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Park, H. J.

Publications and source records attributed to Park, H. J..

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Causal inference using deep-learning variable selection identifies and incorporates direct and indirect causalities in complex biological systems

In complex diseases, causal structure learning across biological variables is critical to identify modifiable triggers or potential therapeutic agents. A limitation of existing causal learning methods is that they cannot identify indirect causal relations, those that would interact through latent mediating variables. We developed the first computational method that identifies both direct and indirect causalities, causal inference using deep-learning variable-selection (causalDeepVASE). To accurately identify indirect causalities and incorporate them with direct causalities, causalDeepVASE develops a deep neural network approach and extends a flexible causal inference method. In simulated and biological data of various contexts, causalDeepVASE outperforms existing methods in identifying expected or validated causal relations. Further, causalDeepVASE facilitates a systematic understanding of complex diseases. For example, causalDeepVASE uniquely identified a possible causal relation between IFN{gamma} and creatinine suggested in a polymicrobial sepsis model. In future biomedical studies, causalDeepVASE can facilitate the identification of driver genes and therapeutic agents.

bioinformatics↗

Evolution of irreversible somatic differentiation

A key innovation emerging in complex animals is irreversible somatic differentiation: daughters of a vegetative cell perform a vegetative function as well, thus, forming a somatic lineage that can no longer be directly involved in reproduction. Primitive species use a different strategy: vegetative and reproductive tasks are separated in time rather than in space. Starting from such a strategy, how is it possible to evolve life forms which use some of their cells exclusively for vegetative functions? Here, we developed an evolutionary model of development of a simple multicellular organism and found that three components are necessary for the evolution of irreversible somatic differentiation: (i) costly cell differentiation, (ii) vegetative cells that significantly improve the organisms performance even if present in small numbers, and (iii) large enough organism size. Our findings demonstrate how an egalitarian development typical for loose cell colonies can evolve into germ-soma differentiation dominating metazoans.

evolutionary biology↗

A three-dimensional Air-Liquid Interface Culture Model for the Study of Epstein-Barr virus Infection in the Nasopharynx

Epstein-Barr virus (EBV) infection is ubiquitous in humans and is associated with the cancer, nasopharyngeal carcinoma. EBV replicates in the differentiated layers of stratified keratinocytes but whether the other cell types of the airway epithelium are susceptible to EBV is unknown. Here, we demonstrate with primary nasopharyngeal cells grown at the air-liquid interface that the pseudostratified epithelium can be susceptible to EBV infection and we report that susceptible cell types with distinct EBV transcription profiles can be identified by single-cell RNA-sequencing. Although EBV infection in the nasopharynx has evaded detection in asymptomatic carriers, these findings demonstrate that EBV latent and lytic infection can occur in the cells of the nasopharyngeal epithelium.

microbiology↗

Identifying genes and cell types with dynamic alternative polyadenylation in multi-cluster single-cell transcriptomics data

Alternative polyadenylation (APA) causes shortening or lengthening of the 3-untranslated region (3-UTR) of genes across multiple cell types. Bioinformatic tools have been developed to identify genes that are affected by APA (APA genes) in single-cell RNA-Seq (scRNA-Seq) data. However, they suffer from low power, and they cannot identify APA genes specific to each cell type (cell-type-specific APA) when multiple cell types are analyzed. To address these limitations, we developed scMAPA that systematically integrates two novel steps. First, scMAPA quantifies 3-UTR long and short isoforms without requiring assumptions on the read density shape of input data. Second, scMAPA estimates the significance of the APA genes for each cell type while controlling confounders. In the analyses on our novel simulation data and human peripheral blood mono cellular data, scMAPA showed enhanced power in identifying APA genes. Further, in mouse brain data, scMAPA identifies cell-type-specific APA genes, improving interpretability for the cell-type-specific function of APA. We further showed that this improved interpretability helps to understand a novel role of APA on the interaction between neurons and blood vessels, which is critical to maintaining the operational condition of brains. With high sensitivity and interpretability, scMAPA shed novel insights into the function of dynamic APA in complex tissues. Key PointsO_LIWe developed a bioinformatic tool, scMAPA, that identifies dynamic APA across multiple cell types and a novel simulation pipeline to assess performance of such tools in APA calling. C_LIO_LIIn simulation data of various scenarios from our novel simulation pipeline, scMAPA achieves sensitivity with a minimal loss of specificity. C_LIO_LIIn human peripheral blood monocellular data, scMAPA identifies APA genes accurately and robustly, finding unique associations of APA with hematological processes. C_LIO_LIscMAPA identifies APA genes specific to each cell type in mouse brain data while controlling confounders that sheds novel insights into the complex molecular processes. C_LI

