bims-crepig Biomed News
on Chromatin regulation and epigenetics in cell fate and cancer
Issue of 2023‒08‒13
nineteen papers selected by
Connor Rogerson
University of Cambridge


  1. Dev Cell. 2023 Aug 03. pii: S1534-5807(23)00347-7. [Epub ahead of print]
      Chromatin accessibility is integral to the process by which transcription factors (TFs) read out cis-regulatory DNA sequences, but it is difficult to differentiate between TFs that drive accessibility and those that do not. Deep learning models that learn complex sequence rules provide an unprecedented opportunity to dissect this problem. Using zygotic genome activation in Drosophila as a model, we analyzed high-resolution TF binding and chromatin accessibility data with interpretable deep learning and performed genetic validation experiments. We identify a hierarchical relationship between the pioneer TF Zelda and the TFs involved in axis patterning. Zelda consistently pioneers chromatin accessibility proportional to motif affinity, whereas patterning TFs augment chromatin accessibility in sequence contexts where they mediate enhancer activation. We conclude that chromatin accessibility occurs in two tiers: one through pioneering, which makes enhancers accessible but not necessarily active, and the second when the correct combination of TFs leads to enhancer activation.
    Keywords:  ATAC-seq; BPNet; ChIP-nexus; Drosophila development; Zelda; chromatin accessibility; enhancers; interpretable deep learning; pioneer factors; transcription factors
    DOI:  https://doi.org/10.1016/j.devcel.2023.07.007
  2. Nat Commun. 2023 Aug 10. 14(1): 4848
      Binding of transcription factors (TFs) promotes the subsequent recruitment of coactivators and preinitiation complexes to initiate eukaryotic transcription, but this time course is usually not visualized. It is commonly assumed that recruited factors eventually co-reside in a higher-order structure, allowing distantly bound TFs to activate transcription at core promoters. We use live imaging of endogenously tagged proteins, including the pioneer TF Zelda, the coactivator dBrd4, and RNA polymerase II (RNAPII), to define a cascade of events upstream of transcriptional initiation in early Drosophila embryos. These factors are sequentially and transiently recruited to discrete clusters during activation of non-histone genes. Zelda and the acetyltransferase dCBP nucleate dBrd4 clusters, which then trigger pre-transcriptional clustering of RNAPII. Subsequent transcriptional elongation disperses clusters of dBrd4 and RNAPII. Our results suggest that activation of transcription by eukaryotic TFs involves a succession of distinct biomolecular condensates that culminates in a self-limiting burst of transcription.
    DOI:  https://doi.org/10.1038/s41467-023-40485-6
  3. Mol Cell. 2023 Aug 01. pii: S1097-2765(23)00523-3. [Epub ahead of print]
      CTCF is a critical regulator of genome architecture and gene expression that binds thousands of sites on chromatin. CTCF genomic localization is controlled by the recognition of a DNA sequence motif and regulated by DNA modifications. However, CTCF does not bind to all its potential sites in all cell types, raising the question of whether the underlying chromatin structure can regulate CTCF occupancy. Here, we report that R-loops facilitate CTCF binding through the formation of associated G-quadruplex (G4) structures. R-loops and G4s co-localize with CTCF at many genomic regions in mouse embryonic stem cells and promote CTCF binding to its cognate DNA motif in vitro. R-loop attenuation reduces CTCF binding in vivo. Deletion of a specific G4-forming motif in a gene reduces CTCF binding and alters gene expression. Conversely, chemical stabilization of G4s results in CTCF gains and accompanying alterations in chromatin organization, suggesting a pivotal role for G4 structures in reinforcing long-range genome interactions through CTCF.
