting enhancers to genes responsible for establishment of cell fates. To understand the contribution of CTCF-mediated chromatin organization to cell lineage commitment, we analyzed 3D chromatin architecture during the differentiation of human embryonic stem cells into pancreatic islet organoids. We find that CTCF loops are formed and disassembled at different stages of the differentiation process by either recruitment of CTCF to new anchor sites or use of pre-existing sites not previously involved in loop formation. Recruitment of CTCF to new sites in the genome involves demethylation of H3K9me3 to H3K9me2, demethylation of DNA, recruitment of pioneer factors, and positioning of nucleosomes flanking the new CTCF sites. Existing CTCF sites not involved in loop formation become functional loop anchors via the establishment of new cohesin loading sites containing NIPBL and YY1 at sites between the new anchors. In both cases, formation of new CTCF loops leads to strengthening of enhancer promoter interactions and increased transcription of genes adjacent to loop anchors. These results suggest an important role for CTCF and cohesin in controlling gene expression during cell differentiation.
    DOI:  https://doi.org/10.1038/s41467-023-41964-6
  2. Nat Commun. 2023 Oct 13. 14(1): 6446
      Chromatin organization controls transcription by modulating 3D-interactions between enhancers and promoters in the nucleus. Alterations in epigenetic states and 3D-chromatin organization result in gene expression changes contributing to cancer. Here, we map the promoter-enhancer interactome and regulatory landscape of glioblastoma, the most aggressive primary brain tumour. Our data reveals profound rewiring of promoter-enhancer interactions, chromatin accessibility and redistribution of histone marks in glioblastoma. This leads to loss of long-range regulatory interactions and overall activation of promoters, which orchestrate changes in the expression of genes associated to glutamatergic synapses, axon guidance, axonogenesis and chromatin remodelling. SMAD3 and PITX1 emerge as major transcription factors controlling genes related to synapse organization and axon guidance. Inhibition of SMAD3 and neuronal activity stimulation cooperate to promote proliferation of glioblastoma cells in co-culture with glutamatergic neurons, and in mice bearing patient-derived xenografts. Our findings provide mechanistic insight into the regulatory networks that mediate neurogliomal synaptic communication.
    DOI:  https://doi.org/10.1038/s41467-023-41919-x
  3. BMC Genomics. 2023 Oct 07. 24(1): 597
       BACKGROUND: Transcription factors (TFs) exhibit heterogeneous DNA-binding specificities in individual cells and whole organisms under natural conditions, and de novo motif discovery usually provides multiple motifs, even from a single chromatin immunoprecipitation-sequencing (ChIP-seq) sample. Despite the accumulation of ChIP-seq data and ChIP-seq-derived motifs, the diversity of DNA-binding specificities across different TFs and cell types remains largely unexplored.
    RESULTS: Here, we applied MOCCS2, our k-mer-based motif discovery method, to a collection of human TF ChIP-seq samples across diverse TFs and cell types, and systematically computed profiles of TF-binding specificity scores for all k-mers. After quality control, we compiled a set of TF-binding specificity score profiles for 2,976 high-quality ChIP-seq samples, comprising 473 TFs and 398 cell types. Using these high-quality samples, we confirmed that the k-mer-based TF-binding specificity profiles reflected TF- or TF-family dependent DNA-binding specificities. We then compared the binding specificity scores of ChIP-seq samples with the same TFs but with different cell type classes and found that half of the analyzed TFs exhibited differences in DNA-binding specificities across cell type classes. Additionally, we devised a method to detect differentially bound k-mers between two ChIP-seq samples and detected k-mers exhibiting statistically significant differences in binding specificity scores. Moreover, we demonstrated that differences in the binding specificity scores between k-mers on the reference and alternative alleles could be used to predict the effect of variants on TF binding, as validated by in vitro and in vivo assay datasets. Finally, we demonstrated that binding specificity score differences can be used to interpret disease-associated non-coding single-nucleotide polymorphisms (SNPs) as TF-affecting SNPs and provide candidates responsible for TFs and cell types.