bioinformatics↗

How sequence populations persist inside a genome

Compared to their eukaryotic counterparts, bacterial genomes are small and contain extremely tightly packed genes. Therefore, discovering a large number of short repetitive sequences in the genomes of Pseudomonads and Enterobacteria is unexpected. These sequences can independently replicate in the host genome and form populations that persist for millions of years. Here we model the interactions of intragenomic sequence populations with the bacterial host. In a simple model, sequence populations either expand until they drive the host to extinction or the sequence population gets purged from the genome. Including horizontal gene transfer does not change the qualitative outcome of the model and leads to the extinction of the sequence population. However, a sequence population can be stably maintained, if each sequence provides a benefit that decreases with increasing sequence population size. But concurrently, the replication of the sequence population needs to be costly to the host. Surprisingly, in regimes where horizontal gene transfer plays a role, the benefit conferred by the sequence population does not have to exceed the damage it causes. Together, our analyses provide a plausible scenario for the persistence of sequence populations in bacterial genomes. More importantly, we hypothesize a limited biologically relevant parameter range, which can be tested in future experiments.

evolutionary biology↗

Why is cyclic dominance so rare?

Natural populations can contain multiple types of coexisting individuals. How does natural selection maintain such diversity within and across populations? A popular theoretical basis for the maintenance of diversity is cyclic dominance, illustrated by the rock-paper-scissor game. However, it appears difficult to find cyclic dominance in nature. Why is this case? Focusing on continuously produced novel mutations, we theoretically addressed the rareness of cyclic dominance. We developed a model of an evolving population and studied the formation of cyclic dominance. Our results showed that the chance for cyclic dominance to emerge is lower when the newly introduced type is similar to existing types, whereas the introduction of an unrelated type improves these chances. This suggests that cyclic dominance is more likely to evolve through the assembly of unrelated types whereas it rarely evolves within a community of similar types.

evolutionary biology↗

The birth of a bacterial tRNA gene

Organisms differ in the types and numbers of tRNA genes that they carry. While the evolutionary mechanisms behind tRNA gene set evolution have been investigated theoretically and computationally, direct observations of tRNA gene set evolution remain rare. Here, we report the evolution of a tRNA gene set in laboratory populations of the bacterium Pseudomonas fluorescens SBW25. The growth defect caused by deleting the single-copy tRNA gene, serCGA, is rapidly compensated by large-scale (45-290 kb) duplications in the chromosome. Each duplication encompasses a second, compensatory tRNA gene (serTGA) and is associated with a rise in tRNA-Ser(UGA) in the mature tRNA pool. We postulate that tRNA-Ser(CGA) elimination increases the translational demand for tRNA-Ser(UGA), a pressure relieved by increasing serTGA copy number. This work demonstrates that tRNA gene sets can evolve through duplication of existing tRNA genes, a phenomenon that may contribute to the presence of multiple, identical tRNA gene copies within genomes.

evolutionary biology↗

Acute characterization of tissue and functional deficits in a clinically translatable pig model of ischemic stroke