    Keywords:  CTCF; G-quadruplex; R-loops; genome organization
    DOI:  https://doi.org/10.1016/j.molcel.2023.07.009
  4. Nat Commun. 2023 08 05. 14(1): 4716
      The inability of adult human cardiomyocytes to proliferate is an obstacle to efficient cardiac regeneration after injury. Understanding the mechanisms that drive postnatal cardiomyocytes to switch to a non-regenerative state is therefore of great significance. Here we show that Arid1a, a subunit of the switching defective/sucrose non-fermenting (SWI/SNF) chromatin remodeling complex, suppresses postnatal cardiomyocyte proliferation while enhancing maturation. Genome-wide transcriptome and epigenome analyses revealed that Arid1a is required for the activation of a cardiomyocyte maturation gene program by promoting DNA access to transcription factors that drive cardiomyocyte maturation. Furthermore, we show that ARID1A directly binds and inhibits the proliferation-promoting transcriptional coactivators YAP and TAZ, indicating ARID1A sequesters YAP/TAZ from their DNA-binding partner TEAD. In ischemic heart disease, Arid1a expression is enhanced in cardiomyocytes of the border zone region. Inactivation of Arid1a after ischemic injury enhanced proliferation of border zone cardiomyocytes. Our study illuminates the pivotal role of Arid1a in cardiomyocyte maturation, and uncovers Arid1a as a crucial suppressor of cardiomyocyte proliferation.
    DOI:  https://doi.org/10.1038/s41467-023-40203-2
  5. Genome Biol. 2023 08 07. 24(1): 181
      BACKGROUND: Although spatial organization of compartments and topologically associating domains at large scale is relatively well studied, the spatial organization of regulatory elements at fine scale is poorly understood in plants.RESULTS: Here we perform high-resolution chromatin interaction analysis using paired-end tag sequencing approach. We map chromatin interactions tethered with RNA polymerase II and associated with heterochromatic, transcriptionally active, and Polycomb-repressive histone modifications in Arabidopsis. Analysis of the regulatory repertoire shows that distal active cis-regulatory elements are linked to their target genes through long-range chromatin interactions with increased expression of the target genes, while poised cis-regulatory elements are linked to their target genes through long-range chromatin interactions with depressed expression of the target genes. Furthermore, we demonstrate that transcription factor MYC2 is critical for chromatin spatial organization, and propose that MYC2 occupancy and MYC2-mediated chromatin interactions coordinately facilitate transcription within the framework of 3D chromatin architecture. Analysis of functionally related gene-defined chromatin connectivity networks reveals that genes implicated in flowering-time control are functionally compartmentalized into separate subdomains via their spatial activity in the leaf or shoot apical meristem, linking active mark- or Polycomb-repressive mark-associated chromatin conformation to coordinated gene expression.
    CONCLUSION: The results reveal that the regulation of gene transcription in Arabidopsis is not only by linear juxtaposition, but also by long-range chromatin interactions. Our study uncovers the fine scale genome organization of Arabidopsis and the potential roles of such organization in orchestrating transcription and development.
    Keywords:  Arabidopsis; ChIA-PET; Chromatin architecture; Transcriptional regulation
    DOI:  https://doi.org/10.1186/s13059-023-03018-4
  6. Cell Rep. 2023 Aug 09. pii: S2211-1247(23)00978-6. [Epub ahead of print]42(8): 112967
      PTEN loss in fetal liver hematopoietic stem cells (HSCs) leads to alterations in myeloid, T-, and B-lineage potentials and T-lineage acute lymphoblastic leukemia (T-ALL) development. To explore the mechanism underlying PTEN-regulated hematopoietic lineage choices, we carry out integrated assay for transposase-accessible chromatin using sequencing (ATAC-seq), single-cell RNA-seq, and in vitro culture analyses using in vivo-isolated mouse pre-leukemic HSCs and progenitors. We find that PTEN loss alters chromatin accessibility of key lineage transcription factor (TF) binding sites at the prepro-B stage, corresponding to increased myeloid and T-lineage potentials and reduced B-lineage potential. Importantly, we find that PU.1 is an essential TF downstream of PTEN and that altering PU.1 levels can reprogram the chromatin accessibility landscape and myeloid, T-, and B-lineage potentials in Ptennull prepro-B cells. Our study discovers prepro-B as the key developmental stage underlying PTEN-regulated hematopoietic lineage choices and suggests a critical role of PU.1 in modulating the epigenetic state and lineage plasticity of prepro-B progenitors.
