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Hurley, J. M.

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

15 recordsLinked to original sources

Proteoform plasticity modulates the temperature response in circadian timekeeping

The molecular circadian clock optimally coordinates an organism's physiology with the light/dark cycle. One commonality among circadian molecular clock proteins is that they undergo alternative splicing, yielding multiple proteoforms. The isoform-specific sequences spliced into clock proteins contain intrinsically disordered regions (IDRs), suggesting that these regions might be intricately involved in cellular regulation. However, the functions of these isoform-specific IDRs in the clock remain poorly defined. Here, we use the core clock repressor FREQUENCY (FRQ) from the fungal circadian model system Neurospora crassa to test the hypothesis that alternative splicing of core clock IDRs yields multiple proteoforms that expand the functional regulatory capacity of FRQ. To do so, we biophysically characterized an IDR specific to the long isoform of the core clock repressor FRQ and identified motifs and molecular behaviors that regulate clock robustness in a temperature-dependent manner. We further compared the interactomes of two FRQ isoforms, identifying distinct functions and interacting proteins that could contribute to temperature regulation. Taken together, our data highlight that isoform-specific IDRs in clock-repressor proteins enhance and expand clock function in a context-dependent manner.

biochemistry↗

Circadian disruption induces sex-specific Alzheimer's pathophysiology and immune cell reprogramming

Circadian disruption (CD) is increasingly recognized as a sex-specific risk factor for Alzheimers disease (AD). However, the mechanisms linking CD to AD, and the role of biological sex in this interaction, are unclear. Immunometabolic regulation is extensively circadianly timed, has sex-specific phenotypes, and plays a role in AD. Therefore, we hypothesized that CD affects the timing of immunometabolism, contributing to the sex-specific effects of CD on AD. To demonstrate this, we subjected male and female APP/PS1 mice to chronic disruptive lighting to model circadian disruption, finding CD induced a female-specific reduction in amyloid plaque burden but an increase in the infiltration of peripheral macrophages into the brain. Concomitantly, we found macrophages exhibited CD-associated immune reprogramming, which in females led to altered immunometabolic timing, an increase of macrophages in the activated state, and elevated levels of reactive oxygen species (ROS), supporting a role for immunometabolism in the sex-specific effects of CD in AD. Graphical Abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=189 SRC="FIGDIR/small/721994v1_ufig1.gif" ALT="Figure 1"> View larger version (60K): org.highwire.dtl.DTLVardef@b9a59forg.highwire.dtl.DTLVardef@289219org.highwire.dtl.DTLVardef@18fe804org.highwire.dtl.DTLVardef@c96bb8_HPS_FORMAT_FIGEXP M_FIG C_FIG HighlightsO_LICircadian disruption reduces A{beta} plaque load specifically in female mice C_LIO_LIPeripheral immune infiltration correlates with reduced A{beta} plaques in females C_LIO_LICircadian disruption coordinates phasing of circadian immunometabolic proteins C_LIO_LIIn females, circadian phase advancement correlates with increased ROS C_LI

molecular biology↗

Alzheimer's Disease and circadian disruption sex-specifically contribute to a loss of bone maintenance in APP/PS1 model mice