    CONCLUSIONS: Our study provides a basis for investigating the regulation of gene expression in a TF-, TF family-, or cell-type-dependent manner. Furthermore, our differential analysis of binding-specificity scores highlights noncoding disease-associated variants in humans.
    Keywords:  Cell type dependency; ChIP-seq; DNA-binding motif; Differential k-mer analysis; Functional genomics; GWAS-SNP; Regulatory SNP; Transcription factor; k-mer-based analysis
    DOI:  https://doi.org/10.1186/s12864-023-09692-9
  4. Science. 2023 Oct 13. 382(6667): eadf5357
      Delineating the gene-regulatory programs underlying complex cell types is fundamental for understanding brain function in health and disease. Here, we comprehensively examined human brain cell epigenomes by probing DNA methylation and chromatin conformation at single-cell resolution in 517 thousand cells (399 thousand neurons and 118 thousand non-neurons) from 46 regions of three adult male brains. We identified 188 cell types and characterized their molecular signatures. Integrative analyses revealed concordant changes in DNA methylation, chromatin accessibility, chromatin organization, and gene expression across cell types, cortical areas, and basal ganglia structures. We further developed single-cell methylation barcodes that reliably predict brain cell types using the methylation status of select genomic sites. This multimodal epigenomic brain cell atlas provides new insights into the complexity of cell-type-specific gene regulation in adult human brains.
    DOI:  https://doi.org/10.1126/science.adf5357
  5. Genome Biol. 2023 Oct 12. 24(1): 227
       BACKGROUND: In several eukaryotes, DNA methylation occurs within the coding regions of many genes, termed gene body methylation (GbM). Whereas the role of DNA methylation on the silencing of transposons and repetitive DNA is well understood, gene body methylation is not associated with transcriptional repression, and its biological importance remains unclear.
    RESULTS: We report a newly discovered type of GbM in plants, which is under constitutive addition and removal by dynamic methylation modifiers in all cells, including the germline. Methylation at Dynamic GbM genes is removed by the DRDD demethylation pathway and added by an unknown source of de novo methylation, most likely the maintenance methyltransferase MET1. We show that the Dynamic GbM state is present at homologous genes across divergent lineages spanning over 100 million years, indicating evolutionary conservation. We demonstrate that Dynamic GbM is tightly associated with the presence of a promoter or regulatory chromatin state within the gene body, in contrast to other gene body methylated genes. We find Dynamic GbM is associated with enhanced gene expression plasticity across development and diverse physiological conditions, whereas stably methylated GbM genes exhibit reduced plasticity. Dynamic GbM genes exhibit reduced dynamic range in drdd mutants, indicating a causal link between DNA demethylation and enhanced gene expression plasticity.
    CONCLUSIONS: We propose a new model for GbM in regulating gene expression plasticity, including a novel type of GbM in which increased gene expression plasticity is associated with the activity of DNA methylation writers and erasers and the enrichment of a regulatory chromatin state.
    Keywords:  DNA demethylation; DNA methylation; Gene body methylation; Gene expression plasticity
    DOI:  https://doi.org/10.1186/s13059-023-03059-9
  6. Nat Commun. 2023 Oct 12. 14(1): 6420
      Identification of factors that regulate chromatin condensation is important for understanding of gene regulation. High-mobility group AT-hook (HMGA) proteins 1 and 2 are abundant nonhistone chromatin proteins that play a role in many biological processes including tissue stem-progenitor cell regulation, but the nature of their protein function remains unclear. Here we show that HMGA2 mediates direct condensation of polynucleosomes and forms droplets with nucleosomes. Consistently, most endogenous HMGA2 localized to transposase 5- and DNase I-inaccessible chromatin regions, and its binding was mostly associated with gene repression, in mouse embryonic neocortical cells. The AT-hook 1 domain was necessary for chromatin condensation by HMGA2 in vitro and in cellulo, and an HMGA2 mutant lacking this domain was defective in the ability to maintain neuronal progenitors in vivo. Intrinsically disordered regions of other proteins could substitute for the AT-hook 1 domain in promoting this biological function of HMGA2. Taken together, HMGA2 may regulate neural cell fate by its chromatin condensation activity.