    Keywords:  CP: Immunology; CP: Molecular biology; PTEN; PU.1; chromatin accessibility; lineage plasticity
    DOI:  https://doi.org/10.1016/j.celrep.2023.112967
  7. iScience. 2023 Aug 18. 26(8): 107360
      Lineage switching can induce therapy resistance in cancer. Yet, how lineage fidelity is maintained and how it can be lost remain poorly understood. Here, we have used CRISPR-Cas9-based genetic screening to demonstrate that loss of SMARCB1, a member of the SWI/SNF chromatin remodeling complex, can confer an advantage to clear cell renal cell carcinoma (ccRCC) cells upon inhibition of the renal lineage factor PAX8. Lineage factor inhibition-resistant ccRCC cells formed tumors with morphological features, but not molecular markers, of neuroendocrine differentiation. SMARCB1 inactivation led to large-scale loss of kidney-specific epigenetic programs and restoration of proliferative capacity through the adoption of new dependencies on factors that represent rare essential genes across different cancers. We further developed an analytical approach to systematically characterize lineage fidelity using large-scale CRISPR-Cas9 data. An understanding of the rules that govern lineage switching could aid the development of more durable lineage factor-targeted and other cancer therapies.
    Keywords:  Cancer; Cellular physiology; Human genetics; Medical microbiology
    DOI:  https://doi.org/10.1016/j.isci.2023.107360
  8. Proc Natl Acad Sci U S A. 2023 08 15. 120(33): e2220472120
      Dysregulation of histone lysine methyltransferases and demethylases is one of the major mechanisms driving the epigenetic reprogramming of transcriptional networks in castration-resistant prostate cancer (CRPC). In addition to their canonical histone targets, some of these factors can modify critical transcription factors, further impacting oncogenic transcription programs. Our recent report demonstrated that LSD1 can demethylate the lysine 270 of FOXA1 in prostate cancer (PCa) cells, leading to the stabilization of FOXA1 chromatin binding. This process enhances the activities of the androgen receptor and other transcription factors that rely on FOXA1 as a pioneer factor. However, the identity of the methyltransferase responsible for FOXA1 methylation and negative regulation of the FOXA1-LSD1 oncogenic axis remains unknown. SETD7 was initially identified as a transcriptional activator through its methylation of histone 3 lysine 4, but its function as a methyltransferase on nonhistone substrates remains poorly understood, particularly in the context of PCa progression. In this study, we reveal that SETD7 primarily acts as a transcriptional repressor in CRPC cells by functioning as the major methyltransferase targeting FOXA1-K270. This methylation disrupts FOXA1-mediated transcription. Consistent with its molecular function, we found that SETD7 confers tumor suppressor activity in PCa cells. Moreover, loss of SETD7 expression is significantly associated with PCa progression and tumor aggressiveness. Overall, our study provides mechanistic insights into the tumor-suppressive and transcriptional repression activities of SETD7 in mediating PCa progression and therapy resistance.
    Keywords:  FOXA1; LSD1; SETD7; lysine methylation; prostate cancer
    DOI:  https://doi.org/10.1073/pnas.2220472120
  9. Nat Struct Mol Biol. 2023 Aug 10.
      We previously reported Paired-Tag, a combinatorial indexing-based method that can simultaneously map histone modifications and gene expression at single-cell resolution at scale. However, the lengthy procedure of Paired-Tag has hindered its general adoption in the community. To address this bottleneck, we developed a droplet-based Paired-Tag protocol that is faster and more accessible than the previous method. Using cultured mammalian cells and primary brain tissues, we demonstrate its superior performance at identifying candidate cis-regulatory elements and associating their dynamic chromatin state to target gene expression in each constituent cell type in a complex tissue.
