bioRxiv Science⌕ Search

Biology subjects

Hainer, S. J.

Publications and source records attributed to Hainer, S. J..

11 recordsLinked to original sources

Benchmarking CUT&RUN analysis using motif enrichment

Background. Cleavage under targets and release using nuclease (CUT&RUN) maps the genome-wide locations of chromatin-associated proteins and provides an improved alternative to chromatin immunoprecipitation sequencing (ChIP-seq) for profiling sequence-specific transcription factor binding sites. Identifying these binding sites plays a critical role in understanding gene regulation, and transcription factors provide a useful setting for benchmarking because their well-defined sequence motifs serve as built-in controls for evaluating performance. Compared with ChIP-seq, CUT&RUN achieves higher resolution and lower background by avoiding cross-linking and bulk precipitation. Its distinct fragment length and cleavage characteristics, however, limit the direct transfer of existing computational tools, which primarily target ChIP-seq data. The performance of these tools on CUT&RUN can depend strongly on preprocessing choices. In this work, we investigate preprocessing strategies for transcription factor CUT&RUN, focusing on fragment length filtering and spike-in calibration. We aim to improve peak detection and provide practical guidance for analysis. Results. We designed a benchmarking method to evaluate peak-calling procedures for CUT&RUN data and the effects of preprocessing approaches, including fragment length filtering and spike-in calibration. We benchmarked the two most widely used peak callers, MACS2 and SEACR, by assessing motif enrichment---the degree to which identified peaks contain the expected transcription factor binding motifs. Filtering for fragments with a length [≤]120 bp generally improved target motif enrichment. Spike-in calibration using heterologous Saccharomyces cerevisiae DNA improved motif elucidation substantially for MACS2, with little benefit for SEACR. By contrast, using Escherichia coli DNA as a spike-in control often failed to produce valid results unless we could meticulously control E. coli contamination. MACS2 performed robustly across samples. SEACR performed especially well on clean, sparse-background datasets, but performed poorly on some datasets with denser background signal and often produced numerous apparent false positives. While MACS2 provided robust results under minor perturbations in fragment length filtering, SEACR exhibited greater sensitivity to such changes. Discussion. Our benchmarking highlights how both peak caller choice and preprocessing strategy shape the analysis of transcription factor CUT&RUN data. By comparing the robustness and limitations of two widely used peak callers, we provide practical guidance on fragment length filtering, spike-in calibration, and tool selection. These findings help improve the processing and interpretation of CUT&RUN data, allowing researchers to more rapidly and reliably utilize this new technology. We expect that our work will guide more informed choices in CUT&RUN analysis and support the development of improved computational methodologies.

bioinformatics↗

FACT depletion results in a temporal cascade of chromatin disruption preceding transcriptional collapse in stem cells

The histone chaperone FACT is essential for chromatin organization and stem cell identity, yet the sequence of events through which FACT maintains chromatin integrity remains unclear. We generate a high-resolution temporal map of events leading to chromatin destabilization and cell identity loss in murine embryonic stem cells following dTAG-mediated depletion of FACT. Loss of FACT initiates a rapid cascade, with nucleosome phasing disruption and reduced H3K4me3 beginning within 10 minutes in a transcription-dependent manner. This architectural destabilization enables pluripotency transcription factors to ectopically occupy gene bodies. FACT loss results in RNA Polymerase II accumulation within 30 minutes and altered H3K36me3 deposition preceding a global transcriptional collapse at 2 hours of FACT depletion. FACT restoration fails to rescue these defects, demonstrating they are largely irreversible. Our findings define a temporal hierarchy in which FACT loss drives progressive deterioration of chromatin architecture, leading to transcriptional collapse in stem cells.

genomics↗

esBAF and INO80C fine-tune subcompartments and differentially regulate enhancer-promoter interactions

