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Platig, J.

Publications and source records attributed to Platig, J..

15 recordsLinked to original sources

Explainable machine learning reveals an RBP regulatory logic of exon skipping

RNA binding proteins (RBPs) regulate the life cycle of an mRNA, often through RBP-RNA interactions. This life cycle includes splicing, whereby the intronic sequence of a pre-mRNA is removed and the exons are joined together. However, the patterns of RBP binding that lead to different splicing outcomes are still incompletely understood. Here, we build machine learning models from RBP-RNA binding and knockdown RNA-seq data for over 168 RBPs in two cell lines (HepG2 and K562) to better understand the binding patterns that predict exon skipping, the predominant form of alternative splicing in humans. We show that models trained exclusively on RBP binding patterns are indeed predictive and that a more sophisticated machine learning model (XGBoost) outperforms simpler linear models. In addition, we are able to extract a biologically interpretable logic embedded in these models. We show that SHAP, a machine learning explainability technique, captures activating and repressive behavior of RBP binding that is position-specific. In addition, we find that SHAP values are predictive of changes in unseen splicing events and that SHAP interactions between pairs of RBPs are predictive of protein-protein interactions. Our results demonstrate that using machine learning with interpretability techniques can reveal a regulatory logic of RBP binding. By estimating the impact of an RBP binding site on a splicing event, the SHAP values also provide a directly testable scientific hypothesis. We anticipate that models designed around biological processes and focused on interpretability will yield actionable biological insights both in splicing and genomics generally.

systems biology↗

Complex Traits Heritability is Highly Clustered in the eQTL Bipartite Network

Complex traits are determined by many loci--mostly regulatory elements--that, through combinatorial interactions, can affect multiple traits. Such high levels of epistasis and pleiotropy have been proposed in the omnigenic model and may explain why such a large part of complex trait heritability is usually missed by genome-wide association studies while raising questions about the possibility for such traits to evolve in response to environmental constraints. To explore the molecular bases of complex traits and understand how they can adapt, we systematically analyzed the distribution of SNP heritability for ten traits across 29 tissue-specific Expression Quantitative Trait Locus (eQTL) networks. We find that heritability is clustered in a small number of tissue-specific, functionally relevant SNP-gene modules and that the greatest heritability occurs in local "hubs" that are both the cornerstone of the networks modules and tissue-specific regulatory elements. The network structure could thus both amplify the genotype-phenotype connection and buffer the deleterious effect of the genetic variations on other traits. We confirm that this structure has allowed complex traits to evolve in response to environmental constraints, with the local "hubs" being the preferential targets of past and ongoing directional selection. Together, these results provide a conceptual framework for understanding complex trait architecture and evolution.

systems biology↗

The Network Zoo: a multilingual package for the inference and analysis of biological networks

Inference and analysis of cellular biological networks requires software tools that integrate multi-omic data from various sources. The Network Zoo (netZoo; netzoo.github.io) is an open-source software suite to model biological networks, including context-specific gene regulatory networks and multi-omics partial correlation networks, to conduct differential analyses, estimate community structure, and model the transitions between biological states. The netZoo builds on our ongoing development of network methods, harmonizing the implementations in various computing languages (R, Python, MATLAB, and C) and between methods to allow a better integration of these tools into analytical pipelines. To demonstrate the value of this integrated toolkit, we analyzed the multi-omic data from the Cancer Cell Line Encyclopedia (CCLE) by inferring gene regulatory networks for each cancer cell line and associating network features with other phenotypic attributes such as drug sensitivity. This allowed us to identify transcription factors that play a critical role in both drug resistance and cancer development in melanoma. We also used netZoo to build a pan-cancer, multi-tiered CCLE map and used it to identify known metabolic hallmarks of cancer and to estimate novel context-specific elements that mediate post-transcriptional regulation. Because the netZoo tools are open-source and there is a growing community of both users and developers, we built an ecosystem to support community contributions, share use cases, and visualize networks online. As additional data types become available and our suite of methods grows, we will expand "the zoo" to incorporate an increasingly sophisticated collection of tools for network inference and analysis.

