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Yosef, N.

Publications and source records attributed to Yosef, N..

At least 37 records · Page 2Linked to original sources

Multimodal profiling reveals tissue-directed signatures of human immune cells altered with age

The immune system comprises multiple cell lineages and heterogeneous subsets found in blood and tissues throughout the body. While human immune responses differ between sites and over age, the underlying sources of variation remain unclear as most studies are limited to peripheral blood. Here, we took a systems approach to comprehensively profile RNA and surface protein expression of over 1.25 million immune cells isolated from blood, lymphoid organs, and mucosal tissues of 24 organ donors aged 20-75 years. We applied a multimodal classifier to annotate the major immune cell lineages (T cells, B cells, innate lymphoid cells, and myeloid cells) and their corresponding subsets across the body, leveraging probabilistic modeling to define bases for immune variations across donors, tissue, and age. We identified dominant tissue-specific effects on immune cell composition and function across lineages for lymphoid sites, intestines, and blood-rich tissues. Age-associated effects were intrinsic to both lineage and site as manifested by macrophages in mucosal sites, B cells in lymphoid organs, and T and NK cells in blood-rich sites. Our results reveal tissue-specific signatures of immune homeostasis throughout the body and across different ages. This information provides a basis for defining the transcriptional underpinnings of immune variation and potential associations with disease-associated immune pathologies across the human lifespan.

immunology↗

ConvexML: Scalable and accurate inference of single-cell chronograms from CRISPR/Cas9 lineage tracing data

Branch length estimation is a fundamental problem in Statistical Phylogenetics and a core component of tree reconstruction algorithms. Traditionally, general time-reversible mutation models are employed, and many software tools exist for this scenario. With the advent of CRISPR/Cas9 lineage tracing technologies, there has been significant interest in the study of branch length estimation under irreversible mutation models. Under the CRISPR/Cas9 mutation model, irreversible mutations - in the form of DNA insertions or deletions - are accrued during the experiment, which are then read out at the single-cell level to reconstruct the cell lineage tree. However, most of the analyses of CRISPR/Cas9 lineage tracing data have so far been limited to the reconstruction of single-cell tree topologies, which depict lineage relationships between cells, but not the amount of time that has passed between ancestral cell states and the present. Time-resolved trees, known as chronograms, would allow one to study the evolutionary dynamics of cell populations at an unprecedented level of resolution. Indeed, time-resolved trees would reveal the timing of events on the tree, the relative fitness of subclones, and the dynamics underlying phenotypic changes in the cell population - among other important applications. In this work, we introduce the first scalable and accurate method to refine any given single-cell tree topology into a single-cell chronogram by estimating its branch lengths. To do this, we perform regularized maximum likelihood estimation under a general irreversible mutation model, paired with a conservative version of maximum parsimony that reconstructs only the ancestral states that we are confident about. To deal with the particularities of CRISPR/Cas9 lineage tracing data - such as double-resection events which affect runs of consecutive sites - we avoid making our model more complex and instead opt for using a simple but effective data encoding scheme. Similarly, we avoid explicitly modeling the missing data mechanisms - such as heritable missing data - by instead assuming that they are missing completely at random. We stabilize estimates in low-information regimes by using a simple penalized version of maximum likelihood estimation (MLE) using a minimum branch length constraint and pseudocounts. All this leads to a convex MLE problem that can be readily solved in seconds with off-the-shelf convex optimization solvers. We benchmark our method using both simulations and real lineage tracing data, and show that it performs well on several tasks, matching or outperforming competing methods such as TiDeTree and LAML in terms of accuracy, while being 10 ~ 100 x faster. Notably, our statistical model is simpler and more general, as we do not explicitly model the intricacies of CRISPR/Cas9 lineage tracing data. In this sense, our contribution is twofold: (1) a fast and robust method for branch length estimation under a gen-eral irreversible mutation model, and (2) a data encoding scheme specific to CRISPR/Cas9-lineage tracing data which makes it amenable to the general model. Our branch length estimation method, which we call ConvexML, should be broadly applicable to any evolutionary model with irreversible mutations (ideally, with high diversity) and an approximately ignorable missing data mechanism. ConvexML is available through the convexml open source Python package.

