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Ray, J.

Publications and source records attributed to Ray, J..

At least 19 recordsLinked to original sources

Dissecting context-dependent cancer vulnerabilities using Perturb-seq

Background CRISPR-mediated viability assays in diverse cancer cell lines have informed cancer biology and precision medicine, but cell fitness is not the only cancer-relevant phenotype. Gene expression profiling provides insight into cellular stress, inflammation, and differential state, while still identifying activation of cell-death pathways. Perturb-seq allows scalable functional genomics screening of expression phenotypes at single-cell resolution, however existing datasets cover only a small number of work-horse cell lines. Results We produced a proof-of-concept Perturb-seq dataset targeting 100 genes in 16 diverse cancer cell lines. In the process, we established methods to address single-cell technical artifacts, identified Cas9-mediated chromosomal aberrations and assessed screen quality. Even with a limited library, we observed common signatures of deleting essential genes as well as context-specific responses based on intrinsic genomic properties of the models. For example, we inferred a previously undescribed relationship between dependence on the ER-golgi transport gene immediate early response 3 interacting protein 1 (IER3IP1) and oxidative stress, demonstrating the potential of integrated Perturb-seq for hypothesis generation. Conclusions We established a framework for building a comprehensive map of post-perturbational transcriptional phenotypes using parallel Perturb-seq experiments across multiple cell lines. We demonstrated that integrated Perturb-seq experiments spanning diverse contexts enable hypotheses about gene function specific to tissue types or cancer subtypes - suggesting large-scale, genome-wide datasets would offer invaluable insight into the highly context-dependent nature of cancer biology.

cancer biology↗

Myeloid IRF5 is required for TLR7-driven inflammatory hemophagocyte differentiation and Macrophage Activation Syndrome

In TLR7-driven macrophage activation syndrome (MAS), inflammatory hemophagocytes (iHPCs) differentiate from Ly6CHI monocytes, phagocytose red blood cells and promote disease, including anemia and thrombocytopenia. We demonstrate here that IRF5 is required for iHPC differentiation and MAS in TLR7-overexpressing (TLR7.1) mice. Both constitutive and myeloid-specific Irf5 deletion reduced iHPCs and improved anemia, thrombocytopenia and survival. Furthermore, therapeutic inhibition of IRF5 ameliorated MAS features and reduced splenic and circulating iHPCs. While cell-intrinsic IRF5 expression was required for iHPC differentiation, it was not required for TLR7.1 Ly6CHI monocyte differentiation and monocyte transcriptional programs. We further show that the transcriptome and chromatin landscape changed dramatically as iHPCs differentiated from TLR7.1 Ly6CHI monocytes. Many transcriptional programs gained in iHPCs were enriched in genes associated with IRF5-binding accessible chromatin regions, including those associated with NF-kB signaling, cytokine and chemokine production, and complement activation. Our data suggest that IRF5 collaborates with other transcription factor families, including NF-kB, ETS and AP1 members, to regulate iHPC gene programs. Together, our findings demonstrate that expression of IRF5 in myeloid cells is critical for MAS, for iHPC differentiation, and acts broadly across iHPC-specific gene programs in TLR7-driven inflammation.

immunology↗

Complex Modulation of IL-6 Signaling by Apelin and Elabela in HTR-8/SVneo Cells Under Cobalt Chloride Induced Chemical Hypoxia

