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Shelton, J. M.

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

9 recordsLinked to original sources

An explainable boosting machine model for identifying artifacts caused by formalin-fixed paraffin embedding

BackgroundFormalin-fixed paraffin-embedding (FFPE) is a widely used, cost-effective method for long-term storage of clinical samples. However, fixation is known to introduce damage to nucleic acids that can present as artifactual bases in sequencing otherwise absent from higher fidelity storage methods such as fresh freezing (FF). Various machine learning methods exist for filtering these variant artifacts, but benchmarking performance can be difficult without reliable truth sets. In this study, we employ a collection of 90 paired fresh-frozen and formalin-fixed paraffin embedded samples from the same tumor to robustly define real and FFPE-derived, artifactual variation and enable objective evaluation of filtering methods. To address existing shortcomings, we propose a novel explainable boosting machine (EBM) model that improves performance, can be easily updated with new data, requires modest computational resources, and is analysis pipeline agnostic, making it broadly accessible. ResultsWe evaluated several methods for limiting FFPE-derived variant artifacts using cohorts of B-cell lymphoma samples. We found capturing local context around variants to be a highly informative, under-utilized feature set not commonly incorporated into many existing machine learning methods. Consequently, we developed a novel algorithm, FIFA, for filtering FFPE artifacts, which uses an EBM model, an interpretable decision-tree-based learning algorithm, to address some of the existing shortcomings. We used four independent cohorts composed of paired lymphoma and cervical cancer samples and a breast cancer cell line with both FF and FFPE samples to define clearly annotated training and test sets and demonstrated improved performance over existing methods. Additionally, FIFA filtering increased relevant biological signals in FFPE breast cancer datasets distinct from the training and testing sets. The EBM framework employed by FIFA is computationally efficient and easily amenable to incorporation of additional datasets due to its generalized additive modeling of features making it straightforward to incorporate new data into existing models dynamically over time. ConclusionsOur novel FFPE variant artifact filtering tool, FIFA, is a marked improvement over existing methods. It can be easily implemented, post hoc, to supplement existing somatic calling pipelines, training and inference can be run quickly across most compute environments, and it can be easily updated online as new training data becomes available. Accordingly, FIFA represents an important advance in retrospective cancer genomics research by further enhancing access to the vast stores of FFPE-archived tumor samples currently in existence.

bioinformatics↗

Timing of immune checkpoint blockade shapes anti-tumor immunity via a clock-dependent chemokine axis

Circadian clocks regulate immunity, yet how they shape the tumor immune microenvironment and influence cancer immunotherapy remains unclear. Here, we show that tumor immune infiltration and immune checkpoint inhibitor efficacy vary by time of day in mice, driven by intrinsic clocks in dendritic cells and CD8+ T cells. Time-of-day modulates the abundance, spatial organization, and cytokine-chemokine production of tumor-infiltrating immune cells. Mechanistically, dendritic cell clocks control expression of Cx3cl1, driving recruitment of CX3CR1+CD8+ T cells and thereby reshaping the tumor immune microenvironment to enhance immunotherapy efficacy. Disruption of this axis abolishes time-of-day-dependent differences in treatment response. These findings identify a circadian mechanism of immune cell recruitment to tumors and provide mechanistic insight into clinical observations linking treatment timing to immunotherapy outcomes. One sentence summaryTime of day determines cancer immunotherapy efficacy through a circadian clock-dependent chemokine axis.

immunology↗

Maintenance of pig brain function under extracorporeal pulsatile circulatory control (EPCC)

Selective vascular access to the brain is desirable in metabolic tracer, pharmacological and other studies aimed to characterize neural properties in isolation from somatic influences from chest, abdomen or limbs. However, current methods for artificial control of cerebral circulation can abolish pulsatility-dependent vascular signaling or neural network phenomena such as the electrocorticogram even when preserving individual neuronal activity. Thus, we set out to mechanically render cerebral hemodynamics fully regulable to replicate or modify native pig brain perfusion. To this end, blood flow to the head was surgically separated from the systemic circulation and full extracorporeal pulsatile circulatory control (EPCC) delivered via a modified aorta or brachiocephalic artery. This control relied on a computerized algorithm that maintained, for several hours, blood pressure, flow and pulsatility at near-native values individually measured before EPCC. Continuous electrocorticography and brain depth electrode recordings were used to evaluate brain activity relative to the standard offered by awake human electrocorticography. Under EPCC, this activity remained unaltered or minimally perturbed compared to the native circulation state, as did cerebral oxygenation, pressure, temperature and microscopic structure. Thus, our approach enables the study of neural activity and its circulatory manipulation in independence of most of the rest of the organism.