The acute stroke phase is a critical time frame used to evaluate stroke severity, therapeutic options, and prognosis while also serving as a major target for the development of diagnostics. To better understand stroke pathophysiology and to enhance the development of treatments, our group developed a translational pig ischemic stroke model. In this study, the evolution of acute ischemic stroke tissue damage, immune response, and functional deficits were further characterized in the pig model. Stroke was induced by middle cerebral artery occlusion in Landrace pigs. At 24 hours post-stroke, magnetic resonance imaging revealed a decrease in ipsilateral diffusivity and an increase in hemispheric swelling and intracranial hemorrhage resulting in notable midline shift. Stroke negatively impacted white matter integrity leading to decreased fractional anisotropy. Similar to acute clinical patients, stroked pigs showed a reduction in circulating lymphocytes and a surge in neutrophils and band cells. Functional responses corresponded with structural changes with reduced exploration in open field testing and impairments in spatiotemporal gait parameters. This novel, acute ischemia characterization provides important insights into tissue and functional level changes in a pig model that can be used to identify treatment targets and future testing of therapeutics and diagnostics.

neuroscience↗

Eco-evolutionary spatial dynamics of non-linear social dilemmas

Spatial dynamics can promote the evolution of cooperation. While dispersal processes have been studied in simple evolutionary games, real-world social dilemmas are much more complicated. The public good, in many cases, does not increase linearly as per the investment in it. When the investment is low, for example, every additional unit of the investment may help a lot to increase the public good, but the effect vanishes as the number of investments increase. Such non-linear behaviour is the norm rather than an exception in a variety of social as well as biological systems. We take into account the non-linearity in the payoffs of the public goods game as well as the natural demographic effects of population densities. Population density has also been shown to impact the evolution of co-operation. Coupling these non-linear games and population size effect together with an explicitly defined spatial structure brings us one step closer to the complexity of real eco-evolutionary spatial systems. We show how the non-linearity in payoffs, resulting in synergy or discounting of public goods can alter the effective rate of return on the cooperative investment. Synergy or discounting in public goods accumulation affects the resulting spatial structure, not just quantitatively but in some cases, drastically changing the outcomes. In cases where a linear payoff structure would lead to extinction, synergy can support the coexistence of cooperators and defectors. The combined eco-evolutionary trajectory can thus be qualitatively different in cases on non-linear social dilemmas.

evolutionary biology↗

Evolution of simple multicellular life cycles in dynamic environments

The mode of reproduction is a critical characteristic of any species, as it has a strong effect on its evolution. As any other trait, the reproduction mode is subject to natural selection and may adapt to the environment. When the environment varies over time, different reproduction modes could be optimal at different times. The natural response to a dynamic environment seems to be bet hedging, where multiple reproductive strategies are stochastically executed. Here, we develop a framework for the evolution of simple multicellular life cycles in a dynamic environment. We use a matrix population model of undifferentiated multicellular groups undergoing fragmentation and ask which mode maximizes the population growth rate. Counterintuitively, we find that natural selection in dynamic environments generally tends to promote deterministic, not stochastic, reproduction modes.

evolutionary biology↗

Alternative Polyadenylation Modifies Target Sites of MicroRNAs with Clinical Potential for Breast Cancer Progression

BackgroundAlternative polyadenylation (APA) shortens or lengthens the 3-untranslated region (3-UTR) of hundreds of genes in cancer. While APA genes modify microRNA target sites in the 3-UTRs to promote tumorigenesis, previous studies have focused on a subset of the modification landscape.\n\nMethodFor comprehensive understanding of the function of global APA events, we consider the total target site landscape of microRNAs that are significantly and collectively modified by global APA genes. To identify such microRNAs in spite of complex interactions between microRNAs and the APA genes, we developed Probabilistic Inference of MicroRNA Target Site Modification through APA (PRIMATA-APA).\n\nResultsRunning PRIMATA-APA on TCGA breast cancer data, we identified that global APA events concentrate to modify target sites of particular microRNAs (target-site-modified-miRNA or tamoMiRNA). TamoMiRNAs are enriched for microRNAs known to regulate cancer etiology and treatments. Also, their target genes are enriched in cancer-associated pathways, suggesting that APA modifies target sites of tamoMiRNAs to progress tumors. Knockdown of NUDT21, a master 3-UTR regulator in HeLa cells, confirmed the causal role of tamoMiRNAs for tumor growth.\n\nConclusionsFurther, the expressions of tamoMiRNA target genes, enriched in cancer-associated pathways, vary across tumor samples as a function of patient-specific APA events, suggesting that APA is a novel regulatory axis for interpatient tumor heterogeneity.