Preeclampsia is a pregnancy complication characterized by hypertension, proteinuria, and end-organ dysfunction. Abnormal placentation leading to reduced placental perfusion may contribute to its development. Previous studies demonstrated that the activation of the apelin receptor (APJ) system has hypotensive, renoprotective, and antioxidant effects in preeclamptic rat models. Apelin and elabela (ELA) can stimulate the proliferation of trophoblast cells, suggesting a role in embryonic development. However, the mechanisms underlying the actions of apelin or ELA in trophoblast cells are not well understood, particularly in hypoxic settings. The immortalized HTR-8/SVneo trophoblastic cells were treated with cobalt chloride (CoCl2) at 0.2 mM for 24 hours to mimic hypoxic conditions. RT-qPCR, ELISA or Western blotting was used to measure mRNA or protein levels of apelin, elabela, and the components of IL-6 signaling in cell lysates or conditioned media. The exposure to CoCl2 increased total apelin and elabela content approximately 2-fold in the conditioned media but did not affect APJ levels. CoCl2 upregulated proinflammatory cytokine concentrations: soluble fms-like tyrosine kinase 1 (sFlt-1), soluble gp130 (sgp130), interleukin-6 (IL-6), and sIL-6 receptor (IL-s6R). Both apelin and elabela downregulated IL-6 mRNA but had no effect on sFlt-1 mRNA. Apelin attenuated sgp130, while ELA decreased the membrane form of IL-s6R. Apelin also decreased the pSTAT3/STAT3 ratio. CoCl2-induced hypoxia upregulated the pro-inflammatory milieu in HTR-8/SVneo cells. Local activation of this peptidergic system may be a compensatory response of the trophoblast cells to hypoxia as exogenous apelin and elabela treatment ameliorated the hypoxia-induced pro-inflammatory milieu.

molecular biology↗

Intrinsic promoter responsiveness dictates sensitivity to transcriptional activation by enhancers

Enhancers activate specific target promoters, but whether intrinsic enhancer-promoter compatibility contributes to this specificity is debated. Recent studies using different reporter assays have reached contradictory conclusions. We compare six reporter assay designs, identify confounders that bias compatibility measurements, and apply improved assays to test 25,000 enhancer-promoter pairs. Promoters differ in their responsiveness to enhancers (>100-fold versus 1.1-fold activation) while enhancers activate all promoters in a similar rank order. Promoter output scales with enhancer activity following a power law, with the exponent varying across promoters. Incorporating this exponent into the Activity-by-Contact model improves prediction of endogenous enhancer effects, explaining why certain active genes are insensitive to distal perturbations and "skipped" by enhancers. Responsiveness is modulated by transcription factor motifs in the core promoter. This work establishes responsiveness as an intrinsic promoter property that enables specific promoters to be highly activated in a landscape of broadly compatible enhancers, while others remain unaffected.

genomics↗

PerturbPlan: An analytical framework for designing Perturb-seq experiments

CRISPR screens with single-cell RNA-seq readouts provide a powerful tool for characterizing the functions of noncoding elements and genes. However, designing these experiments to balance statistical power and cost is challenging, given the large number of design parameters. The only available tool for this purpose is a simulation-based power calculator, but it is computationally costly and requires high-performance computing to run. We derive a novel analytical formula for the power to detect perturbation-expression associations, recapitulating power estimates from the simulation-based tool while reducing runtime by up to seven orders of magnitude. This acceleration unlocks the possibility of interactive single-cell CRISPR screen design. Accordingly, we develop PerturbPlan, an interactive web application built on the analytical power formula. PerturbPlan helps users address 11 design questions for two types of single-cell CRISPR screens, Perturb-seq and targeted Perturb-seq (TAP-seq). We apply PerturbPlan to carry out a comparative analysis of three recent Perturb-seq designs, demonstrating how optimal design varies across experiments of different scales. We also use PerturbPlan to quantify the cost savings of a recent TAP-seq study relative to a hypothetical Perturb-seq study assaying the same perturbations, illustrating how the tool can inform decisions about targeted versus whole-transcriptome readouts. In sum, PerturbPlan is the first tool to facilitate flexible and interactive design of well-powered single-cell CRISPR screen experiments.

genomics↗

MGIDI selection and machine learning reveal harvest index driving traits in sodium azide-induced rice mutants with SSR-based genetic diversity