bioinformatics↗

Calibrated Identification of Feature Dependencies in Single-cell Multiomics

Data-driven identification of functional relationships between cellular properties is an exciting promise of single-cell genomics, especially given the increasing prevalence of assays for multiomic and spatial transcriptomic analysis. Major challenges include dealing with technical factors that might introduce or obscure dependencies between measurements, handling complex generative processes that require nonlinear modeling, and correctly assessing the statistical significance of discoveries. VI-VS (Variational Inference for Variable Selection) is a comprehensive framework designed to strike a balance between robustness and interpretability. VI-VS employs nonlinear generative models to identify conditionally dependent features, all while maintaining control over false discovery rates. These conditional dependencies are more stringent and more likely to represent genuine causal relationships. VI-VS is openly available at https://github.com/YosefLab/VIVS, offering a no-compromise solution for identifying relevant feature relationships in multiomic data, advancing our understanding of molecular biology.

bioinformatics↗

Best practices for perturbation MPRA--a computational evaluation framework of sequence design strategies

The advent of the perturbation-based massively parallel reporter assays (MPRAs) technique has enabled delineating of the roles of non-coding regulatory elements in orchestrating gene expression. However, computational efforts remain scant to evaluate and establish guidelines for sequence design strategies for perturbation MPRAs. Here, we propose a framework for evaluating and comparing various perturbation strategies for MPRA experiments. Under this framework, we benchmark three different perturbation approaches from the perspectives of alteration in motif-based profiles, consistency of MPRA outputs, and robustness of models that predict the activities of putative regulatory motifs. Although our analyses show similar while significant results in multiple metrics, the method of randomly shuffling nucleotides outperform the other two methods. Thus, we still recommend designing sequences by randomly shuffling the nucleotides of the perturbed site in perturbation-MPRA. The evaluation framework, together with the benchmarking findings in our work, creates a resource of computational pipelines and illustrates the promise of perturbation-MPRA for predicting non-coding regulatory activities.

bioinformatics↗

Consensus prediction of cell type labels with popV

Cell-type classification is a crucial step in single-cell analysis. To facilitate this, several methods have been proposed for the task of transferring a cell-type label from an annotated reference atlas to unannotated query data sets. Existing methods for transferring cell-type labels lack proper uncertainty estimation for the resulting annotations, limiting interpretability and usefulness. To address this, we propose popular Vote (popV, https://github.com/YosefLab/popV), an ensemble of prediction models with an ontology-based voting scheme. PopV achieves accurate cell-type labeling and provides effective uncertainty scores. In multiple case studies, popV confidently annotates the majority of cells while highlighting cell populations that are challenging to annotate. This additional step helps to reduce the load of manual inspection, which is often a necessary component of the annotation process, and enables one to focus on the most problematic parts of the annotation, streamlining the overall annotation process.

bioinformatics↗

Deep generative modeling for quantifying sample-level heterogeneity in single-cell omics

The field of single-cell genomics is now observing a marked increase in the prevalence of cohort-level studies that include hundreds of samples and feature complex designs. These data have tremendous potential for discovering how sample or tissue-level phenotypes relate to cellular and molecular composition. However, current analyses are based on simplified representations of these data by averaging information across cells. We present MrVI, a deep generative model designed to realize the potential of cohort studies at the single-cell level. MrVI tackles two fundamental and intertwined problems: stratifying samples into groups and evaluating the cellular and molecular differences between groups, both without requiring a priori grouping of cells into types or states. Due to its single-cell perspective, MrVI is able to detect clinically relevant stratifications of patients in COVID-19 and inflammatory bowel disease (IBD) cohorts that are only manifested in certain cellular subsets, thus enabling new discoveries that would otherwise be overlooked. Similarly, we demonstrate that MrVI can de-novo identify groups of small molecules with similar biochemical properties and evaluate their effects on cellular composition and gene expression in large-scale perturbation studies. MrVI is available as open source at scvi-tools.org.

bioinformatics↗

Deep generative modeling of transcriptional dynamics for RNA velocity analysis in single cells

RNA velocity has been rapidly adopted to guide the interpretation of transcriptional dynamics in snapshot single-cell transcriptomics data. Current approaches for estimating and analyzing RNA velocity can empirically reveal complex dynamics but lack effective strategies for quantifying the uncertainty of the estimate and its overall applicability to the system of interest. Here, we present veloVI (velocity variational inference), a deep generative modeling framework for estimating RNA velocity. veloVI learns a gene-specific dynamical model of RNA metabolism and provides a transcriptome-wide quantification of velocity uncertainty. We show in a series of examples that veloVI compares favorably to previous approaches for inferring RNA velocity with improvements in fit to the data, consistency across transcriptionally similar cells, and stability across preprocessing pipelines for quantifying RNA abundance. Further, we demonstrate that properties unique to veloVI, such as posterior velocity uncertainty, can be used to assess the appropriateness of analysis with velocity to the data at hand. Finally, we highlight veloVI as a flexible framework for modeling transcriptional dynamics by adapting the underlying dynamical model to use time-dependent transcription rates.