    DOI:  https://doi.org/10.1038/s41467-023-42094-9
  7. Dev Biol. 2023 Oct 05. pii: S0012-1606(23)00169-0. [Epub ahead of print]
      Transcriptional responses to the Hedgehog (HH) signaling pathway are primarily modulated by GLI repression in the mouse limb. Previous studies suggested a role for the BAF chromatin remodeling complex in mediating GLI repression. Consistent with this possibility, the core BAF complex protein SMARCC1 is present at most active limb enhancers including the majority of GLI enhancers. However, in contrast to GLI repression which reduces chromatin accessibility, SMARCC1 maintains chromatin accessibility at most enhancers, including those bound by GLI. Moreover, SMARCC1 binding at GLI-regulated enhancers occurs independently of GLI3. Consistent with previous studies, some individual GLI target genes are mis-regulated in Smarcc1 conditional knockouts, though most GLI target genes are unaffected. Moreover, SMARCC1 is not necessary for mediating constitutive GLI repression in HH mutant limb buds. We conclude that SMARCC1 does not mediate GLI3 repression, which we propose utilizes alternative chromatin remodeling complexes.
    Keywords:  BAF; GLI3; Hedgehog; Limb bud; SWI/SNF; Transcriptional repression
    DOI:  https://doi.org/10.1016/j.ydbio.2023.10.001
  8. Nat Commun. 2023 Oct 13. 14(1): 6433
      Nuclear factors rapidly scan the genome for their targets, but the role of nuclear organization in such search is uncharted. Here we analyzed how multiple factors explore chromatin, combining live-cell single-molecule tracking with multifocal structured illumination of DNA density. We find that factors displaying higher bound fractions sample DNA-dense regions more exhaustively. Focusing on the tumor-suppressor p53, we demonstrate that it searches for targets by alternating between rapid diffusion in the interchromatin compartment and compact sampling of chromatin dense regions. Efficient targeting requires balanced interactions with chromatin: fusing p53 with an exogenous intrinsically disordered region potentiates p53-mediated target gene activation at low concentrations, but leads to condensates at higher levels, derailing its search and downregulating transcription. Our findings highlight the role of disordered regions on factors search and showcase a powerful method to generate traffic maps of the eukaryotic nucleus to dissect how its organization guides nuclear factors action.
    DOI:  https://doi.org/10.1038/s41467-023-42133-5
  9. Cell Rep. 2023 Oct 12. pii: S2211-1247(23)01259-7. [Epub ahead of print]42(10): 113247
      Perturbing the transcriptome of mammalian oocytes results in meiotic failure. We previously reported that RNA-exosome-associated RNase, EXOSC10, degrades unwanted protein-coding RNA and processes ribosomal RNA to ensure proper oocyte maturation. Here, we establish oocyte-specific knockout mice of another RNA-exosome-associated RNase, DIS3. Mutant females (Dis3cKO) exhibit significantly reduced fertility because oocytes arrest after the growth phase. Single-oocyte RNA sequencing (RNA-seq) and CUT&Tag analyses show that DIS3 degrades intergenic RNA and mediates transcription silencing that is essential for chromatin condensation and resumption of meiosis. Dis3cKO oocytes exhibit elevated H3K27me3 in a pre-defined manner due to insufficient demethylation. During oocyte growth, EXOSC10 functions with DIS3 to degrade intergenic RNA. Double-knockout oocytes have earlier growth defects and more accumulated transcripts. We conclude that RNA exosomes synergistically degrade unwanted RNA and mediate transcription termination to ensure transcriptome integrity during oocyte development.