Alzheimers Disease and Related Dementias (ADRDs) are linked to reduced bone integrity and increased fracture risk, but the mechanisms that underlie this risk remain poorly defined. Current research suggests that environmental factors, such as diet, sleep, and light exposure can modulate the brain-bone axis, increasing susceptibility to bone loss and fractures. Circadian disruption (CD) associated with ADRDs may exacerbate the effects of disease and aging in the bone. In particular, regulation of bone marrow progenitors may be acutely susceptible to disruption along this axis. Here, we explore the interplay among genetic and environmental factors that influence bone structure, marrow progenitor cell activity, and monocyte-derived macrophages. The APP/PS1 transgenic mouse model (AP) is used as an in vivo model of amyloid-beta deposition. High-resolution micro-computed tomography (CT) identified sex- and genotype-specific responses in trabecular morphometry. Follow-up analysis with Raman spectroscopy (RS) found accumulation of non-enzymatic modifications of the organic matrix and notched three-point bending identified concomitant loss of bone toughness due to both CD and AP. Single-cell RNA sequencing (scRNA-seq) confirmed the presence of oxidative stress signals in the cellular populations of the bone marrow. We further mapped significantly differentially expressed genes (DEGs) from monocytes in the bone marrow to circadian-regulated proteins in monocyte-derived macrophages, revealing dysregulation of circadian timing in macrophages in vitro. These findings offer new insights into how environmental disruptions can exacerbate the progression of neurodegenerative disease and bone degradation. LAY SUMMARYPatients with Alzheimers disease have an increased bone fracture risk, but the biological link between brain and bone disease is not well understood. Everyday factors such as altered light exposure (shift work, screens late at night, etc.) can worsen outcomes in the brain and skeleton. Using a mouse model of Alzheimers disease, we found that both genetic risk and circadian disruption contribute to weaker bone and altered bone quality. We also identified inflammation and stress responses in bone marrow cells, suggesting that bone marrow may play a key role in linking brain disease to bone fragility.

bioengineering↗

Circadian immunometabolic states impart a temporal response to SARS-CoV-2 spike proteins in mammalian macrophages

Circadian rhythms, driven by 24-hour molecular oscillators, or "clocks", widely tune physiology to the daily rhythms of light and dark to enhance organismal fitness. In mammals, the cellular immune response is tightly regulated by these rhythms such that immunometabolic output is coordinated across the day, consolidating macrophage physiology into temporally distinct phases that determine the macrophage response to stimuli. Importantly, key proteins in the macrophage response to viral infection have been found to be under circadian control, and time of day of adjuvant application is known to affect the efficacy of vaccinations, including in the case of the SARS-CoV-2 virus. However, little is known about the molecular changes that underly the temporal response to vaccine application. Therefore, to investigate the circadian response of macrophage physiology to adjuvant exposure, we exposed primary mouse and human macrophages to the SARS-CoV-1 and CoV-2 spike proteins at different times over the circadian day. To further explore the time-of-day effect, we performed a multi-omics analysis and in vitro tissue culture assays examining macrophage responses over circadian time. We found that, conserved across the species, the timing of spike protein exposure dictated two distinct temporal responses which were characterized by hallmarks of immunometabolic suppression and modest immunometabolic activation. Intriguingly, these temporal responses were driven by central metabolic and mitochondrial changes rather than classical immune activation, suggesting immunometabolic control is a primary regulator of the temporal response of immune cells to stimuli.

molecular biology↗

Genetically encoded RNA strand exchange circuits for programmable protein expression and computation in cells

Programmable cellular information processing could advance biomanufacturing of chemicals and medicine, and enable smart, living therapeutics and diagnostics1,2. Nucleic acids circuits based on toehold mediated strand exchange (TMSE) show tremendous potential for cellular programming due to their scalable, composable, and biocompatible parts3-6. However, these circuits are constrained primarily to in vitro applications because genetically encoding them is challenging and the principles of TMSE in cells remain unknown. Here we show the first demonstration of genetically encoded RNA strand exchange circuits, designed analogously to state-of-the-art TMSE circuits, in living cells. To elucidate the design principles of TMSE in cells, we develop toehold exchange riboregulators, which convert TMSE to protein expression, enabling precise control of protein translation rate. We find many of the design principles and parts used for TMSE in vitro transfer to Escherichia coli, allowing construction of multi-layer cascades and logic elements. We also identify caveats where strand exchange in cells differ substantially from cell-free systems, even in lysate from the same bacterial strain7, suggesting active cellular processes are involved. Our results further highlight bounds on strand exchange circuit architectures feasible in cells. We anticipate this study will lay the groundwork for developing advanced cellular circuits, bringing nucleic acid computing from the test tube to the cell8-10 and enabling new applications by connecting TMSE to gene expression. More broadly, our results have implications for RNA:RNA interactions and gene regulation in bacteria and provide a synthetic system for exploring such phenomena.