    DOI:  https://doi.org/10.1038/s41594-023-01060-1
  10. Cell Syst. 2023 Aug 02. pii: S2405-4712(23)00186-2. [Epub ahead of print]
      Despite growing knowledge of the functions of individual human transcriptional effector domains, much less is understood about how multiple effector domains within the same protein combine to regulate gene expression. Here, we measure transcriptional activity for 8,400 effector domain combinations by recruiting them to reporter genes in human cells. In our assay, weak and moderate activation domains synergize to drive strong gene expression, whereas combining strong activators often results in weaker activation. In contrast, repressors combine linearly and produce full gene silencing, and repressor domains often overpower activation domains. We use this information to build a synthetic transcription factor whose function can be tuned between repression and activation independent of recruitment to target genes by using a small-molecule drug. Altogether, we outline the basic principles of how effector domains combine to regulate gene expression and demonstrate their value in building precise and flexible synthetic biology tools. A record of this paper's transparent peer review process is included in the supplemental information.
    Keywords:  eukaryotic gene regulation; high-throughput screening; mammalian synthetic biology; systems biology; transcriptional effector domains
    DOI:  https://doi.org/10.1016/j.cels.2023.07.001
  11. Genes Dev. 2023 Aug 08.
      Polycomb group (PcG) proteins maintain the repressed state of lineage-inappropriate genes and are therefore essential for embryonic development and adult tissue homeostasis. One critical function of PcG complexes is modulating chromatin structure. Canonical Polycomb repressive complex 1 (cPRC1), particularly its component CBX2, can compact chromatin and phase-separate in vitro. These activities are hypothesized to be critical for forming a repressed physical environment in cells. While much has been learned by studying these PcG activities in cell culture models, it is largely unexplored how cPRC1 regulates adult stem cells and their subsequent differentiation in living animals. Here, we show in vivo evidence of a critical nonenzymatic repressive function of cPRC1 component CBX2 in the male germline. CBX2 is up-regulated as spermatogonial stem cells differentiate and is required to repress genes that were active in stem cells. CBX2 forms condensates (similar to previously described Polycomb bodies) that colocalize with target genes bound by CBX2 in differentiating spermatogonia. Single-cell analyses of mosaic Cbx2 mutant testes show that CBX2 is specifically required to produce differentiating A1 spermatogonia. Furthermore, the region of CBX2 responsible for compaction and phase separation is needed for the long-term maintenance of male germ cells in the animal. These results emphasize that the regulation of chromatin structure by CBX2 at a specific stage of spermatogenesis is critical, which distinguishes this from a mechanism that is reliant on histone modification.
    Keywords:  Polycomb body; Polycomb repressive complex 1; adult stem cell; chromatin compaction; phase separation; spermatogonia
    DOI:  https://doi.org/10.1101/gad.350393.122
  12. Cell. 2023 Aug 01. pii: S0092-8674(23)00745-6. [Epub ahead of print]
      A ubiquitous feature of eukaryotic transcriptional regulation is cooperative self-assembly between transcription factors (TFs) and DNA cis-regulatory motifs. It is thought that this strategy enables specific regulatory connections to be formed in gene networks between otherwise weakly interacting, low-specificity molecular components. Here, using synthetic gene circuits constructed in yeast, we find that high regulatory specificity can emerge from cooperative, multivalent interactions among artificial zinc-finger-based TFs. We show that circuits "wired" using the strategy of cooperative TF assembly are effectively insulated from aberrant misregulation of the host cell genome. As we demonstrate in experiments and mathematical models, this mechanism is sufficient to rescue circuit-driven fitness defects, resulting in genetic and functional stability of circuits in long-term continuous culture. Our naturally inspired approach offers a simple, generalizable means for building high-fidelity, evolutionarily robust gene circuits that can be scaled to a wide range of host organisms and applications.
