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Craig, J. M.

Publications and source records attributed to Craig, J. M..

16 recordsLinked to original sources

De novo transformer modeling improves recovery of genetic cell types from sparse single-cell RNA sequencing

Single-cell RNA sequencing (scRNA-seq) simultaneously provides gene-expression profiles and genetic variants from individual cells, creating an opportunity to relate cellular phenotypes to their somatic evolutionary histories. However, delineation of genetic type (GTs) from scRNA-seq remains difficult because most variant positions are unobserved in individual cells and the observed base calls contain substantial false-positive and false-negative errors. We evaluated some existing phylogenetic and imputation methods using one simulated dataset and two empirical tumor datasets. We found that extreme sparsity prevented reliable recovery of known or independently inferred GTs when multiple GTs were present. This led us to adapt the STICI transformer architecture to train a separate model de novo on each sparse cell-variant (CV) matrix. These data-specific models predicted millions of missing bases, greatly reducing matrix sparsity. Phylogenetic analyses of the imputed CV matrices showed substantially improved recovery of GTs in both simulated and empirical datasets. In the empirical dataset, transformer-based analysis also suggested finer-scale genetic structure within some previously reported GTs that was not apparent with the existing methods. These results demonstrate that highly sparse scRNA-seq datasets contain substantially more recoverable lineage information than previously appreciated and that de novo transformer modeling provides an effective approach for recovering much of this hidden information. Nevertheless, sequencing errors persisted, limiting reconstruction of cellular lineage structure and leaving significant room for methodological improvement before expression phenotypes can be examined reliably in the context of their cellular evolutionary relationships.

bioinformatics↗

Single-molecule nanopore-tweezers analysis of transcription elongation by intact and "stalk-less" yeast RNA polymerase II

Single-molecule picometer-resolution nanopore tweezers (SPRNT) enables monitoring of translocation of a nucleic-acid motor protein on a nucleic-acid track with sequence registration, sub-nucleotide spatial resolution, sub-millisecond temporal resolution, and the ability to apply forces that assist or oppose translocation. Recently, we used SPRNT to analyze the translocation of single molecules of Escherichia coli RNA polymerase relative to the DNA template strand during transcription elongation, and we directly detected sequence-dependent pausing and formation of a "half-translocated state" at the E. coli yrbL consensus pause element. Here, we apply SPRNT to analyze the translocation of single molecules of yeast RNA polymerase II (Pol II) relative to the DNA template strand during transcription elongation with single-nucleotide spatial resolution and millisecond-scale temporal resolution at biologically relevant, saturating substrate concentrations; we compare translocation by intact, 12-subunit Pol II to translocation by a 10-subunit Pol II sub-assembly lacking the dissociable Rpb4-Rpb7 Pol II "stalk"; and we assess possible pausing by intact Pol II and stalk-less Pol II at the E. coli yrbL consensus pause element. The results show that intact Pol II elongates more rapidly than stalk-less Pol II and show that neither intact Pol II nor stalk-less Pol II pauses at the E. coli yrbL consensus pause element. One-sentence summaryNanopore tweezers enable monitoring of translocation of RNA polymerase II relative to DNA in transcription elongation with single-nucleotide spatial resolution and millisecond-scale temporal resolution at biologically relevant, saturating substrate concentrations.

molecular biology↗

Longitudinal DNA methylation dynamics distinguish Persistent and Remitted ADHD in childhood and adolescence