neuroscience↗

The Interplay between Mutagenesis and Extrachromosomal DNA Shapes Urothelial Cancer Evolution

Advanced urothelial cancer is a frequently lethal disease characterized by marked genetic heterogeneity. In this study, we investigate the evolution of the genomic signatures caused by endogenous and external mutagenic stimuli and their interplay with complex structural variants. We superimposed mutational signatures and phylogenetic analyses of matched serial tumors from patients with urothelial cancer to define the evolutionary patterns of these processes. We show that APOBEC3-induced mutations are clonal and early, whereas mutational bursts comprising hundreds of late subclonal mutations are induced by chemotherapy. Using a novel genome graph computational paradigm, we observed frequent circular high copy-number amplicons characteristic of extrachromosomal DNA (ecDNA) involving double-minutes, breakage-fusion-bridge, and tyfonas events. We characterized the distinct temporal patterns of APOBEC3 mutations and chemotherapy-induced mutations within ecDNA, gaining new insights into the timing of these events relative to ecDNA biogenesis. Finally, we discovered that most CCND1 amplifications in urothelial cancer arise within circular ecDNA amplicons. These CCND1 ecDNA amplification events persisted and increased in complexity incorporating additional DNA segments potentially contributing selective fitness advantage to the evolution of treatment resistance. Our findings define fundamental mechanisms driving urothelial cancer evolution and have therapeutic implications for treating this disease.

genomics↗

LY6E protects mice from pathogenic effects of murine coronavirus and SARS-CoV-2

LY6E is an antiviral protein that inhibits coronavirus entry. Its expression in immune cells allows mice to control murine coronavirus infection. However, it is not known which immune cell subsets mediate this control or whether LY6E protects mice from SARS-CoV-2. In this study, we used tissue-specific Cre recombinase expression to ablate Ly6e in distinct immune compartments or in all epiblast-derived cells, and bone marrow chimeras to target Ly6e in a subset of radioresistant cells. Mice lacking Ly6e in Lyz2-expressing cells and radioresistant Vav1-expressing cells were more susceptible to lethal murine coronavirus infection. Mice lacking Ly6e globally developed clinical disease when challenged with the Gamma (P.1) variant of SARS-CoV-2. By contrast, wildtype mice and mice lacking type I and type III interferon signaling had no clinical symptoms after SARS-CoV-2 infection. Transcriptomic profiling of lungs from SARS-CoV-2-infected wildtype and Ly6e knockout mice revealed a striking reduction of secretory cell-associated genes in infected knockout mice, including Muc5b, an airway mucin-encoding gene that may protect against SARS-CoV-2-inflicted respiratory disease. Collectively, our study reveals distinct cellular compartments in which Ly6e confers cell intrinsic antiviral effects, thereby conferring resistance to disease caused by murine coronavirus and SARS-CoV-2.

microbiology↗

Citizen-science surveillance of triazole-resistant Aspergillus fumigatus in UK residential garden soils

Compost is an ecological niche for Aspergillus fumigatus due to its role as a decomposer of organic matter and its ability to survive the high temperatures associated with the composting process. Subsequently, composting facilities are associated with high levels of A. fumigatus spores that are aerosolised from compost and cause respiratory illness in workers. In the UK, gardening is an activity enjoyed by individuals of all ages and it is likely that they are being exposed to A. fumigatus spores when handling commercial compost or compost they have produced themselves. In this study, 246 citizen scientists collected 509 soil samples from locations in their garden in the UK, from which were cultured 5,174 A. fumigatus isolates. Of these isolates, 736 (14%) were resistant to tebuconazole: the third most-sprayed triazole fungicide in the UK, which confers cross-resistance to the medical triazoles used to treat A. fumigatus lung infections in humans. These isolates were found to contain the common resistance mechanisms in the A. fumigatus cyp51A gene TR34/L98H or TR46/Y121F/T289A, and less common resistance mechanisms TR34, TR53, TR46/Y121F/T289A/S363P/I364V/G448S and (TR46)2/Y121F/M172I/T289A/G448S. Regression analyses found that soil samples containing compost were significantly more likely to grow susceptible and tebuconazole-resistant A. fumigatus than those that did not, and that compost samples grew significantly higher numbers of A. fumigatus than other samples. ImportanceThese findings highlight compost as a potential health hazard to individuals with pre-disposing factors to A. fumigatus lung infections, and a potential health hazard to immunocompetent individuals who could be exposed to sufficiently high numbers of spores to develop infection. This raises the question of whether compost bags should carry additional health warnings regarding inhalation of A. fumigatus spores, whether individuals should be advised to wear facemasks whilst handling compost or whether commercial producers should be responsible for sterilising compost before shipping. The findings support increasing public awareness of the hazard posed by compost and investigating measures that can be taken to reduce the exposure risk.