    Keywords:  cooperativity; fitness; gene circuits; gene regulation; modeling; specificity; synthetic biology; transcription factor; yeast; zinc fingers
    DOI:  https://doi.org/10.1016/j.cell.2023.07.012
  13. EMBO J. 2023 Aug 11. e113639
      WRKY transcription factors in plants are known to be able to mediate either transcriptional activation or repression, but the mechanism regulating their transcriptional activity is largely unclear. We found that group IId WRKY transcription factors interact with OBERON (OBE) proteins, forming redundant WRKY-OBE complexes in Arabidopsis thaliana. The coiled-coil domain of WRKY transcription factors binds to OBE proteins and is responsible for target gene selection and transcriptional repression. The PHD finger of OBE proteins binds to both histones and WRKY transcription factors. WRKY-OBE complexes repress the transcription of numerous stress-responsive genes and are required for maintaining normal plant growth. Several WRKY and OBE mutants show reduced plant size and increased drought tolerance, accompanied by increased expression of stress-responsive genes. Moreover, expression levels of most of these WRKY and OBE genes are reduced in response to drought stress, revealing a previously uncharacterized regulatory mechanism of the drought stress response. These results suggest that WRKY-OBE complexes repress transcription of stress-responsive genes, and thereby balance plant growth and stress tolerance.
    Keywords:  development; histone; stress tolerance; transcription factor; transcriptional repression
    DOI:  https://doi.org/10.15252/embj.2023113639
  14. Genome Biol. 2023 Aug 10. 24(1): 185
      BACKGROUND: Cleavage Under Targets and Release Using Nuclease (CUT&RUN) is an increasingly popular technique to map genome-wide binding profiles of histone modifications, transcription factors, and co-factors. The ENCODE project and others have compiled blacklists for ChIP-seq which have been widely adopted: these lists contain regions of high and unstructured signal, regardless of cell type or protein target, indicating that these are false positives. While CUT&RUN obtains similar results to ChIP-seq, its biochemistry and subsequent data analyses are different. We found that this results in a CUT&RUN-specific set of undesired high-signal regions.RESULTS: We compile suspect lists based on CUT&RUN data for the human and mouse genomes, identifying regions consistently called as peaks in negative controls. Using published CUT&RUN data from our and other labs, we show that the CUT&RUN suspect regions can persist even when peak calling is performed with SEACR or MACS2 against a negative control and after ENCODE blacklist removal. Moreover, we experimentally validate the CUT&RUN suspect lists by performing reiterative negative control experiments in which no specific protein is targeted, showing that they capture more than 80% of the peaks identified.
    CONCLUSIONS: We propose that removing these problematic regions can substantially improve peak calling in CUT&RUN experiments, resulting in more reliable datasets.
    Keywords:  Bioinformatics; Blacklist; CUT&RUN; Chromatin; Peak calling; Suspect list
    DOI:  https://doi.org/10.1186/s13059-023-03027-3
  15. Nat Aging. 2023 Aug 10.
    