genomics↗

GRAND: A database of gene regulatory network models across human conditions

Gene regulation plays a fundamental role in shaping tissue identity, function, and response to perturbation. Regulatory processes are controlled by complex networks of interacting elements, including transcription factors, miRNAs and their target genes. The structure of these networks helps to determine phenotypes and can ultimately influence the development of disease or response to therapy. We developed GRAND (https://grand.networkmedicine.org) as a database for gene regulatory network models that can be compared between biological states, or used to predict which drugs produce changes in regulatory network structure. The database includes 12,468 genome-scale networks covering 36 human tissues, 28 cancers, 1,378 unperturbed cell lines, as well as 173,013 TF and gene targeting scores for 2,858 small molecule-induced cell line perturbation paired with phenotypic information. GRAND allows the networks to be queried using phenotypic information and visualized using a variety of interactive tools. In addition, it includes a web application that matches disease states to potentially therapeutic small molecule drugs using regulatory network properties. Graphical abstract O_FIG_DISPLAY_L [Figure 1] M_FIG_DISPLAY Modeling gene regulation across human conditions integrates cancer tissues and cell lines, small molecules, and normal tissue networks. C_FIG_DISPLAY

genomics↗

Predicting genotype-specific gene regulatory networks

Understanding how each persons unique genotype influences their individual patterns of gene regulation has the potential to improve our understanding of human health and development and to refine genotype-specific disease risk assessments and treatments. However, the effects of genetic variants are not typically considered when constructing gene regulatory networks, despite the fact that many disease-associated genetic variants are thought to have regulatory effects, including the disruption of transcription factor (TF) binding. We developed EGRET (Estimating the Genetic Regulatory Effect on TFs), which infers a genotype-specific gene regulatory network (GRN) for each individual in a study population. EGRET begins by constructing a genotype-informed TF-gene prior network derived using TF motif predictions, eQTL data, individual genotypes, and the predicted effects of genetic variants on TF binding. It then uses message passing to integrate this prior network with gene expression and TF protein-protein interaction data to produce a refined, genotype-specific regulatory network. We used EGRET to infer GRNs for two blood-derived cell lines and identified genotype-associated, cell-line specific regulatory differences that we subsequently validated using allele-specific expression, chromatin accessibility QTLs, and differential ChIP-seq TF binding. We also inferred EGRET GRNs for three cell types from each of 119 individuals and identified cell type-specific regulatory differences associated with diseases related to those cell types. EGRET is, to our knowledge, the first method that infers networks that reflect individual genetic variation in a way that provides insight into genetic regulatory associations that drive complex phenotypes. EGRET is available through the Network Zoo R package (netZooR v0.9; netzoo.github.io).

systems biology↗

Gene Regulatory Network Inference as Relaxed Graph Matching

Gene regulatory network inference is instrumental to the discovery of genetic mechanisms driving diverse diseases, including cancer. Here, we present a theoretical framework for PANDA, an established method for gene regulatory network inference. PANDA is based on iterative message passing updates that resemble the gradient descent of an optimization problem, OTTER, which can be interpreted as relaxed inexact graph matching between a gene-gene co-expression and a protein-protein interaction matrix. The solutions of OTTER can be derived explicitly and inspire an alternative spectral algorithm, for which we can provide network recovery guarantees. We compare different solution approaches of OTTER to other inference methods using three biological data sets, which we make publicly available to offer a new application venue for relaxed graph matching in gene regulatory network inference. We find that using modern gradient descent methods with superior convergence properties solving OTTER outperforms state-of-the-art gene regulatory network inference methods in predicting binding of transcription factors to regulatory regions.

bioinformatics↗

Multi-omic regulatory networks capture downstream effects of kinase inhibition in Mycobacterium tuberculosis

The ability of Mycobacterium tuberculosis (Mtb) to adapt to diverse stresses in its host environment is crucial for pathogenesis. Two essential Mtb serine/threonine protein kinases, PknA and PknB, regulate cell growth in response to environmental stimuli, but little is known about their downstream ef-fects. By combining RNA-Seq data, following treatment with either a PknA/PknB inhibitor or an inactive control, with publicly available ChIP-Seq and protein-protein interaction data, we show that the Mtb transcription factor (TF) regulatory network propagates the effects of kinase inhibition and leads to widespread changes in regulatory programs involved in cell wall integrity, stress response, and energy production, among others. We also observe that changes in TF regulatory activity correlate with kinase-specific phosphorylation of those TFs. In addition to characterizing the downstream regulatory effects of PknA/PknB inhibition, this demonstrates the need for regulatory network approaches that can incorporate signal-driven transcription factor modifications.

systems biology↗

Connectivity of variants in eQTL networks dictates reproducibility and functionality