Attention-deficit/hyperactivity disorder (ADHD) is a neurodevelopmental disorder, with symptoms that remit or persist over time. Biological mechanisms underlying symptom change remain poorly understood, though epigenetic processes, like DNA methylation (DNAm), may serve as dynamic biomarkers of clinical outcomes. We examined change in DNAm in children and adolescents with and without ADHD, including differences between remitted and persistent ADHD. MethodsWe analyzed 219 saliva samples from 94 participants (aged 9.5-14.5 years) attending 2 to 3 waves of NICAP. DNAm was profiled using the Infinium MethylationEPIC BeadChip. Linear mixed models adjusted for age, sex, medication, batch and cell-proportion assessed longitudinal change. Comparisons included (1) all ADHD cases versus controls, (2) persistent or remitted ADHD versus controls, and (3) persistent versus remitted ADHD. False discovery rate correction controlled for multiple testing (FDR p<0.05). ResultsNo CpGs were statistically different between ADHD and controls, after correction. Compared to controls, the average DNAm at 5 sites was statistically different in persistent or remitted ADHD, and methylation of 3 additional CpGs differentially changed over time in persistent ADHD. Remitted differed from persistent ADHD at four CpGs, including cg21443143 (ZFAT), which showed a unique decline over time. Gene enrichment links findings to brain structures and function, though these did not survive multiple testing. ConclusionOur study identified several epigenetic differences between remitted and persistent ADHD outcomes from typical development, and from each other. Given the early stage of this research, our findings warrant further prospective epigenome-wide studies into these diagnostic trajectories.

genomics↗

Integrating Phylogenies with Chronology to Assemble the Tree of Life

Reconstructing the global Tree of Life necessitates computational approaches to integrate numerous molecular phylogenies with limited species overlap into a comprehensive supertree. Our survey of published literature shows that individual phylogenies are frequently restricted to specific taxonomic groups due to the expertise of investigators and molecular evolutionary considerations, resulting in any given species present in a minuscule fraction of phylogenies. We present a novel approach, called the chronological supertree algorithm (Chrono-STA), that can build a supertree of species from such data by using node ages in published molecular phylogenies scaled to time. Chrono-STA builds a supertree of organisms by integrating chronological data from molecular timetrees. It fundamentally differs from existing approaches that generate consensus phylogenies from gene trees with missing taxa, as Chrono-STA does not impute nodal distances, use a guide tree as a backbone, or reduce phylogenies to quartets. Analyses of simulated and empirical datasets show that Chrono-STA can combine taxonomically restricted timetrees with extremely limited species overlap. For such data, approaches that impute missing distances or assemble phylogenetic quartets did not perform well. We conclude that integrating phylogenies via temporal dimension enhances the accuracy of reconstructed supertrees that are also scaled to time.

bioinformatics↗

Direction-aware functional class scoring enrichment analysis of Infinium DNA methylation data

Infinium Methylation BeadChip arrays remain one of the most popular platforms for epigenome-wide association studies, but tools for downstream pathway analysis have their limitations. Functional class scoring (FCS) is a group of pathway enrichment techniques that involve the ranking of genes and evaluation of their collective regulation in biological systems, but the implementations described for Infinium methylation array data do not retain direction information, which is important for mechanistic understanding of genomic regulation. Here, we evaluate several candidate FCS methods that retain directional information. According to simulation results, the best-performing method involves the mean aggregation of probe limma t-statistics by gene followed by a rank-ANOVA enrichment test using the mitch package. This method, which we call "LAM", outperformed an existing over-representation analysis method in simulations, and showed higher sensitivity and robustness in an analysis of real lung tumour-normal paired datasets. Using matched RNA-seq data we examine the relationship of methylation differences at promoters and gene bodies with RNA expression at the level of pathways in lung cancer. To demonstrate the utility of our approach, we apply it to three other contexts where public data were available. Firstly, we examine differential pathway methylation associated with chronological age. Secondly, we investigate pathway methylation differences in infants conceived with in vitro fertilisation. Lastly, we analyse differential pathway methylation in 19 disease states, identifying hundreds of novel associations. These results show LAM is a powerful method for the detection of differential pathway methylation as compared to existing methods. A reproducible vignette is provided to illustrate how to implement this method.

genomics↗

The influence of prenatal alcohol exposure and maternal diet on offspring DNA methylation: a cross-species study