The genome is compacted in the nucleus through a hierarchical chromatin organization, ranging from chromosome territories to compartments, topologically associating domains (TADs), and individual nucleosomes. Nucleosome remodeling complexes hydrolyze ATP to translocate DNA and thereby mobilize histone proteins. While nucleosome remodeling complexes have been extensively studied for their roles in regulating nucleosome positioning and accessibility, their contributions to higher-order chromatin architecture remain less well understood. Here, we investigate the roles of two key nucleosome remodelers, esBAF and INO80C, in shaping 3D genome organization in mouse embryonic stem cells. Using Hi-C, we find that loss of either remodeler has minimal effects on global compartment or TAD structures. In contrast, subcompartment organization is notably altered, suggesting that esBAF and INO80C contribute to finer-scale chromatin topology. To overcome the limited resolution of Hi-C for detecting regulatory loops, we employed promoter capture Micro-C (PCMC), which revealed that the loss of esBAF or INO80C alters a subset of promoter anchored looping interactions. Although these changes occur at distinct genomic loci for each remodeler, the affected sites are commonly enriched for bivalent chromatin regions bound by OCT4, SOX2, and NANOG (OSN), as well as BRG1 and INO80 themselves. Together, our findings reveal that esBAF and INO80C selectively influence subcompartment identity and enhancer-promoter communication at key regulatory loci, highlighting a previously underappreciated role for nucleosome remodelers in higher-order chromatin organization.

genomics↗

The PBAF chromatin remodeling complex contributes to metal homeostasis through Mtf1 regulation

SWI/SNF chromatin remodeling complexes regulate gene expression by modulating nucleosome positioning, yet their roles in metal homeostasis during skeletal muscle development remain unclear. Here, we uncover distinct functions of the BAF, PBAF, and ncBAF complexes in myoblast proliferation under metal stress. While knockdown (KD) of Baf250a (BAF-specific) or Brd9 (ncBAF-specific) reduces myoblast proliferation, Baf180 (PBAF-specific) KD does not impair cell proliferation under basal conditions. Interestingly, supplementation with copper (Cu) or zinc (Zn) rescues proliferation in Baf250a- and Brd9-deficient myoblasts but paradoxically inhibits growth in Baf180 KD cells. Mechanistically, Baf180 KD disrupts Cu and Zn homeostasis, leading to intracellular Cu accumulation without labile Cu pools and impaired expression of Atp7a, a key Cu exporter. Transcriptomic analyses reveal widespread gene dysregulation in metal-treated Baf180-deficient cells, while metal supplementation promotes pro-proliferative gene expression in Baf250a- and Brd9-KD myoblasts. CUT&RUN assays demonstrate that metal-responsive transcription factor Mtf1 exhibits increased chromatin binding upon Cu treatment, targeting genes involved in stress response and myogenesis. Notably, Mtf1 colocalizes with Baf180 in the nucleus and co-immunoprecipitates with both conserved SWI/SNF subunits and Baf180, suggesting a functional interplay between PBAF and Mtf1 in regulating metal-dependent gene expression. Our findings establish the PBAF complex as a crucial regulator of Cu/Zn homeostasis in myoblast proliferation via Mtf1, while metal supplementation compensates for BAF and ncBAF dysfunction but exacerbates defects in PBAF-deficient cells. This study reveals a novel link between chromatin remodeling, metal signaling, and muscle development, with implications for stress adaptation and metabolic regulation in myogenesis.

molecular biology↗

A direct interaction between the Chd1 CHCT domain and Rtf1 controls Chd1 distribution and nucleosome positioning on active genes

The nucleosome remodeler Chd1 is required for the re-establishment of nucleosome positioning in the wake of transcription elongation by RNA Polymerase II. Previously, we found that Chd1 occupancy on gene bodies depends on the Rtf1 subunit of the Paf1 complex in yeast. Here, we identify an N-terminal region of Rtf1 and the CHCT domain of Chd1 as sufficient for their interaction and demonstrate that this interaction is direct. Mutations that disrupt the Rtf1-Chd1 interaction result in an accumulation of Chd1 at the 5 ends of Chd1-occupied genes, increased cryptic transcription, altered nucleosome positioning, and concordant shifts in histone modification profiles. We show that a homologous region within mouse RTF1 interacts with the CHCT domains of mouse CHD1 and CHD2. This work supports a conserved mechanism for coupling Chd1 family proteins to the transcription elongation complex and identifies a cellular function for a domain within Chd1 about which little is known.

molecular biology↗

Cysteine Rich Intestinal Protein 2 is a copper-Responsive regulator of skeletal muscle differentiation.