A T Lu, Z Fei, A Haghani, T R Robeck, J A Zoller, C Z Li, R Lowe, Q Yan, J Zhang, H Vu, J Ablaeva, V A Acosta-Rodriguez, D M Adams, J Almunia, A Aloysius, R Ardehali, A Arneson, C S Baker, G Banks, K Belov, N C Bennett, P Black, D T Blumstein, E K Bors, C E Breeze, R T Brooke, J L Brown, G G Carter, A Caulton, J M Cavin, L Chakrabarti, I Chatzistamou, H Chen, K Cheng, P Chiavellini, O W Choi, S M Clarke, L N Cooper, M L Cossette, J Day, J DeYoung, S DiRocco, C Dold, E E Ehmke, C K Emmons, S Emmrich, E Erbay, C Erlacher-Reid, C G Faulkes, S H Ferguson, C J Finno, J E Flower, J M Gaillard, E Garde, L Gerber, V N Gladyshev, V Gorbunova, R G Goya, M J Grant, C B Green, E N Hales, M B Hanson, D W Hart, M Haulena, K Herrick, A N Hogan, C J Hogg, T A Hore, T Huang, J C Izpisua Belmonte, A J Jasinska, G Jones, E Jourdain, O Kashpur, H Katcher, E Katsumata, V Kaza, H Kiaris, M S Kobor, P Kordowitzki, W R Koski, M Krützen, S B Kwon, B Larison, S G Lee, M Lehmann, J F Lemaitre, A J Levine, C Li, X Li, A R Lim, D T S Lin, D M Lindemann, T J Little, N Macoretta, D Maddox, C O Matkin, J A Mattison, M McClure, J Mergl, J J Meudt, G A Montano, K Mozhui, J Munshi-South, A Naderi, M Nagy, P Narayan, P W Nathanielsz, N B Nguyen, C Niehrs, J K O'Brien, P O'Tierney Ginn, D T Odom, A G Ophir, S Osborn, E A Ostrander, K M Parsons, K C Paul, M Pellegrini, K J Peters, A B Pedersen, J L Petersen, D W Pietersen, G M Pinho, J Plassais, J R Poganik, N A Prado, P Reddy, B Rey, B R Ritz, J Robbins, M Rodriguez, J Russell, E Rydkina, L L Sailer, A B Salmon, A Sanghavi, K M Schachtschneider, D Schmitt, T Schmitt, L Schomacher, L B Schook, K E Sears, A W Seifert, A Seluanov, A B A Shafer, D Shanmuganayagam, A V Shindyapina, M Simmons, K Singh, I Sinha, J Slone, R G Snell, E Soltanmaohammadi, M L Spangler, M C Spriggs, L Staggs, N Stedman, K J Steinman, D T Stewart, V J Sugrue, B Szladovits, J S Takahashi, M Takasugi, E C Teeling, M J Thompson, B Van Bonn, S C Vernes, D Villar, H V Vinters, M C Wallingford, N Wang, R K Wayne, G S Wilkinson, C K Williams, R W Williams, X W Yang, M Yao, B G Young, B Zhang, Z Zhang, P Zhao, Y Zhao, W Zhou, J Zimmermann, J Ernst, K Raj, S Horvath.
      Aging, often considered a result of random cellular damage, can be accurately estimated using DNA methylation profiles, the foundation of pan-tissue epigenetic clocks. Here, we demonstrate the development of universal pan-mammalian clocks, using 11,754 methylation arrays from our Mammalian Methylation Consortium, which encompass 59 tissue types across 185 mammalian species. These predictive models estimate mammalian tissue age with high accuracy (r > 0.96). Age deviations correlate with human mortality risk, mouse somatotropic axis mutations and caloric restriction. We identified specific cytosines with methylation levels that change with age across numerous species. These sites, highly enriched in polycomb repressive complex 2-binding locations, are near genes implicated in mammalian development, cancer, obesity and longevity. Our findings offer new evidence suggesting that aging is evolutionarily conserved and intertwined with developmental processes across all mammals.
    DOI:  https://doi.org/10.1038/s43587-023-00462-6
  16. Nat Commun. 2023 08 09. 14(1): 4816
      Cholesterol biosynthesis is a highly regulated, oxygen-dependent pathway, vital for cell membrane integrity and growth. In fungi, the dependency on oxygen for sterol production has resulted in a shared transcriptional response, resembling prolyl hydroxylation of Hypoxia Inducible Factors (HIFs) in metazoans. Whether an analogous metazoan pathway exists is unknown. Here, we identify Sterol Regulatory Element Binding Protein 2 (SREBP2), the key transcription factor driving sterol production in mammals, as an oxygen-sensitive regulator of cholesterol synthesis. SREBP2 degradation in hypoxia overrides the normal sterol-sensing response, and is HIF independent. We identify MARCHF6, through its NADPH-mediated activation in hypoxia, as the main ubiquitin ligase controlling SREBP2 stability. Hypoxia-mediated degradation of SREBP2 protects cells from statin-induced cell death by forcing cells to rely on exogenous cholesterol uptake, explaining why many solid organ tumours become auxotrophic for cholesterol. Our findings therefore uncover an oxygen-sensitive pathway for governing cholesterol synthesis through regulated SREBP2-dependent protein degradation.