Sodium azide mutagenesis offers a powerful approach to generate genetic diversity for rice improvement, yet comprehensive characterization of mutant populations using integrated modern breeding tools remains limited. M mutants of BRRI dhan28 induced with sodium azide, were evaluated for 17 agronomic traits and genetic diversity was characterized using 30 SSR markers. The MGIDI was used to characterize elite genotypes and machine learning approaches were used to dissect trait architecture underlying harvest index. The phenotypic variation captured by principal component analysis was 52.12%, and yield was the trait with the highest genotypic variance (278.22) and genotypic coefficient of variation (29.07%). MGIDI analysis detected 10 elite mutants that significantly outperformed within the same environment in combined yield and harvest index. The main predictors of harvest index variability were examined using a Random Forest analysis, and this showed that grain and straw yield were the main predictors of harvest index variability. The SSR markers showed high level of genetic diversity (PIC = 0.264), population structure analysis revealed two subgroups (Fst = 0.0437) and the pairwise genetic distance ranged from 0.000 to 0.733. Procrustean alignment showed a high correlation between molecular and phenotypic variation. An integrated approach of MGIDI selection and prediction of diversity using machine learning underpinned the identification of elite mutants that can be quickly forwarded to breeding programs. This study provides valuable genetic resources and demonstrates that sodium azide mutagenesis combined with modern analytical tools accelerates genetic gains in rice improvement.

plant biology↗

NEST-Scoring, a Novel miRNA Target Gene Profile Network Analysis of Placenta-Derived Extracellular Vesicles in a Transgenic Rat Model of Preeclampsia

Preeclampsia is a multisystem hypertensive disorder of pregnancy and a leading cause of maternal morbidity and mortality. Despite its increasing incidence and the debilitating nature of its cerebrovascular complications, the underlying mechanisms remain incompletely understood. The goals of this study were to 1) determine whether middle cerebral artery (MCA) hemodynamics are altered in late gestation (LG) or two months postpartum in transgenic rats with preeclampsia compared to normal pregnant Sprague-Dawley (SD) rats, and 2) evaluate the microRNA (miRNA) profiles of circulating placental-derived extracellular vesicles (EVPD) using the Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway framework using NEST-Scoring [Node, Edge, System, Topology], a novel target gene profile network analysis. Our data showed elevated blood pressure in transgenic preeclampsia rats at both LG and two months post-partum (PP-2M) compared to normal pregnant SD rats in the setting of hypertension. The heart rate was also significantly higher in preeclampsia rats at LG. No differences were observed in left MCA (LMCA) velocities between strains or time points. However, LMCA resistance and pulsatility indexes were lower at PP-2M in transgenic preeclampsia rats compared to SD rats. Exposure to preeclampsia differentially altered the miRNA profiles of circulating EVPD in transgenic preeclampsia rats at both LG and PP-2M. The identified miRNA targets were associated with key vascular and cellular regulatory pathways, suggesting a mechanistic link between placental dysfunction and postpartum vascular alterations in this preeclampsia model. Overall, this study suggests that the TGA-PE rat model could be a valuable platform to study the mechanistic link between preeclampsia and cerebrovascular disease.

bioinformatics↗

An unbiased survey of distal element-gene regulatory interactions with direct-capture targeted Perturb-seq

Identifying the impact of distal regulatory elements on gene expression is a core challenge in human genetics. Large-scale CRISPR screens have not captured lower effect size element-gene interactions due to selection bias and limited statistical power. We developed a framework for highly powered CRISPR screens, consisting of Direct-Capture Targeted Perturb-seq (DC-TAP-seq), unbiased target selection, and a pipeline accounting for statistical power. Surveying 10,000 random distal element-gene pairs revealed most element-gene interactions have effect sizes <10%, which were virtually undetectable in prior studies. Most interactions occur within 100kb, many elements bind CTCF without classical enhancer chromatin, and housekeeping genes have similar frequencies of distal regulatory elements but with weaker effects. We also highlight limitations of predictive models and suggest that new models consider elements with smaller effect sizes. Our study provides an expanded view of distal regulatory elements and a framework for building more comprehensive maps of distal regulation.

genomics↗

Comparative analysis of convergent and divergent T7 RNA polymerase promoters for the synthesis of dsRNA in vivo and in vitro