Copper (Cu) is an essential trace element required for respiration, neurotransmitter synthesis, oxidative stress response, and transcriptional regulation. Imbalance in Cu homeostasis can lead to several pathological conditions, affecting neuronal, cognitive, and muscular development. Mechanistically, Cu and Cu-binding proteins (Cu-BPs) have an important but underappreciated role in transcription regulation in mammalian cells. In this context, our lab investigates the contributions of novel Cu-BPs in skeletal muscle differentiation using murine primary myoblasts. Through an unbiased synchrotron X-ray fluorescence-mass spectrometry (XRF/MS) metalloproteomic approach, we identified the murine cysteine rich intestinal protein 2 (mCrip2) in a sample that showed enriched Cu signal, which was isolated from differentiating primary myoblasts derived from mouse satellite cells. Immunolocalization analyses showed that mCrip2 is abundant in both nuclear and cytosolic fractions. Thus, we hypothesized that mCrip2 might have differential roles depending on its cellular localization in the skeletal muscle lineage. mCrip2 is a LIM-family protein with 4 conserved Zn2+-binding sites. Homology and phylogenetic analyses showed that mammalian Crip2 possesses histidine residues near two of the Zn2+-binding sites (CX2C-HX2C) which are potentially implicated in Cu+-binding and competition with Zn2+. Biochemical characterization of recombinant human hsCRIP2 revealed a high Cu+-binding affinity for two and four Cu+ ions and limited redox potential. Functional characterization using CRISPR/Cas9-mediated deletion of mCrip2 in primary myoblasts did not impact proliferation, but impaired myogenesis by decreasing the expression of differentiation markers, possibly attributed to Cu accumulation. Transcriptome analyses of proliferating and differentiating mCrip2 KO myoblasts showed alterations in mRNA processing, protein translation, ribosome synthesis, and chromatin organization. CUT&RUN analyses showed that mCrip2 associates with a select set of gene promoters, including MyoD1 and metallothioneins, acting as a novel Cu-responsive or Cu-regulating protein. Our work demonstrates novel regulatory functions of mCrip2 that mediate skeletal muscle differentiation, presenting new features of the Cu-network in myoblasts.

molecular biology↗

Widespread impact of nucleosome remodelers on transcription at cis-regulatory elements

Nucleosome remodeling complexes and other regulatory factors work in concert to build a chromatin environment that directs the expression of a distinct set of genes in each cell using cis-regulatory elements (CREs), such as promoters and enhancers, that drive transcription of both mRNAs and CRE-associated non-coding RNAs (ncRNAs). Two classes of CRE-associated ncRNAs include upstream antisense RNAs (uaRNAs), which are transcribed divergently from a shared mRNA promoter, and enhancer RNAs (eRNAs), which are transcribed bidirectionally from active enhancers. The complicated network of CRE regulation by nucleosome remodelers remains only partially explored, with a focus on a select, limited number of remodelers. We endeavored to elucidate a remodeler-based regulatory network governing CRE-associated transcription (mRNA, eRNA, and uaRNA) in murine embryonic stem (ES) cells to test the hypothesis that many SNF2-family nucleosome remodelers collaborate to regulate the coding and non-coding transcriptome via alteration of underlying nucleosome architecture. Using depletion followed by transient transcriptome sequencing (TT-seq), we identified thousands of misregulated mRNAs and CRE-associated ncRNAs across the remodelers examined, identifying novel contributions by understudied remodelers in the regulation of coding and non-coding transcription. Our findings suggest that mRNA and eRNA transcription are coordinately co-regulated, while mRNA and uaRNAs sharing a common promoter are independently regulated. Subsequent mechanistic studies suggest that while remodelers SRCAP and CHD8 modulate transcription through classical mechanisms such as transcription factors and histone variants, a broad set of remodelers including SMARCAL1 indirectly contribute to transcriptional regulation through maintenance of genomic stability and proper Integrator complex localization. This study systematically examines the contribution of SNF2-remodelers to the CRE-associated transcriptome, identifying at least two classes for remodeler action.

systems biology↗

The mitochondrial Cu+ transporter PiC2 (SLC25A3) is a target of MTF1 and contributes to the development of skeletal muscle in vitro