microbiology↗

Campaign-Based Citizen Science for Environmental Mycology: the "Science Solstice" and "Summer Soil-stice" Projects to Assess Drug Resistance in Air and Soilborne Aspergillus fumigatus

Citizen science projects are often undertaken for ecological and environmental research purposes but also have great potential for use in microbiology research to track the emergence and spread of pathogens in the environment. Science Solstice and Summer Soil-stice are mycology citizen science projects aimed at assessing drug resistance in Aspergillus fumigatus fungal spores found in air and soil, respectively, in the United Kingdom (UK). A. fumigatus plays an important role in the environment as a decomposer of plant material, but is also an opportunistic human lung pathogen. Infection with drug-resistant spores can lead to a worse clinical outcome for the patient. On the first four solstice and equinox days between June 2018 and June 2019, volunteers were asked to collect air samples from their homes and workplaces and return them to our lab in Freepost envelopes. An additional round of samples was requested from volunteers gardens and/or compost on the June 2019 solstice. In total, 787 volunteers returned 2,132 air samples and 509 soil samples, which grew a total of 7,991 A. fumigatus colonies. The estimated total cost of the study was {pound}2,650; the equivalent of 33 pence per A. fumigatus colony grown. Incorporating citizen science into the environmental surveillance of drug-resistant A. fumigatus allowed for the simultaneous collection of hundreds of environmental samples across the entire UK on the same day. The insights generated from this study would not be practical in the absence of public participation and offers opportunities to ask scientific questions that were previously unaskable.

scientific communication and education↗

Elevated prevalence of azole resistant Aspergillus fumigatus in urban versus rural environments in the United Kingdom

Azole resistance in the opportunistic pathogen Aspergillus fumigatus is increasing, dominated primarily by two environmentally-associated resistance alleles: TR34/L98H and TR46/Y121F/T289A. Using an environmental sampling strategy across the South of England we assess the prevalence of azole resistant A. fumigatus (ARAf) in soil samples collected in both urban and rural locations. We characterise the susceptibility profiles of the resistant isolates to three medical azoles, identify the underlying genetic basis of resistance and investigate their genetic relationships. ARAf was detected in 6.7% of the soil samples, with a higher prevalence in urban (13.8%) compared to rural (1.1%) locations. Nineteen isolates were confirmed to exhibit clinical breakpoints for resistance to at least one of three medical azoles, with 18 isolates exhibiting resistance to itraconazole, four to voriconazole, with two also showing additional elevated minimum inhibitory concentration to posaconazole. Thirteen of the resistant isolates harboured the TR34/L98H resistance allele and six isolates carried TR46/Y121F/T289A allele. The 19 azole-resistant isolates were spread across five csp1 genetic subtypes, t01, t02, t04B, t09 and t18 with t02 the predominant subtype. Our study demonstrates that ARAf can be easily isolated in the South of England, especially in urban city centres, which appear to play an important role in the epidemiology of environmentally-linked drug resistant A. fumigatus.

microbiology↗

Captivity and exposure to the emerging fungal pathogen Batrachochytrium salamandrivorans are linked to perturbation and dysbiosis of the amphibian skin microbiome

O_LIThe emerging fungal pathogen, Batrachochytrium salamandrivorans (Bsal) is responsible for the catastrophic decline of European salamanders and poses a threat to amphibians globally.\nC_LIO_LIThe amphibian skin microbiome is strongly associated with disease outcome for several host-pathogen systems, yet its role in Bsal infection remains unresolved. In addition, many in-vivo Bsal studies to date have relied on specimens that have been kept in captivity for long periods without considering the influence of environment on the microbiome and how this may impact the host response to pathogen exposure.\nC_LIO_LIWe characterised the impact of captivity and exposure to Bsal on the skin bacterial and fungal communities of two co-occurring European newt species, the smooth newt (Lissotriton vulgaris) and the great-crested newt (Triturus cristatus).\nC_LIO_LIBsal infection and subsequent mortality in both newt species was associated with perturbation of the skin microbiome and possible dysbiosis. In addition, reduced microbial diversity and changes in microbiome structure accompanied the transition of newts from the wild to captivity, suggesting a possible decline in microbe-associated protection and increased risk of infection by opportunistic pathogens.\nC_LIO_LIOur findings advance current understanding of the role of host-associated microbiota in Bsal infection and highlight important considerations for ex-situ amphibian conservation programmes.\nC_LI

ecology↗