synthetic biology↗

Investigating the consequences of chronic short sleep for metabolism and survival of oxidative stress

In previous work, we found that short sleep caused sensitivity to oxidative stress; here we set out to characterize the physiological state of a diverse group of chronically short-sleeping mutants during hyperoxia as an acute oxidative stress. Using RNA-sequencing analysis, we found that short-sleeping mutants had a normal transcriptional oxidative stress response relative to controls. In both short-sleeping mutants and controls, hyperoxia led to downregulation of glycolytic genes and upregulation of genes involved in fatty acid metabolism, reminiscent of metabolic shifts during sleep. We hypothesized that short-sleeping mutants may be sensitive to hyperoxia because of defects in metabolism. Consistent with this, short-sleeping mutants were sensitive to starvation. Using metabolomics, we identified a pattern of low levels of long chain fatty acids and lysophospholipids in short-sleeping mutants relative to controls during hyperoxia, suggesting a defect in lipid metabolism. Though short-sleeping mutants did not have common defects in many aspects of lipid metabolism (basal fat stores, usage kinetics during hyperoxia, respiration rates, and cuticular hydrocarbon profiles), they were all sensitive to dehydration, suggesting a general defect in cuticular hydrocarbons, which protect against dehydration. To test the bi-directionality of sleep and lipid metabolism, we tested flies with both diet-induced obesity and genetic obesity. Flies with diet-induced obesity had no sleep or oxidative stress phenotype; in contrast, the lipid metabolic mutant, brummer, slept significantly more than controls but was sensitive to oxidative stress. Previously, all short sleepers tested were sensitive and all long sleepers resistant to oxidative stress. brummer mutants, the first exceptions to this rule, lack a key enzyme required to mobilize fat stores, suggesting that a defect in accessing lipid stores can cause sensitivity to oxidative stress. Taken together, we found that short-sleeping mutants have many phenotypes in common: sensitivity to oxidative stress, starvation, dehydration, and defects in lipid metabolites. These results argue against a specific role for sleep as an antioxidant and suggest the possibility that lipid metabolic defects underlie the sensitivity to oxidative stress of short-sleeping mutants.

physiology↗

Dual-Approach Co-expression Analysis Framework (D-CAF) Enables Identification of Novel Circadian Regulation From Multi-OmicTimeseries Data

The circadian clock is a central driver of many biological and behavioral processes, regulating the levels of many genes and proteins, termed clock controlled genes and proteins (CCGs/CCPs), to impart biological timing at the molecular level. While transcriptomic and proteomic data has been analyzed to find potential CCGs and CCPs, multi-omic modeling of circadian data, which has the potential to enhance the understanding of circadian control of biological timing, remains relatively rare due to several methodological hurdles. To address this gap, a Dual-approach Co-expression Analysis Framework (D-CAF) was created to perform perturbation-robust co-expression analysis on time-series measurements of both transcripts and proteins. Applying this D-CAF framework to previously gathered transcriptomic and proteomic data from mouse macrophages gathered over circadian time, we identified small, highly significant clusters of oscillating transcripts and proteins in the unweighted similarity matrices and larger, less significant clusters of of oscillating transcripts and proteins using the weighted similarity network. Functional enrichment analysis of these clusters identified novel immunological response pathways that appear to be under circadian control. Overall, our findings suggest that D-CAF is a tool that can be used by the circadian community to integrate multi-omic circadian data to improve our understanding of the mechanisms of circadian regulation of molecular processes.

bioinformatics↗

NOX2 Inhibition Enables Retention of the Circadian Clock in BV2 Microglia and Primary Macrophages