Double-stranded RNA plays a key role in various biological processes. The discovery of RNA interference, a gene-silencing mechanism, revolutionised the study of gene function. dsRNA has since been used in novel therapeutics and as an agricultural biocontrol alternative to chemical pesticides. Microbial production typically involves expression systems with convergent T7 promoters. However, convergent transcription from DNA-dependent RNA polymerases can lead to transcriptional interference. In this study, we designed multiple plasmid DNA constructs to investigate the effect of convergent and divergent T7 RNA polymerase production of dsRNA via in vitro transcription and in vivo in E. coli, prior to dsRNA yield quantification and analysis of product quality. We demonstrate that higher yields of larger dsRNA are typically obtained using convergent promoters during in vivo production. A typical fold increase of 2.1 was obtained for dsRNA > 400 bp. However, production of smaller dsRNA (< 250 bp) by divergent promoters resulted in increased yields (2.2 fold). Furthermore, our data demonstrates that in vitro transcription production of dsRNA using divergent T7 promoters results in significantly higher yields of dsRNA, with a maximum fold increase of 6.46. Finally, independent of size, we demonstrate that dsRNA synthesised from DNA templates with multiple transcriptional terminators, improved the quality and purity of dsRNA due to decreased formation of dsRNA multimers or aggregates, compared to run-off transcription. This study highlights alternative optimal strategies for the production of a wide range of different sized dsRNA both in vitro and in microbial systems.

synthetic biology↗

Sex Differences in Middle Cerebral Artery Reactivity and Hemodynamics Independent from Changes in Systemic Arterial Stiffness in Adult Sprague-Dawley Rats

Young women are protected against cerebrovascular disease compared with men. However, the underlying mechanisms of sex differences in cerebrovascular function are not well understood. In this study, we determined whether sex differences in middle cerebral artery (MCA) reactivity are accompanied with changes in cerebral or systemic arterial resistance and stiffness in adult 25-week-old Sprague-Dawley (SD) rats. No differences in systolic or diastolic blood pressures were observed between sexes. Heart rate was higher in the female versus male SD. Left MCA pulsatility index (PI) was lower in female versus male SD, while no differences in left intracranial internal carotid artery (ICA) PI was observed between sexes. There were no differences in thoracic aorta or left common carotid artery pulse wave velocity (PWV) between sexes. In isolated MCA segments, female left MCA had lower contraction to potassium, but similar maximal contraction and sensitivity to thromboxane A2 receptor agonist U46619. Pre-incubation with indomethacin lowered maximal response and sensitivity to U46619 in male MCA but not female MCA suggesting that vasoconstrictor prostaglandins may have a greater role in male MCA vs. female MCA. Endothelial nitric oxide synthase (eNOS) and vascular smooth muscle layer thromboxane A2 receptor immunoreactivity were greater in female versus male SD. We conclude that sex differences in the MCA reactivity are associated with a differential functional profile of MCA in adult SD rats independent from changes in systemic PWV. NEW & NOTEWORTHYDespite the debilitating effects of cerebrovascular disease in women, the basis for sex differences in cerebrovascular dysfunction remains incompletely understood. Our study demonstrated that middle cerebral artery reactivity and hemodynamics are not accompanied by changes in central pulse wave velocity in mature adult Sprague-Dawley rats suggesting different mechanisms underlying baseline vascular reactivity of cerebral versus systemic arterial beds.

physiology↗

A lineage-specific nascent RNA assay unveils principles of gene regulation in tissue biology

Gene regulatory mechanisms that modulate RNA Polymerase II activity are difficult to access in mammalian tissues composed of multiple cell lineages. Here, we develop a nascent RNA assay (PReCIS-seq) that measures lineage-specific transcriptionally-engaged Pol II on genes and DNA enhancer elements in intact mouse tissue. By employing keratinocytes as a prototype lineage, we unearth Pol II promoter-recruitment versus pause-release mechanisms operating in adult skin homeostasis. Moreover, we relate active enhancer proximity and transcription factor binding motifs on promoters to Pol II activity and promoter-proximal pausing level. Finally, we find Pol II firing rapidly into elongation on lineage identity genes and highly paused on cellular safeguarding genes in a context-dependent manner. Our work provides a basic platform to investigate mechanistic principles of gene regulation in individual lineages of complex mammalian tissues.

genomics↗

FUSION: A web-based application for in-depth exploration of multi-omics data with brightfield histology