bioinformatics↗

NF-κB inhibitor alpha has a cross-variant role during SARS-CoV-2 infection in ACE2-overexpressing human airway organoids

As SARS-CoV-2 continues to spread worldwide, tractable primary airway cell models that accurately recapitulate the cell-intrinsic response to arising viral variants are needed. Here we describe an adult stem cell-derived human airway organoid model overexpressing the ACE2 receptor that supports robust viral replication while maintaining 3D architecture and cellular diversity of the airway epithelium. ACE2-OE organoids were infected with SARS-CoV-2 variants and subjected to single-cell RNA-sequencing. NF-{kappa}B inhibitor alpha was consistently upregulated in infected epithelial cells, and its mRNA expression positively correlated with infection levels. Confocal microscopy showed more I{kappa}B expression in infected than bystander cells, but found concurrent nuclear translocation of NF-{kappa}B that I{kappa}B usually prevents. Overexpressing a nondegradable I{kappa}B mutant reduced NF-{kappa}B translocation and increased viral infection. These data demonstrate the functionality of ACE2-OE organoids in SARS-CoV-2 research and identify an incomplete NF-{kappa}B feedback loop as a rheostat of viral infection that may promote inflammation and severe disease.

microbiology↗

Directed Shortest Walk on Temporal Graphs

BackgroundThe use of graphs as a way of abstracting and representing biological systems has provided a powerful analysis paradigm. Specifically, graph optimization algorithms are routinely used to address various connectivity queries, such as finding paths between proteins in a protein-protein interaction network, while maximizing objectives such as parsimony. While present studies in this field mostly concern static graphs, new types of data now motivate the need to account for changes that might occur to the elements (nodes) that are represented by the graph on the relationships (edges) between them. Results and DiscussionWe define the notion of Directed Temporal Graphs as a series of directed subgraphs of an underlying graph, ordered by time, where only a subset of vertices and edges are present. We then build up towards the Time Conditioned Shortest Walk problem on Directed Temporal Graphs: given a series of time ordered directed graphs, find the shortest walk from any given source node at time point 1 to a target node at time T [≥] 1, such that the walk is consistent (monotonically increasing) with the timing of nodes and edges. We show, contrary to the Directed Shortest Walk problem which can be solved in polynomial time, that the Time Conditioned Shortest Walk (TCSW) problem is NP-Hard, and is hard to approximate to factor [Formula] for T [≥] 3 and{varepsilon} > 0. Lastly, we develop an integer linear program to solve a generalized version of TCSW, and demonstrate its ability to reach optimality with instances of the human protein interaction network. ConclusionWe demonstrate that when extending the shortest walk problem in computational biology to account for multiple ordered conditions, the problem not only becomes hard to solve, but hard to approximate, a limitation which we address via a new solver. From this narrow definition of TCSW, we relax the constraint of time consistency within the shortest walk, deriving a direct relationship between hardness of approximation and the allowable step size in our walk between time conditioned networks. Lastly we briefly explore a variety of alternative formulations for this problem, providing insight into both tractable and intractable variants. AvailabilityOur solver for the general k-Time Condition Shortest Walk problem is available at https://github.com/YosefLab/temporal_condition_shortest_walk

bioinformatics↗

An Empirical Bayes Method for Differential Expression Analysis of Single Cells with Deep Generative Models

AO_SCPLOWBSTRACTC_SCPLOWDetecting differentially expressed genes is important for characterizing subpopulations of cells. In scRNA-seq data, however, nuisance variation due to technical factors like sequencing depth and RNA capture efficiency obscures the underlying biological signal. Deep generative models have been extensively applied to scRNA-seq data, with a special focus on embedding cells into a low-dimensional latent space and correcting for batch effects. However, little attention has been given to the problem of utilizing the uncertainty from the deep generative model for differential expression. Furthermore, the existing approaches do not allow controlling for the effect size or the false discovery rate. Here, we present lvm-DE, a generic Bayesian approach for performing differential expression from using a fitted deep generative model, while controlling the false discovery rate. We apply the lvm-DE framework to scVI and scSphere, two deep generative models. The resulting approaches outperform the state-of-the-art methods at estimating the log fold change in gene expression levels, as well as detecting differentially expressed genes between subpopulations of cells.