Sustained neuroinflammation is a major contributor to the progression of neurodegenerative diseases such as Alzheimers (AD) and Parkinsons (PD) diseases. Neuroinflammation, like other cellular processes, is affected by the circadian clock. Microglia, the resident immune cells in the brain, act as major contributors to neuroinflammation and are under the influence of the circadian clock. Microglial responses such as activation, recruitment, and cytokine expression are rhythmic in their response to various stimuli. While the link between circadian rhythms and neuroinflammation is clear, significant gaps remain in our understanding of this complex relationship. To further our understanding of this relationship, we studied the interaction between the microglial circadian clock and the enzyme NADPH Oxidase Isoform 2 (NOX2), an enzyme essential for the production of reactive oxygen species (ROS) in oxidative stress, an integral characteristic of neuroinflammation. We examined BV2 microglia over circadian time, demonstrating oscillations of the clock genes Per2 and Bmal1 and the NOX2 subunits gp91phox and p47phox. We discovered the BV2 microglial clock exerted significant control over NOX2 expression and that the inhibition of NOX2 enabled the microglia to retain a functional circadian clock while reducing levels of ROS and inflammatory cytokines. These trends were mirrored in mouse bone marrow-derived primary macrophages. Our findings indicate NOX2 plays a crucial role in the interaction between the circadian clock and the activation of microglia/macrophages into their pro-inflammatory state.

immunology↗

The PAICE Suite Reveals Circadian Post-Transcriptional Timing of Non-Coding RNAs and Spliceosome Components in Mus musculus Macrophages

Circadian rhythms broadly regulate physiological functions by tuning oscillations in the levels of mRNAs and proteins to the 24-hour day/night cycle. Globally assessing which mRNAs and proteins are timed by the clock necessitates accurate recognition of oscillations in RNA and protein data, particularly in large omics data sets. Tools that employ fixed-amplitude models have previously been used to positive effect. However, the recognition of amplitude-change in circadian oscillations required a new generation of analytical software to enhance the identification of these oscillations. To address this gap, we created the Pipeline for Amplitude Integration of Circadian Exploration (PAICE) suite. Here, we demonstrate the PAICE suites increased detection of circadian trends through the joint modeling of the Mus musculus macrophage transcriptome and proteome. Our enhanced detection confirmed extensive circadian post-transcriptional regulation in macrophages, but highlighted that some of the reported discrepancy between mRNA and protein oscillations was due to noise in data. We further applied the PAICE suite to investigate the circadian timing of non-coding RNAs, documenting extensive circadian timing of long non-coding RNAs and small nuclear RNAs, which control the recognition of mRNA in the spliceosome complex. By tracking oscillating spliceosome complex proteins using the PAICE suite, we noted that the clock broadly regulates the spliceosome, particularly the major spliceosome complex. As most of the above-noted rhythms had damped amplitude changes in their oscillations, this work highlights the importance of the PAICE suite in the thorough enumeration of oscillations in omics-scale datasets.

systems biology↗

The formation of a fuzzy complex in the negative arm regulates the robustness of the circadian clock.

The circadian clock times cellular processes to the day/night cycle via a Transcription-Translation negative Feedback Loop (TTFL). However, a mechanistic understanding of the negative arm in both the timing of the TTFL and its control of output is lacking. We posited that the formation of negative-arm protein complexes was fundamental to clock regulation stemming from the negative arm. Using a modified peptide microarray approach termed Linear motif discovery using rational design (LOCATE), we characterized the interaction of the disordered negative-arm clock protein FREQUENCY to its partner protein FREQUENCY-Interacting RNA helicase. LOCATE identified a specific Short Linear Motif (SLiM) and interaction "hotspot" as well as positively charged "islands" that mediate electrostatic interactions, suggesting a model where negative arm proteins form a "fuzzy" complex essential for clock timing and robustness. Further analysis revealed that the positively charged islands were an evolutionarily conserved feature in higher eukaryotes and contributed to proper clock function.