    Keywords:  CP: Molecular biology; RNA degradation; histone modification; mouse oocyte development; pervasive transcription
    DOI:  https://doi.org/10.1016/j.celrep.2023.113247
  10. Stem Cell Reports. 2023 Sep 26. pii: S2213-6711(23)00367-3. [Epub ahead of print]
      Adult neurogenesis occurs in the mammalian olfactory epithelium to maintain populations of neurons that are vulnerable to injury yet essential for olfaction. Multipotent olfactory basal stem cells are activated by damage, although mechanisms regulating lineage decisions are not understood. Using mouse lesion models, we focused on defining the role of Polycomb repressive complexes (PRCs) in olfactory neurogenesis. PRC2 has a well-established role in developing tissues, orchestrating transcriptional programs via chromatin modification. PRC2 proteins are expressed in olfactory globose basal cells (GBCs) and nascent neurons. Conditional PRC2 loss perturbs lesion-induced neuron production, accompanied by altered histone modifications and misexpression of lineage-specific transcription factors in GBCs. De-repression of Sox9 in PRC2-mutant GBCs is accompanied by increased Bowman's gland production, defining an unrecognized role for PRC2 in regulating gland versus neuron cell fate. Our findings support a model for PRC2-dependent mechanisms promoting sensory neuronal differentiation in an adult neurogenic niche.
    Keywords:  Bowman's gland; Polycomb; cell fate; neurogenesis; olfaction; stem cells
    DOI:  https://doi.org/10.1016/j.stemcr.2023.09.008
  11. Methods Mol Biol. 2024 ;2694 29-55
      The dynamics of histone-DNA interactions govern chromosome organization and regulates the processes of transcription, replication, and repair. Accurate measurements of the energies and the kinetics of DNA binding to component histones of the nucleosome under a variety of conditions are essential to understand these processes at the molecular level. To accomplish this, we employ three specific single-molecule techniques: force disruption (FD) with optical tweezers, confocal imaging (CI) in a combined fluorescence plus optical trap, and survival probability (SP) measurements of disrupted and reformed nucleosomes. Short arrays of positioned nucleosomes serve as a template for study, facilitating rapid quantification of kinetic parameters. These arrays are then exposed to FACT (FAcilitates Chromatin Transcription), a non-ATP-driven heterodimeric nuclear chaperone known to both disrupt and tether histones during transcription. FACT binding drives off the outer wrap of DNA and destabilizes the histone-DNA interactions of the inner wrap as well. This reorganization is driven by two key domains with distinct function. FD experiments show the SPT16 MD domain stabilizes DNA-histone contacts, while the HMGB box of SSRP1 binds DNA, destabilizing the nucleosome. Surprisingly, CI experiments do not show tethering of disrupted histones, but increased rates of histone release from the DNA. SI experiments resolve this, showing that the two active domains of FACT combine to chaperone nucleosome reassembly after the timely release of force. These combinations of single-molecule approaches show FACT is a true nucleosome catalyst, lowering the barrier to both disruption and reformation.
    Keywords:  AFM; Chromatin; Confocal fluorescence; DNA; FACT; Histones; Nucleosomes; Optical tweezers
    DOI:  https://doi.org/10.1007/978-1-0716-3377-9_2
  12. Mol Plant. 2023 Oct 10. pii: S1674-2052(23)00320-9. [Epub ahead of print]
      Histone H2A monoubiquitination is associated with transcriptional repression and needs to be removed by deubiquitinases to facilitate gene transcription in eukaryotes. However, the deubiquitinase responsible for genome-wide H2A deubiquitination in plants has yet to be identified. We found that the previously identified PEAT (PWWP-EPCR-ARID-TRB) complex components interact with both the ubiquitin-specific protease UBP5 and the redundant histone acetyltransferases HAM1 and HAM2 (HAM1/2) and thereby form a larger version of PEAT complex in Arabidopsis thaliana. UBP5 functions as an H2A deubiquitinase in a nucleosome substrate-dependent manner in vitro and mediates H2A deubiquitination at the whole-genome level in vivo. HAM1/2 are shared subunits of the PEAT complex and the conserved NuA4 histone acetyltransferase complex and are responsible for histone H4K5 acetylation. Within the PEAT complex, the PWWP components (PWWP1, PWWP2 and PWWP3) directly interact with UBP5 and are necessary for UBP5-mediated H2A deubiquitination, while the EPCR components (EPCR1 and EPCR2) directly interact with HAM1/2 and are required for HAM1/2-mediated H4K5 acetylation. This study not only identifies dual roles of the PEAT complex in H2A deubiquitination and H4K5 acetylation but also illustrates how these processes collaborate at the whole-genome level to regulate transcription and development in plants.