Spatial -OMICS technologies facilitate the interrogation of molecular profiles in the context of the underlying histopathology and tissue microenvironment. Paired analysis of histopathology and molecular data can provide pathologists with otherwise unobtainable insights into biological mechanisms. To connect the disparate molecular and histopathologic features into a single workspace, we developed FUSION (Functional Unit State IdentificatiON in WSIs [Whole Slide Images]), a web-based tool that provides users with a broad array of visualization and analytical tools including deep learning-based algorithms for in-depth interrogation of spatial -OMICS datasets and their associated high-resolution histology images. FUSION enables end-to-end analysis of functional tissue units (FTUs), automatically aggregating underlying molecular data to provide a histopathology-based medium for analyzing healthy and altered cell states and driving new discoveries using "pathomic" features. We demonstrate FUSION using 10x Visium spatial transcriptomics (ST) data from both formalin-fixed paraffin embedded (FFPE) and frozen prepared datasets consisting of healthy and diseased tissue. Through several use-cases, we demonstrate how users can identify spatial linkages between quantitative pathomics, qualitative image characteristics, and spatial --omics

pathology↗

Cohesin-mediated 3D contacts tune enhancer-promoter regulation

Enhancers are key drivers of gene regulation thought to act via 3D physical interactions with the promoters of their target genes. However, genome-wide depletions of architectural proteins such as cohesin result in only limited changes in gene expression, despite a loss of contact domains and loops. Consequently, the role of cohesin and 3D contacts in enhancer function remains debated. Here, we developed CRISPRi of regulatory elements upon degron operation (CRUDO), a novel approach to measure how changes in contact frequency impact enhancer effects on target genes by perturbing enhancers with CRISPRi and measuring gene expression in the presence or absence of cohesin. We systematically perturbed all 1,039 candidate enhancers near five cohesin-dependent genes and identified 34 enhancer-gene regulatory interactions. Of 26 regulatory interactions with sufficient statistical power to evaluate cohesin dependence, 18 show cohesin-dependent effects. A decrease in enhancer-promoter contact frequency upon removal of cohesin is frequently accompanied by a decrease in the regulatory effect of the enhancer on gene expression, consistent with a contact-based model for enhancer function. However, changes in contact frequency and regulatory effects on gene expression vary as a function of distance, with distal enhancers (e.g., >50Kb) experiencing much larger changes than proximal ones (e.g., <50Kb). Because most enhancers are located close to their target genes, these observations can explain how only a small subset of genes -- those with strong distal enhancers -- are sensitive to cohesin. Together, our results illuminate how 3D contacts, influenced by both cohesin and genomic distance, tune enhancer effects on gene expression.

molecular biology↗

Flynotyper 2.0: A tool for rapid quantitative assessment of Drosophila eye phenotypes

About two-thirds of the genes in the Drosophila melanogaster genome are also involved in its eye development, making the Drosophila eye an ideal system for genetic studies. We previously developed Flynotyper, a software that uses image processing operations to identify and quantify the degree of roughness by measuring disorderliness of ommatidial arrangement in the fly eye. This software has enabled researchers to quantify morphological defects of thousands of eye images caused by genetic perturbations. Here, we present Flynotyper 2.0, a software that has an updated computer vision library, improved performance, and a streamlined pipeline for high-throughput analysis of multiple eye images. We also tested several batches of Drosophila eye images to ensure robustness and reproducibility of the updated Flynotyper 2.0 software. Availability and implementationThe source code for Flynotyper 2.0 can be downloaded and installed from https://github.com/girirajanlab/flynotyper-desktop-application.

bioinformatics↗

Sex-Specific Cardiovascular Adaptations to Simulated Microgravity in Sprague-Dawley Rats