molecular biology↗

Conformational Changes in the Negative Arm of the Circadian Clock Correlate with Dynamic Interactomes Involved in Post-transcriptionally Regulated Processes

The circadian clock employs a transcriptional/translational negative feedback loop (TTFL) to anticipate environmental changes due to the Earths diurnal cycle, with regulation of organismal physiology believed to stem from temporal transcriptional activation by the positive arm. However, up to 80% of oscillating proteins do not have rhythmic mRNA, establishing circadian post-transcriptional regulation through unknown mechanisms. Given the pervasive conservation of the intrinsically disordered nature of negative-arm clock proteins, we hypothesized that post-transcriptional regulation may stem from conformational shifts in negative-arm proteins that time vacillations in the constituents of negative-arm macromolecular complexes to time cellular physiology. Our investigation of the negative arm clock protein in Neurospora crassa, FREQUENCY (FRQ), demonstrated temporal conformational fluidity correlated with daily changes in physiologically diverse macromolecular complex components. A parallel investigation of the macromolecular complexes centered around Drosophila melanogaster PERIOD (dPER) and human PERIOD (hPER2) found a similar number and physiological diversity of interacting partners in higher eukaryotes. Short linear motifs (SLiMs) associated with the interactors localized to disordered and phosphorylated regions on the PERs and FRQ, with disordered interactors oscillating in the macromolecular complexes over circadian time. This oscillation correlated with oscillations in post-transcriptionally regulated proteins, suggesting the negative arm may tune cellular physiology and proteostasis post-transcriptionally via vacillations in the circadian negative-arm macromolecular protein complexes.

molecular biology↗

Circadian Control of Heparan Sulfate Levels Times Phagocytosis of Amyloid Beta Aggregates

Alzheimers Disease (AD) is a neuroinflammatory disease characterized partly by the inability to clear, and subsequent build-up, of amyloid-beta (A{beta}). A{beta} clearance is regulated by several pathways and has a circadian component. However, the mechanism underlying the circadian clearance of A{beta} has not been defined. Myeloid-based phagocytosis, a key mechanism in the metabolism of A{beta}, is circadianly-regulated, presenting a potential mechanism for the circadian clearance of A{beta}. In this work, we revealed that the phagocytosis of A{beta}42 undergoes a daily oscillation that is dependent on the circadian clock. We found the circadian timing of global heparan sulfate proteoglycan (HSPG) biosynthesis was the molecular timer for the clock-controlled phagocytosis of A{beta} and that both HSPG binding and A{beta}42 aggregation were essential for this oscillation. These data highlight that circadian regulation in immune cells may play a role in the intricate relationship between the circadian clock and AD. Graphical Abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=131 SRC="FIGDIR/small/442651v1_ufig1.gif" ALT="Figure 1"> View larger version (44K): org.highwire.dtl.DTLVardef@bca9b3org.highwire.dtl.DTLVardef@29575corg.highwire.dtl.DTLVardef@2673c5org.highwire.dtl.DTLVardef@7a8daa_HPS_FORMAT_FIGEXP M_FIG C_FIG

immunology↗

MOSAIC: A Joint Modeling Methodology for Combined Circadian and Non-Circadian Analysis of Multi-Omics Data