Alcohol consumption in pregnancy can affect genome regulation in the developing offspring but results have been contradictory. We employed a physiologically relevant murine model of short-term moderate prenatal alcohol exposure (PAE) resembling common patterns of alcohol consumption in pregnancy in humans. Early moderate PAE was sufficient to affect site-specific DNA methylation in new-born pups without altering behavioural outcomes in adult littermates. Whole-genome bisulfite sequencing of neonatal brain and liver revealed stochastic influence on DNA methylation that was mostly tissue-specific, with some perturbations likely originating as early as gastrulation. DNA methylation differences were enriched in non-coding genomic regions with regulatory potential indicative of broad effects of alcohol on genome regulation. Replication studies in human cohorts with fetal alcohol spectrum disorder suggested some effects were metastable at genes linked to disease-relevant traits including facial morphology, intelligence, educational attainment, autism, and schizophrenia. In our murine model, a maternal diet high in folate and choline protected against some of the damaging effects of early moderate PAE on DNA methylation. Our studies demonstrate that early moderate exposure is sufficient to affect fetal genome regulation even in the absence of overt phenotypic changes and highlight a role for preventative maternal dietary interventions.

genetics↗

Secondary Structure Detection Through Direct Nanopore RNA Sequencing

Eukaryotic reverse transcriptases (RTs) can have essential or deleterious roles in normal human physiology and disease. Compared to well-studied helicases, it remains unclear how RTs overcome the ubiquitous RNA structural barriers during reverse transcription. Herein, we describe the development of a Mycobacterium smegmatis porin A (MspA) nanopore technique to sequence RNA to quantify the single-molecule kinetics of an RT from Bombyx mori with single-nucleotide resolution. By establishing a quadromer map that correlates RNA sequence and MspA ion current, we were able to quantify the RTs dwell time at every single nucleotide step along its RNA template. By challenging the enzyme with various RNA structures, we found that during cDNA synthesis the RT can sense and actively destabilize RNA structures 11-12 nt downstream of its front boundary. The ability to sequence single molecules of RNA with nanopores paves the way to investigate the single-nucleotide activity of other processive RNA translocases.

biophysics↗

Inhibition of the SARS-CoV-2 helicase at single-nucleotide resolution.

The genome of SARS-CoV-2 encodes for a helicase called nsp13 that is essential for viral replication and highly conserved across related viruses, making it an attractive antiviral target. Here we use nanopore tweezers, a high-resolution single-molecule technique, to gain detailed insight into how nsp13 turns ATP-hydrolysis into directed motion along nucleic acid strands. We measured nsp13 both as it translocates along single-stranded DNA or unwinds short DNA duplexes. Our data confirm that nsp13 uses the inchworm mechanism to move along the DNA in single-nucleotide steps, translocating at ~1000 nt/s or unwinding at ~100 bp/s. Nanopore tweezers high spatio-temporal resolution enables observation of the fundamental physical steps taken by nsp13 even as it translocates at speeds in excess of 1000 nucleotides per second enabling detailed kinetic analysis of nsp13 motion. As a proof-of-principle for inhibition studies, we observed nsp13s motion in the presence of the ATPase inhibitor ATP{gamma}S. Our data reveals that ATP{gamma}S interferes with nsp13s action by affecting several different kinetic processes. The dominant mechanism of inhibition differs depending on the application of assisting force. These advances demonstrate that nanopore tweezers are a powerful method for studying viral helicase mechanism and inhibition.

biophysics↗

UPF1 mutants with intact ATPase but deficient helicase activities promote efficient nonsense-mediated mRNA decay

The conserved RNA helicase UPF1 coordinates nonsense-mediated mRNA decay (NMD) by engaging with mRNAs, RNA decay machinery, and the terminating ribosome. UPF1 ATPase activity is necessary for mRNA target discrimination and completion of decay, but the mechanisms through which UPF1 enzymatic activities such as helicase, translocase, RNP remodeling, and ATPase-stimulated dissociation influence NMD remain poorly defined. Using high-throughput biochemical assays to quantify UPF1 enzymatic activities, we show that UPF1 is only moderately processive (< 200 nt) in physiological contexts and undergoes ATPase-stimulated dissociation from RNA. We combine an in silico screen with these assays to identify and characterize known and novel UPF1 mutants with altered helicase, ATPase, and RNA binding properties. We find that UPF1 mutants with substantially impaired processivity, slower unwinding rate, and reduced mechanochemical coupling (i.e. the ability to harness ATP hydrolysis for work) still support efficient NMD in human cells. These data are consistent with a central role for UPF1 ATPase activity in driving cycles of RNA binding and dissociation to ensure accurate NMD target selection.

molecular biology↗

Sequence-dependent mechanochemical coupling of helicase translocation and unwinding at single-nucleotide resolution.