    Keywords:  H2A deubiquitination; H4K5 acetylation; HAM1; NuA4; PEAT; UBP5; histone
    DOI:  https://doi.org/10.1016/j.molp.2023.10.006
  13. Curr Protoc. 2023 Oct;3(10): e899
      Cis-regulatory elements (cREs) and their long-range interactions are crucial for spatial-temporal gene regulation. While cREs can be characterized as accessible chromatin sequences, comprehensively identifying their spatial interactions remains a challenge. We recently developed a method, HiCAR (Hi-C on Accessible Regulatory DNA), which combines Tn5 transposase and chromatin proximity ligation to analyze open chromatin-anchored interactions in low-input cells. Application of HiCAR in human embryonic stem cells and lymphoblastoid cells reveals high-resolution chromatin contacts with efficiency comparable to in situ Hi-C across various distance ranges. Moreover, HiCAR was successfully applied to 30,000 primary human muscle stem cells, showcasing its potential for analyzing chromatin accessibility and looping in low-input primary cells and clinical samples. Here, we provide a detailed step-by-step protocol to perform the updated HiCAR experiments. © 2023 Wiley Periodicals LLC. Basic Protocol 1: Tn5 Transposase Assembly Basic Protocol 2: HiCAR Library Preparation.
    Keywords:  Tn5; chromatin accessibility; chromatin interaction; chromosome conformation capture; restriction enzyme
    DOI:  https://doi.org/10.1002/cpz1.899
  14. BMC Genomics. 2023 Oct 13. 24(1): 614
       BACKGROUND: Chromosomal compartmentalization plays a critical role in maintaining proper transcriptional programs in cell differentiation and oncogenesis. However, currently the prevalent method for comparative analysis of compartmentalization landscapes between different cell types is limited to the qualitative switched compartments.
    RESULTS: To identify genomic regions with quantitatively differential compartmentalization changes from genome-wide chromatin conformation data like Hi-C, we developed a computational framework named DARIC. DARIC includes three modules: compartmentalization quantification, normalization, and differential analysis. Comparing DARIC with the conventional compartment switching analysis reveals substantial regions characterized by quantitatively significant compartmentalization changes without switching. These changes are accompanied by changes in gene expression, chromatin accessibility, H3K27ac intensity, as well as the interactions with nuclear lamina proteins and nuclear positioning, highlighting the functional importance of such quantitative changes in gene regulation. We applied DARIC to dissect the quantitative compartmentalization changes during human cardiomyocyte differentiation and identified two distinct mechanisms for gene activation based on the association with compartmentalization changes. Using the quantitative compartmentalization measurement module from DARIC, we further dissected the compartment variability landscape in the human genome by analyzing a compendium of 32 Hi-C datasets from 4DN. We discovered an interesting correlation between compartmentalization variability and sub-compartments.
    CONCLUSIONS: DARIC is a useful tool for analyzing quantitative compartmentalization changes and mining novel biological insights from increasing Hi-C data. Our results demonstrate the functional significance of quantitative compartmentalization changes in gene regulation, and provide new insights into the relationship between compartmentalization variability and sub-compartments in the human genome.