Men and women have different cardiovascular responses to spaceflight; however few studies have focused on direct comparisons between sexes. Therefore, we investigated cardiovascular system differences, including arterial stiffness between socially and sexually mature 20-week-old male and female Sprague Dawley (SD) rats exposed to hindlimb unloading (HLU) - an analogue for spaceflight-induced microgravity. Two weeks of HLU had no effect on body weight in either male or female rats. The index of arterial stiffness determined by ultrasound, pulse wave velocity (PWV), was greater in the aortic arch and carotid artery of females after HLU versus control females. HLU had no effect on arterial PWV in males. smooth muscle actin, myosin, collagen, elastin, and collagen-to-elastin ratio were not different in rats of either sex in response to HLU. HLU exposure did not alter individual collagen fiber characteristics in studied groups. The levels of G protein-coupled estrogen receptor (GPER) were lower in the aorta of SD females exposed to HLU compared with female controls but not in males. These changes were associated with lower PPAR {gamma} and increased oxidative stress markers (8-hydroxy-2-deoxyguanosine and p47phox) in the females. Diastolic cardiac function was altered in females after HLU versus control females. GPER agonist, G1 prevented the increase in pulse wave velocity and 8-hydroxy-2-deoxyguanosine, without altering PPAR {gamma} or p47phox. Our data revealed that lower GPER in the HLU females contributes to the development of arterial stiffness, and that the SD rat is a suitable model to study the cardiovascular response of females to HLU.

physiology↗

Optimising the production of dsRNA biocontrols in microbial systems using multiple transcriptional terminators.

Crop pests and pathogens annually cause over $100 billion in global crop damage, with insects consuming 5-20% of major grain crops. Current crop pest and disease control strategies rely on insecticidal and fungicidal sprays, plant genetic resistance, transgenes and agricultural practices. dsRNA is emerging as a novel sustainable method of plant protection as an alternative to traditional chemical pesticides. Successful commercialisation of dsRNA based biocontrols requires the economical production of large quantities of dsRNA combined with suitable delivery methods to ensure RNAi efficacy against the target pest. In this study, we have optimised the design of plasmid DNA constructs to produce dsRNA biocontrols in E. coli, by employing a wide range of alternative synthetic transcriptional terminators prior to measurement of dsRNA yield. We demonstrate that a 7.8-fold increase of dsRNA was achieved using triple synthetic transcriptional terminators within a dual T7 dsRNA production system compared to the absence of transcriptional terminators. Moreover, our data demonstrates that batch fermentation production dsRNA using multiple transcriptional terminators is scalable and generates significantly higher yields of dsRNA generated in the absence of transcriptional terminators at both small-scale batch culture and large-scale fermentation. In addition, we show that application of these dsRNA biocontrols expressed in E. coli cells results in increased insect mortality. Finally, novel mass spectrometry analysis was performed to determine the precise sites of transcriptional termination at the different transcriptional terminators providing important further mechanistic insight.

synthetic biology↗

Nanoscale photobiotinylation, pulldown and sequencing of region-specific DNA from intact cells.

Femto-seq is a novel nanoscale optical method that can be used to obtain DNA sequence information from targeted regions around a specific locus or other nuclear regions of interest. Two-photon excitation is used to photobiotinylate femtoliter volumes of chromatin within the nucleus, allowing for subsequent isolation and sequencing of DNA, and bioinformatic mapping of any nuclear region of interest in a select set of cells from a heterogenous population.

genomics↗

Genome-wide identification of fitness determinants in the Xanthomonas campestris bacterial pathogen during early stages of plant infection

Plant diseases are an important threat to food production. While major pathogenicity determinants required for disease have been extensively studied, less is known on how pathogens thrive during host colonization especially at early infection stages. Here, we used randomly barcoded-transposon insertion site sequencing (RB-TnSeq) to perform a genome-wide screen and identify key bacterial fitness determinants of the vascular pathogen Xanthomonas campestris pv. campestris (Xcc) during infection of the cauliflower host plant (Brassica oleracea). This high-throughput analysis was conducted in hydathodes, the natural entry site of Xcc, in xylem sap and in synthetic media. Xcc did not face a strong bottleneck during hydathode infection. 183 genes important for fitness were identified in plant-associated environments with functional enrichment in genes involved in metabolism when only few genes known to be involved in virulence were found to be affected. The biological relevance of 13 genes was independently confirmed by phenotyping single mutants. Notably, we show that the XC_3388, a protein with no known function (DUF1631), plays a key role in the adaptation and virulence of Xcc possibly through c-di-GMP-mediated regulation. This study thus revealed yet unsuspected social behaviors adopted by Xcc individuals when confined inside hydathodes at early infection stages.

microbiology↗