Network analyses are a natural approach for identifying genetic variants and genes that work together to drive disease phenotypes. The relationship between SNPs and genes, captured in expression quantitative trait locus (eQTL) analysis, can be represented as a network with edges connecting SNPs and genes. Existing network methods treat such edges as fixed and known when they are most often thresholded estimates from eQTL regression. We consider various characterizations of an essential feature of nodes of eQTL networks, their degree centrality, that retains different data on eQTLs. We define the network metric of degree to be estimated by false discovery rates, test statistics, and p-values of the eQTL regressions in order to represent how central and potentially influential a SNP is to the network. We calculate degree metrics for data from 21 tissues from the GTEx project to assess the reproducibility, correlation across tissues, and, functional importance of degree.

systems biology↗

Nongenic cancer-risk SNPs affect oncogenes, tumor suppressor genes, and immune function

Genome-wide associations studies (GWASes) have identified many germline genetic variants that are associated with an increased risk of developing cancer. However, how these single nucleotide polymorphisms (SNPs) alter biological function in a way that increases cancer risk is still largely unknown. We used a systems biology approach to analyze the regulatory role and functional associations of cancer-risk SNPs in thirteen distinct tissues. Using data from the Genotype-Tissue Expression (GTEx) project, we performed an expression quantitative trait locus (eQTL) analysis, keeping both cis- and trans-eQTLs, and representing those significant associations as edges in tissue-specific eQTL bipartite networks. We find that each network is organized into highly modular communities that group sets of SNPs together with functionally-related collections of genes. We mapped cancer-risk SNPs to each tissue-specific eQTL network. Although we find in each tissue that cancer-risk SNPs are distributed across the network, they are not uniformly distributed. Rather they are significantly over-represented in a small number of communities. This includes communities enriched for immune response processes as well as communities representing tissue-specific functions. Moreover, cancer-risk SNPs are over-represented in the central \"cores\" of communities, meaning they are more likely to influence the expression of many genes within the same community, thus affecting biological processes. And finally, we find that cancer-risk SNPs preferentially target oncogenes and tumor suppressor genes, suggesting non-genic mutations may still alter the effects of these key cancer-associated genes. This bipartite eQTL network approach provides a new way of understanding genetic effects on cancer risk and provides a biological context for interpreting the results of GWAS cancer studies.

cancer biology↗

Histopathological image QTL discovery of thyroid autoimmune disease variants

Genotype-to-phenotype association studies typically use macroscopic physiological measurements or molecular readouts as quantitative traits. There are comparatively few suitable quantitative traits available between cell and tissue length scales, a limitation that hinders our ability to identify variants affecting phenotype at many clinically informative levels. Here we show that quantitative image features, automatically extracted from histopathological imaging data, can be used for image Quantitative Trait Loci (iQTL) mapping and variant discovery. Using thyroid pathology images, clinical metadata, and genomics data from the Genotype and Tissue Expression (GTEx) project, we establish and validate a quantitative imaging biomarker for immune cell infiltration. A total of 100,215 variants were selected for iQTL profiling, and tested for genotype-phenotype associations with our quantitative imaging biomarker. Significant associations were found in HDAC9 and TXNDC5. We validated the TXNDC5 association using GTEx cis-expression QTL data, and an independent hypothyroidism dataset from the Electronic Medical Records and Genomics network.\n\nOne Sentence SummaryWe use a histopathological image QTL analysis to identify genomic variants associated with immune cell infiltration.

genomics↗

Understanding Tissue-specific Gene Regulation

Although all human tissues carry out common processes, tissues are distinguished by gene expres-sion patterns, implying that distinct regulatory programs control tissue-specificity. In this study, we investigate gene expression and regulation across 38 tissues profiled in the Genotype-Tissue Expression project. We find that network edges (transcription factor to target gene connections) have higher tissue-specificity than network nodes (genes) and that regulating nodes (transcription factors) are less likely to be expressed in a tissue-specific manner as compared to their targets (genes). Gene set enrichment analysis of network targeting also indicates that regulation of tissue-specific function is largely independent of transcription factor expression. In addition, tissue-specific genes are not highly targeted in their corresponding tissue-network. However, they do assume bottleneck positions due to variability in transcription factor targeting and the influence of non-canonical regulatory interactions. These results suggest that tissue-specificity is driven by context-dependent regulatory paths, providing transcriptional control of tissue-specific processes.

genomics↗

A network-based approach to eQTL interpretation and SNP functional characterization