We used single-molecule nanopore tweezers (SPRNT) to resolve the millisecond single-nucleotide steps of Superfamily 1 helicase PcrA as it translocates on, or unwinds, several kb-long DNA molecules. We recorded over 2 million enzyme steps under various assisting and opposing forces in diverse ATP and ADP conditions to comprehensively explore the mechanochemistry of PcrA motion. Forces applied in SPRNT mimic forces and physical barriers PcrA experiences in vivo, such as when the helicase encounters bound proteins or duplex DNA; we show how PcrAs kinetics change with such stimuli. SPRNT allows for direct association of the underlying DNA sequence with observed enzyme kinetics. Our data reveal that the underlying DNA sequence passing through the helicase strongly influences the kinetics during translocation and unwinding. Surprisingly, unwinding kinetics are not solely dominated by the base-pairs being unwound. Instead, the sequence of the single stranded DNA on which the PcrA walks determines much of the kinetics of unwinding.

biophysics↗

Nanopore tweezers measurements of RecQ conformational changes reveal the energy landscape of helicase motion

Helicases are essential for nearly all nucleic acid processes across the tree of life. Using Nanopore Tweezers we observed the small, fast steps taken by single RecQ helicases as they step along and unwind DNA at ultrahigh spatiotemporal resolution. By directly measuring conformational substates of RecQ we determine the coupling between helicase domain motions and chemical reactions that together produce forward motion along the DNA. Application of assisting and opposing forces shows that RecQ has a highly asymmetric energy landscape that reduces its sensitivity to opposing mechanical forces that could be encountered in vivo by molecular roadblocks such as DNA bound proteins. This energy landscape enables RecQ to maintain speed against an opposing load.

biophysics↗

Meta-analysis of genome-wide DNA methylation and integrative OMICs in human skeletal muscle.

Knowledge of age-related DNA methylation changes in skeletal muscle is limited, yet this tissue is severely affected by aging in humans. Using a large-scale epigenome-wide association study (EWAS) meta-analysis of age in human skeletal muscle from 10 studies (total n = 908 human muscle methylomes), we identified 9,986 differentially methylated regions at a stringent false discovery rate < 0.005, spanning 8,748 unique genes, many of which related to skeletal muscle structure and development. We then integrated the DNA methylation results with known transcriptomic and proteomic age-related changes in skeletal muscle, and found that even though most differentially methylated genes are not altered at the mRNA or protein level, they are nonetheless strongly enriched for genes showing age-related differential expression. We provide here the most comprehensive picture of DNA methylation aging in human skeletal muscle, and have made our results available as an open-access, user-friendly, web-based tool called MetaMeth (https://sarah-voisin.shinyapps.io/MetaMeth/).

genetics↗

An epigenetic clock for skeletal muscle

BackgroundAgeing is associated with DNA methylation changes in all human tissues, and epigenetic markers can estimate chronological age based on DNA methylation patterns across tissues. However, the construction of the original pan-tissue epigenetic clock did not include skeletal muscle samples, and hence exhibited a strong deviation between DNA methylation and chronological age in this tissue. MethodsTo address this, we developed a more accurate, muscle-specific epigenetic clock based on the genome-wide DNA methylation data of 682 skeletal muscle samples from 12 independent datasets (18-89 years old, 22% women, 99% Caucasian), all generated with Illumina HumanMethylation arrays (HM27, HM450 or HMEPIC). We also took advantage of the large number of samples to conduct an epigenome-wide association study (EWAS) of age-associated DNA methylation patterns in skeletal muscle. ResultsThe newly developed clock uses 200 CpGs to estimate chronological age in skeletal muscle, 16 of which are in common with the 353 CpGs of the pan-tissue clock. The muscle clock outperformed the pan-tissue clock, with a median error of only 4.6 years across datasets (vs 13.1 years for the pan-tissue clock, p < 0.0001) and an average correlation of {rho} = 0.62 between actual and predicted age across datasets (vs {rho} = 0.51 for the pan-tissue clock). Lastly, we identified 180 differentially methylated regions (DMRs) with age in skeletal muscle at a False Discovery Rate < 0.005. However, Gene Set Enrichment Analysis did not reveal any enrichment for Gene Ontologies. ConclusionsWe have developed a muscle-specific epigenetic clock that predicts age with better accuracy than the pan-tissue clock. We implemented the muscle clock in an R package called MEAT available on Bioconductor to estimate epigenetic age in skeletal muscle samples. This clock may prove valuable in assessing the impact of environmental factors, such as exercise and diet, on muscle-specific biological ageing processes.