bioinformatics↗

Identifying systematic variation at the single-cell level by leveraging low-resolution population-level data

A major limitation in single-cell genomics is a lack of ability to conduct cost-effective population-level studies. As a result, much of the current research in single-cell genomics focuses on biological processes that are broadly conserved across individuals, such as cellular organization and tissue development. This limitation prevents us from studying the etiology of experimental or clinical conditions that may be inconsistent across individuals owing to molecular variation and a wide range of effects in the population. In order to address this gap, we developed "kernel of integrated single cells" (Keris), a novel model-based framework to inform the analysis of single-cell gene expression data with population-level effects of a condition of interest. By inferring cell-type-specific moments and their variation across conditions using large tissue-level bulk data representing a population, Keris allows us to generate testable hypotheses at the single-cell level that would otherwise require collecting single-cell data from a large number of donors. Within the Keris framework, we show how the combination of low-resolution, large bulk data with small but high-resolution single-cell data enables the identification of changes in cell-subtype compositions and the characterization of subpopulations of cells that are affected by a condition of interest. Using Keris we estimate linear and non-linear age-associated changes in cell-type expression in large bulk peripheral blood mononuclear cells (PBMC) data. Combining with three independent single-cell PBMC datasets, we demonstrate that Keris can identify changes in cell-subtype composition with age and capture cell-type-specific subpopulations of senescent cells. This demonstrates the promise of enhancing single-cell data with population-level information to study compositional changes and to profile condition-affected subpopulations of cells, and provides a potential resource of targets for future clinical interventions.

genomics↗

Theoretical Guarantees for Phylogeny Inference from Single-Cell Lineage Tracing

CRISPR-Cas9 lineage tracing technologies have emerged as a powerful tool for investigating development in single-cell contexts, but exact reconstruction of the underlying clonal relationships in experiment is plagued by data-related complications. These complications are functions of the experimental parameters in these systems, such as the Cas9 cutting rate, the diversity of indel outcomes, and the rate of missing data. In this paper, we develop two theoretically grounded algorithms for reconstruction of the underlying phylogenetic tree, as well as asymptotic bounds for the number of recording sites necessary for exact recapitulation of the ground truth phylogeny at high probability. In doing so, we explore the relationship between the problem difficulty and the experimental parameters, with implications for experimental design. Lastly, we provide simulations validating these bounds and showing the empirical performance of these algorithms. Overall, this work provides a first theoretical analysis of phylogenetic reconstruction in the CRISPR-Cas9 lineage tracing technology.

bioinformatics↗

Hepatitis C Virus Infects and Perturbs Liver Stem Cells

Hepatitis C virus (HCV) is the leading cause of death from liver disease. How HCV infection causes lasting liver damage and increases cancer risk beyond viral clearance remains unclear. We identify bipotent liver stem cells as novel targets for HCV infection, and their erroneous differentiation as the potential cause of impaired liver regeneration and cancer development. We show 3D organoids generated from liver stem cells from actively HCV-infected individuals carry replicating virus and maintain low-grade infection over months. Organoids can be infected with a primary HCV isolate. Virus-inclusive single-cell RNA-sequencing uncovered extensive transcriptional reprogramming in HCV+ cells supporting hepatocytic differentiation, cancer stem cell development and viral replication while stem cell proliferation and interferon signaling are disrupted. Our data adds a pathogenesis factor - infection of liver stem cells - to the biology of HCV infection that explains persistent liver damage and enhanced cancer risk through an altered stem cell state.

microbiology↗

Lineage Recording Reveals the Phylodynamics, Plasticity and Paths of Tumor Evolution