    Keywords:  3D genome; Compartment; Compartmentalization; Gene regulation; Hi-C; Nuclear positioning
    DOI:  https://doi.org/10.1186/s12864-023-09675-w
  15. J Mol Biol. 2023 Oct 05. pii: S0022-2836(23)00419-9. [Epub ahead of print] 168308
      Pioneer factors, which can directly bind to nucleosomes, have been considered to change chromatin conformations. However, the binding impact on the nucleosome is little known. Here, we show how the pioneer factor GATA3 binds to nucleosomal DNA and affects the conformation and dynamics of nucleosomes by using a combination of SAXS, molecular modeling, and molecular dynamics simulations. Our structural models, consistent with the SAXS data, indicate that only one of the two DNA binding domains, N- and C-fingers, of GATA3 binds to an end of the DNA in solution. Our MD simulations further showed that the other unbound end of the DNA increases the fluctuation and enhances the DNA dissociation from the histone core when the N-finger binds to a DNA end, a site near the entry or exit of the nucleosome. However, this was not true for the binding of the C-finger that binds to a location about 15 base pairs distant from the DNA end. In this case, DNA dissociation occurred on the bound end. Taken together, we suggest that the N-finger and C-finger bindings of GATA3 commonly enhance DNA dissociation at one of the two DNA ends (the bound end for the C-finger binding and the unbound end for the N-finger binding), leading to triggering a conformational change in the chromatin.
    Keywords:  GATA3; SAXS; asymmetric unwrapping; dynamics; nucleosome; pioneer factor
    DOI:  https://doi.org/10.1016/j.jmb.2023.168308
  16. Nat Microbiol. 2023 Oct 12.
      Trypanosomes are eukaryotic, unicellular parasites, such as Trypanosoma brucei, which causes sleeping sickness, and Trypanosoma cruzi, which causes Chagas disease. Genomes of these parasites comprise core regions and species-specific disruptive regions that encode multigene families of surface glycoproteins. Few transcriptional regulators have been identified in these parasites, and the role of spatial organization of the genome in gene expression is unclear. Here we mapped genome-wide chromatin interactions in T. cruzi using chromosome conformation capture (Hi-C), and we show that the core and disruptive regions form three-dimensional chromatin compartments named C and D. These chromatin compartments differ in levels of DNA methylation, nucleosome positioning and chromatin interactions, affecting genome expression dynamics. Our data reveal that the trypanosome genome is organized into chromatin-folding domains and transcription is affected by the local chromatin structure. We propose a model in which epigenetic mechanisms affect gene expression in trypanosomes.
    DOI:  https://doi.org/10.1038/s41564-023-01483-y
  17. Nucleic Acids Res. 2023 Oct 09. pii: gkad798. [Epub ahead of print]
      The human brain is a complex organ comprised of distinct cell types, and the contribution of the 3D genome to lineage specific gene expression remains poorly understood. To decipher cell type specific genome architecture, and characterize fine scale changes in the chromatin interactome across neural development, we compared the 3D genome of the human fetal cortical plate to that of neurons and glia isolated from the adult prefrontal cortex. We found that neurons have weaker genome compartmentalization compared to glia, but stronger TADs, which emerge during fetal development. Furthermore, relative to glia, the neuronal genome shifts more strongly towards repressive compartments. Neurons have differential TAD boundaries that are proximal to active promoters involved in neurodevelopmental processes. CRISPRi on CNTNAP2 in hIPSC-derived neurons reveals that transcriptional inactivation correlates with loss of insulation at the differential boundary. Finally, re-wiring of chromatin loops during neural development is associated with transcriptional and functional changes. Importantly, differential loops in the fetal cortex are associated with autism GWAS loci, suggesting a neuropsychiatric disease mechanism affecting the chromatin interactome. Furthermore, neural development involves gaining enhancer-promoter loops that upregulate genes that control synaptic activity. Altogether, our study provides multi-scale insights on the 3D genome in the human brain.