bioinformatics↗

3ʹ-UTR shortening disrupts ceRNA crosstalk of housekeeping genes resulting in subtype-specific breast cancer development

Shortening of 3'UTRs (3'US) through alternative polyadenylation (APA) is a post-transcriptional mechanism that regulate expression of hundreds of genes in human cancers. In breast cancer, different subtypes of tumor samples, such as estrogen receptor positive and negative (ER+ and ER-), are characterized by distinct molecular mechanisms, suggesting possible differences in the post-transcriptional regulation between the subtype tumors. In this study, based on the profound tumorigenic role of 3'US interacting with competing-endogenous RNA (ceRNA) network (3'US-ceRNA effect), we hypothesize that the 3'US-ceRNA effect drives subtype-specific tumor growth. However, we found that the subtypes are available in different sample size, biasing the ceRNA network size and disabling the fair comparison of the 3'US-ceRNA effect. Using normalized Laplacian Matrix Eigenvalue Distribution, we addressed this bias and built the tumor ceRNA networks comparable between the subtypes. Based on the comparison, we identified a novel role of housekeeping (HK) genes as stable and strong miRNA sponges (sponge HK genes) that synchronize the ceRNA networks of normal samples (adjacent to ER+ and ER- tumor samples). We further found that distinct 3'US events in the ER- tumor break the stable sponge effect of HK genes in a subtype-specific fashion, especially in association with the aggressive and metastatic phenotypes. Knockdown of NUDT21, a master 3'-UTR regulator in HeLa cells, confirmed the causal role of 3'US-ceRNA effect repressing HK genes for tumor growth. In this study, we identified 3'US-ceRNA effect on the sponge HK genes for subtype-specific growth of ER- tumors.

cancer biology↗

Leveraging collective regulatory effects of long-range DNA methylations to predict gene expressions and estimate their effects on phenotypes in cancer

DNA methylation of various genomic regions plays an important role in regulating gene expression in diverse biological contexts. However, most genome-wide studies have focused on the effect of 1) methylation in cis, not in trans and 2) a single CpG, not the collective effects of multiple CpGs, on gene expression. In this study, we developed a statistical machine learning model, geneEXPLORER (gene expression prediction by long-range epigenetic regulation), that quantifies the collective effects of both cis- and trans- methylations on gene expression. By applying geneEXPLORER to The Cancer Genome Atlas (TCGA) breast and lung cancer data, we found that most genes are affected by methylations of as much as 10Mb from promoter regions or more, and the long-range methylation explains 50% of the variation in gene expression on average, far greater than cis-methylation. The highly predictive genes are related to breast cancer, especially oncogenes and suppressor genes. Further, the predicted gene expressions could predict clinical phenotypes such as breast tumor status and estrogen receptor status (AUC=0.999, 0.94 respectively) as accurately as the measured gene expression levels. These results suggest that geneEXPLORER provides a means for accurate imputation of gene expression, which can be further used to predict clinical phenotypes.

bioinformatics↗

Stochastic population dynamics driven by mutant interactors

Spontaneous random mutations are an important source of variation in populations. Many evolutionary models consider mutants with a fixed fitness chosen from a certain fitness distribution without considering any interactions among the residents and mutants. Here, we go beyond this and consider \"mutant interactors\", which lead to new interactions between the residents and invading mutants that can affect the carrying capacity and the extinction risk of populations. We model microscopic interactions between individuals by using a dynamical payoff matrix and analyze the stochastic dynamics of such populations. New interactions drawn from invading mutants can drive the population away from the previous equilibrium, and lead to changes in the population size -- the population size is an evolving property rather than a fixed number or externally controlled variable. We present analytical results for the average population size over time and quantify the extinction risk of the population by the mean time to extinction.