bioinformatics↗

Placental DNA methylation signatures of maternal smoking during pregnancy and potential impacts on fetal growth

Maternal smoking during pregnancy (MSDP) contributes to poor birth outcomes, in part through disrupted placental functions, which may be reflected in the placental epigenome. We meta-analyzed the associations between MSDP and placental DNA methylation (DNAm) and between DNAm and birth outcomes within the Pregnancy And Childhood Epigenetics (PACE) consortium (7 studies, N=1700, 344 with any MSDP). We identified 1224 CpGs that were associated with MSDP, of which 341 associated with birth outcomes and 141 associated with gene expression. Only 6 of these CpGs were consistent with the findings from a prior meta-analysis of cord blood DNAm, demonstrating substantial tissue-specific responses to MSDP. The placental MSDP associated CpGs were enriched for growth-factor signaling, hormone activity, inflammation, and vascularization, which play important roles in placental function. We demonstrate links between placental DNAm, MSDP and poor birth outcomes, which may better inform the mechanisms through which MSDP impacts placental function and fetal growth.

genomics↗

Individualised MRI training for paediatric neuroimaging in autism spectrum disorders: A child-focused approach

Magnetic Resonance Imaging (MRI) in paediatric cohorts is often complicated by reluctance to enter the scanner and head motion-related imaging artefacts. The MRI scanner environment is highly unusual and may distress younger cohorts, especially in children with sensory sensitivity and separation anxiety. The issue is particularly challenging in children with Autism Spectrum Disorders (ASD), where delivery of instructions for novel task demands in an unfamiliar setting may be limited or less effective due to communication disorder or intellectual disability. These issues together often give rise to excessive head motion that can significantly reduce the quality of images acquired, or render data unusable. Here we report an individualised MRI training procedure that enables young children with ASD to better tolerate the MRI scanner environment based on a child-focused approach and an individualised familiarisation strategy. The training procedure was implemented in a locally recruited study of monozygotic twins (n=12; 6 twin pairs; age range 7.1 to 12.85 years) concordant or discordant for ASD. MRI image quality indices were better or comparable to images acquired from an independent multi-centre ASD cohort. The success of these findings is promising and may be useful to improve the quality of paediatric neuroimaging in similar clinical populations.

neuroscience↗

Supragingival plaque microbiome ecology and functional potential in the context of health and disease

To address the question of how microbial diversity and function in the oral cavities of children relates to caries diagnosis, we surveyed the supragingival plaque biofilm microbiome in 44 juvenile twin pairs. Using shotgun sequencing, we constructed a genome encyclopedia describing the core supragingival plaque microbiome. Caries phenotypes contained statistically significant enrichments in specific genome abundances and distinct community composition profiles including strain-level changes. Metabolic pathways that are statistically associated with caries include several sugar-associated phosphotransferase systems, antimicrobial resistance, and metal transport. Numerous closely-related previously-uncharacterized microbes had substantial variation in central metabolism, including the loss of biosynthetic pathways resulting in auxotrophy, changing the ecological role. We also describe the first complete Gracilibacteria genomes from the human microbiome. Caries is a microbial community metabolic disorder that cannot be described by a single etiology and our results provide the information needed for next generation diagnostic tools and therapeutics for caries.

microbiology↗