    DOI:  https://doi.org/10.1038/s41467-023-40541-1
  17. Cell Rep. 2023 Aug 07. pii: S2211-1247(23)00948-8. [Epub ahead of print]42(8): 112937
      Lineage plasticity is a form of therapy-induced drug resistance. In prostate cancer, androgen receptor (AR) pathway inhibitors potentially lead to the accretion of tumor relapse with loss of AR signaling and a shift from a luminal state to an alternate program. However, the molecular and signaling mechanisms orchestrating the development of lineage plasticity under the pressure of AR-targeted therapies are not fully understood. Here, a survey of receptor tyrosine kinases (RTKs) identifies ROR2 as the top upregulated RTK following AR pathway inhibition, which feeds into lineage plasticity by promoting stem-cell-like and neuronal networks. Mechanistically, ROR2 activates the ERK/CREB signaling pathway to modulate the expression of the lineage commitment transcription factor ASCL1. Collectively, our findings nominate ROR2 as a potential therapeutic target to reverse the ENZ-induced plastic phenotype and potentially re-sensitize tumors to AR pathway inhibitors.
    Keywords:  ASCL1; CP: Cancer; CREB; ROR2; cellular plasticity; neuroendocrine; prostate cancer
    DOI:  https://doi.org/10.1016/j.celrep.2023.112937
  18. Dev Dyn. 2023 Aug 08.
      BACKGROUND: The bHLH transcription factor HAND2 plays important roles in the development of the embryonic heart, face, limbs, and sympathetic and enteric nervous systems. To define how and when HAND2 regulates these developmental systems, requires understanding the transcriptional regulation of Hand2.RESULTS: Remarkably, Hand2 is flanked by an extensive upstream gene desert containing a potentially diverse enhancer landscape. Here, we screened the regulatory interval 200 kb proximal to Hand2 for putative enhancers using evolutionary conservation and histone marks in Hand2-expressing tissues. H3K27ac signatures across embryonic tissues pointed to only two putative enhancer regions showing deep sequence conservation. Assessment of the transcriptional enhancer potential of these elements using transgenic reporter lines uncovered distinct in vivo enhancer activities in embryonic stomach and limb mesenchyme, respectively. Activity of the identified stomach enhancer was restricted to the developing antrum and showed expression within the smooth muscle and enteric neurons. Surprisingly, the activity pattern of the limb enhancer did not overlap Hand2 mRNA but consistently yielded a defined subectodermal anterior expression pattern within multiple transgenic lines.
    CONCLUSIONS: Together, these results start to uncover the diverse regulatory potential inherent to the Hand2 upstream regulatory interval.
    Keywords:  embryonic development; hand factors; transcription
    DOI:  https://doi.org/10.1002/dvdy.646
  19. Proc Natl Acad Sci U S A. 2023 08 15. 120(33): e2211855120
      The spatial segregation of pericentromeric heterochromatin (PCH) into distinct, membrane-less nuclear compartments involves the binding of Heterochromatin Protein 1 (HP1) to H3K9me2/3-rich genomic regions. While HP1 exhibits liquid-liquid phase separation properties in vitro, its mechanistic impact on the structure and dynamics of PCH condensate formation in vivo remains largely unresolved. Here, using a minimal theoretical framework, we systematically investigate the mutual coupling between self-interacting HP1-like molecules and the chromatin polymer. We reveal that the specific affinity of HP1 for H3K9me2/3 loci facilitates coacervation in nucleo and promotes the formation of stable PCH condensates at HP1 levels far below the concentration required to observe phase separation in purified protein assays in vitro. These heterotypic HP1-chromatin interactions give rise to a strong dependence of the nucleoplasmic HP1 density on HP1-H3K9me2/3 stoichiometry, consistent with the thermodynamics of multicomponent phase separation. The dynamical cross talk between HP1 and the viscoelastic chromatin scaffold also leads to anomalously slow equilibration kinetics, which strongly depend on the genomic distribution of H3K9me2/3 domains and result in the coexistence of multiple long-lived, microphase-separated PCH compartments. The morphology of these complex coacervates is further found to be governed by the dynamic establishment of the underlying H3K9me2/3 landscape, which may drive their increasingly abnormal, aspherical shapes during cell development. These findings compare favorably to 4D microscopy measurements of HP1 condensate formation in live Drosophila embryos and suggest a general quantitative model of PCH formation based on the interplay between HP1-based phase separation and chromatin polymer mechanics.
    Keywords:  3D genomics; biophysics; heterochromatin; microscopy; phase separation
    DOI:  https://doi.org/10.1073/pnas.2211855120