evolutionary biology↗

Targeting glutamine metabolism and redox state for leukemia therapy

Acute myeloid leukemia (AML) is a hematological malignancy characterized by the accumulation of immature myeloid precursor cells. AML is poorly responsive to conventional genotoxic chemotherapy and a diagnosis of AML is usually fatal. More effective and less toxic forms of therapy are desperately needed. AML cells are known to be highly dependent on the amino acid glutamine for their survival. Here, we show that blocking glutamine metabolism through the use of a glutaminase inhibitor (CB-839) significantly impairs antioxidant glutathione production in multiple types of AML, resulting in accretion of mitochondrial reactive oxygen species (mitoROS) and apoptotic cell death. Moreover, glutaminase inhibition makes AML cells susceptible to adjuvant drugs that further perturb mitochondrial redox state, such as arsenic trioxide (ATO) and homoharringtonine (HHT). Indeed, the combination of ATO or HHT with CB-839 exacerbates mitoROS and apoptosis, and leads to more complete cell death in AML cell lines, primary AML patient samples and in vivo using mouse models of AML. In addition, these redox-targeted combination therapies are effective in eradicating acute lymphoblastic leukemia cells in vitro and in vivo. Thus, targeting glutamine metabolism in combination with drugs that perturb mitochondrial redox state represents an effective and potentially widely applicable therapeutic strategy for treating multiple types of leukemia.\n\nKey PointsO_LIGlutaminase inhibition commonly impairs glutathione metabolism and induces mitochondrial oxidative stress in acute myeloid leukemia cells\nC_LIO_LIA glutaminase inhibitor synergizes with pro-oxidant drugs in inducing apoptosis and eliminating leukemia cells in vitro and in vivo\nC_LI

cancer biology↗

Ecological feedback on diffusion dynamics

Spatial patterns are ubiquitous across different scales of organization. Animal coat pattern, spatial organization of insect colonies, and vegetation in arid areas are prominent examples from such diverse ecologies. Typically, pattern formation has been described by reaction-diffusion equations, which considers individuals dispersing between sub-populations of a global pool. This framework applied to public goods game nicely showed the endurance of populations via diffusion and generation of spatial patterns. However, how the spatial characteristics, such as diffusion, are related to the eco-evolutionary process as well as the nature of the feedback from evolution to ecology and vice versa, has been so far neglected. We present a thorough analysis of the ecologically driven evolutionary dynamics in a spatially extended version of ecological public goods games. We show how these evolutionary dynamics feedback into shaping the ecology thus together determining the fate of the system.

evolutionary biology↗

Thrombopoietin signaling to chromatin elicits rapid and pervasive epigenome remodeling within poised chromatin architectures

Thrombopoietin (TPO) is a critical cytokine regulating hematopoietic stem cell maintenance and differentiation into the megakaryocytic lineage. However, the transcriptional and chromatin dynamics elicited by TPO signaling are poorly understood. Here, we study the immediate early transcriptional and cis-regulatory responses to TPO in hematopoietic stem/progenitor cells (HSPCs) and use this paradigm of cytokine signaling to chromatin to dissect the relation between cis-regulatory activity and chromatin architecture. We show that TPO profoundly alters the transcriptome of HSPCs, with key hematopoietic regulators being transcriptionally repressed within 30 minutes of TPO. By examining cis-regulatory dynamics and chromatin architectures, we demonstrate that these changes are accompanied by rapid and extensive epigenome remodeling of cis-regulatory landscapes that is spatially coordinated within topologically associating domains (TADs). Moreover, TPO-responsive enhancers are spatially clustered and engage in preferential homotypic intra- and inter-TAD interactions that are largely refractory to TPO signaling. By further examining the link between cis-regulatory dynamics and chromatin looping, we show that rapid modulation of cis-regulatory activity is largely independent of chromatin looping dynamics. Finally, we show that, although activated and repressed cis-regulatory elements share remarkably similar DNA sequence compositions, transcription factor binding patterns accurately predict rapid cis-regulatory responses to TPO.

genomics↗