    DOI:  https://doi.org/10.1093/nar/gkad798
  18. Nucleic Acids Res. 2023 Oct 12. pii: gkad793. [Epub ahead of print]
      Chromatin association of the BRCA1-BARD1 heterodimer is critical to promote homologous recombination repair of DNA double-strand breaks (DSBs) in S/G2. How the BRCA1-BARD1 complex interacts with chromatin that contains both damage induced histone H2A ubiquitin and inhibitory H4K20 methylation is not fully understood. We characterised BRCA1-BARD1 binding and enzymatic activity to an array of mono- and di-nucleosome substrates using biochemical, structural and single molecule imaging approaches. We found that the BRCA1-BARD1 complex preferentially interacts and modifies di-nucleosomes over mono-nucleosomes, allowing integration of H2A Lys-15 ubiquitylation signals with other chromatin modifications and features. Using high speed- atomic force microscopy (HS-AFM) to monitor how the BRCA1-BARD1 complex recognises chromatin in real time, we saw a highly dynamic complex that bridges two nucleosomes and associates with the DNA linker region. Bridging is aided by multivalent cross-nucleosome interactions that enhance BRCA1-BARD1 E3 ubiquitin ligase catalytic activity. Multivalent interactions across nucleosomes explain how BRCA1-BARD1 can recognise chromatin that retains partial di-methylation at H4 Lys-20 (H4K20me2), a parental histone mark that blocks BRCA1-BARD1 interaction with nucleosomes, to promote its enzymatic and DNA repair activities.
    DOI:  https://doi.org/10.1093/nar/gkad793
  19. Nat Methods. 2023 Oct 09.
      Engineered transactivation domains (TADs) combined with programmable DNA binding platforms have revolutionized synthetic transcriptional control. Despite recent progress in programmable CRISPR-Cas-based transactivation (CRISPRa) technologies, the TADs used in these systems often contain poorly tolerated elements and/or are prohibitively large for many applications. Here, we defined and optimized minimal TADs built from human mechanosensitive transcription factors. We used these components to construct potent and compact multipartite transactivation modules (MSN, NMS and eN3x9) and to build the CRISPR-dCas9 recruited enhanced activation module (CRISPR-DREAM) platform. We found that CRISPR-DREAM was specific and robust across mammalian cell types, and efficiently stimulated transcription from diverse regulatory loci. We also showed that MSN and NMS were portable across Type I, II and V CRISPR systems, transcription activator-like effectors and zinc finger proteins. Further, as proofs of concept, we used dCas9-NMS to efficiently reprogram human fibroblasts into induced pluripotent stem cells and demonstrated that mechanosensitive transcription factor TADs are efficacious and well tolerated in therapeutically important primary human cell types. Finally, we leveraged the compact and potent features of these engineered TADs to build dual and all-in-one CRISPRa AAV systems. Altogether, these compact human TADs, fusion modules and delivery architectures should be valuable for synthetic transcriptional control in biomedical applications.
    DOI:  https://doi.org/10.1038/s41592-023-02036-1
  20. Nucleic Acids Res. 2023 Oct 11. pii: gkad825. [Epub ahead of print]
      Various transcript elongation factors (TEFs) including modulators of RNA polymerase II (RNAPII) activity and histone chaperones tune the efficiency of transcription in the chromatin context. TEFs are involved in establishing gene expression patterns during growth and development in Arabidopsis, while little is known about the genomic distribution of the TEFs and the way they facilitate transcription. We have mapped the genome-wide occupancy of the elongation factors SPT4-SPT5, PAF1C and FACT, relative to that of elongating RNAPII phosphorylated at residues S2/S5 within the carboxyterminal domain. The distribution of SPT4-SPT5 along transcribed regions closely resembles that of RNAPII-S2P, while the occupancy of FACT and PAF1C is rather related to that of RNAPII-S5P. Under transcriptionally challenging heat stress conditions, mutant plants lacking the corresponding TEFs are differentially impaired in transcript synthesis. Strikingly, in plants deficient in PAF1C, defects in transcription across intron/exon borders are observed that are cumulative along transcribed regions. Upstream of transcriptional start sites, the presence of FACT correlates with nucleosomal occupancy. Under stress conditions FACT is particularly required for transcriptional upregulation and to promote RNAPII transcription through +1 nucleosomes. Thus, Arabidopsis TEFs are differently distributed along transcribed regions, and are distinctly required during transcript elongation especially upon transcriptional reprogramming.
    DOI:  https://doi.org/10.1093/nar/gkad825