Expression quantitative trait locus (eQTL) analysis associates genotype with gene expression, but most eQTL studies only include cis-acting variants and generally examine a single tissue. We used data from 13 tissues obtained by the Genotype-Tissue Expression (GTEx) project v6.0 and, in each tissue, identified both cis- and trans-eQTLs. For each tissue, we represented significant associations between single nucleotide polymorphisms (SNPs) and genes as edges in a bipartite network. These networks are organized into dense, highly modular communities often representing coherent biological processes. Global network hubs are enriched in distal gene regulatory regions such as enhancers, but are devoid of disease-associated SNPs from genome wide association studies. In contrast, local, community-specific network hubs (core SNPs) are preferentially located in regulatory regions such as promoters and enhancers and highly enriched for trait and disease associations. These results provide help explain how many weak-effect SNPs might together influence cellular function and phenotype.

genomics↗

Tissue-aware RNA-Seq processing and normalization for heterogeneous and sparse data

Although ultrahigh-throughput RNA-Sequencing has become the dominant technology for genome-wide transcriptional profiling, the vast majority of RNA-Seq studies typically profile only tens of samples, and most analytical pipelines are optimized for these smaller studies. However, projects are generating ever-larger data sets comprising RNA-Seq data from hundreds or thousands of samples, often collected at multiple centers and from diverse tissues. These complex data sets present significant analytical challenges due to batch and tissue effects, but provide the opportunity to revisit the assumptions and methods that we use to preprocess, normalize, and filter RNA-Seq data - critical first steps for any subsequent analysis. We find analysis of large RNA-Seq data sets requires both careful quality control and that one account for sparsity due to the heterogeneity intrinsic in multi-group studies. An R package instantiating our method for large-scale RNA-Seq normalization and preprocessing, YARN, is available at bioconductor.org/packages/yarn.\n\nHighlightsO_LIOverview of assumptions used in preprocessing and normalization\nC_LIO_LIPipeline for preprocessing, quality control, and normalization of large heterogeneous data\nC_LIO_LIA Bioconductor package for the YARN pipeline and easy manipulation of count data\nC_LIO_LIPreprocessed GTEx data set using the YARN pipeline available as a resource\nC_LI

bioinformatics↗

Transcriptional landscape of cell lines and their tissues of origin

Cell lines are an indispensable tool in biomedical research and often used as surrogates for tissues. An important question is how well a cell lines transcriptional and regulatory processes reflect those of its tissue of origin. We analyzed RNA-Seq data from GTEx for 127 paired Epstein-Barr virus transformed lymphoblastoid cell lines and whole blood samples; and 244 paired fibroblast cell lines and skin biopsies. A combination of gene expression and network analyses shows that while cell lines carry the expression signatures of their primary tissues, albeit at reduced levels, they also exhibit changes in their patterns of transcription factor regulation. Cell cycle genes are over-expressed in cell lines compared to primary tissue, and they have a reduction of repressive transcription factor targeting. Our results provide insight into the expression and regulatory alterations observed in cell lines and suggest that these changes should be considered when using cell lines as models.\n\nHighlightsO_LICell lines differ from their source tissues in gene expression and regulation\nC_LIO_LIDistinct cell lines share altered patterns of cell cycle regulation\nC_LIO_LICell cycle genes are less strongly targeted by repressive TFs in cell lines\nC_LIO_LICell lines share expression with their source tissue, but at reduced levels\nC_LI

genomics↗

Sexual dimorphism in gene expression and regulatory networks across human tissues

Sexual dimorphism manifests in many diseases and may drive sex-specific therapeutic responses. To understand the molecular basis of sexual dimorphism, we conducted a comprehensive assessment of gene expression and regulatory network modeling in 31 tissues using 8716 human transcriptomes from GTEx. We observed sexually dimorphic patterns of gene expression involving as many as 60% of autosomal genes, depending on the tissue. Interestingly, sex hormone receptors do not exhibit sexually dimorphic expression in most tissues; however, differential network targeting by hormone receptors and other transcription factors (TFs) captures their downstream sexually dimorphic gene expression. Furthermore, differential network wiring was found extensively in several tissues, particularly in brain, in which not all regions exhibit strong differential expression. This systems-based analysis provides a new perspective on the drivers of sexual dimorphism, one in which a repertoire of TFs plays important roles in sex-specific rewiring of gene regulatory networks.\n\nHighlightsO_LISexual dimorphism manifests in both gene expression and gene regulatory networks\nC_LIO_LISubstantial sexual dimorphism in regulatory networks was found in several tissues\nC_LIO_LIMany differentially regulated genes are not differentially expressed\nC_LIO_LISex hormone receptors do not exhibit sexually dimorphic expression in most tissues\nC_LI

genomics↗