Tumor evolution is driven by the progressive acquisition of genetic and epigenetic alterations that enable uncontrolled growth, expansion to neighboring and distal tissues, and therapeutic resistance. The study of phylogenetic relationships between cancer cells provides key insights into these processes. Here, we introduced an evolving lineage-tracing system with a single-cell RNA-seq readout into a mouse model of Kras;Trp53(KP)-driven lung adenocarcinoma which enabled us to track tumor evolution from single transformed cells to metastatic tumors at unprecedented resolution. We found that loss of the initial, stable alveolar-type2-like state was accompanied by transient increase in plasticity. This was followed by adoption of distinct fitness-associated transcriptional programs which enable rapid expansion and ultimately clonal sweep of rare, stable subclones capable of metastasizing to distant sites. Finally, we showed that tumors develop through stereotypical evolutionary trajectories, and perturbing additional tumor suppressors accelerates tumor progression by creating novel evolutionary paths. Overall, our study elucidates the hierarchical nature of tumor evolution, and more broadly enables the in-depth study of tumor progression.

cancer biology↗

PhyloVision: Interactive Software for Integrated Analysis of Single-Cell Transcriptomic and PhylogeneticData

Recent advances in CRISPR-Cas9 engineering and single-cell assays have enabled the simultaneous measurement of single-cell transcriptomic and phylogenetic profiles. However, there are few computational tools enabling users to integrate and derive insight from a joint analysis of these two modalities. Here, we describe PhyloVision: an open source software for interactively exploring data from both modalities and for identifying and interpreting heritable gene modules whose concerted expression are associated with phylogenetic relationships. PhyloVision provides a feature-rich, interactive, and shareable web-based report for investigating these modules, while also supporting several other data and meta-data exploration capabilities. We demonstrate the utility of PhyloVision using a published dataset of metastatic lung adenocarcinoma cells, whose phylogeny was resolved using a CRISPR/Cas9-based lineage-tracing system. Together, we anticipate that PhyloVision and the methods it implements will be a useful resource for scalable and intuitive data exploration for any assay that simultaneously measures cell state and lineage.

bioinformatics↗

MultiVI: deep generative model for the integration of multi-modal data

Jointly profiling the transcriptional and chromatin accessibility landscapes of single-cells is a powerful technique to characterize cellular populations. Here we present MultiVI, a probabilistic model to analyze such multiomic data and integrate it with single modality datasets. MultiVI creates a joint representation that accurately reflects both chromatin and transcriptional properties of the cells even when one modality is missing. It also imputes missing data, corrects for batch effects and is available in the scvi-tools framework: https://docs.scvi-tools.org/.

bioinformatics↗

Identifying cell-state associated alternative splicing events and their co-regulation

Alternative splicing shapes the transcriptome and contributes to each cells unique identity, but single-cell RNA sequencing has struggled to capture the impact of alternative splicing. We previously showed that low recovery of mRNAs from single cells led to erroneous conclusions about the cell-to-cell variability of alternative splicing (1). Here, we present a method, Psix, to confidently identify splicing that changes across a landscape of single cells, using a probabilistic model that is robust against the data limitations of scRNA-seq. Its autocorrelation-inspired approach finds patterns of alternative splicing that correspond to patterns of cell identity, such as cell type or developmental stage, without the need for explicit cell clustering, labeling, or trajectory inference. Applying Psix to data that follow the trajectory of mouse brain development, we identify exons whose alternative splicing patterns cluster into modules of co-regulation. We show that the exons in these modules are enriched for binding by distinct neuronal splicing factors, and that their changes in splicing correspond to changes in expression of these splicing factors. Thus, Psix reveals cell-type-dependent splicing patterns and the wiring of the splicing regulatory networks that control them. Our new method will enable scRNA-seq analysis to go beyond transcription to understand the roles of post-transcriptional regulation in determining cell identity.

genomics↗

Single-cell multi-omic analysis of thymocyte development reveals NFAT as adriver of CD4/CD8 lineage commitment

The development of CD4 and CD8 T cells in the thymus is critical to adaptive immunity and is widely studied as a model of lineage commitment. Recognition of self-MHCI/II by the T cell antigen receptor (TCR) determines the lineage choice, but how distinct TCR signals drive transcriptional programs of lineage commitment remains largely unknown. We applied CITE-seq to measure RNA and surface proteins in thymocytes from wild-type and lineage-restricted mice to generate a comprehensive timeline of cell state for each lineage. These analyses revealed a sequential process whereby all thymocytes initiate CD4 lineage differentiation during an initial wave of TCR signaling, followed by a second TCR signaling wave that coincides with CD8 lineage specification. CITE-seq and pharmaceutical inhibition experiments implicate a TCR/calcineurin/NFAT/GATA3 axis in driving the CD4 fate. Overall, our data suggest that multiple redundant mechanisms contribute to the accuracy and efficiency of the lineage choice.

bioinformatics↗