The loading of copper (Cu) into cytochrome c oxidase (COX) in mitochondria is essential for energy production in cells. Extensive studies have been performed with mitochondrial cuproenzymes, such as Sco1, Sco2 and Cox17, which contributes to the metallation of the oxidase. However, limited information is available on the upstream mechanism of Cu transport and delivery to mitochondria, especially through Cu-impermeable membranes, in mammalian cells. The mitochondrial phosphate transporter SLC25A3, also known as PiC2, is also able to bind Cu+ and acts as an active copper transporter in eukaryotic cells through these membranes, and ultimately aid in the metallation of COX. We used a well-established differentiation model of primary myoblasts derived from mouse satellite cells, where Cu availability is necessary for growth and maturation, and showed PiC2 is a target of MTF1, its expression is induced during myogenesis and favored by Cu supplementation. PiC2 deletion using CRISPR/Cas9 showed that the transporter is required for proliferation and differentiation of primary myoblasts, as both processes are delayed upon PiC2 knock-out. The effects of PiC2 deletion were ameliorated by the addition of Cu to the growth medium, implying the deleterious effects of PiC2 knockout in myoblasts may be in part due to a failure to deliver sufficient Cu to the mitochondria, which can be compensated by other mitochondrial cuproproteins. Co-localization and co-immunoprecipitation of PiC2 and COX also strongly suggest that PiC2 may act to directly load Cu into COX, which was verified by in vitro Cu+-transfer experiments. The data indicate an important role for PiC2 in both the delivery of Cu to the mitochondria, COX and, subsequently, the differentiation of primary myoblasts.

cell biology↗

FACT maintains pluripotency factor expression through gene-distal regulation in embryonic stem cells

The FACT complex is a conserved histone chaperone with essential roles in transcription and histone deposition. FACT is essential in pluripotent and cancer cells, but otherwise dispensable for most mammalian cell types. FACT deletion or inhibition can block induction of pluripotent stem cells, yet the mechanism through which FACT regulates cell fate decisions remains unclear. To determine this mechanism, we used inducible depletion of FACT subunit SPT16 in murine embryonic stem cells paired with genomic factor localization, nascent transcription, and chromatin accessibility analyses. Over a timecourse of SPT16 depletion, nucleosomes invade loci bound by master pluripotency factors and gene-distal DNaseI hypersensitive sites. Simultaneously, transcription of Pou5f1 (OCT4), Sox2, Nanog, and enhancer RNAs produced at the genes associated enhancers are downregulated, suggesting that FACT regulates expression of the pluripotency factors themselves. We find that FACT maintains cellular pluripotency through a precise nucleosome-based regulatory mechanism for appropriate expression of both coding and non-coding transcripts associated with pluripotency.

molecular biology↗

MTF1, a classic metal sensing transcription factor, promotes myogenesis in response to copper.

MTF1 is a conserved metal-binding transcription factor in eukaryotes that binds to conserved DNA sequence motifs, termed metal response elements (MREs). MTF1 responds to metal excess and deprivation, protects cells from oxidative and hypoxic stresses, and is required for embryonic development in vertebrates. We used multiple strategies to identify an unappreciated role for MTF1 and copper (Cu) in cell differentiation. Upon initiation of myogenesis from primary myoblasts, MTF1 expression increased, as did nuclear localization. Mtf1 knockdown impaired differentiation, while addition of non-toxic concentrations of Cu+ enhanced MTF1 expression and promoted myogenesis. Cu+ bound stoichiometrically to a C-terminus tetra-cysteine of MTF1. MTF1 bound to chromatin at the promoter regions of myogenic genes and binding was stimulated by copper. MTF1 formed a complex with MyoD at myogenic promoters, the master transcriptional regulator of the myogenic lineage. These studies establish novel mechanisms by which copper and MTF1 regulate gene expression in myoblast differentiation.

cell biology↗

Profiling of pluripotency factors in individual stem cells and early embryos

Major cell fate decisions are governed by sequence-specific transcription factors (TFs) that act in small cell populations within developing embryos. To understand how TFs regulate cell fate it is important to identify their genomic binding sites in these populations. However, current methods cannot profile TFs genome-wide at or near the single cell level. Here we adapt the CUT&RUN method to profile chromatin proteins in low cell numbers, mapping TF-DNA interactions in single cells and individual pre-implantation embryos for the first time. Using this method, we demonstrate that the pluripotency TF NANOG is significantly more dependent on the SWI/SNF family ATPase BRG1 for association with its genomic targets in vivo than in cultured cells--a finding that could not have been made using traditional approaches. Ultra-low input CUT&RUN (uliCUT&RUN) enables interrogation of TF binding from low cell numbers, with broad applicability to rare cell populations of importance in development or disease.

genomics↗