MotivationCircadian rhythms are approximately 24 hour endogenous cycles that control many biological functions. To identify these rhythms, biological samples are taken over circadian time and analyzed using a single omics type, such as transcriptomics or proteomics. By comparing data from these single omics approaches, it has been shown that transcriptional rhythms are not necessarily conserved at the protein level, implying extensive circadian post-transcriptional regulation. However, as proteomics methods are known to be noisier than transcriptomic methods, this suggests that previously identified arrhythmic proteins with rhythmic transcripts could have been missed due to noise and may not be due to post-transcriptional regulation. ResultsTo determine if one can use information from less-noisy transcriptomic data to inform rhythms in more-noisy proteomic data, and thus more accurately identify rhythms in the proteome, we have created the MOSAIC (Multi-Omics Selection with Amplitude Independent Criteria) application. MOSAIC combines model selection and joint modeling of multiple omics types to recover significant circadian and non-circadian trends. Using both synthetic data and proteomic data from Neurospora crassa, we showed that MOSAIC accurately recovers circadian rhythms at higher rates in not only the proteome but the transcriptome as well, outperforming existing methods for rhythm identification. In addition, by quantifying non-circadian trends in addition to circadian trends in data, our methodology allowed for the recognition of the diversity of circadian regulation as compared to non-circadian regulation. AvailabilityMOSAICs full interface is available at https://github.com/delosh653/MOSAIC. Contacthurlej2@rpi.edu Supplementary informationSupplementary data are available.at Bioinformatics online.

bioinformatics↗

Post-Transcriptional Circadian Regulation in Macrophages Organizes Temporally Distinct Immunometabolic States

Our core timekeeping mechanism, the circadian clock, regulates an astonishing amount of cellular physiology and behavior, playing a vital role in organismal fitness. While the mechanics of circadian control over cellular regulation can in part be explained by the transcriptional activation stemming from the positive arm of the clocks transcription-translation negative feedback loop, research has shown that extensive circadian regulation occurs beyond transcriptional activation in fungal species and data suggest that this post-transcriptional regulation may also be preserved in mammals. To determine the extent to which circadian output is regulated post-transcriptionally in mammalian cells, we comprehensively profiled the transcriptome and proteome of murine bone marrow-derived macrophages in a high resolution, sample rich time course. We found that only 15% of the circadian proteome had corresponding oscillating mRNA and this regulation was cell intrinsic. Ontological analysis of oscillating proteins revealed robust temporal enrichment for protein degradation and translation, providing potential insights into the source of this extensive post-transcriptional regulation. We noted post-transcriptional temporal-gating across a number of connected metabolic pathways. This temporal metabolic regulation further corresponded with rhythms we observed in ATP production, mitochondrial morphology, and phagocytosis. With the strong interconnection between cellular metabolic states and macrophage phenotypes/responses, our work demonstrates that post-transcriptional circadian regulation in macrophages is broadly utilized as a tool to confer time-dependent immune function and responses. As macrophages coordinate many immunological and inflammatory functions, an understanding of this regulation provides a framework to determine the impact of circadian regulation on a wide array of disease pathologies.

molecular biology↗

ECHO: an Application for Detection and Analysis of Oscillators Identifies Metabolic Regulation on Genome-Wide Circadian Output

MotivationTime courses utilizing genome scale data are a common approach to identifying the biological pathways that are controlled by the circadian clock, an important regulator of organismal fitness. However, the methods used to detect circadian oscillations in these datasets are not able to accommodate changes in the amplitude of the oscillations over time, leading to an underestimation of the impact of the clock on biological systems.\n\nResultsWe have created a program to efficaciously identify oscillations in large-scale datasets, called the Extended Circadian Harmonic Oscillator application, or ECHO. ECHO utilizes an extended solution of the fixed amplitude mass-spring oscillator that incorporates the amplitude change coefficient. Employing synthetic datasets, we determined that ECHO outperforms existing methods in detecting rhythms with decreasing oscillation amplitudes and recovering phase shift. Rhythms with changing amplitudes identified from published biological datasets revealed distinct functions from those oscillations that were harmonic, suggesting purposeful biologic regulation to create this subtype of circadian rhythms.\n\nAvailabilityECHOs full interface is available at https://github.com/delosh653/ECHO. An R package for this functionality, echo.find, can be downloaded at https://CRAN.R-project.org/package=echo.find.\n\nContacthurleyj2@rpi.edu\n\nSupplementary informationSupplementary data are available

bioinformatics↗